Aus dem Institut für Parasitologie und Tropenveterinärmedizin des Fachbereichs Veterinärmedizin der Freien Universität Berlin und dem International Livestock Research Institute Assessment of the parasitic burden in the smallholder pig value chain and implications for public health in Uganda Inaugural-Dissertation zur Erlangung des Grades eines PhD of Biomedical Sciences an der Freien Universität Berlin vorgelegt von Kristina Rösel Tierärztin aus Karl-Marx-Stadt (jetzt Chemnitz) Berlin 2017 Journal-Nr.: 3973 Gedruckt mit Genehmigung des Fachbereichs Veterinärmedizin der Freien Universität Berlin Dekan: Univ.-Prof. Dr. Jürgen Zentek Erster Gutachter: Prof. Dr. Peter-Henning Clausen Zweiter Gutachter: Univ.-Prof. Dr. Reinhard Fries Dritter Gutachter: Prof. Dr. Eric Fèvre Deskriptoren (nach CAB-Thesaurus): pigs, value chain, animal parasitic nematodes, Trichinella spp., muscle larvae, newborn larvae, Toxoplasma gondii, public health, epidemiology, meat hygiene, animal housing, Uganda Tag der Promotion: 30.11.2017 Coverbild: Angella Musewa/ILRI “Overcoming poverty is not a task of charity, it is an act of justice.” (Nelson Mandela) Dedicated to the smallholder pig value chain actors in Uganda. Table of contents TABLE OF CONTENTS List of figures ................................................................................................................................. iii List of tables .................................................................................................................................... v List of abbreviations ...................................................................................................................... vi 1 Preface ..................................................................................................................................... 1 1.1 Introduction and study objectives ..................................................................................... 1 1.2 Structure of the thesis ....................................................................................................... 3 2 Literature review ...................................................................................................................... 4 2.1 The history of pigs in Africa ............................................................................................. 4 2.2 Smallholder pig production systems in sub-Saharan Africa ............................................. 6 2.3 Parasites of domestic pigs and their occurrence in East Africa ...................................... 12 2.3.1 Trematoda (flukes) .......................................................................................................... 12 2.3.2 Nematoda (roundworms) ................................................................................................ 12 2.3.3 Protozoa .......................................................................................................................... 17 3 The context for researching smallholder pig value chains in Uganda ................................... 20 3.1 CGIAR Research Framework ......................................................................................... 20 3.2 Study area ....................................................................................................................... 22 3.3 Study site selection and characteristics........................................................................... 25 3.3.1 Geographical targeting .................................................................................................... 25 3.3.2 Stakeholder consultation ................................................................................................. 25 4 Parasites as a production constraint in smallholder pig production systems (Publications I & II) ............................................................................................................... 28 5 Parasites with potential implications for public health (Publications III & IV) .................... 54 6 Knowledge, attitudes and practices of pork consumers (Publication V) ............................... 72 7 Summarizing discussion ........................................................................................................ 79 7.1 Value chain domains as a suitable proxy for the classification of heterogeneous smallholder pig production systems ............................................................................... 79 7.2 Pig parasites as a constraint to farm productivity ........................................................... 80 7.3 Parasite infections with public health implications ........................................................ 81 7.3.1 Gastrointestinal parasites as soil-transmitted zoonotic helminths .................................. 81 7.3.2 Pork-borne zoonoses ....................................................................................................... 81 i Table of contents 7.4 Researching smallholder pig value chains through an integrated approach and participatory methods ..................................................................................................... 85 7.5 Concluding remarks, limitations of the survey and potential future research ................ 87 7.5.1 Major research findings .................................................................................................. 87 7.5.2 Major conclusions ........................................................................................................... 88 8 References .............................................................................................................................. 91 Summary ..................................................................................................................................... 108 Zusammenfassung....................................................................................................................... 110 List of own publications.............................................................................................................. 112 Disclosure of own share in the body of the work ....................................................................... 124 Acknowledgements ..................................................................................................................... 126 Statement of authorship .............................................................................................................. 128 ii List of figures List of figures Figure 2.1 Tethered local breed in Wakiso district, Central Uganda (Kristina Roesel). ................ 5 Figure 2.2 Exotic breed (Large White) in a commercial farm in Masaka district, Central Uganda (Kristina Roesel). ............................................................................... 5 Figure 2.3 Fully confined cross-breed pig in an intensive production unit in Wakiso district, Central Uganda (Kristina Roesel). ............................................................................... 5 Figure 2.4 Ugandan pig farmer tends to her Camborough pigs (Edgar R. Batte in Uganda Daily Monitor, 7 November 2012 (Muhanguzi, 2012)). .. 5 Figure 2.5 Pig tethered under a tree and provided with sweet potato vines for feed, Kiboga district in Central Uganda (Kristina Roesel). .................................................. 8 Figure 2.6 Adult pig confined but piglets able to roam freely in Kamuli district, Eastern Uganda (Kristina Roesel). ............................................................................... 8 Figure 2.7 One type of confinement in a rural setting in peri-urban Wakiso district, Central Uganda (Kristina Roesel). ............................................................................... 8 Figure 2.8 Pigs confined in Kamuli district, Eastern Uganda (Kristina Roesel). ........................... 8 Figure 2.9 Confined pigs in peri-urban Masaka, Masaka district, Central Uganda (Kristina Roesel). ......................................................................................................... 8 Figure 2.10 Commercial pig farm with biosecurity protocol in peri-urban Kampala (Kristina Roesel) .......................................................................................................... 8 Figure 2.11 The distribution of encapsulated Trichinella spp. in Africa reviewed by Mukaratirwa et al. (2013), Murrell and Pozio (2011), Pozio (2007), and Pozio et al. (2005). Map adapted from Pozio et al. (2005). ....................................... 16 Figure 3.1 A livestock value chain and its actors and beneficiaries. Source: Nick Taylor, University of Reading, and Jonathan Rushton, Royal Veterinary College, In: Roesel and Grace (2014). .......................................... 20 Figure 3.2 Delivering CGIAR Research Program on Livestock & Fish (CRP L&F). Structure: Three integrated components. Source: CRP L&F, 2012. .......................... 21 Figure 3.3 Problem tree showing food safety and related market access in the context of whole value chain development (ILRI, 2011). .......................................................... 22 Figure 3.4 Pig density by district shows a higher concentration in the Central, Western and Eastern regions of Uganda. Source: Poole et al. (2015). Category thresholds are as accurate as 14 decimals. ................................................. 23 Figure 3.5 Average pig densities in Uganda show production specific production foci in Mbale, peri-urban Kampala, Kasese and Masaka. Source: Robinson