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National Research Council (US) Committee on Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin; Keusch GT, Pappaioanou M, Gonzalez MC, et al., editors. Sustaining Global Surveillance and Response to Emerging Zoonotic Diseases. Washington (DC): National Academies Press (US); 2009.

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Sustaining Global Surveillance and Response to Emerging Zoonotic Diseases.

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3Drivers of Zoonotic Diseases

“A transcendent moment nears upon the world for a microbial perfect storm. Unlike the meteorological perfect storm—happening just once in a century—the microbial perfect storm will be a recurrent event. The two events share a common feature; a combination of factors is the driving force behind each.”

—Microbial Threats to Health: Emergence, Detection, and Response

(Institute of Medicine, 2003)

Zoonotic disease emergence is a complex process. A series of external factors, or drivers, provide conditions that allow for a select pathogen to expand and adapt to a new niche. The drivers for the most part are ecological, political, economic, and social forces operating at local, national, regional, and global levels. Regions where these factors are most densely aggregated, most highly prevalent, and where risk of a disease event are most intense can be considered zoonotic disease “hotspots.” In this chapter, the committee reviews many of the drivers underlying this process of disease emergence and reemergence. Though not an exhaustive review, it reveals the multiplicity and the complexity of their inter-relationships.

OVERVIEW OF ZOONOTIC DISEASE EMERGENCE AND REEMERGENCE

Zoonotic disease emergence often occurs in stages, with an initial series of spillover events, followed by repeated small outbreaks in people, and then pathogen adaptation for human-to-human transmission. Each stage might have a different driver, and therefore a different control measure. As mentioned in Chapter 2, human immunodeficiency virus-1 (HIV-1) emerged from chimpanzees in Africa, spilling over to humans repeatedly before its global spread (Hahn et al., 2000). This initial phase of emergence was driven by bushmeat hunting and was the primary driver of its emergence. A second phase of emergence was driven by increased urbanization and road expansion in Central Africa beginning in the 1950s, and dispersal of index cases harboring prototype HIV-1 infections that were transmissible from person to person. The virus then entered the rapidly expanding global air travel network and became pandemic, with its emergence in North America, Europe, and Asia, accelerated by changes in sexual behavior, drug use, trade in blood derivatives, and population mobility.

Nipah virus is another example of a recently discovered paramyxovirus with fruit bat reservoir hosts. It caused a large-scale outbreak in Malaysian pig farmers in 1998. It is a growing threat due to its broad host range, wide geographical distribution, high case fatality, reports of human-to-human transmission, and the lack of vaccines or effective therapies (CDC, 1999; Eaton et al., 2006; Gurley et al., 2007). A recent analysis of food-animal production data from the index site—a commercial pig farm in Malaysia—before and during the outbreak shows that the emergence was likely caused by repeated introduction of Nipah virus from the wildlife reservoir into an intensively managed, commercial pig population site planted with mango trees (Daszak et al., 2006). This repeated introduction led to changes in infection dynamics in the pigs and a long-term, within-farm persistence of virus that would otherwise have died out. This causative mechanism has been previously proposed as a driver of highly pathogenic avian influenza (HPAI) H5N1 dynamics in poultry and the emergence of other pathogens (Pulliam et al., 2007).

An overview of how certain factors lead to disease emergence and reemergence is outlined in Figure 3-1. There is currently a great deal of interest in studying the underlying drivers of emerging diseases, from the proximal to the primary, to better target control programs.

FIGURE 3-1. Overview of the driver-pathogen interactions that contribute to the emergence of infectious zoonotic diseases.

FIGURE 3-1

Overview of the driver-pathogen interactions that contribute to the emergence of infectious zoonotic diseases. SOURCE: Treadwell (2008).

THE HUMAN–ANIMAL–ENVIRONMENT INTERFACE

Historical Perspective on the Human–Animal Interface

The hunter-gatherer lifestyle supported early human societies for millennia, and this lifestyle could support an estimated 4 million people worldwide. About 10,000 years ago, hunter-gatherers began to settle, planting crops and husbanding wild animals to the point of domestication. This pattern continued more or less uninterrupted until the end of the 17th century when Thomas Malthus wrote in An Essay on the Principle of Population that human growth would soon outstrip the ability of the world to feed it. Fortunately, Malthusian predictions proved untrue, largely because of the change in agricultural systems from extensive to intensive. This change was accelerated by the growth of large urban centers and the invention of the railway, allowing food to move more freely from the farm to the table. The “Green Revolution”1 further increased crop yields and the separation of humans from the source of their food.

Since the 1960s, the production of food animals has grown phenomenally. Global milk production has doubled, meat production has tripled, and egg production has increased four-fold. Part of this is due to greater numbers of animals. However, genetic enhancement has also played a role, leading to higher overall production per animal.

Current Trends in Animal Protein Production

World demand for animal protein is increasing, and projections for consumption are staggering. Between 2000 and 2030, global meat production is expected to increase by approximately 2 percent per annum until 2015 and then slightly more than 1 percent per annum until 2030 (Steinfeld, 2004). Most of this demand is expected to come from the developing world, where rapid population expansion and higher per-capita incomes will drive people to change from a diet of rice, beans, and corn to one that incorporates more animal protein, a phenomenon known as the “nutrition transition” (Delgado, 2003). How will this demand be met? Most recent growth in intensive agriculture and projected growth for the next 30 years is mostly in the developing world, where intensive food-animal production facilities are being set up. These facilities are almost entirely based on feed grain, and in Asia, feed grain is imported from other parts of the world (see discussion later in this chapter on Global Food Systems and Food Safety). These collective changes in agricultural production and distribution, referred to as the “Livestock Revolution,” are driven by globalization and the developing world’s emerging middle class. The Livestock Revolution is characterized by vertical integration, the introduction of large supermarkets in developing countries, regional concentrations of animals, and a move to locate production facilities geographically at the farthest reaches permitted by regulations (Steinfeld, 2004).

Fueled by a growing population, rising incomes, and related urbanization, the consumption of meat and milk in the developing world grew slightly more than 3 and 2 percent per year, respectively, from 1992 to 2002.2 Growth was particularly strong in China, where over that same period meat and milk consumption grew by nearly 6 and 8 percent per year, respectively. Most of the growth occurred in poultry and swine; beef consumption grew at a much lower rate (see Figure 3-2). In contrast, percapita total meat consumption in the developed world remained practically static in the same period, although there has been a slight shift from beef to chicken.

FIGURE 3-2. Projected production of animal meat by species, 1961–2025.

FIGURE 3-2

Projected production of animal meat by species, 1961–2025. SOURCE: Newcomb (2004). Reprinted with permission from Bio Economic Research Associates, LLC (bio-era™). All rights reserved

This strong expansion and resulting concentration of meat and milk production in the developing world has consequences for global human and animal health, which is explored in more detail later in this chapter. The shift of production to the developing world transfers the industry to a region with generally weak public services and regulatory oversight mechanisms, which were unprepared for fast growth and major structural changes.

Intensified food-animal production has epidemiological consequences (see Box 3-1). Natural herds often have a low rate of reproduction and production. Humans have domesticated animals to ensure a more regular, safer, and convenient food supply. The objective of husbandry is to reach a natural balance between the host and its parasites while promoting efficient and economical production. Any increase in production must be matched with a refinement of management and disease control strategies. Although the factors listed under a “man-made ecosystem” (Box 3-1) are caused by influences of human intervention, their adjustments or maintenance are not necessarily under human control, and could lead to higher levels of disease risk. But at the same time, the level of risk could be reduced through more intensively managed and maintained factors with respect to animal health and well-being.

Box Icon

BOX 3-1

Epidemiological Factors Comparing Natural and Man-made Ecosystems.

DRIVERS INFLUENCING EMERGING AND REEMERGING ZOONOSES

Human Population Growth and Distribution

Global Population Growth

The second half of the 20th century was a time of unprecedented population growth. According to United Nations (UN) estimates and forecasts, the world population more than doubled from an estimated 2.5 billion in 1950 to more than 6.5 billion in 2005 (see Figure 3-3), an annual average growth rate of 1.72 percent (United Nations, 2007). Although growth rates peaked in the late 1960s at slightly more than 2 percent and had declined to slightly more than 1 percent in the first 5 years of the 21st century, annual population increments continued to increase in the late 1980s and were projected to peak at about 8 billion by 2050. The UN’s medium variant forecast, based on the assumption of continued fertility declines in low-income countries, shows the world population continuing to increase to slightly more than 9 billion by 2050.

FIGURE 3-3. World population projections, median variant forecasts.

FIGURE 3-3

World population projections, median variant forecasts. SOURCE: United Nations (2007). Reprinted with permission from the Population Reference Bureau.

Population growth has been unevenly distributed around the globe and is expected to become even more so in the next few decades. The developed countries—essentially Europe, North America, Australia, Japan, and New Zealand—represented nearly a third of the total growth in 1950, a proportion that had declined to less than 19 percent by 2005 (see Figure 3-3). Sub-Saharan Africa has shown the highest growth rates, averaging nearly 3 percent per annum in the late 1980s. The bulk of the absolute population increments have occurred in Asia, with annual increases reaching 57 million around 1985, declining only to slightly less than 50 million by 2005. More than half of these annual increases are now accounted for by South Central Asia, predominantly India, Pakistan, and Bangladesh. The bulk of future population growth is expected to occur in developing countries. The share of world population of the developed countries is forecast to decline to less than 14 percent by 2050, while sub-Saharan Africa is forecast to increase to nearly 20 percent. By 2050, of the global annual increment of 37 million, 22 million will occur in sub-Saharan Africa, whose population will still be increasing by more than 1 percent per annum, and 12 million will occur in South Central Asia (United Nations, 2007).

Population Mobility

Once a zoonotic disease has emerged, its spread in the human population is likely to be facilitated by population movements. Migration, also called long-term population resettlement, is likely to spread diseases that have a long period of latency or duration of infectiousness, whereas short-term mobility for periods of days or weeks, typical of “travel” patterns, may rapidly spread diseases with short resolution periods. The latter is illustrated by the spread of severe acute respiratory syndrome (SARS) from Hong Kong to Toronto within weeks in spring 2003, and the spread of the influenza A(H1N1) virus from Mexico to New York in April 2009.

Measurement of both intra- and international migration is poor, with most estimates coming from census data on birthplace. The global count of foreign-born persons now living in a different country has increased moderately, from about 75 million in 1965 to about 175 million in 2000 (United Nations, 2002). This growth is somewhat misleading, however, because a portion of the increase resulted from the break-up of the Soviet Union. About half of the world’s international migrants have moved between developing countries. As of 1990, the United Nations (2002) estimated that about 13 percent of international migrants were living in Africa, 36 percent in Asia, 21 percent in Europe, 20 percent in North America, 6 percent in Latin America, and 4 percent in Oceania.

Population displacements as a result of conflict or natural disaster are likely to create conditions of crowding and poor sanitation that are highly conducive to the spread of infectious diseases. As of 2007, the Office of the United Nations High Commissioner for Refugees reported a total of 16 million refugees, under its or the United Nations Relief and Works Agency mandates, 26 million persons reported internally displaced as a result of conflict, and 25 million reported internally displaced as a result of natural disasters (UNHCR, 2009). Given the caveat that definitions and data collection procedures have varied over time, the numbers of refugees and internally displaced persons have not changed dramatically over several decades.

Human travel associated with tourism, business, and other moves not associated with changing residence have increased rapidly over the past 50 years and are projected to continue to increase. As shown in Figure 3-4, the revenue passenger kilometers represent the total number of passengers traveling globally multiplied by the number of kilometers they commercially fly, illustrating the increasing number of people and goods that are traveling farther and faster around the globe.

FIGURE 3-4. Volume of global air traffic, 1985–2001, and projection of future trends, 2001–2021.

FIGURE 3-4

Volume of global air traffic, 1985–2001, and projection of future trends, 2001–2021. SOURCE: Adapted from Daszak and Cunningham (2003).

Human movement has significant implications for human and animal health. Not only are travelers (tourists, businesspeople, and other workers) at risk of contracting communicable diseases when visiting tropical countries, but they also can act as vectors for delivering infectious diseases to a different region or potentially around the world, as in the case of SARS. Refugees have become impoverished and more exposed to a wide range of health risks because of their status (Toole and Waldman, 1997), and their populations have been reported to harbor hepatitis B, tuberculosis, and various parasitic diseases (Loutan et al., 1997). Immigrants may come from nations where infectious diseases such as tuberculosis and malaria are endemic, and refugees may come from situations where crowding and malnutrition create ideal conditions for the spread of diseases such as cholera, shigellosis, malaria, and measles (CDC, 1998).

Urbanization

Populations in urban areas are typically less exposed to animal contact than rural populations, depending on the market structures and production systems of live food animals, but urbanites may also live in more crowded conditions conducive to disease transmission. The increase of global population over the past 50 years has been roughly paralleled by an increase in the level of urbanization. In 2005, the world’s population was nearly 50 percent urbanized, a figure forecast to rise to nearly 70 percent by 2050 (United Nations, 2008). Developing countries as a whole, and South Central Asia and sub-Saharan Africa in particular, are somewhat less urbanized than the global average, though the differences have narrowed over time. By contrast, in all regions except sub-Saharan Africa, the rural population is forecast to be declining by 2050, and has probably been declining since the early 1990s in Latin America. Of course, cities grow in part by encroaching on surrounding farmland. The combination of reduced population increments and declining rural populations is likely to increase pressures on land resources in the future.

Human Behavior and Cultural Factors

Researchers have identified several social and cultural factors as drivers of emerging zoonotic diseases (Mayer, 2000; Patz et al., 2000; Daszak et al., 2001; Macpherson, 2005). Changing demographics and unprecedented population movement, as well as increased global flow of people, goods, food-animals, food products, and domestic and wild animals, all affect “microbial traffic” and emerging viral, bacterial, and parasitic zoonoses (Morse, 1993; Mayer, 2000). Social changes resulting in altered land and water-use patterns, intensified agricultural practices, deforestation and reforestation, and human and domestic animal encroachment on wildlife habitats also affect the movement of pathogens. These factors contribute to cross-species pathogen transmission and the emergence of new epidemic diseases that affect humans and animals, including the transmission of zoonotic diseases to humans and the anthropogenic movement of pathogens into new geographic spaces affecting the health of wildlife (Daszak et al., 2001).

Natural and Built Environments

The built environment—environments made, modified, and used by humans—is characterized by a sense of cultural aesthetics that influences how buildings, gardens, ponds, and parks are constructed. Environments are modified not only for aesthetic reasons, but also for utilitarian needs to provide a larger, general population with access to a public good or utility, such as dams for hydroelectric power or canal-building for transportation. Built environments have provided breeding sites for disease vectors such as Aedes aegypti, the mosquito which transmits dengue fever.

Culture, society, and religion influence the kinds of foods people eat, how foods are prepared, and the demand for foods at particular times (Shanklin, 1985). For example, each year 2–4 million Muslims from more than 140 countries make the pilgrimage to Mecca in Saudi Arabia for the Hajj or for Umrah (year-long lesser religious rites). During the religious festivals of Eid al-Adha,3 up to 10–15 million small ruminants or 64 percent of the global trade of live sheep (Shimshony and Economides, 2006) are ritually slaughtered in various countries, including Saudi Arabia where Mecca is located, but even outside urban areas such as Washington, DC, to feed an estimated 12–15 million people. Most of these animals are shipped alive to the Arabian peninsula from countries across the Red Sea in East Africa and the Horn of Africa, where diseases that affect both humans and animals, such as the mosquito-borne disease Rift Valley fever (RVF), are endemic (Ahmed et al., 2006; Davies, 2006). Because animals are dispatched rapidly to preserve their value and the incubation period of diseases such as RVF is days longer than the transport time, conditions are ripe for disease spread. In 2000–2001, RVF was reported in Saudi Arabia (CDC, 2000) and has the potential to become an epidemic if not carefully monitored. Challenges to disease surveillance include not only heavy human and animal traffic and crowded conditions in ports and pilgrimage sites, but also political instability in the region and lack of cooperation among countries, which undermines the reporting of sick animals.

Food Preferences

Taste is a cultural phenomenon that influences food preparation and is also a driver of zoonotic disease transmission and infection. Globalization has also fostered the taste for foods from other cultures that contain raw meat or fish (e.g., sushi), and this can facilitate a number of parasitic zoonoses (Macpherson, 2005). In both Indonesia and China, a preference for the consumption of freshly slaughtered local chicken draws people to “wet markets” that vend live poultry (as well as other animals) for slaughter either onsite or at the buyer’s home (Liu, 2008; Padmawati and Nichter, 2008). Local chickens in Indonesia are considered better tasting, resistant to disease, and strength-enhancing when consumed. Local chickens also fetch a higher price in the market and are trucked to major cities from the countryside to meet demand (Diwyanto and Iskandar, 1999). This practice puts consumers in contact with live fowl and freshly killed wild animals (primates, reptiles, bats, etc.) as well as domesticated animals (e.g., dogs, civets, pigs) and their feces, which may be infected with pathogens and contribute to the transmission of zoonotic diseases such as SARS and HPAI H5N1. Consumer preference for fresh products of wet markets is a complicating factor for health authorities that are trying to reduce health risks.

Bushmeat consumption, especially of primates, has been tied to zoonotic diseases such as HIV and Ebola (Peeters et al., 2002; Chapman et al., 2005; Daszak, 2006). Bushmeat may either be consumed as an inexpensive source of protein or as a sought-after delicacy, according to cultural value related to taste, wealth, and cultural significance. Bushmeat has cultural significance in not only religious rites, which increase demand for meat (Adeola, 1992), but also ethnic identity, nostalgia, and social memory (Holtzman, 2006). The demand for bushmeat is driven by cultural factors as well as wild game availability, poverty, food insecurity,4 and an increased demand for protein. Increases in household wealth, however, appear to shift preference from bushmeat to the meat of domesticated animals (Schmink and Wood, 1992; Stearman and Redford, 1995) or narrow the range of bushmeat species consumed (Hames, 1991; Layton et al., 1991).

Most bushmeat is not taken in a simple subsistence manner, that is, directly from the forest to the table. An estimated 90 percent of all bushmeat consumed moves through a distinct and well-organized market chain, with numerous nodes along the supply chain where the meat changes hands multiple times between the animal’s death and its presence on the dinner table (de Merode and Colishaw, 2006). The exchangers in this process include, among others, hunters, porters, bicycle traders, wholesalers, market-stall owners, and food preparers. Each person handling the meat or carcasses is exposed to the normal flora as well as any pathogens present. Additional sources of infection include the remnants and wastes from the carcasses, which could be scavenged and taken to even more new hosts.

Repeated transmission of viruses to humans, most of which do not result in human-to-human transmission, is termed “viral chatter” (Wolfe et al., 2005). For example, simian foamy viruses are known to infect bushmeat hunters regularly, but to date there has been no evidence of human-to-human transmission (Wolfe et al., 2004). More bushmeat means more viral chatter, which will increase the incidence of human infections, increase the number of pathogens that may infect humans, and increase the probability of eventual human-to-human transmission of one of these agents. As food insecurity increases, the bushmeat market becomes more essential and more lucrative, creating more opportunities for transmission of pathogens to humans.

The consumption of wild-animal products is also driven by cultural dietetic practices related to health promotion and disease treatment, known as zootherapeutics. Animal products are deemed to have medicinal value, and when consumed, play an important role in ethnomedical systems to increase strength as well as enhance virility (Afolayan and Yakubu, 2009) or to treat illness in humans and domestic animals (Martin et al., 2001; Mathias and McCorkle, 2004; Kakati et al., 2006; Mahawar and Jaroli, 2008; Soewu, 2008).

Companion Animals

The popularity of companion animals is a cultural phenomenon subject to social and economic contingencies. These include animals kept for display as well as animals for which humans develop a special relationship that extends beyond the animals’ value for work, substance, or sale. For example, despite the risk of HPAI H5N1, backyard chickens are allowed in the kitchen and treated as companion animals by some Indonesians the same way an American might care for a dog or cat. Fighting cocks are groomed and handled daily by their owners who express considerable affection for them. Primates are kept as pets in parts of the Cameroon where high rates of simian immunodeficiency virus have been recorded (Peeters et al., 2002). Pastoralists in Africa and Hindus in India have special relationships with cattle that extend beyond their monetary or exchange value. Dogs and cats are the most popular companion animals (found in 63 percent of American homes) and are at once associated with positive health benefits ranging from physical health (e.g., lower blood pressure and cholesterol, increased exercise) to mental health (e.g., improved psychological coping with stress, decreased psychotropic medication use among the elderly). At the same time pet ownership increases the chances of zoonotic infection from several different types of diseases (e.g., salmonellosis and Giardia, Cryptosporidium and toxoplasmosis, rabies). The transnational trade in exotic animals from birds to nontraditional companion animals (e.g., prairie dogs that carry monkeypox in the United States) is growing and creating new challenges for both human and animal health professionals and demands their closer collaboration (Pickering et al., 2008).

Global Food Systems and Food Safety

The livestock production system,5 farm and market structure, and farm geography are major variables that define the emergence and consecutive spread of a zoonotic disease.

Production Systems

Seré and Steinfeld (1996), who prepared the standard work on livestock production systems, distinguished two groups of farming systems. The first are the pure animal production systems, in which less than 10 percent of the total value of outputs comes from non-livestock farming activities, can be further differentiated into pure grassland-based systems and landless (or industrial) systems, which buy at least 90 percent of their feed from other enterprises. The second are the mixed farming systems, where livestock farming is associated with cropping. Globally, the mixed farming system is the most important producer of beef and milk. The production of pork is about equally distributed over mixed and industrial systems, whereas the industrial system is the dominant origin of poultry meat. The future will probably see a stagnation of the grazing system, a slight decrease in the mixed farming system, and a continuation of the strong increase in industrial swine and poultry production units (Steinfeld et al., 2006).

Farm and Marketing Structure

Projections suggest that farm size will increase in about one-half of the world, and shrink in the other. Economies of scale in production, and in particular in meeting stricter food safety and environmental standards and the low, marginal returns to labor in the food-animal production sector, will drive the process of the increase in size and scale in the industrialized world. For example, in the United States, the share of the value of pork production from farms with sales of $500,000 increased from 14 percent in 1989 to 64 percent in 2002, and for poultry meat, from 40 to 68 percent over the same period (McDonald et al., 2006). On the other hand, in most developing countries, population pressure has led to an increase in the number of farm holdings and a subsequent decrease in farm size. For example, in India, the number of farm holdings increased from 70 million in 1970–1971 to nearly 98 million in 1985–1986. Farm holdings further increased to approximately 105 million in 1990–1991, with a major shift to landless and marginal farm holdings (AERC, 2005).

Balance of Food Production and Its Ecological Impacts

Livestock production is strongly linked to land. Livestock production uses nearly 4 billion, generally intensively managed hectares (ha) of land, of which 0.5 billion are for feed crops such as corn and soya (33 percent of the total cropland); slightly more than 1 billion are for pasture with relatively high productivity, and the remaining 2 billion ha are extensive pastures with relatively low productivity (Steinfeld et al., 2006). Expansion of demand for food-animal products can be met by intensifying land use, increasing the yield per unit area, or expanding the area under feed crops or grassland. Until the 1960s, increasing the livestock population and expanding the area under feed and fodder crops have been the main trends. As a result, the conversion of natural habitats to pastures and crop land has been rapidly growing. More land has been converted for the growing of crops between 1950 and 1980 than in the preceding 150 years (MEA, 2005). There are major regional differences, however, with continuing strong crop-land area expansion in Asia and Latin America, but a reduction of agricultural landuse in North America and Europe. These trends are expected to continue, with a stronger accelerating conversion of natural habitat into crop land in sub-Saharan Africa (Steinfeld et al., 2006).

Recent trends show a tendency toward intensification, with higher yields per area of feed crops and per animal, and lower feed inputs per unit of production. For example, global corn yields increased from 31,542 hectograms (hg) per ha in 1980 to 50,102 hg per ha in 2005 (FAO, 2009b), and the amount of feed required to produce 1 kilogram (kg) of poultry meat decreased in the United States from 1.92 kg in 1957 to 1.62 kg in 2001 (Havenstein et al., 2003). This increase in productivity has been achieved through a greater use of capital and technology, mainly through purchased goods (e.g., feed and pharmaceutical inputs) and services (e.g., animal health and expert advice).

Parallel Evolution of Marketing Systems and Production Geography

Production and marketing systems develop to supply demand for animal products most efficiently while reducing production and delivery costs. The marketing system differs depending on the pattern of food-animal production. In relatively simple production systems, distances to markets are short, and most products are marketed on foot or fresh in wet markets. Unsold stock or products, after having been in contact with live or fresh material from other origins, are often taken outside the market, thus increasing the chance of disease spread. As economic development progresses further, and distances between producer and consumer lengthen, supermarket chains with more stringent standards emerge. Their share in total sales is rapidly increasing, in particular in East Asia and Latin America (Reardon et al., 2003).

These trends have major implications for the emergence of zoonotic diseases. In countries where consumption and production grow most, which cover a large part of the developing world, there is still a high density of smallholders, together with an emerging, often poor biosecure industrial sector. This was described as a high-risk situation in the emergence of HPAI H5N1 (Slingenbergh et al., 2004). Moreover, the concentration of the larger industrial operations around the urban centers results in major environmental pressures on soil and water. This presents another set of conditions favorable for the emergence of new zoonotic pathogens, although if they are professionally managed and adopt highly integrated production compartments with strict biosecurity measures, they actually reduce the animal-human interface and can reduce the disease pressure. Finally, these risks are further exacerbated by the open market system.

The Case of Poultry Production in Southeast Asia

Smallholder poultry keeping, also known as “backyard poultry,” has been advocated for decades by the Food and Agriculture Organization of the United Nations as a strategy for poverty reduction. The greatest density of poultry is in East and Southeast Asia (see Figure 3-5). Along with wet market supply of fresh poultry, there has been an increasing urbanization of smallholder poultry keeping. As previously mentioned, urbanization of the human population has been rapid, and the migration of people has been accompanied by the migration of their animals. For example, the global distribution of swine appears to be heavily concentrated in East and Southeast Asia, along with poultry (see Figure 3-6). This can present public health concerns and challenges, given that pigs can play a crucial role in influenza ecology and epidemiology because of their susceptibility to both human and avian viruses; scientists consider them a “potential ‘mixing vessel’ for influenza viruses, from which reassortants may emerge” (Capua and Alexander, 2008, p. 4).

FIGURE 3-5. Distribution of poultry in East and Southeast Asia.

FIGURE 3-5

Distribution of poultry in East and Southeast Asia. SOURCE: FAO (2007). Reprinted with permission from FAO.

FIGURE 3-6. Global swine distribution.

FIGURE 3-6

Global swine distribution. SOURCE: FAO (2007). Reprinted with permission from FAO.

Two major trends have occurred in poultry agriculture in the region since the 1960s. First, intensive poultry agriculture was introduced into Thailand in the late 1960s through a strategic partnership between the Charoen Pokphand Corporation (known as “CP Corp”) and Arbor Farms in the United States. This was a core technology that was adopted to create the first fully vertically integrated approach (seeds for animal feed, and animals purposed for fast food) in Asia. In 1978, CP Corp registered as corporation #001 in the People’s Republic of China and introduced the first barns containing more than 5,000 birds into that country. By the 1990s, CP Corp was the largest chicken producer in Asia (Horn, 2004), and by 2003, Thailand was the third largest producer of poultry in the world. It is not known to what extent these coincidental trends may have “set the stage” for the avian influenza outbreaks that have ravaged the region since 2003 (Kimball, 2006). Other issues unique to Southeast Asia confound the control of avian influenza. Waterfowl are asymptomatic reservoirs for HPAI H5N1. Thus, the traditional practice of free-range raising of ducks serves to disseminate infection among vulnerable poultry flocks.

Legal and Illegal Trade

Legal Wildlife Trade

Few reliable estimates can quantify the global illegal trade in wildlife6 or its value, but some estimates are in the billions of dollars annually. Some analysts identify the United States, the People’s Republic of China, and the European Union as the areas with greatest demand, driven by the need for specific animal parts to use in zootherapeutics (e.g., powdered rhino horn), for human consumption (e.g., bushmeat), as symbols of wealth (e.g., hunting trophies), and as exotic pets (e.g., black palm cockatoos). The United States purchases nearly 20 percent of all legal wildlife products on the global market (CRS, 2008). Source countries of both legal and illegal exports tend to include developing countries with rich biological diversity (CRS, 2008).

The World Organization for Animal Health (OIE), acting through the World Trade Organization, deals almost entirely with a series of diseases listed as “notifiable,” which are of importance to agriculture and trade. High-impact diseases that are present in introduced wildlife and that do not affect human or food-animal health are rarely the subject of legislation, even though OIE has the authority to list wildlife diseases as notifiable due to their impact on wildlife and the environment. In both developed and developing countries, the legislative authority and responsibility over human and ecosystem health impacts of the wildlife trade are unclear or poorly coordinated.

A recent study by the Consortium for Conservation Medicine showed that more than half a million shipments containing more than 1 billion live animals were imported into the United States between 2000 and 2006 (Smith et al., 2009). Nearly all of these shipments were designated for commercial purposes (e.g., pet and food trade), and nearly 80 percent contained animals from wild populations (Smith et al., 2009). Annual shipments of live animals traded by the United States increased significantly over the time period of the study, as did the number of individual animals traded.

In the United States, the U.S. Department of Agriculture is responsible for health inspection of wildlife shipments, but only for those animals used in food production. Thus, when wildlife are imported into the United States, they are inspected by the U.S. Fish and Wildlife Service (USFWS)7 to examine their CITES (The World Conservation Union’s Convention on International Trade in Endangered Species of Wild Fauna and Flora) status, but minor clinical signs are unlikely to be reported. Wildlife reservoirs of zoonotic pathogens often show no clinical signs, so they would likely be missed in the USFWS screenings of shipments.

Furthermore, the focus of the agency is conservation, not disease prevention and detection. In 2007, the USFWS processed 188,000 wildlife shipments worth more than $2 billion, conducted 14,000 investigations, and recorded a total of more than 200 million live wildlife legally imported into the United States (Einsweiler, 2008). By the fourth quarter of 2008, USFWS had 114 inspectors stationed at 38 ports of entry/exit and 201 special agents stationed around the country. Even with these resources, the agency physically inspects an average of only 25 percent of all wildlife shipments (Einsweiler, 2008).

The U.S. Centers for Disease Control and Prevention (CDC) also plays a role in regulating and monitoring the U.S. importation of animals used for nonfood production purposes.8 A recent example is the 2003 U.S. outbreak of human monkeypox, a zoonosis harbored by African rodents imported into the United States for the pet trade. After 215 CDC employees spent 65 person-days investigating 72 human cases and confirming 37 of the cases (Marano, 2008), CDC and the Food and Drug Administration (FDA) jointly used emergency powers to ban importation of this pathogen’s species reservoirs and restrict interstate movement of African rodents and prairie dogs. In September 2008, FDA lifted its restrictions on the interstate movement of prairie dogs, but the CDC national importation ban remained in place. A CDC official noted, however, that the ban on African rodents also resulted in an increase in the U.S. importation of rodents for the commercial pet trade from other continents, especially Asia (Marano, 2008).

The trade in wildlife has led to the introduction of pathogens that threaten human and animal health, agricultural production, and biodiversity. The human-mediated introduction of infectious disease and vectors, termed “pathogen pollution” (Daszak et al., 2000), is expected to continue to rise via future expansion of global travel and trade (Cunningham et al., 2003; Daszak and Cunningham, 2003). There appears to be a growing awareness of this impact by the wildlife trade, particularly following SARS and human monkeypox. This adds pressure to deal with the welfare and conservation impact of the trade, in particular the repeated introduction of invasive species (Eterovic and Duarte, 2002; Reed, 2005; Fowler et al., 2007).

ENVIRONMENTAL FACTORS

Emerging infectious diseases are by definition in a process of flux, either rising in incidence, expanding in host or geographic range, or changing in pathogenicity, virulence, or some other factor. It is increasingly clear that large-scale, often anthropogenic, environmental changes are among the most important drivers of emerging zoonoses. These drivers include landuse changes (e.g., deforestation, agricultural encroachment, and urban sprawl), climate change, and more subtle products of anthropogenic change such as biodiversity loss (IOM, 1992; Krause, 1992, 1994; Morse, 1993; Daszak et al., 2000, 2001; Anderson et al., 2004). These drivers often act via complex pathways that are poorly understood. For example, fragmentation, which may be due to suburban expansion of housing developments, generally leads to loss of biodiversity; this has been linked to heightened Lyme disease risk in the northeastern United States (Ostfeld and Keesing, 2000; Allan et al., 2003; LoGiudice et al., 2003).

Unraveling this complexity will require long-term field research to account for annual variation in environmental or other factors. For example, it has taken more than a decade to demonstrate the mechanistic interaction of biodiversity changes and Lyme disease risk in the United States, and the link between El Niño-Southern Oscillation (ENSO), rainfall, and hantavirus pulmonary syndrome in the Southwest desert (Mills et al., 1999). However, these studies have key value to human and animal health in that they demonstrate causative links that can be used, for example, to predict climate-linked outbreaks of vector-borne diseases (Linthicum et al., 1987, 1999).

Deforestation

Rates of deforestation have increased exponentially since the beginning of the 20th century. Although reforestation has been conducted in some developed countries (e.g., parts of Europe and the United States), 2–3 percent of global forests continue to be lost each year with the majority of losses in tropical countries. Deforestation and processes that lead to it have a number of ecosystem consequences. Deforestation decreases the overall habitat available for wildlife species. It also modifies the structure of environments, for example, by fragmenting habitats into smaller patches separated by agricultural activities or human populations. Increased “edge effect” (from a patchwork of varied land uses) can further promote interaction among pathogens, vectors, and hosts. This edge effect has been well documented for Lyme disease (Glass et al., 1995). Similarly, increased activity in forest habitats (through human behavior or occupation) appears to be a major risk factor for leishmaniasis (Weigle et al., 1993). Evidence is mounting that deforestation and ecosystem changes have implications for the distribution of many other microorganisms and the health of human, domestic animal, and wildlife populations.

Deforestation, with subsequent changes in land-use and human settlement patterns, has coincided with an upsurge of malaria and its vectors in Africa (Coluzzi et al., 1979; Coluzzi, 1984, 1994), in Asia (Bunnag et al., 1979), and in Latin America (Tadei et al., 1998). When tropical forests are cleared for human activities, they are typically converted into agricultural or grazing lands. This process is usually exacerbated by road construction, which causes erosion and allows previously inaccessible areas to become colonized by people (Kalliola and Flores, 1998). Cleared lands and culverts that collect rainwater are in some areas far more suitable for larvae of malaria-transmitting Anopheline mosquitoes than are intact forests (Tyssul Jones, 1951; Cruz Marques, 1987; Charlwood and Alecrim, 1989). Deforestation and logging often result in exposure of small groups of people and food-animals to new pathogens, particularly where bushmeat hunting occurs (Wolfe et al., 2000). Finally, land-use changes drive some of these pathogen introductions and migrations, and those changes increase the vulnerability of habitats and populations to these introductions. Human migrations also drive land-use changes that, in turn, drive infectious disease emergence.

Habitat Fragmentation

One of the key products of anthropogenic land-use change is the fragmentation of wildlife habitat, which alters the composition of host species in an environment and the fundamental ecology of microorganisms. Top predators and other species at higher trophic levels usually exist at low-population density and are sensitive to changes in food availability. The smaller patches left after fragmentation reduce sufficient prey populations, causing local extinction of predators and a subsequent increase in the density of their prey species. Smaller fragments in North American forests have fewer small mammal predators and higher densities of white-footed mice, a highly competent reservoir of the Lyme disease pathogen Borrelia burgdorferi (Ostfeld and Keesing, 2000). In these fragments, the risk of Lyme disease infection in people is higher; in less modified habitats, increasing diversity of alternative and less competent reservoirs dilute this risk (Ostfeld and Keesing, 2000). Therefore increasing diversity provides a “dilution effect”—a buffer against disease risk that is lost when habitat is fragmented (Schmidt and Ostfeld, 2001).

Agriculture

Crop Irrigation and Breeding Sites

Agriculture occupies most of the world’s arable land and uses more than two-thirds of the world’s fresh water (Horrigan et al., 2002). The subsequent increase in irrigation reduces water availability for other uses and increases breeding sites for disease vectors. Irrigation development in the southern Nile Delta following construction of the Aswan High Dam has caused a rapid rise in mosquito populations and an increase in the Culex-borne disease, Bancroftian filariasis (Harb et al., 1993; Thompson et al., 1996). Onchocerciasis and trypanosomiasis are further examples of vector-borne parasitic diseases that may be triggered by changing land-use and water management patterns. In addition, large-scale use of pesticides has had other deleterious health effects on farm workers, including poisoning, hormone disruption, and cancer (Blair et al., 2005; Bretveld et al., 2006; Calvert et al., 2008).

Food-Borne Diseases

The expansion of international food trade has led to a series of disease outbreaks and the emergence of some novel agents. U.S. importation of strawberries from Mexico, raspberries from Guatemala, carrots from Peru, and coconut milk from Thailand have caused recent outbreaks. Some recent outbreaks of food-borne diseases in meat and vegetables can also be attributed to domestically produced food. Food safety is an important factor in human health. Food-borne disease accounts for an estimated 76 million illnesses, 325,000 hospitalizations, and 5,200 deaths in the United States each year (CDC, 2005). Other dangers include antibiotic-resistant organisms, such as Cyclospora, Escherichia coli O157:H7, and other pathogenic E. coli associated with hemolytic uremic syndrome in children (Dols et al., 2001).

Secondary Effects

There are secondary health effects associated with agricultural production. Examples include the emerging microbial resistance from antibiotics in animal waste that is found in groundwater fed from farm run-off, and the introduction of microdams for irrigation in Ethiopia that resulted in a seven-fold increase in malaria (Ghebreyesus et al., 1999).

Encroachment into Wildlife Habitat

Alterations of ecosystems and natural resources contribute to the emergence and spread of infectious disease agents. Human encroachment on wildlife habitat has broadened the interface between wildlife and humans, resulting in increased opportunities for both the emergence of novel or reemergence of known infectious diseases in wildlife and their transmission to people. Rabies is an example of a zoonotic disease carried by animals that has become habituated to urban environments. Bats colonize buildings; skunks and raccoons scavenge human refuse; and in many countries, feral dogs in the streets are common and a major source of human infection (Singh et al., 2001).

Infectious diseases can also pass from people to wildlife. Nonhuman primates have acquired measles from ecotourists (Wallis and Lee, 1999). Also, drug resistance in gram-negative enteric bacteria of wild baboons with limited human contact is significantly less common than in baboons near urban or semi-urban human settlements (Rolland et al., 1985).

Climate Change

Climate models for greenhouse warming predict that geographic changes will take place in a number of water-borne (e.g., cholera) and vector-borne (e.g., malaria, yellow fever, dengue, leishmaniasis) diseases. These changes will be driven largely by increases in precipitation leading to favorable habitat availability for vectors, intermediate and reservoir hosts, or warming that leads to expansion of ranges in low latitudes, oceans, or mountain regions. Two phenomena indicate that climate change will likely have a heightened impact on key human diseases. First, a strong link exists between ENSO and outbreaks of RVF, cholera, hantavirus, and a range of emergent diseases (Colwell, 1996; Bouma and Dye, 1997; Linthicum et al., 1999; Anyamba et al., 2009). If ENSO cycles become more intense, as they are predicted to do under climate change scenarios, these events may become more extensive and have greater impact. Secondly, recent expansion of Culicoides species, the vector species that spreads the diseases bluetongue and African Horse Sickness, into Northern Europe, has led to outbreaks of bluetongue there as recently as 2006, and has put Europe on alert for the potential introduction of African Horse Sickness. The recent geographic expansion of this vector species has been hypothesized to have a climate-change link, although this remains a controversial point (Purse et al., 2005; Wilson et al., 2008).

TECHNOLOGICAL CHANGES LEADING TO DISEASE EMERGENCE

Disease Diagnosis and Detection

Routine disease diagnosis has a central role in disease surveillance. Although it is not a direct driver of disease emergence, differences in laboratory diagnostic approaches and diagnostic goals between the human and animal health fields, variable levels of communication, and limited comparison of microbial populations in humans and animals can hinder early recognition of an emerging zoonotic disease event. These factors can delay intervention and response with consequent amplification of the impact in both human and animal populations.

The laboratory infrastructure and approach is quite different in resource-constrained countries. Although some point-of-care assays for targeted diseases such as avian influenza are available for animals, few are actually deployed in laboratories at the district or community level. Assays for zoonotic diseases such as brucellosis—which are simple, commonly used in developed countries, and easily deployed—are not uniformly available in developing countries. Routine infectious disease diagnosis in animals is virtually nonexistent in sub-Saharan Africa and in much of the Near and Far East, where expertise that is on par with most state diagnostic laboratories is simply not available. Diagnosis of animal diseases is often established in the field through familiarity of field personnel, such as veterinarians or community animal health paraprofessionals, with clinical presentations for transboundary infectious diseases of importance to the country for trade and disease-free status. Confirmatory diagnosis is made in national laboratories when possible, and OIE reference laboratories when not. Some of these diseases will be zoonotic (e.g., RVF), while many are not. As a result, diagnosis of zoonotic diseases in developing countries is most often first made in humans. However, diagnosis of zoonotic disease agents is also quite limited in resource-constrained countries except at the national level.

Exceptions can be found, most often supported by a combination of national, donor nation, and nongovernmental organization funding. Examples include the CDC International Emerging Infections program at the Kenya Medical Research Institute, the Uganda Virus Research Unit in Entebbe, and the International Center for Diarrheal Diseases Research, Bangladesh. In general, however, the challenges of routine diagnosis of and communication about zoonotic agents found in developed countries are exponentially amplified in the developing world by a nearly universal lack of sustained laboratory infrastructure for disease diagnosis. As a result, the majority of infectious diseases remain undiagnosed in much of the developing world. The threat of pandemic influenza and other emerging diseases has stimulated donor support to develop the ability to diagnose specific agents in humans. Unfortunately, the animal disease diagnostic infrastructure has not been included in this enhanced donor support in most resource-constrained countries. Additionally and with few exceptions, communication between the human and animal health sectors remains limited.

Early recognition and intervention in an emerging infectious zoonotic disease event is essential to limit spread, whether it involves a novel agent such as the SARS virus or an adaptation of a routinely recognized pathogen such as influenza virus. Limitations in conventional approaches to diagnosis of infectious diseases in humans and animals, while not directly driving emerging disease events, can contribute to spread within the population. Differential diagnoses for unusual disease events need to be expanded to include the unknown or not-yet-discovered pathogen. Recognition of these limitations will help inform a strategic approach toward effective zoonotic disease surveillance.

Farm Management

As identified earlier, the most remarkable trend in farm management over the past 30 years has been toward intensification, which has its origins in the United States. The ready availability of inexpensive grain and the rapid growth of an efficient transportation system have made it possible to supply large concentrations of animals with sufficient feed. As shown in Box 3-1, large-scale facilities in manmade ecosystems permit the production of more units of consumable nutrients produced per unit of input than other systems. Intensive agriculture has since spread to all parts of the world, and it has both advantages and disadvantages (see Box 3-2).

Box Icon

BOX 3-2

Advantages and Disadvantages of Intensive Agriculture Related to Zoonotic Diseases. Advantages Increased ease of monitoring. With animals congregated and the focus on profit, avoiding disease is important in minimizing losses. Consequently, there are (more...)

Disease Management for Food-Producing Animals

As previously mentioned, food-producing animals are economic entities. Disease treatment is not administered to individual animals; instead, the entire herd is monitored. Although it might seem easy to protect the human population from serious zoonotic diseases (e.g., anthrax or Brucella) through vaccination of all at-risk animals, in practice, food-animals are only vaccinated against diseases as a matter of cost–benefit if there is a concern regarding the health of the herd or a high probability of human health risk.

Although the topic of antibiotic resistance is beyond the charge of the committee and is in itself the topic of other major studies, the committee recognized the importance of the issue to make a few observations. Antibiotics are commonly used in food-animals as a prophylactic measure, as “growth promoters,” and as a treatment in a very minor proportion. The use of antibiotics for growth promotion began in the 1940s when the poultry industry discovered that the use of tetracycline-fermentation by-products resulted in improved performance (Stokstad et al., 1949), although the mechanisms for improved performance are not completely understood. Research has suggested that growth promotion works by affecting changes in intestinal tract microorganisms, resulting in better absorption of nutrients and consequently improvements in weight gain (Stock and Mader, 1984; Preston, 1987; Elam and Preston, 2004). Poultry and swine production systems account for most of the use of antibiotics in feed, with 44 and 42 percent of all growth-promotant antibiotics used in these two species, respectively. Beef production is responsible for the remaining 14 percent (Mellon et al., 2001). The discontinued use of fluoroquinolones and macrolides in U.S. broiler production could predispose people to greater health risks as a result of increased illness rates in animals, greater microbial loads in servings from affected animals, and hence increased potential for human illness (Cox and Popken, 2006).

Other investigators have found direct links between the feeding of antibiotics and the presence of resistant bacteria in the vicinity, with potential spread to humans. Tetracycline resistance was found in 77 percent and 68 percent of E. coli and Enterococci isolated from samples obtained at a swine concentrated animal feeding operation (CAFO) in the United States (Stine et al., 2007). In a Danish study (Smith et al., 2002), the application of pig manure as fertilizer for farmland resulted in the detection of elevated occurrences of tetracycline-resistant bacteria in the soil immediately after pig manure slurry was spread. Gibbs and colleagues (2006) evaluated the air plume downwind from a CAFO and found a greater concentration of antibiotic-resistant bacteria within and downwind of the swine facility than upwind. Some reports have postulated an association between human and animal health, food-animal antibiotic resistance, and antibiotic resistance in clinical isolates (Teuber, 2001; Smith et al., 2002). Clearly there is concern regarding low-level antibiotic use in food-producing animals, and more scientific data are needed to develop meaningful policies and procedures to protect both human and animal health while optimizing food-animal production.

Biotechnology and Lack of Biosecurity

Biotechnology has precipitated disease emergence in three ways: (1) through medical innovations; (2) as a result of laboratory escapes; and (3) through personal contact with laboratory animals or biological agents in a research setting. A further area of concern is bioterrorism and the manipulation of microbiological agents to make them more readily contagious or infectious among humans.

Medical Innovations

In recent years, transplantation has resulted in several cases of zoonotic diseases infecting transplant recipients. Perhaps the most widely cited instance was an organ donor who was infected with rabies. His organs subsequently infected and killed four transplant recipients (Burton et al., 2005). A second instance involved two clusters of unusual disease in transplant recipients, in which lymphocytic choriomeningitis virus was eventually diagnosed, with seven or eight transplant recipients dying. The organ donor kept a pet hamster that had a strain identical to those isolated from some of the transplant recipients (Fischer et al., 2006).

Xenotransplantation is the transplantation of living organs, tissues, or cells from one species to another, and is considered by some as a solution to the shortage of human organs and tissues. In the late 1990s, several companies were working with pigs that were genetically modified to have a human gene to help decrease the organ rejection response. These pigs were bred to fill the supply–demand gap for human organ transplantation. However, the discovery of an endogenous porcine retrovirus slowed the enthusiasm for this developing field because it proved extremely difficult to create a population of pigs without this retrovirus. The retrovirus is present in the genome in multiple copies. Researchers feared the virus could emerge from porcine-origin cells in intimate apposition within the circulation of the recipient human and adapt to create a transmissible epidemic (Boneva et al., 2001).

Laboratory Escapes

The SARS virus was grown and studied in numerous laboratories around the world. Spread outside of the laboratory has occurred on several occasions, including accidents in Taiwan, Singapore, and China. The incident in China was particularly worrisome as it resulted in three cycles of person-to-person transmission (Lim et al., 2006). Perhaps the most notable and devastating example of laboratory escape is the 1979 incident at Sverdlovsk, Russia, where anthrax spores were disseminated within a population due to inadequate biosecurity and failure to change filters in a timely and adequate manner. This escape resulted in nearly 70 human deaths (National Security Archive, 2001).

Laboratory Animals or Biological Agents in Research

As biotechnology grows and studies in animals continue, there is always the possibility of zoonotic disease occurring in the scientific staff who are responsible for the care of the animals, or in laboratory workers engaged in microbiological aspects of the disease. There have been numerous instances of humans becoming infected with a zoonotic agent within a laboratory, either through contact with animals or working with the infectious agent. To date none of these has resulted in subsequent person-to-person spread. Examples include glanders, tularemia, Q fever, Venezuelan equine encephalitis, and herpes B (Hall et al., 1982; CDC, 2000; Rusnak et al., 2004).

Bioterrorism

Though intentional release and use of pathogens to threaten a nation’s security is also beyond the scope of this study, it is important to mention that it as a driver for zoonotic diseases. In fact, many of the CDC Category A, B, and C bioterrorism agents—such as anthrax, plague, tularemia, brucellosis, and cryptosporidium—are zoonoses. Much has been written about the potential of biotechnology to create a “superbug,” an organism that could pass rapidly through the population, causing massive morbidity and mortality. To date there is little scientific evidence that this is easily achievable, but the threat remains.

INADEQUATE GOVERNANCE

Inadequate governance systems at the local, national, and international levels are another driver. For purposes of this report, “governance” refers to the structures, rules, and processes that societies individually and collectively use to organize themselves to prevent, prepare for, and respond to human and animal health threats. Each driver analyzed in this chapter raises its own set of governance issues within countries and in the relations between nations. The most effective way to prevent zoonotic disease threats is to bring the various drivers of such threats under better control. However, increasing fears of zoonotic disease emergence and spread underscore the lack of confidence in the legal, regulatory, and enforcement mechanisms established by nations to address the political, economic, and cultural trends that exacerbate zoonotic threats.

Poor governance that undermines a country’s ability to prevent zoonoses from emerging and to control the harm their spread might cause flows from many factors. These include the absence of needed regulatory authority, antiquated rules, uncoordinated policy and governmental capacities, lack of resources to devote to addressing difficult health, social, and economic problems, and the speed and scale of globalization.

Governance capacities are crucial to fund, organize, and operate the rules, personnel, laboratory capabilities, information networks, and response interventions needed to identify zoonotic threats early and to act swiftly against them. Crafting and sustaining integrated human and animal health governance capacities locally, nationally, and globally proves difficult for many reasons ranging from complacency in developed countries to the debilitating effects of widespread poverty in least-developed nations. Despite these difficulties, these capabilities need support by strong governance strategies and mechanisms because they serve national interests for human and animal population health; thus governmental bodies need to take responsibility for disease prevention, surveillance, and response. Failure to do so not only contributes to the emergence and spread of zoonotic pathogens, but also creates a blind spot in any attempts to establish a global system of disease surveillance, prevention, and control. Chapter 7 provides an in-depth discussion about the governance challenges facing countries and the international community.

CONCLUSION

The drivers of zoonotic disease can be quite complex—individually and collectively. Although some of these drivers may be understood in isolation or in their simpler, temporal interactions with each other (e.g., food insecurity for workers in a logging or mining camp in Africa, leading to increased hunting and consumption of bushmeat), the complex ways in which they change over time (sometimes in lengthy intervals as with HIV) and how they interact are not well understood. Constant with the coexistence of humans on the planet are the challenges that the drivers present for when, how, and where zoonotic diseases will emerge.

The committee concludes that there are few efforts for regular or sys tematic review of the scientific information about these drivers. Such a re view is needed to inform strategic action that can mitigate the consequences of drivers by national and global policymakers or international donors dedicated to global development and poverty reduction. The efforts are also minimal when governments or governance entities negotiate international treaties for activities or interests not specifically geared toward protecting human and animal health, but which may impact them. The committee also concludes that dedicated attention and resources to improve our recognition of and comprehension about these factors is a significantly noticeable gap in global zoonotic disease surveillance, reporting, and response efforts.

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Footnotes

1

The term “Green Revolution” was coined by the director of the U.S. Agency for International Development in 1968 to describe the phenomenal growth in production of rice and wheat. The Rockefeller and Ford foundations made research investments to improve breeding varieties combined with expanded use of fertilizers, other chemical inputs, and irrigation. This led to dramatic yields of these grains, particularly in Asia and Latin America, in the late 1960s. Although heralded as a major achievement in establishing levels of national food security for developing countries, it is also criticized for causing environmental damage, including polluting waterways with chemicals, affecting the health of farm workers, and killing beneficial insects and wildlife (IFPRI, 2002).

2

The underlying quantitative parameters driving this growth over the period 1992–2002 are (1) population increases of 1.7 percent per year in the developing world versus 0.4 in the developed world; (2) per-capita gross domestic product increase of 3.9 percent in the developing world versus 0.4 percent in the developed world; and (3) expenditure elasticity (percentage increase in expenditure on an item with a 1 percent increase in total expenditure) for meat in low-income countries of 0.78 percent, in middle-income countries of 0.64 percent, and in high-income countries of 0.36 percent (Searle et al., 2003).

3

Eid al-Adha (Arabic for “Festival of the Sacrifice”) is a major Islamic festival that takes place at the end of the Hajj observed by Muslims throughout the world to commemorate the faith of Ibrahim.

4

In 2007, more than 900 million people suffered from malnutrition due to chronic food insecurity, an increase of 75 million in 1 year (FAO, 2009a). Recent events such as increased farming for use in biofuels, high world oil prices, and escalating consumer demand in emerging economies such as India and China have caused major fluctuations in food security, particularly for the urban poor, raising the number of people who are at least periodically food insecure to 2 billion (FAO, 2009a). Globally, bushmeat forms an important part of the diet for many poor households (de Merode et al., 2004). As prices of imports increase or strife breaks down international market chains, the consumption of bushmeat increases (Karesh et al., 2005).

5

A production system clusters production units (herds, farms, ranches), which, because of the similar environment in which they operate, can be expected to produce according to similar production functions. This similar environment can be characterized by the physical (climate, soils, and infrastructure) and biological environments (plant biomass production, food-animal species composition) and economic and social conditions (prices, population pressure and markets, human skills, and access to technology and other services) and policies (land tenure, trade, and subsidy policies) (Seré and Steinfeld, 1996).

6

Illegal trade in wildlife is defined as “Illicit procurement, transport, and distribution—internationally and domestically—of animal parts and derivatives thereof, in contravention of laws, foreign, and domestic, and treaties. Illegal wildlife trade ranges in scale from single-item, local bartering to multi-ton, commercial-sized consignments shipped all over the world. Wildlife contraband may include live pets, hunting trophies, fashion accessories, cultural artifacts, ingredients for traditional medicines, wild meat for human consumption, and other products” (CRS, 2008, p. 1).

7

The U.S. Fish and Wildlife Service (USFWS) conserves, protects, and enhances fish, wildlife, and plants and their habitats and is responsible for ensuring that imports meet international CITES (The World Conservation Union’s Convention on International Trade in Endangered Species of Wild Fauna and Flora) requirements. The USFWS collaborates with the U.S. Department of Agriculture, the U.S. Food and Drug Administration, the U.S. Centers for Disease Control and Prevention, and U.S. Customs. Globally, it collaborates with the INTERPOL Wildlife Crime Working Group and the Association of Southeast Asian Nations Wildlife Law Enforcement Network (Einsweiler, 2008).

8

The U.S. Centers for Disease Control and Prevention’s Division of Global Migration and Quarantine enforces Department of Health and Human Services’ authority at 20 ports of entry to protect human health and has the authority to restrict importation of animals and products if they pose threats to human health. These may include dogs, cats, turtles, tortoises, terrapins, nonhuman primates, etiologic hosts, vectors, agents, African rodents, persons, carriers, and things (IOM, 2006; Marano, 2008).

Copyright 2009 by the National Academy of Sciences. All rights reserved.
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