Cover drawing by Claude Lumen (my father-in-law) and description of the cover by Jacqueline Magis and Eric Thys (my parents): From one shore to another, from one ocean to another, from one discipline to another, My barque of anthropologist, Charged with new experiences between humans, animals and their environment, Docks to join the luminous white house, Meeting place of knowledge and sciences exchanges.
Pictures of the page chapters by Séverine Thys taken during fieldworks.
Dissertation submitted in fulfillment of the requirements for the degree of Doctor (PhD) in Veterinary Sciences, 2019
Promoters: Prof. Dr. Sarah Gabriël Prof. Dr. Pierre Dorny Prof. Dr. Marleen Boelaert
Laboratory of Foodborne Parasitic Zoonoses Department of Veterinary Public Health and Food Safety Faculty of Veterinary Medicine, Ghent University Salisburylaan 133, B-9820 Merelbeke
ACKNOWLEDGEMENTS ...... 11 ABBREVIATIONS ...... 13 GENERAL INTRODUCTION ...... 15 CHAPTER 1 LITERATURE REVIEW: NEGLECTED ZOONOTIC DISEASES IN GENERAL, THE EPIDEMIOLOGY AND CONTROL OF THREE SELECTED NEGLECTED ZOONOTIC DISEASES AND THE ROLE OF ANTHROPOLOGY IN THE CONTROL ...... 19 1.1 Neglected Zoonotic Diseases ...... 20
1.1.1 The “Zoonotic” component ...... 20 1.1.2. The “Neglected” component ...... 22 1.1.3. The “One Health” approach ...... 24 1.2 Case-studies of three NZDs: Cystic echinococcosis, Taenia solium taeniasis- cysticercosis and rabies ...... 26
1.2.1 Cystic echinococcosis ...... 27 1.2.2 Taenia solium taeniasis/cysticercosis ...... 36 1.2.3 Rabies...... 49 1.3 Role of Anthropology in Neglected Zoonotic Diseases integrated control and in the “One Health” movement...... 62
1.3.1 Anthropology and Health, the concept of “culture” applied to livestock owners and zoonotic risks ...... 63 1.3.2 Anthropology and Health, the concept of “culture” applied to human-animal interactions ...... 67 1.3.3 Anthropology and “One Health” as an integrated control approach ...... 70 1.4 References ...... 75
RATIONALE AND OBJECTIVES ...... 101 Rationale ...... 102
Objectives ...... 103
References ...... 103
CHAPTER 2 MATERIALS AND METHODS: QUALITATIVE RESEARCH ...... 105 2.1 Qualitative research: Definition and Methods ...... 106
2.1.1 Qualitative research in Health ...... 106 2.1.2 Main qualitative methods ...... 108 2.1.3 Sampling strategies in QLR ...... 110
2.2 Anthropological posture within a disease control driven conceptual framing ...... 112
2.3 Case-studies materials and methods ...... 114
2.3.1 Criteria guiding the selection of the three case-studies ...... 114 2.3.2 Methodological approach chosen ...... 114 2.3.3 Focus Group Discussions method ...... 116 2.3.4 Common features of the study design and procedure followed for the three case- studies ...... 117 2.3.5 Permanent reflexivity ...... 125 2.4 References ...... 128
CHAPTER 3 COMMUNITY PERCEPTION AND KNOWLEDGE OF CYSTIC ECHINOCOCCOSIS IN THE HIGH ATLAS MOUNTAINS, MOROCCO ...... 131 3.1 Introduction ...... 132
3.2 Materials and methods ...... 135
3.2.1 Study area ...... 135 3.2.2 Study design ...... 135 3.2.3 Data collection ...... 137 3.2.4 Data processing and analysis ...... 138 3.2.5 Ethical considerations ...... 139 3.3 Results ...... 139
3.3.1 Life cycle of the parasite and knowledge gaps ...... 139 3.3.2 Dogs: perception, role, and status ...... 143 3.3.3 Sheep management and slaughtering practices ...... 147 3.3.4 Control measures: pros and cons ...... 149 3.3.5 Additional measures suggested by the participants ...... 152 3.4 Discussion ...... 154
3.5 Conclusions ...... 159
3.6 Supplementary information ...... 161
3.6.1 Focus Group Discussion guides (Men, Women and Butchers) in English...... 161 3.6.2 Illustrative quotes from the Focus Groups Discussions (“a” to “n”) ...... 165 3.7 References ...... 167
CHAPTER 4 COMMUNITIES’ PERCEPTIONS, KNOWLEDGE AND PRACTICES IN A TAENIA SOLIUM ENDEMIC RURAL AREA IN EASTERN ZAMBIA PART 1: WHY LATRINES ARE NOT USED ...... 171 4.1 Introduction ...... 172
4.2 Materials and methods...... 173
4.2.1 Study area ...... 173 4.2.2 Study design ...... 175 4.2.3 Data collection ...... 177 4.2.4 Data processing and analysis ...... 178 4.2.5 Ethical considerations ...... 178 4.3 Results ...... 178
4.3.1 Latrine availability ...... 182 4.3.2 Latrine use ...... 185 4.4 Discussion ...... 191
4.5 Conclusions ...... 195
4.6 References ...... 195
CHAPTER 5 COMMUNITIES’ PERCEPTIONS, KNOWLEDGE AND PRACTICES IN A TAENIA SOLIUM ENDEMIC RURAL AREA IN EASTERN ZAMBIA PART 2: WHY PIGS ARE FREE- ROAMING ...... 199 5.1 Introduction ...... 200
5.2 Materials and methods...... 201
5.2.1 Study area ...... 201 5.2.2 Study design ...... 201 5.2.3 Data collection ...... 201 5.2.4 Data processing and analysis ...... 202 5.2.5 Ethical considerations ...... 202 5.3 Results ...... 202
5.3.1 People’s perception and knowledge of pig keeping ...... 203 5.3.2 Pigs threats for human health ...... 209 5.3.3 Perception of control options: pros vs cons and suggestions ...... 213 5.4 Discussion and Conclusions...... 215
5.5 References ...... 220
CHAPTER 6 PERCEPTIONS AND PRACTICES OF DOG OWNERSHIP AND RABIES CONTROL IN A COMMUNITY WITH RECENTLY RE-INTRODUCED RABIES AT A HUMAN-WILDLIFE- DOMESTIC ANIMAL INTERFACE IN MPUMALANGA, SOUTH AFRICA ...... 223 6.1 Introduction ...... 225
6.2 Materials and methods ...... 227
6.2.1 Study area ...... 227 6.2.2 Study design ...... 228 6.2.3 Data collection ...... 229 6.2.4 Data processing and analysis ...... 230 6.2.5 Ethical considerations ...... 231 6.3 Results ...... 231
6.3.1 Role of dogs ...... 231 6.3.2 Dog ownership (definition, type of care and duties) ...... 232 6.3.3 Sheep management and slaughtering practices ...... 233 6.3.4 Local knowledge of dog diseases and “Rihuhumbyana” ...... 234 6.3.5 Vaccination ...... 237 6.4 Discussion ...... 242
6.5 Conclusions and recommendations ...... 247
6.6 Supplementary information ...... 249
6.6.1 Study area (including dog rabies vaccination campaigns process and common canine diseases in the study area) ...... 249 6.6.2 Illustrative quotes from the Focus Group Discussions (quotes “a” until “f”) ...... 251 6.7 References ...... 252
CHAPTER 7 GENERAL DISCUSSION: THE ADDED VALUE OF ANTHROPOLOGY FOR AN INTEGRATED CONTROL OF NEGLECTED ZOONOTIC DISEASES IN THE ONE HEALTH MOVEMENT ...... 257 7.1 “Risk”, a conceptual common denominator in interdisciplinary research on zoonoses ...... 258
7.2 Beyond the role of “cultural mediator” for behaviour change in interdisciplinary research on zoonoses ...... 260
7.3 Human–animal relations and a cross-cultural perspective ...... 262
7.4. One Health and integrated control ...... 265
7.5 Challenges ...... 268
7.5.1 Interdisciplinary ...... 268 7.5.2 From local to global and vice versa ...... 269 7.5.3 Socio-ecological approach ...... 271 7.6 The losses and gains: an interdisciplinary dialogue within a disease control driven research ...... 272
7.7 Recommendations and general conclusions: a productive discomfort and constructive conflict ...... 274
7.8 References ...... 277
SUMMARY ...... 285 SAMENVATTING ...... 291 CURRICULUM VITAE ...... 297
As this part of the dissertation will most probably be the first one read, I will do my very best to not forget any of you who know me before and all along this PhD adventure. If I do, please do not take it personnaly as you are certainly in a special place of my heart where no words are needed.
First of all, this PhD work is dedicated to:
The late Prof. dr. Peter Van den Bossche for his mentorship, open-minded spirit, dynamism and avant-guardist science and without whom I would never have started building this specific niche which became a solid bridge with time.
My parents, my ancestors and my life partner for their perpetual guidance, support and infinite love.
I would like to express my sincere and deep gratitude:
To the Belgium Directorate General for Development Cooperation and Humanitarian Aid for the financial support to conduct the research and publication of the three case-studies through the former Strategic Network on Neglected Diseases and Zoonoses (http://www.snndz.net/).
To the Foundation Dubois-Brigué and its jury members (Professors Y. Carlier, N. Clumeck and F. Portaels from the Académie Royale de Médecine de Belgique and Professors S. Geerts, G. Leven and J. Vercruysse from the Koninklijke Academie voor Geneeskunde van België) for the scholarship of one additional year of PhD and for giving more room and recognition to Anthropology and the One Health movement inside the Royal Academy of Overseas Sciences of Belgium.
To my UGhent promoter, Professor Sarah Gabriël of the Faculty of Veterinary Medicine, Ghent University, Belgium who has been my locomotive all along this adventure. From the field trip in Zambia to collect the data until this very last day of reaching the final line of the Public Defense, she never gave up on me and pushed me very far in my research and scientific reflections, while making sure that my self-confidence continues growing and that all of this hard work was worth it. To my promoter Professor Pierre Dorny of the Faculty of Veterinary Medicine, Ghent University, Belgium and the Department of Biomedical Sciences, Institute of Tropical Medicine (ITM) Antwerp, who beside his unbelievable expertise in the field of parasitology, was continuously bringing serenity and positivity along this journey while devoting valuable time to correct, review, discuss my PhD. Together with Prof. Gabriël, they made a great duo and their years of fruitful collaborations together offered me a very
12 | A cknowledgements solid barque to cross all the storms safely and wherein we could also enjoy and celebrate succesful navigation steps. To my promoter of ITM, Professor Marleen Boelaert of the Public Health (PH) Department, who welcomed me in her unit without question, who was always by my side, knowing well when to disarm my stress and anxities. She also supported my carrier choice as well as my operational research side. When fundings were lacking, she always found solutions. By working by her side, I learned so much from her managerial skills, strenght and combativeness.
To the jury members of my Examination Board, Profs G. Janssens, B. Levecke, Prof. P. Bracke from UGent, Dr. N. Antoine-Moussiaux from ULiège and Dr. A. Binot from CIRAD, who accepted and welcomed this hybrid disertation with open and critical eyes, who challenged me and provided me with keys and valuable advice. I also would like to thank them for the fuitful, constructive and very interesting exchanges during the Private Defense.
To my dearest friends collaborators and co-authors from Morocco, Zambia and South Africa, who agreed to jump with me in the qualitative research world, who welcomed me in their field, their institute, their home, their familiy and with whom the word “collaboration” trully finds its palce and meaning.
To Prof. Artama Wayan and the great colleagues from Gadjah Mada Universitas in Indonesia for hosting me in their One Health unit while inspiring me for the first lines of my manuscript.
To my ITM colleagues, Dr. T. Marcotty who was also at the origin of launching this barque into the interdisciplinary sea, and Dr. P. Lefèvre who taught me how to be an anthropologist into this barque; to my young and festive colleagues from the former Animal Health Department; to my ITM ladies (Jasna, Analie, Tine & Co) for their friendship, their light and lunch escapes; to my PH second floor colleagues who answered to my smiles with a bigger one, who calmed my fears, who listened to my tears, who fed me intelectually (with delicious comfort food too), and all that with enourmous admin support (Evelien & Co); and finally, the last but not least, to my “bande de la mort” for the kicker and way beyond.
To my close friends, my chosen family, who know me better than myself and who physically and emotionnaly carried me up to this final PhD harbour. I also would like to thank my water polo team maids for their energic supports and tolerance to my moments of frustration released during trainings and games (sometimes).
To my family for everything, but also for the hosting at the Belgian sea side and at Gesves for the writing retreats, for the magic moonstone for concentration, for the manuscript corrections and inputs, for the drawing talent of the cover, for making me an aunt (“Tata Vrine”) and for believing in me.Thank you, Dank u, Merci.
CART Classification and Regression Trees model
CE Cystic Echinococcosis
CIRAD Centre de Coopération Internationale en Recherche Agronomique pour le Développement
CoAg coproantigen
DALYs Disability Adjusted Life Years
EC EcoHealth
ELISA Enzyme-linked immunosorbent assay
FGD Focus Group Discussion
FAO Food and Agriculture Organization of the United Nations
G Genotype
GI Gastrointestinal
HAHC Hluvukani Animal Health Centre
HCC Human cysticercosis
IDI In-Depth Individual Interview
KAP Knowledge, Attitude, Practices
KZN KwaZulu-Natal
MDA Mass drug administration
MDG Millennium Development Goals
MM Mixed Methods
NCC Neurocysticercosis
NGO Non-Governmental Organisation
NTD Neglected Tropical Disease
NZD Neglected Zoonotic Disease
14 | A bbreviations
OH One Health
OIE World Organization for Animal Health
PA Protected Area
PC Porcine cysticercosis
PCR Polymerase chain reaction
PEP Post-exposure prophylaxis
PO Participative Observation
QLR Qualitative Research
RABV rabies virus
RSA Republic of South Africa
TSTC Taenia solium taeniasis/cysticercosis
USD United States Dollar
WHO World Health Organization of the United Nations
While globalisation has generated many benefits for society, it has also created many new challenges, particularly with regard to animal, human, and environmental health leading to a changing and unstable epidemiological situation (Slingenbergh et al., 2004). Neglected Zoonotic Diseases (NZDs) are common where poverty, reliance on livestock or wildlife for social and financial capital, and the close proximity of people and their animals favour complex transmission (Mableson et al., 2014). Transmission patterns of NZDs are bound by a complex interplay of factors related as much to the individual as to the physical, social, cultural, political and economic environments (Allotey et al., 2010). For most of the NZDs known today, we have the methods and technologies to identify the causative agent, we understand the mechanism by which pathology is induced and have developed treatments (drugs, vaccines, medical or surgical procedures) to cure, manage or control. Yet, for many of them, such as echinococcosis (Deplazes et al., 2017), Taenia solium taeniasis/cysticercosis (Torgerson et al., 2015; de Coster et al., 2018) and rabies (Hampson et al., 2015), the estimated health and economic burden remain globally heavy and the control attempts among marginalised populations in low and middle-income countries remain unsustainable and unsuccessful. Indeed, effectively moving control tools and approaches from research based initiatives to government led large scale and sustained programmes is a complicated socio-political process (Bardosh, 2018). Additionally, to translate tools adapted to local realities into more global control programmes while remaining pertinent locally is extremely challenging.
The unique attributes of (N) ZDs and the shifting sociocultural contexts, reoriented the debates around health and disease requiring us to move beyond what some consider the traditional boundaries of the discipline (Brown and Nading, 2019). Within the “One Health” (OH) concept, which aims to drive improvements in human, animal and ecological health through an holistic and integrated approach, this doctoral project documents the extent of the human-animal-ecosystem interface of three NZDs (echinococcosis, taeniasis-cysticercosis and rabies), each one in a specific endemic setting in Morocco, Zambia and South Africa, respectively, from a socio- anthropological perspective. The project aims at assessing cultural, cognitive and 16 | General Introduction social drivers explaining people’s behaviour with regard to animal husbandry, zoonoses and their control in their specific ecosystem while demonstrating the added value of integrating social and biological perspectives in zoonotic disease control. We thus argue for a deeper analysis of culture and social practice to be included in interdisciplinary dialogue and in the framing of health research.
Divided into three sections, we begin by considering existing work done on NZDs and medical anthropology by starting with the general context of NZDs and the OH concept; next we continue with the clarification of the current epidemiological situation and existing control measures for each of the three studied NZDs, namely cystic echinococcosis, Taenia solium taeniasis/cysticercosis and rabies; and end with the review of the actual role of anthropology in NZDs integrated control and OH. Before presenting the results of the three socio-anthropological studies, we introduce what is qualitative research and the methods used to collect our data, including ethical considerations and researcher’s reflexivity. Finally, the results of our studies and their limitations are discussed following a cross-case analysis allowing us to highlight the importance of including the socio-anthropological approach to contextualise the dynamic of transmission among livestock owners and their community, to identify facilitating factors and barriers to interventions and to support efforts and recommendations to control NZDs that operate in challenging circumstances and with marginalised populations in order to finally better fit community needs. The questions and challenges raised about the interdisciplinary dialogue between social and medical rationales are also discussed.
References
Allotey, P., Reidpath, D., Pokhrel, S., 2010. Social sciences research in neglected tropical diseases 1: the ongoing neglect in the neglected tropical diseases. Health Res. Policy Syst. 8, 1-8. Bardosh, K.L., 2018. Towards a science of global health delivery: A socio-anthropological framework to improve the effectiveness of neglected tropical disease interventions. PLoS Negl. Trop. Dis. 12, e0006537. Brown, H., Nading, A.M., 2019. Introduction: Human Animal Health in Medical Anthropology. Med. Anthropol. Q. 33, 5–23. de Coster, T., Van Damme, I., Baauw, J., Gabriël, S., 2018. Recent advancements in the control of Taenia solium: A systematic review. Food Waterborne Parasitol. 13, e00030. General Introduction | 17
Deplazes, P., Rinaldi, L., Alvarez Rojas, C.A., Torgerson, P.R., Harandi, M.F., Romig, T., . . ., Jenkins, E.J., 2017. Global Distribution of Alveolar and Cystic Echinococcosis. Adv. Parasitol. 96, 315–493. Hampson, K., Coudeville, L., Lembo, T., Sambo, M., Kieffer, A., Attlan, M., . . ., Dushoff, J., on behalf of the Global Alliance for Rabies Control Partners for Rabies Prevention, 2015. Estimating the Global Burden of Endemic Canine Rabies. PLoS Negl. Trop. Dis. 9, e0003709. Mableson, H.E., Okello, A., Picozzi, K., Welburn, S.C., 2014. Neglected Zoonotic Diseases-The Long and Winding Road to Advocacy. PLoS Negl. Trop. Dis. 8, e2800. Slingenbergh, J.I., Gilbert, M., de Balogh, K.I., Wint, W., 2004. Ecological sources of zoonotic diseases. Rev. Sci. Tech. 23, 467–484. Torgerson, P.R., Devleesschauwer, B., Praet, N., Speybroeck, N., Willingham, A.L., Kasuga, F., . . ., de Silva, N., 2015. World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis. PLoS Med. 12, e1001920.
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The label ‘Neglected Zoonotic Diseases’ (NZDs) covers a number of zoonoses primarily endemic to developing countries, with devastating impact on poor and marginalised communities, underestimated burden and low rank on the global health priorities agenda (WHO, 2006; 2009; 2011a). NZDs are defined by Choffnes and Relman (2011) as “diseases transmitted between animal and human hosts — through direct contact, via the environment or sometimes by means of a vector, or carrying species — that are endemic in many developing countries of Africa, Asia, and South and Central America.”
The control of NZDs was identified as a “route to poverty alleviation” by the World Health Organisation in the attempt to meet the Millennium Development Goals (WHO, 2006). This is because of the importance of interactions between human, wildlife and domestic animal populations in developing countries and the concerns about the impacts of neglected, endemic and occasionally epidemic zoonotic pathogens, particularly in marginalised and impoverished communities (Molyneux et al., 2011). In a more system thinking perspective, not only these are diseases generating poverty, they are also the result of poverty generated by broader socio-political and economical drivers. See Dzingirai and all (2017) on how political interests, commercial investments, conflict and securitization do generate patterns of vulnerability, by reshaping the political ecology of disease landscapes, influencing traditional coping mechanisms and affecting health service provision and outbreak responses. These different features raise a growing challenge to the life sciences to understand how these pathogens crossing species barriers are interwoven into complex, non-linear and multifaceted biosocial dynamics that mediate their spread and control (Keck and Lynteris, 2018; Bardosh et al., 2016).
1.1.1 The “Zoonotic” component
The definition of zoonosis has been unstable since its first articulation in the second half of the nineteenth century (Keck and Lynteris, 2018), challenged at its core by the Literature Review | 21 human–animal distinction1 (Woods et al., 2018). We have opted to approach a zoonosis as a disease that is harboured and naturally transmitted directly or indirectly (e.g., by vectors) between vertebrate animals and humans. Nearly 875 (60%) of the 1,461 infectious diseases of people are said to be of animal origin (Berthe et al., 2018). According to a literature review of Taylor et al. (2001), among these zoonotic species identified, 32% are helminths, 31% are bacteria or rickettsia, 19% are viruses or prions, 13% are fungi and 5% are protozoa. Hence, the zoonotic pathogens2 largely confined to animal reservoirs (97%) fit a wide array of epidemiological situations (Slingenbergh et al., 2004), which makes their control complex as the majority (61%) are transmitted by indirect contact (Taylor et al., 2001) through food, water, and the environment.
Endemic zoonoses exert a major morbidity/mortality burden worldwide, amounting to about 1 billion cases of illness and millions of deaths every year (Grace et al., 2012a), but also a major economic burden that extends beyond pure medical costs such as, losses in trade and tourism (Cascio et al., 2011), losses in livestock productivity, decreased carcass value, and deadly epidemics (Okello et al., 2015). Echinococcosis for example, imposes an economic burden in developing countries estimated at USD 2 billion in livestock losses3 (Torgerson and Macpherson, 2011). In order to lower the public health burden and because zoonoses control became a global public good (Cutler et al., 2010), there was a pressing need for advocacy from a global community to control not only the (re)‐emerging zoonoses (e.g. SARS coronavirus), that already attracted the attention of the developed world (Molyneux, 2004), but also the NZDs.
The NZDs occupy a unique position at the interface between zoonotic diseases, neglected diseases and poverty, perpetuated by poor health and threats to livelihoods
1 For instance, Schwabe and Kuojok (1981) placing Echinococcus granulosus on an equal ecological standing with the other animals in the cycle of transmission, hence insisting that the line between humans and non-humans was not fundamentally biological but, in large part, a product of human cultural variations (Mason Dentinger, 2018). 2 In contrast to zooanthroponotic pathogens, which are transmitted from humans to animals and which are an understudied aspect of global health, despite their potential to cause significant disease burden in wild and domestic animal populations and to affect global economies (Epstein and Price, 2009). 3 Production-based losses attributable to infected ruminants include: losses from organs (liver especially) condemnation, reduction in carcass weight, decrease in hide value, decrease in milk production and fertility losses (Budke et al., 2006; Battelli, 2009)
22 | C h a p t e r 1
(WHO, 2006). Changes in demographics and the associated alterations to the environment, climate change, global trade and travel, land use changes and human behaviours have led to the increase of zoonoses (Azim et al., 2008; Hassell et al., 2017).
Since 2008, WHO has listed an initial group of “Neglected Zoonotic Diseases” (NZDs) at which to direct concerted efforts: anthrax, bovine tuberculosis, brucellosis, T. solium cysticercosis, cystic echinococcosis (hydatidosis), leishmaniasis, rabies, and zoonotic trypanosomiasis (sleeping sickness) (WHO, 2011a; Mableson et al., 2014). In addition of foodborne trematodiases and zoonotic schistosomiasis, WHO continues nowadays to address echinococcosis, taeniasis/cysticercosis, human rabies transmitted by dogs, zoonotic human African trypanosomiasis and zoonotic leishmaniasis as specific NZDs. Due to the abundance of risk factors, the likelihood of acquiring one (or more) of NZDs within a smallholder rural marginalised community in developing countries remains high. The initial lack of critical research and policy support made the NZDs equally identified as ‘diseases of neglected populations’ (Doble and Fèvre, 2010).
1.1.2. The “Neglected” component
Although the eight Millennium Development Goals (MDG) from 2000 gave new prominence to the health issues affecting the poor, they have mainly focused on the control of HIV/AIDS, tuberculosis, and malaria (Molyneux, 2004; Sachs, 2006; Hotez et al., 2007), concentrating 80% of the funding invested into research and development for diseases of poverty (Moran et al., 2009). The result of this top-down deliberation, rather than informed by inclusive analysis and/or the prioritisation of development needs (Smith et al., 2015), has automatically confined a large group of unspecified diseases to the “other diseases” category in the eyes of the health policy makers and politicians. The MDG omission, and subsequent gaps in coverage and lack of synergies between sectors, induced an advocacy campaign to focus on these “neglected” diseases.
These diseases, under the collective term “Neglected Tropical Diseases” (NTDs), were sharing two important characteristics (Feasey et al., 2010). First, they predominated Literature Review | 23 in tropical regions, where they tended to coexist4. All strongly associated with poverty and flourishing in impoverished environments, remote, rural areas, in urban slums, or in conflict zones (WHO, 2010), they were diseases of the “bottom billion”5 (Collier, 2007; Hotez et al., 2009). Secondly, these diseases had a low visibility in the rest of the world, because they are not considered a threat in resource rich settings, resulting in little incentive for the industry to invest in developing new or better products; and there is little political voice from the people affected or at risk. Hence, they have been neglected by funders, researchers and policy-makers. Lack of reliable statistics has also held back efforts to bring them out of the shadows (Choffnes and Relman, 2011).
Finally, first 13 diseases (Hotez et al., 2006), then 17 diseases6 and recently 18 diseases7, have been clustered under this label of NTDs since the mid-2000s. With the support of the quantifiable value Disability Adjusted Life Years (DALYs)8, this global advocacy for NTDs led to ambitious targets set for 2020 with a varied range of programmes sharing at least one of three goals; control, elimination or eradication. However, a range of gaps has been identified, amongst which gaps mainly raised by the social sciences sector working on controlling NTDs (Parker et al., 2008; Bardosh, 2014) and those concerned with the social determinants of diseases (Waltner-Toews, 2017), such as lack of understanding by programmatic staff of the contexts in which integrated programmes are implemented and divergence between biomedical and local understandings of the disease. Raised regularly in community-based programmes, these issues relate largely to working with communities and health systems within a real life, uncontrolled environment. Also, the lack of communication between the various players – researchers, policymakers, clinicians, public-private partnerships, donors, and patient advocacy groups – represents a significant missed
4 All low- income countries are affected by at least five NTDs simultaneously, and many individuals who live in those countries are concurrently infected by more than one pathogen (WHO, 2006). 5 The poorest one-six of the world’s population endemic in 149 countries. 6 Dengue, rabies, blinding trachoma, Buruli ulcer, endemic treponematoses (yaws), leprosy (Hansen disease), Chagas disease, human African trypanosomiasis (sleeping sickness), leishmaniasis, cysticercosis, dracunculiasis (guinea-worm disease), echinococcosis, foodborne trematode infections, lymphatic filariasis, onchocerciasis (river blindness), schistosomiasis (bilharziasis), soil-transmitted helminthiases (intestinal worms) (WHO, 2010b) 7 With the inclusion of Mycetoma, chromoblastomycosis, other deep mycoses and snakebite envenoming. 8 http://www.who.int/healthinfo/global_burden_disease/GBD_report_2004update_part4.pdf?ua=1
24 | C h a p t e r 1 opportunity for a comprehensive and holistic approach to sustainable outcomes (Allotey et al., 2010). While the period between 2000 and 2015 saw a 21% drop in people requiring mass or individual treatment and care for NTDs (UN DESA, 2017), the 17 Sustainable Development Goals - MDGs’ successors - have still many challenges to reach the 2030 targets and “free humanity from poverty, secure a healthy planet for future generations, and build peaceful, inclusive societies as a foundation for ensuring lives of dignity for all” (UN DESA, 2018). Many of the endemic zoonoses can be treated and prevented, often with very simple technologies (Cleaveland et al., 2017), but not as long as surveillance, diagnostics, interventions, training, programme delivery, and integrated health planning continue to be done separately with regard to public and animal health (Choffnes and Relman, 2011).
Finally, the processes through which the NZD concept has been raised by agencies, and whether these issues were different for NTDs than for other zoonotic diseases; how some NZDs were pushed in international agendas as priorities compared to other NTDs and more generally what the mechanisms are that bring a neglected disease at the agenda of researchers, agencies and policy makers, are all important topics that would be worth to further investigate within a socio-anthropological framework.
1.1.3. The “One Health” approach
It has long been known that many infections cross the species barriers between humans, domesticated animals and wildlife but the view of this has traditionally been somewhat compartmentalised (Hall and Durrheim, 2011). The current global health challenges described above have prompted a call for more holistic, collaborative, action-oriented approaches toward the goal of logical and practical solutions (Osburn et al., 2009). In this light, the concept created and articulated at the Wildlife Conservation Society in the “Manhattan Principles on One World, One Health” for preventing emerging diseases in human and animal populations and maintaining ecosystem integrity (Cook et al. 2004) has seen an unprecedented revival in the last decades. Defined as “One Medicine” by Schwabe (1984), the conceptual thinking of “One Health”, which has evolved in focus and agendas in the last decade, “recognizes that humans and animals do not exist in isolation, but are parts of a larger whole, a living ecosystem, and that the activities of each member affect the others”. Thus, One Literature Review | 25
Health (OH) considers health as a whole: “that of humans, animals, and the environment they exist on” (Kaplan and Scott, 2011). While the focus was mainly on emerging zoonoses, the FAO–OIE–WHO Tripartite Concept Note (FAO et al., 2010) also recognised that OH implementation in developing countries could also serve to address endemic zoonoses. Integrated control and prevention of such diseases was said to be in everyone’s interest, requiring long-term investment from private and public sources (Gibbs, 2014). While the consensus for an integrative approach to health has been consolidated, its underlying principles still need to be clarified (Zinsstag et al., 2011). Complexity, recognized as an inherent characteristic of natural systems (Wilcox and Colwell, 2005); participation as active involvement and engagement of affected interests and stakeholders in framing the problem and the discovery of adaptive responses (Duboz et al., 2018); and transdisciplinarity to bridge science and practice, and fostering the emergence of social learning and collective intelligence via participation, were advanced by Duboz and colleagues (2018) as the three key principles for a practical methodology for an integrated approach to health.
By adopting a longitudinal, contemporary-historical approach, Angela Cassidy’s research explored the emergence of OH (why OH now?) and traced its origins in the histories of human and animal health, global development, conservation, and infectious diseases (Cassidy, 2016). She finally argued that “OH is a response mounted by specific researchers (and policymakers) to problems manifesting at particular times and in particular places” and therefore not “the result of inevitable progress, but a contingent and context-bound activity that is actively and continually created through persuasive rhetoric and alliance-building” (Cassidy, 2018). Today indeed, there is still no generally unique well-established (legitimate) definition of OH but it is framed as “the collaborative efforts of multiple disciplines working locally, nationally and globally to attain optimal health for people, animals and environment” (FAO et al., 2008). Because lacking of a general theory, OH is commonly more perceived as a “labelled set of activities and agendas” which is still evolving conceptually under the influence of health challenges, scientific advances, but also political, economic, environmental and professional priorities (Bresalier et al., 2015). On the other hand, not having a unique definition can be convenient to have an open movement, allowing take-up for different types of stakeholders and from different socio-cultural, economical and political contexts.
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However, the “One Health Approach” has remained little known outside of special sectors and institutions concerned with infectious diseases and especially zoonoses (Rabozzi et al., 2012). Its operationalisation has so far proven challenging and was mainly provided at the start via isolated case-studies exemplifying its added value (Zinsstag et al., 2012; Okello et al., 2015). Many practical and methodological questions and challenges about how and what levers are needed to foster the necessary interdisciplinary dialogue have also been raised (Frickel et al., 2016), together with how to evaluate them (Rüegg et al., 2018). Nowadays several frameworks that promote a OH study design covering all three health domains has been provided (Lebov et al., 2017; Berthe et al., 2018), as well as several methodologies dedicated to the implementation of interdisciplinary approaches to accompany social actors and principles of integrated approaches to health (see above), notably the use of Systems Thinking as a set of tools for integration and participatory modelling methods to actively involve affected interests and stakeholders to ground the field of inquiry in a specific social-ecological context (Binot et al., 2015; Duboz et al., 2018; Wilcox et al., 2019). Additionally, the linkages of biodiversity and human health have gained important attention in science, policy and society at large, as well as the linkages within a One Health/EcoHealth framework, integrating and mapping future avenues together with approaches to health that have emerged over time such as OH, EcoHealth or Planetary Health (Keune et al., 2017). Whilst having different origins and revealing similarities and differences at the theoretical conceptual level (see Lerner and Berg (2017) and Roger and all (2016) for a more detailed comparison between their set of values and focus such as the status of animal health), these approaches aimed at converging in emphasising “a holistic understanding of health beyond the purely biomedical” (Zinsstag et al., 2012; WHO and CBD secretariat, 2015).
Three neglected zoonotic diseases were studied in specific endemic settings: echinococcosis (Morocco), Taenia solium taeniasis-cysticercosis (Zambia) and rabies (South Africa). Despite available preventive and control tools and approaches, their burden is still heavy (WHO, 2006; 2009; 2011a; 2015a). Included in a “priority NZDs Literature Review | 27 portfolio” of the tripartite FAO-OIE-WHO because of their global importance at the human-animal-environment interface (Landford and Nunn, 2012), these three diseases, fitting well with the mantra of OH, present control challenges requiring new ways of linking disciplines, expertise, local authorities and populations in animal and human health (Lee & Brumme, 2013; Okello et al., 2014).
1.2.1 Cystic echinococcosis
1.2.1.1 Echinococcus granulosus, the ‘dog tapeworm’
Pathogen
Cystic echinococcosis (CE), also known as human hydatidosis, is a neglected zoonotic disease caused by the cestode Echinococcus granulosus (family Taeniidae) and transmitted predominantly in life-cycle patterns involving domestic dogs and livestock. Regarding sylvatic cycles for E. granulosus, only one, clearly independent from domestic transmission has been documented in Australia (dingo - macropodid) although a number of wild mammal species can locally contribute (Romig et al., 2017). In the domestic cycle, dogs are the definitive hosts while domestic ungulates act as the intermediate hosts. Sheep are the most important intermediate hosts, but also other livestock species such as, goats, cattle, swine, Equidae, camels and yaks can be infected (Romig et al., 2017). Humans are accidental dead-end9 intermediate hosts.
Life cycle
The adult E. granulosus (1) inhabits the small intestine of the definitive host. Gravid proglottids, containing embryonated eggs (2) are passed in the dog’s faeces. After oral uptake by a suitable intermediate host, the egg hatches in the small intestine and releases an oncosphere (3) that penetrates the intestinal wall and migrates through the bloodstream to establish in various internal organs, especially the liver and lungs. The oncosphere will develop into the metacestode larval stage, a large tissue cyst (4) that grows slowly and after months/years can reach maturity (hydatid cyst) and contain protoscolices. When organs containing hydatid cysts are eaten by dogs each protoscolex (5) (attach to the intestinal mucosa (6)) has the potential to develop into
9 ‘Dead-end hosts’ refer to host species that can be infected with the metacestode, but that are clearly not part of the life cycle (Romig et al., 2017).
28 | C h a p t e r 1 an intestinal tapeworm within 4 to 7 weeks (1). Accidentally, eggs can be ingested by humans [2], also leading to the development of hydatid cysts [3] in various organs [4] (Eckert and Deplazes, 2004; Agudelo Higuita et al., 2016).
Figure 1.1 Life cycle of Echinococcus granulosus (Life cycle image and information courtesy of DPDx - https://www.cdc.gov/parasites/echinococcosis/biology.html#)
Epidemiology and distribution
Considerable genetic and phenotypic variability exists within the species E. granulosus, resulting in the actual recognition of the following strains/species (Agudelo Higuita et al., 2016), E. granulosus sensu stricto (s.s.) (G1-3), E. equinus (G4), E. ortleppi (G5), and E. canadensis (G6-10), all referred to as E. granulosus s.l. (Craig et al., 2017; Romig et al., 2017). The several strains identified (genotypes G1 to 10) show differences in intermediate host spectrum, biological characteristics and geographical distribution (Moro and Schantz, 2009; Deplazes et al., 2017). Globally, most human cases of CE are caused by the “sheep strain” (G1) of E. granulosus s.s., which has the widest geographical distribution of all Echinococcus species (Romig et al., 2017). With 88% of 1,661 human CE cases characterised to species level worldwide, G1 has by far the largest impact on public health (Alvarez Rojas et al., 2014). Epidemiological data suggest that E. granulosus s.s. is particularly well adapted to sheep as intermediate hosts, which is reflected in high prevalence (Cardona and Carmena, 2013; Deplazes et Literature Review | 29 al., 2017) and high cyst fertility rates or availability to dogs compared to other livestock species (Romig et al., 2017). E. canadensis G6 (“camel strain”) and G7 (“pig strain”) are responsible for 7.3% and 3.7% of human infections worldwide, respectively (Agudelo Higuita et al., 2016).
The highest prevalence of CE in humans and animals is found in South America (Peru, Chile, Argentina, Uruguay, southern Brazil), the Mediterranean region, central Asia, western China, and East Africa (Moro and Schantz, 2006; Agudelo Higuita et al., 2016). In North Africa and the Middle East the incidence rates in humans can exceed 50 per 100,000 person-years (Sadjjadi, 2006; Craig et al., 2007; WHO, 2011b), being for the two last decades the areas where CE has been one of the most important zoonotic diseases (Deplazes et al., 2017).
Figure 1.2 Distribution of Echinococcus granulosus and cystic echinococcosis, worldwide, 2011 (http://www.who.int/echinococcosis/Global_distribution_of_cystic_echinococcosis_2011.p df)
Legend retrieved from WHO (2010): Hight endemic areas: The definition applies only to areas within a specified endemic country. High endemicity areas involve ≥1 state, region, province or district where E. granulosus prevalence in dogs exceeds 5- 10% and where the prevalence of human cystic echinococcosis (hydatidosis) is
30 | C h a p t e r 1 greater than 1–5 cases/100.000 inhabitants annually; Present: E. granulosus is known to be endemic in at least some areas of the country. Domestic animal (and possibly wildlife) and human cystic echinococcosis (hydatidosis) occur regularly; Suspected: E. granulosus may not be recorded in official data or publications, but may occur in wildlife and possibly at low prevalence in domestic animals. Human cystic echinococcosis (hydatidosis) appears not to occur; Rare/Sporadic: E. granulosus has been recorded at low prevalence in domestic animals and may be transmitted in wildlife populations. Human cystic echinococcosis (hydatidosis) cases are only occasionally reported; Probably absent: Countries or territories with no confirmed identifications or reports of E. granulosus in indigenous domestic or wild animal populations. Human cystic echinococcosis (hydatidosis) has not been reported.
Risk factors
Socioeconomic and cultural characteristics are among the best-defined risk factors for CE throughout its broad global range: uncontrolled dogs living closely with people because of access to food, uncontrolled slaughter of livestock, and poor sanitary living conditions (Schantz, 2006). Behavioural, biological and ecological factors are therefore involved in the transmission of this parasite (Otero-Abad and Torgerson, 2013). Infection of dogs occurs by feeding of contaminated offal after home slaughter or by inappropriate discarding practices of infected offal, improper management of abattoirs and slaughterhouses (where roaming dogs have access to condemned offal), or by stray or semi stray dogs scavenging on livestock carcasses left on the pasture (Romig et al., 2017). Humans acquire infection in the same way as other intermediate hosts via intake of egg-contaminated water or food (and also uncooked and unwashed food) or through contaminated soil or objects (with subsequent ingestion of eggs), including dogs’ mouth and fur. Women who are involved in agricultural activities and children in the course of playful and intimate contact with infected dogs are most at risk (Craig et al., 2008). Eggs of E. granulosus can remain viable and infective for months in a moist environment at lower ranges of temperatures (about +4°C to +15°C) (Eckert et al., 2001) and within 180 m of the site of deposition (Bourée, 2001).
Impact
CE has a cosmopolitan distribution and mainly affects pastoral and poor rural communities where people raise livestock in close contact with dogs fed on raw offal Literature Review | 31
(Torgerson and Budke, 2003; Craig et al., 2008). Whereas animals rarely show clinical signs, clinical signs and symptoms in humans may develop months or years after infection and are caused by the expanding cysts and inflammatory reactions (Eckert and Deplazes, 2004). It is a global health problem but also represents a serious animal production concern in many rural areas of the world by causing important economic losses derived from decreased productivity, decreased fecundity and condemnation of viscera (liver, lungs or other infected organs) in the abattoir (Cardona and Carmena, 2013). The latest estimate of the global human disease burden of CE is 188,000 new cases per annum resulting in 184,000 DALYs (0.98 DALYs per case) (Torgerson et al., 2015), and an annual cost of USD 3 billion attributed to health care and livestock losses (Alvarez Rojas et al. 2014; WHO, 2017).
Diagnosis and treatment
The standard diagnostic method for E. granulosus infection in dogs used in prevalence surveys was arecoline purging (Craig et al., 1995). Good progress has been made in immunodiagnosis targeting parasite antigens in dog faeces (coproantigen) (Eckert et al., 2001). In intermediate hosts, the diagnosis of CE is mainly based on necropsy findings although for sheep and goats, ultrasound examination may be used. The diagnosis of CE in humans is based on the identification of cyst structures by imaging techniques, predominantly ultrasonography (US), computerised tomography or magnetic resonance imaging, and by immunodiagnosis (WHO, 2011b).
Classification of cyst types is an important basis for human treatment decisions which are, surgery, percutaneous treatment of the hydatid cysts with the PAIR10 technique, long-term therapy with anthelmintic drugs (albendazole alone or in combination with praziquantel) and “watch and wait” strategy with clinical monitoring (Eckert and Deplazes, 2004).
Cystic echinococcosis in Morocco
In 2012, Morocco recorded an average of 5.2 surgical cases per 100,000 inhabitants and a mortality rate estimated at 2-3% (DELM, 2012) in the whole country. The last ultrasound campaigns conducted in 2014 in the mid-Atlas, found an overall
10 The PAIR technique consists of puncture, aspiration, injection and re-aspiration of hydatid cysts.
32 | C h a p t e r 1 abdominal CE prevalence of 1.9% with significantly higher values in rural communes (Chebli et al., 2017). Expenses due to CE surgery were estimated at USD 2,550,000 (Herrador et al., 2016). Prevalence in animals, according to a rural and urban abattoir- based study (via post-mortem inspection) conducted in five regions of Morocco (data from 2001 to 2004), ranged from 23.0% in cattle, 17.8% in equids, 12.0% in camels, 10.6% in sheep to 1.9% in goats. In rural areas, one dog in two carried E. granulosus (Azlaf and Dakkak, 2006). A recent study conducted between 2010 and 2011 in the province of Sidi Kacem (northwest Morocco) found a prevalence of E. granulosus infection in owned dogs of 35.3% (Dakkak et al., 2017). Although the Moroccan Government established in 2007 an “Inter-Ministerial Committee” and guidelines to combat CE (CILCH, 2007), the disease remains a significant public health problem in this country.
In Morocco, the persistence and spread of CE is closely associated with the following epidemiological factors and drivers (Kachani et al., 2003; Azlaf et al., 2007; Dakkak, 2010; DELM, 2010; El Berbri et al., 2015a; Craig et al., 2017): (1) contact between humans/ livestock and infected dogs: extensive sheep breeding, high number of stray dogs and close proximity of un-dewormed owned dogs living with humans and livestock; (2) an abundance of dogs (1.8 dogs per household) mainly free roaming; (3) poor knowledge of CE (50% of people are unaware of the disease) among livestock owners, coupled with illiteracy; (4) inadequate abattoir infrastructure lacking appropriate facilities and hygiene to which free-roaming dogs have easily access; (5) little or no veterinary inspection at slaughter; (6) behaviours and practices of the rural population: animal slaughtering in fields or at home for family and religious occasions (e.g. the feast of Eïd el-Kebir), habit of leaving carcasses of livestock on the pastures or in rivers, poor human hygiene practice (hand and vegetable washing); (7) the mode of water supply through irrigation thereby disseminating Echinococcus eggs in the environment (soil, food, drinking water) and (8) general very basic infrastructures (e.g. open air uncontrolled dumping of households and markets waste for the sustenance of the stray dog population and access to potential infected raw offal) and limited economic resources in rural and suburban areas. Literature Review | 33
1.2.1.2 Control measures
The biological cycle can be interrupted at various points but controlling the parasitic infection in domestic animals is crucial to reduce the incidence of human disease. Hence the main target for intervention is the definitive host (dog) with the aim to reduce or eliminate adult worm burdens (Brown, 2004) and then the intermediate hosts (sheep and other livestock). The three main existing approaches for dogs are: (1) treatment by arecoline or the anthelmintic drug praziquantel (PZQ); (2) dog population management by culling stray dogs (by shooting or capture and euthanise), spaying or castration (Larrieu and Zanini, 2012) and immunocontraception (Johansen and Penrith, 2009; Lembo et al., 2013) and (3) avoiding dogs having access to infected organs. Targeting intermediate hosts may be undertaken through (1) classical meat inspection at slaughter and condemnation and deconstruction of infected offal; (2) using an infection preventive vaccine (Eg95) based on a cloned recombinant antigen derived from the parasite egg (oncosphere) (Larrieu et al., 2015); (3) using anthelmintics for livestock and/or (4) livestock management by husbandry practices that reduce numbers of older sheep (that have the greatest viable metacestode burden (Torgerson et al., 2009)). For the two latter control measures, respectively chemotherapy of CE in livestock and removing old animals (such as through culling), there is no effective, practical method available nor attempted in practice that could be implemented as part of a CE control programme at this time (Craig et al., 2017). The other existing preventive measures encompass tailored health-educational measures, good personal hygiene, and surveillance (Eckert et al., 2001; Otero-Abad and Torgerson, 2013). To ensure passive/active surveillance of CE (abattoir surveillance for infection in livestock, and hospital surveillance for human infection), actual tools, not yet widely available, include the use of portable ultrasound for human screening within endemic communities, a laboratory-based test (coproantigen enzyme-linked immunosorbent assays (ELISA)) to replace the arecoline purgation test in dogs, computer-based modelling of cost- benefit for interventions and transmission dynamics and predictive modelling for intervention combinations (Torgerson and Heath, 2003; Craig et al., 2007; Craig et al., 2017). For example, simulation models for combined praziquantel deworming of dogs and vaccination of sheep indicate improved efficacy (Torgerson and Heath,
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2003; Lightowlers, 2012). Integrating hydatid control measures with the control of other zoonotic diseases or public health programmes (i.e., ‘One Health’’ approaches) is expected to be more efficient and cost-effective (Narrod et al., 2012). Although so far there are few examples of this regarding CE (Zinsstag et al., 2006; Rabinowitz et al., 2013), the combination with rabies control to manage the size of dog population was recommended to be efficient in place where rabies and CE are co-endemic (Kachani and Heath, 2014). Joshi et al. (2012) also provided a compelling example of the benefits of more participatory, action-research approaches for CE by engaging a local NGO and enrolling as ‘co-researchers’ different stakeholders (government authorities, community leaders and a wide variety of those involved in animal slaughter) in urban areas of Nepal over more than 10 years. Through sustainable platforms established to enhance the local capacity of these diverse social groups, this project led to a significant drop in CE, as well as improvements in garbage collection, the aesthetics of the urban environment and livelihood impacts for butchers and reductions in caste-based discrimination (Joshi et al., 2012).
Although new tools and approaches have become available to assist in planning and implementation of interventions and surveillance strategies since the 1970s (Craig et al., 2017), results derived from epidemiological studies continue to report logistics barriers for mass arecoline purgation and regular mass PZQ treatment of owned dog populations for example (Cabrera et al., 2002), problems of ethics and availability of humane means for dog population management (Kachani and Heath, 2014), as well as the maintenance of risk factors such the ones facilitating the contact of dogs with raw offal (Li et al., 2015), and finally gaps of knowledge of the disease and its transmission among butchers (Besbes et al., 2003), medical professionals (John et al., 2008) and livestock owners (El Berbri et al., 2015).
Currently, the WHO and other stakeholders are pushing towards the validation of effective CE control strategies by 2020 by assisting countries to develop and implement pilot projects such as in Morocco (WHO, 2017). The focus of these prevention programmes is on deworming dogs, improving slaughterhouse practices, public education and dog population management, with a possible role for the vaccination of lambs. For the good implementation of abovementioned control measures several conditions are required. Among others: good organisation, literate Literature Review | 35 rural population compliance, general community approval, participatory planning, cooperation between veterinary and municipality sectors (well-structured agricultural sectors), trained manpower, sustainability and budget of application for long term control, information on the size and location of owned or stray domestic dog populations, hospital-based retrospective and prospective data sets, a set of government meat inspection enforcements, hygienic supervised well equipped slaughter facilities, experienced and well-trained veterinary and medical personnel (Craig et al., 2017).
However, to ensure the optimisation of these pilot interventions, as well as their scaling-up, biomedical expertise will not be enough. Social science studies, for the most part absent from the literature (Bardosh, 2014), would complement epidemiological studies by commenting on the ‘un-cooperative’ behaviour of butchers, the ‘very poor’ inspection implementation of veterinary staff and the physical ‘inadequate’ design infrastructures located within political ‘tensions’ between ministries contributing to E. granulosus transmission (Biu et al., 2006; Kebede et al., 2009; Komba et al., 2012), and by exploring sensitivity to local social determinants, relations, logics and conditions (Bardosh et al., 2016). Local institutional logics are usually mediated by prevailing risk perceptions, economic practices and local socio-political norms. This is best explained by the difficult social position of the veterinary technicians tasked by the state to inspect, and condemn livestock when attempts to remove cysts were perceived as a threat to the profits of local butchers, who would resist inspections to maintain their own informal practices (Bardosh et al., 2016). Even strict regulations as the ones in the European Union are no guarantee to be followed, hence that transmission of echinococcosis will be prevented. Italy, for example, has one of the highest incidences of human CE in the European Union with over 1000 cases treated surgically each year (Brundu et al., 2014).
Health education and community knowledge have the potential to reduce risky behaviour of humans, for example, unhygienic slaughter and dog contact, but education is probably more important for community acceptance and voluntary participation in long-term hydatid-control programmes (Craig et al., 2017). However, education efforts, where CE is often highly endemic (Ito et al., 2003), are unlikely to
36 | C h a p t e r 1 have much impact without addressing other systemic barriers. It is greatly reductionist to defer “ignorance” as the main driver of informal (and ‘unhygienic’) slaughter practices while the local logics (forms of cognitive reasoning that justify certain pathways of action and response), infrastructures and rationales that mediate and reproduce these practices were overlooked (Bardosh et al., 2016). Finally, “top- down” disease management techniques aimed at addressing informal practices can be very ineffective, predominately due to divergences between mainstream biosecurity narratives and approaches and the local interests and routines of smallholder farmers (Leach & Scoones, 2013). The benefit of a systemic approach as well as the importance of adopting a problem solving approach is in line with the three “EcoHealth” methodological pillars which are: Transdisciplinarity implying an inclusive vision of ecosystem-related health problems and requiring the full participation of researchers, community representatives, and decision-makers; Participation, aiming to achieve consensus and cooperation, not only within the community, scientific, and decision-making groups, but also among them; and Equity, involving analysis of the respective roles of men and women, and of various social groups (Lebel, 2004).
1.2.2 Taenia solium taeniasis/cysticercosis
1.2.2.1 Taenia solium, the ‘pork tapeworm’
Pathogen
Taeniasis/cysticercosis is a neglected parasitic zoonosis caused by Taenia solium, a cyclophyllid cestode of the family Taeniidae. Taenia solium has a two-host life cycle (Fig 1.3) involving humans as the definite hosts and pigs as the intermediate hosts. This parasite prevails in many developing countries where open defecation and free roaming of pigs maintain the transmission cycle (Coral-Almeida et al., 2015). Infection in pigs results in porcine cysticercosis (PC), a tissue infection with the metacestode larval stage or cysticercus. In humans the adult tapeworm causes intestinal taeniasis. Humans can also develop cysticercosis upon ingestion of worm eggs (Gonzales et al., 2016). Severe neurological disorders may develop when cysticerci lodge in the central nervous system (neurocysticercosis, NCC), leading to various neurological signs and symptoms, most commonly epileptic seizures and chronic headaches Literature Review | 37
(Carabin et al., 2011; Murrell et al., 2005). While PC is mostly asymptomatic, heavy infections in pigs can also result in seizures and behavioural changes (Trevisan et al., 2017).
Life cycle
Figure 1.3 Life cycle of Taenia solium (Retrieved from https://www.cdc.gov/dpdx/cysticercosis/)
Taeniasis occurs only in the human host, following the consumption of raw or undercooked pork infected with cysticerci, leading to the development of a long, flat, segmented worm in the small intestine (Fig 1.3 where numbers from (1) to (9) refer to the different components of the life cycle). The adult tapeworm develops up to 1 to 5 m in length and is composed of 700 to 1000 proglottids, among which the gravid ones contain between 50,000 and 60,000 eggs each, and remain viable for at least one year (Flisser, 2013). A human Taenia carrier releases gravid proglottids/infective eggs via the stool into the environment. These eggs can survive for months in moist
38 | C h a p t e r 1 conditions. Pigs and humans become infected by ingesting eggs (or gravid proglottids for pigs). When a pig ingests these eggs via its coprophagic behaviour or through contaminated feed and water, oncospheres are released in the gastrointestinal (GI) tract, which migrate through the GI wall and reach various tissues where they develop in the metacestode larval stage (cysticercus). Cysticerci develop in muscle, subcutaneously, and in other tissues causing cysticercosis (Murrell et al., 2005) (PC). In humans, cysticercosis may also occur upon incidental ingestion of eggs via faeco- oral contamination, via contaminated food or water or, possibly, in tapeworm carriers, from proglottids carried into the stomach by reverse peristalsis. Similar to infection in pigs, released oncospheres migrate to striated muscles, as well as to other tissues, where they develop into cysticerci. In humans, the cysticerci have a predilection to establish in the central nervous tissue causing NCC.
Epidemiology and distribution
Historical data of swine domestication, distribution of pigs and colonisation suggest that T. solium was introduced into Latin America and Africa from different regions of Europe during the colonial age, which started 500 years ago, and that the tapeworm of another origin independently spread in Asian countries (Nakao et al., 2002). Cysticerci from these two genotypes of T. solium currently infect pigs worldwide but mainly in developing countries (Donadeu et al., 2016), constituting a serious public health problem and socioeconomic obstacle for pig breeders (Assana et al., 2013; Michelet and Dauga, 2012; Samorek-Pieróg et al., 2018). In Latin America, sub- Saharan Africa (SSA), South and South East Asia (apart from the Muslim areas), T. solium infection and the resulting disease NCC are endemic where pigs are raised as a food source (Murrell et al., 2005; Djurković-Djaković et al., 2013). However, T. solium taeniasis/cysticercosis (TSTC) is also re-emerging in a number of non-endemic countries reported by an increasing number of cases detected in the United States and Europe, primarily because of increased human migration (immigration, travel and local human to human transmission) (Bobes et al., 2014; Gabriël et al., 2015).
All age groups of pigs can be infected; however, prevalence is significantly higher in pigs that are more than 4 months old (Boa et al., 2006) and over-dispersion has been clearly demonstrated, with a very small number of animals harbouring massive infections, and most of the infected pigs harbouring only a few viable cysts (Gilman et Literature Review | 39 al., 2012). The prevalence of PC is typically much higher in endemic areas than either human taeniasis or human cysticercosis (HCC) (WHO, 2015b). Depending on the region, study population and diagnostic technique used, apparent prevalence of human taeniasis is variable across endemic areas ranging between 0% and 13.9% in Africa, 0.2% and 17.2% in Latin America and 0% and 3% in Asia (Coral-Almeida et al., 2015). The same recent meta-analysis reported prevalence of HCC ranging between 0.68% and 34.5% in Africa, 0.9% and 31.2% in Latin America and 0.6% and 19.2% in Asia (Coral-Almeida et al., 2015). Since 2000, prevalence of PC in Africa has been up to 64.6% (Krecek et al., 2008), in South and Central America up to 65.4% (Cortez- Alcobedes et al., 2010), whereas in Asia it has been up to 26% (Prasad et al., 2002).
Figure 1.4 Worldwide distribution of Taenia solium, 2015 (https://www.who.int/taeniasis/Endemicity_Taenia_Solium_2015.jpg)
Risk factors
TSTC is tightly bound to less developed countries with particular cultural, socio- economic, and sanitary conditions affecting mainly the health and livelihoods of subsistence farming communities (Willingham and Engels, 2006). T. solium is transmitted mainly in rural regions where pigs are free roaming and have access to human faeces, due to lack of latrines or type and availability of latrine used and
40 | C h a p t e r 1 outdoor human defecation (Donadeu et al., 2016; Kungu et al., 2017; Samorek-Pieróg et al., 2018). Human to human infection occurs through deficient individual and household sanitation and poor hygiene when handling food. In endemic areas, transmission and persistence of the parasite is clearly related to human behaviours, especially sanitary and eating habits and food preparation (e.g. raw or undercooked grilled pork) for which ethnicity, culture and religion all play important roles (Macpherson, 2005). Human activities such as, husbandry methods (e.g. allowing pigs to roam freely, deliberate use of human faeces for fertilising agricultural fields or feeding pigs), use of untreated or partially treated wastewater in agriculture, home or clandestine slaughtering, unavailable meat inspection services or lack of trained and qualified meat inspectors, selling of infected pork, and general poor and inadequate sanitation in affected communities are important risk factors (Sikasunge et al., 2007; Gweba et al., 2010; Krecek et al., 2012; Michelet and Dauga, 2012; Weka et al., 2013; Mwape, 2018). In addition to gaps of knowledge among livestock owners regarding the complete life cycle of the parasites, especially on how pigs get the infection (Assana et al., 2013), illiteracy, little or unadapted attention to health education (Johansen et al., 2017) as well as limited investments in pig production (e.g. insufficient human resources for slaughterhouse inspection and for managing herds) also constitute risk factors (Assana et al., 2013; Melki et al., 2018). For reasons unconnected to their economic importance such as, the belief that pigs compete with humans for food, and probably also for religious reasons (important Muslim population in Africa for example), pigs are the least studied species regarding distribution, productivity and genetic affiliation of all the major species of domestic livestock in Africa (Blench and MacDonald, 2000).
People living in a household with someone who has a tapeworm have a much higher risk of getting cysticercosis (Coral-Almeida, 2015). Intestinal taeniasis is usually asymptomatic and proglottids of T. solium are mostly passively released with the stools (Allan et al., 1996). Therefore, in community settings many, if not most, carriers of T. solium will neither look for medical care, nor notice the tapeworm segments in their stools, especially when using pit latrines. However, identification of a tapeworm infection is important because of the risk of cysticercosis in the carrier or among close contacts (Garcia et al., 2003). Literature Review | 41
Impact
As a result of the lack of epidemiological information on the distribution of TSTC in developing countries, its burden (especially at the local level) and its economic impact are largely unknown in many regions (WHO, 2015b; Johansen et al., 2017). Yet, results of a study coordinated by the Foodborne Disease Burden Epidemiology Reference Group (FERG) ranked T. solium as the most important foodborne parasite in the world and fourth among all important foodborne pathogens (WHO, 2015a). Every year, TSTC is estimated to cause a great number of NCC-associated epilepsy cases (53 million infected people) and 28,000 human deaths, resulting in 2.8 million disability- adjusted life years (DALYs) (Torgerson et al., 2015; Havelaar et al., 2015). In endemic areas, NCC is the most important parasitic neurological infection, to which almost 30% of acquired epilepsy cases are attributed (Ndimubanzi et al., 2010).
In addition to economic losses in the public health sector, related to NCC, there is also the considerable economic losses farmers face from not being able to sell infected pigs, or not obtaining the correct carcass value (reduced meat value and carcass condemnation) (Gabriël et al., 2017). In some countries, pigs with visible infections, detected by lingual palpation or mucous membrane inspection, fetch a lower price (Grace et al., 2012a). This was estimated as a 30% reduction in price in Cameroon (Praet et al., 2009) and of 46% in a study in Tanzania (CIRAD, 2012). In Peru, an ‘economic cycle’ of T. solium transmission has been described, highlighting difficulties in ensuring a safe pork consumption in endemic areas as there is a clear economic motivation for small scale pork producers to minimise commercial losses by routing pigs into the ‘unofficial’ market (Pawlowski et al., 2005).
Compared to simply calculating the total costs of controlling disease in humans and in animal reservoirs (Zinsstag et al., 2007), there is a broad consensus that the economic analysis of zoonoses control programmes should be based on a holistic measurement of ‘total societal benefits’ (Okello et al., 2018) and by such include the health and economic burden for both the human and veterinary sectors (e.g. cost-of- illness, losses in the agricultural and food sectors and trade impacts) rather than population health burden (e.g., expressed as DALYs) alone (Torgerson, 2013; Havelaar et al., 2015; Trevisan et al., 2017). These reflections have led to the development of “zDALY”, an adjusted indicator to estimate the burden of zoonotic
42 | C h a p t e r 1 diseases (Torgerson et al., 2018). Several recent country-specific studies on the societal burden indicated indeed that this zoonosis imposes a serious public health, agricultural and economic threat for endemic countries and has a substantial impact on subsistence farming communities by reducing their societal and economic wellbeing: Eastern Cape Province, South Africa (Carabin et al., 2006), Cameroon (Praet et al., 2009); Mexico (Bhattarai et al., 2012), Nepal (Devleesschauwer et al., 2014), Tanzania (Trevisan et al., 2017), Zambia (Hobbs et al., 2018), Mozambique (Trevisan et al., 2018) and Lao PDR (Okello et al., 2018).
Diagnosis and treatment
Until the early 1990s, visualisation of taenia eggs by microscopy and observation of proglottids in stool were the only diagnostic methods available for the diagnosis of taeniasis in humans. Because of the poor sensitivity of stool microscopy, and the morphological similarity between the eggs of T. solium and T. saginata (Garcia et al., 2003), new diagnostic tools have been developed, although still presenting wide differences in their performances (Coral-Almeida et al., 2015). A non-commercial coproantigen (CoAg) ELISA has been developed but to get a species-specific diagnosis of T. solium, further work has been done on DNA-based diagnostics providing to date techniques of polymerase chain reaction assays for use on stool (copro-PCR) (WHO, 2015b) as well as a revised T. solium-specific CoAg ELISA (Guezala et al., 2009). For the treatment of human tapeworm carriers, chemotherapy with cestodicides directly destroys the source of infection for humans and pigs by eliminating the tapeworm, preventing both from cysticercosis. Three drugs (praziquantel, niclosamide and albendazole) are currently used for the treatment of human taeniasis. Cestodicides can be administered based on a diagnosis-treatment scheme, or implemented as a mass drug administration (MDA) or track and treat system with a more control and preventive purpose (de Coster et al., 2018).
In 1996, a group of experts developed a set of diagnostic criteria for NCC (Del Brutto et al., 1996) that was updated several times (Zammarchi et al, 2017). The updated set of criteria includes absolute (e.g. demonstration of a scolex within a cyst), neuroimaging (magnetic resonance imaging or computerised tomography brain scans) and clinical/exposure criteria, ideally combined with serological tests for detection of antibodies in blood or cerebrospinal fluid and/or T. solium antigens (Del Literature Review | 43
Brutto et al., 2017). Sero-diagnostic tests targeting antibodies in serum or cerebrospinal fluid, or antigens in serum or urine, may also play a role in case detection and confirmation of NCC in patients without access to neuroimaging, although therapeutic consequences in these settings are still undetermined (Nash and Garcia, 2011; WHO, 2015b). Most of these tools are available only within research activities (WHO, 2015c). Several standardised clinical management guidelines for NCC have been recently developed (Zammarchi et al, 2017; White et al., 2018) but the treatment, the choice of anthelmintic (praziquantel and/or albendazole), anti- inflammatory and anti-epileptic medication as well as neurosurgical approaches, must be tailored to the individual patient (WHO, 2015b; Donadeu et al., 2017).
To detect PC, tongue inspection in live pigs, routine meat inspection at the slaughterhouse, dissection of heart, tongue and masticatory muscles or full carcass dissection, serum antibody detection using Western blotting (Flisser et al., 2006), and serum-antigen detection, can be applied (McCarthy et al., 2012; WHO, 2015b), all with their specific limitations. Several diagnostic techniques are also used to estimate the prevalence of PC, but none of these tests are perfect, making interpretation of results difficult. In the absence of a gold standard, a Bayesian analysis framework offers the possibility to combine prior expert opinion with experimental data to more accurately estimate the real prevalence (Dorny et al., 2004). For the treatment of PC, oxfendazole is generally considered safe, inexpensive, easy to administer and very effective against muscle cysts (Mkupasi et al. 2013). Nevertheless, the drug is not readily available in endemic areas and it also requires a 17 days withdrawal period for consumption of edible parts (Moreno et al., 2012). A highly effective porcine vaccine, TSOL18, has been developed (Flisser et al. 2004; Gonzalez et al. 2005; Lightowlers, 2006) and has shown very high levels of protection in both experimental and field trials (Thomas, 2015). Combining vaccination of all pigs between 1 and 9 months of age with oxfendazole treatment demonstrated an optimal effect if delivered every 4 months (Lightowlers, 2013). A disadvantage of the TSOL18 vaccination though is the need to give animals two to three immunisations, at fairly short intervals, as well as the need for a strict cold chain for the vaccine, rendering the implementation cumbersome (Gabriël et al., 2019).
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Since 2010, eight rapid diagnostic tests for diagnosis of human T. solium infections have been developed (six antibody detecting and two antigen detecting tests), some providing qualitative, others quantitative results (Mubanga et al., 2019). However, the performances of these rapid tests still need improvement, as such the need for more sensitive, specific, field-friendly and inexpensive diagnostic tools (Alexander et al., 2011) to monitor the outcome of control efforts (Lightowlers et al., 2016).
TSTC in Zambia
In many Sub-Saharan African regions, including Zambia, TSTC is endemic and studies have shown the same set of key risk factors as mentioned above (Sikasunge et al., 2007; Mwape et al., 2012). Yet, a more recent study ranking the risk factors in order of importance by using non-parametric methods (Classification and Regression Trees model, CART), identified the number of household members and the age of head of household which are less significant in more conventional risk factor studies, while vice versa, commonly mentioned factors, such as open defecation and free roaming pigs did not appear important in the CART analyses (Mwape et al., 2015). This same study further highlighted the fact that a risk factor determined to be very important in one area might not be ranked as high in another one, suggesting that control options may have to be area specific in this country (Gabriël et al., 2019).
The Eastern Province of Zambia is a region hyperendemic for T. solium, with prevalence of active taeniasis of 6.3–11.9% (by coAg ELISA), of active HCC of 5.8– 14.5% (based on circulating antigen detection, AgELISA), and of PC up to 64% (Dorny et al., 2004; Mwape et al., 2012; Mwape et al., 2013). The adjusted epilepsy prevalence in rural Zambia was estimated as 12.5/1000 inhabitants (Birbeck and Kalichi, 2004), and one recent study conducted in Katete (Eastern Province) identified NCC lesions in 57% of people with epilepsy, making it the most important cause of acquired epilepsy in this area (Mwape et al., 2015). Hobbs et al. (2018) provided some preliminary data on disease burden and economic impact of TSTC in Eastern Zambia and highlighted that of all respondents, 62% had reportedly experienced at least one of the surveyed symptoms typically associated with NCC during the last five years. The productivity losses were estimated at 608 working days per year for the 62 questionnaire respondents with symptoms. The value of infected pigs decreased with Literature Review | 45
55%, and when the animal was determined infected before the sales by tongue palpation, it could not be sold in 95% of the cases (Hobbs et al., 2018).
Although there is not yet a national control programme for TSTC in Zambia, several epidemiological studies have been conducted (see above mentioned references) and intervention strategies are currently being implemented and evaluated such as in the CYSTISTOP project. This is a prospective, large-scale community-based intervention study conducted in the Katete and Sinda Districts in the Eastern Province of Zambia aiming at identifying the best sustainable, cost-effective and culturally-sensitive adapted approaches for control or elimination of TSTC in Zambia. Interventions include, TSOL18 vaccination and oxfendazole treatment in pigs and MDA and health education in humans; the frequency of the interventions is based on the newly developed disease transmission model, cystiSim (Braae et al. 2016) and optimised using Zambian demographic and disease data (Gabriël et al., 2019).
1.2.2.2 Control measures
According to the International Task Force on Disease Eradication11 (since 1993), WHO as well as many authors, TSTC is one of few potentially eradicable infectious diseases based first on its apparently simple life cycle - (a) absence of a significant wildlife reservoir; (b) humans are the only definitive host of T. solium, hence the only source of infection for pigs; and (c) pigs are the preferential intermediate host and can be managed - and secondly, due to the current efficacious and effective intervention tools that have been developed (Schantz et al., 1993; Garcia et al., 2007; Lightowlers, 2010; Michelet and Dauga, 2012; Lightowlers, 2013; Johansen et al., 2014; Thomas et al., 2015; Johansen et al., 2017; Samorek-Pieróg et al., 2018).
11 https://www.cartercenter.org/health/itfde/index.html
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Figure 1.5 Life cycle and control options of Taenia solium in endemic areas (Gabriël et al., 2017)
These available control measures (Fig. 1.5) can be divided into measures targeting the human final host and those targeting the intermediate pig host. The first group, targeting the human final host includes (1) anthelmintic treatment of human tapeworm carriers (through MDA, focus-orientated chemotherapy where specific risk groups are treated irrespective of clinical status or identification and treatment of taeniasis cases), (2) health education, (3) hygienic and sanitary improvements. A second group of control measures, targeting the pig intermediate host includes (4) improved standards of pig slaughtering (e.g. more hygienic slaughtering conditions, appropriate techniques and infrastructures for waste disposal, health inspection of animals prior to slaughter including tongue palpation) and (5) improved standards of meat inspection, (6) proper meat handling at household and community levels (e.g. proper meat cooking), (7) improved pig husbandry and (8) pig antiparasitic treatment (oxfendazole at a dose of 30 mg/kg) and/or (9) vaccination (TSOL18 vaccine – commercially available since November 2016) (Thomas et al., 2015; de Coster et al., 2018; Gabriël et al., 2019). The past 10 years have seen several research initiatives to control the infection through community-based interventions (Carabin et al., 2017) and a number of reviews have been conducted to determine which of Literature Review | 47 these nine key tools are currently available and suitable for T. solium control in sub Saharan Africa (Thomas, 2015; Gabriël et al., 2017; de Coster et al., 2018).
Considering the reviewed strengths and limitations of each of the individual available control strategies (Thomas, 2015; Gabriël et al., 2017; Johansen et al., 2017; de Coster et al., 2018), implementation of combined interventions to prevent and control TSTC has been recommended (FAO and WHO, 2014). For the identification of the best combination for cost-effective prevention and control of TSCT in an endemic situation, five current mathematical disease transmission models have been published since 2014 (de Coster et al., 2018). They can be run in a quick way, are cheap to implement and render rapid theoretical insights in which intervention tool, which algorithm or which stepwise approach of interventions will prove most useful in obtaining control or elimination (Braae et al., 2016; Johansen et al., 2017; Winskill et al., 2017; Lightowlers and Donadeu, 2017; Thomas et al., 2017). All these models suggest that both pig and human treatments are required to obtain a rapid and sustainable impact on disease transmission and presence (de Coster et al., 2018). Elimination of transmission through a one-year intensive programme, was even achieved on a regional scale by Garcia et al. (2016) in Northern Peru when combining human treatment and pig treatment/vaccination.
Beside this recent example, currently, no intervention has persistently interrupted the transmission (Samorek-Pieróg et al., 2018), and control attempts in low-income countries remain unsustainable and unsuccessful (Braae et al., 2016). Evidence-based selection of a combination of approaches optimally aiming at both final human and intermediate animal hosts, will definitively vary for different communities and different geographical locations (Gabriël et al., 2017), raising important questions regarding the appropriateness of a TSTC ‘‘tool-box” of control interventions (Bardosh, 2015). Knowing how to break a cycle from a biological perspective does not necessarily translate into sustainable disease control programmes, especially when official notification on PC is extremely inadequate or inexistent (Samorek-Pieróg et al., 2018). Also, information on distribution and burden of disease is a prerequisite for assessing the cost-effectiveness of control programmes (Trevisan et al., 2017), which can help ensuring political and social commitment, as stakeholder engagement and funding is crucial to mount control efforts (Braae et al., 2019).
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While for instance studies have shown that global eradication of this zoonosis is difficult to achieve in the context of persistence of free-roaming pig production (Assana et al., 2013), results from a recent study in Tanzania demonstrate that pigs from farms where the farmers reported that they practiced total confinement had comparable prevalence of T. solium cysticercosis to free-ranging pigs (Braae et al., 2014). This clearly indicates a ‘missing link’ in the understanding of the transmission dynamics of the parasite and possibly the magnitude of environmental contamination (Braae et al., 2015). There are still gaps of how socio-economic, behavioural and environmental factors influence the occurrence of this parasite (Wardrop et al., 2015). Infection with T. solium is to a large extend socially determined and transmission is associated with habits (Ertel et al., 2017), hence sustainable control and eventually elimination, will require human behaviour change that might take more than one generation to alter (de Coster et al., 2018). In the case of TSTC, the health risk is not perceived as important by villagers, partly because of a lack of knowledge about the disease (Ngowi et al., 2017), the long gap between infection and manifestation of clinical symptoms (Johansen et al., 2014), or symptoms such as epilepsy and severe headache which in many societies are still more associated with issues of belief systems and witchcraft than with an infectious disease (Garcia et al., 2003; Singh et al., 2018), and the huge amount of ill health and deaths related to other infections or non-infectious conditions (Gabriël et al., 2017). Lack of knowledge about the pork tapeworm transmission cycle is not specific to pig farmers but includes consumers and non-consumers of pork, medical and veterinary personnel, policy makers and implementers in developing countries (Ngowi et al., 2008; Kungu et al., 2017). Understanding farmers/community knowledge and practices towards TSTC including pig production, slaughter and consumption practices is key for successful elimination strategies (Maridadi et al., 2011) and for minimising the risks of transmission at the level of the producers, traders, butchers and others working closely with pigs (Burniston et al., 2015). A One Health approach covering not only the human and animal host, but also the (social) environment should be envisaged involving a joint collaboration and effort of veterinarians, medical doctors, agricultural extension officers, researchers (including anthropologists), and relevant governmental agencies to find sustainable solutions for prevention, control and elimination of T. solium (Pawlowski et al., 2005; Trevisan et al., 2017; Carabin et al., Literature Review | 49
2017; Gabriël et al., 2017). Control methods applied to date are unlikely to be replicable on a wide scale (Lightowlers and Donadeu, 2017) unless there is a targeted strategy that builds local institutional capacity and iteratively scales-up over time (Bardosh, 2015) by integrating biomedical and participatory approaches (Bardosh et al., 2014a). Moreover, several TSTC control strategies, e.g. MDA, increased use of latrines and improved hygiene, fit in a larger One Health approach as they have the potential to tackle several diseases at once (de Coster et al., 2018).
1.2.3 Rabies
1.2.3.1 Lyssavirus, the ‘dog virus’
Pathogen
Rabies is a zoonotic viral infection that affects warm-blooded animals and human causing an acute, progressive and almost always fatal lethal neurotropic infection. Rabies is caused by infection with the rabies virus (RABV) belonging to the genus Lyssavirus, family Rhabdoviridae. This disease, first described in Mesopotamia in 3000 B.C, has been known since antiquity as one of the most feared human diseases, lyssa meaning “madness” in Greek and the term rabies coming through Latin from the Sanskrit word rabhas, which means "to do violence" (Wilkerson, 1995; Blancou, 2004). The rabies virus is an RNA virus that has five different proteins encoded in its genome (nucleoprotein (N), phosphoprotein (P), matrix protein (M), glycoprotein (G), and polymerase (L)) inside a ribonucleoprotein core surrounded by a membrane envelope (Rupprecht, 1996).
Life cycle and Pathogenesis
The disease occurs in two epidemiological cycles: urban (canine rabies, with dogs as the principal reservoir and transmitters), predominating in areas of Africa, Asia, and Central and South America, and sylvatic, occurring in wild animals (e.g. bats, raccoons, foxes) with sporadic, occasional transmission to dogs, cats and livestock, or directly to humans, and serving as the maintenance host of the virus (Seimenis et al., 2006). Predominant in developed regions such as Europe and North America, the sylvatic cycle may occur simultaneously with the urban one in some parts of the world. The sylvatic cycle has a complex epidemiology; factors affecting it include the virus strain,
50 | C h a p t e r 1 the behaviour of the host species, ecology and environmental factors. In any ecosystem, often one and occasionally up to three wildlife species are responsible for perpetuating a particular strain of rabies (Iowa State University, 2012).
The dissemination of the rabies virus within the body of a healthy individual (animal or human) (Fig 1.6, from numbers (1) to (5)) starts after inoculation with its replication in muscle at site of the bite (1), followed by the infection of the peripheral nerves (2) after several days or months and then travelling retrogradely to the central nervous system (CNS) (3), infecting the brain (4). After dissemination within the CNS, the virus replicates and spreads centrifugally to numerous other organs in the host such as eyes and kidneys but most importantly the salivary glands (5a-b-c) (Hemachudha et al., 2013).
Figure 1.6 Pathogenesis of rabies virus (Fooks et al., 2014)
Although not all exposures result in symptomatic infections, once rabies symptoms develop, coma and death almost invariably follows (Taylor and Nel, 2015). There are two clinical manifestations of rabies, the furious (classical or encephalitic) and paralytic (“dumb”) forms (Hemachudha et al., 2002). Furious rabies is the most common form of human rabies, accounting for approximately 80% of cases (Mani and Murray, 2006). RABV can be found in saliva, tears and nervous tissues of people or animals with rabies, however, not in faeces, blood, urine and other body fluids (Iowa Literature Review | 51
State University, 2012). Starting with fever, headache, and general weakness or discomfort, the early neurological symptoms of rabies in people can include pain, paraesthesia, or tingling at the site of exposure. As the disease progresses, more specific symptoms appear and may include anorexia, insomnia, anxiety, confusion, slight or partial paralysis, excitation, hallucinations, agitation, hypersalivation, difficulty swallowing, hydrophobia (fear of water) and aerophobia (fear of air) (WHO, 2013; Hemachudha et al., 2013). Death usually occurs within days of the onset of these symptoms. In animals, the initial clinical signs are often nonspecific and may include apprehension, restlessness, anorexia or an increased appetite, vomiting, a slight fever, dilation of the pupils, hyperreactivity to stimuli and excessive salivation. The clinical signs are rarely specific, and it may be difficult to distinguish the furious and dumb forms in animals. The most reliable signs are behavioural changes and unexplained paralysis (Iowa State University, 2012).
Epidemiology and distribution
RABV is one of the 16 species of the genus Lyssavirus currently recognised by the International Committee on the Taxonomy of Viruses (Lefkowitz et al., 2018) and the most important one from a public health perspective (Taylor and Nel, 2015). Rabies is primarily an animal infection. Animals are the only vector and reservoir of the virus and human infection is a ‘spillover’ event occurring through exposure to infected animals (Banyard and Fooks, 2011). Primary key hosts are dogs, foxes, jackals, coyotes, raccoon dogs, skunks, raccoons, mongooses, and bats of multiple species (Blancou, 2008). Each RABV variant is maintained in a particular host, and usually dies out during serial passage in species to which it is not adapted. However, any variant can cause rabies in other species (e.g. skunk RABV variant can infect dogs) (Iowa State University, 2012). Canine RABV causes 99% of the human deaths (WHO, 2013), which are nowadays estimated to approximately 59,000 individuals worldwide each year (Hampson et al., 2015). However, this number may be an underestimation because all rabies deaths are probably not confirmed and /or reported (Taylor et al., 2017). It is said that one person dies of rabies every nine minutes of every day, 40% of whom are children under 15 years of age living in Asia and Africa (WHO-FAO-OIE, 2018). Boys appeared to be affected more often than girls (CATMAT, 2002). There are no global estimates of dog bite incidence; however,
52 | C h a p t e r 1 studies suggest that dog bites account for tens of millions of injuries annually (WHO, 2018), which could be used as an accurate indicator of rabies exposure incidence (Hampson et al., 2008). Although fully preventable, still over 100 countries worldwide remain affected by rabies and around half of the global human population lives in canine rabies-endemic countries and is at risk of exposure (WHO-FAO-OIE, 2018).
Risk factors
Rabies is transmitted similarly to animals and humans when the virus is introduced into bite wounds (see (1) from Fig 1.3), into open cuts in the skin (e.g. scratches) (Manning et al., 2008). There are also rare reports of transmission by other routes such as through corneal and organ transplantations (Srinivasan et al., 2005), by aerosol or airborne transmission (Gibbons, 2002; Johnson et al., 2006), and orally in experimentally infected animals. There is some speculation that oral infection might play a role in rabies transmission among wild animals (Iowa State University, 2012). Contracting rabies through consumption of raw meat or animal-derived tissue has never been confirmed in humans (Wertheim et al., 2009). Human-to-human transmission (through biting, mucosal exposure to infectious materials during medical procedures, kissing or intimate touching, mother-to-foetus transmission) is extremely rare (WHO, 2018). Dog slaughtering for human consumption is also one of the modes of transmission in many Asian countries (e.g. China, Cambodia, Vietnam and Indonesia) and in the African continent (e.g. Ghana, Nigeria and Cameroon), predisposing the butchers to the risk of rabies (Hambolu et al., 2013) during catching, handling, loading, holding, transportation and slaughtering of dogs (Garba et al. 2013). The populations the most at risk of exposure to rabies are the ones living, working, travelling and/or being at high risk of contact with wild animals (particularly bats) in remote rural locations where little or no appropriate preventive vaccination of dogs is carried out, where public health resources are inadequate and people may find difficulty in accessing timely, affordable, adequate post-exposure prophylaxis (PEP) (Warrell and Warrell, 2015; WHO, 2018).
Impact
With the highest case fatality rates of any disease (Hampson et al., 2009), rabies is a serious neglected tropical disease that predominantly affects poor and vulnerable Literature Review | 53 populations. The disease is present in every continent of the world except Antarctica and a few island territories considered RABV free (Taylor and Nel, 2015). Eliminated from western Europe, Canada, the United States of America (USA), Japan and some Latin American countries, canine rabies remains endemic in many parts of the developing world, mainly in Africa and Asia (Knobel et al., 2005), where domestic dogs are the primary maintenance host of the virus, and responsible for the vast majority of human exposures and deaths (WHO, 2018). Human deaths from rabies are significantly underreported in many parts of the world due to poor surveillance, lack of laboratory infrastructure, frequent misdiagnosis to other neurological syndromes (especially in malaria endemic regions (Mallewa et al., 2007)) and the absence of coordination among all the sectors involved, leading to an underestimation of the disease burden (Fooks et al., 2014; WHO, 2018). Based on a simulation model, Hampson and all (2015) estimated that globally canine rabies causes over 3.7 million DALYs and 8.6 billion USD economic losses annually.
Figure 1.7 The distribution of the global burden of rabies. (A) Human rabies deaths per 100,000 persons. Countries shaded in grey are free from canine rabies (Hampson et al., 2015)
In the absence of efficient control at the source, rabies is excessively costly in terms of DALY lost due to premature death (55%), the direct costs of PEP (20%) to the public and private sectors and lost income whilst seeking PEP (15.5%), while the costs to the veterinary sector due to dog vaccination (1.5%) and additional costs to communities from livestock losses (6%) constitute a tiny component of the global economic burden (Anderson and Shwiff, 2013; Hampson et al., 2015).
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Diagnosis and treatment
In humans, laboratory tests of secretions, biological fluids (such as saliva, CSF, tears, serum) and some tissues (such as skin biopsy samples, including hair follicles at the nape of the neck) can be used to diagnose rabies during life (Dacheux et al., 2010) although detection is less efficient (Shankar, 2009). Daily samples should be tested until a diagnosis is confirmed, virus isolation is ideal but takes several days. Unvaccinated patients can be diagnosed by detecting neutralising antibodies (Warrell and Warrell, 2015). Because hydrophobia is also often observed, in developing countries where access to diagnostic tools is often a challenge, water might be offered to suspected patients for diagnostic purposes (Fooks et al., 2014).
Infection with rabies virus in animals can be difficult to diagnose ante-mortem as most diagnostic tests need brain material (Hemachudha et al., 2013). Brain smears or touch impressions are used for the detection of virus antigen with the fluorescent antibody test (Dean et al. 1996) for both human and animal samples, a test which is recommended by both the WHO and OIE (Fooks et al., 2014). However, new techniques such as the direct rapid immunohistochemical test (dRIT) have been developed to avoid the need for expensive fluorescently labelled antibodies and fluorescence microscopes (Lembo et al., 2006). Molecular-based techniques, such as PCR techniques, are becoming more widely accepted and accessible for the diagnosis of rabies (Fooks et al., 2012), and to confirm the origin of the virus isolate (Leung et al., 2007).
Both in humans and animals, there is no effective curative treatment once the symptoms develop (Jackson, 2013). Treatment in humans is therefore often palliative and should include liberal use of sedatives and analgesics as needed to achieve comfort (WHO, 2018; Taylor and Nel, 2015). To date, survival has been well- documented in only 15 cases (Jackson, 2016). In the event of an unvaccinated individual becoming exposed, prompt application of recommended procedures prior to clinical disease will avoid fatalities. Rabies is therefore preventable via several approved PEP recommendations, which consist of thorough wound-cleansing with soap or a viricidal antiseptic (and should not be sutured unless absolutely necessary) and prompt administration of rabies immune globulin (RIG), together with a full course of anti-rabies vaccination (WHO, 2018). Fewer doses and no RIG are given if Literature Review | 55 the person was previously vaccinated (Rupprecht et al., 2006). The suspect animal should be monitored for a period of 10–14 days and if it exhibits signs of rabies, it should be euthanised, its brain tissue should be tested and if negative the PEP of the exposed humans can be discontinued (Leung et al., 2007).
Rabies in South Africa
With the exception of a few areas in the south of the continent, the epidemiology of rabies in Africa is driven by domestic dogs (Cleaveland et al., 2007). In sub-Saharan Africa, the introduction and spread of the RABV variant in Canidae (associated with the domestic dog, black-backed jackal and bateared fox in South Africa) is closely related to European and cosmopolitan viruses (VonTeichman et al., 1995) and correlates with colonial period activities of the late 19th and early 20th century (Nel and Rupprecht, 2007; Weyer et al., 2011). In the Republic of South Africa (RSA) a second major variant of RABV is circulating in Herpestidae species such as mongoose (Nel et al., 2005; Mollentze et al., 2013). RSA had its first known rabies outbreak in domestic dogs (Canis lupus familiaris) confirmed in 1893. The following outbreaks were sporadic, and rabies appeared not to be able to establish itself (Bingham, 2005). Anecdotally reported in the RSA since the 1800s, the first human cases were confirmed in 1928 (following exposures to a rabid mongoose) (Swanepoel, 2004). Since the 1970s most human rabies cases in RSA, where the major animal vector was the domestic dog, have occurred in the coastal Provinces of KwaZulu-Natal (KZN) following an influx of refugees from Mozambique and of Eastern Cape (Swanepoel et al., 1993; Swanepoel, 2004). Sizable outbreaks of canine rabies have been increasingly reported in the past decades from sites where it has been under control for many years and in new geographical zones: in the Free State Province since 2000, in Limpopo Province (first in 1950 and re-emerging after 2005), in Mpumalanga Province since 2008, and introduction into Gauteng Province in 2010-2011 (Cohen et al., 2007; Ngoepe et al., 2009; Mkhize et al., 2010; Sabeta et al., 2013).
Although rabies is a notifiable disease in South Africa since 1977, the surveillance of rabies cases in dogs by veterinary services and collection of data on dog bite injuries by local clinics and district hospitals could be improved and more detailed in some areas (Hergert and Nel, 2013). Weyer et al. (2011) retrospectively analysed a total of 353 laboratory confirmed human rabies cases from RSA between 1983 and 2007,
56 | C h a p t e r 1 mainly from KZN province where rabies was responsible for >9 deaths per year (Weyer et al., 2011) and in 2007, 473 cases of animal rabies were reported in this same province (LeRoux et al., 2018). More recently, a total of 11 human rabies cases were confirmed during the report of the National Institute for Communicable Diseases (from 1 April to 31 December 2017), five cases were confirmed from the Eastern Cape, KZN, Mpumalanga and Limpopo Provinces. In the first three months of 2018, another six cases were reported from KZN (n=4) and Eastern Cape (n=2) Provinces (NICD, 2018).
Rabies persists as a significant human and veterinary public health problem in RSA, including the “Mnisi study area”12 (Marcotty et al., 2009; Conan et al., 2015). Because rabies is a transboundary disease and can re-emerge in areas where successful control programmes have been active for many years (Cohen et al., 2007), these later outbreaks highlight several key failures and challenges to control rabies in RSA, which is a relatively progressive African state (see Cleaveland et al., 2003; Coetzee et al., 2008; Bishop et al., 2010; Brown, 2011; Sabeta et al., 2013; NICD, 2018). Competing public health priorities (rabies needing to be re-prioritised), shortages and prohibitive costs of PEP, inaccessible health-care facilities and deteriorating infrastructure count among the challenges faced by the human health sector. In the animal health sector, there are limited resources for veterinary control measures, low vaccination coverage, lack of sustainable vaccination campaigns, inadequately trained health and veterinary staff both in the public and private sector, combined with an ongoing presence of rabies in wildlife. From an integrated perspective, RSA lacks a human and veterinary partnership in both public and private organisations, a local rabies sequence database and ecological studies of dog populations in rural settlements bordering the fences of conservation areas. Poorly informed communities, increasing numbers of animals and mobility of human and animal populations constitute an additional set of challenges to control rabies in RSA.
12 The Mnisi study area is located in the land of the Mnisi Traditional Authority (MTA) situated in the north-eastern corner of the Bushbuckridge Local Municipality and is the core research and engagement area of the Mnisi Community Programme, Faculty of Veterinary Science, University of Pretoria (UP) (Berrian et al., 2016) Literature Review | 57
1.2.3.2 Control measures
Because rabies is untreatable, prevention is of utmost importance (Leung et al., 2007). In humans, rabies can be prevented (1) by eliminating exposure to rabid animals either by preventing animals to get infected or by conducting programmes to prevent dog bites; (2) by vaccination before (pre-exposure prophylaxis (PrEP)) for individuals who are at high risk of exposure to rabies or to bat lyssavirus (see above) and/or (3) by providing exposed persons with prompt local treatment of wounds combined with the appropriate administration of PEP (Brown et al., 2011; WHO, 2018). Dog bites prevention is based on responsible dog ownership, parental supervision of children around dogs and appropriate behaviour around dogs (Dwyer et al., 2007) and this would reduce the risk of rabies, save the costs of PEP and wound care, eliminate the trauma of dog bites and restore healthy dog–human relationships (WHO, 2018).
As a zoonotic disease, control of rabies infection in the reservoir species, including domesticated animals, through immunisation and population management (Hampson et al., 2009) has been proven for long the most efficient and cost-effective route for reduction of human cases in settings where the disease is endemic (WHO, 2005; Cleaveland et al., 2006; Lembo et al., 2012). Rabies control in domestic dogs especially results in immediate and widespread benefits for human health, animal welfare and conservation, as well as long-term economic benefits to both public and private sectors (Zinsstag et al., 2009). First developed in the 1970s, oral mass vaccination programmes with rabies vaccines applied in attractive baits were designed to eliminate wildlife rabies from a defined area or to prevent spread of the disease by creating an immunological barrier (containment, cordon sanitaire) (WHO, 2018). From a humane, economic and ecological perspective, it is a more appropriate control method than culling (King et al., 2004) and in several countries worldwide it has already allowed the elimination of rabies in carnivores such as foxes, raccoons, and skunks (Rupprecht et al., 2008). Another option can be strategic trapping of wild carnivores and releasing them after parenteral vaccination (trap–vaccinate–release) (WHO, 2018). Although rabies may never be eradicated from all species, because of the presence of lyssaviruses in bats, it is feasible to eliminate canine rabies (Rupprecht et al., 2008).
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In domesticated animals, rabies can be prevented by parenteral vaccination and by the avoidance of contact with rabid wild animals. RABV is the only virus used to date in vaccines and these are available for dogs, cats, ferrets, cattle, sheep and horses. The duration of immunity conferred varies from one to three years (Bishop et al., 2010; Morters et al. 2014). Annual vaccination of domestic dogs, their registration and permanent identification (WHO, 2018), as well as their confinement and application of quarantine measures following importation are key prevention strategies (Rupprecht et al., 2006). To interrupt transmission and eventually eliminate the disease and prevent spillover into accidental hosts, a sustained vaccination coverage of 70% or higher is recommended (Coleman and Dye, 1996) to maintain the required level of herd immunity in the susceptible population despite dog population turnover (births, deaths, animal movement) in the period between campaigns (WHO, 2018). Dog population management to improve and maintain vaccination coverage is challenging, especially for stray dogs. Removal of dogs through mass culling does not decrease dog density nor control rabies in the long run and should not be a part of a rabies control strategy, particularly when vaccination programmes target free- roaming dogs (Morters et al., 2013; WHO, 2018). For this, potent and inexpensive tissue culture vaccines are available and oral vaccination is now being extended from wild mammals to stray or feral dogs (Warrell, 2010) that cannot be restrained or caught (WHO, 2018).
Humane dog population management which consists of humanely managed dog populations by responsible dog ownership and provision of sterilisation services and basic dog health care is an effective strategy for reducing dog population turnover and creating a healthy, sustainable population (Taylor et al., 2017). Euthanasia of an animal suspected of being rabid prevents further transmission to humans and animals and prevents further suffering of the animal (WHO, 2018).
Education and awareness campaigns are acknowledged to be key components of a dog rabies control programme. They aim to increase awareness of the benefits of responsible dog ownership, basic care of bites from animals with suspected rabies and avoiding exposure to animals. It is also recommended that knowledge, attitude and practice surveys be conducted to determine each stage of an education programme on rabies (WHO, 2018). Literature Review | 59
Nowadays, there are tools for controlling dog population and movements, educating communities, integrated dog bite management, immunising humans, dogs and wildlife. There is also technology for diagnosing and monitoring the disease and finally evidence available together with blueprints13 for operationalising control. Therefore, according to the recent United Against Rabies collaboration14, global freedom from the threat of dog-mediated rabies is feasible within our lifetime. However, an integrated investment strategy and intersectoral approach is needed to make this vision a reality (WHO-FAO-OIE, 2018), and to finally move from the biological understanding to the science of rabies elimination with effective actions and policies (Zinsstag, 2013).
Figure 1.8 The United Against Rabies collaboration’s objectives and phased approach to achieve rabies dog-mediated elimination by 2030.
13 Prepared by the Partners for Rabies Prevention, the “rabies blueprint” (http://caninerabiesblueprint.org/) provides guidance to strategically planned and well managed vaccination campaigns with adequate resources (Lembo et al., 2012). 14 After the 2015’s call for action, the following four organisations– the World Health Organization (WHO), the World Organisation for Animal Health (OIE), the Food and Agriculture Organization of the United Nations (FAO) and the Global Alliance for Rabies Control (GARC) – have joined forces to address the goal of zero human dog-mediated rabies deaths by 2030 worldwide.
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Integrated strategies, building blocks of the OH concept, are enhancing intersectoral cooperation among veterinary services, public health and wildlife management to design evidence-based approaches and enhancing their cost effectiveness to control and eliminate rabies, particularly in low-income countries (Cleaveland et al., 2014; WHO, 2018). As successful rabies control generates benefits in terms of improved human and animal health, well-being and safer environments (Häsler et al., 2014), this NTD has been seen as an example of the added value of the OH approach (Cleaveland et al., 2014). These intersectoral collaborations should take place at several coordinating levels (local, national and global) and should address many previously identified control challenges and barriers (see Lembo et al., 2011; Banyard et al., 2013; Meslin and Briggs, 2013; Cleaveland et al., 2014; Léchenne et al., 2015; Fitzpatrick et al., 2016; Knobel et al., 2017; WHO, 2018): Indeed, the integration of strategies could better address communities engagement and awareness to register and vaccinate dogs and to ensure potentially exposed people know how to seek treatment. Reporting and managing dog bites, integrating rabies control activities into all levels of the health service, sharing human and animal diagnostic facilities and bringing together reliable incidence data on animal and human rabies in one shared database, would ensure a better provision of animal and human vaccination (also through cooperation with the pharmaceutical industry and institutions) as well as improve and strengthen surveillance at the level of laboratory diagnosis. In addition to enhance communication with decision makers on the different national and international levels, aligning rabies control activities with other public health or animal disease control programmes (e.g. other canid-associated zoonoses, such as hydatidosis and leishmaniasis) would be more cost-effective and allowing more sustainability.
Between 2007 and 2014, WHO managed a large-scale rabies elimination pilot programme funded by the Bill & Melinda Gates Foundation to reduce human rabies cases in KZN to zero by (1) conducting mass canine vaccination campaigns in strategic areas (planning, understanding of disease epidemiology, creation of a canine vaccine bank, proper training, equipment and support for technical staff), (2) human PEP (improving rabies awareness i.e. when and how to seek treatment, and training of medical staff to recognise, prioritise, and appropriately treat suspected exposures, and improving targeted delivery); (3) data collection: starting small allowed data to Literature Review | 61 evolve with the project and fit various local settings while scaling-up the interventions (WHO, 2015d). Within 7 years of project implementation, canine rabies cases were reduced by 84%, and human rabies cases were reduced to zero, encouraging local government investment and support for sustaining control activities (LeRoux et al., 2018). However, as mentioned above, in the first three months of 2018, another four human rabies cases were reported from KZN (NICD, 2018). Against a backdrop of decades of neglect (Weyer et al., 2011), the adoption of a firm goal to achieve zero human deaths due to canine rabies by 2030 may risk to encounter fairly stereotypical challenges of ‘‘top-down’’ public health interventions in developing countries, known to overlook critical social, cultural, political and economic contexts that mediate effectiveness (Bardosh et al., 2014b).
There remain clearly challenges in mobilising resources for canine vaccination as well as operational barriers that inhibit success in many contexts (Bardosh et al., 2014b; Neevel et al., 2018). Many rabies-endemic countries lack the finances and infrastructure to sustainably vaccinate dogs, conduct surveillance or provide communities with access to rabies vaccines (LeRoux et al., 2018), which means that only very limited data that often are of questionable reliability are available (Hampson et al., 2015). Often perceived as a rare or insignificant disease of humans in developing countries (Coleman et al., 2004), evoking less fear and concern than zoonoses that can spread by human-to-human transmission (e.g. SARS, Ebola), canine rabies is also not considered to be an important disease of economically valuable livestock species, which are the priority for government veterinary services in these endemic regions (Cleaveland et al. 2014). Basic information on how many lives are lost to rabies and the economic costs of preventing disease amongst those exposed are needed to advocate for sustainable control programmes (Hampson et al., 2015) and empowering policy makers to make decisions in an efficient manner (Häsler et al., 2014). For instance, there is a real possibility that current dog rabies vaccine production capacity will be unable to meet demand (Wallace et al., 2017). Research should contribute to fill the gap between knowledge and effective action by addressing the social, political, economic and psychological complexity of effective rabies control interventions (Zinsstag, 2013).
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No single vaccination strategy is likely to be effective in all populations and therefore alternative approaches must be deployed under different settings (Kaare et al., 2009). Understanding aspects of dog ownership, the human-dog relationship, and the ecology of the dog population – all of which may vary geographically or be affected by socio-cultural determinants (Wandeler et al., 1993; Knobel et al., 2008a,b; Hergert and Nel, 2013) – is therefore helpful in guiding long-term rabies control efforts in particular areas. With renewed global attention to rabies, there is a need to think critically about how local realities intersect with technical solutions; on how we should think about the challenges of dog vaccination for rabies and, importantly, on how large-scale canine vaccination projects can navigate local social and ecological complexities in resource-limited settings (Bardosh et al., 2014b). To reach the goal of elimination of rabies by the year 2030, we therefore will have to reach further than veterinary and human medicine and also include biologists, cultural scientists, sociologists and geographers (Léchenne et al., 2015) and by including the department of education such as in the Bohol rabies elimination programme in Philippines (Lapiz et al., 2012). Integrated approaches would need to be extended to a broader systemic understanding of ecological (ecohealth) and social systems (health in social- ecological systems) (Zinsstag et al., 2011; Léchenne et al., 2015).
Similarly to what many scholars working on current emerging infectious diseases agreed on, the broader force for human pathogen evolution is the human modification of the environment, which has resulted in an increase and modification of contact between humans and animals (Daszak et al., 2001; Pearce-Duvet, 2006; Epstein and Price, 2009; Lindahl and Grace, 2015). In the relationships of Homo sapiens with the natural world (animate and inanimate), habitat fragmentation, deforestation, urbanisation and replacement of natural vegetation by crops, arising from settlement and agriculture due to rapid changes of habits and practices within societies, are examples of anthropogenic factors that have modified the wildlife population structure and migration, and reduced biodiversity by creating environments that favour particular hosts, vectors, and/or pathogens (Jones et al., 2013). Concurrently, structural drivers such as, land degradation, neoliberal economic policies, planning Literature Review | 63 initiatives, and the consequently political instability and lack of resources, limit the capacity of certain governments to manage the environment, control diseases, and ensure an effective health system, reinforcing as such inequalities and marginalisation of certain groups like livestock owners from developing countries (Manderson et al., 2009; Dzingirai et al., 2017).
Among the many challenges regarding zoonotic disease control, we can raise the understanding of the complex interactions existing between factors from different sectors, namely human, animal and environmental, but also at and between individual, household, community, national and international levels. From an individual in a community to the wider economy, the role of human behaviours in infectious disease “traffic”15, by changing ecological contexts locally and globally, poses another concern which is to avoid the risk of studying a pathogen without the behaviour/life style/environment of its host(s), which can be a human, an animal or both.
Understanding the dynamic interaction of diverse factors and diverse species in varying contexts is a complex task, yet critical for successful health promotion, disease prevention, and disease control (Manderson et al., 2009). A discipline of observation and interpretation of the causes and consequences of human activities in their socio-cultural context such as anthropology, should play a significant active role to address the forementioned challenges by providing a more holistic interpretation of disease dynamics and to drive public policies (Inhorn and Brown, 1995; Destoumieux-Garzón et al., 2018).
1.3.1 Anthropology and Health, the concept of “culture” applied to livestock owners and zoonotic risks
1.3.1.1 An interdisciplinary human health focus
According to Langdon and Wiik (2010), the main purposes of anthropology are “i) to identify cultural patterns shared by groups of individuals; ii) to deduce what is common in the actions, allocation of meaning, and significance and symbolism
15 Term coined by the virologist Morse (1993) in reference to the movement of infectious disease agents to new species or new individuals (Inhorn and Brown, 1995).
64 | C h a p t e r 1 projected by the individuals on the material and “natural” world; iii) to reflect on the experience of living in society, including that of becoming sick and caring for one’s health, as a highly intersubjective and relational experience, mediated by the cultural phenomenon.”
“Health” is definitively a fundamental category in all cultures and all cultures have medical systems (Brown and Closser, 2016). Culture constitutes a powerful driver as it affects health through numerous pathways, including influence on risk and protective behaviours, the nature of family and social relationships, and the meanings and expectations associated with group memberships based on gender, ethnicity, religion, social class, and other socially defined categories (Bachrach et Abeles, 2004). At the individual level, it is clear also that both logical/rational and intuitive/emotional systems influence behaviours and decision-making (Slovic et al., 2007, Lapinski et al., 2015).
The conceptual point of departure of this thesis is that everyone is embedded in a specific culture, defined as a shared social tradition including language, social norms, and beliefs, and subculture, i.e. a self-organised cultural group that differs in one or more ways from the broader culture because of interests, lifestyles, and customs. (Ember and Ember, 2004). It is essentially those cultures that determine the particularities of human beings who present unique behaviours and thoughts with regard to the experience of illness, as well as particular notions about health and therapeutic practices (Langdon and Wiik, 2010). It is the same fundamental concept of culture that influences how livestock owners behave, adopt practices regarding livestock management and health.
Achieving optimal health and well-being for all members of a society lies as much in the understanding of the factors identified by the behavioural, social, and public health sciences as by the biological ones (Marbry et al., 2008). Human biology and culture are intimately related, and so we should adopt a holistic perspective when we are studying human health and sickness (Brown and Closser, 2016). The history of public health is replete with examples of scholars and practitioners who have attempted to overcome an inherent tension between the biological and social sciences also by urging a synthesis of epidemiological and anthropological perspectives in what was then called ‘tropical medicine’ (Inhorn and Janes, 2007). “Tropical Literature Review | 65 medicine” is now encompassed under the label of “International” or “Global” health since former tropical health issues are now considered to be determined by problems, issues and concerns transcending the strictly tropical regions (Beaglehole and Bonita, 2010). In the field of parasitic diseases for example, one important legacy of these pioneering interdisciplinary scholars (Dunn, 1979), was to move attention away from an asocial risk factor approach to a focus on the assemblage of causal factors (cultural, social, economic, and political) (Inhorn and Janes, 2007). Schwabe offered us an early concrete example of such combined descriptive epidemiologic and anthropologic study when in 1972, he sent an anthropology graduate student, Frank Araujo, to live and work on a Central Valley Basque sheep ranch in order to learn about hydatid disease transmission directly from sheep farmers, examining this community through an ecological lens (Dentinger, 2018). More broadly, the social sciences are recognised indeed to be important for elaboration of causal assemblages and for contextualisation of epidemiologically notable behaviours in social, economic, political, and cultural systems, and thereby contribute to effective behavioural and structural interventions (Janes et al., 2012).
1.3.1.2 An interdisciplinary disease risk focus
The ability to sense and avoid harmful environmental conditions is necessary for the survival of all living organisms and, as Paul Slovic (1987) further wrote, “humans have an additional capability that allows them to alter their environment as well as respond to it”. Cultural systems change as people evaluate the influence of their behaviour in interaction with the environment (Brown and Closser, 2016).
In the field of interdisciplinary research on zoonotic disease, “risk” posed to health is often a central practical and conceptual focus, such as the risks associated with disease emergence, or factors increasing risk of transmission or spread (MacGregor and Waldman, 2017). Many frameworks proposed for work on livestock and wildlife systems and zoonotic disease have thus emphasised the ‘risk environment’ and ‘risk scenarios’ for transmission of organisms and the importance of understanding drivers of risk at different scales (see for example the ‘Strategic Framework for Reducing Risks of Infectious Diseases at the Animal–Human–Ecosystems Interface’ (FAO-WHO-OIE et al., 2008) and Liverani et al. (2013)) (MacGregor and Waldman,
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2017). In reference to the focal distribution of several Neglected Tropical Diseases (NTDs), including zoonotic ones, different local factors, including socio-cultural ones, may be responsible for variations in morbidity and mortality (Manderson et al., 2009). Consequently, successful control of Neglected Zoonotic Diseases (NZDs) in such “hot spots”16, prioritised on the basis of an acknowledgment of the complexity of the poverty-disease cycle (Allotey et al., 2010; Grace et al., 2012), necessitates, in addition to a global overview, studies describing local variations in epidemiological, environmental and socio-cultural factors (Aagaard-Hansen and Chaignat, 2013). With respect to reducing zoonotic risks, the social science dimensions of research are therefore expected to contribute information regarding the cultural beliefs and practices that influence human–animal ‘interactions’ and livestock keeping (MacGregor and Waldman, 2017). For example, work in Lao PDR has contributed valuable data by uncovering the practice of eating raw pork and elucidating its relationship to masculinity and also to the risk of T. solium (Bardosh et al., 2014a). The expanded framework developed by Woldehanna and Zimicki (2015) to analyse human-animal exposure that accounts for social as well as epidemiologic factors in a similar context, is another contribution of social science to assist interdisciplinary teams in contextualising risk, and introducing the understandings of broader drivers of zoonotic disease and of the context of responses.
Finally, because zoonoses account for the most commonly reported emerging and re- emerging infectious diseases in Sub-Saharan Africa (FAO, 2013), anthropologists must continue playing a central role in understanding perceived risks when interacting with animals but also starting to explore cultural variation in attitudes towards other species and how people in different contexts understand animals’ social value, health and welfare (Muehlenbein, 2016). This will allow to address the limited knowledge on (1) how pastoral communities perceive zoonoses in relation to their livelihoods, culture and their wider ecology; (2) on African farmer’s knowledge of opportunities for disease management (Mangesho et al., 2017); and (3) on
16 A “hotspot” is originally referred to a location with high biodiversity and wildlife density that was under significant threat of degradation or destruction as a consequence of human activities (Myers et al., 2000). And it is Jones et al. (2008) who demonstrated the spatial overlap between locations of emerging zoonotic diseases and biodiversity hotspots, and thus trained the researcher's attention on the spatial relationship between biodiversity hotspots and emerging zoonoses. Literature Review | 67
awareness, practices and attitudes toward zoonoses among animal health workers (Swai et al., 2010) and medical practitioners (John et al., 2008) in these settings.
1.3.2 Anthropology and Health, the concept of “culture” applied to human-animal interactions
1.3.2.1 Zoonotic diseases cannot only be concerned with human health alone
While Nading (2013) defines “health” as “the combination of practice and epistemology17 by which people confront disease, the manifestation of symptoms associated with biophysical disorder, and illness, the socially and culturally mediated experience of suffering”, he is also asking himself where animals fit into this definition of health. When studying health knowledges as social phenomena, researchers should, in short, acknowledge that human societies are not composed of human bodies alone. Animals, have always been part of the constitution of human societies, and thus—whether as food sources, as sacred entities, as sentinels, as workers, as goods ‘‘to think with’’, as beloved companions or sometimes as a combination of all these roles (Mullin, 1999; Brown and Nading, 2019)—been part of how human health is realised and perceived (Rock et al., 2007). “Animal” is considered here as both an object influencing human health and a subject of health. Impactful interactions between humans and other organisms commonly are not time-limited but ongoing and “substantially influenced the evolution of humans” (Shipman 2010). Dogs, for example, have had a persistent presence in human communities for probably well over 15,000 years (Germonpré et al. 2009), with significant consequences for both species, beginning with genetic and behavioural changes in wolves that produced dogs and extending to the multiple impacts (e.g. biological, economic, cultural, therapeutic) on humans of close association with dogs (Singer, 2014).
Within anthropology it has long been known that societies have diverse understandings of animals (Macgregor and Waldman, 2017) and this discipline has a long history of examining the place of animals in everyday life and everyday language, perceiving animals merely as a vehicle with which to explore a particular social
17 Epistemology, or the theory of knowledge, is a branch of philosophy that investigates the origin, nature, methods, and limits of human knowledge (The Random House College Dictionary, 1984).
68 | C h a p t e r 1 formation or process (Evans-Pritchard, 1960; Levi-Strauss, 1963; Leach, 1964; Mullin, 1999, 2002). Yet, medical anthropologists, who are concerned with both the causes and consequences of human sickness (Waldstein and Cameron, 2006), have for long demonstrated surprisingly little interest in animals (Fleising, 2000; Franklin, 2001, 2003; Martin, 1995; Rock, 2005), by historically focussing on understanding and explaining only the human side of multispecies interactions (Singer, 2014). The importance of animals has received somewhat more recognition in ethno-veterinary research conducted in non-Western settings (e.g. Nyamanga et al., 2006) (Rock et al., 2007). The contemporary human-animal relationship is considered to be “complex and profound, ranging from exploitation of livestock for food and anthropomorphisation of animals as pets, to live ‘wet markets’ and international trade in animal species” (Zinsstag et al., 2012), and the impact of these diverse human-animal relationships is believed to constitute a threat to all humans on an equal proportion (Wolf, 2015). Animals have then appeared and been framed as vectors of disease in Western and non-Western ethnomedical conceptions of health (Nading, 2013).
1.3.2.2 Multiplicity of worldviews regarding the human–animal interface
Yet, there is a diversity of views regarding the nature of the human–animal interface and of relations between animals and humans and these views could correspondingly affect how people might respond to animal illness and measures to control zoonoses (MacGregor and Waldman, 2017). In that matter, evolutionary and ecological perspectives that can provide valuable insights into pathogen ecology and consequently inform zoonotic disease-control programmes (Karesh et al., 2012), have transformed medical anthropology. From a traditional focus on cultural aspects of health and healing and comparative studies of medical systems (e.g. efforts to classify healthcare systems by assessing similarities and differences among them such as for shamanism, ethnomedicine or biomedicine) to a broader perspective on human health in an environmental context (McElroy, 2004), medical anthropology has a new gaze on animals in human societies. Anthropologists have moved away from an earlier tendency to see animals as merely of economic use to humans, of ritual significance, or as a means to ‘think with’ to reflect on the organisation of human society (Noske, 1993; Mullin, 1999) and are rather attentive to the interactions and Literature Review | 69 entanglements between coevolving species (MacGregor and Waldman, 2017; Keck and Lynteris, 2018).
Thus, with respect to human–animal relations, the utility and validity of the concept of culture (as the anthropological primary object of study) have been rethought by revising assumptions that culture is uniquely human (Fox and King, 2002) and by questioning its systematic hierarchical dualisms: culture/nature, human/animal, mind/body, male/female (Mullin, 2002). In this new mode of anthropological description, animals are not considered as passive carriers of long-term human symbols but as actors in unstable and vulnerable networks of coexistence (Descola 2015; Kelly 2014) within a “mutual causation process” making the distinction between cause and effect meaningless (Guba, 1985). Nowadays, medical anthropologists examine how the health of individuals, larger social formations, and the environment are affected by interrelationships between humans and other species; cultural norms and social institutions; micro and macro politics; and forces of globalisation as each of these affects local worlds (Society for Medical Anthropology, 2015).
Zoonotic disease control indeed adds additional layers of complexity to public health, precisely because it spans different spatial and temporal relations between people, animals, micro-organisms and ecologies (Nading, 2013). The knowledge of Mongolian pastoralists about their cattle (Ruhlmann, 2018) or of Laotian mahouts about their elephants (Lainé, 2018), must be taken seriously when these animals are affected by zoonoses, as they open the spectrum of social relations they generate in the entanglement between health and a multitude of animals, plants or microbes, extending as such the notion of culture to the ‘natural’ world (Wolf, 2015; MacGregor and Waldman, 2017; Keck and Lynteris, 2018).
OH can be understood as a response to this complex interconnectedness following an interdisciplinary approach to research and an inter-sectoral approach to intervention (Rock and Degeling, 2015). Along with acknowledgement that healthy ecosystems and healthy people go together (Whitmee et al., 2015), OH discourse and practice integrate animal health into the equation (Leach et al., 2017), positioning the human- animal interface in a significant site of reconfiguration of global health (Keck and Lynteris, 2018). Most collaboration results from efforts to control a zoonotic disease
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(Dorea et al., 2014). While social scientists have mostly ignored animal health until recent developments in cultural and medical anthropology (see above), few OH proponents have emphasised social conditions or involved social scientists (Rock et al., 2009).
1.3.3 Anthropology and “One Health” as an integrated control approach
1.3.3.1 Anthropology and its integration into the One Health movement
Within the OH framework, more and more research from the natural and social sciences, as well as from public health has contributed to designing surveillance and response policy already on (emerging) zoonotic diseases (Paige et al., 2015). As a sound basis for combating human diseases, animal diseases, and environmental degradation worldwide (Rock et al., 2009), the OH paradigm recognises the importance of understanding social and cultural factors in disease transmission dynamics and in the planning and evaluation of control interventions (Bardosh, 2014). The role of anthropology in interdisciplinary and transdisciplinary OH/EcoHealth (OH/EH) approaches and the inclusion of traditional knowledge systems are therefore gaining increasing support and attention in different fields of interest, such as, health (animal and human) and medicine, ecosystem services, wildlife management, and environmental health (Keune et al., 2017).
The systematic integration of various disciplines to manage health more holistically is often complicated by interdisciplinary and intersectoral barriers to effective collaboration (Lyall et al., 2011). The current institutional architecture in which public funds are allocated to specific ministries hinders development of joint public health programmes, which in the case of zoonotic diseases can result in a fragmented approach to control. Another important challenge is the paradigm debate caused by the philosophical underpinnings that guide the collection and analysis of quantitative and qualitative data which may be viewed differently by disciplines (Häsler et al., 2014). For example, epidemiology is objective and studies populations; anthropology, in contrast, is reflective, subjective and investigates complexity and the individual (Porter, 2006). While it has been suggested that using both approaches in the same study provides, in combination, a superior understanding of research problems than either approach alone (Johnson and Onwuegbuzie, 2004), to date the OH approach Literature Review | 71 and the programme has tended to offer few opportunities for serious social scientific contributions or engagement (Craddock and Hinchliffe, 2015). Furthermore, the OH movement seems to have itself suffered from a relatively marginal social science contribution and from a more important focus on global pandemic threats (Scoones, 2010). One possibility is that OH reproduces a rather top down version of scientific expertise, with the role of social science being relegated to easing delivery and dissemination of pre-established knowledge (Craddock and Hinchliffe, 2015). However, to further develop a more biosocial approach for an integrated control of NZDs in this OH endeavour, there is a need to avoid simplistic framings of ‘the social’ and to recognise that it is often counter-productive to tacitly accept a hierarchy of knowledge in which minimal or partial attention is given to ethnographic and historical research (Melissa Parker, personal communication)
For a OH approach tackling zoonotic diseases, it is essential to address the underlying structural drivers of disease vulnerability (Dzingirai et al., 2017). Several scholars pointed in various way to the critical facts that not everyone (or, indeed, every species) is equally at risk, not every country is equally able to recognise and respond to disease outbreaks, and not all actors in disease interventions possess equal financial or political leverage to make change effective (Craddock and Hinchliffe, 2015). Therefore, undertaking research including the lives of those who experience risks in hotspots on a daily basis, would result in policymakers and practitioners being able to fully comprehend the social and ecological processes that catalyse cross- species pathogen exchange (Paige et al., 2015). It is these local disease–ecosystem– livelihood dynamics that underlie and add up to wider patterns of change, as they interact with larger-scale drivers whether in environment, economy or demography (Leach et al., 2017; Lindahl and Grace, 2015). Incorporating the social sciences into OH approaches by examining the social dimensions of human-animal-disease- interactions can further help address topics such as, consumption patterns, human- animal behaviour or environmental conflicts in a novel way and on a greater scale than ever before (Wolf, 2015). By claiming that disease is a biocultural phenomenon and that social factors generally play a crucial role in the emergence, spread and management of zoonotic diseases, central terms and concepts like “globalisation”,“nature,” or the (human) “body” might also benefit from the integration of a social science perspective (Wolf, 2015).
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The role of anthropologists in the management of OH is therefore interesting to investigate (Keune et al., 2017), especially because a broad range of social scientists emphasise the vital role that a social scientific and critical imagination can bring to the OH approach and argue that, without proper social science engagement, the latter is at risk of derailment (Craddock and Hinchliffe, 2015).
1.3.3.2 Anthropology and its role in the management and conceptualisation of One Health
Although these efforts to work across disciplinary boundaries are welcome, there are also risks in seeking unity, not least the tendency of one health visions to reduce diversity and to under-value the local, contingent and practical engagements that make health possible (Hinchliffe, 2015). OH can be defined as “a generalised and flexible term that captures the will to address the complexities and interrelations that exist between human, animal and ecological health” (Craddock and Hinchliffe, 2015). Understanding this complexity requires the accommodation of multiple, often conflicting, perspectives and narratives, rooted in different value systems and temporal–spatial scales (Waltner-Toew, 2017). What could the inclusion of a wider range of social knowledge add to the conceptualisation of OH?
Among the recent trends in OH scholarship, there is an emerging body of social science and policy literature which explores exactly what OH is and should be about. In other words, in what ways have different scholars conceived of OH, and what are the implications of these competing frameworks? Is OH simply a convenient relabelling of existing activities, or a more radical critique of the ways in which science and health professionals work? What lessons can be learnt from recent attempts to institutionalise OH, and what complications are OH research and practice likely to face in the future? (Kingsley and Taylor, 2017).
One group of studies is concerned with the OH aspirations, for what OH might be able to accomplish with a key fault line towards their orientation about global health (Kingsley and Taylor, 2017). Similar work on OH itself (Craddock and Hinchliffe 2015) argues that the dominant framings of these agendas are strategic and political, working in favour of industry and large institutional actors, often at the expense of local communities and non-profits solutions (Cassidy, 2016) and that global health Literature Review | 73 systems focused on biosecurity and infection control risks, ignoring the larger scale political, economic, and biological processes that create the conditions for disease. Hence, a reading of OH that may be useful in building approaches is one that emphasises solidarity and partnership over defensive biosecurity (Mutsaers, 2015). Therefore, should current global health strategies be supported or reformed? Or, more radically, should global health policy expand beyond a sole focus on the welfare of humans? (Kingsley and Taylor, 2017). And how to address anthropocentric contradictions at the heart of OH (Cassidy, 2018) ? This last question raises what Rock and Degeling (2015) have conceptualised about a solidarity that encompasses not only practices intended to assist other people, but also practices intending to assist non-human others, including animals, plants, or places. Consistent with the social sustainability agenda, Rüegg and colleagues (2018) also support that OH could be a vehicle to prioritise approaches that seek to share both risks and benefits of interventions, where humans and non-humans are considered to be prone to much of the same environmental risks, and have a converging set of interests to their integrity (Capps and Lederman, 2015; Degeling et al., 2016).
The other group of OH scholars is concerned with the concrete ways in which OH projects have been carried out. These studies emphasise how the goals of collaboration and coordination are a good deal easier said than done. Professional competition, conflicting priorities, institutional inertia, and myriad other factors in diverse contexts make the implementation of OH projects a major undertaking (Kingsley and Taylor, 2017). Hence a growing body of social science studies has focused on the political economy of OH (Bardosh, 2016) and on the disjunctures between policies and realities of implementation on the ground (MacGregor and Waldman, 2017; Valeix, 2018). The internationally constructed and framed OH approach to control and eliminate African Trypanosomiasis in Uganda constitutes a concrete example of these tensions faced when translating global notions of OH down to national and district levels (Smith et al., 2015). The case of Rift Valley fever in Kenya is other example where political marginalisation and underdevelopment, irrigation and infrastructure investment, and conflict and securitisation, make pastoral areas and people vulnerable to both 1997–1998 and 2006–2007 outbreaks (Dzingirai et al., 2017). OH approaches for all zoonotic diseases must therefore engage with these
74 | C h a p t e r 1 factors, and not just end with an ‘anti-political’ focus on institutional and disciplinary collaboration (Dzingirai et al., 2017).
Delineating some of the theoretical, methodological and political challenges which lie ahead the implementation of OH approaches, the topics outlined hereabove are the central discussions in the emerging social sciences. Craddock and Hinchliffe (2015) highlighted four ‘tasks’ that may provide particular foci for social scientists in the OH debate: (1) Foregrounding uneven geographies, by questioning the integrity of one world and OH concepts while elucidating the effects that uneven power relations, discrepant risks, and variable access to resources have on vulnerabilities and responses to disease outbreaks; (2) problem framing, by questioning how understandings of global convergence and integrated approaches to control zoonotic disease compare to local/national realities; (3) analysing relations, by interrogating the effects of new kinds of connections as it cannot be presumed that partnering always generates mutual understandings, or more equitable and effective responses; and (4) re-distributing expertise, by questioning the emphasis in OH approaches put on professional experts - global institutions, veterinarians, physicians, public health officials – which can under-value other voices and agencies and efface other less easily codified forms of expertise.
More related to the field of science of communication, information studies and social psychology, Lapinski et al. (2015) recommended another set of conceptual areas that can form a basis for understanding how social science might contribute in meaningful ways to OH challenges: (1) understand how humans contextualise their own health within animal and ecosystem health; (2) understand the ways in which information and communication can improve OH outcomes; and (3) identify the key characteristics of new and emerging communication technologies including how and when they can be used globally for information-seeking and sharing about OH issues.
Very recently (end 2017), the “One Health Commission” launched the “One Health- Social Sciences initiative”18. Its mission is to provide a platform for innovation and
18 The “One Health Commission” is a globally focused organisation chartered in Washington, D.C and dedicated to informing all audiences about the importance of transcending institutional and disciplinary boundaries. It launched the “One Health-Social Sciences initiative”: https://www.onehealthcommission.org/en/programs/one_health_social_sciences_initiative/ Literature Review | 75 integration of all social science disciplines to strengthen the OH movement, offering a forum where abovementioned OH failures and emerging discussions of OH could be raised and addressed following a more critically-engaged, iterative approaches giving equal weight to the social, biological and environmental sciences. Alike MacGregor and Waldman (2017) and many others, we argue for “consideration of a richer range of cross-cultural perspectives that can bring nuanced views from ‘many worlds’ to scholarship on OH and can expand the scope and depth of enquiry”. Living well with animals is essential for the welfare of all species and it is likely among the most pressing and urgent issues of our time (Brown and Nading, 2019).
Aagaard-Hansen, J., Chaignat, C.L., 2013. Neglected tropical diseases: equity and social determinants. Neglected Trop. Dis. 8, 135–157. Agudelo Higuita, N.I., Brunetti, E., McCloskey, C., 2016. Cystic Echinococcosis. J. Clin. Microbiol. 54, 518–523. Alexander, A., John, K.R., Jayaraman, T., Oommen, A., Venkata Raghava, M., Dorny, P., Rajshekhar, V., 2011. Economic implications of three strategies for the control of taeniasis. Trop. Med. Int. Health. 16, 1410–1416. Allan, J.C., Velasquez-Tohom, M., Garcia-Noval, J., Torres- Alvarez, R., Yurrita, P., Fletes, C., . . ., Craig, P.S., 1996. Epidemiology of intestinal taeniasis in four rural Guatemalan communities. Ann. Trop. Med. Parasitol. 90, 157-165. Allotey, P., Reidpath, D., Pokhrel, S., 2010. Social sciences research in neglected tropical diseases 1: the ongoing neglect in the neglected tropical diseases. Health Res. Policy Syst. 8, 1-8. Alvarez Rojas, C.A., Romig, T., Lightowlers, M.W., 2014. Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. Int. J. Parasitol. 44, 9–18. Anderson, A., Shwiff, S.A., 2015. The Cost of Canine Rabies on Four Continents. Transbound. Emerg. Dis. 62, 446–452. Assana, E., Amadou, F., Thys, E., Lightowlers, M.W., Zoli, A.P., Dorny, P., Geerts, S., 2010. Pig- farming systems and porcine cysticercosis in the north of Cameroon. J. Helminthol. 84, 441–446. Assana, E., Lightowlers, M.W., Zoli, A.P., Geerts, S., 2013. Taenia solium taeniosis/cysticercosis in Africa: Risk factors, epidemiology and prospects for control using vaccination. Vet. Parasitol. 195, 14–23. Azim, S., Dojki, F., Ahmad, S.S., Beg, M.A., 2008. Role of Human Behaviour and Parasitic Diseases. Infect. Dis. J. Pakistan 17, 117–148. Azlaf, R., Dakkak, A., 2006. Epidemiological study of the cystic echinococcosis in Morocco. Vet. Parasitol. 137, 83–93.
76 | C h a p t e r 1
Azlaf, R., Dakkak, A., Chentoufi, A., El, B.M., 2007. Modelling the transmission of Echinococcus granulosus in dogs in the northwest and in the southwest of Morocco. Vet. Parasitol. 145, 297–303. Bachrach, C.A., Abeles, R.P., 2004. Social science and health research: Growth at the National Institutes of Health. Am. J. Public Health. 94, 22–28. Banyard, A., Fooks, A., 2011. Rabies and rabies-related lyssaviruses. In: Palmer, S.R., Soulsby, L., Torgerson, P., Brown, D.W.G. (Eds.), Oxford Textbook of Zoonoses: Biology, Clinical Practice, and Public Health Control (2nd ed.). Oxford University Press, Oxford. Banyard, A.C., Horton, D.L., Freuling, C., Müller, T., Fooks, A.R., 2013. Control and prevention of canine rabies: the need for building laboratory-based surveillance capacity. Antiviral Res. 98, 357–364. Bardosh, K., 2014. Global aspirations, local realities: the role of social science research in controlling neglected tropical diseases. Infect. Dis. Poverty. 3, 1-15. Bardosh, K., Inthavong, P., Xayaheuang, S., Okello, A.L., 2014a. Controlling parasites, understanding practices: The biosocial complexity of a One Health intervention for neglected zoonotic helminths in northern Lao PDR. Soc. Sci. Med. 120, 215–223. Bardosh, K., Sambo, M., Sikana, L., Hampson, K., Welburn, S.C., 2014b. Eliminating Rabies in Tanzania? Local Understandings and Responses to Mass Dog Vaccination in Kilombero and Ulanga Districts. PLoS Negl. Trop. Dis. 8, e2935. Bardosh, K., 2015. Achieving “Total Sanitation” in Rural African Geographies: Poverty, Participation and Pit Latrines in Eastern Zambia. Geoforum. 66, 53–63. Bardosh, K.L., 2016. Deadly Flies, Poor Profits, and Veterinary Pharmaceuticals: Sustaining the Control of Sleeping Sickness in Uganda. Med. Anthropol. 35, 338–352. Bardosh, K.L., Berbri, I. El, Ducrotoy, M., Bouslikhane, M., Ouafaa, F.F., Welburn, S.C., 2016. Zoonotic encounters at the slaughterhouse: Pathways and possibilities for the control of Cystic Echonococcosis in Northern Morocco. J. Biosoc. Sci. 48 Suppl 1, S92–S115. Bhattarai, R., Budke, C.M., Carabin, H., Proaño, J. V., Flores-Rivera, J., Corona, T., . . ., Flisser, A., 2012. Estimating the non-monetary burden of neurocysticercosis in Mexico. PLoS Negl. Trop. Dis. 6, e1521. Beaglehole, R., Bonita, R., 2010. What is global health? Glob. Health Action 3, 1–2. Berthe, F.C.J., Bouley, T., Karesh, W.B., Le Gall, F.G., Machalaba, C.C., Plante, C.A., Seifman, R.M., 2018. Operational framework for strengthening human, animal and environmental public health systems at their interface. World Bank Group, Washington, D.C. Besbes, M., Sellami, F., Cheikhrouhou, F., Makni, F., Ayadi, A., 2003. L’abattage clandestin en Tunisie: enquête sur les connaissances et les pratiques des bouchers face à l’hydatidose. Bull. la Société Pathol. Exot. 96, 320–322. Bingham, J., 2005. Canine rabies ecology in southern Africa. Emerg. Infect. Dis. 11, 1337–1342. Binot, A., Duboz, R., Promburom, P., Phimpraphai, W., Cappelle, J., Lajaunie, C., . . ., Roger, F.L., 2015. A framework to promote collective action within the One Health community of practice: Using participatory modelling to enable interdisciplinary, cross-sectoral and multi-level integration. One Health. 1, 44–48. Literature Review | 77
Birbeck, G.L., Kalichi, E.M.N., 2004. Epilepsy prevalence in rural Zambia: a door-to-door survey. Trop. Med. Int. Health. 9, 92–95. Bishop, G.C., Durrheim, D.N., Kloeck, P.E., Godlonton, J.D., Bingham, J., Speare, R., Rabies Advisory Group 2000, 2010. Rabies : guide for the medical, veterinary and allied professions (2nd ed.). Government Printer, Pretoria. Biu, A.A., Ahmed, M.I., Mshelia, S.S., 2006. Economic assessment of losses due to parasitic diseases common at the Maiduguri abattoir, Nigeria. African Scientist 7, 143–145. Blancou, J., 2004. Rabies in Europe and the Mediterranean basin; from antiquity to 19th century. In: King, A.A., Fooks, A.R., Aubert, M., Wandeler, A.I. (Eds.), Historical perspective of rabies in Europe and the Mediterranean Basin. OIE (World Organisation for Animal Health), Paris, pp. 15-24. Blancou, J., 2008. The control of rabies in Eurasia: overview, history and background. Dev. Biol. 131, 3–15. Blench, R.M., MacDonald, K.C., 2000. The origins and development of African livestock; Archaeology, genetics, linguistics and ethnography. University College London Press, Taylor & Francis Group, 546 pp. Boa, M.E., Mahundi, E.A., Kassuku, A.A., Willingham, A.L., Kyvsgaard, N.C., 2006. Epidemiological survey of swine cysticercosis using ante-mortem and post-mortem examination tests in the southern highlands of Tanzania. Vet. Parasitol. 139, 249–255. Bobes, R.J., Fragoso, G., Fleury, A., Garcia-Varela, M., Sciutto, E., Larralde, C., Laclette, J.P., 2014. Evolution, molecular epidemiology and perspectives on the research of taeniid parasites with special emphasis on Taenia solium. Infect. Genet. Evol. 23, 150–160. Bourée, P., 2001. Hydatidosis: Dynamics of transmission. World J. Surg. 25, 4–9. Braae, U.C., Magnussen, P., Lekule, F., Harrison, W., Johansen, M.V., 2014. Temporal fluctuations in the sero-prevalence of Taenia solium cysticercosis in pigs in Mbeya Region, Tanzania. Parasit. Vectors. 7, 1-7. Braae, U.C., Harrison, W., Lekule, F., Magnussen, P., Johansen, M.V., 2015. Feedstuff and poor latrines may put pigs at risk of cysticercosis - A case-control study. Vet. Parasitol. 214, 187–191. Braae, U.C., Devleesschauwer, B., Gabriël, S., Dorny, P., Speybroeck, N., Magnussen, P., . . ., Johansen, M.V., 2016. CystiSim – An Agent-Based Model for Taenia solium Transmission and Control. PLoS Negl. Trop. Dis. 10, e0005184. Braae, U.C., Gabriël, S., Trevisan, C., Thomas, L.F., Magnussen, P., Abela-Ridder, B., . . ., Johansen, M.V., 2019. Stepwise approach for the control and eventual elimination of Taenia solium as a public health problem. BMC Infect. Dis. 19, 1-6. Bresalier, M., Cassidy, A., Woods, A., 2015. One Health in history. In: Zinsstag J. (Ed.), One Health: The Theory and Practice of Integrated Health Approaches. CABI, Wallingford, pp. 1–15. Brown, C.M., Conti, L., Ettestad, P., Leslie, M.J., Sorhage, F.E., Sun, B., 2011. Compendium of animal rabies prevention and control, 2011. J. Am. Vet. Med. Assoc. 239, 609–617. Brown, C., 2004. Emerging zoonoses and pathogens of public health significance - an
78 | C h a p t e r 1
overview. Rev. Sci. Tech. 23, 435–442. Brown, H., Nading, A.M., 2019. Introduction: Human Animal Health in Medical Anthropology. Med. Anthropol. Q. 33, 5–23. Brown, K., 2011. Rabid Epidemiologies: The Emergence and Resurgence of Rabies in Twentieth Century South Africa. J. Hist. Biol. 44, 81–101. Brown, P.J., Closser, S., 2016. Understanding and Applying Medical Anthropology (3rd ed.). Routledge, New York, 460 pp. Brundu, D., Piseddu, T., Stegel, G., Masu, G., Ledda, S., Masala, G., 2014. Retrospective study of human cystic echinococcosis in Italy based on the analysis of hospital discharge records between 2001 and 2012. Acta Trop. 140, 91–96. Burniston, S., Okello, A.L., Khamlome, B., Inthavong, P., Gilbert, J., Blacksell, S.D., . . ., Welburn, S.C., 2015. Cultural drivers and health-seeking behaviours that impact on the transmission of pig-associated zoonoses in Lao People’s Democratic Republic. Infect. Dis. Poverty 4, 1-12. Cabrera, P.A., Lloyd, S., Haran, G., Pineyro, L., Parietti, S., Gemmell, M.A., . . ., Valledor, S., 2002. Control of Echinococcus granulosus in Uruguay: Evaluation of different treatment intervals for dogs. Vet. Parasitol. 103, 333–340. Capps, B., Lederman, Z., 2015. One Health, Vaccines and Ebola: The Opportunities for Shared Benefits. J. Agric. Environ. Ethics 28, 1011–1032. Carabin, H., Krecek, R.C., Cowan, L.D., Michael, L., Foyaca-Sibat, H., Nash, T., Willingham, A.L., 2006. Estimation of the cost of Taenia solium cysticercosis in Eastern Cape Province, South Africa. Trop. Med. Int. Health 11, 906–916. Carabin, H., Ndimubanzi, P.C., Budke, C.M., Nguyen, H., Qian, Y., Cowan, L.D., . . ., Dickey, M., 2011. Clinical manifestations associated with neurocysticercosis: a systematic review. PLoS Negl. Trop. Dis. 5, e1152. Carabin, H., Winkler, A.S., Dorny, P., O’Neal, S., Llanos-Zavalaga, F., Gonzalvez, G., 2017. Taenia solium cysticercosis and taeniosis: Achievements from the past 10 years and the way forward. PLoS Negl. Trop. Dis. 11, e0005478. Cardona, G.A., Carmena, D., 2013. A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet. Parasitol. 192, 10– 32. Cascio, A., Bosilkovski, M., Rodriguez-Morales, A.J., Pappas, G., 2011. The Socio-Ecology of Zoonotic Infections. Clin. Microbiol. Infect. 17, 336–342. Cassidy, A., 2016. One Medicine? Advocating (Inter)disciplinarity at the Interfaces of Animal Health, Human Health, and the Environment. In: Frickel, S., Albert, M., Prainsack, B. (Eds.), Investigating Interdisciplinary Collaboration: Theory and Practice across Disciplines. Rutgers University Press, New Brunswick, pp. 213-235. Cassidy, A., 2018. Humans, Other Animals and ‘One Health’ in the Early Twenty-First Century. In: Woods, A., Bresalier, M., Cassidy, A., Mason Dentinger, R. (Eds), Animals and the Shaping of Modern Medicine - One Health and its Histories. Palgrave Macmillan, Basingstoke, pp. 193–236. Literature Review | 79
CATMAT, Committee to Advise on Tropical Medicine and Travel, 2002. Statement on travelers and rabies vaccine. Can. Commun. Dis. Rep. 28,1-12. Chebli, H., Laamrani El Idrissi, A., Benazzouz, M., Lmimouni, B.E., Nhammi, H., Elabandouni, M., . . ., Tamarozzi, F., 2017. Human cystic echinococcosis in Morocco: Ultrasound screening in the Mid Atlas through an Italian-Moroccan partnership. PLoS Negl. Trop. Dis. 11, e0005384. Choffnes, E.R., Relman, D.A., 2011. The causes and impacts of neglected tropical and zoonotic diseases : opportunities for integrated intervention strategies : workshop summary. National Academies Press, Washington, D.C. CILCH, 2007. Comité interministériel de lutte contre l’Hydatidose/Echinococcose. Ministry of Interior, Rabat. CIRAD, 2012. Porcine cysticercosis in northern Tanzania, http://pigtrop.cirad.fr/fr/content/pdf/5129 Cleaveland, S., Kaare, M., Tiringa, P., Mlengeya, T., Barrat, J., 2003. A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Vaccine 21, 1965–1973. Cleaveland, S., Kaare, M., Knobel, D., Laurenson, M.K., 2006. Canine vaccination-Providing broader benefits for disease control. Vet. Microbiol. 117, 43–50. Cleaveland, S., Hampson, K., Kaare, M., 2007. Living with rabies in Africa. Vet. Rec. 161, 293– 294. Cleaveland, S., Lankester, F., Townsend, S., Lembo, T., Hampson, K., 2014. Rabies control and elimination: a test case for One Health. Vet. Rec. 175, 188–193. Cleaveland, S., Sharp, J., Abela-Ridder, B., Allan, K.J., Buza, J., Crump, J.A., . . ., Halliday, J.E.B., 2017. One Health contributions towards more effective and equitable approaches to health in low- and middle-income countries. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-11. Coetzee, P., Weyer, J., Paweska, J.T., Burt, F.J., Markotter, W., Nel, L.H., 2008. Use of a molecular epidemiological database to track human rabies case histories in South Africa. Epidemiol. Infect. 136, 1270–1276. Cohen, C., Sartorius, B., Sabeta, C., Zulu, G., Paweska, J., Mogoswane, M., . . ., Blumberg, L., 2007. Epidemiology and molecular virus characterization of reemerging rabies, South Africa. Emerg. Infect. Dis 13, 1879–1886. Coleman, P.G., Dye, C., 1996. Immunization coverage required to prevent outbreaks of dog rabies. Vaccine. 14, 185-186. Coleman, P.G., Fèvre, E.M., Cleaveland, S., 2004. Estimating the public health impact of rabies. Emerg. Infect. Dis. 10, 140–142. Collier, P., 2007. The Bottom Billion: Why the Poorest Countries are Failing and What can be Done About It. Oxford University Press, Oxford. Conan, A., Akerele, O., Simpson, G., Reininghaus, B., van Rooyen, J., Knobel, D., 2015. Population Dynamics of Owned, Free-Roaming Dogs: Implications for Rabies Control. PLoS Negl. Trop. Dis. 9, 1-19.
80 | C h a p t e r 1
Cook, R.A., Karesh, W.B., Osofsky, S.A., 2004. The Manhattan Principles on “One World, One Health.” New York: Wildlife Conservation Society. Available online (www.oneworldonehealth.org). Coral-Almeida, M., Gabriël, S., Abatih, E.N., Praet, N., Benitez, W., Dorny, P., 2015. Taenia solium Human Cysticercosis: A Systematic Review of Sero-epidemiological Data from Endemic Zones around the World. PLoS Negl. Trop. Dis. 9, e0003919. Cortez-Alcobedes, M.M., Boggio, G., de Lourdes Guerra, M., de Gavidia, M.R., Reyes, G.C.R., Ferrer, E., . . ., Parkhouse, R.M.E., 2010. Evidence that active transmission of porcine cysticercosis occurs in Venezuela. Trop. Anim. Health Prod. 42, 531–537. Craddock, S., Hinchliffe, S., 2015. One world, one health? Social science engagements with the one health agenda. Soc. Sci. Med. 129, 1–4. Craig, P.S., Budke, C.M., Schantz, P.M., Li, T., Qiu, J., Yang, Y., . . ., Ito, A., 2007. Human Echinococcosis: A Neglected Disease? Trop. Med. Health. 35, 283–292. Craig, P.S., Li, T., Qiu, J., Zhen, R., Wang, Q., Giraudoux, P., . . ., Yang, W., 2008. Echinococcosis and Tibetan communities. Emerg. Infect. Dis. 14, 1674–1675. Craig, P.S., Hegglin, D., Lightowlers, M.W., Torgerson, P.R., Wang, Q., 2017. Echinococcosis: Control and Prevention. Adv. Parasitol. 96, 55–158. Cutler, S.J., Fooks, A.R., Van Der Poel, W.H.M., 2010. Public health threat of new, reemerging, and neglected zoonoses in the industrialized world. Emerg. Infect. Dis. 16, 1–7. Dacheux, L., Wacharapluesadee, S., Hemachudha, T., Meslin, F.-X., Buchy, P., Reynes, J.-M., Bourhy, H., 2010. More Accurate Insight into the Incidence of Human Rabies in Developing Countries through Validated Laboratory Techniques. PLoS Negl. Trop. Dis. 4, e765. Dakkak, A., 2010. Echinococcosis/hydatidosis: A severe threat in Mediterranean countries. Vet. Parasitol. 174, 2–11. Dakkak, A., El Berbri, I., Petavy, A.F., Boué, F., Bouslikhane, M., Fassi Fihri, O., . . ., Ducrotoy, M.J., 2017. Echinococcus granulosus infection in dogs in Sidi Kacem Province (North- West Morocco). Acta Trop. 165, 26–32. Daszak, P., Cunningham, A.A., Hyatt, A.D., 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop. 78, 103–116. Dean, D.J., Abelseth, M.K., Atanasiu, P., 1996. The fluorescent antibody test. In: Meslin, F.-X., Kaplan, M.M., Koprowski, H. (Eds.), Laboratory Techniques in Rabies (4th Ed). World Health Organization, Geneva, pp. 88–89 de Coster, T., Van Damme, I., Baauw, J., Gabriël, S., 2018. Recent advancements in the control of Taenia solium: A systematic review. Food Waterborne Parasitol. 13, e00030. Del Brutto, O.H., Wadia, N.H., Dumas, M., Cruz, M., Tsang, V.C., Schantz, P.M., 1996. Proposal of diagnostic criteria for human cysticercosis and neurocysticercosis. J. Neurol. Sci. 142, 1– 6. Del Brutto, O.H., Nash, T.E., White, A.C., Rajshekhar, V., Wilkins, P.P., Singh, G., . . ., Garcia, H.H., 2017. Revised diagnostic criteria for neurocysticercosis. J. Neurol. Sci. 372, 202–210. Literature Review | 81
DELM, 2010. Ministry of Health of Morocco (Ministère de la Santé du Maroc). Bilan des activités des programmes de lutte contre les maladies parasitaires, année 2010. Direction de l’Epidémiologie et de la Lutte contre les maladies. Service des maladies parasitaires. DELM, 2012. Ministry of Health of Morocco (Ministère de la Santé du Maroc). Situation épidémiologique des maladies parasitaires, année 2012. Direction de l’Epidémiologie et de la Lutte contre les maladies. Service des maladies parasitaires. Deplazes, P., Rinaldi, L., Alvarez Rojas, C.A., Torgerson, P.R., Harandi, M.F., Romig, T., . . ., Jenkins, E.J., 2017. Global Distribution of Alveolar and Cystic Echinococcosis. Adv. Parasitol. 96, 315–493. Descola, P., 2015. Beyond Nature and Culture. University of Chicago Press, Chicago. Destoumieux-Garzón, D., Mavingui, P., Boetsch, G., Boissier, J., Darriet, F., Duboz, P., . . ., Voituron, Y., 2018. The One Health Concept: 10 Years Old and a Long Road Ahead. Front. Vet. Sci. 5, 14. Devleesschauwer, B., Ale, A., Torgerson, P., Praet, N., Maertens de Noordhout, C., Pandey, B.D., . . ., Speybroeck, N., 2014. The burden of parasitic zoonoses in Nepal: a systematic review. PLoS Negl. Trop. Dis. 8, e2634. Djurković-Djaković, O., Bobić, B., Nikolić, A., Klun, I., Dupouy-Camet, J., 2013. Pork as a source of human parasitic infection. Clin. Microbiol. Infect. 19, 586–594. Doble, L., Fèvre, E.M., 2010. Focusing on neglected zoonoses. Vet. Rec. 166, 546–547. Donadeu, M., Lightowlers, M.W., Fahrion, A.S., Kessels, J., Abela-Ridder, B., 2016. Taenia solium: WHO endemicity map update. Relev. Epidemiol. Hebd. 91, 595–599. Donadeu, M., Fahrion, A.S., Olliaro, P.L., Abela-Ridder, B., 2017. Target product profiles for the diagnosis of Taenia solium taeniasis, neurocysticercosis and porcine cysticercosis. PLoS Negl. Trop. Dis. 11, e0005875. Dorea, F.C., Dupuy, C., Vial, F., Reynolds, T.L., Akkina, J.E., 2014. Toward one health: are public health stakeholders aware of the field of animal health? Infect. Ecol. Epidemiol. 4, 24267. Dorny, P., Phiri, I.., Vercruysse, J., Gabriël, S., Willingham, A.., Brandt, J., . . ., Berkvens, D., 2004. A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. Int. J. Parasitol. 34, 569–576. Duboz, R., Echaubard, P., Promburom, P., Kilvington, M., Ross, H., Allen, W., . . ., Binot, A., 2018. Systems Thinking in Practice: Participatory Modeling as a Foundation for Integrated Approaches to Health. Front. Vet. Sci. 5, 1-8. Dunn, F.L., 1979. Behavioural aspects of the control of parasitic diseases. Bull. World Health Organ. 57, 499–512. Dwyer, J.P., Douglas, T.S., van As, A.B., 2007. Dog bite injuries in children--a review of data from a South African paediatric trauma unit. S. Afr. Med. J. 97, 597–600. Dzingirai, V., Bukachi, S., Leach, M., Mangwanya, L., Scoones, I., Wilkinson, A., 2017. Structural drivers of vulnerability to zoonotic disease in Africa. Philos. Trans. R. Soc. B Biol. Sci. 372, 1–9.
82 | C h a p t e r 1
Eckert, J., Gemmell, M.A., Meslin, F.X., Pawlowski, Z.S., 2001. WHO/OIE manual on echinococcosis in humans and animals : a public health problem of global concern. World Organisation for Animal Health. Eckert, J., Deplazes, P., 2004. Biological, Epidemiological, and Clinical Aspects of Echinococcosis, a Zoonosis of Increasing Concern. Clin. Microbiol. Rev. 17, 107–135. El Berbri, I., Ducrotoy, M.J., Petavy, A.-F., Fassifihri, O., Shaw, A.P., Bouslikhane, M., . . ., Dakkak, A., 2015. Knowledge, attitudes and practices with regard to the presence, transmission, impact, and control of cystic echinococcosis in Sidi Kacem Province, Morocco. Infect. Dis. Poverty 4, 1-12. Ember, C.R., Ember, M., 2004. Encyclopedia of Medical Anthropology : Health and Illness in the World’s Cultures. Kluwer Academic/Plenum, New York. Epstein, J.H., Price, J.T., 2009. The significant but understudied impact of pathogen transmission from humans to animals. Mt. Sinai J. Med. 76, 448–455. Ertel, R.L., Braae, U.C., Ngowi, H.A., Johansen, M.V., 2017. Assessment of a computer-based Taenia solium health education tool ‘The Vicious Worm’ on knowledge uptake among professionals and their attitudes towards the program. Acta Trop. 165, 240–245. Evans-Pritchard, E.E., 1960. The Nuer: A description of the modes of livelihood and political institutions of a Nilotic people. Clarendon Press, Oxford. FAO, 2013. World livestock 2013 : Changing disease landscapes. Food and Agriculture Organisation, Rome. FAO, OIE, WHO, UNSIC, UNICEF, the World Bank, 2008. Contributing to One World, One Health. A Strategic Framework for Reducing Risks of Infectious Diseases at the Animal– Human–Ecosystems Interface. Geneva. FAO, OIE, WHO, 2010. The FAO-OIE-WHO Collaboration: Sharing Responsibilities and Coordinating Global Activities to Address Health Risks at the Anima-human- ecosystems Interfaces: a Tripartite Concept Note. World Health Organization. FAO, WHO, 2014. Multicriteria-Based Ranking for Risk Management of Food-Born Parasites, Microbiological Risk Assessment Series 23, FAO/WHO. Feasey, N., Wansbrough-Jones, M., Mabey, D.C.W., Solomon, A.W., 2010. Neglected tropical diseases. Br. Med. Bull. 93, 179–200. Fitzpatrick, M.C., Shah, H.A., Pandey, A., Bilinski, A.M., Kakkar, M., Clark, A.D., . . ., Galvani, A.P., 2016. One Health approach to cost-effective rabies control in India. Proc. Natl. Acad. Sci. U. S. A. 113, 14574–14581. Fleising, U., 2000. The ethology of mythical images in healthcare biotechnology: A methodological approach to uncovering ritualized behavior in the evolution of sickness and healing. Anthropol. Med. 7, 227–250. Flisser, A., Gauci, C.G., Zoli, A., Martinez-Ocaña, J., Garza-Rodriguez, A., Dominguez-Alpizar, J.L., . . ., Lightowlers, M.W., 2004. Induction of protection against porcine cysticercosis by vaccination with recombinant oncosphere antigens. Infect. Immun. 72, 5292–5297. Flisser, A., Rodríguez-Canul, R., Willingham, A.L., 2006. Control of the taeniosis/cysticercosis complex: Future developments. Vet. Parasitol. 139, 283–292. Literature Review | 83
Flisser, A., 2013. State of the art of Taenia solium as compared to Taenia asiatica. Korean J. Parasitol. 51, 43–49. Fooks, A.R., McElhinney, L.M., Horton, D., Banyard, A.C., Johnson, N., Marston, D., . . ., Rupprechtet, C.E., 2012. Molecular tools for rabies diagnosis in animals. In: Fooks, A.R., Müller, T. (Eds.), Rabies control—towards sustainable prevention at the source, compendium of the OIE global conference on rabies control. OIE (World Organisation for Animal Health). pp. 75–87 Fooks, A.R., Banyard, A.C., Horton, D.L., Johnson, N., McElhinney, L.M., Jackson, A.C., 2014. Current status of rabies and prospects for elimination. Lancet. 384, 1389–1399. Fox, R., King, B., 2002. Anthropology beyond culture. Berg, Oxford.Franklin, S., 2001. Sheepwatching. Anthropol. Today 17, 3–9. Frickel, S., Albert, M., Prainsack, B., 2016. Investigating interdisciplinary collaboration : theory and practice across disciplines. Rutgers University Press, New Brunswick, 256 pp. Gabriël, S., Johansen, M.V., Pozio, E., Smit, G.S., Devleesschauwer, B., Allepuz, A., . . ., Dorny, P., 2015. Human migration and pig/pork import in the European Union: what are the implications for Taenia solium infections? Vet. Parasitol. 213, 38-45. Gabriël, S., Dorny, P., Mwape, K.E., Trevisan, C., Braae, U.C., Magnussen, P., . . ., Johansen, M. V, 2017. Control of Taenia solium taeniasis/cysticercosis: The best way forward for sub- Saharan Africa? Acta Trop. 165, 252–260. Gabriël, S., Mwape, K.E., Phiri, I.K., Devleesschauwer, B., Dorny, P., 2019. Taenia solium control in Zambia: The potholed road to success. Parasite Epidemiol. Control 4, e00082. Garba, A.S., Dzikwi, A., Okewole, P., Chitunya-Wilson, B., Tirmidhi, A., Kazeem, H., Umoh, J., 2013. Evaluation of dog slaughter and consumption practices related to the control of rabies in Nigeria. J. Exp. Biol. Agric. Sci. 1, 125–130. García, H.H., Gonzalez, A.E., Gilman, R.H., Cysticercosis Working Group in Peru, 2003. Diagnosis, treatment and control of Taenia solium cysticercosis. Curr. Opin. Infect. Dis. 16, 411–419. García, H.H., González, A.E., Del Brutto, O.H., Tsang, V.C.W., Llanos-Zavalaga, F., Gonzalvez, G., . . ., Gilman, R.H., 2007. Strategies for the elimination of taeniasis/cysticercosis. J. Neurol. Sci. 262, 153–157. García, H.H., Gonzalez, A.E., Tsang, V.C.W., O’Neal, S.E., Llanos-Zavalaga, F., Gonzalvez, G., . . ., Gilman, R.H., Cysticercosis Working Group in Peru, 2016. Elimination of Taenia solium Transmission in Northern Peru. N. Engl. J. Med. 374, 2335–2344. Germonpré, M., Sablin, M.V., Stevens, R.E., Hedges, R.E.M., Hofreiter, M., Stiller, M., Despres, V.R., 2009. Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J. Archaeol. Sci. 36,473-490. Gibbons, R. V, 2002. Cryptogenic rabies, bats, and the question of aerosol transmission. Ann. Emerg. Med. 39, 528–536. Gibbs, E.P.J., 2014. The evolution of One Health: a decade of progress and challenges for the future. Vet. Rec. 174, 85–91. Gilman, R.H., Gonzalez, A.E., Llanos-Zavalaga, F., Tsang, V.C.W., Garcia, H.H., Cysticercosis
84 | C h a p t e r 1
Working Group in Peru, 2012. Prevention and control of Taenia solium taeniasis/cysticercosis in Peru. Pathog. Glob. Health 106, 312–318. Gonzalez, A.E., Gauci, C.G., Barber, D., Gilman, R.H., Tsang, V.C.W., Garcia, H.H., . . ., Lightowlers, M.W., 2005. Vaccination of pigs to control human neurocysticercosis. Am. J. Trop. Med. Hyg. 72, 837–839. Gonzales, I., Rivera, J.T., Garcia, H.H., 2016. Pathogenesis of Taenia solium taeniasis and cysticercosis. Parasite Immunol. 38, 136–146. Grace, D., Mutua, F., Ochungo, P., Kruska, R.L., Jones, K., Brierley, L., . . ., Ogutu, F., 2012. Mapping of poverty and likely zoonoses hotspots. Zoonoses Project 4. Report to the UK Department for International Development. ILRI, Nairobi. Guba, E., 1985. The Context of Emergent Paradigm Research. In: Lincoln, Y. (Ed.), Organizational Theory and Inquiry: The Paradigm Revolution. Sage Publications, Beverly Hills. pp. 79-104. Guezala, M.-C., Rodriguez, S., Zamora, H., Garcia, H.H., Gonzalez, A.E., Tembo, A., . . ., Craig, P.S., 2009. Development of a species-specific coproantigen ELISA for human Taenia solium taeniasis. Am. J. Trop. Med. Hyg. 81, 433–437. Gweba, M., Faleke, O.O., Junaidu, A.U., Fabiyi, J.P., Fajinmi, A.O., 2010. Some risk factors for Taenia solium cysticercosis in semi-intensively raised pigs in Zuru, Nigeria. Vet. Ital. 46, 57–67. Hall, R., Durrheim, D.N., 2011. One Health: much more than a slogan. N. S. W. Public Health Bull. 22, 97–98. Hambolu, S.E., Dzikwi, A.A., Kwaga, J.K.P., Kazeem, H.M., Umoh, J.U., Hambolu, D.A., 2013. Rabies and dog bites cases in lagos state Nigeria: a prevalence and retrospective studies (2006-2011). Glob. J. Health Sci. 6, 107–114. Hampson, K., Dobson, A., Kaare, M., Dushoff, J., Magoto, M., Sindoya, E., Cleaveland, S., 2008. Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies. PLoS Negl. Trop. Dis. 2, e339. Hampson, K., Dushoff, J., Cleaveland, S., Haydon, D.T., Kaare, M., Packer, C., Dobson, A., 2009. Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biol. 7, e53. Hampson, K., Coudeville, L., Lembo, T., Sambo, M., Kieffer, A., Attlan, M., . . ., Dushoff, J., on behalf of the Global Alliance for Rabies Control Partners for Rabies Prevention, 2015. Estimating the Global Burden of Endemic Canine Rabies. PLoS Negl. Trop. Dis. 9, e0003709. Häsler, B., Hiby, E., Gilbert, W., Obeyesekere, N., Bennani, H., Rushton, J., 2014. A One Health Framework for the Evaluation of Rabies Control Programmes: A Case Study from Colombo City, Sri Lanka. PLoS Negl. Trop. Dis. 8, e3270. Hassell, J.M., Begon, M., Ward, M.J., Fèvre, E.M., 2017. Urbanization and Disease Emergence: Dynamics at the Wildlife-Livestock-Human Interface. Trends Ecol. Evol. 32, 55–67. Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Devleesschauwer, B., on behalf of World Health Organization Foodborne Disease Burden Epidemiology Literature Review | 85
Reference Group, 2015. World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLOS Med. 12, e1001923. Hemachudha, T., Laothamatas, J., Rupprecht, C.E., 2002. Human rabies: a disease of complex neuropathogenetic mechanisms and diagnostic challenges. Lancet. Neurol. 1, 101–109. Hemachudha, T., Ugolini, G., Wacharapluesadee, S., Sungkarat, W., Shuangshoti, S., Laothamatas, J., 2013. Human rabies: neuropathogenesis, diagnosis, and management. Lancet Neurol. 12, 498–513. Hergert, M., Nel, L.H., 2013. Dog Bite Histories and Response to Incidents in Canine Rabies- Enzootic KwaZulu-Natal, South Africa. PLoS Negl. Trop. Dis. 7, e2059. Herrador, Z., Siles-Lucas, M., Aparicio, P., Lopez-Velez, R., Gherasim, A., Garate, T., Benito, A., 2016. Cystic Echinococcosis Epidemiology in Spain Based on Hospitalization Records, 1997-2012. PLoS Negl. Trop. Dis. 10, e0004942. Hinchliffe, S., 2015. More than one world, more than one health: Re-configuring interspecies health. Soc. Sci. Med. 129, 28–35. Hobbs, E.C., Mwape, K.E., Devleesschauwer, B., Gabriël, S., Chembensofu, M., Mambwe, M., . . ., Speybroeck, N., 2018. Taenia solium from a community perspective: Preliminary costing data in the Katete and Sinda districts in Eastern Zambia. Vet. Parasitol. 251, 63–67. Hotez, P.J., Ottesen, E., Fenwick, A., Molyneux, D., 2006. The neglected tropical diseases: The ancient afflictions of stigma and poverty and the prospects for their control and elimination. Adv. Exp. Med. Biol. 582, 23–33. Hotez, P.J., Molyneux, D.H., Fenwick, A., Kumaresan, J., Sachs, S.E., Sachs, J.D., Savioli, L., 2007. Control of neglected tropical diseases. N. Engl. J. Med. 357, 1018–1027. Hotez, P.J., Fenwick, A., Savioli, L., Molyneux, D.H., 2009. Rescuing the bottom billion through control of neglected tropical diseases. Lancet. 373, 1570–1575. Inhorn, M.C., Brown, P.J., 1995. The Anthropology of Infectious Disease - International Health Perspectives. Theory and practice in medical anthropology and international health. Routledge, Vol. 4., 512 pp. Inhorn, M.C., Janes, C.R., 2007. The behavioural research agenda in global health: an advocate’s legacy. Glob. Public Health. 2, 294–312. Iowa State University Center for Food Security and Public Health, 2012. Rabies and Rabies- Related Lyssaviruses. Center for Food Security and Public Health Technical Factsheets. 106. http://lib.dr.iastate.edu/cfsph_factsheets/106. Ito, A., Urbani, C., Jiamin, Q., Vuitton, D.A., Dongchuan, Q., Heath, D.D., . . ., Schantz, P.M., 2003. Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in China. Acta Trop. 86, 3–17. Jackson, A.C., 2013. Rabies, in: Viral Infections of the Human Nervous System. Springer Basel, Basel, pp. 211–235. Jackson, A.C., 2016. Human Rabies: a 2016 Update. Curr. Infect. Dis. Rep. 18, 38. Janes, C.R., Corbett, K.K., Jones, J.H., Trostle, J., 2012. Emerging infectious diseases: the role of social sciences. Lancet. 380, 1884–1886.
86 | C h a p t e r 1
Johansen, M.V., Penrith, M.L., 2009. Has culling been properly assessed as a valid and justified control intervention measure for zoonotic diseases? PLoS Negl. Trop. Dis. 3, e541. Johansen, M.V., Trevisan, C., Braae, U.C., Magnussen, P., Ertel, R.L., Mejer, H., Saarnak, C.F.L., 2014. The vicious worm: A computer-based taenia solium education tool. Trends Parasitol. 30, 372–374. Johansen, M.V., Trevisan, C., Gabriël, S., Magnussen, P., Braae, U.C., 2017. Are we ready for Taenia solium cysticercosis elimination in sub-Saharan Africa? Parasitology. 144, 59–64. John, K., Kazwala, R., Mfinanga, G.S., 2008. Knowledge of causes, clinical features and diagnosis of common zoonoses among medical practitioners in Tanzania. BMC Infect. Dis. 8, 1-8. Johnson, N., Phillpotts, R., Fooks, A.R., 2006. Airborne transmission of lyssaviruses. J. Med. Microbiol. 55, 785–790. Johnson, R.B., Onwuegbuzie, A.J., 2004. Mixed Methods Research: A Research Paradigm Whose Time Has Come. Educ. Res. 33, 14–26. Jones, B.A., Grace, D., Kock, R., Alonso, S., Rushton, J., Said, M.Y., . . ., Pfeiffer, D.U., 2013. Zoonosis emergence linked to agricultural intensification and environmental change. Proc. Natl. Acad. Sci. U. S. A. 110, 8399–8404. Joshi, D.D., Sharma, M., Waltner-Toews, D., 2012. Rebuilding Urban Ecosystems for Better Community Health in Kathmandu. In: Charron, D. (Ed.), Ecohealth Research in Practice: Innovative Applications of an Ecosystem Approach to Health. Springer, Ottawa, pp. 191– 201. Kaare, M., Lembo, T., Hampson, K., Ernest, E., Estes, A., Mentzel, C., Cleaveland, S., 2009. Rabies control in rural Africa: evaluating strategies for effective domestic dog vaccination. Vaccine. 27, 152–160. Kachani, M., Macpherson, C.N.L., Lyagoubi, M., Berrada, M., Bouslikhane, M., Kachani, F., El Hasnaoui, M., 2003. Public health education/importance and experience from the field. Educational impact of community-based ultrasound screening surveys. Acta Trop. 85, 263–269. Kachani, M., Heath, D., 2014. Dog population management for the control of human echinococcosis. Acta Trop. 139, 99–108. Kaplan, B., Scott, C., 2011. Who coined the term “One Medicine”? Newsl. One Health Initiat. 4, 20–21. Karesh, W.B., Dobson, A., Lloyd-Smith, J.O., Lubroth, J., Dixon, M.A., Bennett, M., . . ., Heymann, D.L., 2012. Ecology of zoonoses: natural and unnatural histories. Lancet 380, 1936– 1945. Kebede, W., Hagos, A., Girma, Z., Lobago, F., 2009. Echinococcosis/hydatidosis: its prevalence, economic and public health significance in Tigray region, North Ethiopia. Trop. Anim. Health Prod. 41, 865–871. Keck, F., Lynteris, C., 2018. Zoonosis: Prospects and challenges for medical anthropology. Med. Anthropol. Theory. 5, 1-14. Kelly, J.D., 2014. Introduction: The ontological turn in French philosophical anthropology. HAU J. Ethnogr. Theory. 4, 259–269. Literature Review | 87
Keune, H., Flandroy, L., Thys, S., De Regge, N., Mori, M., Antoine-Moussiaux, N., . . ., van den Berg T., 2017. The need for European OneHealth/EcoHealth networks. Arch. Public Health 75, 1–8. King, A.A., International Office of Epizootics., World Health Organization. Collaborating Centre for the Characterisation of Rabies and Rabies-related Viruses., Veterinary Laboratories Agency., 2004. Historical perspective of rabies in Europe and the Mediterranean Basin : a testament to rabies by Dr. Arthur A. King, World Organ. ed. World Organisation for Animal Health. Kingsley, P., Taylor, E.M., 2017. One Health: competing perspectives in an emerging field. Parasitology. 144, 7–14. Knobel, D.L., Cleaveland, S., Coleman, P.G., Fevre, E.M., Meltzer, M.I., Miranda, M.E., . . ., Meslin, F.X., 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull. World Health Organ. 83, 360–368. Knobel, D.L., Laurenson, M.K., Kazwala, R.R., Boden, L.A., Cleaveland, S., 2008a. A cross- sectional study of factors associated with dog ownership in Tanzania. BMC Vet. Res. 4, 5. Knobel, D.L., Laurenson, K.M., Kazwala, R.R., Cleaveland, S., 2008b. Development of an Item Scale to Assess Attitudes towards Domestic Dogs in the United Republic of Tanzania. Anthrozoös. 21, 285–295. Knobel, D.L., Arega, S., Reininghaus, B., Simpson, G.J.G., Gessner, B.D., Stryhn, H., Conan, A., 2017. Rabies vaccine is associated with decreased all-cause mortality in dogs. Vaccine. 35, 3844–3849. Komba, E.V.G., Komba, E. V, Mkupasi, E.M., Mbyuzi, A.O., Mshamu, S., Luwumba, D.,. . .., Mzula, A., 2012. Sanitary practices and occurrence of zoonotic conditions in cattle at slaughter in Morogoro Municipality, Tanzania: implications for public health. Tanzan. J. Health Res. 14, 131–138. Krecek, R.C., Michael, L.M., Schantz, P.M., Ntanjana, L., Smith, M.F., Dorny, P., . . ., Willingham, A.L., 2008. Prevalence of Taenia solium cysticercosis in swine from a community-based study in 21 villages of the Eastern Cape Province, South Africa. Vet. Parasitol. 154, 38– 47. Krecek, R.C., Mohammed, H., Michael, L.M., Schantz, P.M., Ntanjana, L., Morey, L., . . ., Willingham, A.L., 2012. Risk factors of Porcine cysticercosis in the Eastern Cape Province, South Africa. PLoS One 7, 3–7. Kungu, J.M., Dione, M.M., Ejobi, F., Ocaido, M., Grace, D., 2017. Risk factors, perceptions and practices associated with Taenia solium cysticercosis and its control in the smallholder pig production systems in Uganda: a cross-sectional survey. BMC Infect. Dis. 17, 1-9. Lainé, N., 2018. Elephant tuberculosis as a reverse zoonosis: Postcolonial scenes of compassion, conservation, and public health in Laos and France. Med. Anthropol. Theory. 5, 157-176. Landford, J., Nunn, M., 2012. Good governance in “One Health” approaches. OIE Rev. Sci. Tech. 31, 561–575. Langdon, E.J., Wiik, F.B., 2010. Anthropology, health and illness: an introduction to the
88 | C h a p t e r 1
concept of culture applied to the health sciences. Rev. Lat. Am. Enfermagem. 18, 459– 466. Lapinski, M.K., Funk, J.A., Moccia, L.T., 2015. Recommendations for the role of social science research in One Health. Soc. Sci. Med. 129, 51–60. Lapiz, S.M.D., Miranda, M.E.G., Garcia, R.G., Daguro, L.I., Paman, M.D., Madrinan, F.P., . . ., Briggs, D.J., 2012. Implementation of an Intersectoral Program to Eliminate Human and Canine Rabies: The Bohol Rabies Prevention and Elimination Project. PLoS Negl. Trop. Dis. 6. Larrieu, E., Zanini, F., 2012. Critical analysis of cystic echinococcosis control programs and praziquantel use in South America, 1974-2010. Rev. Panam. Salud Pública 31, 81–87. Larrieu, E., Mujica, G., Gauci, C.G., Vizcaychipi, K., Seleiman, M., Herrero, E., . . ., Lightowlers, M.W., 2015. Pilot Field Trial of the EG95 Vaccine Against Ovine Cystic Echinococcosis in Rio Negro, Argentina: Second Study of Impact. PLoS Negl. Trop. Dis. 9, e0004134. Leach, E., 1989. Anthropological Aspects of Language: Animal Categories and Verbal Abuse. Anthrozoös. 2, 151–165. Leach, M., Scoones, I., 2013. The social and political lives of zoonotic disease models: Narratives, science and policy. Soc. Sci. Med. 88, 10–17. Leach, M., Bett, B., Said, M., Bukachi, S., Sang, R., Anderson, N., . . ., Koninga, J., 2017. Local disease-ecosystem-livelihood dynamics: reflections from comparative case studies in Africa. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-18. Lebel, J., 2004. Ecohealth and the Developing World. Ecohealth 1, 325–326. Lebov, J., Grieger, K., Womack, D., Zaccaro, D., Whitehead, N., Kowalcyk, B., MacDonald, P.D.M., 2017. A framework for One Health research. One Health. 3, 44–50. Léchenne, M., Miranda, M.E., Zinsstag, J., 2015. Chap 16: Integrated Rabies Control. In: Zinsstag, J., Schelling, E., Waltner-Toews, D., Whittaker, M., Tanner, M. (Eds.), One Health - The Theory and Practice of Integrated Health Approaches, 2015th ed, Statewide Agricultural Land Use Baseline 2015. CAB International, pp. 176-189. Lee, K., Brumme, Z.L., 2013. Operationalizing the One Health approach: The global governance challenges. Health Policy Plan. 28, 778–785. Lefkowitz, E.J., Dempsey, D.M., Hendrickson, R.C., Orton, R.J., Siddell, S.G., Smith, D.B., 2018. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 46, D708–D717. Lembo, T., Niezgoda, M., Velasco-Villa, A., Cleaveland, S., Ernest, E., Rupprecht, C.E., 2006. Evaluation of a direct, rapid immunohistochemical test for rabies diagnosis. Emerg. Infect. Dis. 12, 310–313. Lembo, T., Attlan, M., Bourhy, H., Cleaveland, S., Costa, P., de Balogh, K., . . ., Briggs, D.J., 2011. Renewed global partnerships and redesigned roadmaps for rabies prevention and control. Vet. Med. Int. 2011, 1-18. Lembo, T., Partners for Rabies Prevention, 2012. The blueprint for rabies prevention and control: a novel operational toolkit for rabies elimination. PLoS Negl. Trop. Dis. 6, e1388. Lembo, T., Craig, P.S., Miles, M.A., Hampson, K.R., Meslin, F.X., 2013. Zoonoses prevention, Literature Review | 89
control, and elimination in dogs. In: Macpherson, C.N.L., Meslin, F.X., Wandeler, A.I. (Eds.), Dogs, Zoonoses and Public Health. CABI, Wallingford, pp. 205–258. Lerner, H., Berg, C., 2017. A Comparison of Three Holistic Approaches to Health: One Health, EcoHealth, and Planetary Health. Front. Vet. Sci. 4, 1-7. LeRoux, K., Stewart, D., Perrett, K.D., Nel, L.H., Kessels, J.A., Abela-Ridder, B., 2018. Rabies control in Kwazulu-Natal, South Africa. Bull. World Health Organ. 96, 360–365. Leung, A.K.C., Davies, H.D., Hon, K.-L.E., 2007. Rabies: Epidemiology, pathogenesis, and prophylaxis. Adv. Ther. 24, 1340–1347. Levi-Strauss, C., 1963. Totemism. Beacon, Boston. Li, D., Gao, Q., Liu, J., Feng, Y., Ning, W., Dong, Y., . . ., Xin, D., 2015. Knowledge, attitude, and practices (KAP) and risk factors analysis related to cystic echinococcosis among residents in Tibetan communities, Xiahe County, Gansu Province, China. Acta Trop. 147, 17–22. Lightowlers, M.W., 2006. Vaccines against cysticercosis and hydatidosis: Foundations in taeniid cestode immunology. Parasitol. Int. 55, S39–S43. Lightowlers, M.W., 2010. Eradication of Taenia solium cysticercosis: A role for vaccination of pigs. Int. J. Parasitol. 40, 1183–1192. Lightowlers, M.W., 2012. Cysticercosis and echinococcosis. In: Mackenzie, J.S., Jeggo, M., Daszak, P., Richt, J.A. (Eds.), One Health: The Human-Animal-Environment Interfaces in Emerging Infectious Diseases. Curr. Top. Microbiol. Immunol. 365. Springer, Berlin, pp. 315–335. Lightowlers, M.W., 2013. Cysticercosis and echinococcosis. Curr. Top. Microbiol. Immunol. 365, 315–335. Lightowlers, M.W., Garcia, H.H., Gauci, C.G., Donadeu, M., Abela-Ridder, B., 2016. Monitoring the outcomes of interventions against Taenia solium: Options and suggestions. Parasite Immunol. 38, 158–169. Lightowlers, M.W., Donadeu, M., 2017. Designing a Minimal Intervention Strategy to Control Taenia solium. Trends Parasitol. 33, 426–434. Lindahl, J.F., Grace, D., 2015. The consequences of human actions on risks for infectious diseases: a review. Infect. Ecol. Epidemiol. 5, 30048. Liverani, M., Waage, J., Barnett, T., Pfeiffer, D.U., Rushton, J., Rudge, J.W., . . ., Coker, R.J., 2013. Understanding and Managing Zoonotic Risk in the New Livestock Industries. Environ. Health Perspect. 121, 873-877. Lyall, C., Bruce, A., Tait,. J., Meagher, L., 2011. Interdisciplinary research journeys : Practical strategies for capturing creativity. Bloomsbury Academic, London. Mableson, H.E., Okello, A., Picozzi, K., Welburn, S.C., 2014. Neglected Zoonotic Diseases-The Long and Winding Road to Advocacy. PLoS Negl. Trop. Dis. 8, e2800. Mabry, P.L., Olster, D.H., Morgan, G.D., Abrams, D.B., 2008. Interdisciplinarity and Systems Science to Improve Population Health. Am. J. Prev. Med. 35, S211–S224. MacGregor, H., Waldman, L., 2017. Views from many worlds: unsettling categories in
90 | C h a p t e r 1
interdisciplinary research on endemic zoonotic diseases. Philos. Trans. R. Soc. B Biol. Sci. 372, 1–9. Macpherson, C.N.L., 2005. Human behaviour and the epidemiology of parasitic zoonoses. Int. J. Parasitol. 35, 1319–1331. Mallewa, M., Fooks, A.R., Banda, D., Chikungwa, P., Mankhambo, L., Molyneux, E., . . ., Solomon, T., 2007. Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg. Infect. Dis. 13, 136–139. Manderson, L., Aagaard-Hansen, J., Allotey, P., Gyapong, M., Sommerfeld, J., 2009. Social research on neglected diseases of poverty: Continuing and emerging themes. PLoS Negl. Trop. Dis. 3, 1–6. Mangesho, P.E., Neselle, M.O., Karimuribo, E.D., Mlangwa, J.E., Queenan, K., Mboera, L.E.G., . . ., Rweyemamu, M., 2017. Exploring local knowledge and perceptions on zoonoses among pastoralists in northern and eastern Tanzania. PLoS Negl. Trop. Dis. 11, 1-22. Mani, C.S., Murray, D.L., 2006. Rabies. Pediatr. Rev. 27, 129–136. Manning, S.E., Rupprecht, C.E., Fishbein, D., Hanlon, C.A., Lumlertdacha, B., Guerra, M., . . ., Hull, H.F., 2008. Human rabies prevention--United States, 2008: recommendations of the Advisory Committee on Immunization Practices. Morbidity and Mortality Weekly Report, Recommendation and Reports / Centers for Disease Control. 57, 1–28. Marcotty, T., Matthys, F., Godfroid, J., Rigouts, L., Ameni, G., Gey van Pittius, N., . . ., van den Bossche, P., 2009. Zoonotic tuberculosis and brucellosis in Africa: neglected zoonoses or minor public-health issues? The outcomes of a multi-disciplinary workshop. Ann. Trop. Med. Parasitol. 103, 401–411. Maridadi, a F., Lwelamira, J., Simime, F.G., 2011. Knowledge and practices related to T. solium Cysticercosis-Taeniasis among smallholder farmers in selected villages in Kilolo District in Iringa Region in Southern Highlands of Tanzania. Int. J. Anim. Vet. Adv. 3, 196–201. Martin, E., 1995. Working across the human-other divide. In: Birke, L., Hubbard, R. (Eds.), Working across the human-other divide. Indiana University Press, Bloomington, pp. 261–275. Mason Dentinger, R., 2018. The Parasitological Pursuit: Crossing Species and Disciplinary Boundaries with Calvin W. Schwabe and the Echinococcus Tapeworm, 1956–1975. In: Woods, A., Bresalier, M., Cassidy, A., Mason Dentinger, R. (Eds), Animals and the Shaping of Modern Medicine - One Health and its Histories. Palgrave Macmillan, Basingstoke, pp. 161–191. McCarthy, J.S., Lustigman, S., Yang, G.-J., Barakat, R.M., García, H.H., Sripa, B., . . ., Basáñez, M.- G., 2012. A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Negl. Trop. Dis. 6, e1601. Melki, J., Koffi, E., Boka, M., Touré, A., Soumahoro, M.-K., Jambou, R., 2018. Taenia solium cysticercosis in West Africa: status update. Parasite 25, 49. Meslin, F.X., Briggs, D., 2013. Eliminating canine rabies, the principal source of human infection: What will it take? Antivir. Res. 98, 291-296 Michelet, L., Dauga, C., 2012. Molecular evidence of host influences on the evolution and Literature Review | 91
spread of human tapeworms. Biol. Rev. 87, 731–741. Mkhize, G.C., Ngoepe, E.C., Du Plessis, B.J., Reininghaus, B., Sabeta, C.T., 2010. Re-emergence of dog rabies in Mpumalanga province, South Africa. Vector. Borne Zoonotic Dis. 10, 921–926. Mkupasi, E.M., Sikasunge, C.S., Ngowi, H.A., Johansen, M.V., 2013. Efficacy and Safety of Anthelmintics Tested against Taenia solium Cysticercosis in Pigs. PLoS Negl. Trop. Dis. 7, e2200. Mollentze, N., Weyer, J., Markotter, W., Le, R.K., Nel, L.H., 2013. Dog rabies in southern Africa: regional surveillance and phylogeographical analyses are an important component of control and elimination strategies. Virus Genes. 47, 569–573. Molyneux, D.H., 2004. “Neglected” diseases but unrecognised successes - challenges and oppurtunities for infectious disease control. Lancet. 364, 380–383. Molyneux, D.H., Hallaj, Z., Keusch, G.T., McManus, D.P., Ngowi, H., Cleaveland, S., . . ., Kioy, D., 2011. Zoonoses and marginalised infectious diseases of poverty: where do we stand? Parasit. Vectors. 4, 1-6. Moran, M., Guzman, J., Ropars, A.-L., McDonald, A., Jameson, N., Omune, B., . . ., Wu, L., 2009. Neglected disease research and development: how much are we really spending? PLoS Med. 6, e30. Moreno, L., Lopez-Urbina, M.T., Farias, C., Domingue, G., Donadeu, M., Dungu, B., . . ., González, A.E., 2012. A high oxfendazole dose to control porcine cysticercosis: Pharmacokinetics and tissue residue profiles. Food Chem. Toxicol. 50, 3819–3825. Moro, P., Schantz, P.M., 2006. Cystic echinococcosis in the Americas. Parasitol. Int. 55, S181– S186. Moro, P., Schantz, P.M., 2009. Echinococcosis: a review. Int. J. Infect. Dis. 13, 125-133. Morse, S.S., 1993. Emerging Viruses. Oxford University Press, New York. Morters, M.K., Restif, O., Hampson, K., Cleaveland, S., Wood, J.L.N., Conlan, A.J.K., 2013. Evidence-based control of canine rabies: a critical review of population density reduction. J. Anim. Ecol. 82, 6–14. Mubanga, C., Mwape, K.E., Phiri, I.K., Trevisan, C., Zulu, G., Chabala, C., . . ., Gabriël, S., 2019. Progress on the development of rapid diagnostic tests for foodborne neglected zoonotic helminthiases: A systematic review. Acta Trop. 194, 135–147. Muehlenbein, M.P., 2016. Disease and Human/Animal Interactions. Annu. Rev. Anthropol. 45, 395–416. Mullin, M.H., 1999. Mirrors and Windows: Sociocultural Studies of Human-Animal Relationships. Annu. Rev. Anthropol. 28, 201–224. Mullin, M.H., 2002. Animals and anthropology. Soc. Anim. 10, 387–393. Murrell, K.D., Dorny, P., World Health Organization, International Office of Epizootics, Nations, Food and agriculture Organizations of the United Nations, 2005. WHO/FAO/OIE guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. OIE (World Organisation for Animal Health).
92 | C h a p t e r 1
Mutsaers, I., 2015. One-health approach as counter-measure against “autoimmune” responses in biosecurity. Soc. Sci. Med. 129, 123–130. Mwape, K.E., Phiri, I.K., Praet, N., Muma, J.B., Zulu, G., van den Bossche, P., . . ., Gabriël, S., 2012. Taenia solium infections in a rural area of Eastern Zambia - A community based study. PLoS Negl. Trop. Dis. 6, 1–9. Mwape, K.E., Phiri, I.K., Praet, N., Speybroeck, N., Muma, J.B., Dorny, P., Gabriël, S., 2013. The Incidence of Human Cysticercosis in a Rural Community of Eastern Zambia. PLoS Negl. Trop. Dis. 7, 1-7. Mwape, K.E., Phiri, I.K., Praet, N., Dorny, P., Muma, J.B., Zulu, G., . . ., Gabriël, S., 2015. Study and ranking of determinants of Taenia solium infections by classification tree models. Am. J. Trop. Med. Hyg. 92, 56–63. Mwape, K.E., 2018. Effectiveness of an education-based control option for human cysticercosis. Lancet Glob. Health 6, e359–e360. Nading, A.M., 2013. Humans, Animals, and Health: From Ecology to Entanglement. Environ. Soc. 4, 60-78. Nakao, M., Okamoto, M., Sako, Y., Yamasaki, H., Nakaya, K., Ito, A., 2002. A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology. 124, 657–662. Narrod, C., Zinsstag, J., Tiongco, M., 2012. A One Health Framework for Estimating the Economic Costs of Zoonotic Diseases on Society. Ecohealth. 9, 150–162. Nash, T.E., Garcia, H.H., 2011. Diagnosis and treatment of neurocysticercosis. Nat. Rev. Neurol. 7, 584–594. Ndimubanzi, P.C., Carabin, H., Budke, C.M., Nguyen, H., Qian, Y.J., Rainwater, E., . . ., Stoner, J.A., 2010. A systematic review of the frequency of neurocyticercosis with a focus on people with epilepsy. PLoS Negl. Trop. Dis. 4, e870. Neevel, A.M.G., Hemrika, T., Claassen, E., van de Burgwal, L.H.M., 2018. A research agenda to reinforce rabies control: A qualitative and quantitative prioritization. PLoS Negl. Trop. Dis. 12, e0006387. Nel, L.H., Sabeta, C.T., Teichman, B., Jaftha, J.B., Rupprecht, C.E., Bingham, J., 2005. Mongoose rabies in southern Africa: a re-evaluation based on molecular epidemiology. Virus Res. 109, 165–173. Nel, L.H., Rupprecht, C.E., 2007. Emergence of lyssaviruses in the Old World: the case of Africa. Curr. Top. Microbiol. Immunol. 315, 161–193. Ngoepe, C.E., Sabeta, C., Nel, L., 2009. The spread of canine rabies into Free State province of South Africa: A molecular epidemiological characterization. Virus Res. 142, 175–180. Ngowi, H.A., Carabin, H., Kassuku, A.A., Mlozi, M.R.S., Mlangwa, J.E.D., Willingham, A.L., 2008. A health-education intervention trial to reduce porcine cysticercosis in Mbule District, Tanzania. Prev. Vet. Med. 85, 52–67. Ngowi, H., Ozbolt, I., Millogo, A., Dermauw, V., Somé, T., Spicer, P., . . ., Carabin, H., 2017. Development of a health education intervention strategy using an implementation research method to control taeniasis and cysticercosis in Burkina Faso. Infect. Dis. Literature Review | 93
Poverty 6, 1-15. NICD, 2018. National Institute for Communicable Diseases - Annual overview 2017/18. Johannesburg. Noske, B., 1993. The Animal Question in Anthropology: A Commentary. Soc. Anim. 1, 185– 190. Nyamanga, P.A., Suda, C., Aagaard-Hansen, J., 2006. Similarities between Human and Livestock Illnesses among the Luo in Western Kenya. Anthropol. Med. 13, 13–24. Okello, A.L., Bardosh, K., Smith, J., Welburn, S.C., 2014. One Health: Past Successes and Future Challenges in Three African Contexts. PLoS Negl. Trop. Dis. 8, 1–7. Okello, A.L., Beange, I., Shaw, A., Moriyón, I., Gabriël, S., Bardosh, K., . . ., Welburn, S.C., 2015. Raising the Political Profile of the Neglected Zoonotic Diseases: Three Complementary European Commission-Funded Projects to Streamline Research, Build Capacity and Advocate for Control. PLoS Negl. Trop. Dis. 9, 1–10. Okello, W.O., Okello, A.L., Inthavong, P., Tiemann, T., Phengsivalouk, A., Devleesschauwer, B., . . ., Allen, J., 2018. Improved methods to capture the total societal benefits of zoonotic disease control: Demonstrating the cost-effectiveness of an integrated control programme for Taenia solium, soil transmitted helminths and classical swine fever in northern Lao PDR. PLoS Negl. Trop. Dis. 12, e0006782. Osburn, B., Scott, C., Gibbs, P., 2009. One World – One Medicine – One Health: emerging veterinary challenges and opportunities. Rev. sci. tech. Off. int. Epiz. 28, 481–486. Otero-Abad, B., Torgerson, P.R., 2013. A Systematic Review of the Epidemiology of Echinococcosis in Domestic and Wild Animals. PLoS Negl. Trop. Dis. 7, e2249. Paige, S.B., Malavé, C., Mbabazi, E., Mayer, J., Goldberg, T.L., 2015. Uncovering zoonoses awareness in an emerging disease “hotspot.” Soc. Sci. Med. 129, 78–86. Pawlowski, Z., Allan, J., Sarti, E., 2005. Control of Taenia solium taeniasis/cysticercosis: From research towards implementation. Int. J. Parasitol. 35, 1221–1232. Parker, M., Allen, T., Hastings, J., 2008. Resisting control of neglected tropical diseases: dilemmas in the mass treatment of schistosomiasis and soil-transmitted helminths in north-west Uganda. J. Biosoc. Sci. 40, 161–181. Pearce-Duvet, J.M.C., 2006. The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease. Biol. Rev. 81, 369-382. Porter, J.D.H., 2006. Epidemiological Reflexions of the Contributions of Anthropology to Public Health Policy and Practice. J. Biosoc. Sci. 38, 133–144. Praet, N., Speybroeck, N., Manzanedo, R., Berkvens, D., Nforninwe, D.N., Zoli, A., . . ., Geerts, S., 2009. The disease burden of Taenia solium cysticercosis in Cameroon. PLoS Negl. Trop. Dis. 3, 1–8. Prasad, K.N., Chawla, S., Jain, D., Pandey, C.M., Pal, L., Pradhan, S., Gupta, R.K., 2002. Human and porcine Taenia solium infection in rural north India. Trans. R. Soc. Trop. Med. Hyg. 96, 515–516. Rabinowitz, P.M., Kock, R., Kachani, M., Kunkel, R., Thomas, J., Gilbert, J., . . ., Rubin, C., the Stone
94 | C h a p t e r 1
Mountain One Health Proof of Concept Working Group, 2013. Toward proof of concept of a one health approach to disease prediction and control. Emerg. Infect. Dis. 19. Rabozzi, G., Bonizzi, L., Crespi, E., Somaruga, C., Sokooti, M., Tabibi, R., . . ., Colosio, C., 2012. Emerging zoonoses: the “one health approach”. Saf. Health Work. 3, 77–83. Rock, M., 2005. Figuring Out Type 2 Diabetes through Genetic Research: Reckoning Kinship and the Origins of Sickness. Anthropol. Med. 12, 115–127. Rock, M., Mykhalovskiy, E., Schlich, T., 2007. People, other animals and health knowledges: Towards a research agenda. Soc. Sci. Med. 64, 1970–1976. Rock, M., Buntain, B.J., Hatfield, J.M., Hallgrímsson, B., 2009. Animal-human connections, “one health,” and the syndemic approach to prevention. Soc. Sci. Med. 68, 991–995. Rock, M.J., Degeling, C., 2015. Public health ethics and more-than-human solidarity. Soc. Sci. Med. 129, 61–67. Romig, T., Jenkins, D., Giraudoux, P., Massolo, A., Craig, P.S., Wassermann, M., . . ., de la Rue, M., 2017. Ecology and Life Cycle Patterns of Echinococcus Species. Adv. Parasitol. 95, 213– 314. Rü egg, S.R., Hä sler, B., Zinsstag, J., 2018. Integrated approaches to health : a handbook for the evaluation of One Health. Wageningen Academic Publishers, 256 pp. Ruhlmann, S., 2018. Dealing with highly contagious animal diseases under neoliberal governmentality in Mongolia. Med. Anthropol. Theory. 5, 99. Rupprecht, C.E., 1996. Rhabdoviruses: Rabies Virus, Medical Microbiology. University of Texas Medical Branch, Galveston. Rupprecht, C.E., Hanlon, C.A., Slate, D., 2006. Control and prevention of rabies in animals: paradigm shifts. Dev. Biol. 125, 103–111. Rupprecht, C.E., Barrett, J., Briggs, D., Cliquet, F., Fooks, A.R., Lumlertdacha, B., . . ., Wandeler, A.I., 2008. Can rabies be eradicated? Dev. Biol. 131, 95–121. Sabeta, C.T., Weyer, J., Geertsma, P., Mohale, D., Miyen, J., Blumberg, L.H., . . ., Paweska, J.T., 2013. Emergence of rabies in the Gauteng Province, South Africa: 2010-2011. J. S. Afr. Vet. Assoc. 84, E1-5. Sachs, J.D., 2006. The neglected tropical diseases. Sci. Am. 296, 33A. Sadjjadi, S.M., 2006. Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol. Int. 55, Supple, S197–S202. Samorek-Pieróg, M., Karamon, J., Cencek, T., 2018. Identification and Control of Sources of Taenia Solium Infection - the Attempts To Eradicate the Parasite. J. Vet. Res. 62, 27–34. Schantz, P.M., Cruz, M., Sarti, E., Pawlowski, Z., 1993. Potential eradicability of taeniasis and cysticercosis. Bull. Pan Am. Health Organ. 27, 397–403. Schantz, P.M., 2006. Progress in diagnosis, treatment and elimination of echinococcosis and cysticercosis. Parasitol. Int. 55, S7–S13. Schwabe, C.W., 1984. Veterinary medicine and human health (3rd ed). Williams & Wilkins, Baltimore. Literature Review | 95
Scoones, I., 2010. Avian influenza : science, policy and politics. Earthscan, London, 261 pp. Seimenis, A., Morelli, D., Mantovani, A., 2006. Zoonoses in the Mediterranean region. Ann. Ist. Super. Sanità 42, 437–445. Shankar, B.P., 2009. Advances in diagnosis of rabies. Vet. World. 2, 74–77. Shipman, P., 2010. The Animal Connection and Human Evolution. Current Anthropology. 51, 519-532. Sikasunge, C.S., Phiri, I.K., Phiri, A.M., Dorny, P., Siziya, S., Willingham, A.L., 2007. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet. Parasitol. 143, 59-66. Singer, M., 2014. Zoonotic Ecosyndemics and Multispecies Ethnography. Anthropol. Q. 87, 1279–1309. Singh, S., Mishra, V.N., Rai, A., Singh, R., Chaurasia, R.N., 2018. Myths and Superstition about Epilepsy: A Study from North India. J. Neurosci. Rural Pract. 9, 359–362. Slingenbergh, J.I., Gilbert, M., de Balogh, K.I., Wint, W., 2004. Ecological sources of zoonotic diseases. Rev. Sci. Tech. 23, 467–484. Slovic, P., 1987. Perception of risk. Science (80-. ). 236, 280–285. Slovic, P., Finucane, M.L., Peters, E., MacGregor, D.G., 2007. The affect heuristic. Eur. J. Oper. Res. 177, 1333–1352. Smith, J., Taylor, E.M., Kingsley, P., 2015. One World-One Health and neglected zoonotic disease: Elimination, emergence and emergency in Uganda. Soc. Sci. Med. 129, 12–19. Society for Medical Anthropology, 2015. What is Medical Anthropology? SMA Blog, http://www.medanthro.net/about/about-medical-anthropology/, accessed May 11, 2019. Srinivasan, A., Burton, E.C., Kuehnert, M.J., Rupprecht, C., Sutker, W.L., Ksiazek, T.G., . . ., Zaki, S.R., 2005. Transmission of Rabies Virus from an Organ Donor to Four Transplant Recipients. N. Engl. J. Med. 352, 1103–1111. Swai, E.S., Schoonman, L., Daborn, C.J., 2010. Knowledge and attitude towards zoonoses among animal health workers and livestock keepers in Arusha and Tanga, Tanzania. Tanzan. J. Health Res. 12, 280–286. Swanepoel, R., Barnard, B.J.H., Meredith, C.D., Bishop, G.C., Bruckner, G.K., Foggin, C.M., Hubschle, O.J.B., 1993. Rabies in southern Africa. 346, 325–346. Swanepoel, R., 2004, Rabies. In: Coetzer, J.A.W., Tustin R.C. (Eds.), Infectious diseases of livestock (2nd ed), Vol. 2. Oxford University Press, Cape Town, pp. 1123–1182. Taylor, L.H., Latham, S.M., Woolhouse, M.E., 2001. Risk factors for human disease emergence. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 983–989. Taylor, L.H., Nel, L.H., 2015. Global epidemiology of canine rabies: past, present, and future prospects. Vet. Med. 6, 361–371. Taylor, L.H., Hampson, K., Fahrion, A., Abela-Ridder, B., Nel, L.H., 2017. Difficulties in estimating the human burden of canine rabies. Acta Trop. 165, 133–140.
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The Random House College Dictionary, 1984. Random House, New York. Thomas, L.F., de Glanville, W.A., Cook, E.A.J., Bronsvoort, B.M.D.C., Handel, I., Wamae, C.N., . . ., Fèvre, E.M., 2017. Modelling the risk of Taenia solium exposure from pork produced in western Kenya. PLoS Negl. Trop. Dis. 11, e0005371. Thomas, L.F., 2015. Landscape analysis : Control of Taenia solium. World Health Organization. Torgerson, P.R., Budke, C.M., 2003. Echinococcosis – an international public health challenge. Res. Vet. Sci. 74, 191–202. Torgerson, P.R., Heath, D.D., 2003. Transmission dynamics and control options for Echinococcus granulosus. Parasitology 127, S143–S158. Torgerson, P.R., Ziadinov, I., Aknazarov, D., Nurgaziev, R., Deplazes, P., 2009. Modelling the age variation of larval protoscoleces of Echinococcus granulosus in sheep. Int. J. Parasitol. 39, 1031–1035. Torgerson, P.R., Macpherson, C.N.L., 2011. The socioeconomic burden of parasitic zoonoses: Global trends. Vet. Parasitol. 182, 79–95. Torgerson, P.R., 2013. One world health: Socioeconomic burden and parasitic disease control priorities. Vet. Parasitol. 195, 223–232. Torgerson, P.R., Devleesschauwer, B., Praet, N., Speybroeck, N., Willingham, A.L., Kasuga, F., . . ., de Silva, N., 2015. World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis. PLOS Med. 12, e1001920. Torgerson, P.R., Rüegg, S., Devleesschauwer, B., Abela-Ridder, B., Havelaar, A.H., Shaw, A.P.M., . . ., Speybroeck, N., 2018. zDALY: An adjusted indicator to estimate the burden of zoonotic diseases. One Health. 5, 40–45. Trevisan, C., Devleesschauwer, B., Schmidt, V., Winkler, A.S., Harrison, W., Johansen, M.V., 2017. The societal cost of Taenia solium cysticercosis in Tanzania. Acta Trop. 165, 141– 154. Trevisan, C., Devleesschauwer, B., Praet, N., Pondja, A., Assane, Y.A., Dorny, P., . . ., Johansen, M.V., 2018. Assessment of the societal cost of Taenia solium in Angónia district, Mozambique. BMC Infect. Dis. 18, 127. UN DESA, 2017. The Sustainable Development Goals Report 2017. United Nations, New York. UN DESA, 2018. The Sustainable Development Goals Report 2018. United Nations, New York. Valeix, S.F., 2018. One Health Integration: A Proposed Framework for a Study on Veterinarians and Zoonotic Disease Management in Ghana. Front. Vet. Sci. 5, 1-7. von Teichman, B.F., Thomson, G.R., Meredith, C.D., Nel, L.H., 1995. Molecular epidemiology of rabies virus in South Africa: evidence for two distinct virus groups. J. Gen. Virol. 76, 73– 82. Wallace, R.M., Undurraga, E.A., Blanton, J.D., Cleaton, J., Franka, R., 2017. Elimination of Dog- Mediated Human Rabies Deaths by 2030: Needs Assessment and Alternatives for Progress Based on Dog Vaccination. Front. Vet. Sci. 4, 1-4. Wandeler, a I., Matter, H.C., Kappeler, a, Budde, a, 1993. The ecology of dogs and canine rabies: Literature Review | 97
a selective review. Rev. Sci. Tech. 12, 51–71. Waltner-Toews, D., 2017. Zoonoses, One Health and complexity: wicked problems and constructive conflict. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-9. Wardrop, N.A., Thomas, L.F., Atkinson, P.M., de Glanville, W.A., Cook, E.A.J., Wamae, C.N., . . ., Fèvre, E.M., 2015. The Influence of Socio-economic, Behavioural and Environmental Factors on Taenia spp. Transmission in Western Kenya: Evidence from a Cross-Sectional Survey in Humans and Pigs. PLoS Negl. Trop. Dis. 9, 1–16. Warrell, D., 2010. Rabies, the Emerging Challenge. Int. J. Infect. Dis. 14, e9–e9. Warrell, M.J., Warrell, D.A., 2015. Rabies: the clinical features, management and prevention of the classic zoonosis. Clin. Med. 15, 78–81. Weka, R.P., Ikeh, E., Kamani, J., 2013. Seroprevalence of antibodies (IgG) to Taenia solium among pig rearers and associated risk factors in Jos metropolis, Nigeria. J. Infect. Dev. Ctries. 7, 67–72. Wertheim, H.F.L., Nghia, H.D.T., Taylor, W., Schultsz, C., 2009. Streptococcus suis: An Emerging Human Pathogen. Clin. Infect. Dis. 48, 617–625. Weyer, J., Szmyd-Potapczuk, A. V., Blumberg, L.H., Leman, P.A., Markotter, W., Swanepoel, R., . . ., Nel, L.H., 2011. Epidemiology of human rabies in South Africa, 1983-2007. Virus Res. 155, 283–290. White, A.C., Coyle, C.M., Rajshekhar, V., Singh, G., Hauser, W.A., Mohanty, A., . . ., Nash, T.E., 2018. Diagnosis and Treatment of Neurocysticercosis: 2017 Clinical Practice Guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Clin. Infect. Dis. 66, e49–e75. Whitmee, S., Haines, A., Beyrer, C., Boltz, F., Capon, A.G., de Souza Dias, B.F., . . ., Yach, D., 2015. Safeguarding human health in the Anthropocene epoch: report of The Rockefeller Foundation–Lancet Commission on planetary health. Lancet. 386, 1973–2028. WHO, 2005. WHO Expert Consultation on rabies. World Health Organ. Tech. Rep. Ser. 931, 1– 88. WHO, 2006. The Control of Neglected Zoonotic Diseases: A route to poverty alleviation, WHO Conference Report. WHO, 2009. Integrated control of neglected zoonotic diseases in Africa; Applying the “One Health” Concept. Rep. a Jt. WHO/EU/ILRI/DBL/FAO/OIE/AU Meet. 84, 147–148. WHO, 2010. Working to overcome the global impact of neglected tropical diseases - First WHO report on neglected tropical diseases. WHO, 2011a. The Control of Neglected Zoonotic Diseases: Community-Based Interventions for Prevention and Control, WHO Conference Report. WHO, 2011b. WHO | Report of the WHO Informal Working Group on cystic and alveolar echinococcosis surveillance, prevention and control. World Health Organization, Geneva. WHO, 2013. WHO Expert Consultation on Rabies. Second report. World Health Organization. Tech. Rep. Ser. 982, 1–139.
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WHO, 2015a. The Control of Neglected Zoonotic Diseases: From advocacy to action, WHO Conference Report. WHO, 2015b. Taenia solium Taeniasis / Cysticercosis Diagnostic Tools 17–18. World Health Organization. WHO, 2015c. Assembling a framework for intensified control of taeniasis and neurocysticercosis caused by Taenia solium - Report of an informal consultation. World Health Organization. WHO, 2015d. Melinda Gates Foundation fund WHO-coordinated project to control and eventually eliminate rabies in low-income countries. Accessed May 2019. https://www.who.int/rabies/bmgf_who_project/en/. WHO, Secretariat of the Convention on Biological Diversity, 2015. WHO | Connecting Global Priorities: Biodiversity and Human Health: A State of Knowledge Review. WHO, CBD, Geneva. WHO, 2017. WHO | Meeting of the WHO Informal Working Group on Echinococcosis (WHO- IWGE). World Health Organization. WHO, 2018. WHO Expert Consultation on rabies. Third report., World Health Organization Tech. Rep. Ser. 1012, 1-183. WHO-FAO-OIE, 2018. WHO | Zero by 30: the global strategic plan to end human deaths from dog-mediated rabies by 2030. World Health Organization. Wilcox, B.A., Colwell, R.R., 2005. Emerging and Reemerging Infectious Diseases: Biocomplexity as an Interdisciplinary Paradigm. Ecohealth 2, 244–257. Wilcox, B.A., Aguirre, A.A., De Paula, N., Siriaroonrat, B., Echaubard, P., 2019. Operationalizing One Heath employing social-ecological systems theory: lessons from the Greater Mekong Sub-region. Front. Public Health. 7, 1-12. Wilkerson, J.A., 1995. Rabies: Epidemiology, diagnosis, prevention, and prospects for worldwide control. Wilderness Environ. Med. 6, 48–96. Willingham, A.L., Engels, D., 2006. Control of Taenia solium cysticercosis/taeniosis. Adv. Parasitol. 61, 509–566. Winskill, P., Harrison, W.E., French, M.D., Dixon, M.A., Abela-Ridder, B., Basáñez, M.-G., 2017. Assessing the impact of intervention strategies against Taenia solium cysticercosis using the EPICYST transmission model. Parasit. Vectors 10, 1-14. Woldehanna, S., Zimicki, S., 2015. An expanded One Health model: Integrating social science and One Health to inform study of the human-animal interface. Soc. Sci. Med. 129, 87– 95. Wolf, M., 2015. Is there really such a thing as “one health”? Thinking about a more than human world from the perspective of cultural anthropology. Soc. Sci. Med. 129, 5–11. Woods, A., Bresalier, M., Cassidy, A., Mason Dentinger, R., 2018. Animals and the Shaping of Modern Medicine - One Health and its Histories. Springer International Publishing, Cham. Zammarchi, L., Bonati, M., Strohmeyer, M., Albonico, M., Requena-Méndez, A., Bisoffi, Z., . . ., Literature Review | 99
Bartoloni, A., 2017. Screening, diagnosis and management of human cysticercosis and Taenia solium taeniasis: technical recommendations by the COHEMI project study group. Trop. Med. Int. Health 22, 881–894. Zinsstag, J., Ould Taleb, M., Craig, P.S., 2006. Editorial: Health of nomadic pastoralists: new approaches towards equity effectiveness. Trop. Med. Int. Health 11, 565–568. Zinsstag, J., Schelling, E., Roth, F., Bonfoh, B., De Savigny, D., Tanner, M., 2007. Human benefits of animal interventions for zoonosis control. Emerg. Infect. Dis. 13, 527–531. Zinsstag, J., Dürr, S., Penny, M.A., Mindekem, R., Roth, F., Menendez Gonzalez, S., . . ., Hattendorf, J., 2009. Transmission dynamics and economics of rabies control in dogs and humans in an African city. Proc. Natl. Acad. Sci. U. S. A. 106, 14996–5001. Zinsstag, J., Schelling, E., Waltner-Toews, D., Tanner, M., 2011. From “one medicine” to “one health” and systemic approaches to health and well-being. Prev. Vet. Med. 101, 148–156. Zinsstag, J., Meisser, A., Schelling, E., Bonfoh, B., Tanner, M., 2012. From “two medicines” to “One Health” and beyond. Onderstepoort J. Vet. Res. 79, 1-5. Zinsstag, J., 2013. Towards a science of rabies elimination. Infect. Dis. Poverty 2, 1-3.
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Neglected Zoonotic Diseases (NZDs) present unique control challenges as one needs to take into account the animal-human-ecosystem interface where they impose a dual burden on communities, affecting livestock and human health (Swanepoel et al., 2010). Several of the more cost-effective NZD control strategies involve reducing disease prevalence in the animal reservoir (Zinsstag et al., 2007), and such control approaches often profoundly impact on the prevalent culture, livelihood and socio- behavioural patterns of the affected communities (Perry et al., 2002). However, NZD control interventions are often implemented neglecting the background of the cultures, norms and belief systems that shape the eco-social niche for the transmission cycles. Little is known about African farmers' knowledge and perception of zoonoses and opportunities for disease management. By adding the social, cultural, political, economic and ecological knowledge and practices of farmers and pastoralists to the research interest in transmission dynamics, the complex relationships between different aspects of the social and biological world would be revealed, contributioning substantially to sustained disease control. To contribute to breaking the vicious cycle between poverty and poor health among livestock owners in endemic and epidemic areas in developing countries, the underlying hypothesis of this work is that an integrated control “toolbox” for NZDs should include an inter- sectoral and transdisciplinary approach comprising a socio-anthropological perspective. Consideration of this social dimension in policy formulation and implementation may lead to NZD control strategies that are more adapted to the local reality and therefore more effective and sustainable (Spiegel et al., 2010).
The state of the art (Chapter 1) raised the following research question:
How can social sciences contribute to the ‘One Health’ approach for NZDs integrated control by understanding and assessing how livestock owners and communities perceive zoonotic diseases and how the socio-cultural context affects/influences the transmission dynamics of NZDs in specific endemic rural environments in developing countries? R a t i o n a l e & O b j e c t i v e s | 103
This doctoral research project aims to explore the contribution of the socio- anthropologist discipline to the One Health perspective regarding the control of endemic zoonotic diseases. This was done through three case-studies targeting different NZDs (echinococcosis, T. solium taeniasis-cysticercosis and rabies), each of them in one of their rural endemic hotspot settings. This thesis assesses cultural, cognitive and social drivers explaining people’s knowledge, perceptions and behaviour with regard to animal husbandry, zoonoses and their control in their specific ecosystem.
The thesis specific objectives are:
1. To identify the socio-cultural determinants of transmission of specific NZDs on the level of the human host, animal host and local environment and their interplay, including knowledge and perception of the zoonoses.
2. To identify barriers to NZD control options and added value of inter-sectoral collaborations between health, veterinary and other relevant sectors at the local level within their specific socio-ecosystems.
3. To contribute to the elaboration of recommendations for a more adapted and sustainable integrated control of NZDs.
4. To share and disseminate these anthropological research findings in cross- disciplinary dialogues and constructive collaborative efforts with the animal and human health sectors engaged in the control of NZDs.
Perry, B.D., Randolph, T.F., McDermott, J., Sones, K.R., Thornton, P.K., 2002. Investing in Animal Health research to alleviate poverty. Tate, London. Spiegel, J.M., Dharamsi, S., Wasan, K.M., Yassi, A., Singer, B., Hotez, P.J., . . ., Bundy, D.A.P., 2010. Which new approaches to tackling neglected tropical diseases show promise? PLoS Med. 7, 5–9. Swanepoel, F., Stroebel, A., Moyo, S., 2010. The role of livestock in developing communities: Enhancing multifunctionality. University of the Free State and CTA, Cape town, South Africa. Zinsstag, J., Schelling, E., Roth, F., Bonfoh, B., De Savigny, D., Tanner, M., 2007. Human benefits of animal interventions for zoonosis control. Emerg. Infect. Dis. 13, 527–531.
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Albert Einstein
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2.1.1 Qualitative research in Health
Providing a precise definition of qualitative research (QLR) is not easy as there is no single, accepted way of doing qualitative research and it also offers a rich and varied set of strategies and methods. A number of writers have attempted to capture the essence of qualitative research by offering working definitions or by identifying a set of key characteristics. In the Handbook of Qualitative Research (2000), Denzin and Lincoln propose the following definition:
Qualitative research is a situated activity that locates the observer in the world. It consists of a set of interpretive, material practices that makes the world visible. These practices (...) turn the world into a series of representations including fieldnotes, interviews, conversations, photographs, recordings and memos to the self. At this level, qualitative research involves an interpretive, naturalistic approach to the world. This means that qualitative researchers study things in their natural settings, attempting to make sense of, or to interpret, phenomena in terms of the meanings people bring to them.
Althought QLR shares investigation features of any scientific research, it belongs to a different paradigm than the one of laboratory experimentation (e.g. experimental, and quasi-experimental approaches in veterinary sciences or in psychology) and its core practice of isolating variables in strictly controlled situations (Henwood, 2014). Sometimes known as real-world inquiry (Robson, 2011), QLR mainly seeks to provide the opportunity to investigate and express the diversity and richness of social life in an explorative and analytical (inductive) manner (Papps, 2005). QLR is also often defined in terms of what it is not, such as “any type of research that produces findings not arrived at by statistical procedures or other means of quantification” (Strauss and Corbin, 1998). If comparisons are often drawn between quantitative and qualitative traditions in research, it is in no way meant to be read as inferring that one research tradition is superior to the other. Rather, this thesis would like to construct bridges and demonstrate the added value of social and biomedical scientists becoming more conversant with each other’s concepts and methods. Both research traditions make important contributions to various bodies of knowledge, through their ability to pose Materials & Methods | 107 and address different types of research questions (Papps, 2005). Quantitative methods are intended to achieve breadth of understanding while qualitative methods are for the most part, intended to achieve depth of understanding (Patton, 2002).
In their open letter to The BMJ editors, Greenhalgh et al. (2016) highlighted the complementarity of both approaches in health such as “the importance of qualitative research in health can be seen from the perspective that not all quantitative studies with statistical validity provide all the information needed for planning health services, policy making and also new leads to further research. In fact, qualitative studies provide leads for doing further research which cannot be quantified by quantitative studies. There are several areas which require confidentiality of information such as behaviours related to risk involving HIV, sexually transmitted diseases, and those involving social stigma such as in leprosy, tuberculosis where qualitative methods provide immense information in addition to quantitative methods of data collection. Both the methods in combination are needed to substantiate any pitfalls in data collection and getting desired information on health (Greenhalgh et al., 2016).
This rich complementarity also applies in epidemiology. While epidemiologists often link “health” to “disease” which, technically, means a biomedically measurable lesion or anatomical or physiological irregularity, anthropologists see “health” as “illness”, a broader construct, consisting of physical, psychological, and social well-being, including role functionality (Ember and Ember, 2004). The latter definition works better cross-culturally because it is based on the notion that the world is socially constructed by its participants and therefore implying that individuals inhabit a social, personal and relational world that is complex, layered, and can be viewed from different perspectives (Papps, 2005). The epidemiological aim of describing and analysing facts related to the distribution and determinants of diseases in human and animal populations in order to develop appropriate control startegies and improve human and animal health systems, would surely benefit from the use of qualitative methods which mainly aim to better understand what meaning those constructions such as “health” (through language (stories, conversations), systems of meaning, memory, rituals and institutions) have for the participants (McCleod, 2001). There is this common acknowledgment that all behaviour occurs within a social, political, and
108 | C h a p t e r 2 historical context, which in turn shapes behaviour, and the ways in which behaviours are understood (Papps, 2005).
2.1.2 Main qualitative methods
Besides biographical methods such as life histories and narratives, and analysis of documents and texts, the three most common qualitative data collection methods are focus group discussions, in-depth interviews, and participant observations. Each method is particularly suited for obtaining a specific type of data. Although different, they all contain the same key aspects of methodology which define a QLR (Table 2.1).
Table 2.1 Landmarks of a more qualitative approach in social sciences (table adapted from www.who.int/tdr/publications/documents/rcs-methods.pdf) More Qualitative approach
Searching to know What ? Why ? and How ?
Production of words
Open process
Description of attitudes, emotions, values, (of a reality said subjective)
Study of individuals as unique and complex case
Small numbers of informants
Flexible, dynamic process
More valid, less reliable*
Describe the reality as seen by individuals
* Validity is one of the fundamental concepts and a crucial issue as it refers to the accuracy and trustworthiness of instruments, data, and findings in research. It means that your findings truly represent the phenomenon you are claiming to measure, that the data collected provide a real picture of the topic studied. The validity of data is therefore tied to the validity of instruments. While validity implies the extent to which the research instrument measures, what it is intended to measure, reliability refers to whether or not you or another researcher get the same answer by using an instrument to measure something more than once (Bernard, 2006). Because the more you try to understand the perception, the reality, the emotions of others (aim of qualitative approaches), the more the reproduction of data is difficult to get (aim of Materials & Methods | 109 quantitative approaches). Data collected in QLR present therefore a high validity and a low reliability because the methods are less structured hence less reproducible.
• Focus group discussions (FGDs) are effective in eliciting data on the cultural norms of a group and in generating broad overviews of issues of concern to the cultural groups or subgroups represented. They are used where the group process will itself illuminate the research issue (Krueger, 1994).
• In-depth interviews (IDIs) are optimal for collecting data on individuals’ personal histories, perspectives, and experiences, particularly when sensitive topics are being explored and to generate hypotheses by exploring a context or a new topic. Out of the different forms that interwiews can take (going from the very informal conversational interview until the very structured closed, fixed response interview), IDI is positioned just after the less structrured interview form (informal discussions) and use an interview guide. A key feature is their ability to provide an undiluted focus on the individual and the opportunity they offer for clarification and detailed understanding (Ritchie and Lewis, 2003).
• Participant observation (PO) in which the researcher joins the constituent study population or its organisational or community setting to record actions, interactions or events that occur (Ritchie and Lewis, 2003) and tries to learn how life is like for an “insider”, while remaining a objective “outsider”. It is appropriate for collecting data on naturally occurring behaviours in their usual contexts. Observations only also offers the opportunity to record and analyse behaviour and interactions as they occur, although not as a member of the study population (Ritchie and Lewis, 2003).
These three methods can be used as a standalone research method or as part of a multi-method design, depending on the needs of the research and the population studied. The principles of ‘mixed methods’ (MM) approach, which is often discussed in the context of combining qualitative and quantitative methods are also applied while using more than one qualitative method to carry out an investigation since each brings a particular kind of insight to a study. These MM principles are the acceptance of pragmatism as leading paradigm, research question as guiding element, mixing data, integrated interpretation, collaboration across disciplines and will to move beyond traditional boundaries of one’s discipline (Punch, 2009). But more generally, what has been called the fundamental principle of MM research is combining the
110 | C h a p t e r 2 methods in a way that achieves complementary strengths and nonoverlapping weaknesses (Johnson and Onwuegbuzie, 2004).
To gain greater rigor and more in-depth understanding of the issues or phenomena in question, another key practice commonly used in QLR is the data triangulation: seeking out multiple sources of data and use multiple data-gathering techniques (S. K. and Given, 2008). Triangulation is a term first used in connection with the validity of 'measurements' derived from structured quantitative data (Campbell and Fiske, 1959) and which has been widely adopted and developed as a concept by qualitative researchers as a means of investigating the 'convergence' of both the data and the conclusions derived from them (Denzin, 1994). It It is also often cited as one of the central ways of 'validating' qualitative research evidence. But because this validating function raised many challenges from an ontological and epistemological perspectives, several authors now argue that the value of triangulation lies in extending understanding through the use of multiple perspectives or different types of 'readings', hence giving a fuller picture of phenomena and not necessarily a more certain one (Richie and Lewis, 2003).
2.1.3 Sampling strategies in QLR
Similar as within a quantitative framework, it is also not necessary in QLR to collect data from everyone in a community in order to get valid findings, even if it would be possible. Only a sample (that is, a subset) of a population is selected for any given study. The study’s research objectives and the characteristics of the study population (such as size and diversity) determine which and how many people to select. The three most common sampling methods used in QLR are purposive sampling, convenience sampling and snowball sampling (S. K. and Given, 2008). The three are specific types of non-probabilistic method. It is important to highlight the fact that probability sampling would be inappropriate for qualitative research. Unlike some statistical research, qualitative research does not set out to estimate the incidence of phenomena in the wider population (Richie and Lewis, 2003).
• Purposive sampling is the identification of a sample group that reflects the phenomenon being investigated. It groups participants according to preselected criteria relevant to a particular research question (e.g. men owning at least one dog Materials & Methods | 111 in an infected rabies area in South Africa). The criteria we choose allow us to focus on people we think would be most likely to have experience, know about, or have insights into the research topic. Subsequently, the community is visited and – using recruitment strategies appropriate to the location, culture, and study population – people who fit these criteria are identified.
• Convenience sampling relies on data collection from population members who are conveniently available to participate in study. There are no inclusion criteria identified prior to the selection of subjects nor any clear sampling strategy besides certain practical criteria, such as easy accessibility, geographical proximity, availability at a given time, or the willingness to participate. Some qualitative researchers (Patton, 2002) made a distinction between “opportunistic” (participants are selected as they arise during the course of fieldwork, melding the sample around the fieldwork context as it unfolds) and “convenience” sampling (participants are selected because they are accessible and therefore relatively easy for the researcher to recruit).
• Snowball sampling – also known as chain referral sampling – is considered a type of purposive sampling. In this method, participants or informants with whom contact has already been made use their social networks to refer the researcher to other people who could potentially participate in or contribute to the study (e.g. as they are members of the same group or share similar interests that are relevant to the project at hand). Snowball sampling is often used to find and recruit “hidden populations”, that is, groups not easily accessible to researchers through other sampling strategies.
These three techniques highlight that non-probability sampling requires the researcher to make the final decision in terms of who does and does not participate in the study. Often, these techniques are used together to recruit individuals to participate in the study.
Sample sizes, which may or may not be fixed prior to data collection, depend on the resources and time available, as well as the study’s objectives. In contrast with quantitative sampling methods, purposive, convenient and snowball methods place primary emphasis on saturation (i.e., obtaining a comprehensive understanding by continuing to sample until no new substantive information is acquired) (Miles and Huberman, 1994). The inability to specify the exact number of required participants
112 | C h a p t e r 2 for a qualitative study stems from the limitation posed by theoretical saturation, that is, the point in the research beyond which no new concepts, themes, or discursive constructions emerge from the analysis (Oberle, 2002). Sampling in QLR is therefore most successful when data review and analysis are done in conjunction with data collection. The number of participants is less important than the quality of the sample which has to represent possible diversity (maximum variation).
How this PhD was born is an essential question to be addressed at this stage as this work is definitively not a pure thesis in Anthropology, neither a pure thesis in Veterinary Sciences, but rather a thesis including a compilation of socio- anthropological case-studies in veterinary and medical sciences. To clarify such an applied posture taken by an anthropologist, we thought it was indispensable to explain within which context the initial scientific interdisciplinary question was raised and how it was translated into a PhD objective. The advantages and disadvantages of this approach on research quality and dialogue among medical and social rationales regarding animal and human health, will be further discussed in Chapter 7. We hope these clarifications will inform future interdisciplinary work and address the possible concerns that may arise for a mutual understanding.
Indeed, no basic social sciences questions were at the origin of this PhD. While the thesis introduction is describing the NZDs issues in a more holistic perspective of health, the case-studies used to illustrate the added value of anthropology for their integrated control were conceptually framed following a disease-control driven research objective instead of a social-science driven one. Indeed, at the origin of these case-studies, there was a need expressed by veterinarians and medical epidemiologists to understand and concretely address the non-efficiency of certain implemented control measures regarding specific NZDs in one of their specific endemic hotspots. Corresponding with the period of the emergence of the OH concept at the global health agenda, this need was translated in a call for an investigation from another more appropriate discipline. The one chosen was anthropology which, at that time (in 2009), was already quite an avant-gardist step forward for the movement itself. In contrast with the EcoHealth concept, which came later and was designed by Materials & Methods | 113 disease ecologists working in the field of biodiversity conservation and was defined as an ecosystem approach to health, tending to focus on environmental and socioeconomic issues, the OH paradigm was rather dealing with biomedical questions, with an emphasis on zoonoses, and remaining historically more health science-driven (Roger et al., 2016). In such a context and with the preconceived idea that one can have about another discipline’s role and epistemology, social sciences came here on top of a biomedical rationale with a disease specific focus to explore and document social causes of these diseases.
While it would have been the reverse process within a social research framework (deconstruct the problem and then see how health is influenced by all the social and cultural structures), the construction of such objective granted in a disease-control framework has several consequences. The focus of the research was on the beliefs and practices that structure the behaviour of humans among each other and vis-à-vis animals. Yet, these beliefs and practices are rooted in the institutions that organize the gendered social organisation of reproduction (kinship) and production (agriculture) for instance, but the characteristics of these institutions could not be highlighted because the criteria guiding the selection of these three case-studies were also pathogen and disease-driven. Each case-study context was analysed mainly by an epidemiological approach, which made it difficult to deconstruct the problem otherwise than a sole medical problem or to identify the consequences of societal arrangements. This explains why our research questions and the obtained results are very descriptive and, as such, more or less detached from broader discussions in the social sciences regarding the main features of social organisation and health such as, the political-economy, kinship structures and demography, social class structure and belief systems of horticultures, pastoralist societies, or advanced agricultures. The studies could not go further in deconstructing the representations from medical entities and provide more elements about their divergence with social local rationales in terms of symbolism, etiology and, further, communities’ issues and priorities.
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2.3.1 Criteria guiding the selection of the three case-studies
Although we engaged in multi-sited ethnography, apart from being focused on NZDs and sharing a common method of inquiry, no systematic logic underlies the choice of the cases, which were selected opportunistically from institutional partnerships and long-lasting research collaborations in these endemic areas. Therefore, no comparative research was purposively applied between them as careful selection of societies is a prerequisite to study the common and case-specific social causes of health and illness, as well as a good strategy to disentangle global from specific (social) causes (see Bartlett and Vavrus (2017) for the comparative case study approach).
The objective was rather to exemplify that in whatever context (social, cultural, political, economical, local-global, urban-rural,…), at whatever level (macro-meso- micro) and for whatever (zoonotic) disease, adding an anthropological approach is beneficial to improve the understanding, the development and the implementation of more adapted integrated and sustainable control measures.
2.3.2 Methodological approach chosen
For our three case-studies, we attempted to follow the same qualitative approach for collecting data both to generate the same quality of data and to demonstrate the variety of findings that can be obtained, all very context specific.
According to the goals of our research (better understand how people perceive the three specific Neglected Zoonotic Diseases (NZDs) studied, the related risk, and how such perceptions modify and control behaviours), the characteristics of the study participants (small holder livestock owners from rural African settings), the audience for the research (veterinarians and medical doctors involved in negected zoonotic disease control), the funders of the research (the Belgian Directorate General for Development Cooperation and Humanitarian Aid), and the academic position and multidisciplinary environment of the researchers themselves, we designed the three studies around the FGD method. However, for triangulation purpose, we also combined approaches (Table 2.2) that generate data through the interventions of the Materials & Methods | 115 research (FGDs and IDIs including informal discussions) and one that focusses on spontaneously occurring events (PO). With these qualitative methods, we ensured for each case study the identification of issues that concern people, instead of dealing with problems that we assumed were present (Silverman, 2000).
Although entailing many biases (see 2.3.4.7. Ethical considerations), FGD were selected as the main method because it has been an often used method in health research and often perceived by the biomedical disciplines as the most effective means of going directly to the target audience to find out what is on their minds and obtaining open feedback. The fact that the group process helps people to identify and clarify their views is considered to be an important advantage compared with IDIs (Kitzinger, 1995). Because the group functions as a promoter of synergy and spontaneity by encouraging the participants to comment, explain, disagree, and share their views, experiences and opinions are voiced that might not surface during individual interviews (Tausch and Menold, 2016).
In our three situations, this choice was further supported by the fact that we did not want to seek quantitative information nor consensus among our research participants but rather a wider range of different ideas and perceptions existing among our target studied groups. The information searched for was not thought sensitive (topics not related to the private sphere of individuals), and as such possible to be discussed in a group. Also because of the time and funding limitation (that is often occurring when qualitative study is included as an ad hoc component of an epidemiological-quantitative research project), the FGD method is preferred as it is known to produce very valuable and in-depth information in a relatively short period of time and at a low cost. However, the major disadvantage is that FGDs causes greater logistical problems than IDIs for instance and might only lead to socially accepted answers and statements. Unexpected conflicts, power struggles, and other group dynamics may inhibit discussion. Also, there is less control by the moderator and data are more difficult to analyse.
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Table 2.2 Materials and methods summary per case study Case- Echinococcosis Taeniasis/ Rabies studies in Morocco cysticercosis in South Africa in Zambia Study design Location High Atlas, South of Kakwiya catchement in Mnisi Community, a Marrakech (rural area) Petauke district in the site located in Eastern province of Zambia Mpumalanga (rural area) Province in north- east South Africa (rural area) Period of data From October to From July to August 2010 From October to collection November 2009 November 2011 Focus Group In 10 villages: In 7 villages: In 3 villages: Discussions 8 FGDs with men 7 FGDs with men 6 FGDs with men (FGDs) (livestock owners) 7 FGDs with women 6 FGDs with women 2 FGDs with butchers 7 FGDs with children (10- 5 FGDs with children 8 FGDs with women 18 yrs) (10-18 yrs) (wives) 2 FGDs with students Each of the three (girls) categories of groups were stratified by dog ownership status Individual in- 1 Medical officer (a male depth interviews nurse) 1 Veterinary assistant (woman) Participant Homes and farms of Kakwiya Rural Health Village life, interface Observations sheep owners, villages, Centre (RHC), Boma, with wildlife (Park), Douar authorities, market, villages the veterinary clinic, slaughterhouses, etc. etc. Informal Villagers, Caïds (chief of Villagers, health workers Villagers, Discussions the rural municipality environmental appointed by the state), managers, veterinary drivers students, etc.
2.3.3 Focus Group Discussions method
FGDs have been used by researchers in the social and behavioural sciences for more than 80 years. In particular, this methodology has been used in fields as disparate as evaluation research, education, sociology, marketing, public health, and politics (Morgan, 1996).
FGDs are open group discussions involving people (specifically selected) with similar backgrounds and experiences, discussing a specific topic of interest with the researcher(s) in a permissive, non-threatening environment. The group of participants is guided by a moderator, who introduces topics for discussion and helps the group to engage in the discussion (Krueger & Casey, 2000). A key feature of focus Materials & Methods | 117 groups is that data emerges through interaction within the group (Ritchie and Lewis, 2003). Participants can therefore “feed off each other” as they respond to each other’s comments and they can support or disagree with one another, creating more energy and thus more data. According to the FGD methodology, groups typically should have between 6 and 10 people. Below 6, it may be difficult to sustain a discussion; above 10, it may be difficult to control it (Krueger & Casey, 2000).
Stewart et al (2007) advance seven uses for FGDs (see box below) and stress that it is not a collection of individual interviews with comments directed solely through the researcher.
Aims of Focus Group Discussions: - For the collection of general background information on a topic of interest - For generating research hypotheses that can be tested through larger quantitative studies - For stimulating new ideas and creative concepts - For identifying potential problems with a new programme or service - For generating impressions of services, programmes or products - For learning how participants talk about the topic of interest which can assist with the design and construction of other research tools such as questionnaires - For assisting with the interpretation of previously obtained quantitative results
2.3.4 Common features of the study design and procedure followed for the three case-studies
In this section, we describe the general common study design and procedure we followed during our case studies. The specificities of the materials and methods for each case study (e.g. study area) are descibed and included in their respective chapter.
2.3.4.1 Purposive sampling
In the study areas, villages were randomly selected and in each village separate FGDs were held with homogeneous groups of approximately 8 participants according to their availability and willingness to participate. Based on the selection criteria, which were decided according to the study's aims and the nature of the population being studied, (stratified) purposive sampling was conducted to compose the different categories of FGDs so that groups (e.g. men and women livestock owners) and
118 | C h a p t e r 2 subgroups (e.g. men owning dogs and men not owning dogs) can be compared (Patton, 2002). Although estimated in advance, the final total number of FGDs for each group was obtained when data saturation was reached. In practice, as it is impossible to know everything about a topic, the saturation of data was estimated based on the pre-analysis done during the fieldwork such as the day by day observations, discussions and moreover from the de-briefings organized with the research team every evening after the collection of FGDs or IDIs. More practical and organisational issues were also factors influencing the final number of FGDs conducted such as the availability of research partners and participants, length of stay in the field and funding resources.
2.3.4.2 Local language
Because in each case study the main researcher was not fluent in the local language, and because the research was a collaborative work aiming at building capacities in qualitative research among our partner institutions, the moderation of the discussions was always conducted by a local facilitator identified and trained for this task. To not hamper the fluidity and dynamic of the discussions, the one moderating the discussion was always assisted with a reporter/translator who, as discrete as possible, was helping the main researcher to follow the discussions.
2.3.4.3 FGDs topic guide
The FGDs followed a general topics guide, designed by the principal investigator together with the research team and pre-tested during the facilitator training period. For that part of the study, the research team (most generally the local institutional partners) helped with the elaboration of the questions (to be adapted to the context and the disease), the order of the topics to be discussed, the translation of the topic guides in local language and the organisation of the pre-testing sessions. The topics addressed different aspects related to the specific objectives. They were put in a specific order to start from more general topics (e.g. dog management practices) to lead to more specifc topics on awareness of the disease and its impact. From the topics guide we formulated questions with the local facilitators to make it easier for them to animate the discussion; however, it was made clear that there was always enough room for the facilitator to change wording and phrasing whenever they felt this was Materials & Methods | 119 necessary (depending on the discussion). To remain interactive and ensure control of the process, a feed back session was held with the facilitators after every day of data collection, to discuss the discussions’ contents, the eventual addition or modification of questions/topics.
2.3.4.4 Data collection
Participants were informed of the purpose of the study. It was made very clear that participation in the discussion was voluntary and anonymous to the researchers and that the data would only be used for research purposes. After recruitment of the participants in the FGDs, we invited them to sit in a circle or around a table in a quiet indoor or outdoor place. Copies of informed consent letters were provided to each participant and read aloud for the benefit of those who cannot read. Opportunities to ask questions was provided before asking them to sign the informed consent or verbally consent when they were illiterate, acknowledging their voluntary participation in the study. Everybody was also well-informed on how the discussion would be moderated. Next, the facilitator began the meeting by giving a short introduction about the ground rules of a FGD and highlight the importance of confidentiality of all participants. At this stage, each participant was asked whether they agreed to be filmed or not. Refreshments were provided to all participants during the discussion. The name of the disease discussed was not specifically mentioned because it was essential to start from the participants’ initial perceptions and knowledge. Male and female participants met in separate groups and the discussions were moderated by a facilitator of the same gender while the presence of a second facilitator (acting as reporter and translator for the researcher) and the researcher was as discrete as possible so as not to interfere with the discussion or influence it in any way. The laters were also recording possible non-verbal messages that might indicate how the group was feeling about the topic under discussion. In addition, the presence of two facilitators (generally the second local faciltator and the researcher) at every discussion led to a more uniform approach and reduced the undesirable response effects. However, when the presence of the researcher and/or of the second facilitator seemed to influence the discussions in any way (more silences and less answers , shyness, body languages showing discomfort,…), they stopped attending the meeting.
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To ease the work of transcription, the group discussions were video-recorded when participants agreed, possibly without filming the faces of the people, or tape-recorded when they did not agree to the video. The main reason for recording is to allow transcription and translation afterwards while making sure respondent participation was captured anonymously. This was generally done by the moderators as they were in a better position to translate the discussions that they facilitated. The focus group discussions lasted between 25 and 90 minutes.
2.3.4.5 Data analysis
The analysis started already during the fieldwork when it was needed to make some rapid choises such as changing or adding a question, to deepen the conversation. The transcriptions and the notes taken during the discussions as well as general field notes and pictures taken during the fieldwork were used to answer the research questions. To improve interpretation reliability, the written translated transcripts were reviewed independently by other researchers from each study before accepting them for analysis. The analysis of the non-numerical data was supported by the NVivo® software (QSR International Pty. Ltd., Melbourne, Australia, 2008), which allows to classify and sort data; examine relationships and trends in the data. Following a thematic analysis, the major themes were separately identified through coding by the other researchers involved in the study following an inductive approach. Any differences were discussed until consensus was reached. The meaning was extracted from the data, leading patterns identified and presented within a qualitative framework, which is a combination of deductive and inductive analysis. We followed the so-called “Cut-and-paste Technique” (coding the transcript sections that are relevant to the research question and organise them according to a classification system for major topics and issues) and the approach of “content analysis” (examining the content of the discussion and discovering meaning and its particular implications for the research question). The results are presented using anonymous representative quotes and anecdotes.
2.3.4.6 Non quantification of FGD data
One has to acknowledge that there are several schools when it comes to the analysis of qualitative data. In some cases, the text data generated in focus group discussions Materials & Methods | 121
(i.e. transcripts of the words spoken by participants) can be analyzed in a semi- quantitative way (see Chapter 7 in Stewart et al., 2007). In fact, during the process of data analysis, there is indeed always some “quantification” (counting). This counting helps to identify recurrent emerging themes. It also helps not to bias results by “talkative participants”. However, it would be misleading to present these counts as “results” in a paper because they have no statistical relevance. This is due to the fact that in FGD research the sampling is non-probabilistic.
Several scholars emphasise that presenting the counts or the frequencies of statements foregoes the purpose of the qualitative approach. Grudens-Schuck et al. (2004) wrote “A report of results from focus groups should not present major findings via frequencies or statistics because ‘counting’ leads readers to believe that percentages or frequencies are true for a much wider population (which they are not)” (Grudens- Schuck et al., 2004). Fern (2001) also stated: “Focus groups method isn’t meant to create generalizations of this type and its procedures offer none of the protections that would permit them to do so”.
In our studies and publications, the frequency with which certain statements are made has a negligible importance in this approach. Because our studies were not designed for a quantitative purpose nor to insure representativeness of a wider group of people, we think that quantifying our data would have weakened our results. We looked at what were the different issues and why some seemed to be more important than others (issues raising the main discussion or being the better detailed), not at how many issues there were nor how many people considered each of these issues. Informing the readers about the number of FGDs wherein a specific theme emerged during the discussion would only have a small descriptive value but certainly none in term of inference, representativeness nor interpretative purpose. The readers would still not know if the concept was only mentioned by one participant or several ones in each group, how much passion or force was behind the comments, if individual respondents remained consistent in their views, if the participants cited it as an important concept… All these criteria are included in qualitative data analysis and interpretation after conducting FGDs. However, the qualitative results obtained may certainly lead to the development of a more accurate quantitative research in the future.
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2.3.4.7. Ethical considerations
For each of the case-studies, the protocol elaborated was submitted for review to an ethical committee in Belgium and in the country where the study was planned to be conducted. As these committees were generally more used to deal with quantitative research or randomised control trials, differences in ethic and deontological codes between social sciences and biomedical sciences raised issues and frustrations. Qualitative research methods needed to be explained often extensively, while requirements which did not easily apply to qualitative research needed to be fulfilled. While social sciences are following a constructivism paradigm based on the ontological assumption that an objective reality does not exist since all realities are socially constructed, medical science is following a scientific paradigm implying that a single reality exists about a social phenomenon which can be understood using quantifiable facts obtained by adopting quantitative data collection and analysis methods (Haq, 2015). Patience, flexibility and tenacity are therefore key because in the end, we, researchers and regulators, all start from the same point which is that ethics matter and sharing a view that ethics is about what is right, good and virtuous (Israel and Hay, 2006).
The way in which access is negotiated on the ground, including how researchers need to make studies accessible to participants, the issue of reciprocity, how researchers' own characteristics impact on the relationship with participants, and ethical issues, can be critical to the success of a study (Ritchie and Lewis, 2003). The literature provides few examples of ethical issues in qualitative health research. Even though FGDs have been used in a great variety of health research fields, the method and its particular recent use in health research is rarely reflected. Systematic reviews of factors influencing the results of focus groups as well as advantages, disadvantages, and pitfalls are missing (Tausch and Menold, 2016).
With the help of the local partners to guide us in the implementation of the research in the field, cultural sensitivities that could have been raised by the research topic, appropriate strategies for dealing with them, particular questioning techniques to make the study accessible to the participant, appropriate language to use in approaching them, anticipation of the possible barriers to participation and provision to help to overcome these barriers, local authorisations and hierarchy or Materials & Methods | 123 organisational structures and procedures, were taken into account and respected.
The issues of reciprocity, meaning how the researcher can give something in return for the assistance, time and thought given by research participants (e.g. incentives such as small cash payment, school materials, condiments, a copy of the report or key findings, donations to charity or local community project) was also discussed with the local research team. For example in the Moroccan study, the main appropriate measure was to accept the hospitality offered by the participants (sharing a meal, tea) and secondly, when possible, provide free veterinary consultations and/or educative presentation about cystic echinococcosis. While such measures help to encourage participation, they also go some way to making research more of an exchange, albeit not necessarily an equal one (Ritchie and Lewis, 2003).
Among the other ethical arrangements made, we asked and obtained from all participants their consent to participate to the studies. The key ethical issue in the conduct of all social research is whether those being studied are placed at risk by those doing the studying (Bernard, 2006). Most social science research is therefore equated with confidentiality, privacy and informed consent, to ensure that people who participate in research will be protected from harm. This means providing participants with information about the purpose of the study, the funder, who the research team is, how the data will be used, and what participation will require of them, the subjects likely to be covered how much time is required and so on (Ritchie and Lewis, 2003). It also means to make a reasonable balance between over- informing and under-informing to not deter potential participants, or curtail their spontaneous views by being over-specific about the objectives and subject while making people adequately prepared for what the interview will require of them (Ritchie and Lewis, 2003). Following FGDs methodologies, remaining anonymous about what was been said during the discussions was required from the participants. Yet, this may be difficult to comply with as the topics discussed were not sensitive and because participants were generally from the same villages.
Informed consent also means that participants exercise their rights as autonomous persons to voluntarily accept or refuse to participate in the study. Yet, voluntary participation is an issue that may require particular emphasis where research is conducted by people who also have a professional relationship with sampled
124 | C h a p t e r 2 participants, which may lead to feelings of obligation or gratitude for instance (Holloway and Wheeler, 1996). When minors were involved, consent was sought from parents or tutors. Some were orally obtained as there were situations in which standard procedures for obtaining written informed consent were culturally or contextually inappropriate to the participants. The reasons were to avoid the high illiteracy in the study population, also because written consent was seen as a breach of confidentiality by the participants and finally because the signature required for a written consent was introducing formality in the procedure, affecting trust between respondents and researchers.
However, consent is not absolute and needs to be assessed, and sometimes renegotiated, particularly during data collection and it does not in itself guarantee ethical research. In some research settings, this very act of asking informed consent and the aim of safeguarding participants’ rights and well-being in the research setting may place them at risk of harm in their social context (rather than affording them protection) (Orb et al., 2001).
Finally, it is also important to keep in mind that each step of a FGD research holds potential bias, starting with subjectivity of the researcher, research questions (researchers impose their categories and implicit interpretations), choice and recruitment of participants, formulation of the questions (dichotomy, biased), language barriers (the role and subjectivity of the translator, risk of withholding information, misunderstandings), choices and function of the moderator (expert, not neutral, dynamism of the discussion), selective listening and memory of the researcher, followed by the transcription (recording’s problems, transcriptor’s fatigue) and the translation, and, finally, during the analysis phase (choices of themes, selection of the discussion’s extracts). To avoid these biases, the FGD methodology has set up several good practices guidelines and series of quality controls (see text- box below), but the most important one with all QLR is to be able to identify and reflect on the bias when analysing the data and presenting the findings (Given, 2008).
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Rigourous strategies to avoid bias (modified from M. Van Dormael and P. Lefèvre, course content 2004-2005) - Continuous reflexivity: researcher’s point of view explicit at each step (presupposed, system of values, interests…) - Vigilance in the choice and construction of the tools. Test tools to allow constant adaptation - Well-reasoned and progressive construction of the sample (observed situations, interviewed people...) - Familiarity with the field (period of time minimal) - Systematic recording of observations; notes completed as soon as possible after being collected - Paying attention to atypical observations - Beware about the nature of social relationship (sympathies or not, power relationship...) - Triangulation, maximum variation sampling, contextualisation, critical case examination - Distinct analysis by different researchers to confront data interpretation - Systematic documentation of process and context (extern validity): keeping track of methodological changes which should be transparent and be made traceable. - Restitution of the results (even orally) to the studied group
Above all, the need for qualitative researchers is to be flexible and adaptable in their approach, to have a commitment to understanding the perspective of the participant, to make research studies accessible to different groups, to be non-judgemental, and to treat participants with respect (Ritchie and Lewis, 2003).
2.3.5 Permanent reflexivity
As a researcher, we are part of the social settings and we are the instrument that measures. Our mere presence will always have an effect on the discourse of the actors, the course of events and consequently on the data collected. Therefore, it is essential to recognize that the attention to the events of interest are filtered through our lens, the field will have an impact on us, we will have an impact on the field and certain aspects are limited while others are enhanced by our identity. We need to constantly examine if there is any possible bias in the collected information related to who we are or in the methods used.
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2.3.5.1 About the researcher
In each of the three settings, I tried to adopt a neutral posture when entering in the field to avoid becoming either an advocate or a critic of the events witnessed. What is most important in the field is to adopt a critical attitude towards ourselves and our own pre-conceptions.
About my personal and social identity, there are fixed aspects that directly relate to the data gathering such as my gender. Being a woman can certainly limit but also facilitate my access to information and to places. It all depends on the attitudes adopted, the empathy for people and the respect of these limitations, codes related to the gender or any cultural sensitivities. This is why for the moderation of the FGDs we tried matching interviewer and participants on gender (a male moderator for men groups and a female moderator for women groups).
As there are other aspects fixed and from the social identity to take into account such, age and age group (socially), ethnicity, nationality (other social identities), marital status, … does this imply that the interviewer and interviewee should always be people of the same age, gender, community,…? It is important to think about how the researcher's characteristics might enhance or intrude on data collection and to weigh up the relative risk of cultural collusion versus unhelpful power dynamics. Involving people who are from the participant's cultural group or who have direct experience of the research issues in design decisions or in co-moderating interviews and focus groups may be a more useful approach than matching (Ritchie and Lewis, 2003).
Among the three research teams from the case-study, I was generally the youngest and by not being the one conducting the FGDs as well as not being a medical doctor nor a veterinarian, my position of authority was always mitigated in the field. This more “naïve” position was a great advantage to make people feel free and willing to explain to me, via the moderator, what they know about the topic and the problems faced. But I also made sure to not promise anything that I could not ensure, to avoid creating false hope and disappointments. Even if the local partners and research teams were well known in the studied areas, I always tried to show that I was not totally associated with them as I did not know beforehand what was the community’s perception about them, their project and involvement. Luckily, the rooted Materials & Methods | 127 connections between the research teams and the populations were more a strength than a weakness.
2.3.5.2 About Anthropology
Embedded in qualitative research are the concepts of relationships and power between researchers and participants (Orb et al., 2001). The introduction of power imbalance into the interview setting is unlikely to be conducive to open discussion (Ritchie and Lewis, 2003). Therefore, an important reflexive question to be addressed is about the place and role of anthropology in a neo-colonialism context.
The strong structural and historical drivers behind today’s research, as well as the development and cooperation between the North and the South, cannot be denied and continue maintaining power game relationships at macro-meso and micro levels, and certainly regarding tropical public health. Heggenhougen and Pedersen (1997) suggested to apply Kleinman’s concept of “therapeutic alliance” in tropical public health, to help bridging the gap of cultural and socio-economic differences not only between the healer and the patient, but between public health and the communities from these settings, the “others”. The process of bridging will depend on an understanding of the “other”, the norms, the context and the problems of a particular group of people concerned. And because the profession of anthropologists is to cross borders and to understand people who are different from themselves, anthropologists were seen to be particularly useful in providing insight for the establishment of such alliance (Heggenhougen and Pedersen, 1997).
It is true that anthropology has its roots ethically, practically, analytically and institutionally in its history and in the West (Latour,…). The discipline can criticise that history but it cannot disavow it completely either (Moore and Sanders, 2006). Yet, anthropology is changing because the world is changing, and the “others” are not anymore restricted to the non-western traditional populations, nor the ones leaving in non-western settings, nor being the ones studied only within a local scope. Already since the twentieth-century, the anthropology set itself against the nineteenth- century evolutionism and the idea that all cultures were ranged along line towards progress and civilisation set by western values and understandings (Herskovits, 1972). It is not because our studied local communities were not substantially
128 | C h a p t e r 2 differentiated from each other, certainly because of the opportunistic selection of the cases, that they were all seen as one uniform non-western traditional societies without taking the core differences between them seriously. Anthropological epistemology is ultimately about the way we imagine others as human beings. The challenge for anthropology is that its claim to truth must be based on the changing nature of others’ imaginations, on the way they see the world, their culture, their response to globalisation, unequal power relations, and inequalities, as well as opportunities they perceive for change, for personal and social advancement, for well- being and security (Appadurai, 1990).
Appadurai, A., 1990. Disjuncture and Difference in the Global Cultural Economy. Theory, Cult. Soc. 7, 295–310. Bartlett, L., Vavrus, F., 2017. Comparative Case Studies: An Innovative Approach. Nord. J. Comp. Int. Educ. 1, 5-17. Bernard, H.R., 2006. Research methods in Anthropology (4th ed): Qualitative and Quantitative Approaches. AltaMira Press, Oxford. Campbell, D.T., Fiske, D.W., 1959. Convergent and discriminant validation by the multitrait- multimethod matrix. Psychol. Bull. 56, 81–105. Denzin, N.K., 1994. Postmodernism and deconstructionism. In Dickens, D.R., Fontana, A. (Eds.), Postmodernism and Social Inquiry. University College London Press , London. Denzin, N.K., Lincoln, Y.S. (Eds.), 2000. Handbook of Qualitative Research. Sage Publications, London. Ember, C.R., Ember, M., 2004. Encyclopedia of Medical Anthropology : Health and Illness in the World’s Cultures. Kluwer Academic/Plenum, New York. Fern, E.F., 2018. Advanced Focus Group Research. Sage Publications, London. Given, L., 2008. The SAGE Encyclopedia of Qualitative Research Methods. Sage Publications, Thousand Oaks, CA. Greenhalgh, T., Annandale, E., Ashcroft, R., Barlow, J., Black, N., Bleakley, A., , Ziebland, S., 2016. An open letter to The BMJ editors on qualitative research. BMJ. 352, i563. Grudens-Schuck, N., Allen, B.L., Larson, K., 2004. Methodology Brief: Focus Group Fundamentals. Iowa State University Extension. Haq, M., 2014. A comparative analysis of qualitative and quantitative research methods and a justification for use of mixed methods in social research. Annual PhD Conference, University of Bradford Business School of Management. Heggenhougen, H.K., Pedersen, D., 1997. The relevance of anthropology for tropical public health: a historical perspective. Trop.Med.Int.Health. 2, A5-10. Materials & Methods | 129
Henwood, K., 2014. Qualitative Research. In: Teo, T., (Ed.), Encyclopedia of Critical Psychology. Springer, New York. Herskovits, M., 1972. Cultural Relativism. Random House, New York. Holloway, I., Wheeler, S., 1996. Qualitative Research for Nurses. Blackwell Science, Oxford. Israel, M., Hay, I., 2006. Research ethics for social scientists : Between ethical conduct and regulatory compliance. Sage, London, 193 pp. Krueger, R.A., 1994. Focus groups: A practical guide for applied research (2nd ed). Sage Publications, Thousand Oaks, CA. Krueger, R.A., Casey M.A., 2000. Focus Groups: A Practical Guide for Applied Research (3rd ed). Sage Publications, Thousand Oaks, CA. McLeod, J., 2001. Qualitative research in counselling and psychotherapy. Sage Publications, London. Miles, M.B., Huberman, A.M., 1994. Qualitative data analysis: An expanded sourcebook (2nd ed). Thousand Oaks, CA: Sage Publications. Moore, H., Sanders, T., 2006, Anthropology in theory: issues in epistemology. Blackwell Publishing, Malden, MA. Morgan, D.L., 1998. The Focus Group Guidebook. Sage Publications, Thousand Oaks, CA. Oberle, K.M., 2002. Ethics in qualitative health research. Ann. R. Coll. Physicians Surg. Can. 35, 563–566. Orb, A., Eisenhauer, L., Wynaden, D., 2001. Ethics in Qualitative Research. J. Nurs. Scholarsh. 33, 93–96 Papps, F.A., 2005. Guide to qualitative research. Paper prepared for the Research Ethics Board and Research Grants Council, University of Prince Edward Island. Patton, M.Q., 2002. Qualitative research and evaluation methods (3rd ed). Sage Publications, Thousand Oaks, CA. Punch, K., 2009. Introduction to research methods in education. Sage Publications, London. Ritchie, J., Lewis, J., 2003. Qualitative research practice: A Guide for Social Science Students and Researchers. Sage Publications, Ltd. Robson, C., 2011. Real world research (3rd ed). Wiley, Chichester. Silverman, D., 2000. Doing Qualitative Research. Sage Publications, London. Stewart, D.W., Shamdasani, P.N., Rook, D.W., 2007. Focus groups: Theory and practice (2nd ed). Sage Publications, Thousand Oaks, CA. Strauss, A.L., Corbin, J., 1998. Basics of Qualitative Research: Grounded Theory Procedures and Techniques (2nd ed). Sage Publications, Thousand Oaks, CA. Tausch, A.P., Menold, N., 2016. Methodological Aspects of Focus Groups in Health Research: Results of Qualitative Interviews With Focus Group Moderators. Glob. Qual. Nurs. Res. 3, 1-12.
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Based on the paper:
Cystic echinococcosis (CE), also known as human hydatidosis, is a neglected zoonotic parasitic disease caused by the cestode Echinococcus granulosus. Dogs and wild Canidae are the definitive hosts, while domestic Ungulates act as intermediate hosts. Humans are accidental dead-end hosts. Considerable phenotypic and genetic variability exists within the E. granulosus species. Several strains have been identified with differences in intermediate host spectrum, biological characteristics, and geographical distribution (Moro and Schantz, 2009). Globally, most human cases of CE are caused by the sheep strain E. granulosus sensu stricto (characterised as the genotypes G1, G2 and G3) (Agudelo Higuita et al., 2016). A common misconception is that humans become infected when eating uncooked meat. In reality, CE is transmitted via the faeco-oral route. Intermediate hosts become infected through ingestion of parasite eggs that are passed through the dog’s faeces. Humans are infected when consuming contaminated food or water, or through close contact with infected soil or objects (with subsequent ingestion of eggs), including dogs’ mouths and fur. An infection in livestock and humans leads to the development of a hydatid cyst in the liver, lungs, or more rarely, other organs (Grosso et al., 2012). While animals rarely show clinical symptoms, clinical signs and symptoms in humans may develop months or years after infection, and are caused by the expanding cysts and Cystic Echinococcosis in Morocco | 133 inflammatory reactions (Eckert and Deplazes, 2004). Severe cases can only be treated surgically.
CE is a worldwide health problem primarily affecting pastoral and poor rural communities where people raise livestock in close contact with dogs fed on raw offal (Torgerson and Budke, 2003). The latest global burden of CE is estimated at 184,000 Disability-Adjusted Life Years (DALYs), - one DALY being defined as one year of healthy life lost due to ill-health, disability and/or early death -, for a total cost of US$3 billion attributed to CE-related health care costs and losses in the livestock sector (Torgerson et al., 2015).
CE is highly endemic in North Africa and the Middle East. In these regions, incidence rates in humans can exceed 50 per 100,000 person-years (WHO, 2011; Deplazes et al., 2017). In 2012, Morocco recorded an average of 5.2 surgical cases per 100,000 inhabitants and a mortality rate estimated at 2-3% (DELM, 2012). A retrospective survey (2007-2017) in the province of Khénifra shows a maintained incidence rate of 8.62 per 100,000 inhabitants (Ezzahra F. et al., unpublished data). The last epidemiological study in the Mid Atlas showed a prevalence of abdominal CE of 1.9% based on ultrasound examination (Chebli et al., 2017). Official data from the Ministry of Health reported 722 surgical CE cases in 2014 (DELM, 2014). The overall annual cost to both the Moroccan health and livestock sector has been valued at nearly €1,000,000, though data are fragmented (El Berbri et al., 2015). According to a study conducted in five regions of Morocco, prevalence of infection ranges from 23.0% in cattle, 17.8% in Equidae, 12.0% in camels, 10.6% in sheep, to 1.9% in goats. In rural areas, one dog in two carries E. granulosus (Azlaf and Dakkak, 2006). A study conducted in the province of Sidi Kacem (northwest Morocco) between 2010 and 2011 found an E. granulosus infection prevalence of 35.3% in pet dogs (Dakkak et al., 2017). Although Morocco is considered a highly endemic country for CE (Deplazes et al., 2017), this obvious lack of data illustrates clearly the persisting neglect of zoonotic diseases in terms of funding opportunities for epidemiological research, of national health priorities, and consequently of validation of effective CE control strategies and of efficient surveillance measures.
Illiteracy, weak infrastructure and limited economic resources in rural and suburban areas in Morocco play a major role in the distribution of CE. The irrigation systems,
134 | C h a p t e r 3 extensive sheep breeding, high numbers of stray dogs, and poor hygiene in slaughterhouses create ideal conditions for transmission (Marcotty et al., 2013). Both women involved in agricultural activities, and children who come into close contact with dogs, are particularly at risk (DELM, 2010). Control of echinococcosis is difficult due to the complex nature of the parasite’s life cycle, the number of animal species acting as potential (intermediate) hosts, and the requirement for intersectoral cooperation between agricultural, veterinary, and health authorities (Craig et al., 2017). Nowadays, the Eg95 vaccine for sheep (Lightowlers et al., 1996), registered in some parts of the world, combined with cestodicidal treatment of dogs, shows a strong potential to control this disease (Larrieu et al., 2015).
Although the Moroccan Government established an “Inter-Ministerial Committee” in 2007 and drew up guidelines to combat CE (CILCH, 2007), the disease remains a significant public health problem in this country. Currently, hydatidosis control programme managers in Morocco wish to gain a better understanding of the type of risk behaviours that persist in rural populations, and why they persist. This may improve the impact of their control efforts. Dar and Alkarmi (1997) were the first to emphasise the importance of socio-economic and cultural issues in CE control in the Maghreb and the Middle-East (Dar and Alkarmi, 1997; Battelli et al., 2002; Kachani et al., 2003; Battelli, 2009; Dakkak, 2010). Several authors have highlighted the role of human behaviour in the epidemiology of (re-)emerging parasitic zoonoses. Studies in Asian (Schantz et al., 2003; Van Kesteren, 2013; Li et al., 2015), South American (Moro et al., 2008; Acosta-Jamett et al., 2010), and sub-Saharan African populations (Macpherson et al., 1989), as well as the Mediterranean region (primarily Tunisia and Algeria) (Besbes et al., 2003; Benabid et al., 2007; Aoun et al., 2009; Kayouèche et al., 2009), indicate that human risk behaviour associated with poor understanding of the parasite life cycle by the population has a negative impact. However, no study has extensively studied the socio-cultural determinants influencing human behaviour and CE transmission, and no research is available for the High Atlas region.
The objective of this study is therefore to document the reasons behind certain risk behaviours and the socio-cultural determinants hindering the control of CE. By assessing the knowledge gaps about the E. granulosus life cycle and transmission, the role of dogs in this rural society, the community perceptions, practices and knowledge Cystic Echinococcosis in Morocco | 135 regarding sheep and offal management, the study aims to propose more appropriate and effective strategies to overcome barriers, and hence contribute to better control of CE.
3.2.1 Study area
We conducted a qualitative research project based on focus group discussions in a predominantly rural area in the Northern fringes of the High Atlas Mountains, 30 to 50 km south of Marrakech in the Al Haouz province of Morocco. The study region was selected based on reports indicating high prevalence of E. granulosus in humans, sheep, and dogs (Report of the Haouz office, unpublished data), presence of extensive sheep breeding, a large number of free-roaming dogs, and backyard slaughtering without veterinary inspection. Six rural municipalities and one town (Tahannaout) were selected with the approval of the local authorities. The ten villages located among these seven municipalities were randomly selected from villages where the Caïd (chief of the rural municipality appointed by the state) agreed to the study.
The El Haouz province has a population of 484,312 (RGPH19 record from 2004), of which 90% is rural. The main ethnolinguistic group in this area is the Berbers. Their religion is mainly Muslim, and they speak the Atlas Tamazight language, which differs from Arabic. Agricultural activities include extensive sheep breeding and growing of cereals and olives. The livestock population is about 135,265 heads divided into sheep (86%), goats (8.5%), Equidae (3%), and cattle (2.6%).
3.2.2 Study design
Twenty focus group discussions (FGDs) were conducted in ten douars (villages), with a total of 175 participants (83 women and 92 men) (Table 3.1). In exchange for their time, participants were offered veterinary services. To respect the gender sensitivity of rural Muslim culture, ensure women’s participation, and maximise disclosure, none of the FGDs were mixed gender. Based on the initial study design, we held separate
19 Recensement Général de la Population et de l’Habitat
136 | C h a p t e r 3 homogeneous FGDs with male (n = 8) and female (n = 8) villagers, and male butchers (n = 2) since these groups have supposing contrasting perspectives and exposure risks regarding health in general, sheep keeping, and the use of dogs. In the course of the field work we visited a high school where we conducted FGDs with female students (n = 2) initially selected under the same eligibility criteria of the other women groups. Heterogeneous groups are likely to hamper the quality of the data (Morgan, 1998; Grudens-Schuck, 2004). The villagers were mostly sheep farmers, and the FGDs were conducted in Berber or Arabic languages, according to the audience. The number of FGDs conducted allowed us to reach “theoretical data saturation” (Yardley, 2000).
Table 3.1 Characteristics of the focus group discussions (FGD) by rural municipality
FGD Number of participants Municipality Category No. Female* Male* 1 Tahannaout (town; 930 m**) Students 9 2 Students 6 3 Aghouatim (510 m) Villagers 7 4 Villagers 6 5 Oukaimeden (2670 m) Villagers 11 6 Villagers 12 7 Villagers 10 8 Villagers 7 9 Villagers 12 10 Amizmiz (1100 m) Villagers 11 11 Villagers 6 12 Aghmat (670 m) Villagers 7 13 Villagers 7 14 Butchers 8 15 Villagers 11 16 Ourika (860 m) Villagers 4 17 Villagers 9 18 Villagers 11 Cystic Echinococcosis in Morocco | 137
19 Aït Ourir (680 m) Butchers 8 20 Villagers 13 N= 83 N= 92
* Separate FGDs for women and men ** Meters Above Sea Level
3.2.3 Data collection
Data collection took place from October to November 2009. The FGDs consisted of approximately 8 participants (Table 3.1), selected on the basis of their availability and willingness to participate. The question guide was pre-tested in one FGD for each gender among veterinary students from Rabat and fine-tuned during the course of the field work in the study area. To ensure quality of the data collection, two investigators (Séverine Thys & Hamid Sahibi) attended every discussion. Three trained facilitators, all familiar with Arabic and Berber languages, switched roles for each discussion. All FGDs took place in a quiet room in the village (e.g., a living room, classroom, meeting room in house of Caïd, medical consultation room, or administrative room in a slaughterhouse). The discussions lasted about 40 min. The topics covered are presented in Table 3.2. The topics addressed were slightly adapted according to the group to ensure their interest and active involvement in the discussion (see 3.6.1 Supplementary information).
Table 3.2 Discussion guide by topic and group Topic addressed Topic Men* Women** Butchers 1) Knowledge and perceptions of echinococcosis Y Y Y • Knowledge • Treatment & prevention • Impact 2) Sheep management Y N N • Role of sheep • Management problems • Cysts 3) Perception of dogs Y Y N • Positive and negative aspects of dogs • Feeding of dogs • Stray dogs
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4) Perception of control options Y Y Y • Stop feeding dogs with sheep cysts • Feeding of dogs by owners • Burying or burning sheep carcass/offal to prevent dogs from eating them • Discourage dog ownership • Kill stray dogs • Replace sheep with goats 5) Slaughtering practices and cysts in sheep N Y Y • Slaughtering practices • Waste management • Cysts 6) Hygiene N Y N • Hand washing • Water use 7) Economical aspects N N Y • Price setting • Knowledge • Treatment & prevention • Impact * Sheep farmers ** Farmers’ wives and female students Legend : Y: yes; N: no
All discussions commenced with questions on disease knowledge in order to ascertain whether participants spontaneously linked CE to any hosts (sheep and dogs), and whether other transmission factors would be suggested. All discussions were video-recorded except for one FGD with women who refused. Therefore, this FGD was audio recorded only. The facilitator was always assisted by a reporter.
3.2.4 Data processing and analysis
All FGD recordings were transferred from the video-camera to the computer of Séverine Thys and the files were burned to Compact Discs as back up and to be shared among the research team. Tarik Rahali and the two field assistants (Ahlam Marossi and Laila El Jirari) transcribed and translated directly the recorded Arabic or Berber discussions into word documents in French. To improve reliability, two researchers (Séverine Thys & Tarik Rahali) independently reviewed the written transcripts before entering them into the analysis software, being aware that despite the precautions taken some original meanings might have been lost. Text analysis of the transcriptions and the notes taken during the FGDs was supported by the use of NVivo Cystic Echinococcosis in Morocco | 139
10® software (QSR International Pty. Ltd., Melbourne, Australia, 2008), which allows data classification and sorting, and exploration of relationships and trends. Three investigators (Séverine Thys, Ahlam Marossi & Tarik Rahali) each independently coded the major themes emerged from each topic using an inductive approach. They discussed any differences until consensus was reached.
The main results of each topic listed in Table 3.2 are described in more detail and illustrated with anonymous quotes, chosen for their appropriateness and revealing quality. The order used to present opinions and ideas shared by the participants for each topic reflects the level of importance given by the participants to these topics (going from a strong to a weaker consensus). The purpose is to highlight observed patterns and respect what was said in the discussions as much as possible. In view of their substantial input, participants did not seem intimidated by the venues. In general, men were more talkative than women. The ranking of perceived acceptable or non-acceptable control measures included in Table 3.4 was obtained by creating new PROS and CONS categories and sub-categories for each measure based on the word of the participants and cross-cutting them.
3.2.5 Ethical considerations
We obtained ethical clearance from the Agro-Veterinary Institute Hassan II Biomedical Research Ethics Committee (003–02-10). We sought approval from local authorities and community leaders before the study commenced. Finally, we sought individual oral consent from all FGD participants to video-record the discussion. Participation was entirely voluntary and no names were recorded. We took care to phrase the questions appropriately and respectfully.
3.3.1 Life cycle of the parasite and knowledge gaps
3.3.1.1 CE in humans
Most participants were aware of the disease, knew it mainly affects women and children, and were of the opinion it is now more widespread than in the past. Most of the CE cases they knew were not from their village but quite a few participants
140 | C h a p t e r 3 mentioned cases among family members or their neighbours. Five focus group participants (three women, a butcher, and a man) said they had a cyst removed surgically a few years earlier.
“How many women and children infected? About animals, it must be 90%, especially in the area of the mountain where there are many dogs. It is widespread, and people do not know anything, children run alongside, anyone can be infected by the cyst to the liver or other. People are not aware, they know there are diseases, that it has consequences but do not know that dogs are the cause, there is a letting go. The disease we know, they say that the cause is dogs, but there is negligence from all around”. (Focus group\Women Ourika municipality)
In Arabic, “Alakyass almaiya” means hydatid cysts (in human and sheep). Some names given by the participants to this disease were more closely linked to cysts (cyst disease, livestock cysts, hydatid cysts disease), others to dogs (dog disease, cyst of dog, dog microbe, the dog trouble) and some also to the liver (liver disease, cyst of the liver). No specific local name was given to CE in humans, except for the term “Tamought”, which in Berber means “disease”. Respondents identified the cause of CE as a “microbe” or a “virus.” In all the discussions the term “parasite” was only mentioned once by the participants.
The women mentioned the liver as the main organ where cysts were located. They also listed the uterus (vagina, ovaries), belly (intestines, kidneys), and lungs (only twice).
Hydatid cysts were perceived as a dangerous, deadly and evil disease, painful also (especially by women), and affecting health. Few stressed the importance of early treatment but mentioned that this is costly. Only one woman considered this disease not to be contagious. Very few were able to discuss or describe the symptoms, and those who could describe them had personally experienced CE. They mainly mentioned loss of energy (difficulty to move, sleep, or eat), digestive disorders (swollen belly, vomiting), loss of weight and becoming pale-yellow. Two women said that these cysts also prevented women from getting pregnant.
Although most participants said that surgery and medication were the main treatment for this disease (even if these were not perceived as effective), they also mentioned that those infected rarely go to hospital as a first recourse. They would Cystic Echinococcosis in Morocco | 141 first seek healing from traditional healers. As a result, CE diagnosis and treatment is often delayed. Sometimes misdiagnosis contributes to this delay.
“It is the liver jaundice. You take olive oil but without any result. A woman told me to take honey and sulfur, but I have been told that it is not good, you could die (laughs). I looked for honey, but my mother did not let me eat it, she told me it is dangerous. So, I went to see the doctor. Once the X-ray was made, he asked me if we had dogs in the village. I said yes. He told me that dogs cause this cyst, that I ate the (sheep) meat or even the hair of the dog that I have inhaled without noticing it. (…)”. (Focus group\Women Amizmiz municipality)
Early surgical removal of the cyst(s) was considered to provide a complete cure, though a few women stated that cysts might recur. Students considered surgery to be risky. Men especially identified dogs most often as the cause of CE in people, followed by consumption of infected offal (liver) or infected meat. Eating or drinking ware touched by a dog, touching or ingesting their hairs, contracting a bite, or contact with their breath, saliva, or dog in labour were mentioned as additional modes of transmission (3.6.2_Quote a).
Poor hygiene, cats, animals in general, infected livestock, climate (cold, wind, humid, polluted air), and contaminated drinking water were mentioned as other potential sources of infection. For many others, the origin was either unknown, or clearly not the consequence of eating mutton (3.6.2_Quote b).
In contrast to male villagers, the butchers saw infected offal rather than dogs as a cause of CE. They believed that even being rich or having good personal hygiene did not prevent anyone from getting a cyst. Compared to men, women pointed less to dogs or offal as the cause of cysts in humans (3.6.2_Quote c).
3.3.1.2 CE in sheep
While the topic “hygiene” was specifically discussed with women, the “sheep management” one was specifically discussed with the male villager groups. Therefore, answers from men dominate this section. However, this does not mean that men were more knowledgeable about this issue than the three other groups. Cysts were observed in sheep by men at varying frequencies, and most commonly during the feast of Eïd el-Kebir when they slaughter sheep at home to celebrate the Sacrifice of
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Ibrahim. Among butchers, only one person reported that he also often observed cysts. Other infected animals mentioned included bovines, goats, and rabbits.
“If you want, I can give you an estimate. For example, let’s say I kill 10 or 15 sheep, I would say that I found cysts in 5 or 6 of them, and me, I slaughter not often, just for the Eïd or other occasions, such as for example during the harvest. We find the cysts during the harvest period. My father used to slaughter a sheep or a goat whenever we started the wheat harvest, and at that time exactly the animals showed cysts.” (Focus group\Men Oukaimeden municipality)
Cysts were associated with sheep living in close contact with dogs, sick sheep, douar or from the mountainous region, sheep grazing along the oued (river), or on meadows. Cysts were more often observed during the dry season or the harvest. All groups concurred that cysts were mostly observed in the liver of slaughtered sheep. The lungs and intestines were also mentioned. Three butchers specifically mentioned that cysts were also known to be found in gallbladder, kidneys, and throat.
Most participants did not know the origin of the infection. The dog was mentioned most often as the cause of cysts (dogs eating infected offal, living together with animals, dog smell/ bite), followed by water (rain, river, hot water), infected offal, different causes according to the animal (butchers), and finally sheep feed (especially salt) (students) (3.6.2_Quote d).
According to one butcher, humans were also a source of infection for sheep. None of the participants reported observing clinical symptoms of CE in live sheep, although finding cysts at slaughter was often associated with lower weight gain during the fattening period.
Consumption of the cysts was almost unanimously considered as a threat to human health, though not always related to CE. Eating infected offal was considered harmful for dog and sheep health (mentioned by the butchers and the women). One group of men stressed that cooking alone did not kill all the germs. One man referred to it as the “evil eye.” The few participants who did not perceive the cysts as dangerous explained that they did not consider them to be a disease (e.g. some people considered the cysts as God’s creatures living inside the animals and did not believe there was anything bad about them), cooking could kill the cysts, though they had a bitter taste and disgusting aspect. Quite a few respondents Cystic Echinococcosis in Morocco | 143 mentioned that they could not properly evaluate the danger of these hydatid cysts in general.
Finally, we found that there was some confusion during the discussion between hydatid cysts in the human liver and gynaecological cysts. Participants also made some distinction between the type of cysts found in animal meat and that some aspects of rabies transmission were included into the perceived life cycle of E. granulosus, e.g. dog bites as a mode of infection.
3.3.2 Dogs: perception, role, and status
Overall, dogs were perceived as harmful animals, especially stray dogs, which were seen as useless. Men had the most negative perception about dogs, female students the least negative. Thirty-nine topics were mentioned regarding the dogs’ harmfulness. We classified them into seven more generic emerging themes relating to: hygiene (I), nature of the dog (II), roaming pattern (III), care (IV), human health (V), general nuisance (VI), and safety (VII). Themes and their respective sub-themes were listed from most to least mentioned (Table 3.3).
Table 3.3 Aspects perceived as negative for dogs, and for each of the four categories in the FGD
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(1) to (6): The six main nuisances mentioned regarding dogs M: Men; W: Women; B: Butchers; S: Students MI: most mentioned sub-theme by Men; WI : most mentioned sub-theme by Women; BI : most mentioned sub-theme by Butchers; SI : most mentioned sub-theme by Students M1: most mentioned theme by Men (Dogs’ nature) ; W1: most mentioned theme the by Women (Moving); B1: most mentioned theme by Butchers (Hygiene); S1: most mentioned theme by Students (Hygiene) : No quotes found to be coded in this sub-theme a. Quote from female students focus group from Tahannaout municipality; b. Quote from male focus group from Aghouatim municipality; c. Quote from female focus group from Aghmat municipality; d. Quote from male focus group from Amizmiz municipality; e. Quote from female focus group from Aghmat municipality); f. Quote from butchers focus group from Aghmat municipality; g. Quote from female focus group from Aghouatim municipality.
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Most topics covered under negative aspects of dogs related to free-roaming owned dogs as well as stray dogs, which were perceived as a threat to people’s health and security. This is in contrast to non-roaming owned dogs, which have a role in the community such as guarding, shepherding and hunting. In addition, owned dogs are usually better taken care of, though from a hygiene point of view, they were still very much perceived as a threat.
“… But the most dangerous category are dogs that do not serve to guard, herd or hunt. People feed them occasionally, but they stay and sleep outside next to the houses. The souk day, they go and hang out near the slaughterhouse, and other days, they fetch carcasses of dead animals in the ravines. Then they go in the forest where they breed and multiply and become a real problem…” (Focus group\Men Aghouatim municipality)
Some respondents compared dogs to wolves (or to wild animals, predators), gathering in packs and preventing people from moving about freely, especially at night or around places where dogs can find food. Five different groups even referred to the same incident related to feral dogs that had attacked and eaten a teacher (3.6.2_Quote e).
Female students were more likely to view dogs as pets than other groups were. They agreed that not taking good care of these animals, and the associated hygiene issues were a problem, especially if the dogs entered the house. For the butchers, the hygiene issue also came first (in Morocco, dogs are prohibited in slaughterhouses), but the care and the safety risks posed by dogs were not perceived to be that much of a problem. Female respondents especially stressed the risks of being attacked or bitten by dogs. Men perceived the nature of dogs as the main negative aspect and in particular mentioned their insatiability.
A few positive characteristics of dogs were cited such as their resistance/strength, mainly as a result of their ability to find food by themselves. Some participants, especially among the student groups, remarked that dogs also have a soul and therefore the right to live. For some, dogs were companions and essential in their life. None of the butchers had anything positive to say about dogs. Some of the men used the term “Hachakoum” immediately after pronouncing the word “dog”. Hachakoum means “excuse my language” and is used after an obscene, unhealthy, dirty, noxious word. In Morocco, rural populations use this term to designate dogs, donkeys, pigs, Cystic Echinococcosis in Morocco | 147 rubbish, faeces, etc. Some participants talked of the obligation to wash anything touched or contaminated by a dog seven times to purify the place and allow the angel to return. It compels owners to take good care of their dogs (3.6.2_Quote f).
3.3.3 Sheep management and slaughtering practices
Sheep were perceived as “life pillars”, a source of income and savings, as well as carrying prestige, especially during the religious festival of Eïd el-Kebir. Participants saw many advantages of sheep compared to goats, stating their economic and cultural importance. Women take care of the livestock (feeding, watering, cleaning the sheep pen), and this was also acknowledged by a few men (3.6.2_Quote g).
Sheep do not cause any nuisance or pose any threat to human health with the exception of the hydatid cysts or an infected liver. Some respondents said that imported sheep from another Moroccan region tend to get sick more easily. Men said they were in charge of slaughtering and selling the meat at the souk (market). Slaughtering is mainly carried out at home, unless by butchers, and primarily for the Eïd el-Kebir festival. Other occasions such as weddings and harvest festivals were also mentioned. Animals are killed inside the house, in front of the house, in the stable, at the souk, on the ground, or on a tree trunk, and usually not far from a water source. While the men’s role (sheep owner, father, family chief, grandfather, imam) is to slaughter the sheep, the women’s responsibilities are to wash, manage offal, and prepare the meat and tea.
“She washes the stomach and prepares the liver and cooks it, and prepares food for the children (…) And it is also she who deals with waste disposal and cleaning.” (Focus group\Men Ourika municipality)
Sheep were also clandestinely slaughtered by butchers or in official slaughterhouses. Besides slaughtering, the butchers’ roles is weighing/selling meat, and inspecting organs. There are different categories of butchers, such as Maalem (master butcher) and his trainee, skaytiya (retailer, wholesaler), and aarif (butcher spokesperson). The Imam was also mentioned as being present from time to time to say a prayer before the throat of the animal is slit (3.6.2_Quote h).
Meat inspection is compulsory, and performed by veterinarians who sanction clandestine slaughtering. Veterinarians inspect the lungs, liver, head, and foetus,
148 | C h a p t e r 3 while butchers only look at liver and lungs. The livestock owners said they examine the liver, lungs, heart, and gall-bladder when carrying out a home slaughtering. A few men also mentioned corruption, lack of veterinarians, as well as poor slaughtering conditions (lack of hygiene) (3.6.2_Quote i).
Intestines, liver, lungs, stomach (and its contents), gall bladder, heart, and foetus are examined after slaughter. Bones, horns, and gall bladder are discarded, as well as the stomach contents, which are sometimes used as fertiliser. Offal, when considered healthy, as well as heads and legs, are mainly kept for the preparation of traditional dishes. The butchers consider offal as real sellable meat, and lungs, heart, intestines, and especially the liver are noble organs with cultural and economic value. It is considered a great disappointment, frustration, and shame especially for the head of the household who bought or raised the sheep, if the animal slaughtered for the Eïd el-Kebir celebration did not have a big, healthy liver.
“Besides, you know what? People here are poor, and somebody who slaughters a sheep from time to time will not easily throw the liver away that he was looking forward to, to prepare a nice barbecue for him and his children. And there are also those who slaughter a sheep only once a year, on the day of the Eïd Elkebir, you understand? Sometimes people see that there is some stuff in the liver and close their eyes or give no importance because their children wait to eat this liver.” (Focus group\Men Amizmiz municipality)
The reasons mentioned for discarding offal -besides the presence of hydatid cysts- were the fact that they were inedible (e.g. stomach contents), unhealthy, not useful, not appetising, or presenting suspicious lesions (abscesses, white spots, nodules, blackening, holes). While these were mostly discarded preventively, the repulsive aspect of their consumption was a major motivating factor as well.
The management of offal with hydatid cysts can approached three different ways, independent from location/ type of slaughtering (3.6.2_Quote j): (1) removal of the infected part of the organ only (the main method and only method performed by the butchers), (2) removal of the entire organ, and (3) consumption of the whole offal. The latter approach was the least mentioned and only by a few men and women.
Different treatments of the infected parts were explained by the participants. Most treatments enabled dogs access to the cysts, including frequently throwing the offal Cystic Echinococcosis in Morocco | 149 with cysts to the dogs, or ‘discarding the infected parts’ without clear indication of where and how they were thrown away. Places where the infected organs were disposed of included: garbage pits close to as well as far away from the house, in a plastic bag, in the river, in the street, and adjacent to the slaughterhouse. Practices preventing the dogs from accessing the cysts included burying (which was not a habit in the region), burning, drying, and staining with Cresyl, a chemical disinfectant based on phenols which gives a repugnant smell to the condemned meat. There was a consensus among the butchers that dogs should not be allowed in the slaughterhouse, although one woman said: “when the butchers come out, the dogs are eating” (Focus group 10\Women Amizmiz municipality), which means that dogs do have access to waste inside the slaughterhouse.
In most cases, the aforementioned actions did not prevent dogs from accessing the infected offal. With the exception of the butchers, it is important to highlight that more participants mentioned behaviours which allow dogs access to infected offal, rather than those behaviours preventing it. This gap was more pronounced among men. Explicitly giving infected tissues to dogs (and cats) was the action most often mentioned, and mainly by men.
3.3.4 Control measures: pros and cons
In this section we present the participants’ knowledge and perceptions of several suggested CE control measures (Table 3.4).
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Table 3.4 Participants’ knowledge and perceptions of suggested CE control measures: pros and cons Perceived acceptable control Perceived non-acceptable control measures measures Rank Measure Advantages Measure Obstacles 1 Kill stray dogs Help Replace sheep Against the only eliminate with goats culture (food dogs and habits, religion); their threats many disadvantages of goat herding 2 Stop feeding dogs Contribute to Kill all dogs Some dogs have with sheep cysts decreasing a role (useful) the disease and the right to live (have a soul) 3 Feeding dogs Prevent dogs Stop feeding dogs Cysts can be personally going out to with sheep cysts found anywhere look for their else (souk, food and slaughterhouses) returning with diseases 4 Prevention versus More efficient Feeding dogs Impossible to treatment* than yourself educate a dog treatment (big appetite) 5 Kill all dogs Fewer Kill stray dogs only Dogs always problems reappear (reproduction difficult to control) especially if culling campaigns are not carried out regularly 6 Bury infected offal Prevent No more owning Dogs are needed dogs’ access dogs to offal 7 Stop owning dogs Not specified Do not throw away Too costly and carcases time consuming to bury them 8 Stop throwing Avoid the Bury wasted offal Dogs have a away carcasses bad smell strong sense of smell and offal is not buried deep enough Cystic Echinococcosis in Morocco | 151
9 Replace sheep Healthier Burn infected offal Too costly with goats meat with fewer cysts found (less contacts with dogs) 10 Burn infected offal Prevent dogs Reduce dogs’ Not the best having access to method to control access to slaughterhouses** the disease offal and because it does people not come from having to the retrieve them slaughterhouse Avoid bad but from the smell pastures
* Control measures suggested only to men, women and student groups ** Control measure suggested only to the butchers
Both men and women’s groups discussed the positive views and obstacles relating to implementation of CE control measures. In general, female students were more often opposed to these control measures, especially to those related to dogs. Butchers were generally more in favour of all these measures.
Of the ten proposed control measures suggested for discussion in the FGDs (Table 3.4), killing stray dogs was the one that got the biggest consensus from all the groups. However, a few obstacles mentioned included difficulty in controlling dogs’ reproduction, and the inefficiency of this action if it was not implemented regularly and long-term. The female students were the only ones who did not support the killing of all dogs. Both the women’s FDG and the female students highlighted the disadvantages of this measure, including the useful roles for dogs, the fact that dogs are living creatures and had souls (this also applies to stray dogs), and the need for management of dog carcasses. Some butchers feared this measure would never become properly implemented and would therefore not be sufficient to eradicate the disease.
Men were more likely to be in favour of the prevention of feeding cysts to dogs than the other groups, and generally agreed that it could contribute to a reduction of the disease, but not to its eradication (3.6.2_Quote k). Nevertheless, men also said this was a bad solution as dogs would continue to find cysts elsewhere (souk,
152 | C h a p t e r 3 slaughterhouse, …); free roaming stray dogs could bring the “badness” from another source, and the implementation would fail due to lack of sensitisation and people’s carelessness. In addition, few women across the FGDs considered this a bad strategy. On the other hand, men generally considered burying offal an important measure, primarily to prevent dogs’ access to it. Similarly, it was primarily the men who were in favour of the idea of stopping the indiscriminate disposal of carcasses. The reasons for this are firstly to avoid the smell, secondly to implement the law, and thirdly, to prevent dogs’ or wild animals’ getting hold of the carcasses. Some men and butchers expressed scepticism about these measures for the following reasons: the high cost of burying or burning cadavers, the time required to do so, disposal of carcasses is not commonplace (lack of awareness), and carcasses are not usually buried deep enough, allowing dogs to dig them up.
All groups opposed the replacement of sheep with goats, and men generally did not look favourably on feeding dogs (to prevent them looking for other food). According to the men, most local dogs are strays without an owner and are therefore uncontrollable. Dogs, in general, would always be on the lookout for more food, and dog food was too expensive. Preventing dogs from roaming around in the slaughterhouse was only proposed as a control measure to the butchers who said that not only was this measure already implemented, it was also not the most efficient way of controlling the disease.
Men 8 (M8): “But the disease is not here that it appears or in the slaughterhouse, but elsewhere when herds are circulating in the prairies and between villages.” M6: “(When herds are circulating) with the dogs, two or three dogs.” M2: “Some owners have four dogs, and sheep are not vaccinated nor dewormed. There is a misconception. He thinks that if he treats these animals they will not be in good condition anymore, and he maintains the presence of four-five dogs with him.” M6: “And it is from the dogs that comes this disease.” (Focus group\Butchers Aït Ourir municipality)
3.3.5 Additional measures suggested by the participants
In addition to these 10 strategies to control CE, participants also suggested alternatives for themselves and authorities (veterinary services and the government). Cystic Echinococcosis in Morocco | 153
They also asked to combine all the suggested control measures and include an improved awareness.
Individual measures
Individual measures to be enacted by all included improved hygiene, especially before cooking (washing hands, food, and cooking utensils), blocking animals’ access to the house, avoiding consumption of food touched by dogs, avoiding consumption of hydatid cysts, and fencing pastures. Participants also suggested burying animal carcasses sufficiently deep and with the help of others. Dog owners should take greater care of their animals, stop them roaming freely, feed and train them, and prevent their access to livestock when they are sleeping and being fed in their pen.
Measures to be implemented by the authorities
Control strategies suggested for implementation by veterinarians and the government mainly by male participants included dog vaccination (which does not currently exist for CE).
Women 8 (W8): “But why Europeans live with dogs but are not affected by the disease?” W1: “They vaccinate them.” (Focus group\Women Amizmiz municipality) A number of measures actually related to improved implementation of the aforementioned strategies included: creation of specific places for stray dogs, a more regular and synchronised culling of dogs, organised pick up of dog cadavers and infected offal, and more regular inspection of all carcasses by veterinarians. The latter should also provide more assistance to farmers (treatment and advice, even via a free phone number), encouraging farmers/people to take better care of their animals.
A male FGD advocated for the prohibition of slaughtering at home as a solution for CE control. They also suggested improved strategy implementation by imposing fines on those that do not apply the control measures, and the signing of implementation agreements.
Awareness measures
Those who had heard of CE or hydatid cysts said they had been informed by the medical sector, the media, their network, veterinarians, charitable associations, religious organisations, schools, ministries, and butchers. Women received health
154 | C h a p t e r 3 information mainly from the media, and butchers only via veterinarians. Students obtained information from various sources, but not via veterinarians or butchers. Men learned about this disease primarily via the medical sector and associations (3.6.2_ Quote l, m and n).
In some of the discussions there was a demand for raised awareness and health promotion for CE, at both village and individual level, but especially amongst dog owners.
Some specific recommendations were made for improved awareness tools. Television, often used as a dissemination channel, was not considered efficient because villagers either did not have access to a television, or they were working in the field all day. In addition, explanations given in newspapers were often too difficult to understand and led to more confusion and misunderstanding. Hence, it was suggested to firstly make visits (face-to-face sessions) and tour the whole region, specifically rural areas which receive less attention than urban areas. Secondly, the display of illustrated posters in the Berber language was also deemed important because not everybody speaks or understands French or Arabic. In particular, women emphasised that everyone should share their knowledge about the disease with their family, friends, and community, and promote the adoption of appropriate behaviours. The health promotion messages and visits had to be carried out by “intellectuals”, and the scientific community. Media (mainly radio, and following face-to-face sessions), rural associations, health facilities, ministry of health, schools, religious representatives (imam), and veterinarians were suggested as appropriate relays for the dissemination of these health messages.
This qualitative study offers a deeper understanding of why rural communities in Morocco are engaged in behaviours resulting in the improper disposal of viscera at slaughtering, leading to high risk of E. granulosus infection in dogs (El Berbri et al., 2015). The study was conducted in an epidemiological context representative of other rural settings in Morocco (Chebli et al., 2017) and neighbouring countries (Sadjjadi, 2006), where CE is principally maintained in a domestic dog-sheep cycle and affects mainly women and children. Respondents described specific risk behaviours leading Cystic Echinococcosis in Morocco | 155 to a very high environmental contamination with parasite eggs including inadequate sanitary practices regarding offal management, abundance and proximity of free roaming dogs looking for food, and low awareness of transmission risks.
Similar to previous studies carried out amongst the Berber people from the Middle Atlas (central Morocco) (Kachani et al., 2003), our results show that the occurrence of CE in both humans and animals is widely known in the studied community. Hydatid cysts and lesions were recognised and well described by our respondents, but their knowledge of the transmission cycle and the link to human disease was relatively poor and fragmented. In contrast to pastoralists (Craig et al., 2017) and findings from a Knowledge, Attitude and Practices (KAP) study conducted in the Northwest of Morocco (Chebli et al., 2017), our study population was well-aware of dogs being a source of infection, to the point of naming CE “dog disease” or “dog cysts”. However, how dogs get infected and how they transmit the disease to humans and livestock was not well known by many of the participants.
By partitioning the life cycle of E. granulosus according to its transmission paths between the three hosts (humans, sheep, dogs), and organising all related quotes accordingly, we could picture participants’ perceived life cycle of the parasite (Fig. 3.1), and identify the corresponding knowledge gap(s). A perceived life cycle was described by Marcotty et al. (2013) using preliminary data.
As in our previous study on Taenia solium (Thys et al., 2016), very few people had a comprehensive view of the parasite life cycle. While some pieces of the puzzle were easily identified (e.g. risks dog poses to human health), others were often lacking (e.g. infection of dogs through feeding on infected organs), and some putative hosts were erroneously added (e.g. cats). Finally, some transmission paths between hosts were easily identified (e.g. humans getting cysts from dogs), although the knowledge on how the disease was transmitted from one host to the other was not always accurate (e.g. humans getting cysts from dogs by their breath).
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Figure 3.1 The real (A) and perceived (B) life cycle of Echinococcus granulosus in High Atlas, Morocco. Adapted from Marcotty et al. (2013)
In contrast with the recent Moroccan KAP study (Chebli et al., 2017), we observed that the main knowledge gaps varied between the stakeholders. The female students had very poor knowledge in general. They perceived the threats from the dogs as less serious compared to the other groups, and saw dogs more as pets. Very few butchers identified the dogs as a source of infection for humans, as for them the main risk for contracting CE in humans was eating infected offal. On the other hand, butchers were well aware that dogs could infect sheep. Very few women but most men made the link between infected offal and dog infection. Yet, more women than men considered eating infected offal less of a health issue. For men, the biggest problem was the disease transmission from dogs to humans.
These data are very important to build efficient and adapted health promotion messages because the specific knowledge gaps explain several of the risk behaviours, especially regarding infected offal management. If women’s responsibilities are to clean and manage viscera but, at the same time, these women do not perceive the hazard of feeding dogs with infected offal, the parasite’s life cycle will be maintained. This finding is in line with other Moroccan studies that highlighted that safe disposal of offal with cysts is downplayed because only human consumption of cysts is Cystic Echinococcosis in Morocco | 157 considered holding a disease risk and not consumption by dogs (Chebli et al., 2017; Bardosh et al., 2016). Undeniably, offal are very often made accessible to dogs, voluntarily or involuntarily, at slaughterhouses, souks, open air uncontrolled dumping, streets, and rivers, which is the main reason for the persistence of the disease (Eddi et al., 2006). These offal management practices however, are not only mediated by lack of awareness, but also by various social determinants including religion, gender, and food preparation norms of sheep offal, which influence how households consume and discard infected offal. During the Eïd el-Kebir festival, the Moroccan tradition consists of preparing organ meat such as sheep liver and heart on the day of slaughter. The liver is grilled first by the men of the family partly for practical and sanitary reasons (organs are best eaten fresh), but mainly because of the liver’s symbolic and social value which strongly competes with its commercial value (Brisebarre, 2002). As a “concentrated life form”, the liver of the animal is considered as the seat of the filial love, hence the importance of its physical integrity especially during the yearly sheep sacrifice festival. Other viscera are also seen as preserving the honour of the family (Mahdi, 1998) and attracting the “Baraka” (flow of blessings and grace) to the whole family (Brisebarre, 2002). Consequently, all damages, black spots, and cysts should be removed from the organs and disposed of, which often makes them accessible to dogs (3.6.2 above offal management practices), allowing the maintenance of the parasite’s life cycle.
The place given to dogs by the Muslim culture and some related religious precepts translated from the Koran by Imams in hadiths (Muslim laws) explain why dogs should be well treated like all other God creatures (dogs have a soul and therefore the right to live) or killed if they attack, but also why they are so often blamed as the source of cysts found in humans even though they are asymptomatic for E. granulosus infection. A close relationship with them is discouraged since they are hygienically and spiritually perceived as impure animals. This is even more the case for “unwanted” stray dogs, because they chase away protective angels from entering a house. The dirt brought by impure animals needs to be washed away. These Muslim cultural and religious beliefs, referring to the miasma theory (Karamanou et al., 2012), constitute probably an underlying explanation of several practices regarding dog keeping in the Middle East and North Africa, where stray dogs are abundant, and
158 | C h a p t e r 3 where there is often no legislation in relation to responsible dog ownership and formal control of reproduction (Kachani and Heath, 2014).
According to our results, dogs, even owned, most often roam freely, and this may be because tying them up would imply to physically touch their “impurity”. In the context of Tibetan herdsmen, Heath et al. (2006) advocated for more participatory planning between dog-owners and community leaders to enable a choice of possible control strategies that suit both the social and economic status of a particular target community. However, waste management and hygiene negligence, both from the rural communities and the authorities, was often mentioned in our study as a barrier to any control measures. This discrimination of rural and more remote areas by the state and by the authorities felt by our studied population was also identified in recent studies conducted in Morocco (Ducrotoy et al., 2015; Bardosh et al., 2016; Bennis et al., 2017).
Aside from the control measures discussed, health promotion, including health education and awareness creation, was spontaneously raised by some participants. Others recommended several methods for organising and implementing these awareness-raising campaigns in a more effective way, e.g. face-to-face meetings, radio messages in Berber language, etc. These proposals should certainly be considered when designing awareness programmes.
The dissemination of the life cycle of E. granulosus and risk factors contributing to human infections is the biggest challenge for CE control (Heath et al., 2006). Ducrotoy et al. (2015), who evaluated an integrated health messaging intervention for five zoonotic diseases in northwest Morocco, including CE, showed similar findings. Their intervention had different outcomes according to the target audience (men, women, and children) because of the educative role and norms at household level, and children remained the most receptive group (Ducrotoy et al., 2015). Behavioural Change Education regarding dog keeping, livestock husbandry, personal hygiene, and home-based slaughter practices is important but would never be enough to tackle conceptual and operational challenges in the design of efficient interventions at the “human-animal-ecosystem” interface (Bardosh et al., 2016).
The scope of our research mainly focused on the biosocial dynamics of the parasite at the household level, yet the ones in place at slaughterhouse level also present a lot of Cystic Echinococcosis in Morocco | 159 challenges for controlling this disease, as highlighted by Bardosh et al. (2016). The butcher groups made fewer comments regarding dogs because the topic of perception, role, and status of dogs was not included in their FGDs (3.6.2 Table 3.2). As a powerful lobby group and because of the complex socio-political processes that exist among the different stakeholders involved in slaughterhouses management such as veterinary technicians and politicians (Bardosh et al., 2016), butchers may have strategically controlled their answers when asked about the presence of dogs in the slaughterhouse, the management of discarded offal, and meat inspection to avoid getting attention from the authorities and the implementation of additional control measures on their work.
Sheep management was not included in the discussion guide for women. However, we discovered that women are the ones taking care of the livestock (although the decision-making still remains the responsibility of the men). This observation further emphasises the importance of identifying, understanding, and integrating all the pertinent actors related to the targeted health problem when elaborating a disease control programme, and thus also including the role of women in livestock management.
The observed differences regarding CE perception between four social strata raise the challenge of engaging these different social groups in CE prevention and control. This means that looking at each group category and their prioritised control measures might be a good approach as previously advocated by Battelli (2009). However, to remain feasible and “saleable” to programme managers, the specificities of each group should be jointly prioritised through a consensual participative approach.
For example, free roaming dogs are key in the continued disease transmission in our studied ecosystem. Supporting dog-owners by, identifying their needs, dog neutering, awareness campaigns, mobile vet care, free deworming, etc., is essential for effective CE control, but interventions for the management of stray dogs in this rural remote area must also be designed. In our study, killing unowned stray dogs perceived as harmful was identified as the most acceptable control measure, despite Islam not allowing the killing of any living beings. Therefore, stray dogs should be visually
160 | C h a p t e r 3 distinguished from free-roaming owned dogs, by collars, ear tags, etc.. Local authorities should also elaborate integrated strategies through the rabies control programme created in 2000 by the ONSSA (Office National de Sécurité Sanitaire des Produits Alimentaires)20 to manage the size of dog populations. Also, to restore the trust of the population in their local authorities and ensure a successful and long-term hydatid disease control programme, integrating “mediators” such as local associations and NGOs could be explored.
As culture is always evolving, adapted control measures must be implemented and negotiated with the population to be effective and sustainable. Therefore, we suggest a reflective bottom-up approach of progressive problem solving starting with a mapping of all the stakeholders involved in this control programme, and a qualitative evaluation of their respective knowledge of this programme and its activities, their role, their perception of its efficiency, and implementation beyond an epidemiological rationale. Indeed, the social relationships or political and anthropological levers could enhance the promotion of collective action and empowerment in terms of diseases management (e.g. power games among different social groups not only regarding their practices in terms of risk factors and the social linkages among groups and their relationship to authorities, beyond health authorities). At the same time, it would be beneficial when redesigning and implementing the activities of the Moroccan CE control programme to improve CE knowledge of both medical professionals and communities via health promotion techniques, taking into account the socio-cultural context of these groups. Medical doctors working in these remote areas could play an important role in knowledge transfer of CE control, while students who were perceived and perceived themselves in our study as “vanguards” of behaviour change within their immediate families and the wider community could also make a considerable contribution.
Finally, vaccination of sheep was not included in the discussions as this was not available as a control option at the time of our study (2009). However, the Institute of Agriculture and Veterinary Hassan II (Rabat), together with the support of Belgian
20 http://www.onssa.gov.ma/fr/sante-animale/programme-de-prophylaxie/rage-animale Cystic Echinococcosis in Morocco | 161 universities21 is currently evaluating the efficacy and acceptability of the Eg95 vaccine for sheep.
3.6.1 Focus Group Discussion guides (Men, Women and Butchers) in English.
The guides elaborated for the Focus Group Discussions for each of the three group categories (Men, Women and Butchers), documented in the research protocol and translated from French to English for the purpose of this publication.
1) Men
Knowledge and perceptions of echinococcosis
Have you ever heard about cysts in people (men, women, or children) ? What is the name given? Where in the body are these cysts located? Is it frequent in this village ? How important is this disease in relation to your health? What is the impact on daily life? What happens when somebody develops such a disease? How do you treat it ? How can you prevent it? What is the origin of these cysts according to you ? How can we interrupt the development of these cysts? How can we control the cysts? How do we remove the cysts? Sheep management
Sheep role
What are according to you the positive aspects of sheep keeping ? For which reasons sheep are useful? What are the negative aspects of sheep keeping ? What are they dangerous for ? Issues of management
What do you experience as major issues regarding sheep management ? Where are the sheep slaughtered ? How many sheep approximatively are slaughtered in this locality ? Regarding home slaughter: How is it done ? Do you have a special location where to do it? What kind of specific precautions do you take? Who is involved in the activities related to slaughter ? What do you keep/throw away ? What do you do with the waste ?
21 http://www.ares-ac.be/fr/cooperation-au-developpement/pays-projets/projets-dans-le- monde/item/78-prd-renforcement-de-la-strategie-de-lutte-contre-l-echinococcose-zoonotique-au- maroc-aspects-veterinaires-economiques-et-sociologiques
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Cysts (Echinoccocus)
Have you ever found white large cysts on a carcass of a sheep ? On which parts? How often ? What did you do when you found these cysts ? What is the origin of these cysts? Do you find them also in other animals? How similar/different are those cysts compared to these found in sheep ? How harmful can be these cysts ? For sheep health? For human health? What would happen if dogs eat these cysts? What would happen if a person eat these cysts? Perception of dogs
Positive and negative aspects of dogs
According to you what are the positive aspects of dogs ? For which reasons dogs are useful or needed? What are the negative aspects of dogs? In which case they represent a danger or a nuisance ?
Feeding of dogs
What dogs are fed with ? Do feed them yourself? Where are they looking for their food?
Stray dogs
What do you think of stray dogs ? For what are they useful ? For what are they harmful ? How do they impact your village (beside rabies) ?
Perception of control options
Imagine that we propose several control measures against echinococcosis (or use local name). What would be the principals obstacles to implement them: Method 1 : Stop feeding dogs with sheep cysts ? Method 2 : Feeding of dogs by owners? And their puppies ? Method 3 : Burying or burning sheep carcass/offal to prevent dogs from eating them ? Method 4 : Discourage dog ownership ? Method 5 : Kill stray dogs ? Method 6 : Replace sheep with goats ?
2) Women
Knowledge and perceptions of echinococcosis
Have you ever heard about cysts in people (men, women, or children) ? What is the name given? Where in the body are these cysts located? Is it frequent in this village ? Cystic Echinococcosis in Morocco | 163
How important is this disease in relation to your health? What is the impact on daily life? What happens when somebody develops such a disease? How do you treat it ? How can you prevent it? What is the origin of these cysts according to you ? How can we interrupt the development of these cysts? How can we control the cysts? How do we remove the cysts? Slaughtering practices and cysts in sheep
Slaughtering practices
Regarding home slaughtering: How is it done ? Do you have a special location where to do it? What kind of specific precautions do you take? Who is involved in the activities related to slaughtering ?
Waste management
What do you keep/throw away ? What do you do with the waste ?
Cysts (Echinococcus)
Have you ever found white large cysts on a carcass of a sheep ? On which parts? How often ? What did you do when you found these cysts ? What is the origin of these cysts? Do you find them also in other animals? How similar/different are those cysts compared to these of sheep ? How harmful can be these cysts ? For sheep health? For human health? What would happen if dogs eat these cysts? What would happen if a person eats these cysts? Perception of dogs
Positive and negative aspects of dogs
According to you what are the positive aspects of dogs ? For which reasons dogs are useful or necessary? What are the negative aspects of dogs? In which case they represent a danger or a nuisance ?
Feeding of dogs
What dogs are fed with ? Do you feed them yourself ? Where are they looking for their food?
Stray dogs
What do you think of stray dogs ? For what are they useful ? For what are they harmful ? How do they impact your village (beside rabies) ?
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Hygiene
What is the origin of the drinking water for your household? What is the source of water you use to wash vegetables? What do you think about the quality of the water you are using to wash vegetables ? Does it happen sometimes to eat crude vegetables without having washed them before ? How available is the water to wash your hands before eating? For you ? For your children ? Perception of control options
Same questions as for Men and Butchers.
3) Butchers
Slaughtering practices and cysts in sheep
What does your work consist of, and particularly the slaughtering activities ? What do you keep/throw away ? What do you do with the waste ? What do you think about the way slaughtered animal waste is currently managed ? How could it be more optimal for you ? What methods would be more appropriate according to you ? What is missing for improving your work conditions? What is missing for improving slaughter conditions? (How often do you get veterinary inspections in the slaughterhouses ? Which organs are controlled? What does happen with the condemned offal ? What kind of sanctions are there in case of violations ?) Do dogs have access to the slaughterhouses ? How do you perceive their presence there ? How could access of dogs in the slaughterhouses be restricted ? What are the barriers to implement your suggestions ? Cysts (Echinoccocus)
Have you ever found white large cysts on a carcass of a sheep ? On which parts? How often ? What did you do when you found these cysts ? What is the origin of these cysts? Do you find them also in other animals? How similar/different are those cysts compared to these of sheep ? How harmful can be these cysts ? For sheep health? For human health? Knowledge and perceptions of echinococcosis
Have you ever heard about cysts in people (men, women, or children) ? What is the name given? Where in the body are these cysts located? Is it frequent in this village ? Cystic Echinococcosis in Morocco | 165
How important is this disease in relation to your health? What is the impact on daily life? What happens when somebody develops such a disease? How do you treat it ? How can you prevent it? What is the origin of these cysts according to you ? How can we interrupt the development of these cysts? How can we control the cysts? How do we remove the cysts? What would happen if dogs eat these cysts? What would happen if a person eats these cysts? Economic aspects
How is the price of a sheep established? Which are the factors that do raise the price or reduce the price ? What is the value of a liver ? How can we ensure that the liver is in good state ?
Perception of control options
Same questions as for Men and Women.
3.6.2 Illustrative quotes from the Focus Groups Discussions (“a” to “n”)
Quotes (“a” to “n”) selected from the Focus Group Discussions conducted in the Hight Atlas in Morocco (October - November 2009) to illustrate the results.
Quote_a: Focus group of men from the Amizmiz municipality: “I was saying that the dog did burp in front of its owner who was eating and who had fallen ill just after. Probably that badness is transmitted by the saliva of the dog or just by the smell or the breath coming out of his mouth and which goes through the breath of its owner”
Quote_b : Focus group of men from the Ourika municipality: “Only with the smell you can get sick if these things are thrown in the open air.”
Quote_c: Focus group of butchers from the Aghmat municipality “Because this cyst found in sheep (it) is called the dog sickness, and this cyst, this ball of water, if it breaks out, it can be a danger even to the butcher.”
Quote_d: Focus group with men from the Aït Ourir municipality “The animal infected by the cyst will not live, dear Mister (appearing very self- confident). You know, sheep during a heat wave, under the sun until their fat gets hot, and then they go to drink very cold water, here and there in various streams. And well, I tell you, it is what causes cysts.”
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Quote_e: Focus group with men from the Amizmiz municipality: “Dogs can eat human flesh. Someone from the region of Rhamana had told me one day, and I swear to you, that dogs had attacked a schoolteacher who was traveling on her motorbike. They had devoured her and had left only the hair on the spot.”
Quote_f: Focus group with men from the Aghmat municipality: M2: “But if you have a dog you have to take care of it before God.” M9: “Of course.” M5: “These people don't understand, but you know that if you don't take care of him you will be cursed, and you'll be in sin...” M2: “You will have it on your conscience.” M5: “You have to give him to eat and take care of him.” M2: “If you are able to do it, it is good. If not, let him go, free him.” M4: “And if he doesn't want to leave, you must kill him, right”
Quote_g: Focus group with women from the Oukaimeden municipality: “Watching TV, only at night after having finished what we have to do: do the housekeeping, meal preparation, laundry and of course take care of animals by feeding them and get them out to be able to clean the fold.”
Quote_h: Focus group with butchers from the Aghmat municipality: M7: “Among us, there are some who dismember, some who slaughter and some who do not dismember...” M6: “There are some maalems with their apprentices...” M7: “Bosses with their apprentices...” M3: “The maalems of the balance, "experts of the meat weighing".” M7: “And there are wholesalers.” M8: “There are the skaytiya who deal with offal and resell them.”
Quote_i: Focus group with men from the Aït Ourir municipality: “Because finally we (speaking as a butcher) just look at the liver and lungs. If there is a sleazy thing we inform the owner and we remove it, but we are never sure.”
Quote_j: Focus group with men from the Aghouatim municipality: “If there are many (cysts), we throw the liver away, if there are few, we remove the infected part, and we keep the rest.” Cystic Echinococcosis in Morocco | 167
Quote_k: Focus group with men from the Oukaimeden municipality: “(...) because I do not think that dogs eating these cysts will have the illness.”
Quote_l: Focus group with butchers from the Aït Ourir municipality: “Bah Yes, we do not remain silent in front of veterinarians, we ask them to explain us the origin of everything. For example for cysts, they tell us it is because the animals live with dogs, and these dogs defecate near animals that can eat it, and animals will also be sick and reject these cysts for dogs.”
Quote_m: Focus group with students from the Tahannaout municipality: “Excuse me, a teacher taught us in Islamic education. The sheep slaughtered the day of Eïd must not be eaten meat before 24 hours because the cells are still alive, blood circulation is still functional.”
Quote_n: Focus group with men from the Amizmiz municipality: “There are doctors who say that it (cyst) probably comes from food contaminated by the dogs or cats hair...”
Acosta-Jamett, G., Cleaveland, S., Cunningham, A.A., Bronsvoort, B.M. deC, 2010. Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission. Prev. Vet. Med. 94, 272–281. Agudelo Higuita, N.I., Brunetti, E., McCloskey, C., 2016. Cystic Echinococcosis. J. Clin. Microbiol. 54, 518–23. Aoun, K., Benabid, M., Galai, Y., Chahed, M.K., Bouratbine, A., 2009. [The current risk factors for hydatidosis in Tunisia]. Med. Trop. 69, 311. Azlaf, R., Dakkak, A., 2006. Epidemiological study of the cystic echinococcosis in Morocco. Vet. Parasitol. 137, 83–93. Bardosh, K.L., Berbri, I. El, Ducrotoy, M., Bouslikhane, M., Ouafaa, F.F., Welburn, S.C., 2016. Zoonotic encounters at the slaughterhouse: Pathways and possibilities for the control of Cystic Echonococcosis in Northern Morocco. J. Biosoc. Sci. 48 Suppl 1, S92–S115. Battelli, G., Mantovani, A., Seimenis, A., 2002. Cystic echinococcosis and the Mediterranean Region: A long-lasting association. Parassit. 44, 43–57. Battelli, G., 2009. Echinococcosis: Costs, losses and social consequences of a neglected zoonosis. Vet. Res. Commun. 33, S47–S52. Benabid, M., Chahed, M.K., Nouira, R., Galai, Y., Bouratbine, A., Aoun, K., 2007. Knowledge, Behaviour and Implications on Hydatidosis Transmission in Tunisia. Rev Tun. Infect. 1, 22–28.
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Bennis, I., Thys, S., Filali, H., De Brouwere, V., Sahibi, H., Boelaert, M., 2017. Psychosocial impact of scars due to cutaneous leishmaniasis on high school students in Errachidia province, Morocco. Infect. Dis. Poverty 6, 1-8. Besbes, M., Sellami, F., Cheikhrouhou, F., Makni, F., Ayadi, A., 2003. L’abattage clandestin en Tunisie: enquête sur les connaissances et les pratiques des bouchers face à l’hydatidose. Bull. Soc. Pathol. Exot. 96, 320–322. Brisebarre, A.M., 2002. Le statut du mouton du sacrifice de l’Ayd al-kabir: Rapport à l’animal, à son sang et à sa viande. Anthropozoologica. 35, 39-50. Chebli, H., Laamrani El Idrissi, A., Benazzouz, M., Lmimouni, B.E., Nhammi, H., Elabandouni, M., . . ., Tamarozzi, F., 2017. Human cystic echinococcosis in Morocco: Ultrasound screening in the Mid Atlas through an Italian-Moroccan partnership. PLoS Negl. Trop. Dis. 11, e0005384. CILCH, 2007. Comité interministériel de lutte contre l’Hydatidose/Echinococcose. Ministry of Interior, Rabat. Craig, P.S., Hegglin, D., Lightowlers, M.W., Torgerson, P.R., Wang, Q., 2017. Echinococcosis: Control and Prevention. Adv. Parasitol. 96, 55–158. Dakkak, A., El Berbri, I., Petavy, A.F., Boué, F., Bouslikhane, M., Fassi Fihri, O., . . ., Ducrotoy, M.J., 2017. Echinococcus granulosus infection in dogs in Sidi Kacem Province (North- West Morocco). Acta Trop. 165, 26–32. Dakkak, A., 2010. Echinococcosis/hydatidosis: A severe threat in Mediterranean countries. Vet. Parasitol. 174, 2–11. Dar, F.K., Alkarmi, T., 1997. Public health aspects of cystic echinococcosis in the Arab countries. Acta Trop. 67, 125–132. DELM, 2010. Ministry of Health of Morocco (Ministère de la Santé du Maroc). Bilan des activités des programmes de lutte contre les maladies parasitaires, année 2010. Direction de l’Epidémiologie et de la Lutte contre les maladies. Service des maladies parasitaires. DELM, 2012. Ministry of Health of Morocco (Ministère de la Santé du Maroc). Situation épidémiologique des maladies parasitaires, année 2012. Direction de l’Epidémiologie et de la Lutte contre les maladies. Service des maladies parasitaires. DELM, 2014. Ministry of Health of Morocco (Ministère de la Santé du Maroc). Bilan des activités des programmes de lutte contre les maladies parasitaires, année 2014. Direction de l’Epidémiologie et de la Lutte contre les maladies. Service des maladies parasitaires. Deplazes, P., Rinaldi, L., Alvarez Rojas, C.A., Torgerson, P.R., Harandi, M.F., Romig, T., . . ., Jenkins, E.J., 2017. Global Distribution of Alveolar and Cystic Echinococcosis. Adv. Parasitol. 96, 315–493. Ducrotoy, M.J., Yahyaoui Azami, H., El Berbri, I., Bouslikhane, M., Fassi Fihri, O., Boué, F., . . ., Bardosh, K.L., 2015. Integrated health messaging for multiple neglected zoonoses: Approaches, challenges and opportunities in Morocco. Acta Trop. 152, 17–25. Eckert, J., Deplazes, P., 2004. Biological, Epidemiological, and Clinical Aspects of Cystic Echinococcosis in Morocco | 169
Echinococcosis, a Zoonosis of Increasing Concern. Clin. Microbiol. Rev. 17, 107–135. Eddi, C., Katalin, de B., Juan, L., William, A., Andrew, S., Daniela, B., Joseph, D., 2006. Veterinary public health activities at FAO: Cysticercosis and echinococcosis. Parasitol.Int. 55 Suppl, S305–S308. El Berbri, I., Ducrotoy, M.J., Petavy, A.-F., Fassifihri, O., Shaw, A.P., Bouslikhane, M., . . ., Dakkak, A., 2015. Knowledge, attitudes and practices with regard to the presence, transmission, impact, and control of cystic echinococcosis in Sidi Kacem Province, Morocco. Infect. Dis. Poverty 4, 1-12. Grosso, G., Gruttadauria, S., Biondi, A., Marventano, S., Mistretta, A., 2012. Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World J. Gastroenterol. 18, 1425–1437. Grudens-Schuck, N., Allen, B.L., Larson, K., 2004. Methodology Brief: Focus Group Fundamentals. Iowa State University Extension. Heath, D., Yang, W., Li, T., Xiao, Y., Chen, X., Huang, Y., . . ., Qiu, J., 2006. Control of hydatidosis. Parasitol. Int. 55, 247–252. Kachani, M., Macpherson, C.N.L., Lyagoubi, M., Berrada, M., Bouslikhane, M., Kachani, F., El Hasnaoui, M., 2003. Public health education/importance and experience from the field. Educational impact of community-based ultrasound screening surveys. Acta Trop. 85, 263–269. Kachani, M., Heath, D., 2014. Dog population management for the control of human echinococcosis. Acta Trop. 139, 99–108. Karamanou, M., Panayiotakopoulos, G., Tsoucalas, G., Kousoulis, A.A., Androutsos, G., 2012. From miasmas to germs: a historical approach to theories of infectious disease transmission. Infez. Med. 20, 58–62. Kayouèche, F., Chassagne, M., Benmakhlouf, A., Abrial, D., Dorr, N., Benlatreche, C., Barnouin, J., 2009. Facteurs socio-écologiques associés au risque d’hydatidose familiale dans la wilaya de Constantine (Algérie) à travers l’interview de ménages résidant en zones urbaine et rurale. Rev. Med. Vet. 160, 119–126. Larrieu, E., Mujica, G., Gauci, C.G., Vizcaychipi, K., Seleiman, M., Herrero, E., . . ., Lightowlers, M.W., 2015. Pilot Field Trial of the EG95 Vaccine Against Ovine Cystic Echinococcosis in Rio Negro, Argentina: Second Study of Impact. PLoS Negl. Trop. Dis. 9, e0004134. Li, D., Gao, Q., Liu, J., Feng, Y., Ning, W., Dong, Y., . . ., Xin, D., 2015. Knowledge, attitude, and practices (KAP) and risk factors analysis related to cystic echinococcosis among residents in Tibetan communities, Xiahe County, Gansu Province, China. Acta Trop. 147, 17–22. Lightowlers, M.W., Lawrence, S.B., Gauci, C.G., Young, J., Ralston, M.J., Maas, D., Heath, D.D., 1996. Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunol. 18, 457–62. Macpherson, C.N., Craig, P.S., Romig, T., Zeyhle, E., Watschinger, H., 1989. Observations on human echinococcosis (hydatidosis) and evaluation of transmission factors in the Maasai of northern Tanzania. Ann. Trop. Med. Parasitol. 83, 489–497.
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Mahdi, M., 1998. Se Sacrifier pour sacrifier: prescription sociale et impératifs religieux. In: Brisebarre, A.M. (Ed.), La fête du mouton. Un sacrifice musulman dans l’espace urbain. CNRS Editions, Paris, pp. 283–315. Marcotty, T., Thys, E., Conrad, P., Godfroid, J., Craig, P., Zinsstag, J., . . ., Boelaert, M., 2013. Intersectoral collaboration between the medical and veterinary professions in low- resource societies: The role of research and training institutions. Comp. Immunol. Microbiol. Infect. Dis. 36, 233–239. Morgan, D.L., 1998. The Focus Group Guidebook. Sage Publications, Thousand Oaks, CA. Moro, P.L., Cavero, C.A., Tambini, M., Briceno, Y., Jimenez, R., Cabrera, L., 2008. [Practices, knowledge and attitudes about human hydatidosis in Peru]. Rev. Gastroenterol. Peru. 28, 43–49. Moro, P., Schantz, P.M., 2009. Echinococcosis: A review. Int. J. Infect. Dis. 13, 125-133. Sadjjadi, S.M., 2006. Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol. Int. 55 Suppl, S197–S202. Schantz, P.M., Wang, H., Qiu, J., Liu, F.J., Saito, E., Emshoff, A., Ito, A., Roberts, J.M., Delker, C., 2003. Echinococcosis on the Tibetan Plateau: prevalence and risk factors for cystic and alveolar echinococcosis in Tibetan populations in Qinghai Province, China. Parasitology. 127 Suppl, S109-20. Thys, S., Mwape, K.E., Lefèvre, P., Dorny, P., Phiri, A.M., Marcotty, T., Phiri, I.K., Gabriël, S., 2016. Why pigs are free-roaming: Communities’ perceptions, knowledge and practices regarding pig management and taeniasis/cysticercosis in a Taenia solium endemic rural area in Eastern Zambia. Vet. Parasitol. 225, 33–42. Torgerson, P.R., Devleesschauwer, B., Praet, N., Speybroeck, N., Willingham, A.L., Kasuga, F., . . ., de Silva, N., 2015. World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis. PLOS Med. 12, e1001920. Torgerson, P.R., Budke, C.M., 2003. Echinococcosis – an international public health challenge. Res. Vet. Sci. 74, 191–202. Van Kesteren, F., Mastin, A., Mytynova, B., Ziadinov, I., Boufana, B., Torgerson, P.R., . . ., Craig, P.S., 2013. Dog ownership, dog behaviour and transmission of Echinococcus spp. in the Alay Valley, southern Kyrgyzstan. Parasitology 140, 1674–1684. WHO, 2011. WHO | Report of the WHO Informal Working Group on cystic and alveolar echinococcosis surveillance, prevention and control. World Health Organization, Geneva. Yardley, L., 2000. Dilemmas in qualitative health research. Psychol. Health 15, 215–228.
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Based on the paper:
Taenia solium taeniasis/cysticercosis is an important neglected parasitic zoonosis prevailing in many developing countries. Many surveys carried out in Africa have identified the general lack of and use of sanitary facilities as the major risk factors for cysticercosis (Ngowi et al., 2004; Sikasunge et al., 2007; Assana et al., 2010; Pondja et al., 2010). Studies have demonstrated the positive effects of health education on the incidence of porcine cysticercosis in Tanzania (Ngowi et al., 2008) and on the prevention of epilepsy in Kenya (Wohlgemut et al., 2010). However, an increased use of latrines could not be demonstrated. Many sanitation projects, implemented by governments or NGOs, which led to the construction of latrines in rural areas, faced refusal of the communities to use them and adopt safe hygienic practices (Dellström Rosenquist, 2005; Phaswana-Mafuya and Shukla, 2005; Avvannavar and Mani, 2008) because the drives to motivate latrine adoption were often not identified and interpreted in messages and strategies to promote sanitation grounded in a given cultural context (Jenkins and Curtis, 2005). Unfortunately, in many African rural communities, open defecation practices were not adequately analyzed or taken into account before project formulation and implementation. Practicing open air Taenia Solium in Zambia Part 1 | 173 defecation is linked not only to the presence or absence of water or latrines, but also to social and cultural determinants (Kar and Chambers, 2008).
Improved latrine use as a control measure potentially has implications for many other sanitation-related pathogens (Esrey, 1996; Hunt, 2001; Murrell et al., 2005), such as soil-transmitted helminths (Bethony et al., 2006) and diarrhoeal agents (Prüss-Ustün et al., 2008). According to the World Bank, 2.5 billion people worldwide live today without access to improved sanitation and 1 billion of these people practice open defecation. In sub-Saharan Africa, 70% of the population still lack access to improved sanitation, thereby indicating the urgent need for improvement (World Bank, 2013). Currently, T. solium control programme managers need to understand why latrines are not used in endemic areas of Africa. Even though the significance of social and behavioural influences on the spread of human cysticercosis is known (Ngowi et al., 2008), culturally adapted control measures have not yet been implemented in endemic areas such as Zambia where the prevalence of T. solium cysticercosis in rural areas (in both human and pigs) is very high (Phiri et al., 2002; Sikasunge et al., 2008; Mwape et al., 2013, 2012).
The objective of this research was therefore to assess the communities’ perceptions, practices and knowledge regarding latrines in a T. solium endemic rural area in Eastern Zambia, in order to identify possible barriers to their construction and use and to propose, eventually, adaptations of strategies to overcome cysticercosis, and other sanitation related diseases locally.
4.2.1 Study area
Focus group research was conducted in a rural area (Kakwiya) in Petauke district in the Eastern province of Zambia. The Kakwiya Rural Health Centre (RHC) has a catchment population of 11,344 (Clinic headcount records). People practice subsistence farming, growing mostly maize and groundnuts primarily for home consumption and pig production is common. The main ethno-linguistic group in this area is the Nsenga, which have a matrilineal descent. The district was selected based on reports indicating high porcine (Sikasunge et al., 2008) and human cysticercosis prevalence, presence of a high number of free-roaming pigs, and reports of cysts
174 | C h a p t e r 4 observed in pigs slaughtered in backyards (Mwape et al., 2012). The Kakwiya catchment counts approximately 261 households and 138 individual toilets which is equivalent to an overall toilet coverage of 52.9%. The number of toilets varied quite markedly between villages (Table 4.1). There are no communal toilets as such. The sanitation facilities found in the study area were built following the simple pit latrine model. Completed, partially completed or abandoned, they generally consist of a pit dug into the ground, sometimes covered by a hygienic slab made from crushed stones and cement with a hole. Latrines were covered with a shelter (with or without a roof) and fitted simply with a sack or sometimes with a door.
Table 4.1 Latrine coverage in the study area (Kakwiya catchment). Latrine Number of Number of No. Village coverage Households toilets (%) 1 Kakwiya 97 56 57.7 2 Chifwiti 22 10 45.5 3 Kambawino 1 0 0.0 4 Mzeka 5 4 80.0 5 Chonjo 8 2 25.0 6 Lubangu 3 1 33.3 7 Komboka 5 3 60.0 8 Sikabi 1 0 0.0 9 Maseya 1 1 100.0 10 Nsamba 15 6 40.0 11 Misolo 63 40 63.5 12 Chawala 1 0 0.0 13 Wonzi 1 0 0.0 14 Chiludzu 3 0 0.0 15 Mulembelembe 11 8 72.7 16 Chilima 1 0 0.0 17 Chingolo 2 0 0.0 18 Kalikeka 1 0 0.0 19 Maloba 9 2 22.2 20 Chisenga 3 2 66.7 21 Mutambanjeleka 8 3 37.5 Total 261 138 52.9 Taenia Solium in Zambia Part 1 | 175
4.2.2 Study design
Twenty-one focus group discussions (FGDs) were conducted totaling 172 participants including 56 men, 58 women and 58 children (below the age of 18) from seven villages (Table 4.2). The seven villages were randomly selected from villages around the health centre because of its central position. They were not included in recent biomedical surveys to avoid information and sensitisation biases. Separate FGDs were held with men, women and children in each village since these groups have different perceptions and behaviours regarding sanitation (gender dependent) (Avvannavar and Mani, 2008). In addition, working with heterogeneous groups is likely to hamper the quality of the data (Morgan, 1998; Grudens-Schuck et al., 2004). For children, the FGDs were gender-mixed because, unlike adults, they were able to speak freely regardless of age and gender.
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Table 4.2 Characteristics of the focus group discussions. FGD Number of participants Village Category No. Male Female Village 1 Wonzi Children 4 4 2 Wonzi Women 8 24
3 Wonzi Men 8
4 Chimphanje Children 4 5 5 Chimphanje Women 8 25
6 Chimphanje Men 8
7 Sikalinda Children 4 4
8 Sikalinda Women 8 24 9 Sikalinda Men 8
10 Nyazowani Children 4 4
11 Nyazowani Women 8 24
12 Nyazowani Men 8
13 Chimanja Children 5 4 14 Chimanja Women 8 25
15 Chimanja Men 8
16 Chiludzu Children 5 3
17 Chiludzu Women 8 24 18 Chiludzu Men 8
19 Mtuna Children 4 4
20 Mtuna Women 10 26
21 Mtuna Men 8
To ensure the validity of the data collected, FGDs have been conducted until reaching data saturation (no additional data were found leading to more information related to our research questions) from the seven different villages and from the three different subgroups. Taenia Solium in Zambia Part 1 | 177
4.2.3 Data collection
The data collection took place from July to August 2010. Each FGD consisted of approximately 8 participants. Participants were selected from the villages based on their availability and willingness to participate. The FG discussion guide was pre- tested and fine-tuned in one FGD performed with male participants from a village outside the study area. Three facilitators (a female nurse, a male environmental health technician and a male community health volunteer), all familiar with the Nsenga language, were identified and trained to moderate, observe and record the FGDs. The training consisted of a two-day course during which they were briefed on the study objectives and on FGD moderation skills. Facilitators switched roles for each discussion. All the FGDs took place at the Kakwiya RHC because of its central geographical location and practical aspects. To avoid biases related to the fact that the venue was not neutral in terms of health, the first set of questions was about general pig management.
The average duration of the discussions was about an hour. The following topics were covered: the perception of pig breeding in the communities, knowledge and perceptions of taeniasis/cysticercosis infection and related risk behaviours such as people’s latrine perception and reasons for not using latrines (defecation practices, latrine management, building responsibility, socio-cultural obstacles); and opinions on control measures. All discussions were recorded on a video camera to facilitate the transcription of a discussion involving several individuals at the same time. Encouraged by our key informants, the use of a video camera was pre-tested and did not seem to be intrusive or affecting the discussions. The facilitator was always assisted by a reporter. To ensure the good implementation and follow up of the study, the main researchers (Séverine Thys & Kabemba E. Mwape) attended every discussion.
In this paper, only results pertaining to people’s latrine perception, reported practices and factors that lead to lack of use of these sanitary facilities are presented and discussed.
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4.2.4 Data processing and analysis
The FGDs were transcribed and translated into English by two research assistants and two researchers who took turns in both tasks. To improve interpretation reliability, the written transcripts were reviewed independently by the two same researchers before accepting them for analysis. The analysis of the transcriptions and the notes taken during the FGDs was supported by the NVivo 8® software (QSR International Pty. Ltd., Melbourne, Australia, 2008), which allows to classify and sort data; examine relationships and trends in the data. The major themes were separately identified through coding by the same two main researchers of the study following an inductive approach. Any differences were discussed until consensus was reached.
4.2.5 Ethical considerations
Ethical clearance was obtained from the University of Zambia Biomedical Research Ethics Committee (003-02-10) and from the Ethical Committee of the Antwerp University Hospital in Belgium (10 03 3 704). Further approval was sought from the local authorities and community leaders before commencement of the study. Finally, before the start of each FGD, permission was sought from the individual subjects to enter the research and to video record the discussion. Written informed consent was obtained from each participant and from parents (or guardians) for children under 18 years old. Participation in the discussion was voluntary and no names nor pictures were recorded in the transcripts. Questions were appropriately phrased to avoid embarrassing people and also to tackle sensitive issues or taboos. FGDs with children took place after school hours.
The results highlight the different themes that emerged in the analysis. To reflect as much as possible what was expressed in the discussions, the order used to present the themes in each sub-sections reflects the level of importance given by the participants to these topics (going from a strong to a weaker consensus). No significant differences were observed between villages (very homogeneous), we indicate when the main ideas were mentioned across all the FGDs and where consensus or differences arose the most among the three different categories of FGDs Taenia Solium in Zambia Part 1 | 179 conducted (men, women and children). Results are illustrated with anonymous quotes, selected on the basis of their representativeness, appropriateness and revealing quality.
Table 4.3 List of themes and sub-themes per topic (5) according to men, women and children groups.
A. Latrine availability Topic 1: Perceived Sub-themes Men Women Children presence/absence of latrines*
No latrines available No latrines at home (1) V Not yet completed V No latrines in the village V V Latrines not shared V No latrines for visitors V V V No latrines in the field V Latrines available Latrines shared (3) V V Not every household V V Latrines at home (2) V V V Few latrines in the village V V Many latrines in the village V
Topic 2: Obstacles to Sub-themes Men Women Children build latrines* Men’s responsibility not Men’s laziness V assumed (1)
When a man gets married V Difficult for unmarried women V Men too drunk V Public use (other V V V latrines available) (2) Poverty (3) V V V
Not if not forced by law V
How to build is unknown V No people available to V help Not enough education V about the goodness of latrine
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Not a habit V V V
B. Latrine use Topic 3: Open Sub-themes Men Women Children defecation VS Latrine use* Open defecation (1) V Latrine use V Topic 4: Arguments in Sub-themes Men Women Children favor of the use of latrines* Participate to good Protect pigs from eating feces V V V hygiene (1) Not washing hands after open defecation V A toilet is more hygienic (less dirty) V Not effective if not every household have V V a toilet Prevent flies to contaminate food (with V V V human feces) Discard all the bad things from the V intestines in one pit Prevent diseases (2) V V V More comfortable (3) Not being disturbed by pigs pushing you V V before finishing When you have diarrhea V V Less far than going to the bush V V When it's raining V More visual privacy When the bush has been burnt (no V V leaves) Less risk to meet relatives V Feeling of freedom if the taboo is V respected When it's night V Give dignity V V Nothing good about open V defecation Topic 5: Arguments Sub-themes Men Women Children NOT in favor the use of latrines* Taboos (1) V Not building one latrine V per house (2) Lack of privacy (3) Cannot hide yourself (more shy, feel not V V free) Taenia Solium in Zambia Part 1 | 181
Latrine not well made V V Be careful to not let blemish after use V Risk to see nakedness V Too nearby village V Less convenient Washing hands is not easier V V V Create a queue V V Easier to head to the bush V Does not allow to check for worms V Need to carry things to clean the toilet V Not a habit V V Not comfortable Scary for children (fall in the pit) V Be in contact with dirt (diseases) V V V Flies V Smell V Punctual absence of When working in the field V V latrines When emergency V When traveling V When private use (lock at V the door) Maintenance difficult 100% cleanness is impossible V Need to often replace the door V Pit is quickly full V No more food for pigs V V How to use latrine is V V unknown Promotion of latrines V failed Men enjoy more open V defecation (1) – (2) – (3): The three first themes or sub-themes which obtained the most important consensus among the 21 focus groups (indifferently from the group types) * For each of the five topics, the themes and sub-themes are ordered from the most mentioned to the least mentioned ones, indifferently from the groups. V: A check indicates for which of the groups (men, women, children) a higher consensus was expressed regarding each of the themes and sub-themes identified compared to the other groups.
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4.3.1 Latrine availability
4.3.1.1 Topic 1: Perceived presence and absence of latrines
In this section, we describe how people perceived the presence and absence of latrines in their village in order to identify factors that explain latrine availability.
People generally referred as much to situations with as without the presence of latrines. On the overall, participants agreed on: 1) the general absence of latrines at home (no latrines at home, no latrines for visitors, not yet completed), especially women; 2) the presence of latrines in some homes (latrines at home, shared and not shared with neighbours) (acknowledged by all categories); 3) that latrines are public among neighbours, a perception mostly shared among men and women groups (Table 4.3). The distinction between having a latrine at home and the presence of latrines in the village revealed a distinction between private and communal uses of sanitation facilities.
Participants further stated that a household with a latrine had dignity and respect as visitors, passersby or guests unaccustomed to using the bush, could easily be allowed to use the facility. A latrine therefore was a necessary feature of hospitality. This was especially highlighted by people whose household was situated in close proximity to the roads:
“There is dignity especially for visitors. When a visitor comes at home and asks to use a latrine, you easily point it out. That person may be happy not to go in the bush. There is respect at a home if there is a latrine”. (Focus group\Men Mtuna village)
“… Having a toilet gives one high sense of respect and dignity” (Focus group\Men Wonzi village)
Conversely, at village level, the presence of latrines (latrines shared with neighbours, few and many latrines in the village) was more mentioned than latrine absence (no latrines in the village, not in the field and not shared with neighbours), except among children FGDs who pointed out that if you need to defecate while you are working in the field, you do not have other options that doing it in the open. Taenia Solium in Zambia Part 1 | 183
Even if latrines were mentioned to be available in the community, men and women stated that there were few of them, and that sharing these facilities was a common practice.
“[…] But you find that in the village there are maybe five or six toilets and everybody rushes there. You cannot stop them. The toilet becomes for common use and therefore the traffic to the toilet is very high”. (Focus group\Men Chiluzu village)
Finally, even if very few participants mention that some of the latrines were incomplete (Table 4.3), They expressed a certain willingness to build latrines, although it was not often considered a priority.
4.3.1.2 Topic 2: Obstacles to build latrines
From all the 21 FGDs, eight obstacles (Table 4.3) were identified as contributing to the lack of latrines. Because the Nsenga observe traditionally a matrilineal descent, a newly married couple lives in the wife’s relative’s household and the custom implies that when a man gets married, he ought to build his own latrine because of the taboos of a man sharing a latrine with his parents-in-law (see paragraph on taboos). In this cultural context, the responsibility of latrine construction clearly belongs to men but a constraint mentioned by the participants was that men did not consider the construction of a latrine for themselves as a priority. This lack of motivation was mostly explained (mainly by women) by the fact that some men were lazy, or preferred to spend time drinking alcohol.
The existence of other latrines in the village was the second consensual argument raised by the participants to explain the non-prioritisation of latrine construction. Indeed no taboos were observed for sharing latrines with people from another household or with non-relatives. Participants commonly stated that it was also not well accepted that the toilet owner refused access to other community members. Refusal could create conflicts or have negative consequences on social relations. In addition, some male and female participants recognised that refusing access to neighbours would reduce all the benefits of having a latrine (prevent diseases, prevent pigs from eating human feces, prevent contamination of kitchen utensils) by forcing people to defecate in the bush or near their homes. The hesitations expressed about the placement of locks on latrine doors and its implications for the sanitation
184 | C h a p t e r 4 of the village reflected the tension between private use (leading to eventual envy, jealousy, no more benefits for the community health) and communal use (leading to increased latrine cleaning and maintenance, rapid filling of the pit, sharing the cost and responsibility). In both kinds of use, the risk of disrupting interpersonal relations was a potential obstacle to start constructing latrines. As expressed by one man participant:
“… you would find that you are a newly married couple. It is just you and your wife only, you have no children, and then you decide that instead of me going to the bush let me build a toilet. Once you finish building the toilet you realise that your neighbour has a large family. Then you think that if I allow these people to use my toilet it will soon be full so you look for a lock and start locking it like in town. But after some time you realise that these pigs we keep will eat their human waste since they do not have a toilet and affect me as well. You stop locking your toilet.” (Focus group\Men Chiluzu village)
A third obstacle mentioned was the lack of means to construct a latrine. This was an important constraint and commonly identified in the three groups. It was stated that some people could not afford to build a latrine of good quality materials, according to the local standard criteria of a latrine (roof, proper door, walls high enough,…) pursuing the gain of visual privacy. The physical appearance of the latrine had a bearing on whether it was used or not regarding the level of privacy offered (see latrine perceived advantages). However, local materials were often not of sufficient quality.
A fourth and fifth constraint highlighted in our study were the lack of knowledge on how to build latrines and the lack of awareness on their advantages for some participants. They pointed out that educating people about the benefits of a latrine would eradicate all the misunderstandings or erroneous conceptions. Men insisted more on the need of more “persistent” and “sustained” sanitation education campaigns, women made more reference to the hygienic benefits that campaigns would result in. The 6th reason described by some women is that unmarried women were facing great difficulties to have latrines built since the construction of latrine is a man’s responsibility.
“Those hired persons refuse. I started a long time ago, since my latrine collapsed. I am not used to be frequently going in the bush. I usually start to construct another Taenia Solium in Zambia Part 1 | 185
on the moment I realise the one I am using has become half full. However, nowadays the hired men refuse; you may have money and tender it. They would say, “Why don’t they get married so their husband can do it for them?” (Focus groups\Women Mtuna village)
Finally, the last obstacle raised to latrine construction was that it was simply not yet considered as a habit to defecate in a toilet.
4.3.2 Latrine use
4.3.2.1 Topic 3: Latrine use versus open defecation
Even when latrines are present, going to the bush in order to defecate in the open is a common practice, and a culturally accepted norm in the area. It appeared that men were the ones enjoying more to defecate in the open (see obstacles to use latrines) than others. As a general finding about pros and cons of latrine use, more comments against than in favor were mentioned during the FGDs.
4.3.2.2 Topic 4: Arguments in favor of the use of latrines
Participants manifested a strong consensus that latrine use contributed to a better hygiene and prevents diseases. Additionally, greater comfort, dignity and increased privacy were mentioned. When exploring the benefits of sanitation within communities and households, the last common argument shared, especially among women was that “there is simply nothing good about open defecation” (Table 4.3).
Latrine use contributes to good hygiene
All groups and especially women considered that the presence of a latrine ensured hygiene in a household mainly because it prevented pigs from eating human feces, and avoided them contaminating kitchen utensils left on the ground with dirt and feces that could bring diseases (see next section).
Men and women also pointed out that, as long as all households had no latrine, no benefits would be realised, as many would still be openly defecating.
Another common perceived advantage was the prevention of food contamination by flies, as by using latrines, all human feces would be gathered in one pit instead of being
186 | C h a p t e r 4 everywhere in the open. According to some comments from children, latrines were the place where you could “discard all the bad things from the intestines”.
“… Because after eating the food we need to get rid of the waste material so if we have a toilet we do all that in the toilet.” (Focus group\Children Nyazowani village)
Latrine use prevents diseases
It appeared that participants connected the use of latrines with their own improved health but not always straight line.
“We prevent diseases, since pigs can’t get into the toilet to eat our feces.” (Focus group\Women Chimphanje village)
They alluded to the fact that latrines prevented diseases in general and some specific diseases as cholera or dysentery by preventing pigs, flies and unwashed hands to contaminate food with human feces. There were linkages with the risk of diarrhea and HIV transmission only when participants referred to the pigs’ habit of eating feces of sick persons.
“If a pig eats feces of an AIDS patient and they come to feed from your plates, and then the other person without AIDS comes to feed from that plate without washing it, he will contract the disease.” (Focus groups\ Men Sikalinda village)
Latrine use is more comfortable, provides more privacy and increases dignity
In the FGDs, there was a strong consensus, especially among women, that “one advantage of using latrines was not being disturbed by pigs pushing you before finishing”. Adults stated that latrines were more often used when someone was suffering from diarrhea. Afraid of not reaching the bush on time and be embarrassed in front of fellows, they would rather use latrines (indicating a matter of comfort and convenience rather than family or personal health protection).
W1: “Another disadvantage of not having a toilet is when you have diarrhea, it is embarrassing and difficult… and you can't go to the neighbours, worse still it may be too late to get to the bush. When you are in the bush you find that a pig is even waiting for you to finish, I can’t manage that”.
W2: “Worse if you live in the middle of the village, you’ll mess yourself up before you even get to the bush.” (Focus groups\Women Sikalinda village) Taenia Solium in Zambia Part 1 | 187
Mainly for men, using latrine offered a greater comfort when they were situated closer than the bush and when it rained. It was also very important for many to avoid being seen defecating in the open, especially men, by the opposite sex or by their in laws:
“The other advantage of having a toilet is that sometimes you run to the bush to go and help yourself… then you find that your mother in law is just squatting a few meters away from you. Because you are in such a hurry you do not see her and you help yourself but even if she has finished she will not leave until when you leave. In the case of a toilet at home people will see that a person has entered the toilet and nobody will come until when you are through posting your mail. That is when they also can write their letters and come to post them.” (Focus groups\Men Mkopeka village)
Another major factor in favor of latrines, mentioned by participants in the context of privacy, was the seasonal availability of good defecation sites around the village. In the dry season, the bush was usually burnt for agricultural purposes, making them not dense and high enough anymore to hide villagers who wanted to defecate in the open. Some participants, mostly males, revealed that it was quite more convenient to use latrines at night. As latrines did not always have a proper door, using it at night will avoid others to see you.
“…You know that our toilets do not have proper doors like those in town so during the day if you go in the toilet children may find you squatting helping yourself. But in the night it is better no one can see you.” (Focus group\Men Chiluzu village)
At night, latrines presented the additional advantage of reducing the risk of being exposed to hazards in the bush. Along with the seeking of more privacy, participants further stated that the use of latrine gave more dignity in the sense that you could hide from the others when defecating:
“Toilet should be one of dignity, not going to the bush” (Focus group\Women Mtuna village)
4.3.2.3 Topic 5: Obstacles to use latrines
Thirteen reasons were identified for not using latrines (Table 4.3) in order to facilitate the flow of the reading, some themes are grouped together. The greatest consensual
188 | C h a p t e r 4 reasons among all FGDs that arise were: 1) the taboos related to sanitation practices, 2) the fact that not all households had a latrine and 3) the fact that latrines did not offer enough privacy resulting in a loss of dignity for the user. For women and children, the main factor that leaded to not using latrines was the unavailability of the facilities, while for men traditional taboos seemed to be the central issue.
Latrine use entails cultural taboos
In general when the different socio-cultural obstacles for the use of latrines were addressed, most of the comments were made by men. This showed that men were much more concerned about the respect of taboos than the other two groups.
Moderator: “What is a bad thing that can arise from people sharing a latrine, even for example with an in-law?”
M1: “You may meet each other at the latrines when both are coming from different locations as you know how the intestines work, for example when an in-law is coming from the field and may be unaware that the in-law had gone to the latrine” M8: “You may not be aware of it”
M1: “When you meet each other at the latrines, it becomes embarrassing”
M8: “It is like you have been undressed” (Focus groups\Men Mtuna village)
As such, other people, especially children, are not allowed to see their parents or adults go to the latrine. In the study area, traditional taboos meant that the head of household (father) could not share the same latrine with his mother-in-law, his children-in-law, older children (adults) of his own household, his grown-up daughters and his younger children when the risk to be seen was too high or when young children will use the latrine just after their father. Often, men went to the bush pretending to go to the field, gather firewood or hunt mice (a common delicacy in the region) not to be seen entering a latrine by children.
“What we are saying is true and still happens, where you see a man picks up his axe on the shoulder and goes to the bush pretending that he is going to fetch fire wood and yet he is going to help himself, especially now that the grass has been burnt. You come back carrying a piece of fire wood just to hood wink the children when your main purpose was to go to the toilet”. (Focus group\Men Chiluzu village) Taenia Solium in Zambia Part 1 | 189
It seemed that these taboos were strongest between in-laws and in particular between mothers and sons-in-law.
“I would be right to say we do not use the toilet the way we should because here we have a lot of respect for each other. Our culture does not allow us to use the same toilet with your grown-up daughters, son or daughter-in-law, mother-in-law and all other people. What has killed us in the villages are these cultural norms which we have clung to for so long. Our friends in town find nothing wrong with all this. They all use the same toilet in the house.” (Focus group\Men Chiludzu village)
Bypassing these prohibitions was considered as a lack of respect and decency similar to being seen undressed. For this reason, some of the participants suggested having two latrines at the same household. When asked if they had no problems being seen going to the latrine in full view of their daughter in-law, a male participant stated:
“Yes, it is a problem, because your daughter in-law would find that may be you miss the hole and shit on the side or she would find a very big heap and start saying this man really shits. In our communities that does not show respect. It is always a good idea in that case to have two toilets.” (Focus group\Men Mkopeka village)
On the other hand no taboos seemed to be observed between parents and very young children, between wife and husband, between women and neighbour’s children, in town and with neighbours as they often did share latrines in the community. Sons were freer to share the same latrine with the head of the family than daughters. Fewer taboos were observed between people of the same gender. Although the origin of those taboos and reasons to observe them were not very explicitly explained in the discussions, in one way or another all the further arguments against the use of latrines developed in this section were linked to the importance of respecting those sanitation taboos. Compounded by the existing taboos, women considered that if not every home owns at least one latrine, the practice of open defecation will not end and no benefits will be realised. Despite the men also stating this and acknowledging the benefits that would arise from the use of latrines, they were still the major obstacle towards the construction of more latrines (see above).
Latrine use causes a lack of privacy and is less convenient and comfortable
At the first sight, this sub-section can look contradictory with the advantages foreseen earlier by the participants regarding the use of latrine. However when participants
190 | C h a p t e r 4 were asked why people did not use latrines, some responded that most of the available latrines were not in a very good state. The walls were too low, they lacked a roof and a lockable door (many only had a cloth or a sack as a door) thus compromising privacy. This lack of privacy mainly mentioned by men, included the fear of leaving dirt after the latrine use as well as the risk to see nakedness. They also mentioned that latrines were often built in the centre of the village, which prevented people from using them because they would be seen entering or leaving them.
The convenience perception about the use of latrines was not unanimous and presented also different opinions. It appeared that for some women and men the use of latrines was not necessarily more convenient than open defecation to fulfill its benefit of improving hygiene. First, because it was not easy to wash hands after the use of the latrine (no water supply nearby) and secondly, because it was not convenient to carry material to clean the latrine.
For some men especially, the few latrines available created quite rapidly a queue, which was not convenient in case of an urgent need (e.g. diarrhea). In addition, the queue led people know that you need to defecate (risk to be seen). Complete cleanness of such public latrines, needed to fulfill the required social norms of privacy, convenience and comfort, was also impossible to achieve due to maintenance difficulties. The most important reason was to be exposed to dirt, bad smell and flies. It was also mentioned to be a scary place for children (dark, big hole wherein they could fall,…). According to some children, it was simply easier to go to the bush to relieve oneself also because it was more difficult to find a latrine when people work in the fields or when they were travelling. One woman mentioned that the way the latrines were built (pit latrine) did not allow checking for worms and could delay the identification of a parasitic infection. Another inconvenience to use latrine according to some men and children, was that it did not allow pigs to feed on their feces. Open defecation was a common and affordable solution for the pig’s owner to face feed shortage. Finally, more children than women admitted that using latrines was simply not a habit and that men from the older generation manifested a strong reluctance to build latrines.
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Limited knowledge on latrines
If preventing diseases was an argument in favor of the use of latrines, it was not always evident for the participants that adequate maintenance was one of the most important determinants to ensure the health benefit of a latrine. According to the men it was difficult to teach children how to use a latrine properly. Also, equipment sometimes freely distributed by sanitation programmes was not always properly used.
“In addition there was indeed a programme which was making stand plate for the toilet and giving them to people for free. Some have stored them in their houses and some are using them to stand on them when they are taking a bath. They do not use them for the purpose they were intended for. There is indeed a need for sustained education in this area of our day living.” (Focus group\Men Chiluzu village)
Mainly men considered that latrine promotion failed, as it did not convince them to construct and use latrines properly.
Considering the results presented in this manuscript, it is clear that the transmission of T. solium can easily continue in this very suitable fecal contaminated environment where few infrastructure for safe excreta disposal are available and correctly built or used and therefore allowing free roaming pigs to maintain the lifecycle in such endemic area. While poverty may be a contributing reason for the lack of latrines in many communities, it does not explain why some people continue to practice open defecation long after their community has been provided with water points and learned about latrines and hygiene practices (Dittmer, 2009). Choosing latrines means changing defecation practices and because sanitation behaviours tend to be strongly culturally conditioned, we chose to discuss our results mainly through user lenses (Jenkins and Curtis, 2005) and socio-cultural lenses (Douglas and Wildavsky, 1982).
Like Jenkins and Curtis (2005) in Benin, we found among the arguments in favor of using latrines, drives related to prestige (gaining more respect and dignity from visitors), to well-being (better hygiene by protecting pigs from eating feces, more comfort by not being disturbed by pigs pushing you before finishing, more visual
192 | C h a p t e r 4 privacy) and situational drives (when it’s raining, when bush has been burnt, when you have diarrhea). But from a consumer perspective, these authors also demonstrated through their model of motivation for latrine adoption in rural Benin that at least one drive is needed (among the 11 that they found) to motivate real changes in sanitation behaviour as long as barriers do not suppress the expression of this specific drive (Jenkins and Curtis, 2005).
Out of our FGDs, several obstacles for building and using latrines were identified such as sanitation taboos (avoiding sons and mothers-in-law to share the same latrines), the lack of privacy (latrines not well built, the queue) and the lack of comfort (too scary for children, flies, smell). It means that in our studied context the different obstacles identified would need to be addressed first in order to arise sufficient intensity for positive drives to be translated in concrete action taken by the target population. Complementary of Jenkins and Curtis’ model, Avvannavar and Mani’s conceptual model of people’s approach to sanitation (Avvannavar and Mani, 2008) can let us better understand the interplay of socio-cultural factors that determine how people take care of their primal urge.
In the category “culture” and “fear & superstition”, their model offers us the opportunity to discuss the taboos we identified related to sanitation practices. For the authors, attitudes and beliefs about revulsion to feces vary between cultures. Examples are numerous in Africa. In the Akan culture (Ghana) for example, the word “shit”, is as taboo as the thing itself and people when going to the bush to defecate, need to wear a blinder pretending that they will not be seen if they see nobody (Van der Geest, 1998). In Uganda, sharing latrines with in-laws is a taboo and the use of latrines could affect women’s fertility and also cause miscarriage (Robert and Akiiki Kusiima, 1998). In the Eastern Cape Province of the Republic of South-Africa, human feces were found in the bush because people were afraid to share latrines to avoid being bewitched (Phaswana-Mafuya and Shukla, 2005). However our results demonstrate that the type of descent, matrilineal or patrilineal, is also an important factor that has a significant influence on the sanitation practices of a community.
In our study, although no taboos seem to be observed between wife and husband, between women and neighbour's children, in town or with neighbours, a man could not share the same latrine with his mother-in-law, his children-in-law, older children Taenia Solium in Zambia Part 1 | 193
(adults) of his own household, his grown-up daughters, his younger children. Similar taboos have been reported in a number of other African communities, reflecting important social norms. In Eastern Cape Province (RSA), for instance, stakeholders stated that people prefer to defecate in the bush because sharing a latrine as a father- in-law with his daughter-in-law is perceived as a disgrace (Phaswana-Mafuya and Shukla, 2005). In the case of a sanitation programme (Community-Led Total Sanitation programme, CLTS) introduced in a Kenyan district, the taboo for a father- in-law’s feces to mix with those of his daughter(s)-in-law was also described resulting to gender-segregated open defecation sites in the forests (Bwire, 2009).
The origin of the taboos we identified and reasons to respect them are not very explicitly explained by the participants. It seems however logical in a matrilineal society to observe very strict proscribed behaviours towards the maternal in-law’s in order to limit contact and ensure respect. Mary Douglas in “Purity and danger: An analysis of the concepts of pollution and taboo” explained that the father in the matrilineal Trobrianders and Ashanti is credited with being an involuntary source of danger; he is an intruder (Douglas, 1966). If we look at the previous examples from patrilineal societies, the reported latrine practices taboos (Father and daughter-in- law) are in fact simply reversed in our setting (Mother and son-in-law) because we are in a matrilineal society. Furthermore, being in a matrilineal or patrilineal system allows us to better understand firstly, the gender division of tasks about latrine construction and secondly, the social norms in such societies in terms of privacy, both having a strong influence on why latrines are not built or not used.
Seeking privacy, in general and from in-laws in particular, seems to be the main underlying motivation for people to use or not latrines. Using latrines when natural vegetation does not suffice to hide in the bush contextualises and highlights the importance given to privacy and the fear to be seen going or openly defecating, especially by relatives. Embarrassment and shame that occur if being seen is the expression of a transgressed norm that underlies a number of taboos related to the matrilineal descent of this community. The perceived benefits of a latrine depends on the way it has been built and its construction is in turn strongly linked to the respect of socio-cultural sanitation practices. In our setting the benefit would be not to be seen (privacy) in order to feel free, less shy and respectful towards cultural taboos.
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However, the actual sanitation situation entails no or badly constructed latrines that do not offer enough privacy (e.g. no proper door, too small walls, no roof, rickety superstructures) and therefore also contributes to why latrines are not used. Avvannavar & Mani (2008) consider that the human tendency to seek privacy is the modified animal behaviour attributed to the deep primal territorial tendencies. In our research, we can apply this theory as such: “By not willing to be seen or to see you when you are defecating” could be another way for men in a matrilineal system to mean that “by not defecating in the same latrine of my mother-in-law, I show respect about her territory as I am a stranger in her family”.
In general, the topic of sanitation was mostly developed by female participants. Women were more spontaneous and free to speak about latrine issues and related sanitary behaviours. The particular social, economic and political structures in most African contexts make women more concerned about sanitation and domestic duties than men (Drangert, 2004) who carry out construction and maintenance of facilities according to the gender division of tasks. That explains why the common practice in the water and sanitation sector is to involve women, not only as a target group, but in the organisation of activities at the local level (Cairncross et al., 2005). In our study however, resistance to abandoning open defecation practice was mainly expressed by men. As the role of latrine construction belongs to male participants, addressing men’s knowledge and beliefs could benefit sanitation programmes in many ways. If men do not see latrine construction/use as a priority or if they do not know how to build it, latrine coverage and use will not raise. In this specific situation, not getting married can be a handicap for women to have their own pit latrine built.
In regard to sanitation taboos, in certain cases, taboos themselves can be used as arguments in favor of the use of latrines in order to facilitate even more their respect. In the CLTS study in Kenya for instance, where the targeted communities are observing quite similar cultural norms and defecation practices as in our study, the facilitators were able to break one of the defecation taboos by showing that a pit latrine located within the homestead will complicate the task for an intruder who sought to bewitch others by accessing their intended victim’s feces (less discrete, difficult to dig up the feces) (Bwire, 2009). Taenia Solium in Zambia Part 1 | 195
The existing challenges of cysticercosis control in endemic regions require a “people- centred” preventive approach that addresses both the perception of the disease and its management. Control strategies should also be directed to the patterns of people’s behaviour associated with the phases of transmission of the disease (Hesse et al., 2012). In this specific study we focused on people’s perceptions, knowledge and reported behaviours regarding the use and the construction of latrines.
Out of our findings, several entry points for promoting the use of latrines were identified and discussed. Seeking privacy and taboos were both identified as the key factors influencing the possession and use of sanitation facilities. These findings reinforce why latrine promotion messages should not only focus on health benefits. Some taboos can be explained by the type of descent (matri- or patrilineal). By acknowledging that the descent is also a factor that influences sanitation behaviours and regulates a number of norms and practices, we can more easily anticipate the type of taboos that could entail the adoption of hygienic practice related to sanitation.
A concrete proposition that could be made is to start building per homestead gender specific latrines instead of household specific latrines, each of them located in two different places to respect privacy. But unless programme planners are not totally convinced of the necessity to direct interventions not only at women but at men as well and focus also on men issues (practices, beliefs and knowledge), latrine building and use will not be efficiently promoted. Our results also stress the importance of anthropological studies for an in-depth understanding of sanitation practices within particular contexts in order to enhance the design of adapted interventions. Finally, going beyond medical questions and risk factors could be an interesting complementary approach to identify incentives that will foster people’s change, in order to co-design interventions with the community members themselves.
Assana, E., Amadou, F., Thys, E., Lightowlers, M.W., Zoli, A.P., Dorny, P., Geerts, S., 2010. Pig- farming systems and porcine cysticercosis in the north of Cameroon. J. Helminthol. 84, 441–446. Avvannavar, S.M., Mani, M., 2008. A conceptual model of people’s approach to sanitation. Sci. Total Environ. 390, 1–12.
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Bethony, J., Brooker, S., Albonico, M., Geiger, S.M., Loukas, A., Diemert, D., Hotez, P.J., 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 367, 1521–1532. Bwire, B., 2009. Breaking shit taboos: CLTS in Kenya. In: Plan Kenya Country Programme Progress Report. Plan International Kenya, Nairobi, pp. 91-96. Cairncross, S., Shordt, K., Zacharia, S., Govindan, B.K., 2005. What causes sustainable changes in hygiene behaviour? A cross-sectional study from Kerala, India. Soc. Sci. Med. 61, 2212–2220. Dellström Rosenquist, L.E., 2005. A psychosocial analysis of the human-sanitation nexus. J. Environ. Psychol. 25, 335–346. Dittmer, A.W., 2009. Towards Total Sanitation: Socio-cultural barriers and triggers to total sanitation in West Africa. WaterAid Rep., 12 pp. Douglas, M., 1966. Purity and Danger, an Analysis of Concepts of Pollution and Taboo. Frederick A. Praeger, New York. Douglas, M., Wildavsky, A.B., 1982. Risk and Culture: An essay on the selection of technical and environmental dangers. University of California Press, Berkeley. Drangert, J.-O., 2004. Norms and Attitudes Towards Ecosan and Other Sanitation Systems, EcoSanRes Publications Series. Stockholm Environment Institute. Esrey, S.A., 1996. Water, Waste, and Well-Being: A Multicountry Study. Am. J. Epidemiol. 143, 608–623. Grudens-Schuck, N., Allen, B.L., Larson, K., 2004. Methodology Brief: Focus Group Fundamentals. Iowa State University Extension. Hesse, A.A.J., Nouri, A., Hassan, H.S., Hashish, A.A., 2012. Parasitic infestations requiring surgical interventions. Semin. Pediatr. Surg. 21, 142–150. Hunt, C., 2001. How Safe is Safe? A Concise Review of the Health Impacts of Water Supply, Sanitation and Hygiene. WELL study produced under Task 509. WELL, Leicestershire. Jenkins, M.W., Curtis, V., 2005. Achieving the “good life”: Why some people want latrines in rural Benin. Soc. Sci. Med. 61, 2446–2459. Kar, K., Chambers, R., 2008. Handbook on Community-Led Total Sanitation. Plan International, UK. Morgan, D.L., 1998. The Focus Group Guidebook. Sage Publications, Thousand Oaks, CA. Murrell, K.D., Dorny, P., World Health Organization, International Office of Epizootics, Nations, Food and agriculture Organizations of the United Nations, 2005. WHO/FAO/OIE guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. OIE (World Organisation for Animal Health). Mwape, K.E., Phiri, I.K., Praet, N., Muma, J.B., Zulu, G., van den Bossche, P., . . ., Gabriël, S., 2012. Taenia solium infections in a rural area of Eastern Zambia - A community based study. PLoS Negl. Trop. Dis. 6, 1–9. Mwape, K.E., Phiri, I.K., Praet, N., Speybroeck, N., Muma, J.B., Dorny, P., Gabriël, S., 2013. The Incidence of Human Cysticercosis in a Rural Community of Eastern Zambia. PLoS Negl. Taenia Solium in Zambia Part 1 | 197
Trop. Dis. 7, 1-7. Ndimubanzi, P.C., Carabin, H., Budke, C.M., Nguyen, H., Qian, Y.J., Rainwater, E., . . ., Stoner, J.A., 2010. A systematic review of the frequency of neurocyticercosis with a focus on people with epilepsy. PLoS Negl. Trop. Dis. 4, 1-17. Ngowi, H.A., Carabin, H., Kassuku, A.A., Mlozi, M.R.S., Mlangwa, J.E.D., Willingham, A.L., 2008. A health-education intervention trial to reduce porcine cysticercosis in Mbulu District, Tanzania. Prev. Vet. Med. 85, 52–67. Ngowi, H.A., Kassuku, A.A., Maeda, G.E.M., Boa, M.E., Carabin, H., Willingham, A.L., 2004. Risk factors for the prevalence of porcine cysticercosis in Mbulu District, Tanzania. Vet. Parasitol. 120, 275–283. Phaswana-Mafuya, N., Shukla, N., 2005. Factors that could motivate people to adopt safe hygienic practices in the Eastern Cape Province, South Africa. Afr. Health Sci. 5, 21–28. Phiri, I.K., Dorny, P., Gabriel, S., Willingham, A.L., Speybroeck, N., Vercruysse, J., 2002. The prevalence of porcine cysticercosis in Eastern and Southern Provinces of Zambia. Vet. Parasitol. 108, 31–39. Pondja, A., Neves, L., Mlangwa, J., Afonso, S., Fafetine, J., Willingham, A.L., . . ., Johansen, M.V., 2010. Prevalence and Risk Factors of Porcine Cysticercosis in Angonia District, Mozambique. PLoS Negl. Trop. Dis. 4, 1-5. Prüss-Ustün, A., Bonjour, S., Corvalán, C., 2008. The impact of the environment on health by country: a meta-synthesis. Environ. Health 7, 1-10. Robert, M., Akiiki Kusiima, B., 1998. Community use of pit-latrines in Mubende District. Child Health and Development Centre, Uganda. Sikasunge, C.S., Phiri, I.K., Phiri, A.M., Dorny, P., Siziya, S., Willingham, A.L., 2007. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet. Parasitol. 143, 59–66. Sikasunge, C.S., Phiri, I.K., Phiri, A.M., Siziya, S., Dorny, P., Willingham, A.L., 2008. Prevalence of Taenia solium porcine cysticercosis in the Eastern, Southern and Western provinces of Zambia. Vet. J. 176, 240–244. Van der Geest, S., 1998. Akan Shit: Getting Rid of Dirt in Ghana. Anthropol. Today. 14, 8–12. Wohlgemut, J., Dewey, C., Levy, M., Mutua, F., 2010. Evaluating the efficacy of teaching methods regarding prevention of human epilepsy caused by Taenia solium neurocysticercosis in Western Kenya. Am. J. Trop. Med. Hyg. 82, 634–642. World Bank, 2013. Infographic: What’s a Toilet Worth. Accessed May 2019. http://www.worldbank.org/en/news/feature/2013/08/30/whats-a-toilet-worth- infographic.
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Based on the paper:
Studies in Africa have shown that the widespread occurrence of free-roaming pigs and the underuse of sanitary facilities are the key factors for the transmission of T. solium (Ngowi et al., 2004; Sikasunge et al., 2007; Assana et al., 2010; Pondja et al., 2010). According to Lekule and Kysgaard (2003), about 80% of pigs kept in East and Southern Africa are raised under the traditional free-ranging system. This system, though characterised also by lower fecundity rates, lower feed conversion and higher mortality rates, allows poor farmers to keep livestock without large capital investments (Thomas et al., 2013). This free-range practice contributes to the maintenance of T. solium transmission; whereby poor smallholders remain at risk for taeniasis/cysticercosis but also for Neglected Zoonotic Diseases (NZDs) in general. The NZDs are drivers for pushing these populations into more destitution (Seimenis, 2012). They also present unique control challenges as one needs to take into account the animal-human-ecosystem interface and because they inflict a dual burden on communities, affecting livestock and human health (Swanepoel et al., 2010). Several of the more cost-effective NZD control strategies involve reducing disease prevalence in the animal reservoir (Zinsstag et al., 2007), often profoundly impacting on the prevalent culture, livelihood and socio-behavioural patterns of the affected communities (Perry et al., 2002). Taenia Solium in Zambia Part 2 | 201
The present paper focusses on the social and cultural knowledge and practices relating to free-range pig keeping and T. solium infections, with the aim to study the complex relationships between different sociological and biological aspects and emphasising on who and what is responsible for population patterns of health, disease, and well-being (Krieger, 2001). Embedded in a One Health approach, the objective of this study was to identify possible barriers to pig related control measures, and eventually, adaptations of strategies to overcome cysticercosis locally.
5.2.1 Study area
The research was conducted at Kakwiya Rural Health Centre (RHC) in Petauke district of the Eastern province of Zambia. The RHC has a catchment population of 11,344 (Clinic headcount records). People practice subsistence farming, growing mostly maize and groundnuts primarily for home consumption. Pig production is common; most households have owned pigs at least once mainly to resolve financial issues. The main ethno-linguistic group in this area is the Nsenga, which has a matrilineal descent. The district was selected based on reports indicating high porcine cysticercosis prevalence of 14.6% in pigs (Sikasunge et al., 2008) and presence of a high number of free-roaming pigs (Phiri et al., 2002; Sikasunge et al., 2007). Only villages (n=21) within a radius of 8 km from Kakwiya RHC were selected for this study consisting approximately 261 households (Thys et al., 2015).
5.2.2 Study design
Twenty-one focus group discussions (FGDs) were conducted as described in detail by Thys et al. (2015) (see Table 4.2). According to our study design, focus groups participants included both pig keepers and non-pig keepers (Thys et al., 2015).
5.2.3 Data collection
The data collection took place from July to August 2010 (cfr 3.2.3 for details). The following topics were covered (Table 5.1): the perception of pig breeding in the communities and its role, knowledge and perceptions of taeniasis/cysticercosis and related risk behaviours and opinions on control measures.
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Table 5.1 Themes explored Themes Perception of Pig Perception Knowledge and Perception of control pigs management of risk perceptions of (direct contact) behaviour Taeniasis /Cysticercosis
Sub- - Positive and - Management When - Knowledge - Confinement of pigs negative problems (producer) themes aspects of pigs How - Treatment & - Feeding of pigs prevention - Boiling meat - Role of pigs Why (consumers) - Roles - Impact distribution in (stigmatisation…) - Meat inspections animal husbandry (producers)
- Washing vegetables (consumers) - Treatment/vaccination of pigs* * The porcine cysticercosis vaccine is not yet available.
5.2.4 Data processing and analysis
The two main risk factors identified in the literature, open defecation and free- roaming pigs, were also the two main themes that emerged from the discussions in our study. The first theme has been described by Thys et al (2015). In order to identify and understand the potential obstacles to pig confinement and other control options for T. solium from a socio-cultural point of view, it was necessary to understand on the one hand, why people raise pigs, how pigs are managed, and what pigs’ negative aspects are; and, on the other hand, what people’s knowledge and perception are about pig’s threats for human health and whether free-roaming pig management is considered to be a risky practice.
(also cfr 4.2.4 for details)
5.2.5 Ethical considerations
(cfr 4.2.5 for details)
The results highlight the different themes that emerged in the analysis (Fig 5.1). To reflect as much as possible what was expressed in the discussions, the order used to present participants’ perceptions in each section reflects the level of importance given by the participants to these topics (going from a strong to a weaker consensus). No substantial differences were observed between villages (very homogeneous). Taenia Solium in Zambia Part 2 | 203
Figure 5.1 Results structure
5.3.1 People’s perception and knowledge of pig keeping
5.3.1.1 Why do people raise pigs?
Pig rearing was reported to be a transitory activity, launched when households expected financial issues to be resolved, and often stopped after African swine fever outbreaks or shortage of feed. All households had owned pigs at least once, hence all focus group participants had a similar background knowledge about pig management. The main purpose of rearing pigs was to “help when problems occurred” and as such played an essential socio-economical role by addressing financial, traditional and agricultural issues.
“What we have just explained are the good things about pigs. Like using money to support school-going children by buying school uniforms for example; at agricultural fields as well, eating at funerals. After we have slaughtered it people can consume it, during celebrations or feasts, people eat such meat”. (Focus group\Women Wonzi village)
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Selling pigs allowed the family to raise money to help with agricultural activities but also to replace materials.
Secondly, it allowed people to buy household goods and thirdly to pay for health care, transport, school fees and justice fines. Except for the hiring of field workers, all groups had a financial advantageous viewpoint about the role of the pigs. Traditionally, pork was mentioned to be the meat mostly cooked and served to guests during big celebrations (funerals, weddings, Christmas celebrations, initiation ceremonies). It was very much appreciated for its taste by men, particularly the fat from the neck area, while women mentioned it for its use as relish for hunger alleviation. The perceived advantages of pigs were for men that they multiplied very quickly, grew faster and were easier to rear than cattle with regard to slaughtering and cooking. For women, the benefit was that pigs offered more meat than goats.
5.3.1.2 How are pigs managed?
Roles and responsibilities
In general, the daily management of pigs was done by women and children because they were most often at home, while the men were responsible for building kraals to enclose pigs at night. The tasks attributed to the children were, feeding the pigs, bringing them into the kraal at night and catching them when necessary. By belief and superstition, these tasks were especially attributed to people (mainly children) who had a “good rearing hand”:
“In Nsenga land we have a belief that with a particular child who has a good rearing hand, the animals would usually multiply.” (Focus group\Men Chiluzu village)
Even though most of the tasks are managed by women and children, the final decision to sell or slaughter a pig or to seek care would be taken by men who are considered as the pig owners.
Management problems: free-roaming versus confinement
Among several problems identified by the respondents regarding pig management, the main and recurrent ones were all related to feeding issues, especially during the rainy season because food in general was very limited (Table 5.2). These problems were also the most discussed among the children groups. Taenia Solium in Zambia Part 2 | 205
“Those that are without kraals just roam about scavenging on feces and whatever food they may find. Like at our home I call to feed them three times a day and after each feeding they go back and continue with the scavenging. The problem with pigs is that they never stop eating, but in the evening they come back to sleep.” (Focus group\Children Nyazowani village)
According to the participants, even without kraals pigs should be fed three times per day with maize bran or leftovers. The disadvantages expressed of not being able to feed pigs properly were that they scavenged and ate (human) feces, they were less healthy (no gain of weight nor good breeding) and that they got lost (owned by another feeder or died). Few respondents mentioned that it also led pigs to eat their piglets and that it was more difficult to sell their pigs (better price for pigs that did not scavenge because of the perceived disadvantages raised above).
Feed shortage was therefore the main argument against pig’s confinement, especially during the rainy season when there was no cropping. Though the perceived disadvantages of free-roaming pigs were more often discussed than its advantages, the majority of pig owners let their pigs roam free and men were the ones more in favour of this practice.
Table 5.2 List of pros and cons for pigs free-roaming practice as expressed by participants Pros (more men groups) < Cons (more children groups)
“Face food shortage” Allow “bad” scavenging (feces, dirt)
“Pigs stay at home (if fed)” Pigs have more risk to contract diseases
“Pigs more happy, less weak” Allow pigs to bring diseases to humans
“Allow pigs to access feces” “Create conflict with neighbours”
“No more need to be protected from wildlife” “Not taking good care of pigs”
“Avoid pigs to develop Polio” “Allow pigs to move a lot and disappear for days”
“Get fatter” “Difficult to identify pigs”
“Alright for pigs raised not for our own consumption “Nothing is good about roaming freely” but just for sale”
“More freedom for the owner (other priorities)” “No protection against wildlife”
“Clean the village from dirt” “Allow dirt (pig feces) in the village”
“Enough bush” “Not easy to catch pigs for slaughtering”
“No threat of stealing” “Bad rearing practice” <: More citations with cons than pros regarding free-roaming pig husbandry practice in general.
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Besides feed shortage issues, the other reasons expressed for letting pigs roam freely were that even without confining pigs in a kraal, pigs would stay around the house if properly fed every day, that pigs were happier and less weak when free-roaming and finally that it allowed pigs to eat feces which was perceived as an efficient way of ridding the village of dirt.
“The other reason is inadequate feed. We fear that if we enclose pigs, they may die. So, it’s better to allow them to be free so that they can eat anything they find.” (Focus group\Men Chimphanje village)
The danger to be attacked by wildlife or to be stolen by someone was not perceived as a threat and for some women the free-roaming practice avoided pigs to get diseases that made the pigs recumbent and locally perceived as polio.
“Now to just decide that time and start to confine them, you may find all of them have a pig disease outbreak. Even the joints would become weak, fail to walk and get polio” (Focus group\Women Mtuna village)
A few participants mentioned that pigs that were allowed to roam freely were usually pigs that were raised to be sold and not for household consumption presumably because of scavenging perceived risks.
Regarding the disadvantages of free-roaming pigs, the most important, and especially mentioned by the children was indeed that there was no control on what pigs fed on. The second argument against was that pigs were more inclined to contract a disease and thirdly, for women mainly, that it allowed pigs to bring diseases to humans.
“That [pigs confinement] would be a good idea; since the pigs would eat the right food and would not go round scavenging. It also means that even us we would be protected from the diseases which affect pigs and humans; that would be very good.” (Focus group\Women Chiluzu village)
Another issue raised by men was that it created conflict and juridical cases with neighbours as pigs were sometimes eating their maize or destroying their crops while roaming around. Rearing pigs this way was also perceived as not providing good care to pigs because “nothing was good about roaming freely”. It also allowed pigs to move a lot, sometimes disappearing for days, making it difficult to identify them, especially when they were many. Additionally they were difficult to catch for slaughtering. Taenia Solium in Zambia Part 2 | 207
“When they are many, they reproduce. In that case, I would sell some to buy maize bran. However, when they are many I don't know if a pig has been stolen or has died. Even when I would need to slaughter it, such as at a funeral, it may be difficult to find a pig. Even calling it to be fed, a pig can run away because it is not used to being fed.” (Focus group\Men Mtuna village)
Pig health
When a pig was found ill, generally participants first tried to isolate it from the others to avoid pig-to-pig transmission. The owner usually rapidly took the decision to slaughter the animal for human consumption before it died on its own. Because they often did not know how to treat, what medicines were available as these could only be found with the local veterinary assistant or at the District Veterinary Officer’s office, many kilometers away, they chose to slaughter the pig before it died on its own. If not, they would not be able to sell the meat door-to-door within the village as very few people would buy meat from a pig that they knew had died from a disease. Depending on how long the pig was sick before dying, the meat would or would not be eaten:
“When a pig dies on its own, some of us don’t eat it; some eat it depending on how the meat appears because sometimes the pig is sick for just two days and dies, such a pig is eaten. But one that has been sick for some time and loses weight is not eaten, it is just thrown away.” (focus group\Men Chimphanje village)
According to children, diseases can leave animals with the blood at slaughtering:
“Yes because if it died on its own, we may not eat the meat but if I kill it before it dies all the disease in the blood would come out.” (focus group\Children Nyazowani village)
5.3.1.3 What are pigs’ negative aspects?
Even if comments showed more people liking eating pork than disliking it, the negative aspects of pigs were much more discussed than their positive ones. In general, women and children expressed more negative aspects about pigs than men. The overall and main perceived negative aspects about pigs were their insatiable appetite and eating habits, which especially included its coprophagous character of
208 | C h a p t e r 5 eating human feces (even if properly fed by the owners), crops, but also dirt, babies left on the ground without surveillance and cadavers not buried deeply enough.
“Sometimes when a woman has a miscarriage, because they say that a still born child should not be buried very deep, the pig would go to the graveyard and dig out the foetus and start to eat it. Then we slaughter the same pig and eat the meat, which is very bad” (Focus group\Women Mkopeka village)
Another negative aspect well mentioned in all groups but more especially among women was that pigs brought diseases mainly by contaminating kitchen utensils or water (see also below). Pigs were considered as carriers of germs:
“Sometimes you would find that a pig comes directly from eating stool and finds a child eating something, it would go to the plate and eat from the plate and the child without realising would just continue eating the food. Therefore, it is difficult to prevent diseases that are transmitted by a pig.” (Focus group\Women Mkopeka village)
Another issue with raising pigs was that they could all die at once because of African swine fever during the hot season, creating a big economic loss for the household. The last main problem of raising pigs, mentioned almost only by men, was that pigs sometimes developed nsembe, which means “maize bran” in Nsenga. This word is commonly used to describe the T. solium cysts found in pork, under the tongue or in the eyes. These cysts were also called “Masese” because they also looked like the solid part remaining after brewage of a local beer, the small granules of maize not ground used to feed pigs, which was also the main perceived origin of their occurrence.
“That residue, masese, from beer brewing, if you feed it to the pigs they get the nsembe.” (Focus group\ Men Chimphanje village)
Another strong belief was that cysts appeared in pigs when the feeder had “bad hands” (bad herd management) or because of something in their feed like oil. Few people acknowledged that cysts origin was unknown and very few women only, said that cysts appeared because of pigs eating human feces. On the question of how to prevent cysts in pigs, men and children first mentioned the use of vaccine or medicines, followed by avoiding to feed pigs with masese, replacing the person responsible for feeding the pigs, adding ash in the feed or buying commercial feed, and finally confining pigs. However, in general, there was no consensus on whether Taenia Solium in Zambia Part 2 | 209 cysts in pigs were preventable or not, curable or not, if treatment was available or not and on the potential effects on humans.
5.3.2 Pigs threats for human health
Pigs as a source of diseases were strongly acknowledged by almost all participants but there were discussions on the kind of diseases that were transmitted from pigs to humans and how.
5.3.2.1 Disease transmission
For all participants the bad eating habits of pigs, in particular, the feeding on human feces was the source of disease. This coprophagous behaviour could infect people via contaminated water, food, plates (see above) or it could infect the pork and make people sick when they ate that meat. Epilepsy (fitting) was the most common condition, mainly mentioned by women:
“Yes and when they eat the feces, the feces go into the meat and then we eat the meat. And sometimes that is why you find worms in children and some suffer from fits because of eating pork.” (Focus group\Women Chiluzu village)
For men, pigs were also responsible for diarrhea and for all the three groups, they were also responsible for worm infestations:
“When I eat pork, the pigs will bring diseases. They bring diseases such as worms, and diarrhea. In nsenga, we just say “minyolo” [i.e.worms].” (Focus group\men Sakalinda village)
“… If I have bloody diarrhea, and that pig eats the feces. The following day we say let’s slaughter this pig, for sure those diseases are transmitted to those children who consume the pork. Even us who have consumed the pork, it means we have contracted such diseases. It is because of that pig that has brought the disease. That’s the badness of pigs.” (Focus group\men Mtuna village)
A few men considered AIDS to be also transmitted to humans via the same transmission route as expressed in the citations above. A few children mentioned malaria and cholera transmission as occurring via this same way.
Getting Mashabe, a local expression of being possessed with evil spirits, was another negative factor of keeping pigs according to some children and eating pork when
210 | C h a p t e r 5 breast feeding was considered to be dangerous by a few women. Finally, pigs could also lead to human death according to a few women:
“Pigs give worms and nsembe. All that; even death; worm infestation kills.” (Focus group\Women Mtuna village)
5.3.2.2 Pork preparation
Meat preparation (e.g. meat not well cooked or cooked too quickly, meat not well cleaned, especially the intestines, dirty cooking utensils) was also perceived as a threat to human health. More specifically, the methods of cooking meat were discussed. It could be roasted, roasted and then boiled, just boiled, shokas (grilled), cooked, boiled and fried, thoroughly cooked or dried. Participants were mainly in favor of boiling meat because it killed the worms, germs and helped to protect against diseases. Finally, they also preferred this type of cooking because it made the T. solium cysts (nsembe) disappear. Drying the meat before boiling was considered to be even more effective to drain the water out of the cysts. However, according to women groups, roasting was the way the meat was mostly prepared and preferred by the men. Women said that men preferred roasted meat while drinking a beer, because there was no risk of overcooking and it was quicker. Roasted meat also allowed to conserve the meat longer and therefore to be eaten later or by customers who drank beer. However, for women, eating raw or roasted pork was perceived as a threat for human health.
5.3.2.3 Pork consumption
To judge if the meat was eatable or not, participants referred to several criteria most generally linked to the overall meat appearance (color of the blood, smell,…). The presence of fat (from the neck) was also an important criteria used to buy and eat pork according to men and women. How the pig died was an important concern for men before buying pork. For instance, mainly men explained that when the meat looked redder than usual it meant that the pig died on its own or was sick before being slaughtered. Checking for the presence of cysts (e.g. in the muscles, in the mouth on the tongue) was a third criteria mentioned equally by men and women. Taenia Solium in Zambia Part 2 | 211
“It is important because nsembe suggests that the pig is sick. Nsembe shows if the pig is sick or not. So, the person who wants to kill a pig will have to use a wire to open the mouth and if there are whitish things under the tongue, you know that it is sick.” (Focus group\men Sikalinda village)
Finally, eating uninspected meat was seen as a threat to health for a few participants.
5.3.2.4 Eating meat with nsembe and epilepsy (“kunyu”)
Even if the zoonotic aspect of eating pork with cysts was targeted (especially by women), participants had poor knowledge on human cysticercosis in general and did sometimes confound it with other infections. A few women perceived human cysts as a disease of witchcraft from which only women suffered in the form of vaginal cysts called “masale” in Nsenga. There were also more comments mentioning occasions when meat with cysts was eaten. The cyst was considered comestible, tasting like rice (popping sound) for some and for others not that tasty but giving a “burst in the mouth”.
“Nsembe are very nice. When one is eating, the person feels very nice. They mix with fat, in fact, pork is just irresistible. Even if you wanted to refuse, you end up saying that I will only eat for today, and tomorrow I will not eat. Today I will eat since I have found it here.” (Focus group\Men Sikalinda village)
Meat with cysts was also associated with drunk people to whom this kind of meat was usually sold. For men and children, meat with cysts was never thrown away even if it would take more time to be sold for a reduced price. People usually bought infected meat because of a craving for meat.
“I had raised nineteen pigs then someone came from the Boma (nearest town). He bought one and took it to Boma. After slaughtering it he found the nsembe, he returned the following day with the meat and we were agreeable because he was not going to be allowed to sell that meat at Boma because he would be arrested. I gave him fifty percent of the money and he then sold the meat in the surrounding villages. But it should actually have been thrown away.” (Focus group\Men Mkopeka village)
Almost all groups associated eating pork with Kunyu (fitting). However, this was not attributed to an eventual presence of cysts in people’s brain (neurocysticercosis).
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“Yes and when they (pigs) eat the feces, the feces go into the meat and then we eat the meat. And sometimes that is why you find worms in children and some suffer from fits because of eating pork.” (focus groups\Women village Chiluzu)
Nearly all groups acknowledged the presence of an epileptic person in their village and sometimes in their own household. Two main types of epilepsy were identified by all groups: a bewitched one (the most mentioned), and a natural one (congenital, hereditary, genetic).
“Sometimes it happens that there are two people from the locality suffering from the same disease, they all go to the same hospital and one gets cured and the other continues to suffer from the same disease and eventually dies, we would therefore conclude that the other one was suffering from natural fits while the other had been bewitched.” (focus group\Men village Nyazowani)
Other food stuffs mentioned that could make people suffer from epilepsy besides pork included meat from warthog, fat mice, anything that died on its own, cat fish, bush meat and eggs. Therefore, according to some women only, the prohibition of eating pork and certain other food was considered as a treatment against epilepsy.
“I also have two children who had epilepsy but when I stopped them from eating pork they got better. They have not been fitting for the past 4 years now.” (Focus group\Women Chimphanje village)
Perceived as a deadly disease (not treatable, fatal) according to women and children, mainly because of seizures, the main burdens impacting life of epileptics and their family in daily life were physical injuries (burns by falling in fire; drowning in a pond, falling from trees or bicycle), stigmatisation (cannot get married or the marriage could not last long anyway, prohibition to eat some food, cannot be rich, cannot be greeted) and the unpredictable manifestations of the daily seizures (seizures while making love, cooking, eating, on the road, during celebration).
“Sometimes it happens so often, that after feeling each other and when you are ready to make love then that is when you have seizures. After so many disappointments you give up and say let me go and try somewhere else, then the marriage breaks up.” (Focus group\Men Chiluzu village) Taenia Solium in Zambia Part 2 | 213
5.3.3 Perception of control options: pros vs cons and suggestions
5.3.3.1 Pigs confinement
The need for feeding pigs when they are enclosed was the main disadvantage perceived especially among men groups. A second important disadvantage raised mainly by children was the difficulty to build kraals (not manageable, lack of awareness, not enough skills, kraals wood preferably used for cooking). The fact that pigs became lame, weak, unhappy and thinner when enclosed was an argument mainly expressed by women (pigs need space). The laziness or reluctance by men to build kraals was also raised by women. The laziness was attributed to a lack of care in general, other priorities and because they were not compelled to any law. In addition to the list of pros for the practice of free-roaming pigs (see Table 5.2), few participants (among men and children) raised the fact that confining pigs was not a common practice in the area, that pig owners were not used to it and did not want to argue with their wives regarding the priority of wood use.
“That’s unfortunately the tradition we have copied from our parents. This trend has continued here in the village. For those whose parents used to confine pigs, goats etc, it is easier for the younger generation to continue the trend wherever they go. It is the same for those whose parents were not confining. It looks like people feel it is much easier to let the pigs roam than think of the trouble of looking for wood to construct kraals. Sometimes, when you make a kraal, women use the wood support for a kraal as firewood for cooking. Instead of arguing with them, I let it happen and think of not building another one in the future.” (Focus group\Men Mtuna village)
Even if, in general, most participants were against it, advantages of enclosing pigs were mostly expressed by the children. Confining would avoid disease transmission, avoid pigs eating (human) feces, and allow a better control of pig feed. Furthermore, enclosing pigs was considered manageable and perceived as a good preventive measure against pigs bringing diseases and avoiding juridical cases (discussions with the neighbour).
Some people mentioned factors that should be dealt with in order to confine pigs: Confining pigs could not work with this breed of pigs or while there was a disease outbreak (e.g. African swine fever). The enclosure should be large enough to let pigs roam about; the confining should be combined with vaccination and drug support and
214 | C h a p t e r 5 finally, the cooperation between men and women should be more efficient in terms of task repartition and decision-making.
5.3.3.2 Meat inspection
The main problem with meat inspection by veterinary or public health services, mainly expressed by women, was the lack of inspectors. They did not know where it could be done and there was no inspection for pigs slaughtered at home and for the pork served at funerals. However, men were the ones who mainly felt bad to throw meat away and were afraid of the consequences of inspection. Another problem with meat inspection, expressed by children, was corruption: inspectors could be accused of cheating, uninspected meat could be sold elsewhere in any case, and people selling meat could always lie that their meat had been inspected.
“Others may cleverly announce that they were going to have meat inspected but turn back before having it inspected. On their return, they can lie that the meat was inspected when in fact not.” (Focus group\Children Mtuna village)
The issue of transport, both for the meat inspectors and for farmers to take pigs for inspection, was also mentioned. Finally, a few children and men considered it as a waste of time and money.
The arguments in favour of official pig inspection were mainly raised among women groups. This control measure was welcomed as it would allow knowing if the meat had a disease or not (and what was its origin) and preventing people from getting sick. Destroying (burry or burn) infected meat was not perceived as a problem mainly by women. In general, participants would feel more free and happy to consume meat without concern if they knew that it was declared suitable for human consumption.
Finally, overall meat inspection was seen as relatively manageable but should preferably be done by a veterinarian. Alternatively, the participants were also prepared to learn how to do it themselves.
5.3.3.3 Pig vaccination
There was a general fear among participants that the cost of vaccination would be too high or that the government would first offer the vaccination for free and after a while ask for contribution. Taenia Solium in Zambia Part 2 | 215
“The problem is the small contribution. At first even with cattle the government was offering free service and teaching the people on good animal husbandry, but immediately they started asking for the same contributions… People started failing to pay. You notice now that there are more deaths in cattle.” (Focus group\Men Chiluzu village)
The second problem expressed was transport of the pigs to the clinic to get the vaccine, especially if they were many pigs.
As a preventive measure, one or two participants flagged other problems: the safety of vaccination in general (suspicion), the need not to vaccinate pigs that were already sick (easy to diagnose and therefore too late to vaccinate), the difficulty to catch free- roaming pigs, and finally the need for appropriate sensitisation. Beside these disadvantages, participants, mainly men, were in favour of pig vaccination. Regarding their contribution for the vaccination expenses, participants, especially women, generally agreed, as it would protect pigs from diseases and assure them to eat good meat or avoid pig’s owners to kill their pigs. Few respondents suggested to combine vaccination with treatment if a pig was sick or to learn how to vaccinate pigs themselves.
This study looked into the socio-cultural determinants of free-roaming pig management in eastern Zambia where T. solium taeniasis/cysticercosis remain endemic (WHO, 2015) and indicating high taeniasis and cysticercosis prevalence of 6.3% and 5.8%, respectively (Mwape et al., 2012). It identified well established reasons for free-roaming but revealed also several key perceptions of pig owners explaining why this traditional low-input system is still maintained in this area, like in many other East and Southern African countries where both pig keeping and pork consumption have increased in the last three decades (Lekule and Kyvsgaard, 2003; Thomas et al., 2013; Mwang'onde et al., 2014; Zirintunda and Ekou, 2015; Lipendele et al., 2015).
Our results highlight the strong paradox observed between the persistence of the free-ranging practice and participants’ perception of pigs. While pig’s natural ability as a scavenger was obviously viewed as an advantage, their indiscriminate feeding
216 | C h a p t e r 5 habit was the main negative aspect of pigs commonly shared by the respondents. From a socio-economical perspective, the lower fixed cost (savings in terms of feeds, pen construction and time management) explains why this pig production system is more permanent than others (Lekule and Kyvsgaard, 2003). It can be set up to offset unexpected or anticipated major expenses (help for agricultural field work, school fees, justice fines, funeral ceremonies) but can also be stopped if all pigs died (e.g. during African swine fever outbreaks), are sold, or are consumed by the household. In the eastern African context, the flexibility that this traditional management offers seems to be what resource-poor farmers are looking for. Even if it is less productive and finally leads to low profit, it solves the farmers’ actual (financial) problems. Unlike what Lipendele et al. (2015) suggested for the Tanzanian context and Kagira et al. (2010) for Western Kenya, this poor pig management is opted for not only because of a lack of farming knowledge, but also because of pragmatism, habits and prioritisation in a survival context.
These latter factors can mitigate the observed paradox. Participants were well aware that this free-roaming practice allows pigs to access and feed on human feces, and could therefore become a threat for human health. Despite the perceived health risk, pigs owners still chose to raise their pigs in a free-range system, as it is more practical and economical, given the availability and the high cost of feed. This expressed constraint was very often identified in other traditional and smallholder pig herding systems (Kagira et al., 2010) and is often mentioned in control programmes for taeniasis/cysticercosis. In this area where humans and pigs compete for the same food source (maize milling), how sustainable could it be to ask pigs owners to enclose their pigs while feed at an affordable price with higher nutritive value is not steadily available? Furthermore, recent data have even shown that confinement of pigs is not the only solution to porcine cysticercosis as the confined animals may also get infection from contaminated feedstuff (Braae et al., 2015).
The gender and the social structure of communities have both a strong influence on the way responsibilities and tasks are assigned to women and men, girls and boys, also in the sector of livestock management in developing countries (FAO, 2010). These traditional gender roles explain why children, women and men in our study expressed a different perception regarding free-roaming pigs practice. The Taenia Solium in Zambia Part 2 | 217 responsibility of the kraal construction for pigs clearly belonged to men, while women are responsible for cooking, carrying water, fetching firewood and tending animals. However, like in many agro-rural patriarchal communities, the decision-making belongs to men, including decisions regarding pig management. Therefore, even if female participants were more in favor of enclosing pigs for hygiene and health reasons, this would not influence the current situation, as this position is not supported by the men. Children manifested a stronger willingness to enclose the pigs maybe because they are the main feeders. With fences it would be easier for them to manage this responsibility, be less disturbed by pigs and be considered as “good rearing hand”. The continued practice to maintain free-roaming pigs despite the perceived risk for health is likely due to the fragmented and limited knowledge about cysticercosis (pig and human) and neurocysticercosis but also because of the long delay between exposure and possible clinical signs and symptoms. Participants acknowledged that people could get sick by eating pork (well-cooked or not) and also indirectly by eating food or drinking water contaminated with human feces brought by pigs. However, they blamed more the bad eating habits of pigs than the practice of free-roaming. The fact that some women mistook human cysticercosis with vaginal cysts confirms that even though fragmented knowledge seems to be present on T. solium and its related health risk, the level of knowledge and understanding of risk factors, transmission and prevention is largely insufficient.
Health education has a major role to play. Johansen et al (2014) addressed the obstacles for obtaining a simple and meaningful health message with regard to a zoonotic disease such as T. solium taeniasis/cysticercosis. Because the scientific name itself is complicated, and being a zoonosis, health information needs to be provided to many different stakeholders across disciplines and sectors. As the life cycle of T. solium further complicates the message (one worm causing three diseases) (Johansen et al., 2014), the fragmentation and confusion of knowledge are understandable and could explain why some participants even believe that people could get AIDS or malaria while eating pork from pigs that ate feces from a sick person.
A potential limitation of this study, specifically regarding disease knowledge is that all the discussions took place in a room of rural health centre, which could have influenced participants to share reminders on what they previously heard or have
218 | C h a p t e r 5 learned from the health personal about this disease. This could even more be the case for women who are usually targeted by health promotion because of their traditional gender role related to care and hygiene education. We tried to limit this influence by starting the FGD with pig related discussion points.
Regarding control options other than enclosing pigs, all the ones proposed seemed to be more or less acceptable for implementation. Main concerns were the cost and that the Zambian government would not subsidise adequately and permanently the cost of the vaccine nor the logistics for its distribution once it will become commercially available. On the other hand, pig owners were quite keen on being trained for vaccination or pig treatment in order to manage the prevention and control themselves in exchange of free vaccine and treatment. What also needs more investigation is knowledge about slaughtering and meat inspection regulations because some citations suggested that pigs owners will not enclose their pigs nor adopt other preventive behaviours such as building latrines (Thys et al., 2015) unless they are forced by the law. Which suggests that if pig owners are not feeling obliged to do it or are not well informed about the regulations, the control and meat inspection will not be correctly implemented. For biosecurity purpose, the international institutions for human and animal health are not in favor of scavenging pig production systems in developing and transition countries because of the associated health risks and the difficulty for the farmers to introduce effective biosecurity measures (FAO, 2010). However, the debate on finding ways to keep pigs enclosed has been ongoing for some time. Lekule and Kyvsgaard (2003) suggested five possible strategies for the development of the pig industry in resource-poor communities. Among the identification of traits suitable for marginal environments and the genetic characterisation of local breeds of pigs, the development of strategies based on cheap feed stuffs that are locally produced would be the most necessary solution to convince pig owners to abandon the free-roaming production system.
Engaging the agronomy sector into the elaboration of a community-based intervention in order to control T. solium in this particular socio-cultural- environmental context would help out disease control managers to develop more integrated, sustainable and appropriate strategies by solving the obvious competition between animal feed and food for the population in periods of food shortage. Social Taenia Solium in Zambia Part 2 | 219 epidemiology, a method to capture important information on the social distribution and social determinants of health (Berkman and Kawachi, 2014) could also be more often incorporated into studies of disease transmission in relation to the life-cycle of T. solium along with spatial ecology and movement data of pigs (Thomas et al., 2013). By investigating people’s behaviours such as, the time and place of open defecation, meat preparation and cooking habits or patterns of pork consumption among men and during funerals, we could better answer why and when people get the most infected.
Finally, the role distribution according to gender is clearly a cultural feature that must not be underestimated when implementing a programme in order to include the total targeted population and address these different groups (men, women, children) not only with specific messages but also with adapted communication methods following a participatory and integrated approach. Encourage them through standard health education would not be enough, however cultural norms, practices and beliefs can always be used as arguments going in favor of new control strategies and facilitate even more their respect. For example, the belief that children with “a good hand” can avoid pigs to get cysts while feeding them could be a very important entry point in order to build a more convincing dialogue with men who remain the decision-makers for pig management in this Nsenga community. Additionally, extension messages should especially focus on men since they are also the most exposed to undercooked meat, translating in a higher taeniasis prevalence in men in this region (Mwape et al., 2012) and hence presenting a risk of egg transmission to the rest of the household. Although this set of recommendations falls under the One Health umbrella which acknowledges the close relationship between humans, animals and ecosystems, their practical implementation in the Zambian health policy context should be the object of further investigations.
To conclude we advocate for more appropriate solutions regarding pig feeding, the integration of gender issues in adapted educational messages and also in the method to increase disease knowledge, the implementation of subsidised pig treatment and vaccination and finally for a more bottom-up multidisciplinary approach. There is indeed a dire need to overcome disjunctions between biomedical and social research
220 | C h a p t e r 5 and hence better integrate the socio-cultural barriers and local considerations identified into control interventions.
Assana, E., Amadou, F., Thys, E., Lightowlers, M.W., Zoli, A.P., Dorny, P., Geerts, S., 2010. Pig- farming systems and porcine cysticercosis in the north of Cameroon. J. Helminthol. 25, 1-6. Berkman, L.F., Kawachi, I., 2014. A Historical Framework for Social Epidemiology. In: Social Epidemiology (2nd ed). Oxford University Press, Oxford. Braae, U.C., Harrison, W., Lekule, F., Magnussen, P., Johansen, M.V., 2015. Feedstuff and poor latrines may put pigs at risk of cysticercosis - A case-control study. Vet. Parasitol. 214, 187-191. FAO, 2010. Good practices for biosecurity in the pig sector - Issues and options in developing and transition countries. FAO (Food and Agriculture Organisation), Rome. Johansen, M.V., Trevisan, C., Braae, U.C., Magnussen, P., Ertel, R.L., Mejer, H., Saarnak, C.F., 2014. The Vicious Worm: a computer-based Taenia solium education tool. Trends Parasitol. 30, 372-374. Kagira, J., Kanyari, P., Maingi, N., Githigia, S., Ng'ang'a, J.C., Karuga, J., 2010. Characteristics of the smallholder free-range pig production system in Western Kenya. Trop. Anim. Health Prod. 42, 865-873. Krieger, N., 2001. Theories for social epidemiology in the 21st century: An ecosocial perspective. Int. J. Epidemiol. 30, 668-677. Lekule, F.P., Kyvsgaard, N.C., 2003. Improving pig husbandry in tropical resource-poor communities and its potential to reduce risk of porcine cysticercosis. Acta Trop. 87, 111-117. Lipendele, C.P., Lekule, F.P., Mushi, D.E., Ngowi, H., Kimbi, E.C., Mejer, H., . . ., Johansen, M.V., 2015. Productivity and parasitic infections of pigs kept under different management systems by smallholder farmers in Mbeya and Mbozi districts, Tanzania. Trop. Anim. Health Prod. 47, 1121-1130. Mwang'onde, B.J., Nkwengulila, G., Chacha, M., 2014. The risk factors for human cysticercosis in Mbulu District, Tanzania. Onderstepoort J. Vet. Res. 81, E1-E5. Mwape, K.E., Phiri, I.K., Praet, N., Muma, J.B., Zulu, G., Van den Bossche, P., . . ., Gabriël, S., 2012. Taenia solium Infections in a Rural Area of Eastern Zambia-A Community Based Study. PLoS Negl. Trop. Dis. 6, e1594. Ndimubanzi, P.C., Carabin, H., Budke, C.M., Nguyen, H., Qian, Y.J., Rainwater, E., . . ., Stoner, J.A., 2010. A systematic review of the frequency of neurocyticercosis with a focus on people with epilepsy. PLoS Negl. Trop. Dis. 4, e870. Ngowi, H.A., Kassuku, A.A., Maeda, G.E.M., Boa, M.E., Carabin, H., Willingham, A.L., 2004. Risk factors for the prevalence of porcine cysticercosis in Mbulu District, Tanzania. Vet. Parasitol. 120, 275-283. Perry, B., Randolph, T., McDermott, J., Sones, K., Thornton, P., 2002. Investing in Animal Health research to alleviate poverty. Tate, London. Phiri, I.K., Dorny, P., Gabriel, S., Willingham, A.L., Speybroeck, N., Vercruysse, J., 2002. The prevalence of porcine cysticercosis in Eastern and Southern Provinces of Zambia. Vet. Parasitol. 108, 31-39. Taenia Solium in Zambia Part 2 | 221
Pondja, A., Neves, L., Mlangwa, J., Afonso, S., Fafetine, J., Willingham III, A.L., . . ., Johansen, M.V., 2010. Prevalence and risk factors of porcine cysticercosis in Angonia District, Mozambique. PLoS Negl. Trop Dis. 4, e594. Seimenis, A., 2012. Zoonoses and poverty - a long road to the alleviation of suffering. Vet. Ital. 48, 5-13. Sikasunge, C.S., Phiri, I.K., Phiri, A.M., Dorny, P., Siziya, S., Willingham, A.L., 2007. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet. Parasitol. 143, 59-66. Sikasunge, S., Phiri, I.K., Phiri, A.M., Siziya, S., Dorny, P., Willingham, A.L., 2008. Prevalence of Taenia solium porcine cysticercosis in the Eastern, Southern and Western provinces of Zambia. Vet. J. 176, 240-244. Swanepoel, F., Stroebel, A., Moyo, S., 2010. The role of livestock in developing communities: Enhancing multifunctionality. University of the Free State and CTA, Cape town, South Africa. Thomas, L.F., de Glanville, W.A., Cook, E.A., Fevre, E.M., 2013. The spatial ecology of free- ranging domestic pigs (Sus scrofa) in western Kenya. BMC. Vet. Res. 9, 1-12. Thys, S., Mwape, K.E., Lefevre, P., Dorny, P., Marcotty, T., Phiri, A.M., . . ., Gabriel, S., 2015. Why Latrines Are Not Used: Communities' Perceptions and Practices Regarding Latrines in a Taenia solium Endemic Rural Area in Eastern Zambia. PLoS Negl. Trop. Dis. 9, e0003570. WHO, 2015. Investing to overcome the global impact of neglected tropical diseases: Third WHO report on neglected tropical diseases. In: Professor Peter Holmes, C.S.-N. (Ed.). Zinsstag, J., Schelling, E., Roth, F., Bonfoh, B., de Savigny, D., Tanner, M., 2007. TI - Human benefits of animal interventions for zoonosis control. Emerg. Infect. Dis. 13, 527-531. Zirintunda, G., Ekou, J., 2015. Occurrence of porcine cysticercosis in free-ranging pigs delivered to slaughter points in Arapai, Soroti district, Uganda. Onderstepoort J. Vet. Res. 82, 1-5.
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Based on the abstract of the 14th International Conference of the Association of Institutions for Tropical Veterinary Medicine (25 – 29 August 2013, Indaba Hotel and Conference Centre, Johannesburg, South Africa) and ready to be submitted to the Journal Anthrozoös (https://www.tandfonline.com/loi/rfan20):
Séverine Thys1 , Darryn L. Knobel2,3, Gregory Simpson4, Jacques Van Rooyen5, Tanguy Marcotty6, Sarah Gabriël1, Pierre Dorny7,8 and Marleen Boelaert9
1. Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium 2. Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Old Soutpan Road, Ondersterpoort, 0110, South Africa; 3. Department of Biomedical Sciences, Ross University School of Veterinary Medicine, Main Road, Basseterre, St Kitts and Nevis; 4. Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Old Soutpan Road, Ondersterpoort, 0110, South Africa; 5. Herding for Health Programme, Africa Field Division, Conservation International, 20 Dreyer Street, Claremont, Cape Town, South Africa; 6. Faculty of Science, University of Namur, Rue de Bruxelles 61, 5000 Namur, Belgium; 7. Department of Virology, Parasitology, and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium; 8. Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium; 9. Department of Public Health, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium.
Rabies in South Africa | 225
Rabies is endemic in many parts of the developing world, where domestic dogs are the primary maintenance host of the virus, and responsible for the vast majority (>90%) of human exposures and deaths (WHO, 2018). Once clinical signs develop, rabies is almost invariably fatal. It is transmitted when the virus is introduced into bite wounds, open cuts in the skin, or onto mucous membranes from saliva or other potentially infectious material such as neural tissue (Manning et al., 2008). Canine rabies is a neglected disease that predominantly affects poor and vulnerable populations living in rural areas in Africa and Asia (Knobel et al., 2005). Although important progress has been made in Africa on vaccine coverage in dogs (Davlin and VonVille, 2012), challenges in mobilising resources as well as cultural and operational barriers still remain to be better understood and contextually addressed (Bardosh et al., 2014; Jibat et al., 2015). As a result of various public awareness campaign initiatives (Balaram et al., 2016), nowadays, populations in developing countries are relatively well aware about the existence of the disease, with in some regions an improved understanding of key issues relating to rabies exposure and prevention (Lembo et al., 2012; Hasanov et al., 2018). Yet, differences between biomedicine and local understandings, as well as critical knowledge gaps on rabies prevention strategies and on the appropriate response to dog bites, are still affecting attitudes and practices towards general rabies control (Hergert and Nel, 2013; Sambo et al., 2014). Highly underreported due to, a lack of surveillance and laboratory infrastructure (Fooks et al., 2014), a lack of reliable field-based tests (Warrell and Warrell, 2015) and misdiagnosis (Mallewa et al., 2007), the burden of rabies (estimated at 59,000 human deaths and 8.6 billion USD economic losses annually) impacts public health sector budgets, local communities and livestock economies in the poorest regions of the world (Hampson et al. 2015).
Both rabies in dogs and humans can be controlled and in certain instances eliminated in developing countries by mass vaccination of dogs (summarised in Table 1 of Cleaveland et al., 2006, Zinsstag et al., 2009). Regarded as today’s most cost-effective strategy, mass dog vaccination programmes over consecutive years have been advised by the recent Global Strategic Plan to end human deaths from dog-mediated rabies by 2030 (WHO-FAO-OIE, 2018).
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To control rabies, it is estimated that at least 70% of the dog population should be vaccinated during annual vaccination campaigns (WHO, 2018). Understanding dog ownership dynamics, the human-dog relationship, and the ecology of the dog population, all of which may vary geographically or be affected by socio-cultural determinants (Knobel et al., 2008), is therefore helpful in guiding long-term rabies control efforts in particular areas.
Rabies was re-introduced into the Bushbuckridge District, Republic of South-Africa (RSA) in January 2008 (Mkhize et al., 2010), and subsequently spread throughout the district, resulting in at least 380 suspected cases in dogs and other animals, and one human death. Two years later, in 2010, a rabies outbreak occurred in dogs in urban areas of Gauteng resulting in a human fatality (Sabeta et al., 2013). Although both outbreaks were brought under control through free mass vaccination of dogs, it highlighted the risk of reintroduction of the disease into areas with low dog vaccination coverage, and the need to understand peoples’ perceptions of dog ownership and the determinants of behaviour towards rabies control in these low- income communities, urban as well as rural. However, anthropological studies on canine vaccination in Africa remain scarce (Bardosh et al., 2014).
To understand how local realities intersect with technical solutions (Bardosh et al., 2014) and how challenges of dog vaccination for rabies may be addressed in this particular South African context, we conducted a socio-anthropological study among a population experiencing a recent reintroduction of rabies at the human-wildlife- domestic animal interface. Beside assessing levels of awareness, socio-cultural control barriers and identifying gaps in knowledge to improve educational messages that accompany vaccination campaigns and correct post-exposure prophylaxis (PEP) after dog bite, another expected outcome of this qualitative study was to inform future quantitative work on aspects of rabies epidemiology, dog ecology and ownership, to further combine results to make recommendations on rabies control policy and vaccination implementation. Rabies in South Africa | 227
6.2.1 Study area
Combined with informal discussions and participative observations, a qualitative research study was conducted in a site that falls within the Mnisi Community Programme (MCP), a joint initiative by the University of Pretoria, the Mpumalanga Veterinary Services and the Mnisi Traditional Authority, to promote sustainable livelihoods through research into human and animal health, animal production and resource utilisation (https://www.up.ac.za/mnisi-community-programme). The Mnisi study area (Fig 6.1 and 6.6.1 Supplementary information) is located in the Bushbuckridge District in Mpumalanga Province in north-east South Africa. The Mnisi community contains approximately 29,500 ha of communal land and shares 75% of its boundary with wildlife reserves (Berrian et al., 2016).
Figure 6.1 The Map of the Mnisi study area (outlined in light green), Mpumalanga Province, Republic of South Africa, highlighting the location of the three selected villages (black circles). Image courtesy of Mnisi Community Programme, University of Pretoria.
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6.2.2 Study design
Eighteen focus group discussions (FGDs) were conducted in three villages of which one was a pre-test exploitable for analysis (FGD 01), including a total of 146 participants (50 women, 48 men and 48 children) (Table 6.1). The three villages were selected from those where the headmen (traditional leaders), acting as the gatekeepers to the villages, agreed to the study and had time to organise people to come and participate. Separate homogeneous FGDs were held with men, women and children (from minimum 10 years old and under the age of 18) in each village. These groups were created since they may have different perceptions and behaviours regarding dog and rabies management and heterogeneous groups are likely to hamper the quality of the data (Morgan, 1998; Grudens-Schuck et al., 2004). To evaluate possible differences in perceptions, FGDs were also stratified by dog ownership status, with ownership defined as having at least one dog in the yard of their household. This resulted in FGDs with participants from households owning one or more dogs, FGDs with participants not owning dogs and FGDs with mixed ownership groups, some participants owning dogs and others not (Table 6.1). The groups were constituted based on the willingness and availability of the participants who met the inclusion criteria of the respective group category (e.g. being a woman not owning a dog) and who were preferably not belonging to the same households as other participants to obtain a wider range of ideas and perceptions from the community. We were unable to put a group together of male non-dog-owners. The FGDs were conducted in the local language “Shangaan” and its number and variation allowed us to reach “theoretical data saturation” (Yardley, 2000).
Table 6.1 Characteristics of the focus group discussions (FGD) by dog ownership status, group categories and villages. Focus group Dog ownership Group categories Villages Number of discussions status participants number 01 Mixed Women Dixie 10 02 Mixed Women Islington 6 03 Non-owners Women Islington 5 04 Owners Men Islington 9 05 Mixed Men Islington 9 06 Mixed Children Islington 11 07 Owners Women Gottenburg 7 Rabies in South Africa | 229
08 Non-owners Women Gottenburg 8 09 Mixed Men Gottenburg 6 10 Owners Men Gottenburg 5 11 Owners Children Gottenburg 9 12 Non-owners Children Gottenburg 8 13 Mixed Women Dixie 7 14 Owners Women Dixie 7 15 Mixed Men Dixie 9 16 Mixed Men Dixie 10 17 Owners Children Dixie 10 18 Non-owners Children Dixie 10 TOTAL Mixed (8) Women groups Dixie (7) N=146 Non-owners (4) (7) Islington Women Owners (6) Men groups (6) (5) (50) Children groups Gottenburg Men (48) (5) (6) Children (48)
6.2.3 Data collection
Data collection took place from October to November 2011. The number of participants per FGD varied from 5 to 11 (Table 6.1). Three facilitators (one man and two women) from the MCP, fluent in Shangaan and familiar with the study area and the animal-human health issues, were identified and trained to moderate, report and translate to the principal investigator (ST). All the FGDs took place in outdoor places, such as in a participant’s yard. The moderator, reporter and translator roles were switched after each discussion.
The discussions lasted about 40 minutes and were recorded on a video camera. The following topics were discussed: perception of dogs (ownership, roles of dogs, positive and negative aspect, etc.), dog management (type of care, barriers to veterinary care, etc.), perception of risk behaviours (healthy dog, vaccination, bites, etc.), knowledge and perception of rabies (canine and human rabies, treatment, prevention, etc.) and perception of control options (vaccination, role of the government, dog sterilisation, culling stray dogs, etc.). The themes discussed were slightly adapted to the group category in order to ensure their interest and active participation during the discussion.
We complemented this data collection by systematically engaging in informal discussions with villagers, livestock keepers, school teachers, nurses and veterinary technicians, and used a participatory observation approach during meetings with
230 | C h a p t e r 6 livestock owners and their dogs (Fig 6.2), at the human clinic following up an incident of dog bite, and during encounters at the Hluvukani Animal Health Centre (HAHC) for the diagnosis of a rabid dog.
Figure 6.2 The Picture of dogs with cattle and livestock owners at the dip tank.
6.2.4 Data processing and analysis
We transcribed the recordings of the FGDs and translated them from Shangaan into English. To improve reliability, three researchers (Séverine Thys, Darryn Knobel & Greg Simpson) independently reviewed the written transcripts before entering them into the software. Text analysis of the transcriptions and the notes taken during the FGDs was supported by the NVivo 11® software (QSR International Pty. Ltd., Melbourne, Australia, 2008), which allows to classify and sort data and explore relationships and trends. The principal investigator (Séverine Thys) elaborated the coding tree with the major themes emerging, following an inductive approach, and discussed it together, until consensus was reached with the other investigators (Darryn Knobel, Greg Simpson, Jacques Van Rooyen, Tanguy Marcotty, Sarah Gabriël, Pierre Dorny and Marleen Boelaert).
The main results of each topic discussed are described in more detail and illustrated with anonymous quotes, chosen for their representativeness, appropriateness and revealing quality. To highlight the observed patterns and respect as much as possible what was expressed in the discussions, the order used to present opinions and ideas shared by the participants for each topic reflects the level of importance given by the participants to these topics (going from a strong to a weaker consensus). Rabies in South Africa | 231
6.2.5 Ethical considerations
Ethical clearances were obtained from the Research Ethics Committee of the Faculty of Humanities, University of Pretoria (South Africa), from the Ethical Committee of the Antwerp University Hospital (Belgium) and from the Institutional Review Board of the Institute of Tropical Medicine (11 29 3 779). We sought approval from the local authorities and community leaders before the commencement of the study.
Finally, we sought individual written consent from the participants to enrol in the FGD and to video record the discussion. Participation was entirely voluntary, and no names were recorded. We took care to phrase the questions appropriately and respectfully. Written informed consent was obtained from each participant 18 years of age or older, and from parents (or guardians) for children participants. Written assent was obtained from children older than 10 years old and under 18 years old. FGDs with children were not conducted during the school hours.
6.3.1 Role of dogs
Results indicate that communities owned dogs primarily for security reasons: to guard houses, cattle herds, and fields from thieves, wildlife and witches, and secondarily for hunting.
Hunting dogs, usually from a special breed and bought at a high price (up to 1000 Rand), were highly valued in the Mnisi community despite the illegality of hunting wildlife. Dogs were also seen as a source of income a business only mentioned by men and children. Companionship was also raised especially by children (to play and make people happy). Finally, for men, owning dogs was also part of their ancestral lifestyle and for ritual reasons.
“It is a custom as it is part of our culture, we grew up finding that our parents and elders like dogs.” (Focus group\Men owner Gottenburg village)
Although dogs were sometimes considered as livestock by their owner, hence deserving the same care, they were not consumed. Yet, one participant mentioned that eating rabid dogs was to be avoided to prevent rabies (see part on rabies transmission to humans).
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6.3.2 Dog ownership (definition, type of care and duties)
A dog owner, usually man or boy, was defined as someone who was followed by his dog, who liked dogs and did not fear them and who had a dog in his yard. It was the person who took care of the dog, like a farmer for his livestock or a “father” for his children. One child also mentioned that dog owners were the ones always eating meat, referring to the wildlife hunted by dogs. All participants preferred owning male dogs because in comparison to females they do not get pregnant, attract less males, are deemed stronger, run faster and are more aggressive.
Taking care of a dog primarily included providing appropriate food for it to be healthy and not looking for its own food out of the yard.
“Most of us do have an interest in keeping dogs or animals but the problem is we don’t know how to take good care of them. […] You just don’t put your dog in your yard and think it will take care of itself; so if you don’t feed it once it goes out of the yard and will steal and also bite people.” (Focus group\Men mixed Dixie village)
This was reflected in the prevalent view that roaming around for food was perceived as a risk for the dog’s health (see part about dog diseases) and damage to third parties, creating conflicts with the “victims” as dog owners, considered responsible of their animals, would have to pay for the damages. This was perceived very problematic in a rural context of poverty and unemployment.
“You have to pay as the community does know whose dog it is.” (Focus group\Men mixed Islington)
Stealing (eggs, chicken and goats) and biting (people and other animals) were the two main negative aspects of dogs. Among the health threats perceived from dogs, being bitten by a dog was the first one mentioned by all the groups but more often by dog owners (from dog owners and mixed groups). The following health risks were also mentioned: eating food touched by dogs (licking dishes, defecating and urinating in the yard on the vegetables, sharing the same water), eating after touching dogs (playing, brushing them) and finally children being in contact with puppies. The women were the only ones who raised those two last issues.
Taking a sick dog to the veterinarian was the second main duty for a dog’s owner although many stated that reaching the animal clinic was difficult mainly because of Rabies in South Africa | 233 the distance, lack of transport or money to pay for it. The other options mentioned were bringing dogs to the dip tank22 (Fig 6.2) of their village (green flags on Fig 6.1), calling the veterinarian or using traditional medicine. As a third duty, mainly according to men and dog owners, a person owning dogs should make sure they were safe inside the yard (build good fences, chain it during the day and release it during the night). This was to avoid troubles with people (stealing and biting), to be sure the house was well guarded and to also ensure the dogs were safe from people (e.g. being stolen, poisoned or hit by a car) or from wildlife (e.g. being killed by a lion). Among the other main perceived duties, participants (mainly owners and mixed groups) mentioned: treat them well (like a person), train them well in the sense of not stealing, not defecating indiscriminately and not biting, and vaccinate them.
The importance and level of care given to dogs depended on what they were used for (e.g. for security, for hunting) and differed between groups. In general, women seemed to care less about dog welfare than men or children: for them feeding dogs was too expensive, dogs were useless because they do not produce meat, hence they preferred investing their time and money in livestock.
6.3.3 Sheep management and slaughtering practices
There were two principal categories of dogs: owned and unowned dogs, the latter called “Mgewu” in Shangaan, meaning “street” dogs mirroring the concept of “street” kids. Rather than totally ownerless, they were considered as neglected.
“All have owners; it's only that their owners are unable to take good care of them.” (Focus group\Women mixed Dixie)
Nevertheless, unowned dogs were mainly regarded as the ones that steal, live in the street, look unhealthy (skinny, shedding their fur, not neat) and are dangerous because they suffer from diseases (e.g. “Kwashiorkor”), bite or even kill people. Women and the groups of dog owners were the ones mostly discussing this category of unowned dogs.
22 A government tank where livestock can be immersed in an acaricide and used as a weekly meeting point for veterinary monitoring.
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Owned but unwanted dogs were said to be sold (children groups), given (mainly men groups and dog owners) or killed (women groups and non-dog owners):
“You neither kill nor sell for money.” (Focus group\children owners Dixie) “Some people do come in search of puppies, and I just give them away. [..]. And I will just choose the ones I need first.” (Focus group\Men owners Gottenburg) “We just hang it into the bush and left it to die there.” (Focus group\Women non- owners Islington)
Among the owned ones, there were subcategories such as the hunting dogs that seemed to have a very particular status compared to other useful dogs such as, “security guards” or “shepherd” dogs.
6.3.4 Local knowledge of dog diseases and “Rihuhumbyana”
On the question about the diseases dogs can get, the men and the mixed ownership groups shared most of the information. Rabies was mentioned most often and is called “Rihuhumbyana” in Shangaan. A suspected rabid dog was described to be first of all a dog willing to bite anything found on its way (people, animals and things), getting mad (acting strangely, not being as usual and running like dancing), shedding its fur, not eating, not willing to be approached, being numb. As other signs of rabies infection in dogs, a few mentioned salivating and shivering. Being “co-infected with Kwashiorkor,” running away and living in the bush were also once mentioned by the participants.
The second most common disease of dogs was “Kwashiorkor”, a medical term probably borrowed from the Shangaan word for children suffering from malnutrition, re-used to designate a similar state of health that makes dogs scratch and shed fur when they are not well fed.
“Sorry there is something in need to say… Diseases that affect dogs we can compare it like a toddler, as if is not well fed it will suffer of kwashiorkor. The toddler’s skin will look pale showing that the child suffers of malnutrition do you understand? As I own a dog, I have to take good care of it as compared to my own dear child whom if sick must be taken to hospital. So we have dogs but we do not regularly take them to the clinic.” (Focus group\Men mixed Dixie) Rabies in South Africa | 235
It was also often considered as the symptoms of a rabid dog. The third main kind of disease mentioned was the one dogs were getting when eating fish bones from cans. All these three perceived “diseases” seemed somehow related to rabies.
Moderator (Mod): “How do you define a healthy dog? How can you see that this dog is healthy?”
Women (W) 7: “Only by looking at it. If it is well fed it attracts you but some dog’s skin is worn out.”
W4 & W5: “Shedding of fur.”
W7: “You can be able to spot that they are unhealthy and suffer of malnutrition. As they are sometimes given fish bones and you can tell that they are not safe.”
W3: “It is not good feeding dogs with fishes.”
[…]
W4: “They sometimes lick fish cans in the dumping hole, so we need to burn those tins after use.” (Focus group\Women non-owners Gottenburg)
Among other diseases and conditions mentioned to be affecting dogs, participants listed in their own words: ticks, worms, “AIDS”, blisters, coughing, female back becoming reddish, snake bites and unknown diseases coming from the forest.
Although rabies was not well known in general nor experienced by the participants in their village, a dog bite in a human was always associated with a risk of rabies. Rushing to the health clinic, both as victims or as dog owners, was the most frequently mentioned first response in this situation. The conflicts arising in the aftermath of a dog bite between victims, dog owners and the health clinic were mainly mentioned by women. Dog owners are expected to pay for all the victims’ costs in case of a dog bite, including transport to the health centre and treatment. The victims have to open a police case before a treatment can be given.
“My concern is with the owners of dogs that are so dangerous, they are very rude, if you come gently they will be so harsh just like their dogs; you will be even scared of telling whose dog is responsible. And when you go to the clinic, they will say “We will not help unless you provide a letter from the police station”. (Focus group\Women non-owners Gottenburg)
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All the FGD participants expressed a clear preference for not culling a suspected rabid dog after a bite incident because despite rabies many other reasons could cause a dog to bite, i.e. someone chasing/beating dogs, bitches with puppies, dogs defending their homestead from strangers or provocation.
“Yes, because everyone makes mistakes, but a dog cannot speak”. (Focus group\Women non-owners Gottenburg)
The alternatives proposed were to have the dog examined by a veterinarian, to chase it away or to tie it until it was examined by a veterinarian or died, as there was no place to take them (e.g. animal refuge). Instead of killing the suspected rabid dog, some participants, mainly male owners, also suggested to get it vaccinated or injected (6.6.2_Quote a) but some women mentioned that owners will just abandon them. Several statements indicate that the participants perceive rabies as a treatable disease, in humans as well as in dogs after a bite incident. Humans were said to be cured with pills, injection and treatment from the clinic or by traditional medicine (6.6.2_Quote b). Dogs were said to be treated by injections, by feeding them well and by bringing them to the veterinarian.
Regarding the transmission of rabies to humans, the dog was the only one to be blamed and mainly from its bites (saliva alike snake poison, mixing with blood). According to women groups, humans could also be infected if they were eating meat from animals that were bitten by a rabid dog or by sharing their drinking water or dishes licked by it. Non-vaccinated dogs, living together with dogs as they do with children (sharing the same water and air, dog fur in the food), eating meat from a rabid dog (6.6.2_Quote c) and eating without washing hands after touching a dog, were the other rabies transmission pathways mentioned by the participants.
On the other hand, the origin of the disease in dogs was mainly unknown. Some people suggested dogs were infected by wild animals from the game reserves, such as jackals and hyenas, while sharing the same places for eating (6.6.2_Quote d) or feeding on infected bushmeat (e.g. warthog meat) or beef. Although elusive, this link between rabies, wildlife and hunting was stressed again when a woman from FGD 02 said that “dogs that do not go hunting will never contract rabies”.
Beside other dogs, ticks, antelopes and the air of the game reserve were also blamed by few participants for the disease. Some participants perceived rabies as a natural Rabies in South Africa | 237 disease among dogs. Feeding dogs on fish bones from cans was also mentioned by a few men to be the origin of rabies in dogs.
Among the measures mentioned to prevent rabies, dog vaccination and regularly consulting a veterinarian were the two most important. Keeping dogs well (well tied, not eating from elsewhere) and not raising too many dogs were also stressed as preventive measures, as well as burning the carcasses of rabid dogs.
“They say if it [the dog] is rabid it has to be burnt when it dies, it is not recommended that we eat.” (Focus group\Women mixed Dixie)
6.3.5 Vaccination
6.3.5.1 Dog vaccination in general
Participants were aware of the value of vaccination in general (not specifically for rabies) to prevent dogs from becoming sick and spreading diseases. Dog vaccination was said to be for preventing rabies, kwashiorkor and hair loss (shedding of fur), AIDS and famine.
Each of the studied group categories considered vaccination essential. Women most commonly said that vaccination of dogs prevent them from transmitting disease to humans through bite and only women mentioned that vaccinating dogs was indicated for dogs that bite people or are aggressive. For men and children, the purpose of vaccinating dogs was rather curative. A few male owners said dog vaccination was to avoid transmission of infection to cattle by bites and to avoid dogs to be killed if they bite someone. Very few participants said they did not know the real purpose of dog vaccination.
Regarding the timing of vaccination, some participants said it had to be done when they were informed that the veterinarians were coming, when it was time as the dogs should “stay injected” (immunised) all the time. For two groups of owners (women and men), vaccinating dogs had to be done when dogs were still young but after the age of 3 months.
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6.3.5.2 Vaccination against rabies
The main perceived aim of dog vaccination against rabies was that bites from dogs would not infect humans anymore and that, except for children participants, the rabies vaccine would prevent the disease. Also, a curative purpose of dog vaccination was mentioned by both dog-owners and children non-owners but not by women.
6.3.5.3 Barriers against dog vaccination
For the non-dog owners, dog vaccination was efficient and no barriers or negative effect were perceived from it. For the dog owners and mixed groups, barriers perceived to vaccination were more often raised than its efficiency; it was also mentioned that vaccination was not working on every dog (6.6.2_Quote e).
In total, five different narratives were reported by the participants regarding rabies vaccination, each of them providing key information about what was experienced as barriers to their participation to dog vaccination campaigns.
(1) “Injection is to cure dogs after having bitten somebody. If it dies….”
This first narrative raised the confusion existing between curative injection (with a purpose of treating) and vaccination (with a purpose of preventing), both administered by ways of a syringe. Hence, for dog owners if the dog dies a few hours or days after receiving an injection (for treatment), the vaccine will be responsible of its death, even if it died after being hit by a car.
Children (C) 1: “Ours at home was injected and died.”
C2: “This one is grieving.”
[…] C1: “The problem is that after it was injected it just got worse and died.”
C3: “Got crippled.”
C1: “It suddenly, eishh..”
[…] C3: “Didn’t they poison it?” (Focus group\Children mixed Islington)
(2) “Vaccination is a plan for game lodges to kill hunting dogs”
This narrative came mostly from informal discussions with people owning dogs for hunting and who were experiencing conflicts with owners of game lodges and the park management. Dogs were said to be killed sometimes by eating poisoned meat Rabies in South Africa | 239 balls thrown during the night in the yard of people owning hunting dogs. From participant observations and informal discussions with community members, hunting wildlife inside as well as outside the Kruger National Park and private game parks is illegal and considered as poaching, even small game hunting. However, for the community, the land and the wildlife still belong to them and their ancestors. In addition to remaining a traditional activity for the Shangaan, hunting is also a means to survive and face unemployment (getting food for the family and making money by selling bushmeat).
(3) “Vaccination makes dogs weaker, less aggressive, and having less appetite”
The third narrative was built around the belief that after receiving the vaccine, dogs looked generally less active and less aggressive, hence less capable to remain a good “security guard” to protect them against thieves and aggressions or to hunt.
M1: “With dog vaccination? I once had dogs back then. After being vaccinated, they seem less strong than the way they used to be, they were weakened.”
M5: “They look numb.”
M1: “Yes. But when not vaccinated, you find that they do not. They seem strong. But if not vaccinated its aggressiveness stays the same. But if vaccinated its aggressiveness becomes less.” (Focus group\Men owners Gottenburg)
The origin of this belief seemed to come from the posters found in the veterinary clinics or health centres showing a picture of a very aggressive rabid dog and saying that in order to avoid that (an aggressive dog), dogs need to be vaccinated against this disease (Fig 6.3).
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Figure 6.3 The Picture of the poster found at the Hluvukani Animal Health Centre.
(4) “Dogs are trained to not bite, hence less risk to spread rabies, hence no need for vaccination”
According to this fourth narrative, a dog by nature or by being well trained by its owner will not bite people unless they deserve it.
“If your dogs had not been trained once they bark, and they bite that person, you as an owner have a problem with your dogs. You did not train them to know that people do visit your home.” (Focus group\Men owners Gottenburg)
This means that if a dog does not bite people, there is no risk of infecting people with rabies, hence no need to vaccinate it against this disease. This belief is sustained by the other idea that rabies was seen as a natural disease in dogs.
“According to its nature, a dog is not expected to bite people, and does not bite people with no reason. Its teeth shiver if it wants to bite a person.” (Focus group\Men owners Islington).
(5) “Not knowing for which disease the vaccination is for”
The last narrative hindering dog vaccination is based on the lack of information said to be given by the veterinarians or animal health technician, or people helping during vaccination campaigns, about the vaccination purpose and the vaccine content. Rabies in South Africa | 241
“It depends on what the vaccination is for, both between dogs and livestock, as we do not have a broad knowledge on that. As maybe if you feel the pain, they [animal health technician] might just inject you only a part of vaccination, and that gets complicated after. There are many diseases maybe for which vaccination would be for.” (Focus group\Men mixed Dixie)
6.3.5.4 Dog vaccination campaigns
The ones who agreed to participate in further vaccination campaigns, mainly men and children, raised some conditions: only if they are not at work/school, if the campaign takes place nearby their home and if dogs do not die following the injection. Some participants were also willing to assist veterinarians, mainly children and women, and as such learning more about how to prevent diseases.
The dog owners made also some recommendations to the state veterinarians regarding those campaigns: to have more frequent vaccination and veterinarian’s visits, be consistent in the follow-up, better explain why and against which disease veterinarians are vaccinating their animals, honour the scheduled vaccination campaigns and inform them on time.
6.3.5.5 Barriers to access the veterinary clinics
For all the three villages, the levels of accessibility of the dog population to animal health care was hampered by the fact that the clinics were too far from their home and that they rarely have a private transport to carry the dog as it is not allowed to bring a dog in public transport in South Africa, including taxis (6.6.2_Quote f). Therefore, finding a way to reach the clinic was considered to be difficult and too expensive.
Also, the issue of not having enough phone credit to call a veterinary clinic in case of emergency, the lack of information (not knowing where and when to go), the general lack of knowledge, laziness and the fact that the dog can recover spontaneously, were the other barriers mentioned.
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6.3.5.6 Role of the government to keep dogs safe
Generally, the groups mixing dog owners and non-owners were the most talkative about how the government could or should support people regarding dog management. On the contrary, the groups of dog owners and the children were very quiet about it, but getting veterinary drug supplies and being assisted with feed for dogs, respectively were considered the most important support for all the groups. The main support adults, except the owners, were asking from the government was free dog vaccination (6.6.2_Quote g). Adults were also asking to be assisted for food (and water) and more importantly for men to be taught on how to prevent dogs from getting sick. According to some respondents, the government should also provide a nearby animal health clinic, mobile veterinarians, a social grant for the dog owners (to make them more implicated in vaccination campaigns and to decrease the number of street dogs), and build a shelter to keep unwanted dogs. The non-owners were only requesting free dog vaccination and assistance with dog feed from the government.
The main findings of our study highlight key socio-cultural factors among the Mnisi community affecting health-seeking and control behaviours regarding rabies control measures, especially dog vaccination and dog bite management. Although there has been a growing scientific interest in dog rabies control in Africa during the last two decades (Jibat et al., 2015), we present to our knowledge the first socio- anthropological study of contemporary rabies dog vaccination in South-Africa.
This study illustrates that vaccination is clearly influenced by local dog ownership practices, which in turn are mediated by several contextual factors: historical, social, cultural, political, economic and ecological. Many epidemiological surveys and studies on Knowledge, Attitudes and Practices that were conducted to identify rabies knowledge gaps, characterised the human-dog relationships (dog densities, dog ecology and dog ownership), identified rabies vaccination and human rabies risk factors, and captured the relative prevailing importance of social and cultural factors played in the field of rabies control and elimination (Matibag et al., 2007; Kaare et al., 2009; Sambo et al., 2014; Digafe et al., 2015; Schildecker et al., 2017; Wallace et al., 2017 among others). Rabies in South Africa | 243
Some dog population characteristics reported in our study were similar to other African settings such as, a high proportion of male and young-owned dogs, a small proportion of dogs actually ownerless, a high turnover rate and a large proportion of free roaming dogs (low level of confinement) (Jibat et al., 2015; Barbosa et al., 2018;). All these factors affect density and immune status of a dog population and are seen as factors limiting vaccination coverage (Davlin and VonVille, 2012). Yet, they are also directly associated with the socio-economic values and cultural habits of a society attributed to dogs, which are in turn influencing dog ownership status and management (Fekadu, 1993; Aiyedun et al., 2012).
Utilitarian value also tended to dictate dog management rather than purely culturally- defined beliefs (Bardosh et al., 2014). However, if this functional relationship with dogs was true for feeding and general care management, compliance to dog vaccination was strongly hindered by a set of beliefs and rumours, especially among the “hunting dogs”, even when the necessary financial arrangements had been made, i.e. the vaccine applied free of charge and mobile vaccination campaigns. Hunting dogs, usually purchased, were the most valued, by providing food and income from wildlife. These dogs have a closer bonds with their owners developed during the long and dangerous walks and the time spent together in the bush, therefore adding more incentive to provide good care. Yet, they were in fact the least likely to be vaccinated against rabies in contrast with Tanzanian findings (Sambo et al., 2014). This specific unwillingness to vaccinate them was not so much related to lacking basic knowledge about vaccination in general but rather to not having sufficient trust in the aim of the vaccination campaign. A mistrust originated most probably from the particular historical, socio-economic and ecological context in relation with the colonial period, the establishment of Protected Areas (PAs), and the Kruger National Park (KNP) management (DeGeorges and Reilly, 2008; Anthony, 2007; Cock and Fig, 2000). Established on land traditionally occupied and used by indigenous people, the past and current perceived injustices of the KNP bring the communities sometimes into conflict with wildlife and park authorities as the livelihoods of local human communities residing on the edge of these PAs often involve the direct exploitation of natural resources (Anthony, 2007). Beside the advantages towards adjacent conservation areas including, employment opportunities, recreation, wildlife conservation, protection from wildlife, educational opportunities, and donations, the
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Mnisi community reported disadvantages such as, wildlife damage to crops and predation of livestock, safety risks to community members, unfair employment practices, wildlife poaching/crime, and restricted access to natural resources such as grazing land and firewood (Berrian et al., 2016).
Already identified in other studies (Ali et al., 2013; Bardosh et al., 2014; Muthiani et al., 2015; Castillo-Neyra et al., 2017), participation to rabies vaccination campaigns was also at stake because of irregular, low frequency of mass vaccination campaigns, tenuously scheduled follow-up times, lack of information about the vaccines and the process of the campaign. Barriers such as inadequate schedules, could also be solved by avoiding school or work time for example, as suggested by men and children who are the ones most willing and in charge to bring the dogs. The suggestion made by women and children to assist the veterinarians during the campaign raised the importance given by our participants to gain more knowledge but also to get an opportunity to dispel possible suspicions.
Vaccine hesitancy due to mistrust with human vaccination programmes in developing countries (Mills et al., 2005; Cobos Muñoz et al., 2015), and increasingly in developed ones (Dubé et al., 2013), is replete among the literature. The following barriers to human vaccination may also apply to veterinary vaccination programmes: rumours, conspiracies, concerns about the quality of the vaccine, i.e. counterfeit, expired or of low quality, especially when delivered for free, side effects and harmfulness, unclarity about the benefits of vaccination (Yahya, 2007; Abakar et al., 2018), but also divergences in issues of power, knowledge, religion, interests and social norms between different social groups (Bardosh et al., 2014). Differences between biomedical and local understandings, which are known to lead to community resistance to vaccination programmes (Waller and Homewood, 1997) were also captured in our narratives: misperception of vaccination purposes, i.e. curing instead of preventing due to the same act of injecting, rumours on elimination of hunting dogs orchestrated by lodge managers due to Human-Wildlife Conflicts, the vaccine making dogs less aggressive, due to misleading health promotion messages of posters, the belief that a well-trained dog does not bite and therefore is not harmful for the community, and finally, suspicions due to a lack of information about the vaccine. Rabies in South Africa | 245
Although respondents demonstrated reasonably good knowledge of rabies, including its zoonotic component with especially the role of dogs in transmission and common clinical signs in animals and humans, multiple opinions were identified about its source, control and treatment among the different groups.
All groups of respondents did not have a clear idea of how dogs become infected with rabies and blamed wildlife. Living at the edge of the KNP, speculations about wildlife playing a role in rabies transmission makes sense, although not being accurate. Despite the frequent occurrence of rabies in the black-backed jackal in the Limpopo province, bordering Mpumalanga province in the north, jackals have not played a notable role in the transmission of rabies in the KNP (Mkhize et al., 2010). The mention of a rabies source from other animals (generally mammals) is usually depending on the respondents’ environmental and fauna context. For example, in an Ethiopian setting, equines and cats were the other animals transmitting rabies to humans (Digafe et al., 2015). The participants used the term ‘Kwashiorkor’ to designate a condition characterised by a set of signs that is probably the result of malnutrition, and they related this condition to canine rabies signs resulting from the ingestion of fish bones from cans found in open air dumping areas. The word “kwashiorkor” is said to come from the Ga language from Accra, Ghana, which means “the disease of the deposed child when the next one is born”, reflecting the development of the condition in an older child who has been weaned from the breast when a younger sibling comes (Williams, 1973). In South Africa where malnutrition remains a serious problem, despite the policy interventions in the two decades since the end of apartheid (Madhavan and Townsend, 2007), Kwashiorkor could be a similar cultural concept among Shangaan people than the original one from Ghana and/or a new term integrated in the Shangaan language following the implementation of nutrition campaigns and policies. Moreover, the use for an animal disease of a term that describes a severe form of human protein malnutrition, further stresses the zoonotic characteristic of rabies but also more generally how humans contextualise their own health within animal and ecosystem health (Lapinski et al., 2015). The origin of the narrative about the harmfulness of fish bones more precisely, usually found in the street trashes and supposing infecting free-roaming dogs not well fed with rabies or “Kwashiorkor”, is probably a confusion with botulism, a disease that can be acquired by consuming canned fish (Johnston et al., 1963). Although difficult
246 | C h a p t e r 6 to fully relate on, it also looks like a way to underpin the lack of good provision of care provided by dog owners because of the poverty affecting the community (Wallace et al., 2017; Barbosa Costa et al., 2018). Starvation and thirst were also mentioned by Ethiopian respondents as causes of rabies in dogs (Serebe et al., 2014).
Even if a dog’s bite was always associated with rabies risk, it was also a source of conflict between dog owners and bite victims, which could hamper good health care management. Having their dog culled and being held responsible to pay for someone’s medical treatment was a relative motivation for dog owners to participate to rabies control (Bardosh et al., 2014). However, from the bite victim perspective, this ownership responsibility was felt as a social pressure to not disclose the dog nor the owner identity. This was supported by the risk that the cause of the bite incident is attributed to the victims, highlighting that the notion of social responsibility of the owner and the victims reflect generally much broader divisions within the community (Bardosh et al., 2014).
Our qualitative research managed to provide dense information on reasons for not vaccinating dogs, which was a gap identified by the systematic review of Davlin and VonVille (2012) on canine rabies vaccination and domestic dog population characteristics in the developing world. Several vaccination barriers were found similar to that in other developing countries. Due to the qualitative research approach, even among the common patterns observed, local barriers emerged which often remain the keys to improve compliance.
Another added value was the inclusion of different groups among household members (women, men and children) and to have tried to also examine the perspective of non-dog owners in regard of dog ownership practice, social responsibility and rabies control awareness.
However, our study and the data obtained have several limitations. We omitted to include the perspectives of other local actors (such as frontline health and veterinary workers and lodge managers) who by their perceptions, behaviours and contexts are also influencing dog vaccination campaigns. Capacities, norms, and policies of implementing institutions also play a central role in rabies control efforts (Bardosh et al., 2014). The non-homogeneity of certain groups regarding the dog ownership Rabies in South Africa | 247 status may have caused information bias as well as hampering participation in the discussion and discomfort.
In conclusion, these data provide information with potentially immediate local benefits as well as longer and wider term implications for a more widespread participation in dog rabies vaccination in the Mnisi community of South Africa.
The recommendations developed from this study are likely to have an implication for Public Health and could offer some applications to vaccination programmes in other areas also located at a human-wildlife-domestic animal interface and beyond. As canine rabies poses a threat not only to human health, but also for dog welfare and wildlife conservation, the lack of trust should be addressed (or restored) at several levels:
- Develop an Information, Education and Communication programme on rabies knowledge gaps and the misinterpretations of messages regarding vaccination.
- Clarify the procedure in the case of dog bite incidents and adapt it, e.g. by removing the need for a police report before start of treatment, in order to avoid barriers to care access and delays, to protect the victims from the dog owners’ possible dishonesty or reprisals but also to ease the communication between health officers and veterinarians/animal health workers.
- Involve health clinics and game lodges in vaccination campaigns in order to address rumours.
- Include more regularity, sensitisation and time during rabies vaccination campaigns.
- Invite community members who manifested interest to participate actively to the implementation of vaccination campaigns for moving towards more community- directed vaccination efforts for rabies.
- Address Human-Wildlife Conflict issues for a sustainable development by ensuring that the interventions are effective in term of community-equity rather than emphasising only on the efficacy of current tools and strategies (Bardosh et al., 2014). A cross-cultural research approach to prevent and mitigate conflict and aid in
248 | C h a p t e r 6 coordinated action will be highly useful in advancing an understanding of human– wildlife conflict (Manfredo and Dayer, 2004).
- Broaden the constituency for support, offering the potential for developing integrated control measures that involve veterinary public health, tourism, wildlife conservation and animal welfare agencies (Regea, 2017).
Furthermore, mixed methods investigations adopting a socio-ecological approach focused explicitly on the dynamic interactions between nature and society and committed to place-based and solution-driven research across multiple scales (Gardner et al., 2013) would be very adequate in such human-wildlife-domestic animal interface settings. This kind of investigation could especially follow up on the Grover et al. (2018) study on the spatiotemporal rabies epidemiology conducted in the private reserve at the unfenced western boundary of the KNP in eastern Mpumalanga Province. A large number of rabid dogs were found in the reserve between 2009 and 2014, posing a continuous threat to wildlife, as high rates of between-species transmission increase the probability of host shifts (Grover et al., 2018). Although several plausible explanations were suggested by the authors such as, diseased dogs deliberately being disposed of in the reserve, a more detailed anthropological study would be necessary to confirm this theory.
Intimately related to people’s behaviours regarding dogs, the ecologies of the different dog categories (especially hunting dogs getting in the PAs) are also major drivers of the maintenance and transmission patterns of rabies, which once identified spatially would provide a better understanding and control in the specific ecosystem of the studied area. Quantitative data on dog ecology and epidemiological role (movements, contact networks) would therefore be gathered through participatory protocols with local stakeholders and combined with qualitative data in order to link social and ecological systems. Rabies in South Africa | 249
6.6.1 Study area (including dog rabies vaccination campaigns process and common canine diseases in the study area)
Approximately 40,000 people live in 8,500 households in the community (Statistics South Africa, 2012). The unemployment rate in this area in 2011 was 52.6%, substantially higher than the national rate of 29.8% (Statistics South Africa, 2012). Over two-third of the population aged 20 years and older had not completed secondary school, and the majority of the population (96%) lives in formal housing with a mean household size of 4.0 persons (Conan et al., 2015).
Following the diagnosis of canine rabies in the area, a dog population census and door-to-door free vaccination campaign was conducted in two of the villages (Athol and Clare) in the study area in September 2009 (G. Simpson, personal communication). These data were collected from all households in the villages, identified from aerial survey photographs. A total of 848 households were identified in the two villages. Of these, 219 (26%) owned dogs, with an average of two dogs per dog-owning household. The total owned dog population in the two villages was 430, of which 46% were under one year old. Vaccination coverage prior to the campaign was only 36%. Retrospective interviews revealed a high estimated dog-bite incidence rate of 500 bites/100,000 people/year (G. Simpson, personal communication). In the study area, there are no private veterinary practices, but there are state veterinary services. The animal health needs of the Mnisi area and the surroundings are also met at a subsidised rate by the HAHC (Fig 6.1) run by the Faculty of Veterinary Science of the University of Pretoria (UP) (Conan et al, 2015). The provincial state veterinary services have strengthened regular dog rabies vaccination campaigns since the disease re-emerged in Bushbuckridge in 2008 (Mkhize et al., 2010).
The following process is used by the provincial state veterinary services for the dog rabies vaccination campaigns: (1) Identify the area that needs vaccination looking at where rabies cases are in animals and previous vaccination campaign records; (2) Draw maps of the area; (3) Divide the area into sections; (4) Assign each section to a team composed of 2 to 5 people which is made up of at least one animal health technician and assistants; (5) Go down each road in the section and ask the owners if
250 | C h a p t e r 6 they have dogs and vaccinate them; (6) Give vaccination certificates to the owners; (7) Go back to follow up on houses that had no one at home at the time of first visit. Rabies vaccination for dogs is and has been free of charge in the Mnisi study area.
According to the local regulation, the correct procedure for dog bite is to immediately wash the wound with a disinfectant, go to a health centre as soon as possible where post exposure prophylaxis is given by administering 5 doses of rabies vaccine over a 28 day period, and injecting rabies immunoglobulin at the wound site. Additionally, the nurse treating a dog bite victim should call the HAHC or veterinary services, to initiate an investigation into the circumstances of the bite and the health and rabies vaccination status of the biting dog. The regulations are that suspected rabies cases are to be investigated by veterinary services and if animals are showing signs of rabies, they will be euthanised, but if not they can be quarantined and observed for 10 days. If euthanised the brain is sent for rabies testing (Bishop et al., 2010).
The following process is used by the provincial state veterinary services for the dog rabies vaccination campaigns: (1) Identify the area that needs vaccination looking at where rabies cases are in animals and previous vaccination campaign records; (2) Draw maps of the area; (3) Divide the area into sections; (4) Assign each section to a team composed of 2 to 5 people which is made up of at least one animal health technician and assistants; (5) Go down each road in the section and ask the owners if they have dogs and vaccinate them; (6) Give vaccination certificates to the owners; (7) Go back to follow up on houses that had no one at home at the time of first visit. Rabies vaccination for dogs is and has been free of charge in the Mnisi study area.
The majority of dogs in the community have the morphological appearance of the Africanis landrace (Gallant, 2002), although there is some phenotypic evidence of interbreeding with western breeds (Conan et al., 2015). From July to December 2011, the common canine diseases registered by HAHC are presented in Table S6.1. Out of 286 dogs seen during this period, mainly diagnosed with external parasites, one dog was suspected with rabies and two dogs had bitten humans and therefore underwent rabies investigation.
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Table S6.1 Canine diseases registered at Hluvukani Animal Health Centre per month from July until December 2011. Month 2011 Canine diseases and infections July Mange, babesiosis, malnutrition August Gastroenteritis, babesiosis, mange September Ehrlichiosis, fractures, mites October Ectoparasites (including mange), helminthiasis November Babesiosis, demodicosis, malnutrition December Ehrlichiosis, helminthiasis, mango fly
6.6.2 Illustrative quotes from the Focus Group Discussions (quotes “a” until “f”)
Quote a_ Focus group of men owners from Islington (FGD 04):
“Yes, and be vaccinated and no other way, after three months be checked if they still have the disease.”
Quote b_ Focus group of men owners from Gottenburg (FGD 10):
“I have noticed one thing traditionally that I have seen a lot when a dog accidentally bites someone. Its owners used to remove a single fur from its skin. They burn it. And rub the wound [with the ashes] where there is teeth marks.”
Quote c_ Focus group of women owners from Dixie (FGD 01):
“Like if my dog is rabid and is in pain, and we decide to kill it and then eat the meat, that is when we will be infected.”
Quote d_ Focus group of men mixed from Islington (FGD 05):
“It comes from jackals, hyenas and dogs eat where those animals had eaten and therefore get infected by the disease”.
Quote e_ Focus group of men owners from Gottenburg (FGD 10):
Mod: “Ok. Does vaccination work in dogs?”
Man (M)3: “We can call it luck as in some dogs it works well in some it doesn’t.”
M2: “Yes, it is luck to work on yours.”
M4: “In some it does and in others it does not.”
Quote f_ Focus group of men mixed from Islington (FGD 05):
“M3: Where am I going to put it? Can you board a taxi along with it?
M8: It is also already dangerous for the one sitting next to it.
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M4: It is dangerous.
M8: Even to myself, I will just be hurt, but … Yes, it is too hectic.”
Quote g_ Focus group of men mixed from Gottenburg (FGD 09):
“Dogs are like cattle we have to pay when they are sick, but if they are to be vaccinated it must be free as we are just preventing diseases. But if they say we have to pay, we will.”
Abakar, M.F., Seli, D., Lechthaler, F., Schelling, E., Tran, N., Zinsstag, J., Muñoz, D.C., 2018. Vaccine hesitancy among mobile pastoralists in Chad: a qualitative study. Int. J. Equity Health. 17, 1-10. Aiyedun, J.O., Olugasa, B.O., 2012. Identification and analysis of dog use, management practices and implications for rabies control in Ilorin, Nigeria. Sokoto J. Vet. Sci. 10, 1-6. Ali, A., Ahmed, E., Sifer, D., 2013. A study on knowledge, attitude and practice of rabies among residents in Addis Ababa, Ethiopia. Ethiop. Vet. J. 17, 19-35. Anthony, B., 2007. The dual nature of parks: attitudes of neighbouring communities towards Kruger National Park, South Africa. Environ. Conserv. 34, 236–245. Balaram, D., Taylor, L.H., Doyle, K.A.S., Davidson, E., Nel, L.H., 2016. World Rabies Day - a decade of raising awareness. Trop. Dis. Travel Med. Vaccines. 2, 1-9. Barbosa Costa, G., Gilbert, A., Monroe, B., Blanton, J., Ngam Ngam, S., Recuenco, S., Wallace, R., 2018. The influence of poverty and rabies knowledge on healthcare seeking behaviors and dog ownership, Cameroon. PLoS One 13, e0197330. Bardosh, K., Sambo, M., Sikana, L., Hampson, K., Welburn, S.C., 2014. Eliminating Rabies in Tanzania? Local Understandings and Responses to Mass Dog Vaccination in Kilombero and Ulanga Districts. PLoS Negl. Trop. Dis. 8, e2935. Berrian, A.M., van Rooyen, J., Martínez-López, B., Knobel, D., Simpson, G.J.G., Wilkes, M.S., Conrad, P.A., 2016. One Health profile of a community at the wildlife-domestic animal interface, Mpumalanga, South Africa. Prev. Vet. Med. 130, 119–128. Bishop, G.C., Durrheim, D.N., Kloeck, P.E., Godlonton, J.D., Bingham, J., Speare, R., Rabies Advisory Group 2000, 2010. Rabies : guide for the medical, veterinary and allied professions (2nd ed.). Government Printer, Pretoria. Castillo-Neyra, R., Brown, J., Borrini, K., Arevalo, C., Levy, M.Z., Buttenheim, A., . . ., Paz-Soldan, V.A., 2017. Barriers to dog rabies vaccination during an urban rabies outbreak: Qualitative findings from Arequipa, Peru. PLoS Negl. Trop. Dis. 11, e0005460. Cleaveland, S., Kaare, M., Knobel, D., Laurenson, M.K., 2006. Canine vaccination-Providing broader benefits for disease control. Vet. Microbiol. 117, 43–50. Cobos Muñoz, D., Monzón Llamas, L., Bosch-Capblanch, X., 2015. Exposing concerns about vaccination in low- and middle-income countries: a systematic review. Int. J. Public Health. 60, 767–780. Rabies in South Africa | 253
Cock, J., Fig, D., 2000. From colonial to community based conservation: Environmental justice and the national parks of South Africa. Soc. Transit. 31, 22–35. Coleman, P.G., Dye, C., 1996. Immunization coverage required to prevent outbreaks of dog rabies. Vaccine. 14, 185-186. Conan, A., Akerele, O., Simpson, G., Reininghaus, B., van Rooyen, J., Knobel, D., 2015. Population Dynamics of Owned, Free-Roaming Dogs: Implications for Rabies Control. PLoS Negl. Trop. Dis. 9, 1-19. Davlin, S.L., VonVille, H.M., 2012. Canine rabies vaccination and domestic dog population characteristics in the developing world: A systematic review. Vaccine. 30, 3492–3502. Davlin, S.L., Lapiz, S.M., Miranda, M.E., Murray, K.O., 2014. Knowledge, attitudes, and practices regarding rabies in Filipinos following implementation of the Bohol Rabies Prevention and Elimination Programme. Epidemiol. Infect. 142, 1476–85. DeGeorges, P.A., Reilly, B.K., 2008. A critical evaluation of conservation and development in Sub-Saharan Africa. The Edwin Mellen Press, Lewiston, New York, 572 pp. Digafe, R.T., Kifelew, L.G., Mechesso, A.F., 2015. Knowledge, attitudes and practices towards rabies: questionnaire survey in rural household heads of Gondar Zuria District, Ethiopia. BMC Res. Notes 8, 1-7. Dubé, E., Laberge, C., Guay, M., Bramadat, P., Roy, R., Bettinger, J., 2013. Vaccine hesitancy: An overview. Hum. Vaccin. Immunother. 9, 1763–73. Dürr, S., Mindekem, R., Kaninga, Y., Doumagoum Moto, D., Meltzer, M.I., Vounatsou, P., Zinsstag, J., 2009. Effectiveness of dog rabies vaccination programmes: comparison of owner-charged and free vaccination campaigns. Epidemiol. Infect. 137, 1558–67. Fekadu, M., 1993. Canine rabies. Onderstepoort J. Vet. Res. 60, 421–427. Gallant, J., 2002. The story of the African dog. University of KwaZulu-Natal Press, 124 pp. Gardner, T.A., Ferreira, J., Barlow, J., Lees, A.C., Parry, L., Vieira, I.C.G., . . ., Zuanon, J., 2013. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368, 1-11. Grover, M., Bessell, P.R., Conan, A., Polak, P., Sabeta, C.T., Reininghaus, B., Knobel, D.L., 2018. Spatiotemporal epidemiology of rabies at an interface between domestic dogs and wildlife in South Africa. Sci. Rep. 8, 1-9. Grudens-Schuck, N., Allen, B.L., Larson, K., 2004. Methodology Brief: Focus Group Fundamentals. Iowa State University Extension. Hampson, K., Coudeville, L., Lembo, T., Sambo, M., Kieffer, A., Attlan, M., . . ., Dushoff, J., on behalf of the Global Alliance for Rabies Control Partners for Rabies Prevention, 2015. Estimating the Global Burden of Endemic Canine Rabies. PLoS Negl. Trop. Dis. 9, e0003709. Hasanov, E., Zeynalova, S., Geleishvili, M., Maes, E., Tongren, E., Marshall, E., . . ., Horton, D.L., 2018. Assessing the impact of public education on a preventable zoonotic disease: rabies. Epidemiol. Infect. 146, 227–235. Jibat, T., Hogeveen, H., Mourits, M.C.M., 2015. Review on dog rabies vaccination coverage in
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Africa: a question of dog accessibility or cost recovery? PLoS Negl. Trop. Dis. 9, e0003447. Kaare, M., Lembo, T., Hampson, K., Ernest, E., Estes, A., Mentzel, C., Cleaveland, S., 2009. Rabies control in rural Africa: evaluating strategies for effective domestic dog vaccination. Vaccine. 27, 152–160. Knobel, D.L., Cleaveland, S., Coleman, P.G., Fevre, E.M., Meltzer, M.I., Miranda, M.E., . . ., Meslin, F.X., 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull. World Health. Organ. 83, 360–368. Knobel, D.L., Laurenson, M.K., Kazwala, R.R., Boden, L.A., Cleaveland, S., 2008. A cross- sectional study of factors associated with dog ownership in Tanzania. BMC Vet. Res. 4, 1-10. Lapinski, M.K., Funk, J.A., Moccia, L.T., 2015. Recommendations for the role of social science research in One Health. Soc. Sci. Med. 129, 51–60. Lembo, T., Partners for Rabies Prevention, 2012. The blueprint for rabies prevention and control: a novel operational toolkit for rabies elimination. PLoS Negl. Trop. Dis. 6, e1388. Madhavan, S., Townsend, N., 2007. The social context of children’s nutritional status in rural South Africa. Scand. J. Public Health. Suppl. 69, 107–17. Mallewa, M., Fooks, A.R., Banda, D., Chikungwa, P., Mankhambo, L., Molyneux, E., . . ., Solomon, T., 2007. Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg. Infect. Dis. 13, 136–9. Manfredo, M.J., Dayer, A. a., 2004. Concepts for Exploring the Social Aspects of Human– Wildlife Conflict in a Global Context. Hum. Dimens. Wildl. 9, 1–20. Manning, S.E., Rupprecht, C.E., Fishbein, D., Hanlon, C.A., Lumlertdacha, B., Guerra, M., . . ., Hull, H.F., 2008. Human rabies prevention--United States, 2008: recommendations of the Advisory Committee on Immunization Practices. Morbidity and Mortality Weekly Report, Recommendation and Reports / Centers for Disease Control. 57, 1–28. Matibag, G., Kamigaki, T., Kumarasiri, P., Wiiewardana, T., Kalupahana, A., Dissanayake, D., . . ., Tamashiro, H., 2007. Knowledge, Attitudes, and Practices Survey of Rabies in a Community in Sri Lanka. Environ. Health Prev. Med. 12, 84–89. Mills, E., Jadad, A.R., Ross, C., Wilson, K., 2005. Systematic review of qualitative studies exploring parental beliefs and attitudes toward childhood vaccination identifies common barriers to vaccination. J. Clin. Epidemiol. 58, 1081–8. Mkhize, G.C., Ngoepe, E.C., Du Plessis, B.J., Reininghaus, B., Sabeta, C.T., 2010. Re-emergence of dog rabies in Mpumalanga province, South Africa. Vector Borne Zoonotic Dis. 10, 921– 926. Morgan, D.L., 1998. The Focus Group Guidebook. Sage Publications, Thousand Oaks, CA. Mosimann, L., Traoré, A., Mauti, S., Léchenne, M., Obrist, B., Véron, R., . . ., Zinsstag, J., 2017. A mixed methods approach to assess animal vaccination programmes: The case of rabies control in Bamako, Mali. Acta Trop. 165, 203–215. Muthiani, Y., Traoré, A., Mauti, S., Zinsstag, J., Hattendorf, J., 2015. Low coverage of central point vaccination against dog rabies in Bamako, Mali. Prev. Vet. Med. 120, 203–9. Rabies in South Africa | 255
Regea, G., 2017. Review on Economic Importance’s of Rabies in Developing Countries and Its Controls. Arch. Prev. Med. 2, 015–021. Sabeta, C.T., Weyer, J., Geertsma, P., Mohale, D., Miyen, J., Blumberg, L.H., . . ., Paweska, J.T., 2013. Emergence of rabies in the Gauteng Province, South Africa: 2010-2011. J. S. Afr. Vet. Assoc. 84, E1-5. Sambo, M., Lembo, T., Cleaveland, S., Ferguson, H.M., Sikana, L., Simon, C., . . ., Hampson, K., 2014. Knowledge, Attitudes and Practices (KAP) about Rabies Prevention and Control: A Community Survey in Tanzania. PLoS Negl. Trop. Dis. 8, e3310. Serebe, S.G., Tadesse, K.A., Yizengaw, H.A., Tamrat, S.M., 2014. Study on community knowledge, attitude and practice of rabies in and nearby Gondar town, North West Ethiopia. J. Public Health. Epidemiol. 6, 429–435. Statistics South Africa, 2012. Census 2011 Municipal Report—Mpumalanga. Statistics South Africa, Pretoria. Wallace, R.M., Mehal, J., Nakazawa, Y., Recuenco, S., Bakamutumaho, B., Osinubi, M., . . ., Wamala, J., 2017. The impact of poverty on dog ownership and access to canine rabies vaccination: Results from a knowledge, attitudes and practices survey, Uganda 2013. Infect. Dis. Poverty. 6, 1-22. Warrell, M.J., Warrell, D.A., 2015. Rabies: the clinical features, management and prevention of the classic zoonosis. Clin. Med. 15, 78–81. WHO, 2018. WHO Expert Consultation on rabies: Third report. World Health Organization. WHO-FAO-OIE, 2018. WHO | Zero by 30: the global strategic plan to end human deaths from dog-mediated rabies by 2030. World Health Organization. Williams, C.D., 1973. The Story of Kwashiorkor*. Nutr. Rev. 31, 334–340. Yahya, M., 2007. Polio vaccines—“No thank you!” Barriers to polio eradication in Northern Nigeria. Afr. Aff. (Lond). 106, 185–204. Yardley, L., 2000. Dilemmas in qualitative health research. Psychol. Health. 15, 215–228. Zinsstag, J., Dürr, S., Penny, M.A., Mindekem, R., Roth, F., Menendez Gonzalez, S., . . ., Hattendorf, J., 2009. Transmission dynamics and economics of rabies control in dogs and humans in an African city. Proc. Natl. Acad. Sci. U. S. A. 106, 14996–5001.
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Three socio-anthropological case-studies addressed perception and knowledge of Neglected Zoonotic Diseases (NZDs) and opportunities for integrated disease control in endemic rural African settings among small-scale livestock owners and communities: Cystic echinococcosis (CE) in Morocco among a Berber population from the High Atlas, Taenia solium taeniasis/cysticercosis (TSTC) in Zambia among the Nsenga ethno-linguistic group from a district of the Eastern Province and rabies in South Africa among Shangaan people of the Mnisi community from Mpumalanga Province. Each study explored how socio-cultural factors and knowledge gaps affect, influence and explain behaviours with regard to health and animal husbandry management and consequently the likelihood for the livestock owners to adopt or not control measures. Cross-case analysis highlights how complex social, cultural, political, economic and environmental determinants influence interventions to control endemic zoonoses, how transmission dynamics are rather biosocial than purely biomedical and how cultural beliefs and broader understandings of health and well-being might affect knowledge regarding zoonoses.
The understanding of such factors allowed us to illustrate and demonstrate how and why social sciences, anthropology in particular, could contribute to the “One Health” (OH) approach for NZDs integrated control but also how challenging it is in practice.
By uncovering practices that facilitate the spread of pathogens between animals and humans, our work not just identified barriers to disease control but addressed the “when”, “how”, “where” and “why” of these barriers: why infected sheep offal is given to dogs (chapter 3), why latrines are not used or built (chapter 4), why pigs are left free roaming (chapter 5) and why dogs are not vaccinated (chapter 6). Our interdisciplinary work allowed us to inform about a nuanced understanding of how people experience and indeed conceptualise risk within a wider web of structural factors such as the intersection of poverty and gendered divisions of labour affecting risk of T. solium in an endemic area in Eastern Zambia (chapter 5).
Culture affects risk perceptions by conditioning people to notice and value certain interactions, relationships, and objects (Decker et al., 2010), but the relative presence General Discussion | 259 of pathogens in the local ecology influences in turn cultural and inter-personal differences in human personality (Prokop et al., 2010). In humans, many psychological phenomena appear to serve as an anti-pathogen defence, which implies the prediction of specific kinds of cultural differences, e.g. differences in food preparation (Sherman and Billing, 1999), marriage structures (Low, 1990), parenting practices (Quinlan, 2007) and mate preferences (Gangestad et al., 2006). Fincher et al. (2008) also found that worldwide variation in historical and to a lesser extent current pathogen prevalence substantially predicted societal tendencies towards individualism or collectivism. For instance, within ecological regions characterised by a higher prevalence of infectious diseases, human cultures are characterised by a greater collectivism as the behaviours that define collectivism may function in the service of anti-pathogen defence, and thus be especially adaptive under conditions of high pathogen prevalence (Fincher et al., 2008).
Furthermore, in contexts of fragile livelihoods, disease risk might not be people’s sole concern or they might not have the resources to take up protective measures or the most effective ones. Risks, as conceptualised by zoonotic disease specialists or by animal and human health workers are not necessarily the same as those conceptualised by livestock owners (MacGregor and Waldman, 2017). Indeed, in our Zambian case-study, farmers did not perceive the advantages of confining pigs, especially when it came to food shortages and time or wood needed to build a pig house. Even if negative aspects (health risks) of free-range pig keeping were perceived, people seemed inclined to take the risk as confining pigs might directly and immediately threaten their broader well-being. How people think about and decide what to do with a sick animal, for example, may not be influenced only by decisions about economic gain or about potential disease spread (MacGregor and Waldman, 2017). Gender plays also an important role because even if women, and also children, seemed to have a higher perception of the risks for TSTC, they lacked authority in terms of decision-making compared to men (chapters 4 and 5). Decisions on animal treatment and management are not straightforward and seldom the domain of one person. Despite the seemingly clear cultural norms on who is nominally responsible to make decisions about the welfare of the animals and how they are kept (e.g. confining pigs or not), dispersed to other households (e.g. in South Africa, the receiving of cattle as a ‘bride price’ called lobola or the introduction of a bull for
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‘breeding’), sold or slaughtered, negotiation and contestation may result in far less predictable outcomes as indicated by many studies done among pastoralists from east and southern Africa (see in Ainslie, 2005; de Vries et al., 2006 and Swanepoel et al., 2010).
Consequently to such accounts, insights from anthropology would be needed to unravel these dynamics to determine who should be targeted by zoonosis control information messages (e.g. not only women but men for health sanitation campaign) and to understand who has the power to decide whether to implement suggested campaign strategies or comply with regulatory measures (MacGregor and Waldman, 2017).
In the realm of OH research, our case-studies’ results further support the findings of Wallace et al. (2015) and many others for endemic (Valeix, 2018) as well as emerging zoonoses (Scoones, 2010), in that livelihood, farming practices or gender roles, among others, are seldom a matter of choice or open to change through behavioural nudges23 or top-down efforts to raise public understanding (Craddock and Hinchliffe, 2015). Anthropology in interdisciplinary public health research has contributed to the identification of points of transmission of zoonotic organisms. Yet, we have to make sure that an exclusive focus on risk in studying the social dimensions of zoonoses does not increase the likelihood that, in interdisciplinary consortia, people’s cultural logics or social practices come to be cast in negative terms (such as ignorance or superstition), and as beliefs or behaviours that exacerbate risk and require changing (MacGregor and Waldman, 2017). When virologists and epidemiologists raise questions regarding the perception of zoonotic risks, anthropologists remain often reduced to the role of data-providers on ‘how “natives” think’ or on hygienic (infection-stopping) or unhygienic (infection-promoting) beliefs and practices (Keck and Lynteris, 2018), and for which a simple linear process of social engineering is
23 The concept of “Nudge” refers to small changes in the physical or social environment that make specific behaviours more likely driven by automatic responses requiring little cognitive engagement, controlled by our state of mind and triggered by features of the environment (Kelly and Barker, 2016). General Discussion | 261 enough to inform strategies for achieving individual behavioural change (Napolitano and Jones, 2006; Panter-Brick et al., 2006). However, human behaviour is the result of the interplay between habit, automatic responses to the immediate and wider environments, conscious choice and calculation, and is located in complex social environments and cultures (Michie et al., 2014). The concept of culture is itself complex and implies an ongoing, dynamic process and changing health-related behaviour is notoriously difficult to initiate and sustain.
Kelly and Barker (2016) suggested that in medicine and policy making, discussions about behaviour change are subject to six common misapprehensions24 which have driven to the elaboration of repeatedly ineffective interventions, often delivered at great cost in terms of money, resources and lost opportunities, ignoring the accumulated learning from more than two centuries of psychological, sociological and anthropological evidence (Kelly and Barker, 2016). Health campaigns can have an important role and can be effective, but they are but one part of a total and multi-level strategy. Giving people information does not make them change (e.g. lung cancer and give up smoking or obesity and willing to go on a diet), even less in the realm of the prevention (Marteau et al., 2015). It is not because people are unaware about the fact that they, and their families, should be using latrines instead of defecating in the open (chapter 3) or running to the clinic when being bitten by a dog (chapter 4). What people say is that a multitude of other things in life get in the way of them doing this (e.g. respecting a taboo and role repartition about responsibilities of building and using latrines, clinic too far and the obligation to denounce the owner of the dog that did bite). Rational assessment alone based on economic utility theory does not drive behaviour. There is also an automatic system which responds to environmental (e.g., access to an environment and services that facilitate behaviour) and psycho-social prompts (e.g. habitual tendencies, the nature of social relations, aspects of self- concept and identity) in a way that requires very little conscious engagement
24 (1) Understanding human behaviour is just common sense, it is so obvious that it needs little or no serious thought; (2) Changing health behaviour is simply a matter of getting the packaging of messages right (often drawn with commercial advertising analogy); (3) Knowledge and information from expert sources is sufficient to drive behaviour change; (4) People act rationally, they do what they know to be sensible and logical after critical and rational appraisal of the evidence; (5) People act irrationally, they are unknowledgeable about their own behaviour; (6) believing that it is possible to predict behaviours accurately (Kelly and Barker, 2016).
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(Lapinski et al., 2015). If people do not act rationally all the time, neither are they always irrational, they have their own reasons for doing things, which may appear irrational for others. It is therefore still very difficult to say with any certainty how individual people will behave in any given situation (Kelly and Barker, 2016). Derived from the social and psychological sciences, Kelly and Barker (2016) proposed that starting with the behaviour, identifying who is behaving and where, and working backwards using regressive inference (understand the preceding conditions of the specifics) is a much more profitable avenue for developing interventions instead of predictive single unilinear causal models.
Also, why policy makers are often falling back about “getting people to change their behaviour” instead of adapting control measures based on local context? The spectrum of options, tools and theories existing between changing people behaviours and adapting the control measures to the context is wide and should be combined accordingly. Yet, regarding health-related behaviours of zoonotic diseases among livestock owners, there is an additional layer of complexity to take into account: the human–animal and multi-species relations.
The implication of animals as sources of human disease has generated complex patterns of problematisation of human-animal contact and entanglement (Brown and Kelly, 2014; Muehlenbein, 2016). The relatively rapid anthropogenic change, namely the human manipulation of Earth’s ecosystems characterising the new geological era called “Anthropocene” (Crutzen and Stoermer, 2000), has reoriented debates around health and disease, requiring us to move beyond what some consider the traditional boundaries of the discipline (Brown and Nading, 2019). Examples of topics that force such movement are among others (1) zoonotic diseases, e.g. the increased interspecies contacts and the consequent shift in biopolitics to address it, (2) antimicrobial resistance, e.g. the intersections between intensive animal production and new forms of pathogenicity, (3) veterinary medicine, e.g. contributions made to comparative epidemiology and human public health (4) animal therapeutics, e.g. pets contributing to emotional and physical well-being or animals for sentinel species that now aid in the control of zoonotic pathogens as veterinary subjects, and (5) food and General Discussion | 263 farming, e.g. the welfare of livestock for the safety and abundance of human food. Following that call, our work initiated by veterinary and public health scholars, is also an attempt to pursue the recent aim of several medical and environmental social scientists to bring medical anthropology together with animal studies25 in ways that highlight the contribution of anthropology to interdisciplinary research on zoonoses and the impact of this research on contemporary practices of global health (Keck and Lynteris, 2018). Through our three case-studies, we revealed at some length how human-animal engagements respectively, with sheep, pigs and dogs are culturally shaped and understood in social terms. We also underpinned the implications that such cultural beliefs, e.g. taboos related to latrine use, narratives related to dog vaccination against rabies at the edge of wildlife conservation areas, might have for the consideration of what is natural and what is social while these opposed categories are taken for granted in the biomedical world and shaping OH discourse and research (MacGregor and Waldman, 2017).
Together with the emergence of multi-species ethnography (Kirksey and Helmreich, 2010), social scientists became interested in how health brings humans and animals together (Nading, 2013) or how people’s interactions with ecosystems and animals affect exposure to disease in the context of their daily lives, livelihoods and socio- economic activities and how people’s social differences — by gender, age, wealth, occupation — affect these interactions (Leach et al., 2017). In the case of rabies in the Mnisi community for example (Chapter 6), barriers about free dog vaccination presented an additional layer of complexity when concerning the category of “hunting” dogs. Their role in the community and the ancestral practice of hunting were socially inter-related and moreover embedded in the particular historical, socio- economic and ecological context of this South African area in relation with the colonial period, the establishment of Protected Areas, and the Kruger National Park management. Refusing to vaccinate these dogs, as well as purposely putting the sick ones inside the fenced Parks (Grover et al., 2018), could also be seen as a way to resist
25 Since the last three decades, Animal Studies or Human-Animal Studies is a rapidly growing interdisciplinary field incorporating scholarship from the humanities (e.g. literature, philosophy, history), social sciences, and natural sciences to investigate the past and present complex and multidimensional relationships between humans and animals (Taylor, 2013; Waldau, 2013)
264 | C h a p t e r 7 to the hegemony of the “whites” and the multiple inequalities and mistrust that have resulted.
“The goal in multi-species ethnography should not just be to give voice, agency or subjectivity to the nonhuman — to recognize them as others, visible in their difference —but to force us to radically rethink these categories of our analysis as they pertain to all beings” (Kirksey and Helmreich, 2010). As Philippe Descola (2015) and other anthropologists have argued, on the basis of a comparative analysis of a wide range of ethnographic work across the continents, native classificatory systems usually offer a continuum, rather than sharp divisions, among humans and other animal species. Indeed, human dispositions and behaviours are attributed not only to animals but also to spirits, monsters, and artefacts, contrasting to modern Western models, which generally see the categories of human and non-human as clearly defined and mutually exclusive (Peterson, 1998). In the case of Maasai and their relation with livestock, Galaty (2014) suggested that not only do people know, think about and interrelate with cattle, cattle know and think about people, shaping their interactions accordingly. Also, the place given to dogs by the Muslim culture explained for example the apparent ambiguous relationship observed between them and sheep owners in the High Atlas (Chapter 3) and consequently the implications of related practices regarding dog keeping in an CE endemic area. While dogs should be well treated like all other God creatures (dogs have a soul and therefore the right to live), a close relationship with them is discouraged since they are hygienically and spiritually perceived as impure animals, chasing away protective angels from entering a house for instance. Yet, the worldview that dominates zoonotic disease research is a view of humans and animals as biological organisms which has particular philosophical roots as suggested by Vivieros de Castro (1998). According to him, the Western ontology about the interface between nature and society is natural rather than social, “humans are organisms like the rest, body-objects in ‘ecological’ interaction with other bodies and forces, all of them ruled by the necessary laws of biology and physics” (de Castro, 1998) . By remaining in these nature-culture dichotomies, we would have missed the strong impact on toilet use played by a social “law” which is a taboo related to the sharing of a latrine with the mother-in-law in a matrilineal society, and which is contributing to the maintenance of the T. solium life cycle (Chapter 4). General Discussion | 265
Anthropology is both a natural science and a humanistic discipline, mediating between human biology and ecology on one hand and the study of human understanding on the other (Lindenbaum, 2008). Therefore, we argue that anthropological work in general is apt to emphasise the historical, contextual specificity of any particular human-animal relationship and to underline how categories, including those of “human” and “animal,” are not unavoidable nor universal but shaped in particular contexts and in different ways by actors with often conflicting perspectives and interests (Mullin, 2002). This has implications on how animals are valued, treated and prioritised (Zinsstag et al., 2015), which in turn has implications for the problems of zoonotic disease control.
Now the questions are how this kind of knowledge can be brought into OH debates, and if the current OH movement addressing zoonoses is willing to rethink its very categories, “by acknowledging the evidence of existing different worldviews of the assumed sociality of human–animal relations, and hence to grapple with the practical implications of this for engagement in field sites, for knowledge sharing, and for the design of interventions” ? (MacGregor and Waldman, 2017).
Although still limited, addressing the above questions is what could add the inclusion of a wider range of social knowledge to the conceptualisation of OH in the field of NZDs and more broadly. Including the different ways of thinking about animals and about species’ boundaries in disease control solutions, could enable novel ways of addressing zoonotic diseases which have closer integration with people’s own cultural norms (MacGregor and Waldman, 2017). For example, it could be addressing men’s knowledge and beliefs and including them in sanitation programmes instead of focussing latrine promotion messages only on women, as men are often the ones responsible for the construction of the latrines and represented in our case-study the group that preferred open defecation the most (Chapter 4). This might in turn influence our scientific ways of seeing our own disciplinary cultures (Haverkort, 2006) and generate the construction of integrated solutions such as elaborating together with the community, veterinarians, nutritionists and agronomists solutions
266 | C h a p t e r 7 to address food shortage in a Zambian rural area in order to allow pigs to be fed properly while remaining confined (Chapter 5).
If we take the example of the veterinary public health sector, the emphasis of OH on multi- and interdisciplinary cooperation has already led to the extension of its approach, such as reducing its traditional emphasis on veterinary biomedical interventions targeting single hazards (e.g. drugs and vaccines) and take a team approach instead, one that examines multiple dimensions of a shared problem (Stephen and Karesh, 2014). Positioned as a strong leader of OH, the veterinary position has adjusted and shifted with the changing need of society and within its new area of work - the ecosystem health - (Gibbs and Gibbs, 2013). Veterinary investigations and actions are more systems-based and recognise that health outcomes are derived from complex socio-ecological interactions (Stephen and Karesh, 2014). Including our case-studies, examples of veterinarians co-applying social science methodology to better understand the human dimensions of animal disease control and surveillance are more and more numerous (e.g. Sawford at al., 2012; Burniston et al., 2015, Hobbs et al., 2019). Many studies of zoonoses have also seen veterinarians working in concert with public health professionals to examine the role of the social determinants of health on community risk (Davlin et al., 2013; Schurer et al., 2013; El Berbry et al., 2015). And recently, veterinary medicine has drawn ethnographic attention (Keck, 2016). However, there is still little in the literature on the complexities of the context in which the veterinary profession operates and strives to achieve OH outcomes in policy and practice (Mbilo et al., 2018), especially in low and middle-income countries where veterinarians are generally in short supply, under-resourced, and where their contributions to public health are underestimated (Rosol et al., 2009; Valeix, 2018).
While delivering concrete results and empirical evidence of several OH added values (e.g reduced time to detection of joint disease burden, societal cost of disease and sharing of costs, interventions with highest leverage, access to care, food security and ecosystem services (Zinsstag et al., 2015)), the OH community continues to face several challenges such as, how to best promote and support multisectoral actions for health while for instance there is no shared conception of health (and disease) across General Discussion | 267 veterinary26, medical and environment sectors (Stephen and Karesh, 2014). Integrated approaches represent complex systems of communication and collaboration that are difficult to delimit and they are embedded in an ecological and cultural context where no element can be considered independently (Rüegg et al., 2018). Located at a human-wildlife-domestic animal interface, our rabies case-study illustrated how crucial the collaborations are among sectors and non-scientific stakeholders (e.g. game lodge managers) to address mistrust and the related threats posed to human health, but also for dog welfare and wildlife conservation (Chapter 6).
However, as a pivotal aspect of implementing OH approaches, the concept of “integration” itself lacks a universal definition. Words like “collaboration”, “cooperation” and “coordination”, often used interchangeably in OH papers, are more generally seen as elements of, or complementary to, integration (Alexsson and Alexsson, 2006). The ones who have attempted to integrate socio-economic and ecological drivers of disease into broad, systemic models, processes and frameworks, have grown them out of distinct scholarly cultures, each with their own languages, dialects, cultures and conferences (Waltner-Toews, 2017). Consequently, when translated at the local and national levels, strong differences in perspectives about OH among different professions can be major barriers to integration of those professions into OH implementation (Smith et al. 2015; Valeix, 2018). “Integration” is not achieved spontaneously, as well as trust between stakeholders and communities (Binot et al., 2015; Cleaveland et al., 2017), and, although having different goals does not necessarily make engagement impossible, it is essential to reflect on the framing, philosophical, personal values and applied meanings of such key concepts among the different stakeholders. An understanding for instance of the role veterinarians play among other stakeholders in managing zoonotic diseases and how their role might be enhanced at a national and local scale in developing countries would be an added value with respect to integration in OH (Valeix, 2018). By proposing a framework to
26 For instance, Gunnarson (2006) found that few veterinary textbooks in pathology, epidemiology, internal medicine and other areas had any health or disease definition at all. For those that had, the definitions could be split into five categories (health as normality, health as biological function, health as homeostasis, health as physical and psychological well-being and health as productivity including reproduction) but they all had little impact on how health and disease were handled within the profession (Gunnarson, 2006).
268 | C h a p t e r 7 probe the social dimensions and power dynamics among professional participants of a OH programme in Ghana, Valeix (2018) informed about this missing link. Others raised the fact that good, strong, new governance27 and funding strategies are required to ensure that collaborations extend beyond the current urgent issue or funding opportunity (Bennett et al., 2018; Rüegg et al., 2018). But again, how this process will be built? How to get to grips with governing multisectoral actions for health in low-income and middle-income countries, especially in a situation where the starting position of the different actors is not equitable and where the differences in status, power, and resource availability are tremendous? (Haverkort, 2006). Here, in contexts of poverty and affliction, health system research tends to be down the list of priorities and disciplinary divisions remain more firmly entrenched. At the same time, wealthier scientific and development partners are often focused more on generating evidence for new tools and technologies (Bardosh, 2018).
Methodological and conceptual challenges will be addressed across three themes: (1) interdisciplinarity, (2) how to go from local to global and vice-versa, and (3) the socio- ecological approach.
7.5.1 Interdisciplinary
From a methodological and human point of view, interdisciplinarity, including applied anthropology to health (zoonotic diseases) is a long and difficult road. In multiple disciplinary approaches, there is this continuum of involvement to varying degrees ranging from multidisciplinary (working independently with several disciplines; drawing on knowledge from them but staying within their boundaries), to interdisciplinarity (working together on a same project between several disciplines; analyzing, synthesising and harmonising links between disciplines into a coordinated and coherent whole) and finally transdisciplinarity (working across and beyond several disciplines, including stakeholders, non-scientists and non-academic
27 Governance defined as “the complex mechanisms, processes, relationships and institutions through which citizens and groups articulate their interests, exercise their rights and obligations, and mediate their differences” (WHO, 2011). General Discussion | 269 participants; integrating the natural, social and health sciences in a humanities context, and transcends their traditional boundaries) (Flinterman et al., 2001; Tress et al., 2005) . Although increasingly encouraged and demonstrating benefits, pursuing such multiple disciplinarity is also demanding and facing many barriers such as language problems, insufficient time or funding for the project, institutional constraints, authorship issues, discipline conflicts, or unequal power among disciplines (Choi and Pak, 2007). In the case of interdisciplinarity wherein we framed our collaborative and integrative work, “interdisciplinarity only has a chance if those who belong to the cultures of social science and those of the culture of medicine give up their ethnocentric fear of dissenting beliefs and accept the practical consequences of the conviction that reality itself is multidisciplinary” (Van der Geest, 1995).
Furthermore, the multiple types of convergences of scientific disciplines observed in the Anthropocene era imply not just technical issues which delay the process (e.g. few interdisciplinary ethical committees, few interdisciplinary peer-reviewed journals, few reviewers feeling at ease in this exercise,…) but a thoroughly moral problem, laced with questions of responsibility such as “who can act, and how?” instead of “how should we act?” (Brown and Nading, 2019). This issue of “response-ability” (Haraway, 2008; Latour, 2014) may due to the fact that converging multiple scientific disciplines together implies larger systems of power and knowledge that evolve and are changing over time, including human health and animal health sectors, quantitative and qualitative research, economic and well-being benefits, international and national priorities.
7.5.2 From local to global and vice versa
Linking an understanding of local realities (including biomedical and environmental data) into global health programmes while embedding them successfully in health systems and ensure they are still reaching their full potential in diverse local settings, remains very challenging (Bardosh, 2018). Given the diversity of local biological, environmental and social worlds (including politics and economy), developing universal strategies that can be neatly adapted to any local context (e.g. for emerging infectious diseases) is impossible (Wolf, 2015). Therefore, the pertinent question that
270 | C h a p t e r 7 should be answered is how to synergise top-down and bottom-up approaches rather than how to address globally local socio-cultural barriers?
First of all, local adaptation does not occur in isolation from broader multilevel governance structures involving governments, donors, international agencies, NGOs and the private sectors (Bardosh et al., 2017b). Indeed, following the OH demands of institutional and intersectoral collaborations, new “global assemblages” (Ong and Collier, 2006) have emerged in which a broader range of actors is claiming the right to manage interventions, monitor spending, and determine beneficiaries (Brown, 2015). This is why Okello and colleagues (2015) underlined that the process analysis by which national policy is developed to control the NZDs across endemic regions is somewhat a more fundamental starting point for recommendations for their control, particularly given the multi-sectoral, multi-actor approaches required. Furthermore, the organising logics (“One-isms”) involved in translating control projects across international, national, and local scales often undervalue diversity and locally contingent practices involved in the production of health (Hinchliffe, 2015; MacGregor and Waldman, 2017) focussing on animals as carriers of diseases that might cause harm to humans rather than as companions, co-workers, or even relatives (Rock, 2017). The mismatch in professional and cultural interests and values between researchers and policymakers can also be a significant barrier to linking sound knowledge with effective action and salient policy as well as very constructive and innovative solutions (Bardosh et al., 2017a).
The understanding of macro-level drivers definitively constitutes therefore an important part of analysing such micro-level dynamics. For example, dynamic global drivers of change in livestock systems, including economic growth and income, demographic and land use changes, dietary adjustments and technological change, shape political and economic structures that affect poor farmers and marginal producers as well as those reliant on livelihoods in animal supply chains (Steinfeld et al., 2006). It is less the local findings that should be scaled-up than the approaches elaborated to efficiently integrate the complex and varying dynamic of transmission and their multiple components. Hence, the question should become at what scale can community-based approaches be successfully used and what is involved in scaling- up? (Bardosh et al., 2017b). General Discussion | 271
7.5.3 Socio-ecological approach
By following the natural evolution of the OH movement, our work reflects also the gap identified by numerous scholars conducting to a certain convergence of EcoHealth and One Health (Zinsstag, 2012; Gibbs and Gibbs, 2013; Preston et al., 2013). While OH is helping to pave a path forward by fostering development of the intellectual tools for a collaborative, integrated approach, the movement still suffers from a lack of strong environmental stakeholders (Destoumieux-Garzón et al. 2018; Khan et al. 2018). With the fear for pandemics being a strong driver for the OH movement (Gibbs, 2014), the call for collaboration has prevailed human health attitude toward disease events in animals as an “us vs. them” paradigm that considers the degree of threat that animals themselves pose to humans (Rabinowitz et al. 2008). Consequently, the negative framing of « nature » in OH discourses as a danger for humanity could also be considered as a barrier to collaboration and explain a weaker inclusion of environmental science in OH communities (Antoine-Moussiaux et al., 2019).
Yet, becoming increasingly consensual among experts in its modern formulation (Gibbs, 2014), the OH movement is finally calling for a shift in perspective from “us vs. them” to “shared risks” (Rabinowitz et al. 2008). This is in line with ecosystem approaches to health (Rapport et al. 1999), recognising an inextricable linkage between people and nature. These approaches emphasise that humans must be seen as a part of human–environment systems or social-ecological systems (SES) (Ostrom, 2007). Together with a multi-sectoral and multi-disciplinary approach at various levels, adopting a socio-ecosystem approach to address the environmental dimension for zoonotic health problems would fill this gap. This approach is for instance already well developed and supported by the South-East Asian OH movement (Roger et al., 2016). It will also allow the OH communities of practice to address many of the pressing determinants of health that will confront us in the next century such as water security, biodiversity conservation, climate change, social justice, equitable access to resources, pollution and land use planning, factors that have also a profound impact on human health, animal health and welfare (Stephen and Karesh, 2014).
The SES concept is borrowed from the paradigm of ‘sustainability science’ that focuses explicitly on the dynamic interactions between nature and society and is committed to place-based and solution-driven research across multiple scales
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(Gardner et al., 2013). Global changes from human activities, describing the conditions of the Anthropocene, include profound alterations of ecosystems and the services they provide to humanity (Carpenter et al., 2012). Adopting this approach means in practice taking into account ecological and social dynamics at play, in link with epidemiological patterns to understand of how ecological processes (e.g. hosts and reservoirs populations dynamics, movements, contacts) interact with social processes (risk perception, local practices, power games, surveillance and control measures' acceptability by beneficiaries) at the animal–human–environment interface (Binot et al., 2015)
By following and adopting a disease control driven research instead of a social one, what did we lose and what did we win in terms of interdisciplinary dialogue? We would like to reflect on how the discipline of anthropology and its main research techniques can be effectively and efficiently involved in NZDs control, without however neglecting their own specific methodological requirements.
Anthropology is presented as a framework to better understand the NZD control context, in order to propose and accompany more efficient changes in attitude, practice, knowledge, interactions at local actors’ level. As such, the case-studies present a restrictive use of anthropology, expressed in terms of “knowledge”, “awareness”, “practices”, “attitudes” (cfr. KAP studies), which can be easily taken up by researchers from other disciplines. Yet, this transfer of technical competencies remains indissociable from the acquisition of a set of concepts and, more globally, from a theoretical approach which favours the study of the meaning and of social relationships. This is why this work offers real monographs (notably regarding the perception of dogs for different sociocultural categories), which is also promising for designing efficient and adapted health promotion messages. The take-over has its limits.
Although it is different for a study of the social etiology of specific NZDs than for a study on the health consequences of societal arrangements, differences and similarities of the gendered organisation of kinship and economic production should General Discussion | 273 have been additional selection criteria for the selected case studies. With political dimension, economic burden, public health, geographical scope, rural development, international agencies as guiding selection criteria, we would have been able to also better highlight challenges and issues regarding the appropriateness of a disease control toolbox for each of the case studies.
The particular anthropological posture used in this work raises a more critical question: Is it not in contradiction with the purpose of anthropology? Is it not “instrumentalisation” or “manipulation” to be asked as an anthropologist to contribute at improving the efficacy of an exogenous intervention that is not co- constructed with local stakeholders, and consequently contributing threatening the communities by deconstructing social mechanisms and levers for actions? To remain in the dialogue, we think that such anthropological implication should not be questioned in terms of instrumentalisation from a discipline to another. The essence is about respect, and especially the respect for the epistemological characteristics and the methodological approaches specific to each discipline. Following Lefèvre and de Suremain (2002) experiences, more fundamentally, anthropology can contribute through the development of common conceptual frameworks, elaborated from an interdisciplinary dialogue instituted from the conception of the research to its conclusion.
Although this observation precisely explains all the drawbacks of our work (no social questions were raised, lack of an in-depth elaboration on theory and concepts relevant to understand the social context in more general and abstract terms, no destructuration of the medical rationale, no in-depth reflections at macro-societal levels, few considerations of other institution and organisation at play, which can constitute barriers or levers for collective action,…), this PhD brings something new in the framework of a complementarity between social and medical sciences. Because applied research is concerned with using the knowledge acquired through research to contribute directly to the understanding of a contemporary issue, in order to face new health challenges, this bridge that we built will provide to the OH movement and future interdisciplinary research team, capacities to engage in a more fruitful and vigorous dialogue with social scientists.
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Our work, initiated with the first case-study of CE in Morocco, at a period when the OH concept was entering in the sphere of European Union’s projects28, followed and also fed the evolution of this movement. After ten years working in this field, we built this specific research niche and network, at the interface with the biomedical and the biosocial world. In multiple scientific and academic fora, we continuously have shared and disseminated these anthropological research findings in cross-disciplinary dialogues and constructive collaborative efforts with the animal and human health sectors engaged in the control of NZDs and beyond. Moreover, we deeply think that it is not too late for our seeds to hatch today. On the contrary, if OH is a way to hone our peripheral vision through the understanding and engaging the whole set of complex interactions - feedback loops, non-linear dynamics, cascade effects at different scales- , it will not succeed without serious engagement and cooperation (rather than passive understanding) of all kinds of actors (farmers included), and without a serious and rigorous study of the associations (the sociability) that make health possible and ill- health and or disease more prevalent (Craddock and Hinchliffe, 2015). Central to the concept of OH is the need to bring disparate actors, from the national, district and local level, into new forms of relationship (Bardosh et al., 2016). As culture is always evolving, adapted control measures must be implemented and negotiated with the population in order to be effective and sustainable.
According to us, an initial step should be a multi-disciplinary understanding of the transmission by employing the disease hotspot, informed by epidemiological data (e.g. High Atlas in Morocco for CE, Petauke district in Zambia for TSTC and Mnisi study area for rabies) as an analytical tool to mark out sites where different variants of human– animal–nonhuman entanglements facilitate the movement of pathogens (Brown and Kelly, 2014). Furthermore, we should ask ourselves which of our main anthropological findings in our three case-studies – the perceived life cycle of E.
28 The European Union's Seventh Framework Programme (FP7/2007-2014) included projects such as Integrated Control of Neglected Zoonoses in Africa (ICONZ - www.iconzafrica.org), One Health Next Scientific Generation in the Sahel and Maghreb (OH-NEXTGEN - www.oh-nextgen.eu) and Advocacy for Neglected Zoonotic Diseases (ADVANZ - www.advanz.org/) (Okello et al., 2015). General Discussion | 275 granulosus and place of dogs among Muslim sheep owners; the type of descent, matrilineal or patrilineal, as important factor that has a significant influence on the sanitation practices of a rural community; gendered resource management and priorities regarding free-roaming breeding practices in poor rural communities; and dog vaccination narratives in a human-wildlife conflicts area - can be used to refine intervention strategies. Answering this will first require thinking about the context of implementation (including resource-constraints and working norms) and also about the prioritisation process (Bardosh et al., 2017a). Therefore, we suggest that this reflective bottom-up approach of progressive problem solving is initiated already within a multi-disciplinary team. Therefore, we recommend to start with the mapping of all the stakeholders involved in the control programme and qualitatively evaluate what is their respective knowledge about this programme and its activities, their role, and their perception about its efficiency and implementation. The following steps would be to organise several round table meetings with the different categories of stakeholders, separately or mixed, where both qualitative and quantitative findings should be presented and discussed to design new and more adapted control measures by using several negotiations, mind mapping and planning techniques according to the specific audience.
When decisions on which interventions can be implemented will be made by such integrative process, we further argue that integrating rapid ethnography29 into scaled-up OH programmes together with epidemiological research can guide NZDs control. Rapid ethnography will provide the vital social context to contribute to explaining epidemiological findings as well as local understandings and responses to our intervention strategy and potential future avenues for developing more culturally-appropriate interventions (Bardosh et al., 2014). Concretely, regarding the delivery of interventions, this could be the flexible socio-anthropological framework developed by Bardosh (2018) to improve the effectiveness of neglected tropical disease interventions. It includes five “intervention domains” where the effectiveness
29 Since Scrimshaw and Hurtado (1988) posed the question, “must one spend a year in the field collecting ethnographic data in order to make useful recommendations for a health program?”, a wide range of rapid research approaches quickly emerged and includes rapid ethnography defined as the collection of field methods to capture the complexities of service provision, the social and cultural factors shaping healthcare use and delivery, and the nuanced practices of care provision in short timeframes (Bentley et al., 1988; Vindrola-Padros and Vindrola-Padros, 2018).
276 | C h a p t e r 7 of the interventions should be negotiated and determined at the local level: 1) the terrain of intervention (including seasonality and geographical variability); 2) community agency (including local knowledge, risk perceptions, behaviours, leadership and social pressure); 3) the strategies and incentives of field staff (skills, motivations, capabilities and support); 4) the socio-materiality of technology (characteristics of intervention tools and the adoption process itself); and 5) the governance of interventions (policy narratives, available expertise, bureaucracy, politics and the utilisation of knowledge).
However, the implementation of this framework requires a strong emphasis on the use of social research data to shape the implementation, the value of critical self- reflection and the acceptance that intervention approaches (including the proposed biomedical strategies) may need to be changed in the field (Bardosh et al., 2014). Anthropological theory has a powerful grasp of the connection between broad-scale social structures and intimate lived realities, and its methods are perhaps unequalled in capturing the nuances of context (Closser and Finley, 2016). We are convinced that interdisciplinary teamwork is useful and even substantial for solving complex real world problems such as the control of NZDs in developing countries, because such problems do not stay within artificial academic disciplinary boundaries (Choi and Pak, 2006). Yet, we also would like to stress that anthropologists themselves must adopt a new reflexivity and have a careful examination of the biases and conventions of the discipline to make the most of their contributions such as accepting the need for speed and adjusting their approach (Jordan, 2013; Closser and Finley, 2016). If the context changes, solutions may change as well as the notion of “truths” depending on the context and narrative. In the context of a ‘real world’ of evolving species, changing cultures and unstable climates, scientific attitudes must therefore be examined and untangled creating scholarly and public spaces for managing constructive and high- quality conflicts (Waltner-Toews, 2017).
As “newcomers” in the field of veterinary and medical science working on zoonoses, anthropologists involved in the OH movement and working on human-animal-disease interactions are also newcomers in the field of medical anthropology. The idea of integration of knowledge, by taking the best of the disciplines or the best of both scientific and local knowledge, is not always realistic and it can create discomfort. Yet, General Discussion | 277 people need to prepare for chaos and accept uncertainty as a natural condition (cfr the concept of “non-linear thinking”). We cannot control the entire universe but we can communicate with applied health fields the same way we would ask health professionals to communicate with our ethnographic participants: in thoughtful, culturally appropriate language, with an eye to their needs and perspectives and the resources they have within reasonable access (Closser and Finley, 2016). All effective collaboration requires mutual respect, trust and acknowledgement of the complementary skills of all parties. For instance, finding an equilibrium between changing behaviours and adapting the control measures to the human practices is a valuable and constructive outcome that can emerge from collaborative work.
Our research highlights a diversity of core values rooted in different systems and temporal–spatial scales that often gives rise to a gap between policy and practice, and raises the concern that cross-cultural perspectives (MacGregor and Waldman, 2017) are still underrepresented in the multiple OH narratives and their management. The realm of the human-animal-disease-interactions has been limited to ‘natural versus cultural’ domains and frequently conceived of as biological phenomena in OH studies instead of a biocultural one which rather integrates the social and cultural dimensions generated by the human-animal relations. Incorporating anthropology into OH approaches should provide a more nuanced and expanded account of the fluidity of bodies, categories and boundaries as drawn up by existing ethnographies on cattle in east and southern Africa for example (Galaty, 2014). Moreover, exploring the lives of those who experience these complex entanglements between humans, animals, and pathogens on a daily basis, would allow policymakers and practitioners to fully comprehend the social and ecological processes that catalyse today’s cross-species pathogens.
Ainslie, A., 2005. Farming Cattle, Cultivating Relationships: Cattle Ownership and Cultural Politica in Peddie District, Eastern Cape. Soc. Dyn. 31, 129–156. Antoine-Moussiaux, N., Janssens de Bisthoven, L., Leyens, S., Assmuth, T., Keune, H., Zinsstag, J., . . ., Vanhove, M.P.M., 2019. The good, the bad and the ugly: framing debates on nature in a One Health community. Sustain. Sci. (in press) https://doi.org/10.1007/s11625- 019-00674-z Axelsson, R., Axelsson, S.B., 2006. Integration and collaboration in public health--a conceptual
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framework. Int. J. Health Plann. Manage. 21, 75–88. Bardosh, K., Inthavong, P., Xayaheuang, S., Okello, A.L., 2014. Controlling parasites, understanding practices: The biosocial complexity of a One Health intervention for neglected zoonotic helminths in northern Lao PDR. Soc. Sci. Med. 120, 215–223. Bardosh, K.L., Berbri, I. El, Ducrotoy, M., Bouslikhane, M., Ouafaa, F.F., Welburn, S.C., 2016. Zoonotic encounters at the slaughterhouse: Pathways and possibilities for the control of Cystic Echonococcosis in Northern Morocco. J. Biosoc. Sci. 48 Suppl 1, S92–S115. Bardosh, K.L., Scoones, J.C., Grace, D., Kalema-Zikusoka, G., Jones, K.E., de Balogh, K., . . ., Dzingirai, V., 2017a. Engaging research with policy and action: what are the challenges of responding to zoonotic disease in Africa? Philos. Trans. R. Soc. B. Biol. Sci. 372, 1-10. Bardosh, K.L., Ryan, S.J., Ebi, K., Welburn, S., Singer, B., 2017b. Addressing vulnerability, building resilience: Community-based adaptation to vector-borne diseases in the context of global change. Infect. Dis. Poverty 6, 166. Bardosh, K.L., 2018. Towards a science of global health delivery: A socio-anthropological framework to improve the effectiveness of neglected tropical disease interventions. PLoS Negl. Trop. Dis. 12, e0006537. Bennett, S., Glandon, D., Rasanathan, K., 2018. Governing multisectoral action for health in low-income and middle-income countries: Unpacking the problem and rising to the challenge. BMJ. Glob. Health. 3, e000880. Bentley, M.E., Pelto, G.H., Straus, W.L., Schumann, D.A., Adegbola, C., de la Pena, E., . . ., Huffman, S.L., 1988. Rapid ethnographic assessment: Applications in a diarrhea management program. Soc. Sci. Med. 27, 107–116. Binot, A., Duboz, R., Promburom, P., Phimpraphai, W., Cappelle, J., Lajaunie, C., . . ., Roger, F.L., 2015. A framework to promote collective action within the One Health community of practice: Using participatory modelling to enable interdisciplinary, cross-sectoral and multi-level integration. One Health. 1, 44–48. Brown, H., Kelly, A.H., 2014. Material proximities and hotspots: Toward an anthropology of viral hemorrhagic fevers. Med. Anthropol. Q. 28, 280–303. Brown, H., 2015. Global health partnerships, governance, and sovereign responsibility in Western Kenya. Am. Ethnol. 42, 340–355. Brown, H., Nading, A.M., 2019. Introduction: Human Animal Health in Medical Anthropology. Med. Anthropol. Q. 33, 5–23. Burniston, S., Okello, A.L., Khamlome, B., Inthavong, P., Gilbert, J., Blacksell, S.D., . . ., Welburn, S.C., 2015. Cultural drivers and health-seeking behaviours that impact on the transmission of pig-associated zoonoses in Lao People’s Democratic Republic. Infect. Dis. Poverty. 4, 1-12. Carpenter, S.R., Folke, C., Norström, A., Olsson, O., Schultz, L., Agarwal, B., . . ., Spierenburg, M., 2012. Program on ecosystem change and society: An international research strategy for integrated social-ecological systems. Curr. Opin. Environ. Sustain. 4, 134–138. Choi, B.C.K., Pak, A.W.P., 2006. Multidisciplinarity, interdisciplinarity and transdisciplinarity in health research, services, education and policy: 1. Definitions, objectives, and General Discussion | 279
evidence of effectiveness. Clin. Investig. Med. 29, 351–364. Choi, B.C.K., Pak, A.W.P., 2007. Multidisciplinarity, interdisciplinarity, and transdisciplinarity in health research, services, education and policy: 2. Promotors, barriers, and strategies of enhancement. Clin. Investig. Med. 30, 224–232. Cleaveland, S., Sharp, J., Abela-Ridder, B., Allan, K.J., Buza, J., Crump, J.A., . . ., Halliday, J.E.B., 2017. One Health contributions towards more effective and equitable approaches to health in low- and middle-income countries. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-11. Closser, S., Finley, E.P., 2016. A New Reflexivity: Why Anthropology Matters in Contemporary Health Research and Practice, and How to Make It Matter More. Am. Anthropol. 118, 385–390. Craddock, S., Hinchliffe, S., 2015. One world, one health? Social science engagements with the one health agenda. Soc. Sci. Med. 129, 1–4. Crutzen, P.J., Stoermer, E.F., 2000. The “Anthropocene.” Global Change Newsletters. 41, 17– 18. Davlin, S., Lapiz, S.M., Miranda, M.E., Murray, K., 2013. Factors associated with dog rabies vaccination in Bhol, Philippines: Results of a cross-sectional cluster survey conducted following the island-wide rabies elimination campaign. Zoonoses Public Health. 60, 494– 503. de Castro, E.V., 1998. Cosmological Deixis and Amerindian Perspectivism. J. R. Anthropol. Inst. 4, 469–488. Decker, D.J., Evensen, D.T.N., Siemer, W.F., Leong, K.M., Riley, S.J., Wild, M.A., . . ., Higgins, C.L., 2010. Understanding risk perceptions to enhance communication about human-wildlife interactions and the impacts of zoonotic disease. ILAR J. 51, 255–261. Descola, P., 2015. Beyond Nature and Culture. University of Chicago Press, Chicago. Destoumieux-Garzón, D., Mavingui, P., Boetsch, G., Boissier, J., Darriet, F., Duboz, P., . . ., Voituron, Y., 2018. The One Health Concept: 10 Years Old and a Long Road Ahead. Front. Vet. Sci. 5, 1-13. de Vries, D., Leslie, P., McCabe, J., 2006 Livestock acquisitions dynamics in nomadic pastoralist herd demography: A case study among Ngisonyoka herders of South Turkana, Kenya. Hum. Ecol. 34, 1–25. El Berbri, I., Ducrotoy, M.J., Petavy, A.-F., Fassifihri, O., Shaw, A.P., Bouslikhane, M., . . ., Dakkak, A., 2015. Knowledge, attitudes and practices with regard to the presence, transmission, impact, and control of cystic echinococcosis in Sidi Kacem Province, Morocco. Infect. Dis. Poverty 4, 1-15. Fincher, C.L., Thornhill, R., Murray, D.R., Schaller, M., 2008. Pathogen prevalence predicts human cross-cultural variability in individualism/collectivism. Proc. R. Soc. B. Biol. Sci. 275, 1279-1285. Flinterman, J.F., Teclemariam-Mesbah, R., Broerse, J.E.W., Bunders, J.F.G., 2001. Transdisciplinarity: The New Challenge for Biomedical Research. Bull. Sci. Technol. Soc. 21, 253–266.
280 | C h a p t e r 7
Galaty, J.G., 2014. Animal spirits and mimetic affinities: The semiotics of intimacy in African human/animal identities. Crit. Anthropol. 34, 30–47. Gangestad, S.W., Haselton, M.G., Buss, D.M., 2006. Evolutionary foundations of cultural variation: Evoked culture and mate preferences. Psychol. Inq. 17, 75–95. Gardner, T.A., Ferreira, J., Barlow, J., Lees, A.C., Parry, L., Vieira, I.C.G., . . ., Zuanon, J., 2013. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368, 1-11. Gibbs, E.P.J., 2014. The evolution of One Health: a decade of progress and challenges for the future. Vet. Rec. 174, 85–91. Gibbs, S.E., Gibbs, E.P., 2013. The historical, present, and future role of veterinarians in One Health. Curr. Top. Microbiol. Immunol. 365, 31–47. Grover, M., Bessell, P.R., Conan, A., Polak, P., Sabeta, C.T., Reininghaus, B., Knobel, D.L., 2018. Spatiotemporal epidemiology of rabies at an interface between domestic dogs and wildlife in South Africa. Sci. Rep. 8, 1-9. Gunnarsson, S., 2006. The conceptualisation of health and disease in veterinary medicine. Acta Vet. Scand. 48, 1-6. Haraway, D.J., 2008. When species meet. University of Minnesota Press, 360 pp. Haverkort, B., 2006. Dialogues within and between different sciences : issues and strategies from endogenous perspective. Mov. Worldviews - Reshaping Sci. Policies Pract. Endog. Sustain. Dev. 345–362. Hinchliffe, S., 2015. More than one world, more than one health: Re-configuring interspecies health. Soc. Sci. Med. 129, 28–35. Hobbs, E.C., Mwape, K.E., Phiri, A.M., Mambwe, M., Mambo, R., Thys, S., . . ., Gabriël, S., 2019. Perceptions and acceptability of piloted Taenia solium control and elimination interventions in two endemic communities in eastern Zambia. Transbound. Emerg. Dis. Jordan, B., 2016. Advancing ethnography in corporate environments : Challenges and emerging opportunities. Routledge, 228pp Keck, F., 2016. Veterinary Anthropology: When Medical Anthropology Meets Animal Studies. Med. Anthropol. Theory. September 7. Accessed May 2019. http://www. medanthrotheory.org/read/6385/veterinary-anthropology. Keck, F., Lynteris, C., 2018. Zoonosis: Prospects and challenges for medical anthropology. Med. Anthropol. Theory. 5, 1-14. Kelly, M.P., Barker, M., 2016. Why is changing health-related behaviour so difficult? Public Health. 136, 109–116. Khan, A., Naz, K., Ahmed, H., Simsek, S., Afzal, M.S., Haider, W., . . ., Yayi, G., 2018. Knowledge, attitudes and practices related to cystic echinococcosis endemicity in Pakistan. Infect. Dis. Poverty. 7, 1-15. Kirksey, S.E., Helmreich, S., 2010. The Emergence of Multispecies Ethography. Cult. Anthropol. 25, 545–576. Lapinski, M.K., Funk, J.A., Moccia, L.T., 2015. Recommendations for the role of social science General Discussion | 281
research in One Health. Soc. Sci. Med. 129, 51–60. Latour, B., 2014. Agency at the Time of the Anthropocene. New Lit. Hist. 45, 1–18. Leach, M., Bett, B., Said, M., Bukachi, S., Sang, R., Anderson, N., . . ., Koninga, J., 2017. Local disease-ecosystem-livelihood dynamics: reflections from comparative case studies in Africa. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-18. Lefèvre, P., de Suremain, C.-É., 2002. Approches multiples Les contributions pourquoi , comment et à quelles conditions ? Cah. Santé 12, 77–85. Lindenbaum, S., 2008. Review. Understanding kuru: the contribution of anthropology and medicine. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363, 3715–3720. Low, B.S., 1990. Marriage systems and pathogen stress in human societies. Integr. Comp. Biol. 30, 325–340. MacGregor, H., Waldman, L., 2017. Views from many worlds: unsettling categories in interdisciplinary research on endemic zoonotic diseases. Philos. Trans. R. Soc. B Biol. Sci. 372, 1–9. Marteau, T.M., Hollands, G.J., Kelly, M.P., 2015. Changing population behavior and reducing health disparities: Exploring the potential of “choice architecture” interventions. In: Kaplan, RM., Spittel, M., David, DH. (Eds.), Population Health: Behavioral and Social Science Insights, AHRQ Publication, Rockville, pp. 105-125. Mbilo, C., Léchenne, M., Mauti, S., Chitnis, N., Tschopp, R., Zinsstag, J., 2018. Rabies in dogs, livestock and wildlife: a veterinary perspective. Rev. Sci. Tech. Off. Int. Epiz. 37, 331–340. Michie, S., West, R., Campbell, R., Brown, J., Gainforth, H., 2014. ABC of behaviour change theories. Silverback Publishing, 504 pp. Muehlenbein, M.P., 2016. Disease and Human/Animal Interactions. Annu. Rev. Anthropol. 45, 395–416. Mullin, M., 2002. Animals and anthropology. Soc. Anim. 10, 387–393. Nading, A.M., 2013. Humans, Animals, and Health: From Ecology to Entanglement. Environ. Soc. 4, 60–78. Napolitano, D.A., Jones, C.O.H., 2006. Who needs “pukka1 anthropologists”? A study of the perceptions of the use of anthropology in tropical public health research. Trop. Med. Int. Heal. 11, 1264–1275. Okello, A.L., Beange, I., Shaw, A., Moriyón, I., Gabriël, S., Bardosh, K., . . ., Welburn, S.C., 2015. Raising the Political Profile of the Neglected Zoonotic Diseases: Three Complementary European Commission-Funded Projects to Streamline Research, Build Capacity and Advocate for Control. PLoS Negl. Trop. Dis. 9, 1–10. Ong, A., Collier, S.J., 2006. Global assemblages : technology, politics, and ethics as anthropological problems. Wiley-Blackwell Pub, 494 pp. Ostrom, E., 2007. A diagnostic approach for going beyond panaceas. Proc. Natl. Acad. Sci. U. S. A. 104, 15181–15187. Panter-Brick, C., Clarke, S.E., Lomas, H., Pinder, M., Lindsay, S.W., 2006. Culturally compelling strategies for behaviour change: A social ecology model and case study in malaria
282 | C h a p t e r 7
prevention. Soc. Sci. Med. 62, 2810–2825. Peterson, A.L., 1998. Nature and Society: Anthropological Perspectives by Philippe Descola and Gisli Palsson (Eds). Agric. Human Values. 15, 179–183. Preston, N.D., Daszak, P., Colwell, R.R., 2013. The human environment interface: Applying ecosystem concepts to health. Curr. Top. Microbiol. Immunol. 365, 83–100. Prokop, P., Usak, M., Fancovicová, J., 2010. Risk of parasite transmission influences perceived vulnerability to disease and perceived danger of disease-relevant animals. Behav. Processes. 85, 52–57. Quinlan, R.J., 2007. Human parental effort and environmental risk. Proceedings. Biol. Sci. 274, 121–125. Rabinowitz, P.M., Odofin, L., Dein, F.J., 2008. From “Us vs. Them” to “Shared Risk”: Can Animals Help Link Environmental Factors to Human Health? Ecohealth. 5, 224–229. Rapport, D.J., Bohm, G., Buckingham, D., Cairns, J., Costanza, R., Karr, J.R., . . ., Whitford, W.G., 1999. Ecosystem Health: The concept, the ISEH, and the important tasks ahead. Ecosyst. Health. 5, 82–90. Rock, M.J., 2017. Who or what is ‘the public’ in critical public health? Reflections on posthumanism and anthropological engagements with One Health. Crit. Public Health. 27, 314–324. Roger, F., Caron, A., Morand, S., Pedrono, M., de Garine-Wichatitsky, M., Chevalier, V., . . ., Binot, A., 2016. One Health and EcoHealth: the same wine in different bottles? Infect. Ecol. Epidemiol. 6, 1-4. Rosol, T.J., Moore, R.M., Saville, W.J.A., Oglesbee, M.J., Rush, L.J., Mathes, L.E., Lairmore, M.D., 2009. The need for veterinarians in biomedical research. J. Vet. Med. Educ. 36, 70–75. Rü egg, S.R., Hä sler, B., Zinsstag, J., 2018. Integrated approaches to health : a handbook for the evaluation of One Health. Wageningen Academic Publishers, 256 pp. Sawford, K., Vollman, A.R., Stephen, C., 2012. A focused ethnographic study of Sri Lankan government field veterinarians’ decision making about diagnostic laboratory submissions and perceptions of surveillance. PLoS One. 7, e48035. Schurer, J.M., Ndao, M., Skinner, S., Irvine, J., Elmore, S.A., Epp, T., Jenkins, E.J., 2013. Parasitic Zoonoses: One Health Surveillance in Northern Saskatchewan. PLoS Negl. Trop. Dis. 7, e2141. Scoones, I., 2010. Avian influenza : Science, policy and politics. Earthscan, London, 261 pp. Sherman, P.W., Billing, J., 1999. Darwinian Gastronomy: Why We Use Spices. Bioscience 49, 453–463. Smith, J., Taylor, E.M., Kingsley, P., 2015. One World-One Health and neglected zoonotic disease: Elimination, emergence and emergency in Uganda. Soc. Sci. Med. 129, 12–19. Steinfeld, H., Wassenaar, T., Jutzi, S., 2006. Livestock production systems in developing countries: Status, drivers, trends. Rev. Sci. Tech. 25, 505–516. Stephen, C., Karesh, W.B., 2014. Is One Health delivering results? Introduction. Rev. Sci. Tech. 33, 375–92. General Discussion | 283
Swanepoel, F., Stroebel, A., Moyo, S., 2010. The role of livestock in developing communities: Enhancing multifunctionality. University of the Free State and CTA, Cape town. Taylor, N., 2013. Humans, Animals, and Society: An Introduction to Human-Animal Studies. Lantern, New York. Tress, B., Tress, G., Fry, G., 2005. Researchers’ Experiences, Positive and Negative, in Integrative Landscape Projects. Environ. Manage. 36, 792–807. Valeix, S.F., 2018. One Health Integration: A Proposed Framework for a Study on Veterinarians and Zoonotic Disease Management in Ghana. Front. Vet. Sci. 5, 1-7. van der Geest, S., 1995. Overcoming ethnocentrism: how social science and medicine relate and should relate to one another. Soc. Sci. Med. 40, 869–872. Vindrola-Padros, C., Vindrola-Padros, B., 2018. Quick and dirty? A systematic review of the use of rapid ethnographies in healthcare organisation and delivery. BMJ Qual. Saf. 27, 321–330. Waldau, P., 2013. Animal studies : an introduction. Oup Usa, 384 pp. Waltner-Toews, D., 2017. Zoonoses, One Health and complexity: wicked problems and constructive conflict. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 1-9. WHO, 2011. Health systems strengthening glossary. Accessed in May 2019. https://www.who.int/healthsystems/hss_glossary/en/index5.html Wolf, M., 2015. Is there really such a thing as “One Health”? Thinking about a more than human world from the perspective of cultural anthropology. Soc. Sci. Med. 129, 5–11. Zinsstag, J., 2012. Convergence of EcoHealth and One Health. Ecohealth 9, 371–373. Zinsstag, J., Schelling, E., Waltner-Toews, D., Whittaker, M., Tanner, M., 2015. One Health - The Theory and Practice of Integrated Health Approaches (2015th ed), Statewide Agricultural Land Use Baseline 2015. CAB International.
While globalisation has generated many benefits for society, it has also created many new challenges, particularly with regard to human, animal, and environmental health. Neglected Zoonotic Diseases (NZDs) are common where poverty, reliance on livestock or wildlife for social and financial capital, poor resilience, and the close proximity of people and their animals favour transmission. These features also raise a growing challenge to the life sciences to understand how these pathogens crossing species barriers are interwoven into non-linear and multifaceted biosocial dynamics that mediate their spread and control. Despite available methods and technologies to identify the causative agents, to understand the mechanism by which pathology is induced and to develop the treatments to cure, manage or control, their dual burden on communities, affecting both livestock and human health, is still heavy. Several of the more cost-effective NZD control strategies involve reducing disease prevalence in the animal reservoir, and such control approaches often profoundly impact on the prevalent culture, livelihood and socio-behavioural patterns of the affected communities including the social relations and social practices that mediate porous boundaries between humans and animals. We studied three NZDs in specific endemic settings: cystic echinococcosis (Morocco), Taenia solium taeniasis-cysticercosis (Zambia) and rabies (South Africa). This thesis aimed to illustrate and demonstrate the importance of including the socio-anthropological approach to contextualise the dynamic of disease transmission among livestock owners and their community, including knowledge and perception of zoonoses, to identify facilitating factors and barriers to interventions and to support efforts to control NZDs that operate in challenging circumstances and with marginalised populations in order to finally better fit community needs. Fitting well with the mantra of “One Health” (OH), present NZDs control challenges require new ways of linking disciplines, expertise, local authorities and populations in animal and human health.
In the first chapter a general review of the literature on the different components of the PhD project is presented. Divided into three sections, the chapter begins by considering existing work done on NZDs and medical anthropology by starting with the general context of NZDs and the OH concept; next with the clarification of the current epidemiological situation and existing control measures for each of the three 286 | S u m m a r y studied NZDs, and ends with the review of the actual role of medical anthropology in NZDs integrated control and the OH movement.
Following this chapter, the rationale and objectives of the thesis are given. The objectives consist of (1) identifying the socio-cultural determinants of transmission of specific NZDs, including knowledge and perception of the zoonoses; (2) identifying barriers to NZDs control options and added value of inter-sectoral collaborations between health, veterinary and other relevant sectors; (3) contributing to the elaboration of recommendations for a more adapted and sustainable integrated control of NZDs; and (4) sharing and disseminating these anthropological research findings in cross-disciplinary dialogues and constructive collaborative efforts.
The second chapter describes briefly the methods and materials used to collect the data of our three case-studies by first introducing what is qualitative research in general and how qualitative and quantitative approaches are complementary in the field of health and disease control. It also includes ethical considerations and researcher’s reflexivity.
In the third chapter, the reasons behind certain risk behaviours and the socio- cultural determinants hindering the control of cystic echinococcosis (CE) were documented among a Berber population living in the High Atlas Mountains, Morocco. Stratified by gender with villagers, butchers and students, a total of 20 focus group discussions (FGDs) conducted in ten villages that were purposely selected for their CE prevalence allowed us to assess the knowledge gaps about the E. granulosus life cycle and transmission, the role of dogs in this rural society, the community perceptions, practices and knowledge regarding sheep and offal management. The study aimed to propose more appropriate and effective strategies to overcome barriers, and hence contribute to better control CE. This Berber community considered CE to be a severe and relatively common disease in humans and animals but had a poor understanding of the parasite’s life cycle. Risk behaviour and disabling factors for disease control were mainly related to cultural practices in sheep breeding and home slaughtering, dog keeping, and offal disposal at home, as well as in slaughterhouses. Participants in our FGDs were supportive of control measures such as, management of canine populations, waste disposal, and S u m m a r y | 287 monitoring of slaughterhouses. The uncontrolled stray dog population and dogs having access to offal (both at village dumps and slaughterhouses) suggest that authorities should be more closely involved in CE control. Our findings further highlighted the need for improved knowledge about the transmission cycle of the parasite among communities and health professionals. Inter-sectoral collaboration between health staff, veterinarians, and social scientists appeared to be crucial for sustainable control of CE.
The fourth and fifth chapters concerned the case-study on T. solium taeniasis/cysticercosis conducted among the Nsenga ethno-linguistic group in a T. solium endemic rural area of the Eastern Province in Zambia. A total of 21 FGDs were organised separately with men, women and children, in seven villages from Petauke district and covered the topics about the perception of pig breeding in the communities and its role, knowledge and perceptions of taeniasis/cysticercosis and related risk behaviours and opinions on control measures. Embedded in a OH approach, the objective of this case-study was to identify possible barriers to control measures, and eventually, adaptations of strategies to overcome cysticercosis locally. Because the data collected were very dense, we decided to present them in two parts. In the fourth chapter the themes presented are related to perceived latrine availability and perceived latrine use. The findings reveal that latrines were not constructed in every household because of the convenient use of existing latrines in the neighbourhood. Latrines were perceived to contribute to good hygiene mainly because they prevent pigs from eating human faeces. Men expressed reluctance to abandon the open-air defecation practice mainly because of toilet- associated taboos with in-laws and grown-up children of the opposite gender. When reviewing conceptual frameworks of people’s approach to sanitation, we found that seeking privacy and taboos hindering latrine use and construction were mainly explained in our study area by the fact that the Nsenga observe a traditionally matrilineal descent. These findings indicate that in this local context latrine promotion messages should not only focus on health benefits in general. Since only men were responsible for building latrines and mostly men preferred open defecation, sanitation programmes should also be directed to men and address related sanitary taboos in order to be effective. The fifth chapter presents the
288 | S u m m a r y communities’ perceptions, reported practices and knowledge regarding management of pigs and Taeniasis/cysticercosis (including neurocysticercosis). The related findings reveal that the perception of pigs and their role in society, the distribution of the management tasks among the family members owning pigs and environmental aspects prevailing in the study area affected pig confinement. People had a fragmented knowledge of the pork tapeworm and its transmission. Even if negative aspects/health risks of free-range pigs keeping were perceived, people were ready to take the risk for socio-economic reasons. Finally, gender played an important role because women, and also children, seemed to have a higher perception of the risks but lack power in terms of economic decision-making compared to men. Currently, pig confinement was not seen as an acceptable method to control porcine cysticercosis by many farmers in Eastern Zambia, vaccination and treatment seemed to be more appropriate. Embedded in a OH approach, disease control programmes should therefore ensure a complementary appropriate set of control strategies by engaging new sectors such as, agronomy, spatial ecology and finally consider the socio-cultural context, which is likely to enhance the development of control methods that could be accepted by the communities.
The sixth chapter describes a case-study on the perceptions and practices of dog ownership and rabies control in a community with recently re-introduced rabies at a human-wildlife-domestic animal interface in Mpumalanga Province in north-east South Africa. Combined with informal discussions and participative observations, 18 FGDs with men, women and children - stratified by dog ownership status - were organised in three villages in Mnisi, a Shangaan community in the . The participants highly valued hunting dogs despite hunting wildlife being illegal. Although people did not have a clear idea of how dogs acquire rabies, they were aware of the presence of the disease and its zoonotic nature. A dog’s bite was always associated with rabies risk but was also a source of conflict between dog owners and bite victims, hampering good bite health care management. Dog vaccination is perceived as a mean to prevent diseases from spreading to humans and other animals, to protect them from diseases but also to cure. Lack of awareness, misinterpretation of health promotion messages and beliefs among adults seem to hinder participation in rabies vaccination campaigns. The use of qualitative research allowed for a more comprehensive and in- S u m m a r y | 289 depth understanding of the socio-cultural and environmental barriers to rabies vaccination in Mnisi. Involving hospitals and game lodges in vaccination campaigns would help to tackle rumours, clarify dog bite cure and dog vaccination procedures and improve the relationship with the community. Further anthropological studies focusing on people owning dogs for hunting may help to better understanding rabies transmission patterns and risk factors at the human-wildlife-domestic animal interface in this community.
In the seventh chapter, we discuss the findings of our research on a cross-case basis which highlights how complex social, cultural, political, economic and environmental determinants influence interventions to control endemic zoonoses, how transmission dynamics are rather biosocial than purely biomedical and how cultural beliefs and broader understandings of health and well-being might affect knowledge regarding zoonoses. The understanding of such factors allowed us to illustrate and demonstrate how and why social sciences, anthropology in particular, could contribute to the OH approach for NZDs integrated control but also how challenging it is in practice, especially regarding the complexity of interdisciplinarity and of the translation of findings from local to global and vice versa. Finally, we call for more studies with a socio-ecological approach to possibly help integrating more efficiently both qualitative and quantitative findings and different worldviews about animal-human relations in order to address holistically many of the pressing determinants of health. The latter have also a profound impact on human and animal health and welfare such as related to water security, biodiversity conservation, climate change, social justice, equitable access to resources, pollution management and land use planning. The questions and challenges raised about the interdisciplinary dialogue between social and medical rationales are also discussed.
Hoewel de globalisering veel voordelen heeft opgeleverd voor de samenleving, heeft deze ook veel nieuwe uitdagingen met zich meegebracht, met name wat betreft de gezondheid van mensen, dieren en het milieu. Verwaarloosde zoönotische ziekten (VZZ) komen vooral voor op plaatsen waar armoede, sociale en financiële afhankelijkheid van vee of wild, slechte veerkracht, en het samenleven van mensen en hun dieren de transmissie bevoordelen. Deze kenmerken induceren ook een groeiende uitdaging voor de biowetenschappen om te begrijpen hoe deze soort- overschrijdende pathogenen verweven zijn in een niet-lineaire en veelzijdige biosociale dynamiek die hun verspreiding en bestrijding beïnvloeden. Ondanks de beschikbaarheid van methoden en technologieën om de oorzakelijke pathogenen te identificeren, hun pathogenese te begrijpen, alsook om de behandeling, het management en de controle te ontwikkelen, blijven de VZZ nog steeds een zware, dubbele belasting op de gemeenschappen veroorzaken, door zowel de dier- en menselijke gezondheid aan te tasten. Onder de meest kostenefficiënte controlestrategieën voor VZZ zijn deze die de ziekteprevalentie in het dierenreservoir verminderen. Nochtans kunnen dergelijke controlemaatregelen een grote invloed hebben op de heersende cultuur, het levensonderhoud en de sociale gedragspatronen van de getroffen gemeenschappen, met inbegrip van de sociale relaties en praktijken die de poreuze grenzen tussen mens en dier bemiddelen. We bestudeerden drie VZZ in specifieke endemische locaties: cysteuze echinococcosis (Noord-Afrika: Marokko), Taenia solium taeniasis-cysticercose (zuidelijk Afrika: Zambia) en rabiës (zuidelijk Afrika: Zuid-Afrika). Dit proefschrift had tot doel de meerwaarde van het toevoegen van een socio-antropologische aanpak in de controle van VZZ aan te tonen en te duiden. De socio-antropologische aanpak draagt bij tot het contextualiseren van de dynamiek van ziektetransmissie bij veehouders en hun gemeenschap, met inbegrip van kennis en perceptie van zoönosen. Deze aanpak is ook belangrijk om faciliterende factoren en hinderpalen voor interventies te identificeren en om bij te dragen tot het bestrijden van VZZ in uitdagende omstandigheden en bij gemarginaliseerde populaties, met als doelstelling om uiteindelijk beter aan de behoeften van de gemeenschappen te voldoen. Aansluitend bij de mantra van "One Health" (OH), vereisen de huidige uitdagingen van VZZ bestrijding in de dier- en volksgezondheid 292 | Samenvattin g nieuwe inzichten om disciplines, expertise, lokale autoriteiten en populaties aan elkaar te koppelen.
In het eerste hoofdstuk wordt een algemeen overzicht gegeven van de literatuur betreffende de verschillende onderdelen van dit doctoraat. Verdeeld in drie secties, begint het hoofdstuk met de bespreking van het bestaande werk over VZZ en medische antropologie met eerst de algemene context van VZZ en het OH-concept. Vervolgens worden de huidige epidemiologische situatie en de bestaande controlemaatregelen voor elk van de drie bestudeerde VZZ belicht. Het hoofdstuk eindigt met de recensie van de feitelijke rol van de medische antropologie in geïntegreerde controle van VZZ en in de OH-beweging.
Na dit hoofdstuk worden de rationale en de doelstellingen van het proefschrift gegeven. De doelstellingen bestaan uit (1) het identificeren van de socio-culturele determinanten van de overdracht van specifieke VZZ, met inbegrip van kennis en perceptie van de zoönosen; (2) het identificeren van hinderpalen voor VZZ-controle opties en de toegevoegde waarde van intersectorale samenwerking van de gezondheidssector, de veterinaire sector en andere relevante sectoren; (3) het bijdragen tot de uitwerking van aanbevelingen voor een meer aangepaste en duurzame geïntegreerde bestrijding van VZZ; en (4) het uitwisselen en verspreiden van deze antropologische onderzoeksresultaten via interdisciplinaire dialogen en constructieve samenwerkingsinspanningen.
Het tweede hoofdstuk beschrijft kort de methoden die werden gebruikt om de gegevens van de drie casusstudies in te zamelen. Eerst wordt een inleiding gegeven over de betekenis van kwalitatief onderzoek. Vervolgens wordt uitgelegd hoe kwalitatieve en kwantitatieve benaderingen complementair zijn op het gebied van gezondheid en ziektebestrijding.
In het derde hoofdstuk worden de beweegredenen voor bepaalde risicogedragingen en de socio-culturele determinanten die de bestrijding van Cysteuze Echinococcose (CE) belemmeren, gedocumenteerd onder een Berber-bevolking van het Hoge Atlas- gebergte van Marokko. Op basis van 20 focusgroep-discussies (FGD) met dorpelingen, slagers en studenten, gestratificeerd per geslacht en uitgevoerd in tien dorpen die weloverwogen werden geselecteerd voor hun CE-prevalentie, konden we de Samenvatting | 293 kennislacunes over de E. granulosus-levenscyclus en -transmissie evalueren, alsook de rol van honden in deze rurale samenleving en de gemeenschapspercepties, -praktijken en -kennis met betrekking tot schapen en het beheer van slachtafval. De studie beoogde om meer passende en doeltreffende strategieën voor te stellen om hinderpalen te overwinnen, en dus bij te dragen tot een betere controle van CE. Deze Berber-gemeenschap beschouwde CE als een ernstige en relatief veel voorkomende ziekte bij mens en dier, maar had een slecht begrip van de levenscyclus van de parasiet. Risicogedrag en factoren die de ziektebestrijding belemmeren waren voornamelijk gebonden aan culturele praktijken in schapenhouderijen en thuisslachtingen, het houden van honden en het verwijderen van slachtafval bij thuisslachting en in slachthuizen. Deelnemers aan de FGD waren voorstander van controlemaatregelen, zoals het beheer van hondenpopulaties, slachtafvalverwerking en toezicht op slachthuizen. De ongecontroleerde zwerfhondenpopulatie en honden die toegang hebben tot slachtafval (zowel in dorpsstortplaatsen als in slachthuizen) suggereren dat de autoriteiten nauwer moeten betrokken worden bij de CE-controle. Onze bevindingen benadrukten verder de nood aan een betere kennis over de transmissiecyclus van de parasiet onder de gemeenschappen en gezondheidswerkers. Intersectorale samenwerking tussen gezondheidswerkers, dierenartsen en sociale wetenschappers blijkt cruciaal te zijn voor een duurzame controle van CE.
De vierde en vijfde hoofdstukken hadden betrekking tot casusstudies over T. solium Taeniasis/Cysticercose (TSTC) uitgevoerd in de Nsenga etnisch-linguïstische groep in een T. solium-endemisch plattelandsgebied van de oostelijke provincie in Zambia. Een totaal van 21 FGD werden in zeven dorpen van het Petauke-district georganiseerd met afzonderlijk, mannen, vrouwen en kinderen. De besproken thema’s waren de perceptie van varkenshouderij in de gemeenschappen en haar rol, de kennis en percepties van TSTC en de gerelateerde risicogedragingen en meningen over bestrijdingsmaatregelen. Ingebed in een OH-benadering, hadden deze casusstudies als doelstelling de mogelijke hinderpalen voor controle te identificeren en desgevallend lokale aanpassingen van strategieën voor te stellen. Omdat de verzamelde gegevens zeer talrijk waren, werden deze in twee delen gepresenteerd. In het vierde hoofdstuk zijn de voorgestelde thema's gerelateerd aan de perceptie
294 | Samenvattin g van de beschikbaarheid en het gebruik van latrines. Uit de bevindingen bleek dat latrines niet in elk huishouden worden gebouwd vanwege het handige gebruik van bestaande latrines in de buurt. Er werd waargenomen dat latrines bijdragen tot een goede hygiëne, vooral omdat ze beletten dat varkens menselijke uitwerpselen eten. De mannen uitten terughoudendheid om de praktijk van de openlucht-ontlasting op te geven, hoofdzakelijk wegens taboes gebonden aan het gemeenschappelijk gebruik van een toilet met leden van de schoonfamilie en met adolescenten van het andere geslacht. Bij het bestuderen van de regelgevingskaders voor de aanpak van mensen wat betreft hygiëne, vonden we dat het zoeken naar privacy en de taboes op latrinegebruik en -bouw, in ons studiegebied voornamelijk uitgelegd kon worden door de traditie van een traditioneel matrilineaire afstamming bij de Nsenga’s. Deze bevindingen geven aan dat in deze lokale context promotieboodschappen voor het gebruik van latrines niet enkel gericht moeten zijn op gezondheidsvoordelen in het algemeen. Aangezien enkel de mannen verantwoordelijk zijn voor de bouw van latrines en zij meestal de voorkeur geven aan openlucht-ontlasting, moeten, om effectief te zijn, sanitaire programma’s zich ook richten op mannen en op de gerelateerde sanitaire taboes. Het vijfde hoofdstuk stelt de percepties van de gemeenschappen en de gerapporteerde praktijken en kennis voor met betrekking tot varkenshouderij en taeniasis/cysticercose (met inbegrip van neurocysticercose). Uit de ingewonnen gegevens blijkt dat de perceptie van varkens en hun rol in de samenleving, de verdeling van de beheertaken onder de familieleden en de milieuaspecten van het studiegebied de opstalling van varkens beïnvloeden. De mensen hadden een gefragmenteerde kennis van de varkenslintworm en de transmissie ervan. Zelfs als de negatieve aspecten en de gezondheidsrisico’s gebonden aan varkenshouderijen met buitenloop gekend waren, waren de mensen wegens sociaaleconomische redenen bereid om het risico te nemen. Tenslotte speelde het geslacht een belangrijke rol, omdat vrouwen, maar ook kinderen, een hogere perceptie van de risico's leken te hebben, maar niet genoeg macht hebben in termen van economische besluitvorming in vergelijking met de mannen. Het opstallen van varkens werd door vele boeren in het oosten van Zambia niet gezien als een aanvaardbare methode om varkenscysticercose te controleren. Daarentegen werden vaccinatie en behandeling als meer aanvaardbare opties aanzien. Ingebed in een OH-aanpak, moeten de programma’s voor ziektecontrole een waaier aan Samenvatting | 295 complementaire controlestrategieën verzekeren, door het inzetten van nieuwe sectoren, zoals landbouw of ruimtelijke ecologie en moet er rekening gehouden worden met de sociaal-culturele context, wat de ontwikkeling van door de gemeenschappen aanvaarbare controlemethoden kan versterken.
Het zesde hoofdstuk beschrijft een casusstudie over de percepties en praktijken van het bezit van honden en rabiëscontrole in een rurale gemeenschap in de provincie Mpumalanga, Noordoost Zuid-Afrika. In deze gemeenschap, gelegen aan de grens van het Kruger Nationaal Park werd recent opnieuw rabiës vastgesteld. In combinatie met informele discussies en participatieve observaties, werden 18 FGD georganiseerd in drie dorpen in Mnisi, een Shangaan-gemeenschap. De stratificatie van mannen, vrouwen en kinderen gebeurde op basis van het bezit van honden. De deelnemers waardeerden zeer sterk het bezit van jachthonden, niettegenstaande het feit dat de jacht op wild illegaal is. Hoewel de mensen niet over een duidelijk idee beschikten van hoe honden door rabiës besmet geraken, waren ze bewust van de aanwezigheid van de ziekte en van het zoönotische aspect. Een hondenbeet werd steeds geassocieerd met een risico op rabiës, maar was ook een bron van conflict tussen hondenbezitters en bijtslachtoffers, wat een gepaste beetverzorging belemmerde. De vaccinatie van honden wordt aanzien als een middel om te voorkomen dat ziekten zich naar mens en andere dieren verspreiden, om hen te beschermen tegen deze ziekten, maar ook om hen te genezen. Gebrek aan besef, verkeerde interpretatie van gezondheidsboodschappen en overtuigingen onder volwassenen lijken de deelname aan rabiës vaccinatiecampagnes te belemmeren. Het gebruik van kwalitatief onderzoek liet toe een volledigere en meer diepgaande kennis van de sociaal- culturele en milieu hinderpalen voor rabiësvaccinatie in Mnisi te bekomen. Het betrekken van ziekenhuizen en game lodges in vaccinatiecampagnes kan helpen om geruchten te bestrijden, procedures te verduidelijken voor het verzorgen van hondenbeten en bij hondenvaccinatie, en zou de relatie met de gemeenschap kunnen verbeteren. Bijkomende antropologische studies gericht op eigenaars van jachthonden in deze gemeenschap kunnen helpen om de transmissiepatronen en risicofactoren van rabiës beter te begrijpen op het niveau van de mens-wild- huisdierinterface.
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In het zevende hoofdstuk bespreken we de bevindingen van ons onderzoek op basis van een cross-casusanalyse, waarin wordt benadrukt hoe complexe sociale, culturele, politieke, economische en milieudeterminanten invloed hebben op interventies om endemische zoönoses te controleren, hoe transmissiedynamiek eerder biosociaal dan zuiver biomedisch is en hoe culturele overtuigingen en bredere inzichten van gezondheid en welzijn de kennis van zoönosen kunnen beinvloeden. Het begrijpen van dergelijke factoren liet ons toe aan te tonen hoe en waarom de sociale wetenschappen, antropologie in het bijzonder, kunnen bijdragen tot de OH- benadering van de geïntegreerde controle van VZZ. Het toonde echter ook aan hoe uitdagend dit is in de praktijk, vooral met betrekking tot de complexiteit van interdisciplinariteit en de vertaling van bevindingen van lokaal naar globaal en omgekeerd. Tot slot pleiten wij voor meer studies met een sociaalecologische benadering om desgevallend te helpen bij een meer efficiënte integratie van zowel kwalitatieve als kwantitatieve bevindingen als van verschillende levensbeschouwingen over de relatie tussen mens en dier, om zodoende meer holistisch de nijpende determinanten van gezondheid te benaderen. Dit laatste heeft ook een diepgaande invloed op de gezondheid en het welzijn van mens en dier, zoals in het kader van waterveiligheid, behoud van biodiversiteit, klimaatverandering, sociale rechtvaardigheid, billijke toegang tot hulpbronnen, vervuilingsbeheer en ruimtelijke ordening.
Full name: SEVERINE THYS
Date of birth: 24 April 1981
Place of birth: Brussels, Belgium
Occupation: Anthropologist/ Researcher
Organisation: Ghent University (Faculty of Veterinary Medicine), Salisburylaan 133, 9820 Merelbeke, Belgium
Email address: [email protected]
In 2004, Ms. Thys obtained a Master in Anthropology from the Université Libre of Brussels, and after some years working in the field of mental disablement, she was awarded a complementary multi-university master in Public Health, orientation Health and Development (ULB, ULg, UCL). From 2009 to 2018 she worked as an academic assistant at the Institute of Tropical Medicine (Antwerp, Belgium) (ITM), where she was involved in the study of perceptions of zoonotic diseases in rural communities: Echinococcosis in Morocco, Cysticercosis in Zambia, Rabies in South Africa and in Indonesia, and Human African Trypanosomiasis in Guinea. She was during 5 years the coordinator of a strategic network on Zoonoses and Neglected Diseases, generously supported by the Belgian Directorate-general for Development Cooperation and Humanitarian Aid , aiming at fostering intersectoral collaboration and to promote the concept of "One Health" among the institutional partners of ITM. She was a co-investigator in three FP7 EU projects (ICONZ, ADVANZ, NEXTGEN). In the early days of the Ebola Virus Disease epidemic in West Africa in 2014, she volunteered to be deployed in Guinea for the Global Outbreak and Alert Response Network (GOARN) of the World Health Organization. She started a Ph.D. at Ghent University, Faculty of Veterinary medicine, in 2014 on the “The added value of Anthropology for integrated control of Neglected Zoonotic Diseases in the One Health movement”, and obtained a scholarship from the Dubois-Brigué Foundation for an additional year of PhD research (2018) during which she was based at the Gadjah 298 | Curriculum Vitae
Mada Universitas in Yogyakarta, Indonesia, in the One Health/EcoHealth Collaborating Center.
Up to date, Séverine Thys has 15 international publications, of which five as the first author. She is also the author of a chapter in a book on “Framing Animals as Epidemic Villains” edited by Palgrave Macmillan (in press). As a speaker at several international congresses and as a lecturer on qualitative methodologies in several master programs in Belgium and abroad, she is continuing building bridges by launching a One Health Belgium Network together with representatives of different ministries, universities, and civil organizations.
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Pablo Picasso