Sustainable interventions for an emerging livestock disease problem in Tanzania

Lead Research Organisation: University of Glasgow
Department Name: College of Medical, Veterinary, Life Sci

Abstract

This project has been developed in response to concerns of livestock-keeping communities who have reported major mortality losses in sheep and goats due to an emerging disease problem, known locally as Ormilo. Our preliminary studies support a growing consensus that Ormilo is the disease cerebral coenurosis, a fatal, neurological disease of sheep and goats caused by a tapeworm infection (Taenia multiceps). Sheep and goats are infected by ingesting the parasite eggs shed in the faeces of dogs (the definitive host), with clinical disease occurring when the parasite larvae migrate to the brain and form cysts. Dogs are in turn infected when they consume the brains of affected sheep and goats.

Current levels of coenurosis appear to be unprecedented and a cause of major concern among the poorest livestock-keeping families, particularly pastoralists who are increasingly dependent on sheep and goats for livelihoods and food security. Ormilo is now ranked as the highest priority disease in most pastoral communities of northern Tanzania. Several factors may be contributing to the current upsurge in cases including a shift to keeping of small ruminants in preference to cattle, a rapid increase in dog populations, and the practice of livestock-owners of feeding dogs the brains of affected animals.

This project aims to develop simple, sustainable interventions that can be adopted easily by livestock-keepers and dog-owners to prevent infection and reduce the burden of disease. The project will focus on two interventions: (a) developing and disseminating culturally-approrpriate information to livestock-keepers on the life cycle of the parasite, and the importance of not feeding brain tissue to dogs (with burning a simple alternative); (b) anthelminthic treatment of dogs with praziquantel every three months. An important additional benefit of de-worming dogs would be the effective control of Echinococcus granulosus, the cause of human hydatid disease (cystic echinococcus), a potentially fatal disease which is known to be an important but neglected human health problem in pastoral communities of East Africa. With a similar life-cycle involving dogs and small ruminants, hydatid disease may also be increasing, but cases will not become apparent for several years. An effective intervention in dogs at this stage could avert a major future human health problem.

The final output of the proposed project will be a business development plan, which charts a subsequent course of remedial Ormilo intervention. The plan will depend to a large extent on whether Ormilo is a localised or widespread/regional animal health issue and the willingness of farmers to pay for praziquantel treatment of dogs. Market research to better understand the scale of the Ormilo problem and demand for interventions will involve analysis of detailed Ormilo prevalence data being generated through other on-going studies, household econometric and wilingness-to-pay studies, as well as stakeholder workshops. Further work will involve development of materials for dissemination to livestock-keeping communities and training courses for NGOs and animal health professions. By working with project partners with experience of developing solutions for livestock interventions (GALVmed), we will explore both NGO-based delivery strategies and market-led approaches through which animal health supply chains could be developed for delivery of praziquantel to a large population of livestock-keepers, potentially extending to countries in the East African region (eg. Kenya and Ethiopia).
 
Description This grant contributed to a study of the causes and prevalence of a neurological syndrome in small ruminants which is a growing cause of concern to pastoralists in northern Tanzania. In total, 95% of surveyed households reported cases of neurological syndrome in the previous 12 months. By village, the 12-month period prevalence ranged from 11-34%, representing a total loss of about 10,000 affected animals. Dog ownership and the practice of feeding livestock brains to dogs were both identified as significant risk factors at the household level. Cysts consistent with Taenia multiceps infection were detected in the brain or spinal cord of 82% of clinically-affected animals (n=39) that underwent post-mortem examination. Coenurosis associated with T. multiceps infection is typically fatal, and can lead to substantial financial and production losses for livestock-dependent communities through death, predation or via premature slaughter of affected animals and a reduced market value. Our findings highlight the importance of this neglected livestock disease problem and the urgent need to implement effective control measures to control this disease in pastoral communities in Tanzania.An extension of this cross-sectional study, carried out in 773 households in 11 pastoral and agropastoral villages, revealed a 12-month period prevalence of 10.5% in small ruminants, and a 14.4% prevalence of taeniid infection in dogs.

Further work has been completed to investigate community-based interventions involving three pillars of control. The first pillar is to block transmission to the definitive host through preventing dogs eating the brains of slaughtered small ruminants; the second pillar is through anthelminthic treatment of dogs to reduce infection intensity in dogs; the third is to reduce environmental contamination through removal of dog faeces. The intervention study was conducted in a pastoral community, and launched with a baseline survey, followed by community meetings and a participatory workshop involving over 150 community members. Participants received information about the life cycle of T. multiceps and known ways to interrupt the life cycle. Through participatory methods, community members proposed their own strategies for intervention and breaking the transmission cycle, decided to de-worm dogs, collect dog faeces for testing and disposal, and to dispose of brains by burning rather than feeding to dogs or throwing out into the bush. The proportion of cases where brains were burnt rose from 5.2% at baseline to 83% within four weeks and remained between 60% and 100% for the duration of study (a further 26 weeks). Over the same period, the number of cases in the village fell by 68%.

Despite a high level of adoption of prevention measures and an initial reduction in cases, cases are still being reported. A possible explanation is that these are occurring as a result of buying-in replacement animals that are incubating the disease. A further challenge is that, while preventive measures are likely to be effective in reducing disease burden, these are only likely to be effective if practiced by all members of a community, as a single infected dog has the potential to infect a large number of sheep and goats. Although we are working with communities and the animal health sector to encourage uptake of behavioural preventive measures, livestock vaccines are still likely to be welcomed by farmers an additional measure to confer more direct protection.

A YouTube video explaining (in the local language) the life cycle of Taenia multiceps and possible preventive measures, was produced and disseminated initially in the study village, but through word-of-mouth, the video was subsequently widely distributed, with evidence from the survey carried out in our linked research project (BB/S013857/) that the information had reached 15% of householders in a neighbouring district.

The results from this study demonstrating the impact of coenurosis and the challenges of behavioural interventions have stimulated interested in the development of a livestock vaccine against Taenia multiceps. This has resulted in new collaborations with the University of Melbourne (Dr. M. Lightowlers), the Moredun Research Institute (Dr. A. Nisbet) and Onderstepoort Biological Products (Dr. B. Dungu) to explore the development of livestock cestode vaccines in East Africa.

The study also catalysed a collaboration with the WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis, Italy (Dr. F. Tamarozzi) for work on a cestode parasite (Echinococcus granulosus), which is the cause of human cystic echinococcosis, a potentially fatal but neglected human infection, with a very similar life cycle to Taenia multiceps. The collaboration led to a successful grant application for a pilot ultrasound survey of human cystic echinococcosis in the same communities affected by T. multiceps, and genetic analysis of the parasite in linked human and livestock populations. Through the work of this follow-up study, high-risk communities were identified and the potential for developing combined Taenia/Echinococcus livestock vaccines is currently being explored.

These results have also informed the design and implementation of a detailed econometric analysis of losses due to T. multiceps which is being carried out by a Tanzanian PhD student registered at a partner institution (Nelson Mandela African Institution of Science and Technology) in Tanzania.
Exploitation Route Results from this study highlighting the high prevalence of cerebral coenurosis have attracted considerable interest, including among Ministry of Livestock and Fisheries, livestock/development NGOs working in East Africa (e.g. Sidai, GALVmed), the Bill and Melinda Gates Foundation, FAO and other academic groups (e.g. University of Bristol). Results have also been communicated through the International Veterinary Vaccinology network and discussions are underway with research partners (see above) to develop protocols for a potential vaccine trial of a small ruminant vaccine against T. multiceps (potentially combined with E. granulosus) in Tanzania.

The YouTube video we developed on Taenia multiceps has the potential for widespread dissemination and impact in the East African region, where the disease appears to be widespread, which we hope to achieve through communication with FAO, pastoral/livestock NGOs and other academic groups (e.g. University of Bristol).
Sectors Agriculture, Food and Drink

 
Description The engagement with communities as part of this research and the co-development of preventive interventions that address a disease of substantial concern has had several non-academic impacts, including building of trust between researchers and pastoral communities, as well as generating economic benefits through a substantial reduction of losses from coenurosis. A YouTube video explaining (in the local language) the life cycle of Taenia multiceps and possible preventive measures, was produced and disseminated initially in the study village, but through word-of-mouth, the video was subsequently widely distributed, with evidence from the survey carried out in our linked research project (BB/S013857/) that the information had reached 15% of householders in a neighbouring district. The video has also been made available to FAO and NGO partners in Tanzania for further dissemination. The research provided the platform for further linked work on Echinococcus granulosus, a parasite that causes human cystic echinococcosis. The similarity of the life cycle (involving domestic dogs and small ruminants) has raised concerns that factors driving the emergence of Taenia multiceps in sheep and goats may also be increasing the risk of cystic echinococcosis in people. A pilot ultrasound survey conducted in northern Tanzania demonstrated a cyst prevalence of 1.3% in people in pastoral communities with an abattoir survey detecting cysts in 34.2% livestock in pastoral communities. The study reinforced the need for interventions targeting transmission routes that would prevent both diseases, including safe disposal of livestock cysts and deworming of dogs, and which would have dual benefits for livestock and human health.
Sector Agriculture, Food and Drink
Impact Types Societal,Economic

 
Description Research Grant - Pilot Ultrasound Survey of Human Cystic Echinococcosis in Tanzania
Amount € 20,000 (EUR)
Organisation European Society of Clinical Microbiology and Infectious Diseases (ESCMID) 
Sector Charity/Non Profit
Country Switzerland
Start 04/2019 
End 09/2021
 
Title Cystic echinococcosis in northern Tanzania: a pilot study in Masaai livestock-keeping communities 
Description  
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://researchdata.gla.ac.uk/id/eprint/1299
 
Title Taenia multiceps coenurosis in Tanzania: a major and under-recognised livestock disease problem in pastoral communities 
Description  
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
 
Description Collaboration with Moredun Research Institute on development of livestock vaccines against cestode parasites in East Africa 
Organisation Moredun Research Institute
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Established links with researchers at the Moredun Research Institute for potential transfer of technology relating to cestode vaccine production from the University of Melbourne to MRI to ensure sustainability of research in this area following the retirement of key researchers at the University of Melbourne.
Collaborator Contribution Agreement to partner on future research to progress development of livestock vaccines against cestode parasites in East Africa.
Impact Research protocols established and funding applications drafted.
Start Year 2020
 
Description Collaboration with Tanzania Veterinary Laboratory Agency 
Organisation Tanzania Veterinary Laboratory Agency
Country Tanzania, United Republic of 
Sector Public 
PI Contribution Collaboration with TVLA on research on the aetiology of livestock abortion (Cleaveland PI on BMGF-funded award), Crimean Congo Haemorrhagic Fever (Cleaveland co-PI on DTRA-funded award) and Rift Valley fever (Cleaveland co-I on UKRI award led by Lord, Liverpool School of Tropical Medicine).
Collaborator Contribution TVLA provide support for field epidemiological studies and laboratory diagnosis.
Impact Publications, co-supervision of PhD student, training courses.
Start Year 2021
 
Description Collaboration with University of Melbourne for development of a livestock vaccine against cestode parasites 
Organisation University of Melbourne
Country Australia 
Sector Academic/University 
PI Contribution Established links with the researchers at the University of Melbourne to take forward research for development and evaluation of livestock vaccines against Taenia and Echinococcus parasites in East Africa.
Collaborator Contribution Establishment of protocols for vaccine development and evaluation, joint drafting of research funding applications.
Impact Protocols established to optimise antigen and adjuvant combinations and carry out preliminary field studies of safety and immunogenicity in East Africa.
Start Year 2020
 
Description UoG - KCRI- Istituto Superiore di Sanità, WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis, Rome, Italy 
Organisation National Institute of Health
Country Italy 
Sector Public 
PI Contribution .
Collaborator Contribution .
Impact .
Start Year 2019
 
Description Chair of session on Global Health Security at World One Health Congress 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Cleaveland chaired a session on Global Health Security at the on-line World One Health Congress, which triggered some interesting debate around One health priorities and operationalisation, epidemic preparedness, governance, leadership and mentorship.
The congress website recorded 44,456 users.
Distribution: 1106 researchers, 562 governments, international organisations.; 61 industry participants; 17 press.
Year(s) Of Engagement Activity 2020
URL https://worldonehealthcongress.org
 
Description Community sensitisation meetings 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Study participants or study members
Results and Impact These were a series of community meetings held with village leaders of 4 villages in Longido and Ngorongoro district in Nothern Tanzania, in order to sensitise the community to ongoing and upcoming University of Glasgow projects. Meetings began with an overview of research on Taenia multiceps carried out as part of SEEDZ and subsequent projects. This included showing attendees the life cycle of the parasite (via leaflets and video) and suggestions on ways it can be prevented. Discussion then moved onto informing the community about upcoming research in prevention of zoonoses and other livestock diseases including mobilising key members to facilitate research.
Year(s) Of Engagement Activity 2019
 
Description District and ward medical and veterinary health providers meeting - AD + JV 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact A workshop attended by medical and veterinary health providers from the district and ward level from four districts in Tanzania. The aim was to deliver key outcomes from ZELS and related University of Glasgow projects and to spark discussion across sectors on ways to reduce impacts of zoonoses in pastoral communities. The event used Ketso - a particpatory toolkit used to faciliate creative discussion - to gather intervention ideas from attendees. Discussion primarily focused on the practicalities of implementation, particularly focusing on raising awareness and introducing compulsory vaccination as key ways to prevent zoonoses. As a result of the workshop, plans were made for further engagement with attendees, including creation of a zoonoses factsheet to assist ward and district health workers in further engagement with pastoral communities.
Year(s) Of Engagement Activity 2020
 
Description Early Career Workshop 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Online presentation on "One Health: insights from research on endemic zoonoses" as part of a British Council workshop linking early career researchers from UK and the Shangahi Jiao Tong University, hosted and organised by the University of Edinburgh.
Year(s) Of Engagement Activity 2021
 
Description Final SEEDZ Workshop 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact The SEEDZ project hosted a final two-day workshop in Arusha and invited a number of Tanzanian stakeholders to attend including representatives from the Tanzanian One Health Coordination Desk, TVLA, NIMR, MoH&SW, Ministry of Livestock and Fisheries, and FAO ECTAD, the Norhern Zonal Veterinary Centre (ZVC) and District Veterinary Officers from Karatu, Mbulu, Meru, Longido, Babati, Monduli, Simanjiro and Arusha District Coucils. Community leaders and local and international NGOs also attended, including GALVmed and Haki Kazi Catalyst. Researchers from Tanzanian and International institutions were also in attendance, including the University of Glasgow, Institute of Development Studies, Washington State University, University of Otago, Duke University, Scotland's Rural College, Kilimanjaro Christian Medical University College, Soikoine University of Africulture, University of Dar es Salaam and the International Livestock Research Institute. The first day was attended by 69 people and provided an overview of the work being carried out across Tanzania as part of the ZELS programme, including outputs from the SEEDZ, HAZEL and Brucella projects and the Life on the Edge project. The second day involved a participatory problem-solving session using Ketso? tools and focussed on interventions and policy implications of the research presented on the first day.
Year(s) Of Engagement Activity 2018
 
Description George MacDonald medal presentation - Royal Society of Tropical Medicine and Hygiene 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Webinar presentation on "One Health Interventions: Recognising Interconnections, Addressing Inequalities" in relation to award of the George MacDonald medal from the Royal Society of Tropical Medicine and Hygiene.
Year(s) Of Engagement Activity 2022
URL https://rstmh.org/events/george-macdonald-medal-talk-professor-sarah-cleaveland
 
Description Keynote presentation - Zoonoses 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Keynote presentation at the virtual conference "Internatoinal Symposium on Zoonoses Research"
Year(s) Of Engagement Activity 2021
URL https://g-f-v.org/en/events/zoonoses-2021-international-symposium-on-zoonoses-research/
 
Description Poster presentation at World One Health Congress (Jennika Virhia) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Poster presented by Dr. Jennika Virhia on "But our goats are dizzy: participatory epidemiology, co-produced research and endemic zoonoses in northern Tanzania" at the World One Health Congress.
The congress website recorded 44,456 users.
Distribution: 1106 researchers, 562 governments, international organisations.; 61 industry participants; 17 press.
Year(s) Of Engagement Activity 2020
URL https://worldonehealthcongress.or
 
Description Presentation - World One Health Congress 2022 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presentation given by S. Cleaveland on "Pilot survey of cystic echinococcosis in Masaai livestock-keeping communities of northern Tanzania". In-person attendance of ~ 250 participants with additional participants (up to ~ 1000 people) able to access the recording on demand. Sparked questions and discussion. Request for further participation has resulted in invitation to speak at the European Congress of Clinical Microbiology and Infectious Diseases in Copenhagen (2023).
Year(s) Of Engagement Activity 2022
URL https://worldonehealthcongress2022.miceapps.com/client/sites/view/WOH2022
 
Description Rabies in the Americas - One Health keynote presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Rabies in the Americas keynote presentation on "One Health contributions towards more effective and equitable approaches to health", which triggered lively discussion.
Year(s) Of Engagement Activity 2021
URL http://rita2021.com.br/index_en.html
 
Description SEBI-TZ, Tanzanian Veterinary Association, 5-8 December 2018, Arusha Tanzania 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A presentation at Tanzanian Veterinary Association 'Supporting Evidence Based Interventions - Causes and Extent of Reproductive Loss and Mortality of Domestic Ruminants in Tanzania (SEBI-TZ)' , 5-8 December 2018, Arusha Tanzania
Year(s) Of Engagement Activity 2018
 
Description Taenia multiceps coenurosis in Tanzania: a major and under-recognised livestock disease problem in pastoral communities, Tanzanian Veterinary Association, 5-8 December 2018, Arusha Tanzania 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A presentation at Tanzanian Veterinary Association Taenia multiceps coenurosis in Tanzania: a major and under-recognised livestock disease problem in pastoral communities' , 5-8 December 2018, Arusha Tanzania
Year(s) Of Engagement Activity 2018
 
Description Videos and brochures on One Health research at University of Glasgow 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Production of video and brochures around One Health themes and dissemination at the World One Health Congress in 2020 via the Scottish Institutions' virtual "Hub".
Year(s) Of Engagement Activity 2020