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Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin: Workshop Summary
2
The Convergence of Forces Responsible for Zoonoses
Marguerite Pappaioanou, one of the co-chairs of the Committee, opened the meeting, by welcoming committee members, invited speakers, and other guests. The workshop participants were from Africa, Asia, Europe, Latin America, and the United States and brought a wide spectrum of expertise, experience, and background to the discussions. Pappaioanou reviewed the purpose of the workshop, which was to obtain information for the committee to consider in its deliberations in meeting the committee’s charge described in Chapter 1.
Sponsor representative Dennis Carroll of the U.S. Agency for International Development used the public and political responses to growing recognition of the potential threat posed by highly pathogenic avian influenza (HPAI) virus H5N1, which he described as “one part sensation and one part puzzlement,” to illustrate the issues surrounding surveillance. The sensation, he explained, was the looming specter of a pandemic and the puzzlement was “Is it really going to happen?” In response, he noted, the U.S. Congress has significantly increased its support for federal government efforts both to preempt a pandemic and to prepare for one.
Carroll explained that the public attention to H5N1 was important for two reasons. First, the risk is undeniable. This particular virus exists and is in circulation. It has the potential to mutate into a pathogen that can spread rapidly among humans and have a high fatality rate. The influenza epidemic of 1918 and other more recent epidemics illustrate the significant threat of diseases to human life and health. However, Carroll noted, the vastly increased mobility of today’s human population is one factor that
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Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin: Workshop Summary
could make an H5N1 epidemic a more sweeping public health emergency than the world has ever faced.
Second, and perhaps more important, is the fact that “H5N1 is a wakeup call.” The H5N1 threat raises questions of how the virus has had the opportunity to spread globally as quickly as it has, how novel this threat may be, and what potential exists for other zoonotic diseases to emerge in the same way. Carroll presented a list of infectious diseases and pathogens that have emerged since 1973, shown in Figure 2-1, to demonstrate the scope of the potential threat posed by zoonotic diseases.
These newly identified diseases have emerged primarily as a result of significant changes in human activity, including population growth, increased demand for animal protein, increased wealth and rapid travel by people and their animals, changes to the environment, and human encroachment on farm land and previously undisturbed wildlife habitats. Other pathogens could follow a similar pathway. Thus, Carroll explained, it is very important for policy makers to understand the kind of surveillance and action that will be needed to protect the public and the benefits they provide, and it is up to the scientific and public health community to make this case. He suggested that the current status of global surveillance systems
FIGURE 2-1 Infectious diseases and pathogens newly identified from 1973–2004.
SOURCE: Carroll (2008).
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in both human and animal populations and the strength of the veterinary health systems are insufficient to preempt a pandemic or to handle an emerging one. “What’s needed,” in his view, “is a new paradigm, a means for tapping expertise from all sectors, and thinking in a broadly preventive way, to reform animal husbandry and alter the ways people and industries interact with domestic animals and wildlife.” The interactions among many factors—from rapid mass transportation to increased consumption of animal protein to wilderness encroachment—have intensified the threat posed by zoonotic diseases. The global community involved with disease surveillance and coordination will be needed to confront this challenge.
HOW ZOONOSES DEVELOP
Tracee Treadwell of the Centers for Disease Control and Prevention (CDC) provided a detailed look at the interacting forces that lie behind the emergence of new zoonoses and the reemergence of existing ones. Not long ago, researchers thought infectious diseases were a problem of the past. Figure 2-2 shows that mortality rates from infectious disease in the
FIGURE 2-2 Infectious disease mortality rate in the United States, 1900–1996.
SOURCE: Armstrong et al. (1999). Reprinted with permission of JAMA.
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United States have declined dramatically since 1900. As recently as 1976, Treadwell noted, Lewis Thomas, then Dean of the Yale Medical School, remarked that there are “no new diseases to be discovered.”
Although the United States has not recently experienced anything approaching the sharp spike in the graph representing deaths caused by the influenza pandemic in 1918, a number of significant epidemics caused by other infectious diseases with the potential to spread globally have occurred in the past 15 years. Treadwell explained that most of the epidemics in the past 15 years listed in Table 2-1 were either zoonotic in origin or likely to be proven as such once ongoing research is complete.
This upsurge in the emergence of infectious diseases, as listed in Table 2-1, relates to noteworthy changes in the human population and human behaviors. As noted by Jones and colleagues (2008), many places around the world can be described as “hotspots” of emerging infectious disease. These include areas of high biodiversity and high human population density, which may be changing the human–animal–ecosystem interface with increasingly frequent and complex contact. Treadwell provided a detailed look at the interactions among humans, animal, and the environment—and the ways these interactions affect the development of pathogens—to set the context for discussion of how to prevent, monitor, and respond to developing diseases most effectively.
TABLE 2-1 Select Significant Outbreaks of Emerging Diseases (1993–2007)
Date
Disease/Pathogen (location or agricultural/food crop affected if specified)
2007
Progressive inflammatory neuropathy
2006
E. coli (spinach, lettuce)
2005
H5N1 influenza
2004
Marburg virus
2003
Severe Acute Respiratory Syndrome (SARS)
2002
Noroviruses
2001
Anthrax
2000
Rift Valley fever
1999
West Nile virus
1998
Nipah virus (Malaysia)
1997
H5N1 influenza (Hong Kong)
1996
BSE and new variant Creutzfeldt-Jakob disease (United Kingdom)
1995
Ebola virus (Zaire)
1994
Plague (India)
1993
Hantavirus
SOURCE: Treadwell (2008).
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HUMAN FACTORS
The human factors that influence the development of pathogens include genetic and biological factors; social, political, and economic factors; human health, behavior, and attitudes; and activities such as transport and trade. In each of these areas, the human population has changed dramatically in recent years. Perhaps the most obvious change has been the growth in human population. The world’s population was less than 3.5 billion in 1950, but reached approximately 6.5 billion in 2005 and is projected to top 11 billion by 2100 (Kern, 2008). As demographer Thomas Malthus predicted 200 years ago in his treatise An Essay on the Principle of Population, population expansion has presented significantly increased challenges in sustaining the food supply. The most significant challenges have included the increased consumption of animal protein and products, and the changing practices of animal husbandry and production. Figure 2-3 shows the increase in consumption in the developed and developing parts of the world since 1983.
In 2007, Treadwell observed, more than 21 billion animals were produced, and demand for animal protein is projected to grow by 50 percent by 2020. To meet this demand, agricultural businesses have developed new husbandry practices by increasing production of food animals (par-
FIGURE 2-3 World meat consumption projections from 1983–2017.
SOURCE: Created with data from Organisation for Economic Co-operation and Development/Food and Agriculture Organization of the United Nations (2008).
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ticularly poultry, swine, and cattle) and confining these large numbers of animals in concentrated animal feed operations, and resource-poor farmers are raising these animals on small crop-livestock farms1 that are typically land-constrained. Treadwell mentioned that there are approximately 800 million worldwide poor who own livestock; of those poor who are livestock keepers, more than 70 percent and 95 percent in Africa and Asia, respectively, depend on livestock for their livelihoods (Ayalew et al., 2005; Devendra et al., 2005). These farmers, Treadwell said, have few resources to vaccinate or protect their animals against parasites and other pathogens, creating a situation where large numbers of confined animals are more susceptible to disease. Demand for animal protein has also meant an increase in consumption of bushmeat,2 as well as illegal smuggling of bushmeat and other animal products. Large quantities of animal waste, high-density animal production, and increased interaction with infected bush animals have all played a role in the transmission of pathogens. Chapter 3 provides a detailed look at how this occurs with specific species.
Technological advances have also affected the development of pathogens. Treadwell noted that a billion people cross international borders every year—or 25 persons per second. They are also transporting goods, including meat and other food, on a vast scale, which means that animals and pathogens can travel farther and faster than ever before. Treadwell pointed out that the economic value of global trade in 2006 was $12 trillion, and that six million documented food shipments enter the United States every year, though only a fraction of those are inspected. Significantly more are probably imported illegally, she added.
The largest proportion of human population growth is taking place in the least developed countries, where poverty rates are the highest. As the human population has grown, it has also shifted to dwelling in urban areas. Treadwell reported that by 2030, 60 percent of the world’s population is expected to live in cities. By 2015 there will be 22 megacities (metropolitan areas characterized by extremely high density and populations of
1
Animals raised in a mixed crop-livestock system have multiple purposes including providing milk, meat, fiber, hides, manure for soil amendment, traction, and as a means of accumulating assets (Devendra et al., 2005).
2
“Bushmeat” is a term commonly used for meat of terrestrial wild animals, killed for subsistence or commercial purposes throughout the humid tropics of the Americas, Asia, Australia, and Africa. The types of wild animals hunted for meat affect a broad range of species (some endangered or threatened), including elephants, ungulates, apes and other primates, rodents, and birds. The Association of Zoos and Aquariums notes: “Bushmeat hunting and meat preparation may expose people to emerging infectious diseases, such as Ebola and SIV (simian immunodeficiency virus, which as been identified as the origin of HIV/AIDS). Bushmeat is a short-term ‘band-aid’ which cannot ultimately resolve the long-term plight driving it: lack of food security, scarcity of jobs, and growing human population pressures” (Eves et al., 2002).
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more than 10 million people) in the world, 17 of which will be located in developing countries. More than three billion people already live in urban areas (UNPD, 2007); and among urban dwellers in developing nations, 78 percent live in poverty. Urban slum dwellers in developing countries may have significant contact with both domestic and wild animals, and high concentrations of both people and animals provide prime conditions for the emergence of zoonoses.
ENVIRONMENTAL FACTORS
Pathogens are also affected by environmental changes, most of which are widely viewed as traceable to human activity. Changes in temperature and humidity patterns, drought and desertification, novel weather patterns, and other changes have affected the geographic ranges in which species can thrive and have altered lifecycles and microclimates.3 These changed patterns are expected to affect the prevalence, competency, distribution, and movements of vector-borne human and animal pathogens and their vectors (Harvell et al., 2002; Sutherst, 2004).
Treadwell spoke of how changes in climate and weather patterns can affect how people grow and harvest food, fiber, and fuel, as well as the habitats of both animals and humans. Both she and Carroll acknowledged that with pollution and the greater demand for natural resources, people and livestock are encroaching more and more on wild lands and into new environments that expose them to novel pathogens through increased exposure to previously isolated wildlife. The health of the animals may also be impacted by changes on the landscape through altered stress physiology, metabolism (directly through temperature changes, indirectly through diet changes), and inbreeding as populations decline or are isolated. As habitat loss and human encroachment continue, wildlife animals will need to change how they move to accommodate their new surroundings. For example, suburban sprawl disrupts the migration pathways and habitats of wildlife, so they must turn to backyards and parks—previously the animals’ habitat—for food. This leads to increased contact between humans and wildlife and greater opportunities for disease transmission.
Political unrest was also identified by Treadwell as being able to affect the environment as well as plant and animal life. She provided examples of war, complex humanitarian emergencies, disasters related to or exacerbated by the built environment (e.g., flooding associated with the breakage of a dam), or bioterrorism as all potentially having lasting impacts on the envi-
3
Data from the Intergovernmental Panel on Climate Change leave little room for doubt that the world is getting warmer (IPCC, 2007).
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ronment. Those changes can affect the types of plant food available in an area and, in turn, affecting the balance between predators and prey.
ANIMAL FACTORS
Finally, the growing human population, changes in human activity, and changes in the environment can affect animal health and behavior. Developed nations in particular have seen a considerable reduction in the availability of land for both domestic and wild animals. Animals may behave differently in changed habitats or as they adapt to a new geographic range. Their health and feeding preferences may be altered, and other factors may affect the balance within an ecosystem. Changes in animal population balances (for instance, predator/prey relationships or vector control mechanisms) can impact disease transmission risk, and an overabundance of some animals (such as deer in the United States) and underabundance of others (such as amphibian loss and mosquito control) both also impact disease risk. Animal health and reproductive capacity may be compromised by pollution exposure; animals may be exposed to new disease-causing agents as they move or come into contact with humans and other species; and animals’ acquired resistance to disease may be reduced by fast-paced changes in their environment.
CHALLENGES
“If you put all of these things together, what do you have? You have an absolute melting pot for disease emergence, reemergence, and persistence,” Treadwell explained. Figure 2-4 illustrates how these various developments interact to promote the emergence of new diseases, and the reemergence and persistence of existing ones.
These interactions provide ideal circumstances for pathogens that once affected only animals to evolve into agents that can cause primary infection in humans. Examples include rabies, transmitted through direct animal–human contact, and Ebola, which can cause limited outbreaks through animal–human contact and then human–human contact. The next evolutionary stage is to an agent that can cause a sustained outbreak via animal–human or human–human contact (e.g., Chagus or influenza A). Eventually, given the right circumstances, a pathogen may develop into an agent transmitted only among humans (e.g., HIV). These stages are illustrated in Figure 2-5. This picture of pathogen development illustrates the changing and complicated interactions among animals and humans as the critical factor in the evolution of pathogens.
The challenge for controlling emerging diseases with such complex etiology is that no single agency has either the mandate or the capacity
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FIGURE 2-4 Human–animal–ecosystem domain interface.
SOURCE: Treadwell (2008).
to address the entire landscape of zoonotic disease, Treadwell explained. Globally, the World Health Organization (WHO), the World Organization for Animal Health (OIE4), and the Food and Agriculture Organization of the United Nations (FAO) each play a role, and have been working to better coordinate their activities. Within the United States, the responsibility is spread across many government departments and programs, each with its own focus and interests. Table 2-2 highlights the principal focus of the seven U.S. government agencies that play a role in zoonotic disease control.
The Centers for Epidemiology and Animal Health at the U.S. Department of Agriculture (USDA) Animal and Plant Health Inspection Service are mandated to provide timely information and technical services on foreign animal diseases and agriculturally related animal diseases. While not explicitly mandated, their work and the work of many other agencies listed in Table 2-2 crosses over into the realm of zoonotic diseases. Treadwell said the National Center for Zoonotic, Vector-borne, and Enteric Diseases at CDC has been working closely with colleagues across various agencies (as listed in Table 2-2) that are concerned about controlling zoonotic diseases.
4
Office International des Epizooties, commonly known as the World Organization for Animal Health.
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FIGURE 2-5 Five stages through which pathogens of animals evolve to cause diseases confined to humans.
SOURCE: Wolfe et al. (2007). Reprinted with permission of Nature.
Another CDC effort, called BioPHusion, analyzes data such as numbers of hospital visits and reports of related conditions in order to develop policies and procedures targeted to specific risks. MicrobeNet, another CDC resource, is a curated, non-redundant sequence reference database that provides both phenotypic and genotypic information on an expanding number of ribosomal gene sequences.
These examples are just a few of the efforts to improve disease prevention and surveillance to emerging pathogens, more of which are discussed in Chapters 3 and 4. But Treadwell enumerated some challenges that face policy makers, researchers, and others concerned about preventing and responding to emerging zoonoses. The challenges include:
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TABLE 2-2 U.S. Government Agencies Concerned with Zoonotic Disease Control
Agency
Focal Orientation
Agency for International Development (Department of State)
International development—increasing involvement in improving capacity to detect and respond to zoonoses, primarily avian influenza
Department of Agriculture
Animal health—focus on economic threat to U.S. agriculture and quality of animal therapies
Department of Commerce
Marine mammals—protecting, conserving, and managing marine species
Department of Defense
Force protection—general health threat to soldiers (potential bioweapon threat)
Department of Health and Human Services
Human health—minimization/mitigation of public health threat of zoonoses
Department of Homeland Security
Bioterrorism—preventing/controlling access to potential biothreats
Department of the Interior
Wildlife—protecting wildlife populations and inspecting wildlife shipments imported to the United States
SOURCES: NRC (2005); Treadwell (2008).
The roles that governments, educational institutions, and the private sector should play are not entirely clear, which leaves the possibility of gaps and overlaps.
The health of humans, animals, and the environment all exist on a continuum, so integrated strategies are needed that consider each factor.
Tremendous health disparities exist among human (and animal) populations, which present pressing moral and ethical concerns that need to be addressed.
Because these diseases can show up in diverse communities, diverse tools and strategies are needed to detect and respond effectively to future diseases.
The potential impact of an outbreak could be unprecedented; and thus call for an unprecedented response. The impact could go far beyond tragic health outcomes and have profound effects on economies.
Treadwell closed with the observation that the factors that allow for a microbial storm are already well entrenched. Consequently, the biggest challenge may be for those in a position to understand the risk to effectively promote a “one world–one health”™ way of thinking, which will provide
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the grounding for necessary shifts in habitual or traditional ways of thinking and acting.5
Participants in a panel discussion were asked to consider the existing configuration of institutions concerned with zoonotic disease, and how those institutions and their relationships might need to change. They offered a variety of observations on the situation Treadwell had described. Committee co-chair Gerald Keusch opened the discussion with the observation that although a global surveillance system is the critical goal, international health organizations “do not exist in a vacuum” and they must interact with other institutions in the public and private sectors—at the national and international levels—as well as the academic community. They are critical components of a civil society, but the committee wants to consider carefully whether the current configuration of institutions is the most effective one for addressing the problem of zoonotic diseases.
Discussant Nancy Cox offered lessons that CDC had learned from HPAI. She noted that recent outbreaks had provided examples of effective reporting, but that follow-up investigation—of how many infections have actually occurred, for example—was less effective. CDC received funding to implement systematic surveillance, she explained, which enabled the agency to more fully view the complexity of the undertaking. Not only did CDC have to navigate relationships with the USDA, the livestock industry, and veterinarians at the state level and in diagnostic laboratories, but CDC also found a need to develop specific standard operating procedures to ensure that all concerned would have the opportunity to prepare and respond, but that the public would not be needlessly frightened away from perfectly safe activities.
The tracing of H5N1 and Severe Acute Respiratory Syndrome (SARS) viruses also illustrates the kinds of mechanisms that are most effective. In Vietnam, Cox explained, close cooperation between the human and animal health sectors made it possible to trace bird viruses and follow the pathway of disease spread. Much of the work was made possible by genetic research indicating that the source of the viruses was in southern China.
One vital component in cooperation is transparency, Cox said. Because viruses do not recognize political borders, sharing information about infections and measures to control them—such as culling large numbers of birds, or addressing entrenched cultural practices that increase risks including the
5
The American Veterinary Medical Association defines the term “one world–one health™” as “the collaborative efforts of multiple disciplines working locally, nationally, and globally to attain optimal health for people, animals, and our environment” (AVMA, 2008). The concept was first proposed by veterinary epidemiologist and parasitologist Dr. Calvin W. Schwabe, who used the term “one medicine” in the 1960s to capture the vital importance of considering medical and veterinary issues jointly in the study of zoonotic diseases (Schwabe, 1984; Kahn et al., 2008). “One world–one health” is a trademark of the Wildlife Conservation Society.
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preference to purchase live poultry—are absolutely necessary to identify and control emerging viruses. She noted that this transparency is critical because H5N1 is only the best known of many potentially lethal avian influenza viruses. The challenge in developing the partnerships that make transparency possible is “finding the resources to do the things that we all know need to be done,” Cox said.
Stéphane de La Rocque of FAO echoed the importance of the one world–one health™ approach, noting that FAO responded to high-profile diseases such as SARS, West Nile virus, and Rift Valley fever by actively collaborating with multiple government agencies and others. Nevertheless, those who run surveillance systems are always trying to catch up with new manifestations that need to be tracked. “For many diseases, you will see no clinical sign in animals if you do not have your active surveillance system, if you don’t go in the field, if you don’t go to sample, or if you don’t have a good diagnostic chain,” he explained. He believes the answer is strong support for sustainable surveillance, including diagnostic capacity. The challenge is what he described as an “erosion of expertise.” In many cases, as new or reemerging diseases appear—such as Bluetongue that is reemerging in Europe via a new vector—not enough researchers with relevant expertise are available where and when they are needed to identify the ecology of the disease and to work in the field.
This point was reinforced by Marlo Libel, of WHO’s Pan American Health Organization (PAHO), who explained that a key challenge for the organization has been to work with individual countries to identify and characterize risks in order to mobilize the necessary resources. Libel noted that cooperation has increased among the health services in Latin American countries, but added that changes in ecosystems have created new high-risk areas that favor the development of new pathogens and the reemergence of existing ones, such as yellow fever. Surveillance that can detect epizootic diseases (epidemics in animal populations) in domestic and wildlife populations early on is critical to protecting the human population, he asserted.
In Latin America, Libel observed, more laboratories need the appropriate quality control and biosafety capabilities to deal with samples safely and to test them quickly. Furthermore, he sees a need for more standard operating procedures for communicating and coordinating among the research centers, universities, and other institutions. WHO, through PAHO, is working with institutions in this region to build capacity for the necessary risk assessment, he said, but improving communication about the risks requires engaging in the political contexts involved, and making sure that decision makers have evidence-based information they need to make assessments and provide resources. An additional policy challenge, which has been a focus for FAO, OIE, and WHO, is to fine-tune the balance of investments in the surveillance and early warning systems with those required to make
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sure countries and institutions can respond adequately to the risks those systems identify.
Alejandro Thiermann of OIE also focused on the sustainability of surveillance systems. He noted that OIE was founded in the 1920s to collect and share information on animal health in order to prevent disease dissemination and to promote trade. That goal remains the mission of the organization’s 172 member nations, but Thiermann reminded the group that each nation has unique circumstances and pressures, as well as different veterinary infrastructures. Moreover, many of the problems under discussion are perhaps likeliest to develop in areas of the world with the weakest veterinary infrastructures. Thus the immediate challenge is for the world to support disease monitoring in those areas that need it, while the longer term challenge is to develop greater political will to support a truly global approach to surveillance. Many of these issues were raised again in subsequent discussions.