Successful adoption of a One Health approach could have far-reaching impacts on poverty alleviation, health and food security, particularly in developing countries through integrated control of neglected zoonoses. However, the practical implementation of this approach presents many challenges. Anna Okello and colleagues argue that, for effective implementation, lessons learned and ‘best practice’ must be led by national and regional stakeholders drawn from a variety of disciplines. High-profile regional and international institutions can play an important role in the global governance of One Health by encouraging individual countries to devise appropriate tailored solutions that are workable within their own context.
- British Veterinary Association
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‘ONE Health’ is becoming a 21st century exhortation, but the intricate relationships and linkages between animal health and the wellbeing of human beings have been noted over many centuries. Today, One Health links animal and human health together with the ecosystems in which we live. This framework has political and socioeconomic dimensions addressing increasing human population, land degradation, poverty, food security and globalisation. Sustainable healthy ecosystems to support the planet's species, and the people whose livelihoods depend upon them, is a fine goal; however, the true test of One Health lies in its practical realisation, particularly in developing countries where the stakes are much higher (FAO 2008). In addition to the health professions, many different disciplines can make a contribution to One Health. Efforts are being made to attract development specialists, wildlife and environment experts, socioeconomists and other contributors into One Health networks.
Revival of the One Health concept in the 21st century
The connectivity between animals, humans and the environment has been recognised for centuries. James Harlan Steele, a former USA assistant surgeon-general, noted that ‘The relation of animal disease to human disease was observed in the ancient civilisations of Babylon, the Nile Valley, and China. They were described by Leviticus in the Old testament, by Hippocrates in Greece, and by Virgil and Galen in Rome’ (Steele 1964). In his book ‘Guns, Germs and Steel’, Jared Diamond (1997) puts it more bluntly: ‘Questions of the animal origins of human disease lie behind the broadest pattern of human history, and behind some of the most important issues of human health today’. Examples of the relationship between zoonotic disease and human tragedy are seen throughout history, the most notorious being the ‘Black Death’, spread by rats, that killed millions of people in the Middle Ages. Jubilation surrounding the end of the First World War was marred by the 1918/19 ‘Spanish flu’ pandemic, which was probably linked to influenza strains circulating in birds (Taubenberger and others 2005). Recent outbreaks of human sleeping sickness in Uganda have been linked to unrestricted cattle restocking in districts that had experienced decades of civil unrest (Fèvre and others 2001, Picozzi and others 2005).
The 1997 H5N1 avian influenza outbreak was the tipping point in the revival of the One Health concept. The highly pathogenic avian influenza (HPAI) H5N1 epizootic – mostly affecting birds with ‘spillover’ into other species, including people – followed a series of zoonotic disease scares caused by severe acute respiratory syndrome (SARS), Nipah and West Nile viruses, all of which prompted calls for closer international collaboration for surveillance and control. The Global Response to Avian Influenza (GRAI) attracted broad, strong and rapid political support, in part due to a recognition that emerging diseases in animals can have both health and economic impacts across many continents. However, the main driver for the exceptional political response was most likely based on fear amid a series of alarming and politically disastrous health-related crises that occurred over the period 1990 to 2005 in developed countries (see Gibbs 2005).
The One Health Initiative Taskforce Report from the American Veterinary Medical Association (AVMA) defines One Health as the ‘collaborative effort of multiple disciplines working locally, nationally, and globally to attain optimal health for people, animals and our environment’ (AVMA 2008). The external action arm of the European Union (EU) (one of the driving forces behind the GRAI and the globalisation of the One Health approach) adopted the following definition: ‘The improvement of health and well-being through (i) the prevention of risks and the mitigation of effects of crises that originate at the interface between humans, animals and their various environments, and (ii) promoting a cross-sectoral, collaborative, ‘‘whole of society’’ approach to health hazards, as a systemic change of perspective in the management of risks’. This EU definition aligns with the approach adopted by the Food and Agriculture Organization (FAO). The World Health Organization (WHO) and the World Organisation for Animal Health (OIE) have more restricted definitions, focusing on zoonotic threats.
Pressure on resources
Sixty-one per cent of the known human infectious diseases are commonly attributed to have originated in animals, with emerging infectious diseases being twice as likely to be associated with zoonotic disease (Taylor and others 2001). The World Bank has estimated that zoonotic disease outbreaks in the past 10 years have cost the health and livestock sectors $US 20 billion globally; this figure leaps to $US 200 billion when external costs such as loss of trade, tourism and tax revenues are considered (Anon 2010a). The causes of this worldwide spike in zoonotic diseases are complex, but may be related to the increase in global demand for animal protein together with the emergence of newly developing economies and intensification of farming systems (Delgado and others 1999). Increased contact with wildlife through poaching, bushmeat consumption and intrusion of farming systems into natural habitats all increase the potential for zoonotic diseases to spill over from their wildlife reservoirs into domestic animals and humans, as seen with Ebola virus and human immunodeficiency virus (HIV). Slash and burn agriculture was implicated in the 1998 Nipah virus outbreak in Malaysia (Kaw 2003). The distribution of vectorborne zoonoses such as Rift Valley fever, human African trypanosomiasis and West Nile fever could all potentially be affected by climate change (Anon 2010a). Globalisation and tourism facilitate the spread of people, animals and animal products throughout the world, often in less time than a pathogen's incubation period, that is, ‘pathogens as hitchhikers’ (Gibbs 2005). Unsafe movements of animals can introduce disease into naive populations, such as the 2003 monkeypox outbreak in the USA traced to the shipment of rodents from West Africa; it has also been estimated that tens of millions of animals are exported from Asia for use in traditional medicine and food. The pressure currently placed on the world's strained resources has led to the AVMA's concern that the ‘world’s latest generation could be the first in history to experience a reduction in life expectancy and health in general' as a result of exposure to emerging diseases and our increasing interdependence with animals and their products (AVMA 2008).
A recent One Health report describes changing agricultural systems, globalisation and deforestation as examples of ‘upstream’ contributions to zoonotic disease emergence, and experts argue that a greater understanding of upstream factors is required to promote a shift of focus away from ‘fire-fighting’ towards a more proactive One Health approach (Anon 2010a). Closer collaboration between veterinary, medical and ecological disciplines for the diagnosis, surveillance and control of emerging zoonotic infections should become a priority.
One Health and poverty alleviation
The sixth of the Millennium Development Goals (MDG) agreed by the United Nations in 2000 aims ‘to combat HIV/AIDS, malaria, and other diseases’; the ‘other diseases’ are known as the ‘neglected tropical diseases’ and it is estimated almost every person in the ‘bottom billion’ (Collier 2007) is affected by at least one of these neglected diseases (Hotez and others 2009). The WHO recognises a group of ‘neglected zoonotic diseases’ within the neglected tropical diseases, including anthrax, bovine tuberculosis (TB), brucellosis, cysticercosis/neurocysticercosis, cystic echinococcosis, rabies and human African trypanosomiasis (WHO 2009). Neglected zoonoses are endemic throughout the developing world where conditions for their transmission are ideal. Poor sanitation, close living arrangements between people and animals, intense farming practices as a result of diminishing land resources, and traditional cultural practices – these all contribute to infectious diseases in people or animals or, in the case of zoonoses, both. Besides affecting the health of people in these poorest communities, zoonotic disease contributes to livestock productivity losses (or death), placing a great strain on those whose livelihoods depend upon them.
In 2007, the WHO published an eight-year ‘Global plan to combat Neglected Tropical Diseases’, in which the link between neglected diseases, poverty and the MDG was acknowledged, together with a ‘focus on populations and interventions rather than specific diseases’ (WHO 2007). In 2005, the UK Commission for Africa also recommended specific funding for the neglected diseases; however, progress towards this has been slow, with concerns that the ‘big three’ diseases (malaria, HIV/AIDS and TB) receive disproportionate attention (Molyneux 2008). The burden of endemic zoonotic disease in poor communities is poorly represented due to gross under-reporting and misdiagnosis. This has a serious knock-on effect in terms of funding for both research and control (Maudlin and others 2009). Most neglected tropical diseases can be controlled with relatively little cost and have been described as the ‘low hanging fruit’ of the world's disease burden (Molyneux 2008). Present investment in the control of these diseases is perceived to be neither fair nor sensible and, given the very clear relationship between these diseases and poverty, it is difficult to rationalise their ‘neglect’ (Maudlin and others 2009).
The tools used for disease prioritisation, such as the disability-adjusted life year (DALY), have been criticised as not being applicable to neglected diseases (Canning 2006) and to zoonoses in particular (Maudlin and others 2009). It is argued that ‘hidden’ morbidities, including anaemia, diarrhoea, and loss of work and education opportunities associated with neglected tropical diseases, are not captured by traditional calculation methods (Canning 2006). Focus should centre instead on the cost-benefits of interventions, which, in the case of many neglected diseases, are high, with the treatments being efficacious, pro-poor and easy to implement (Molyneux 2008).
There is a need to engage policy analysts, institutional advocates and the public if the true burden of neglected disease is to be reduced. Many countries do not consider zoonotic diseases important ‘simply because the diagnostic capacity to detect them hardly exists’ (Zinsstag and Tanner 2008). The potential for under-reporting is common for diseases where diagnostics are unavailable or access to health services is poor, as is often the case in rural areas of developing countries where risk factors for zoonoses are high. When considering national disease surveillance, social researchers can help to identify hotspots of disease circulation and focus surveillance activities. The ‘big three’ can share symptoms with zoonoses; for example, the undulating fever usually assumed to be malaria in endemic areas is also a common symptom of brucellosis, leptospirosis and first-stage sleeping sickness. Some 50 to 80 per cent of fevers attributed to malaria are due to other causes (Zinsstag and Tanner 2008), and malaria misdiagnosis contributes to the cycle of ill health and poverty (Amexo and others 2004). Participants in a recent focus group discussion in Uganda described their belief that drinking raw milk (a risk factor for brucellosis) causes malaria (A. Okello, personal communication).
Implementation of One Health strategies to control both neglected and emerging zoonoses in developing countries is not without its challenges. Surveillance may be neglected due to many factors but frequently because of a lack of incentive for smallholder farmers, whose investments in biosecurity may not be reflected in demonstrable market returns (FAO 2008). The first international congress on One Health (Anon 2011a) highlighted several successful One Health field initiatives being implemented in various parts of the world, including PREDICT, a global early warning system for emerging diseases from the United States Agency for International Development (USAID) based on SMART wildlife surveillance (Anon 2011b). The 1999 FAO/OIE/WHO veterinary public health conference recognised that opportunities for cross-disciplinary collaboration are not confined to specific regions, do not respect international borders and may extend across ethnic and political divides (FAO 2003). The benefits of a One Health approach for surveillance and control of zoonotic diseases in developing countries were reiterated in a keynote speech by Ester Schelling at a WHO/EU/ILRI/FAO/OIE/AU joint meeting on neglected zoonoses in Nairobi in 2007 (WHO 2009). Institutional support for the control of neglected zoonoses is growing, and by simultaneously saving lives and securing livelihoods, the control of neglected zoonotic diseases offers a real and highly cost-effective opportunity for alleviating poverty, especially in remote rural communities and marginalised peri-urban communities (WHO 2009).
Cross-sectoral integrated approaches for One Health worldwide
An integrated approach to One Health through ‘the creation of linkages among existing programmes to improve the delivery of health interventions given existing commitments and resources’ (Grépin and Reich 2008) is difficult to deliver in practice. Questions of institutional roles and responsibilities inevitably arise, with integration often interpreted as being interdisciplinary, interorganisational or intergovernmental, depending on the organisation promoting it.
The GRAI was launched in January 2006 at the International Ministerial and Pledging Conference of Beijing, cohosted, organised and sponsored by the Chinese government, the European Commission and the World Bank. Apart from financial pledges ($US 2 billion), an unprecedented political and interinstitutional process was launched in Beijing. The ‘trust-based’ collaboration between key political actors (EU, the USA and the UN) established five subsequent years of cooperation on avian influenza, pandemic preparedness and readiness and related issues. The ‘Beijing Principles’ were adopted by more than 100 countries, regional bodies, international organisations and representations of the civil society, and established a new type of collaboration, based on instant diplomacy. One of the conditions was the production and adoption by national governments of integrated work plans for the control of HPAI. The EU insisted that such plans should foster long-term capacity building by being adaptable for threats other than HPAI. Subsequent progress has been made at international ministerial conferences held in Bamako (December 2006), New Delhi (December 2007), Sharm El-Sheikh (October 2008) and Hanoi (April 2010). Trust-based exchanges in New Delhi led to a soft agreement to promote the One Health approach as a natural extension of the GRAI. In October 2008, FAO/OIE/WHO/UNICEF/World Bank and the UN System Influenza Coordination produced ‘Contributing to One World, One Health: A Strategic Framework for Reducing the Risks of Infectious Diseases at the Animal-Human-Ecosystems Interface’ (FAO 2008). This framework addresses emerging diseases with the potential for ‘significant transboundary or socioeconomic impacts’ arising at the animal-human-ecosystems interface and, while the focus is mainly on emerging zoonoses, implementation in developing countries could serve to address endemic zoonoses. The most recent international ministerial conference on animal and pandemic influenza took place in Hanoi in April 2010, where more than 70 countries, regional bodies and international organisations recognised the need to address gaps in public health and animal health systems to reduce the impact of zoonoses, avert potential pandemics of animal origin, mainstream investments and capacity in country health systems, and to address the One Health challenges (Anon 2010b).
The international approach has perhaps focused too much on ‘emergency response’, rather than improving understanding of disease dynamics in animals before a human health issue arises (Anon 2010a). Many feel greater emphasis should be placed on early warning systems and outbreak prevention from reservoir populations (Anon 2010a). During the 1999 West Nile virus outbreak in New York, veterinarians reported dozens of crows dying some months before the human cases; however, the surveillance network did not clarify who was responsible for investigation of the bird deaths and subsequent communication with public health officials (Kahn 2006). Outbreaks of Rift Valley fever in Mauritania were considered to be yellow fever until public health services were notified of cattle abortions by the Ministry of Livestock (Zinsstag and others 2007). Lessons have been learned from such examples, and international and regional collaboration to combat H5N1 influenza is unprecedented.
The WHO has emphasised stakeholder participation and political commitment for sustainable control of zoonotic diseases that suggests individual countries be responsible for ‘sustainable collaboration activities’ and should capture ‘the momentum generated by avian influenza’ (WHO 2008). National platforms set up as a result of HPAI control and surveillance programmes may evolve into collaborations for other zoonotic diseases such as rabies and brucellosis (A. Okello, personal communication). There has been no systematic survey of the current status of the interministerial task forces set up in response to avian influenza; however, the first evaluation of the outcomes and impact of the GRAI (European Commission 2010) notes that the impact of the response to avian and pandemic influenzas has benefited the control of other diseases of animals and humans. An interesting example concerns Lao PDR, where the National Avian and Human Influenza Coordination Office, created in 2006, has been upgraded to a broader National Emerging Infectious Diseases Coordination Office (NEIDCO). There have also been recommendations that the ad hoc interministerial task forces often formed in zoonotic disease outbreaks, such as anthrax and Rift Valley fever, be formalised into long-standing platforms for risk analysis and prevention for a range of endemic zoonoses (Zinsstag and Tanner 2008).
Veterinarians and physicians working together
Combining animal and human health disciplines is complicated; despite calls for ‘common sense to prevail’ (Van der Zeijst 2008) progress has been slow, particularly in developing countries where collaboration has often been ‘totally lacking’ (Zinsstag and others 2005). Closer cross-disciplinary collaboration could be promoted through zoonotic disease research centres or joint response teams using the model established for the pastoralist-livestock vaccination programmes in Chad in 2002 (Zinsstag and others 2005). The success of mass drug administration interventions where several neglected tropical diseases coexist presents a natural entry point for integrated public health programmes (Lammie and others 2006). Collaboration between veterinary and public health services through shared transport costs, laboratory facilities, joint training, stocks of reagents, cold chain storage and community mobilisation offer other ways of integration, but these are often poorly documented and based on person-to-person arrangements instead of interinstitutional and formally agreed – hence sustainable – collaborations (Schelling and others 2005). Progress in this area has, however, been made through programmes and projects funded under the GRAI and One Health umbrellas (A. Vandersmissen, personal observations). One Health is gaining support in the USA as the underlying principle for national disease control frameworks, but preparedness to cope with zoonotic disease outbreaks is variable, with ‘200 different government offices and programmes responding to five zoonotic diseases’ (Gibbs 2005).
To promote and sustain interest in comparative research, there have been recommendations to change the way research is funded; for example, by promoting ‘joint funding streams from human, animal and environmental health sectors to support integrated public health programmes’ (Pappaioanou 2010) and prioritisation of research grants to teams promoting professional collaboration and interdisciplinary research (Kahn 2006). The AVMA cites progress in higher educational teaching over the past five years in this regard, which has improved linkages between public health and veterinary schools (AVMA 2008).
Opportunities for private sector engagement in zoonotic disease control
Despite the traditional view of zoonotic disease control as a public good, there is extensive support and justification for the role of the private sector in this area of One Health (Holden 1999). Potential benefits lie not only in the control of disease in animal populations, but also in ecosystem management. There is growing support for the control and prevention of zoonotic disease in domestic animal reservoirs (Zinsstag and others 2007, Maudlin and others 2009, Anon 2010a). Many zoonotic diseases can be controlled or prevented via vaccination programmes, administration of insecticide in order to create animal ‘baits’ for vectorborne disease, or simple therapeutics to break transmission. Examples include rabies, brucellosis or avian influenza vaccination programmes, spraying cattle to repel tsetse flies to prevent transmission of human African trypanosomiasis, or treatment of pigs with oxfendazole as an adjunct to human interventions against cysticercosis (Gonzalez and others 1997). In all cases, there exist opportunities for private sector engagement. Aside from the clear opportunities for the pharmaceutical industry to benefit through sales and further development of therapeutic drugs and vaccines, there are prospects for animal traders and for commercial and smallholder farmers to contribute to zoonosis control by promotion of good practice and participation in quality control programmes. There remain issues with the level of incentive available within current market structures, particularly in developing countries, for individuals to participate in such programmes.
It is interesting to compare global financial and institutional support for health interventions exclusively benefiting people in developing countries with that for neglected zoonoses. Human health interventions such as measles vaccination or HIV/AIDS prevention programmes attract strong moral and empathetic support, leading to significant funding being directly funnelled to health ministries. The case of ‘who pays’ for zoonotic disease control is harder to define, despite the seemingly obvious benefits to society. For some zoonoses, while the human health risks are important, dealing with the animal infection might provide the most effective control route (WHO 2006).
Examples of emergency control of zoonotic disease outbreaks from the USA and the UK have been analysed in terms of ‘who pays’. In the USA, the federal government has overwhelmingly contributed to payment for control and compensation to farmers (E. P. Gibbs, personal communication); for example, the 1999 outbreak of West Nile virus in the USA saw large financial contributions to research and other public good activities from the federal government, while individual owners of horses were responsible for the costs associated with clinical disease and preventive vaccination. Similarly, in the case of bovine spongiform encephalopathy in the UK, the government funded the cost of the eradication campaigns and compensation to farmers; a similar approach is taken for the ongoing control of bovine TB. In such cases, public funding was related to the sense of urgency; however, the expectation that governments provide similar financial support for the control of endemic zoonoses, particularly in developing countries where the true burden is either unknown or underestimated, is unrealistic.
Control of endemic zoonoses often requires interventions within domestic animal populations. Due to the privatised nature of veterinary services in most countries, either the individual animal owner or the appropriate animal industry is often expected to contribute financially. Expecting a farmer to pay for what they may view as a ‘public health’ service, with little perceived direct reward, is a difficult proposition, and national programmes need to ensure that a willingness to pay is considered within any proposals. In a recently initiated Ugandan intervention against human African trypanosomiasis, farmers pay the full cost for spraying their cattle against the tsetse fly vector (Anon 2011c) but ‘willingness to pay’ often stems from the additional benefit that the treatment controls ticks, and from the money saved from purchasing drugs against tickborne diseases (S. C. Welburn, personal communication). In New Zealand, farmers pay (either directly to private veterinarians or via slaughterhouse levies) to have their livestock tested for bovine/cervine TB and ovine brucellosis (A. Okello, unpublished observations). However, this willingness to pay may be directly related to the heavy penalties (fines and market exclusion) imposed for non-participation.
In many developing countries where market incentives are few, animal movement restrictions are poorly enforced and compensation for condemned livestock is rarely implemented, there may be little to motivate farmers to cooperate with surveillance programmes and even less to pay for interventions. New strategies are needed to encourage farmer engagement, address under-reporting and strengthen national veterinary services. Certain industries (for example, those involved in the trade of wild animals and their products) need to be encouraged to participate in surveillance and control programmes (Anon 2010a). Incentives through subsidised veterinary services and improved market opportunities could be considered.
Public-private partnerships (PPP) are gaining momentum in many development programmes worldwide and, given the public and private good aspects of zoonotic disease control, may offer an attractive option. A PPP ‘Stamp Out Sleeping Sickness’ has been successfully implemented in northern Uganda against human trypanosomiasis, targeting the animal reservoir of disease. At present, the bill for the public good aspect in many programmes is taken up by the donor community rather than national governments. Cost-sharing across ministries (and sectors) must be addressed for sustainable zoonotic disease control in the future.
Integrated control of neglected zoonoses
Conceptual support for global One Health interventions, policy frameworks and institutional collaboration is growing, especially for implementation in developing countries, where conditions for the emergence and spread of zoonotic disease are arguably more favourable than in developed countries, and where healthy ecosystem services are perceived to be most vulnerable.
Integrated approaches for the control of the neglected zoonoses may offer a new paradigm for One Health, adding value to the practical implementation of ‘public health’ measures. The cost-effectiveness of interventions against zoonotic diseases have been assessed by a number of studies, including the use of animal-to-human transmission models (Roth and others 2003, WHO 2006, Zinsstag and others 2007). Where assessments calculate the economic contribution of each sector towards disease control (as a percentage of overall benefits gained to that sector from being disease-free), zoonoses control is shown to be highly cost-effective (Zinsstag and Tanner 2008).
A five-year research project funded by the EU, ‘Integrated Control of Neglected Zoonoses in Africa’ (ICONZ) examines a number of integrated animal interventions for the control of neglected zoonoses, with a strong element of innovation and public engagement (ICONZ 2009). ICONZ involves 21 European and African universities and research institutes working on case studies of zoonotic disease clusters in seven African countries: Morocco, Mali, Nigeria, Uganda, Tanzania, Mozambique and Zambia. The need for zoonosis control programmes to consider both human and animal health factors, along with monetary and other benefits to society, can encourage participation from public health services in interventions ‘that may otherwise never be cost-effective from a health sector point of view alone’ (WHO 2006). It is envisaged that this large collaborative project, targeting the neglected zoonotic diseases, will fill vital knowledge gaps that currently exist, particularly on the burden of neglected zoonoses, and provide a strong evidence base to support policy decisions at the international, regional and national levels in developing countries.
The need for political ownership and for leadership in the global implementation of the One Health approach is now recognised, with several high-profile experts, officials and institutions stepping up to the role. Such leadership should, by definition, be cross-sectoral, based on networks (including existing ones). The AVMA is one such example; its One Health Initiative Task Force report of 2008 is intended to be ‘a blueprint to guide implementation or to transform the vision into action’ (AVMA 2008). Leadership is required on many levels if the concept is to become effective in the long term. The establishment of successful One Health approaches around the world will require not just cross-sectoral engagement and collaboration, but a profound understanding of institutional missions, capacities and roles and responsibilities, in order for new methods of collaboration to be realised (Anon 2010a).
It is perhaps those in developing countries who have the greatest opportunity to contribute towards sustainable implementation of the approach. While support and guidance can be gained from international and regional collaborations, the ultimate responsibility lies within individual countries to develop a framework evolving from local issues, rather than relying on an imposed, top-down approach; as summarised by Malaysian virologist S. K. Lam: ‘While the One Health initiative is to be lauded, the solutions may not lie in the implementation of methods found suitable for the developed world. One size does not fit all here. What is to replace deforestation, open burning or free-range poultry farming? Perhaps encouraging eco-tourism will prevent deforestation. A more pragmatic and innovative approach as well as a paradigm shift needs to be implemented to enable any hope that this noble initiative will turn from a dream to a reality’ (Lam 2010).
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