Abstract

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SINOPSIS

INTRODUCTION

Human, animal, and environmental health are inextricably linked in our modern, highly globalized society. We expect better health, secure food, clean water, and more comfort from limited natural resources. Balancing competing demands of human health, animal health, and sustainable environmental health is a grand challenge of our time. As the distance between human, domestic animal, and wildlife populations narrows and global trade and travel amplify our connectivity, pathogens shared by humans and animals have concurrently emerged.¹ Since 1999, among many examples, humans experienced outbreaks of West Nile virus in the United States and Europe, severe acute respiratory syndrome (SARS) virus in China, Middle East respiratory syndrome coronavirus (MERS-CoV) in the Middle East, and the emergence of the Ebola virus in West Africa. Shared pathogen exchange is perhaps best illustrated in the case of influenza, where humans serve as the source of influenza A virus (IAV) infection of pigs, and, after further evolution of the virus, it returns from pigs to humans, causing new outbreaks. The 2009 influenza outbreak was the most recent example of this cycle of human and animal infection. The failure to address interspecies transmission and ensuing pandemics as a one health issue has created the opportunity for continued emergence of novel IAV like H3N2v that emerged as a human pathogen during the agricultural fair season.²

These events highlight the complex interactions between human, animal, and environmental health and the importance of addressing medicine and health in a scientific manner that considers all contributing factors. Advancement of health at this level of complexity requires integration of medical disciplines spanning individual care to public health, with basic and applied sciences from atomic structure to sociology providing the knowledge base as shown in the Figure. The concept of One Medicine One Science (COMOS) builds on the idea that the basic biological processes underlying health and disease share common features such that medical knowledge and expertise in one species is relevant and applicable to other species. The scientific approach that expands our understanding of biological processes and the rational basis for medical practice is the same for all species. Thus, COMOS provides common ground to assist the organization of interdisciplinary groups to seek solutions to health challenges at local and global scales. Another aspect of COMOS is development of forums that, in addition to medical and scientific participants, includes industry, governmental and nongovernmental policy makers, and funders to assist in communicating the interconnectedness of human, animal and environmental health to a broad audience so that development of public policies that guide health priorities and investments at the national and international level are informed by the best scientific knowledge.

ONE HEALTH

The concept of one health emphasizes the interconnectedness of animal, environmental and human health, and has become a part of the health security and international development lexicon.³ The 2005 revised International Health Regulations and 2014 Global Health Security Agenda (GHSA) are 2 of many instruments that cement this connection/relationship/interdependence. At the international launch of the GHSA, the United States and 30 other countries, the World Health Organization (WHO), Food and Agriculture Organization (FAO), and World Organisation for Animal Health (OIE) agreed to work to prevent, detect, and respond to global infectious disease threats from the perspective of one health. Years before the release of the GHSA, the US Agency for International Development established the Emerging Pandemic Threats Program to “prevent, detect, and control” animal and human pathogens. These activities, which promote one health approaches in the United States and globally, are an important beginning but fall short of providing the robust scientific and culturally informed approach that is needed to address real world challenges.

Much dialogue on one health has focused on emerging disease surveillance, public health preparedness, and policy issues without connecting these issues to the scientific foundations that underlie pathogen emergence, global health threats, food security, environmental health, social organization, communication, and implementation of health, security, and safety measures. This limitation has resulted in a perceived and apparent separation of science and policy, sometimes diluting the utility of the one health movement. This article builds on the discussions and dialogue about the science of one health and its connection to policy that were held at the International Conference on One Medicine One Science (iCOMOS; www.icomos.umn.edu) in 2014 and to be held again in 2016.⁴ In particular, it was concluded that the key roles of food and medicine in addressing health needs of a changing world require the support of rigorous science that empowers informed decision-making and development of useful policies. The goal of iCOMOS is to examine the connections between science and one health policy implementation by (1) focusing on case studies and research that demonstrate the successful integration of human, animal, plant, and environmental health and social and behavioral sciences; (2) examining the science-policy connection by convening panels that include scientists, policy makers, and representatives from private industry; and (3) conducting forward-looking workshops in areas of research, collaboration, and policy formulation. iCOMOS-2014 was focused on 2 of the most important grand challenges of our time—food safety/security and emerging infectious diseases.^4,5

FOOD SECURITY: FEEDING THE WORLD NOW AND IN THE FUTURE

Good policy must be based on objective scientific studies that integrate epidemiology, ecology, microbiology, social science, and economics to balance the expectation of safe and nutritious food with the need for efficient and profitable production, and sustained environmental health. Given that an estimated 870 million people are currently suffering from malnutrition and that the combination of human population growth and consumer preference shifts associated with a rising global middle class are expected to exacerbate this problem, global production and delivery of food for protein, energy, and micronutrients must not just be maintained, it must be increased.⁶ In addition, existing land and water resources are already strained and their availability for agriculture will likely decrease, especially as the impacts of climate change shift traditional production regions. The obvious solution is to produce more efficiently, yet the very strategies that promote efficient production of food, such as concentrated farming systems, monoculture cropping, and chemical inputs of fertilizer, pesticides, and herbicides, have unintended consequences that threaten human, animal, and environmental health.

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Ensuring that sufficient food is not only safely and efficiently delivered to consumers but that it is produced in ways according to local preferences presents another paradox. Consumer demand for local and organic production systems actually increases the greenhouse gas footprint of most developed and many developing country food systems, depending on the crop or animal product^8–10 and also can increase food safety risks relative to today’s widely used production systems.¹¹ Those producers that remain local are often small in size, thus limiting benefits of scale, and many use organic methods, which can limit their ability to prevent disease through approaches such as constructing barriers and facilities for containment. The result is increased contact with wildlife, which increases opportunities for the transmission of infectious diseases to crops, livestock, and humans. For instance, interaction between domestic poultry and wild waterfowl reservoirs has resulted in the introduction of new IAV,¹² and the movement of H5 HPAI from domestic poultry to free-flying bird populations demonstrates that the exchange can be bidirectional,¹³ which changes paradigms of transboundary disease spread.

The interface between wildlife and agriculture will only increase as more land is converted for agricultural use to meet consumer demands, thus forcing wildlife into shrinking habitats or to adapt to increased contact with humans and livestock. Housing food animals inside helps to protect animal health, prevent cross-species disease transmission, and improve production efficiency, but it does not always meet consumer preference for local needs and resources. Nontherapeutic (nonclinical) antibiotic use in food animals is a tool that promotes production efficiency, but it has been associated with a rise in antibiotic resistance of human pathogens. However, epidemiological and ecological studies fail to support a causal link; instead, these studies indicate the spread of antibiotic resistance from humans to pigs and chickens.¹⁴ In the future, the World Food Summit global food strategy of “providing access for all people at all times to sufficient, safe, and nutritious food to maintain a healthy and active life” must be expanded to include considerations for environmental sustainability, animal welfare and non-nutritional aspects of public health.¹⁵ Progress toward these goals requires strong linkage of scientific knowledge and discovery that helps both to advance medical practice and health improvement as well as inform health policy development.

EMERGING INFECTIOUS DISEASES: EVOLVING PATHOGEN RISK IN A CHANGING WORLD

Human population expansion and exploration has increased as never before, and thus attention to the risk of disease emergence at the interface between humans, domesticated animals, and wildlife is increasingly important. While many human pathogens have wildlife reservoirs,¹ the converse is also an issue. Humans and their companion animals have triggered epidemic plagues of canine distemper in Serengeti lions¹⁶ and morbillivirus in Pacific seals¹⁷ while spreading influenza A to food animal species.¹⁸ Other dramatic changes include the explosive growth in global travel and trade patterns and legal and illegal trade in live animals, animal products, and wildlife as well as effects of climate change on all of the above. Retrospective and emerging analyses may provide insights into these systems. However, focusing on the processes and mechanisms that facilitate pathogen evolution and emergence will help us prepare for unpredictable new outbreaks, thus raising awareness of prevention and control policies that could reduce both the likelihood and magnitude of disease emergence and its resulting effects on animals and humans.

Single approaches to comprehend and anticipate disease emergence, especially using simplified disease models, are unlikely to produce informative insights involving environmental factors, multiple reservoirs, and complex human-animal-environment interactions.¹⁹ Concepts of wildlife reservoirs and spill-over/cross-species transmission into food animal and human populations followed by expansion and outbreak potential have been developed into mathematical models. Although not a predictor in itself, models of zoonotic transmission dynamics have made valuable contributions to inform public health recommendations for control of novel H1N1 influenza and SARS and are crucial for understanding pathogen transmission patterns and changes in disease epidemiology.²⁰

Human orthopoxvirus infection is a highly relevant example in which modeling based on rigorously collected data provides prevention strategies for a highly plausible emergent disease. The global human population is increasingly susceptible to smallpox due to the cessation of vaccination programs following eradication. Loss of crossreactive immunity has opened an ecological niche that can and has been replaced by related orthopoxviruses, including monkeypox in the Congo and novel orthopoxvirus in the country of Georgia.²¹ Emergence of new orthopoxvirus outbreaks with pandemic potential is possible as human-infectious poxviruses circulate in natural reservoirs. The recent discovery of viable smallpox in a US Food and Drug Administration refrigerator on the National Institutes of Health (NIH) campus recently reinvigorated the discussion of both susceptibility and/or risks from infections to smallpox.²² The specter of a new pandemic, fueled by relatively recent experience with the emergence of AIDS and new influenza viruses, has driven the US Centers for Disease Control and Prevention, the NIH-National Institute of Allergy and Infectious Diseases, the US Department of Agriculture, the US Agency for International Development, and others to develop programs focused on predictive modeling of and early detection and response to novel pathogens that have evolved under a complex set of pressures such as environmental pollution, land use changes, new trade patterns, climatic change, and other anthropogenic factors. The role of medicine in addressing individual and public health needs to be supported by rigorous science that empowers informed decision-making and development of useful policies in the face of unexpected disease threats.

The rapid growth and persistence of the ongoing outbreak of Ebola virus in West Africa presents an unfortunate but perfect opportunity for implementing science-based policy at the crossroads of emerging infectious disease ecology and sustainable food security. Experts hypothesize that Ebola virus entered the West African population through consumption of infected fruit bats, a plausible scenario given local food needs and practices.^23,24 The ongoing outbreak has stressed social organization and an already thin public health infrastructure to the breaking point in the affected countries. It threatens to exacerbate baseline food insecurity as disease control measures and fear shut down food and agriculture systems, further stressing local food security.²⁵ This situation makes for the “perfect storm” of grand challenges in the one health arena. Frighteningly, while more