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Equine Veterinary Journal ISSN 0425-1644 DOI: 10.1111/evj.12359

Science in brief: Report on the first Havemeyer workshop on infectious diseases in working equids, Addis Ababa, Ethiopia, November 2013 The authors prepared this report, but all workshop participants contributed and are cited throughout the report, and their names and affiliations are listed in Supplementary Item 1.

Introduction The working equid is of vital importance in many low-income countries where horses, mules and donkeys are the primary means of transport and traction. Notwithstanding basic husbandry and welfare needs, infectious diseases compromise the health and welfare of these working animals, which in turn threatens the livelihoods of the most vulnerable members of society. A workshop on Infectious Diseases of Working Equids was held in Addis Ababa, Ethiopia in November 2013, attended by 35 participants representing academia, nongovernmental organisations (NGOs), governmental institutions and the World Organization for Animal Health (OIE). The aim of the workshop was to identify ways to reduce the burden of infectious diseases in working equids worldwide. The specific workshop goals were as follows: 1) to identify the global working equid population and define its role in low-income countries with respect to food security, poverty alleviation and gender equity; 2) to collate the current knowledge of infectious diseases in working equids and identify key priority pathogens responsible for high morbidity and mortality; 3) to identify current diagnostic, surveillance, treatment and prevention strategies for infectious diseases in working equids and identify gaps and strategies needed for future control programmes; 4) to identify current and future roles and responsibilities of various institutions and stakeholders in infectious disease control of working equids and ways to engage them in effective disease reduction; and 5) to identify key focus areas with the greatest opportunities for impact on the occurrence of infectious diseases affecting working equids and form consensus opinions on the future goals and strategies to reduce the impact of infectious diseases on working equids. Workshop presentations focused on the role of working equids and their impact on livelihoods, priority infectious diseases, surveillance and disease control strategies, regulatory policies, the role of institutions in disease control, research gaps and funding opportunities. This workshop report focuses on the following 3 areas: working equids and their role in livelihoods; infectious diseases of working equids; and solutions and strategies for the future.

Working equids and livelihoods The world equine population is estimated to be 112 million (approximately 58.5 million horses, 43 million donkeys and 10.5 million mules), although this is likely to be a gross underestimate [1]. Guthrie (University of Pretoria, South Africa) described the global distribution of equids as follows: 46 million in the Americas; 7 million in Europe; 33 million in Asia; and 25 million in Africa. For many countries, there are no accurate data regarding their working equid populations, with traditional livestock census data routinely omitting the working equids, resulting in our incomplete understanding of the world equid population. Guthrie and Reed (The Brooke, UK) explained that the majority of the world’s equids are working equids, many residing in low-income, net food-importing countries (more than one-third of all equids, and >50% of all donkeys). Population numbers reported by the United Nations Food and Agriculture Organization (FAO) have shown the number of working animals to be increasing on the African continent, although they are decreasing in many other areas of the world. In Central and South America, horses remain common on smallholder farms in spite of the increasing adoption of tractors, and animal-drawn carts are quite widely used for rural and urban transport. In many parts of Africa, animal traction continued expanding during the 20th century due to its promotion by commodity companies and extension services. Donkeys increased in numbers from 15.3 to 19.5 million in the decade from 2002 to 2012 [1], and

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the geographical range of these animals, the ‘donkey line’, has moved southward on the African continent. In East Africa, animal traction is gradually increasing, notably in Tanzania, with one million working animals, and in Uganda. Animal use is slowly diversifying from the traditional ploughing and pulling of carts to increased use for weeding and conservation tillage, as well as increased use of donkeys for transport and light tillage. Within Ethiopia, 5 million donkeys are used for pack transport. Horses and mules are used widely for riding, although in many towns, urban horse carts are being replaced by motorised three-wheelers. In Southern Africa, animal traction has been in use since the 17th century, making it traditional in many smallholder systems. In recent decades, it has been promoted and is spreading in several countries, including Malawi, Namibia and Zambia. In North Africa, in particular Morocco and Egypt, the widespread traditional use of work animals remains important in agriculture. Reed reviewed a number of studies demonstrating the extensive impact of working equids on the livelihoods of millions of individuals worldwide. These equids perform numerous activities, including the transportation of goods, people and construction materials, as well as being used in agricultural and tourism activities [2–4], as described by Reed and Aklilu (SPANA, Ethiopia). They have a role in reducing poverty, providing food security, enhancing rural development and promoting gender equity for millions worldwide, many of whom are in the ‘bottom billion’ of the world’s growing 7 billion population [5,6]. These animals are especially important to vulnerable groups, to landless communities and to women, for whom they can provide an effective entry point to income-generating activities [7,8]. Working equids currently have a limited place within many animal health systems and are largely absent from agricultural policy, research and education [4]. They are frequently not included in disease eradication and vaccination campaigns, and despite many equine diseases featuring on the OIE notifiable disease list, these diseases are not included in government disease surveillance systems. Working equids do not usually feature in legislation or guidelines, and if slaughtered for food consumption and animal products, are not usually included in the meat inspection systems. The importance of animals to the livelihoods of the poor is clear; however, more information is available on the role of livestock to livelihoods than on working animals. Stringer (SPANA, UK) and several other presenters described how the contribution of working animals to livelihoods is generally not well understood or recognised at the level of national or international government. Despite ownership of a working animal often enabling a family to benefit practically and economically, these animals may be perceived as having a low status at both local community and national governmental level.

Infectious diseases of working equids Several workshop contributors, including Aklilu, Reed and Stringer, stated that health and welfare of working equids is often compromised in many low-income countries as a result of the impoverished situations in which their owners live, challenging environmental and climatic conditions [9], the availability of appropriate medications and vaccines, and the widespread use of ineffective or harmful traditional therapies. The OIE standards for working equid welfare were reviewed by Bastiaensen (OIE, Kenya) and include freedom from malnutrition and thirst, distress and fear, pain and discomfort, and disease. Achieving these freedoms depends on the availability and affordability of resources, as well as owner knowledge of constraints relating to feed and nutrition, water and hydration, working capacity, disease prevention and equine healthcare management [10,11]. Equine Veterinary Journal 47 (2015) 6–9 © 2014 EVJ Ltd

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The prevalence and severity of health problems vary between countries and equid species [9]. As described by Aklilu, among the most prevalent of health constraints to working equids are wounds, often caused by poor management practices, such as overloading and inappropriate harness [7,9]. Notwithstanding the significant and overbearing compromises to the first 6 of the OIE standards, there is considerable peer-reviewed evidence that infectious diseases are an important constraint to the health and productivity of working equids [11–20]. However, there are limited data quantifying the occurrence, prevalence and distribution of many infectious diseases in working equids in the large populations in low-income countries. Guthrie and others described how many countries that are known to have large populations of working equids do not have an OIE official status for certain diseases, and many countries have no reporting history regarding many infectious diseases. Nevertheless, as described by several presenters, there is clear evidence of a wide regional distribution of several highly impactful diseases, which were reviewed in a series of summary presentations.

Viral diseases Newton (Animal Health Trust, UK) proposed that the most significant viral pathogens of working equids include African horse sickness virus, the encephalitides (Eastern/Western and Venezuelan equine encephalitis viruses), equine infectious anaemia virus, equine influenza virus, equine herpesvirus-1, rabies and West Nile virus. These diseases are widely distributed and cause considerable morbidity and mortality, but are often incompletely reported throughout the world.

Bacterial diseases Newton and Wernery (Central Veterinary Laboratory, Dubai) described important infectious bacterial diseases affecting working equids as including Burkholderia mallei (glanders), Clostridium tetani and Streptococcus spp.

Parasitic diseases Sutton (University of Glasgow, UK) described the wide distribution of parasitic agents seen in working equids. The most impactful parasitic infections may be gastrointestinal nematode infection (caused by large and small strongyles and Parascaris equorum), piroplasmosis caused by Theileria equi or Babesia caballi, and trypanosomiasis caused by Trypanosoma evansi (surra, transmitted by biting flies) and Trypanosoma brucei brucei, congolense and vivax (transmitted by tsetse flies).

Fungal diseases The most important fungal disease of working equids as described by Pinchbeck (University of Liverpool, UK) and Wernery, is epizootic lymphangitis, caused by Histoplasma capsulatum var. farciminosum. In regions where this disease is prevalent, such as large parts of Ethiopia, it is ranked as the most important infectious disease of horses in participatory studies conducted with owners [21,22]. In addition to these specific causes of infectious disease, several participants reported on the common occurrence of 3 types of syndromic diagnosis in working equids in the low-income countries in which they worked, which were a respiratory syndrome, a neurological syndrome and anaemia. The causes remain largely undifferentiated, but the high

prevalence and morbidity associated with these syndromes, together with the high priority assigned to them in participatory studies by owners, warrants urgent investigation to determine whether there is an infectious aetiology. Given the numerous infectious diseases that affect working equids, it is challenging but important to prioritise the pathogens on which to focus disease mitigation efforts. There was extensive discussion of the criteria for prioritisation, and the impact on animal welfare, socioeconomic impact on and importance to animal owners, prevalence, virulence and the potential for intervention were proposed as the most important factors. With these criteria in mind, the participants at the workshop, through a qualitative risk assessment framework, listed the diseases of the highest priority for investigation and specific intervention in an approximate rank order as African horse sickness, epizootic lymphangitis, tetanus, glanders and parasitic diseases, including gastrointestinal parasites, piroplasmosis and trypanosomiasis. There are 3 important caveats to this priority list. First, rabies was not included in the high-priority list because policies and interventions that reduce the occurrence of rabies in all mammals will also reduce the devastating impact of this disease in working equids. Second, while this was an international workshop, the workshop participants drew on experience primarily from Africa, the Middle East and the Indian subcontinent, and their opinions reflect these regional views. Third, it is critical to determine the role of infectious agents in the aetiology of the respiratory, neurological and anaemia syndromes described above, because these are viewed as highly impactful on the health of working equids. Such investigation could easily add to the list of the most highly impactful infectious agents; for example, influenza virus might be found to have a critical role in respiratory syndrome.

Solutions and strategies Identifying the impediments to progress in reducing the burden of infectious diseases in working equids was an important goal of the workshop, and Reid (Royal Veterinary College, UK), citing FAO, led a second prioritisation process to reach a consensus opinion on the key barriers in the following 3 categories: technical, social–behavioural and institutional (Table 1). This prioritisation exercise strongly identified the 3 most critical impediments to progress to be: 1) lack of data at a technical level; 2) limited equine-specific owner knowledge and education at a social–behavioural level; and 3) the low status of working equids at an institutional level. Technical data are crucial to all aspects of interventions to reduce the burden of infectious disease, but generating data requires a significant investment of time and resources. Examples of the types of data needed include the current and previous infection state of specific equid populations, disease distributions, population dynamics and disease epidemiology and equid ecology. Data are needed in order to make informed treatment decisions and to design and evaluate effective disease control strategies, ensuring interventions are valid. It was agreed that a more systematic approach to data collection is needed, including the use of systematic reviews to identify data gaps. Fevre (University of Liverpool, UK) explained how diagnostic methodology affects disease surveillance using brucellosis diagnosis in Kenya, and also gave examples from human disease problems, such as rabies and cysticercosis, of how under-reported and neglected diseases can be investigated even when data are sparse. Other sectors have faced many of the same challenges that the working

TABLE 1: Impediments to reducing the burden of infectious disease in working equids Technical

Social–behavioural

Institutional

• Data regarding numbers and movement of equids, specific disease epidemiology and ecology • Surveillance for occurrence of infectious diseases

• Owner knowledge and education about equine health and management • Understanding of socioeconomic impact of working equids • Impact of poverty and low priority of equids

• Equine status

• Veterinary resources (veterinarian training, availability of diagnostics, vaccines and therapeutics)

• Resource prioritisation • National animal health policies and infrastructure

The principal challenges in each category are listed in ranked priority. Equine Veterinary Journal 47 (2015) 6–9 © 2014 EVJ Ltd

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TABLE 2: Categorisation of priority diseases and syndromes, with strategies to achieve progress towards their mitigation Disease category

Examples

Ranked strategies for mitigation

1. Major technical equine data impediments to progress are limited. There is a good understanding of disease pathogenesis, diagnosis and prevention. Most technical data gaps are in terms of surveillance

African horse sickness, glanders, rabies, tetanus and gastrointestinal nematodes

2. Significant gaps exist in our understanding of disease pathogenesis, diagnosis and prevention. In addition, there are significant gaps in terms of disease surveillance

Epizootic lymphangitis, piroplasmosis, trypanosomiasis

3. Disease syndromes with an unknown/uncertain aetiological diagnosis, but significant prevalence and impact

Diagnoses of respiratory syndrome, neurological syndrome and anaemia

1. Advocacy at the institutional level, focusing on the positive socioeconomic impact of working equids on economies and owners and the negative impact of these diseases 2. Education of owners and society about equine management and welfare 3. Improved surveillance at both the national and the international level 1. Increased research to address technical data gaps in pathogenesis, diagnosis, treatment and prevention. Working groups will be an important strategy to achieve this goal effectively 2. Advocacy in order to secure significant new research funding from existing and new sources 3. Improved surveillance at both the national and the international level 1. Improved surveillance based on ‘gold-standard’ diagnostic approaches (post mortem/culture) to elucidate syndrome aetiology and epidemiology

equid sector is currently facing, and lessons can be learnt. Pinchbeck reviewed the key epidemiological knowledge gaps and explained how participatory studies can be used to overcome some of the challenges to collect data concerning these problems. The opportunities for tackling the technical data gaps were discussed, and included greater collaboration and coordination, conducting multipathogen studies in the same populations, economies of scale, and also sharing of samples between organisations to allow testing for multiple pathogens. Gaining funding support and changing social–behavioural and institutional factors require the quantification of the relative impact of infectious diseases on equids and their owners. Bojia (Donkey Sanctuary, Ethiopia) explained that a thorough understanding of the context within which these animals and their owners live and work is important in order to achieve disease control. The importance of understanding equine ecology was also emphasised by Morley (Colorado State University, USA), drawing on contemporary and historical equine disease outbreaks to make this point. There needs to be recognition of the complexity of communities and that community engagement is essential for the long-term success and sustainability of programmes. Reed commented that modern communication platforms, including social media, were already being used successfully to this end. In the future, these same technologies may be used for surveillance, if a way can be found to capture their potential. Pritchard (The Brooke, UK) described the role of government and governmental policy in disease control and the need for effective evidence-based advocacy to achieve this end. The workshop had the goal of developing consensus on strategies to reduce the impact of specific infectious diseases. To achieve this, each of the prioritised diseases or disease syndromes was categorised according to our level of technical understanding, and then strategies to address the impediments to progress were identified for each category (Table 2), in effect combining the 2 risk assessments. For diseases for which there is a strong body of evidence-based scientific understanding of pathogenesis, diagnosis and prevention strategies (category 1), the most important impediments are the technical data gaps in surveillance, addressing social–behavioural impediments through knowledge-transfer initiatives and addressing institutional impediments by effective advocacy to governments and funding bodies based on the socioeconomic importance of working equids to animal owners and economies and the negative impact of these diseases. For diseases such as epizootic lymphangitis (category 2), while there is a substantial body of evidence documenting the serious and widespread impact, there remains a lack of basic epidemiological knowledge about the occurrence, prevalence, impact, risk factors and transmission routes of this disease. In addition, such diseases require improved diagnostics, ideally point-of-care tests, and extensive research is needed on treatment and preventative measures. For this category of diseases, there is a clear and urgent need for new funding sources to support research as the highest priority. The final group of diseases (category 3) are syndromic, and for these diseases,

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epidemiological and investigative research is the most pressing priority. Addressing all of these infectious disease challenges could be facilitated by the formation of an OIE ad hoc working group to start working on standards for working equids, which would also raise the profile of working equids in international animal health. This goal has been achieved since the workshop (P. Bastiaensen, personal communication), and the first meeting was in June 2014. Workshop participants recognised that infectious diseases are one of several key welfare challenges faced by working equids, with other problems including low quality of nutrition, harness design, inappropriate workloads and farriery-related issues. Infectious diseases also interact extensively with these other health challenges, and in many instances are the issues that owners prioritise as important. A holistic approach to these health challenges will be important for success.

Future directions and conclusions This workshop demonstrated the continued and growing socioeconomic importance of working equids to the livelihoods of people in low-income countries and the extensive impact of infectious disease on working equids. This issue clearly demands action. The workshop identified and prioritised the key impediments to disease control at technical, social–behavioural and institutional levels that need to be addressed and identified which impediments were the most critical for the highest-impact diseases affecting working equids. Timoney (University of Kentucky, USA) and others strongly argued that by far the greatest challenge remains the lack of funding for research and initiatives in this area, which results from the relatively low priority assigned to working animals in general, and to working equids specifically, by funding agencies and government institutions. Data-driven advocacy will be required in order to change attitudes. Global networks of investigators can play a critical role in building this more robust evidence base. A. Stringer Society for the Protection of Animals Abroad (SPANA), London, UK D. P. Lunn College of Veterinary Medicine, North Carolina State University, Raleigh, USA S. Reid Royal Veterinary College, Hatfield, UK

Authors’ declaration of interests Andrew Stringer is employed by SPANA, one of the organisations that contributed funding for the workshop. Equine Veterinary Journal 47 (2015) 6–9 © 2014 EVJ Ltd

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Sources of funding Funding to support this workshop was provided by The Dorothy Russell Havemeyer Foundation. Additional support was provided by SPANA, The Brooke and The Donkey Sanctuary.

Acknowledgements The authors want to thank all sponsors of the workshop, and are particularly grateful for the assistance and support of Mr Gene Pranzo and The Dorothy Russell Havemeyer Foundation.

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12. Aklilu, N., Batten, C., Gelaye, E., Jenberie, S., Ayelet, G., Wilson, A., Belay, A., Asfaw, Y., Oura, C., Maan, S., Bachanek-Bankowska, K. and Mertens, P.P.C. (2012) African horse sickness outbreaks caused by multiple virus types in Ethiopia. Transbound. Emerg. Dis. 61, 185-192. 13. Alemu, T., Luckins, A.G., Phipps, L.P., Reid, S.W.J. and Holmes, P.H. (1997) The use of enzyme linked immunosorbent assays to investigate the prevalence of Trypanosoma equiperdum in Ethiopian horses. Vet. Parasitol. 71, 239-250. 14. Ameni, G. (2006) Epidemiology of equine histoplasmosis (epizootic lymphangitis) in carthorses in Ethiopia. Vet. J. 172, 160-165. 15. Ayele, G., Bojia, E., Getachew, M., Tesfaye, M., Manyahilishal, E., Amare, B., Abebe, A., Seyoum, F. and Anzuino, G. (2010) Important factors in decision making in tetanus cases in donkeys: experience of donkey health and welfare project, Ethiopia. In: The 6th International Colloquium on Working Equids: Learning from Others, Ed: The Brooke, The Brooke, New Delhi, India. pp 195-199. 16. Duguma, B. (2007) Seroprevalence and Risk Factors for Equine Herpes Virus 1 (EHV-1) and 4 (EHV-4) in Working Equids, Central Ethiopia, MSc Thesis, University of London. 17. Fikru, R., Reta, D., Teshale, S. and Bizunesh, M. (2005) Prevalence of equine gastrointestinal parasites in western highlands of Oromia, Ethiopia. Bull. Anim. Health Prod. Afr. 53, 161-166. 18. Getachew, M., Innocent, G.T., Trawford, A.F., Reid, S.W.J. and Love, S. (2010) Epidemiological features of fasciolosis in working donkeys in Ethiopia. Vet. Parasitol. 169, 335-339. 19. Okell, C.N., Pinchbeck, G.P., Stringer, A.P., Tefera, G. and Christley, R.M. (2012) A community-based participatory study investigating the epidemiology and effects of rabies to livestock owners in rural Ethiopia. Prev. Vet. Med. 108, 1-9. 20. Pearson, R., Alemayehu, M., Tesfaye, A., Allan, E., Smith, D. and Asfaw, M. (2001) Use and management of donkeys in peri-urban areas of Ethiopia, Phase 1. University of Edinburgh and Ethiopian agricultural research organization collaborative project, Centre for Tropical Veterinary Medicine, Draught animal power technical report 5. 21. Scantlebury, C., Pinchbeck, G., Reed, K., Gebreab, F., Zerfu, A., Aklilu, N., Mideksa, K. and Christley, R. (2010) Participatory assessment of the impact of epizootic lymphangitis in Ethiopia. In: The 6th International Colloquium on Working Equids: Learning from Others, Ed: The Brooke, Brooke, New Delhi, India. pp 184-186. 22. Stringer, A.P., Christley, R.M., Bell, C.E., Gebreab, F., Tefera, G., Reed, K., Trawford, A. and Pinchbeck, G.L. (2009) Participatory Situation Analysis (PSA): owner perceptions of working equid health and disease in Ethiopia. International Society of Veterinary Epidemiology and Economics (ISVEE) Conference.

Supporting information Additional Supporting Information may be found in the online version of this article at the publisher’s website: Supplementary Item 1: Participants in the first Havemeyer workshop on infectious diseases in working equids, Addis Ababa, Ethiopia, November 2013.

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Science in brief: Report on the first Havemeyer workshop on infectious diseases in working equids, Addis Ababa, Ethiopia, November 2013.

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