Chapter 18 Emerging Diseases at the Interface of People, Domestic Animals, and Wildlife*
Increasingly, diseases are moving among people, domestic animals, and wildlife, creating concerns about food safety, public health, and wildlife conservation.49 Some of these diseases have existed for millennia, whereas others are emerging or reemerging, gaining the ability to jump between species and overloading traditional methods of disease surveillance and prevention. In a list of 1407 human pathogens, 58% are known to be zoonotic; 177 are categorized as emerging or reemerging, and zoonotic pathogens are twice as likely to be in this category as nonzoonotic pathogens.100
The impact on human populations may be significant. The 2004 Joint United Nations (UN) Program on HIV/AIDS report on the global epidemic stated that mortality from human immunodeficiency virus (HIV) exceeded 20 million people in the 20 years since first diagnosed in 1980. HIV-1 and HIV-2 were introduced into humans through separate cross-species transmission of simian immunodeficiency virus. HIV-1 is believed to have arisen through transmission from chimpanzees and HIV-2 from sooty mangabeys (Cercocebus atys).40
Wildlife species under severe environmental pressure are threatened by extinction from the spread of novel pathogens. Chytridiomycosis, caused by Batrachochytrium dendrobatidis, has been implicated in the massive mortality and global decline in a variety of amphibian species.45 International trade is thought to play a key role in the worldwide dissemination of this disease.27,60
Livestock production and market access to animal protein have been increasingly threatened by the emergence of disease. Since 1992, the economic damages from livestock diseases alone has totalled more than $60 billion. Outbreaks of bovine spongiform encephalopathy, foot-and-mouth disease, avian influenza, rinderpest, and other diseases have prompted governments to impose trade embargoes and to mandate animal culling with increasing frequency. In 2003, the UN Food and Agricultural Organization (FAO) reported that one third of global meat trade was subject to embargoes because of disease outbreaks.2
Globalization is the dominant international system that has made the world an increasingly integrated place, resulting in both threats and opportunities.30 The global movement of people, animals, and their products has had profound effects on wildlife, livestock, and public health through the unchecked legal and illegal trade in exotic pets and bush meat. Human population increases and the desire for improved standards of living promote have intensified agricultural practices, pollution of air and water, and the unsustainable use of natural resources. There is little evidence to date that climate change has played a significant role in the resurgence of infectious disease. However, many believe that soon global climate change will be responsible for regional climate alterations that affect physical and biologic systems.68
Hunting, Pets, and Globalized Trade in Wildlife
The local hunting of wildlife or bush meat is an ancient practice that forms the fabric of community culture at the rural wildlife interface (Fig. 18-1). Although these fundamental practices have always posed a cross-species disease risk to the local community, they have been mitigated through cultural practices. Ecologic changes, as created by increased human population density, forest fragmentation via road building, and rural development, alter the relationships of pathogens to hosts.70 These changes, along with increased human movement and the globalized trade in animals for food and pets, facilitate rapid movement to distant sites and greater human-pathogen contact.99
The World Trade Organization’s 2005 statistics note that in 2004 the global merchandise trade rose by 21% to 8.9 trillion U.S. dollars, with agriculture accounting for $783 billion. There is no breakdown of the share of trade in wildlife, but each year an estimated 350 million live plants and wild animals are shipped globally.12 The poorly regulated wildlife component of global trade facilitates infections via microbial travel46 at scales that not only cause human disease outbreaks, but also threaten livestock, international trade, rural livelihoods, native wildlife populations, and the health of ecosystems.42
Surveys of live wildlife from markets in Guangzhou, China, included masked palm civets (Paguma spp.), ferret badgers (Melogale spp.), barking deer (Muntiacus spp.), wild boar (Sus) spp., hedgehogs (family Erinaceidae), foxes (Vulpes spp.), squirrels (family Sciuridae), bamboo rats (Cannomys spp.), gerbils (Rhombomys spp.), various species of snakes, and endangered leopard cats (Felis spp.), as well as domestic dogs, cats, and rabbits.3 Following the 2003 severe acute respiratory syndrome (SARS) outbreak, 838,500 wild animals were reportedly confiscated from the markets in Guangzhou, China.7
Daily, wild birds and reptiles flow through trading centers, where they are in contact with dozens of other species before being shipped to other markets, sold locally, or freed back to the wild as part of religious customs or because they are unwanted pets. In a single market in North Sulawesi, Indonesia, up to 90,000 mammals are sold per year.22 In a survey conducted at a market in Thailand over 25 weekends, more than 70,000 birds of 276 species were sold81 (Fig. 18-2). In lieu of precise trade data, a conservative estimate is that in Asia alone, tens of millions of wild animals are shipped regionally and globally for food, pets, or use in traditional medicine every year.
The global movement of animals for the pet trade is estimated to be a multibillion-dollar industry (Fig. 18-3). Between November 1994 and January 1995, U.S. Department of Agriculture (USDA) personnel inspected 349 reptile import shipments with a total of 117,690 animals originating from 22 countries. Ticks were removed from one or more animals in each of 97 shipments. Infested shipments included 54,376 animals in total.13
The estimate for trade and local and regional consumption of bushmeat in central Africa alone is over 1 billion kg/year,96 and estimates for consumption in the Amazon basin range from 67 to 164 million kg annually.72 In central Africa, the majority of wild animals harvested are small mammals (including small antelope and primates), birds, and reptiles. Assuming an average body weight of 5 kg results in a conservative estimate of 200 million animals in central Africa and 12 to 35 million in the Amazon basin. The increasingly global scope of this trade, coupled with rapid modern transportation and the reality that markets serve as network nodes rather than as product endpoints, dramatically increases the movement and potential cross-species transmission of the infectious agents that every animal naturally hosts.
Monkeypox
Monkeypox is a rare, viral, smallpox-like disease from central and western Africa that was first diagnosed in laboratory primates in 1958. The first human cases were reported in 1970 in Africa. An outbreak in the Democratic Republic of Congo in 1997 was reported to have infected 88 people, with three deaths, all in children younger than 3 years.39
In late May and early June 2003, the first cases of a febrile rash illness in people were reported from Wisconsin, Illinois, and Indiana. Most affected people had been in close contact with recently purchased ill prairie dogs (Cynonys ludovicianus) that had been held with a recent shipment of African rodents. The African rodents that spread the disease had been legally shipped from Ghana to the United States in April 2003 for the pet trade. The shipment included a number of species, and studies indicated that two rope squirrels (Funisciurus), a Gambian rat (Cricetomys), and three dormice (Dryomys) were carrying the monkeypox virus.34 By early July, 71 nonfatal human cases from six states were reported to the Centers for Disease Control and Prevention (CDC).10 Before this event, nonendangered rodents from Africa were legally shipped into the United States for the pet trade with no regulatory controls. Subsequently, restrictions were placed on U.S. importation of African rodents.
Severe Acute Respiratory Syndrome
SARS was first recognized as a newly emerging human disease in November 2002 in Guangdong Province, China.93 Symptoms included high fever, respiratory illness progressing to pneumonia, in some cases diarrhea, and death. The disease first spread to Hong Kong and thereafter across five continents and 25 countries via infected people.71 In April 2003, a new coronavirus was discovered to be the causative agent. In July 2003, the World Health Organization (WHO) listed the number of probable SARS cases in humans at 8437, with 813 deaths.8 Evidence of viral infection, often without signs, was also detected in palm civets (Paguma) farmed in the region.33 The initial suggestion of a link between civets and SARS led to a government directive to cull more than 10,000 masked palm civets in the province despite the ambiguity of the disease link.9 Later, viral evidence was also detected in raccoon dogs (Nyctereutes) and ferret badgers (Melogale), as well as domestic cats. It now appears that the palm civet served as an artificial market-induced host or amplification host, along with a number of other possible species. Subsequent studies determined that three species of horseshoe bat (Rhinolophus)28 were found to be the natural reservoir host for closely related SARS-like coronaviruses.51,56
Bats have been found to be reservoir hosts for a number of viral pathogens, including Lyssa, Nipha,101 Hedra, and Ebola viruses. Their role in emerging disease spread appears to be significant.
Ebola Hemorrhagic Fever
Ebola hemorrhagic fever (Ebola) is named after the river in the Democratic Republic of Congo (DRC, formerly Zaire), where it was first identified. Chimpanzees and humans share 98% of their DNA, and gorillas and humans share 97%.80 Therefore, bush meat in the form of nonhuman primates poses a particularly high risk of cross-species infection into humans. The first three known outbreaks of Ebola occurred between 1976 and 1979 in DRC and Sudan. Between 2000 and 2004, five human Ebola outbreaks were documented in western central Africa. Epidemiologic studies indicated that these outbreaks resulted from multiple introductions of virus from infected animal sources. The index cases were mainly hunters, and all were infected while handling dead animals, including gorilla (Gorilla), chimpanzee (Pan troglodytes), and duiker (Cephalophus).53 Thereafter, outbreaks spread quickly among people, especially through caregivers, and were documented to almost wipe out entire villages.31,52 In people, the symptoms are referable to multiple organ effects, with internal and external hemorrhaging. The Zaire subtype of Ebola virus has been known to have a case-fatality rate of almost 90%, and the Sudan subtype has a rate of approximately 50%.82
Ebola has been linked to declines in western equatorial Africa great ape populations. There is evidence that other forest animals, such as the duiker, are also affected.53 Data do not exist on total numbers of nonhuman primates and duikers that have died of the disease, but it is believed that Ebola rivals hunting as the major threat to ape populations.92 For some time, the natural reservoir host remained elusive.75 Bats were long postulated as a potential reservoir host, as recently confirmed in three species of fruit bat.54
The movement of nonhuman primates for use in biomedical research has also proved to be a source for the spread of Ebola-related viruses. In 1989, a closely related simian hemorrhagic fever was diagnosed in Reston, Virginia, in imported cynomolgus monkeys from the Philippines that died during quarantine. Named Ebola Reston, the disease was later found not to cause human disease.62
Effect of Human Population Growth on Agricultural Practices
By July 2005, the world had an estimated 6.5 billion human inhabitants, 380 million more than in 2000. About 95% of all population growth is occurring in the developing world and 5% in the developed world. By 2050, it is estimated that the world population will increase by 2.6 billion.6 For the 50 years preceding 2000, agriculture focused on meeting the food, feed, and fiber needs of a growing human population. In the next 50 years, the challenge will be not only feeding an expanding human population, but also doing so in a world of declining resources, including water and arable land.47
Large-scale agriculture is susceptible to outbreaks of disease. The 1983-1984 poultry epidemic of highly pathogenic avian influenza in the northeast United States caused markets to drop by $349 million during the 6-month period of the disease.18 The economic impacts of the Nipah virus outbreak in Malaysia in 1997-1998 was estimated to cost $350 to $400 million, whereas the 2001 foot-and-mouth disease outbreak in England and Europe was estimated to have cost markets almost $30 billion (U.S. dollars).66 In the developed world, agribusiness and government commitments to quality farm practices and rigorous health inspection have created a predominantly safe food supply. To provide food animal protein at the levels required, the industry has moved toward more intensive practices that increase productivity through selective breeding for desirable market traits and large-scale biosecure facilities. These characteristics may also leave operations vulnerable to the introduction and rapid spread of pathogens via errant contact with wildlife or the global movement of animals and products from areas that do not practice similar levels of biosecurity.
Transmissible Spongiform Encephalopathies
The transmissible spongiform encephalopathies include chronic wasting disease of cervids, scrapie of sheep, bovine spongiform encephalopathy (BSE) of cattle, and Creutzfeldt-Jakob disease (CJD) of humans. They are caused by pathogenic prions, which are transmissible particles devoid of a nucleic acid genome and composed of a modified isoform of normal prion protein.77 These prion proteins are extremely resistant to inactivation by ultraviolet light, ionizing radiation, steam sterilization, and almost all forms of traditional disinfection.
From October 1996 to November 2002, 129 cases of vCJD were reported in the United Kingdom, 6 in France, and 1 each in Canada, Ireland, Italy, and the United States.11 The World Organization for Animal Health (OIE) has listed more than 184,296 cases of BSE in UK cattle alone as of September 2005. As confirmed, 13 species of zoo animals, including Bovidae and Felidae, have died as a result of infection with the BSE agent.25
Chronic wasting disease (CWD) is a prion disease of wild and farmed cervids in North America.97 It was first recognized in a research herd of mule deer (Odocoileus hemionus) in Colorado in 1967. In 1985, it was diagnosed first in elk (Cervus elaphus) and then in mule deer in a limited region of Colorado. It is believed that the increase in deer and elk farming and the movement of animals for that industry in the United States and Canada provided a means for spread. It has since been diagnosed in multiple states and regions both in captive and free-ranging cervids. Conversion of human prion protein by CWD-associated prions has been demonstrated in an in vitro cell-free experiment15 but, to date, investigations have not identified evidence for CWD transmission to humans.14
Avian Influenza
Avian influenza is an infectious disease of birds caused by type A strains of the influenza virus. Wild birds, predominantly ducks, geese, and shore birds, are the reservoir species for the low-pathogenic strains of avian influenza A virus (LPAI) in nature.95 In these species, it does not usually cause illness. The virus is subtyped on the basis of the antigenic properties of hemagglutinin (HA, or H) and neuraminidase (NA, or N) glycoproteins; 16 HA and 9 NA subtypes have been demonstrated. Viruses containing subtypes H5 and H7 have been observed to become highly pathogenic avian influenza (HPAI) in poultry. HPAI has been isolated primarily from commercially raised birds, including chickens, turkeys, quail, guinea fowl, and ostrich (Struthio camelus). Influenza A viruses of the H5 and H7 subtypes have also been detected in a variety of mammals, including humans. The H5N1 influenza A viruses have been detected in birds, pigs, cats, leopards, tigers,44 and people in Asia.64
Live bird markets that sell a wide variety of domestic and wild bird species to the public provide the perfect conditions for genetic mixing and spread of flu viruses.94 In addition, traditional poultry livestock practices that bring people into close contact with domestic fowl and promote the mixing of wild and domestic waterfowl also provide opportunities for domestic wildlife viral exchange and spread into humans. Such an occurrence may have been the cause of the avian flu (H5N1) outbreak in Hong Kong in 1997 and again in late 2003-2004 throughout Asia. Once established in poultry in Asia, a combination of intensive production methods and high-volume poultry movement, in addition to poor sanitation and hygiene, allowed the disease to spread.
In 2005, the H5N1 HPAI was isolated from migratory waterfowl on Quinghai Lake, China,21 and from a wild whooper swan in Mongolia.1 However, it remains unclear whether migratory waterfowl are effective carriers of the disease or rapidly succumb to the infection before they spread the disease, as may have happened in Mongolia. Calls for mass culling of wild birds have been countered by conservation groups and the FAO.4
Of greater concern should be the global trade in domestic and wild birds. An illegal shipment of two crested hawk-eagles (Spizaetus nipalensis), smuggled into Europe from Thailand, was seized at the Brussels International Airport in October 2004. Both birds appeared clinically normal, and both were positive for the H5N1 HPAI.91
The threat posed by avian influenza goes beyond the food supply to becoming a lethal virus that is easily spread among people, a global pandemic. Such a scenario portends grave risk to the economies of nations and to the health of people. The report of the U.S. National Intelligence Council identified a global pandemic as the single most important threat to the global economy.38 As of December 2005, WHO confirmed 142 human cases, with 74 resulting in death. These tragic statistics pale compared with the greater human disease threat. Genetic reassortment of the H5N1 precursor viruses that caused the initial human outbreak in Hong Kong in 1997 may be traced to outbreaks in poultry in China and seven other east Asian countries between 2003 and early 2004. This same virus has been fatal to humans in the region.55 The fear is that the H5N1 viruses will gain the ability to spread efficiently among people, causing a global pandemic.
There is good reason for concern. In the 20th century, there have been three global pandemics, all believed to have originated from birds.73 The most severe was the 1918 Spanish influenza pandemic virus (H1N1), which was estimated to have killed 20 to 50 million people worldwide. Pandemic influenza may originate through at least two mechanisms: (1) reassortment between an animal virus and a human virus that yields a new virus; and (2) direct spread and adaptation of a virus from animals to humans.16 The characterization of the reconstructed 1918 Spanish influenza pandemic virus84 showed that the direct spread and adaptation of the avian influenza virus caused the pandemic.
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