Thys et al. BMC Public Health (2019) 19:118 https://doi.org/10.1186/s12889-018-6372-y RESEARCH ARTICLE Open Access Community perception and knowledge of cystic echinococcosis in the High Atlas Mountains, Morocco Séverine Thys1,2* , Hamid Sahibi3, Sarah Gabriël4, Tarik Rahali5, Pierre Lefèvre6, Abdelkbir Rhalem3, Tanguy Marcotty7, Marleen Boelaert1 and Pierre Dorny8,2 Abstract Background: Cystic echinococcosis (CE), a neglected zoonosis caused by the larval stage of the tapeworm Echinococcus granulosus, remains a public health issue in many developing countries that practice extensive sheep breeding. Control of CE is difficult and requires a community-based integrated approach. We assessed the communities’ knowledge and perception of CE, its animal hosts, and its control in a CE endemic area of the High Atlas Mountains, Morocco. Methods: We conducted twenty focus group discussions (FGDs) stratified by gender with villagers, butchers and students in ten Berber villages that were purposefully selected for their CE prevalence. Results: This community considers CE to be a severe and relatively common disease in humans and animals but has a poor understanding of the parasite’s life cycle. Risk behaviour and disabling factors for disease control are 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 focus group discussions were supportive of control measures as management of canine populations, waste disposal, and monitoring of slaughterhouses. Conclusions: 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. This study also highlights 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 appears to be crucial for sustainable control of this parasitic zoonosis. Keywords: Cystic echinococcosis, Disease control, Dog, Sheep, Neglected zoonosis, Anthropology, Focus group discussion, Morocco Background genetic variability exists within the E. granulosus species. Cystic echinococcosis (CE), also known as human hyda- Several strains have been identified with differences in tidosis, is a neglected zoonotic parasitic disease caused intermediate host spectrum, biological characteristics, by the cestode Echinococcus granulosus. Dogs and wild and geographical distribution [1]. Globally, most human Canidae are the definitive hosts, while domestic cases of CE are caused by the sheep strain E. granulosus Ungulates act as intermediate hosts. Humans are acci- sensu stricto (characterized as the genotypes G1, G2 and dental dead-end hosts. Considerable phenotypic and G3) [2]. A common misconception is that humans be- come infected when eating uncooked meat. In reality, * Correspondence: [email protected] CE is transmitted via the faeco-oral route. Intermediate 1Department of Public Health, Institute of Tropical Medicine, Nationalestraat hosts become infected through ingestion of parasite eggs 155, 2000 Antwerp, Belgium that are passed through the dog’s faeces. Humans are in- 2Department of Virology, Parasitology, and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, fected when consuming contaminated food or water, or Belgium through close contact with infected soil or objects (with Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Thys et al. BMC Public Health (2019) 19:118 Page 2 of 15 subsequent ingestion of eggs), including dogs’ mouths Control of echinococcosis is difficult due to the complex and fur. An infection in livestock and humans leads to nature of the parasite’s life cycle, the number of animal the development of a hydatid cyst in the liver, lungs, or species acting as potential (intermediate) hosts, and the more rarely, other organs [3]. While animals rarely show requirement for intersectoral cooperation between agri- clinical symptoms, clinical signs and symptoms in cultural, veterinary, and health authorities [17]. Now- humans may develop months or years after infection, adays, the Eg95 vaccine for sheep [18], registered in and are caused by the expanding cysts and inflammatory some parts of the world, combined with cestodicidal reactions [4]. Severe cases can only be treated surgically. treatment of dogs, shows a strong potential to control CE is a worldwide health problem primarily affecting this disease [19]. pastoral and poor rural communities where people raise Although the Moroccan Government established an livestock in close contact with dogs fed on raw offal [5]. “Inter-Ministerial Committee” in 2007 and drew up The latest global burden of CE is estimated at 184,000 guidelines to combat CE [20], the disease remains a sig- Disability-Adjusted Life Years (DALYs), − one DALY be- nificant public health problem in this country. Currently, ing defined as 1 year of healthy life lost due to ill-health, hydatidosis control program managers in Morocco wish disability and/or early death -, for a total cost of US$3 to gain a better understanding of the type of risk behav- billion attributed to CE-related health care costs and iours that persist in rural populations, and why they per- losses in the livestock sector [6]. sist. This may improve the impact of their control CE is highly endemic in North Africa and the Middle efforts. Dar and Alkarmi (1997) were the first to East. In these regions, incidence rates in humans can ex- emphasize the importance of socio-economic and cultural ceed 50 per 100,000 person-years [7, 8]. In 2012, issues in CE control in the Maghreb and the Middle-East Morocco recorded an average of 5.2 surgical cases per [21–25]. Several authors have highlighted the role of hu- 100,000 inhabitants (DELM, 2012) and a mortality rate man behaviour in the epidemiology of (re-)emerging para- estimated at 2–3% [9]. A retrospective survey (2007– sitic zoonoses. Studies in Asian [26–28], South American 2017) in the province of Khénifra shows a maintained [29, 30], and sub-Saharan African populations [31], as well incidence rate of 8.62 per 100,000 inhabitants (Ezzahra F as the Mediterranean region (primarily Tunisia and et al., unpublished data). The last epidemiological study Algeria) [32–35], indicate that human risk behaviour asso- in the Mid Atlas showed a prevalence of abdominal CE ciated with poor understanding of the parasite life cycle by of 1.9% based on ultrasound examination [10]. Official the population has a negative impact. However, no study data from the Ministry of Health reported 722 surgical has extensively studied the socio-cultural determinants in- CE cases in 2014 [11]. The overall annual cost to both fluencing human behaviour and CE transmission, and no the Moroccan health and livestock sector has been val- research is available for the High Atlas region. ued at nearly €1,000,000, though data are fragmented The objective of this study is therefore to document [12]. According to a study conducted in five regions of the reasons behind certain risk behaviours and the Morocco, prevalence of infection ranges from 23.0% in socio-cultural determinants hindering the control of CE. cattle, 17.8% in Equidae, 12.0% in camels, 10.6% in By assessing the knowledge gaps about the E. granulosus sheep, to 1.9% in goats. In rural areas, one dog in two life cycle and transmission, the role of dogs in this rural carries E. granulosus [13]. A study conducted in the society, the community perceptions, practices and know- province of Sidi Kacem (northwest Morocco) between ledge regarding sheep and offal management, the study 2010 and 2011 found an E. granulosus infection preva- aims to propose more appropriate and effective strat- lence of 35.3% in pet dogs [14]. Although Morocco is egies to overcome barriers, and hence contribute to bet- considered a highly endemic country for CE [7], this ob- ter control of CE. vious lack of data illustrates clearly the persisting neglect of zoonotic diseases in terms of funding opportunities Methods for epidemiological research, of national health prior- Study area ities, and consequently of validation of effective CE con- We conducted a qualitative research project based on trol strategies and of efficient surveillance measures. focus group discussions in a predominantly rural area in Illiteracy, weak infrastructure and limited economic the Northern fringes of the High Atlas Mountains, 30 to resources in rural and suburban areas in Morocco play a 50 km south of Marrakech in the Al Haouz province of major role in the distribution of CE. The irrigation sys- Morocco. The study region was selected based on reports tems, extensive sheep breeding, high numbers of stray indicating high prevalence of E. granulosus in humans, dogs, and