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Infectious Disease Movement in a Borderless World: Workshop Summary 3 Mobile Animals and Disease OVERVIEW As discussed in the previous chapter, trade in livestock, poultry, and animal products precipitated the emergence of several important zoonotic diseases, including H5N1 influenza and bovine spongiform encephalopathy (BSE). The essays collected in this chapter consider additional mobile animals, such as pets, wildlife, research animals, and insect vectors (with and without their various hosts) as factors in infectious disease emergence. In addition to introducing diseases to new animal and human populations, some of these animals are changing ecosystems in ways that alter the transmission dynamics of infectious diseases. The first paper, by workshop speaker Nina Marano and colleagues of the Centers for Disease Control and Prevention (CDC), describes regulatory procedures designed to reduce the threat of zoonotic diseases to the United States. The CDC is one of four government agencies that regulate the importation of animals based on their risk for zoonotic disease; the others are the Department of Homeland Security (Customs and Border Protection), the Department of Agriculture (Animal and Plant Health Inspection Service), and the Department of the Interior (Fish and Wildlife Service). Marano et al. review the CDC’s animal regulations, including those that were developed in response to such noteworthy events as an Ebola outbreak among research animals in a government primate research facility in Reston, Virginia; the emergence of monkeypox in pet prairie dogs; the detection of zoonotic viruses in bushmeat; and the presence of highly pathogenic avian influenza in imported birds. Until recently, the CDC’s regulatory actions to address disease threats from imported animals have been largely reactive, species-specific, and pathogen-
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Infectious Disease Movement in a Borderless World: Workshop Summary specific, the authors state. Now the agency—much like the Food and Drug Administration (FDA) as described by Acheson in the previous chapter—is engaged in developing a “risk based, proactive approach to preventing the importation of animals and vectors that pose a zoonotic disease risk,” according to Marano et al. This effort, which they describe in some detail, focuses on the systematic and targeted surveillance of high-risk animals, animal products, and vectors in their countries of origin. Rapid expansion of trade and transportation during the Industrial Revolution resulted in the global proliferation of mosquito-borne diseases, such as dengue and chikungunya. Thanks to today’s globalized economy, these and other vector-borne diseases—once considered well-controlled in industrialized countries—are poised for resurgence, while others, such as West Nile viral fever and chikungunya, have significantly expanded their geographic range. In his contribution to this chapter, workshop speaker Paul Reiter, of Institut Pasteur, examines the role of human activities in the dispersal of several important insect vectors (such as the mosquito species that transmit malaria and yellow fever to humans) and of vector-borne diseases of both humans and animals, including chikungunya, West Nile viral fever, Rift Valley fever, and bluetongue. He also predicts future range expansions for certain vectors and vector-borne diseases; for example, he expects that Aedes gambiae, “perhaps [the] most effective malaria vector on earth,” will migrate northward out of its native home in sub-Saharan Africa, and also across the Atlantic to South America. Reiter, who captured the first specimen of the mosquito species Aedes albopictus in the United States in 1983, and who subsequently discovered that this Asian native had been distributed globally in shipments of used tires, observes that, while “it is not difficult to survey a species once it has been detected, it is much more difficult to detect new introductions when they occur, particularly when cargoes are imported in locked containers.” Therefore, he concludes, “with a few exceptions—e.g., the enforcement of vaccination requirements—we must expect the continued establishment of new exotic species as an inevitable consequence of modern transportation technology.” Might it be possible to prevent the emergence of infectious diseases by anticipating and blocking the movements of pathogens into new ecosystems? This question is posed by speaker Andy Dobson of Princeton University and Sarah Cleaveland of the University of Glasgow in this chapter’s final essay. Through a detailed examination of the circumstances that led up to the emergence of Nipah virus in Malaysia, the authors provide a number of insights into how other “novel” pathogens are likely to emerge, and they suggest a series of general questions that must be answered in order to predict and prevent future outbreaks of emerging infectious diseases. To quantify the risk presented by a novel microbe to a potential host, Dobson and Cleaveland explain, information must be gathered and assessed at each of several stages in the development of an epidemic, from characterizing the back-
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Infectious Disease Movement in a Borderless World: Workshop Summary ground of all potential pathogens to analyzing transmission dynamics among novel hosts. “Ultimately the only way we can quantify the risk of novel microbes to humans (and domestic livestock) is to create a huge phylogeny of all pathogens and their hosts,” they write. “We then need to examine the pathology of closely related pathogens, in their reservoir hosts and other host species they infect and examine the factors that modify virulence and transmissibility.” Such an effort “will require considerable capacity-building in areas that are woefully underfunded,” they acknowledge. PUBLIC HEALTH IMPACT OF GLOBAL TRADE IN ANIMALS Nina N. Marano, D.V.M., M.P.H.,1 G. Gale Galland, D.V.M., M.S.,1 Jesse D. Blanton, M.S.,2 Charles E. Rupprecht, D.V.M., Ph.D.,2 James N. Mills, Ph.D.,2 Heather Bair-Brake, D.V.M., M.P.H.,1 Betsy Schroeder, M.P.H.,1 Martin S. Cetron, M.D.1 Centers for Disease Control and Prevention Introduction Zoonoses are diseases that are transmissible from animals to people. The prevention and management of zoonoses in humans pose unique considerations for surveillance and detection of these diseases and require acknowledgment of the role of animals in disease transmission. Wildlife and animals intended for the pet trade can serve as hosts for a variety of well-known and emerging zoonotic pathogens. The Centers for Disease Control and Prevention’s (CDC’s) regulations exist to prevent the importation of animals and animal by-products that pose a risk to public health. However, globalization of the food supply, consumer goods, and live animals—combined with human behaviors and preferences for the exotic—are ever-growing risk factors for translocation to the United States of zoonotic diseases from parts of the world where they are endemic (or exist in a reservoir state) (Smith et al., 2009). This paper describes the CDC’s regulatory framework for mitigating response to the introduction of zoonotic diseases, which has traditionally been reactive. The challenges of the twenty-first century call for a more proactive approach rooted in a risk-based strategy to prevent the introduction of animals and vectors that pose a risk to public health. 1 Division of Global Migration and Quarantine. 2 Division of Viral and Rickettsial Diseases.
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Infectious Disease Movement in a Borderless World: Workshop Summary CDC’s Animal Regulations: Mitigating Public Health Threats Under Section 361 of the Public Health Service Act3 (42 USC § 264), the CDC is responsible for regulations to prevent the introduction, transmission, and spread of communicable diseases from foreign countries into the United States. The CDC currently regulates the importation of nonhuman primates, dogs and cats, small turtles, African rodents, civets, and Asian birds to prevent the entry of zoonotic diseases and also regulates the importation of etiologic agents, hosts, and vectors (HHS, 2001). Nonhuman Primates Nonhuman primates (NHPs), particularly those recently captured in the wild, may harbor agents in their blood or other body tissues that are infectious to humans. Persons working in temporary and long-term animal holding facilities and individuals involved in transporting animals (e.g., cargo handlers and inspectors) are especially at risk for infection. NHPs are a potential source of pathogens that can cause severe or fatal disease in humans, including filoviruses, hepatitis, herpes B virus, rabies, tuberculosis, and parasitic infections (NRC, 2003). Some cynomolgus, African green, and rhesus monkeys imported into the United States have been previously demonstrated to be infected with Ebola Reston virus (CDC, 1990). An epidemiologic link between hepatitis A infections in NHPs, especially chimpanzees, and their caretakers has been demonstrated (Robertson, 2001). Herpes B virus is a zoonotic agent that naturally infects only macaque monkeys causing mild illness or no illness but can cause fatal encephalomyelitis in humans. Previously reported fatal cases of herpes B virus disease in humans have been caused by animal bites, scratches, or mucous membrane contact with infected materials (Cohen et al., 2002). NHPs, especially macaques, are highly susceptible to tuberculosis and rabies and most are imported from areas of the world with a high prevalence of these diseases in humans and animals (CDC, 1993). NHPs may also be a source of flaviviruses (e.g., yellow fever virus), which may be transmitted to humans by mosquitoes that have previously fed on an infected NHP (Mansfield and King, 1998); transmission of yellow fever to humans in NHP research work has also occurred (Richardson, 1987). Quarantine requirements for imported NHPs are designed to reduce these infectious disease risks. Since October 10, 1975, the CDC, through 42 CFR § 71.53, has prohibited the importation of NHPs except for scientific, educational, or exhibition purposes. Under this regulation, NHP importers are required to register with the CDC and this registra- 3 The Public Health Service Act is a U.S. federal law enacted in 1946. The full act is captured under Title 42 of the United States Code “The Public Health and Welfare,” Chapter 6A, “Public Health Service.” Under Section 361 of the Public Health Service Act (42 U.S.C. § 264), the U.S. Secretary of Health and Human Services is authorized to take measures to prevent the entry and spread of communicable diseases from foreign countries into the United States and between states.
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Infectious Disease Movement in a Borderless World: Workshop Summary tion must be renewed every two years. NHPs are required to be held in quarantine for a minimum of 31 days following entry into the United States. This regulation also requires registered importers to maintain records on imported NHPs and to immediately report illness suspected of being communicable to humans. Imported NHPs and the offspring of imported NHPs may not be maintained as pets, a hobby, or as an avocation with occasional display to the general public. Additional requirements for importers of NHPs were developed and implemented in response to specific public health threats. On January 19, 1990, the CDC published interim guidelines for handling NHPs during transit and quarantine in response to identification of Ebola virus (Reston strain) in NHPs imported from the Philippines (CDC, 1990). In April 1990, there was confirmation of Ebola virus infection in four NHP caretakers, and serologic findings suggested that cynomolgus, African green, and rhesus monkeys posed a risk for human filovirus infection. As a result of these findings, the CDC placed additional restrictions and permit requirements for importers wishing to import these species. Dogs The CDC restricts the importation of dogs primarily to prevent the entry of rabies (CDC, 2003a). Rabies is a lyssavirus that causes a fatal encephalitis in mammals. In the United States, widespread mandatory vaccination of dogs has eliminated the canine variant of rabies and dramatically reduced the number of human cases (Velasco-Villa et al., 2008). However, canine rabies virus variants continue to be imported via unvaccinated dogs from areas where rabies is enzootic, such as Asia, Africa, the Middle East, and parts of Latin America. Globally, canine variants are responsible for most of the estimated 55,000 human rabies deaths worldwide each year (HHS, 2001; WHO, 2009). Since May 2004, there have been at least four documented instances of dogs being imported to the United States from rabies enzootic areas that subsequently were diagnosed with rabies, necessitating extensive public health investigations to identify persons at risk of exposure and in need of post-exposure prophylaxis (PEP), as shown in Table 3-1 (CDC, 2008b). “In May 2004, an unvaccinated puppy was flown from Puerto Rico to Massachusetts as part of an animal rescue program. The day after arrival, the puppy exhibited neurologic signs, was euthanized, and was subsequently confirmed to have rabies” (CDC, 2008b), with a variant identified as enzootic to dogs and mongoose from Puerto Rico. Among 11 people evaluated, 6 persons were recommended to receive PEP because of potential exposure (personal communication, Frederic Cantor, Massachusetts Department of Public Health, June 20, 2004; CDC, 2008b). “In June 2004, an unvaccinated puppy adopted by a U.S. resident in Thailand was confirmed to have rabies by the California Department of Public Health” (CDC, 2008b), and a dog rabies virus variant identified as enzootic to Thailand. Of 40 persons interviewed for potential rabies exposure, 12 received PEP (personal communication, Ben Sun, California Department of Public Health, August 16,
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Infectious Disease Movement in a Borderless World: Workshop Summary TABLE 3-1 Importations of Rabid Dogs to the Continental United States, 2004-2008 Month/Year No. of Dogs with Rabies/No. of Animals in Shipment Territory or Country of Origin No. of persons receiving PEP/No. of persons interviewed May 2004a 1/6 Puerto Rico 6/11 June 2004b 1/1 Thailand 12/40 March 2007c 1/2 India 8/20 June 2008d 1/24 Iraq 13/38 Based on data from: aMassachusetts Department of Public Health. bCalifornia Department of Public Health. cAlaska Department of Health and Social Services. dNew Jersey Department of Health and Senior Services. 2004; CDC, 2008b). “In March 2007, a puppy was adopted by a U.S. veterinarian while volunteering in India…. The puppy was flown in cargo to Seattle, Washington then adopted by another veterinarian in Juneau, Alaska, where it was flown seven days after arrival” (CDC, 2008b). The puppy exhibited neurologic signs and was confirmed to have rabies by the Alaska Department of Health and Social Services, with a dog rabies virus variant identified as enzootic to India. Of 20 persons interviewed for potential rabies exposure, eight received PEP (Castrodale et al., 2008). Most recently in June 2008, a shipment of 24 dogs and 2 cats arrived in the United States from Iraq as part of an international animal rescue operation. Subsequently, an 11-month-old dog from this group became ill; rabies was confirmed and the virus was determined to be a rabies virus variant associated with dogs in the Middle East. During the public health investigation, 13 of 28 persons were identified with potential exposure of sufficient magnitude to initiate PEP (personal communication, Faye Sorhage, New Jersey Department of Health and Senior Services, July 1, 2008). In all four of these cases, the rabies viruses were identified as exotic variants circulating in dogs and terrestrial wildlife in the animal’s country or region of origin, and were associated with human fatalities. Besides the threat of human and domestic animal exposure and the direct public health, veterinary, and economic consequences associated with PEP, particularly during times when supplies of rabies biologics are less than ideal, such events serve to underline the fragility of the canine rabies virus-free status in the United States posed by such introductions. The introduction of canine rabies, and its potential to become enzootic again in domestic animals or wildlife, would increase the demand for prophylaxis and exacerbate fragile supplies of rabies vaccines and immune globulins. Moreover, other lyssaviruses besides rabies virus persist in the Old World. The danger of importation posed by these agents is greatly magnified because current human and veterinary rabies vaccines do not
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Infectious Disease Movement in a Borderless World: Workshop Summary cross-protect against lyssaviruses from other phylogroups and no pan-lyssavirus vaccines are on the horizon for serious commercial development. Since canine variants of rabies remain a very serious health threat in many other countries, preventing the entry of potentially infected dogs into the United States is a critical public health priority. CDC requires dogs entering the United States to be vaccinated for rabies or, if they are not vaccinated, that the importer agree to have the dog vaccinated and confined for 30 days after rabies vaccination to allow for acquisition of vaccine-induced immunity (HHS, 2001). The CDC is currently considering amending its regulations to institute further requirements for entry of dogs and other pet animals to the United States to prevent importation of rabies. Etiologic Agents, Hosts, and Vectors Under Section 71.54 of the Public Health Service Act (Foreign Quarantine4) the CDC also regulates etiologic agents, hosts, and vectors (2003b). This regulation means that a person may not import into the United States, or distribute after importation, any etiologic agent or any arthropod or other animal host or vector of human disease, or any exotic living arthropod or other animal capable of being a host or vector of human disease unless accompanied by a permit issued by the director. “All live bats require an import permit from the CDC and the U.S. Department of Interior’s Fish and Wildlife Services, and may not be imported as pets” (CDC, 2008c; see also HHS and CDC, 2003a). We are particularly concerned about bats as reservoirs for infectious agents, as we recognize that Marburg virus is clearly associated with a species of bat called Rousettus aegyptiacus, at least in Uganda, and one or more other species are almost surely associated with Ebola virus (Calisher et al., 2006). In addition, bats are known to be the keystone reservoirs for viruses such as rabies virus, other lyssaviruses related to rabies, and henipaviruses and have most recently been identified as the reservoir for severe acute respiratory syndrome (SARS) coronavirus (Cui et al., 2007). Any living insect or other arthropod that is known or suspected of containing an etiologic agent (human pathogen) requires a CDC import permit, and vector snail species capable of transmitting a human pathogen require a permit as well (CDC, 2008c; HHS, 2001). CDC limits imports of small turtles; those with a shell length of less than four inches may not be imported for any commercial purpose (CDC, 2008d; HHS and CDC, 2003b). “This rule was implemented in 1975 after it was discovered that small turtles frequently transmitted Salmonella to humans, particularly young children” (CDC, 2008d; see also HHS, 2001). 4 The provisions of 42 CFR Part 71 of the Public Health Service Act (Foreign Quarantine) contain the regulations to prevent the introduction, transmission, and spread of communicable disease from foreign countries into the States or possessions of the United States.
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Infectious Disease Movement in a Borderless World: Workshop Summary Zoonotic pathogens are important not only because of the known illnesses they cause—which can move to new parts of the world—but also because of new human diseases that can arise from animal sources. In 2003, an outbreak of SARS in humans spread worldwide, and the initial transmission to humans was linked to infected civets sold for food in [Chinese wet markets]. The emergence of SARS in humans following exposure to wild animals is an example of how a previously unrecognized zoonotic disease can quickly cause unexpected illness in human populations. (CDC, 2007b) In 2003, the CDC issued an order to ban the importation of civets because of concerns at the time that these animals were involved in the transmission of SARS coronavirus to humans (CDC, 2004a). Birds Since 1997, and to the present, the outbreaks of avian influenza H5N1 in birds and humans are a prime example of how globalization of the food supply affects public and animal health. In November 1997, the Hong Kong Special Administrative Region Department of Health5 detected new cases of a human illness caused by an avian influenza H5N1 virus. By late December, the total number of confirmed new cases had climbed to 17, of which 5 were fatal…. Except for one doubtful unconfirmed case, all illnesses or laboratory evidence of infection was in patients who had been near live chickens (e.g., in market places) in the days before onset of illness, which suggested direct transmission of virus from chickens to human rather than person-to-person spread…. Because these cases occurred at the beginning of the usual influenza season in Hong Kong, public health officials were concerned that human [influenza] strains might cocirculate with avian influenza strains to generate human and avian reassortant viruses with [the] capacity for efficient person-to-person spread. [In December 1997,] veterinary authorities began to slaughter all 1.6 million chickens present in wholesale facilities or vendors within Hong Kong, and importation of chickens from neighboring areas was stopped. Subsequently, no more human cases caused by avian influenza virus were detected. (Snacken et al., 1999) Highly pathogenic avian influenza (HPAI) H5N1 in poultry and wild birds reemerged in Asia in 2003 and has become established as a veterinary and human health threat throughout the world, presenting challenges for control due to the widespread geographic areas and large numbers of poultry that are affected. 5 See http://www.who.int/mediacentre/factsheets/avian_influenza/en/#history (accessed July 13, 2009).
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Infectious Disease Movement in a Borderless World: Workshop Summary Because birds imported into the United States from countries with HPAI H5N1 could pose a risk for human infection or spread of virus to U.S. birds, in 2004 the CDC issued emergency orders to ban the importation of birds and bird products from specific countries with HPAI H5N1. These orders mirrored similar regulatory actions taken by the U.S. Department of Agriculture Animal and Plant Health Inspection Service (USDA/APHIS) to prevent the importation of birds with HPAI H5N1 (CDC, 2007a). On January 21, 2008, the CDC published a notice in the Federal Register seeking public comment on a proposal to rescind its bird embargoes (CDC, 2004b). In 2004, when HPAI H5N1 was first recognized as a threat, CDC took emergency action to ban the importation of birds and thus prevent the disease from entering the United States. Since that time, partnerships with public health and agricultural agencies around the world have increased the capacity for surveillance and communication about emerging outbreaks of HPAI [H5N1]…. All the bird embargoes currently in force under USDA regulations will remain in force. (CDC, 2009) CDC continues to work closely with USDA, the World Health Organization, the World Animal Health Organization, the Food and Agriculture Organization, and individual ministries of health to monitor the situation regarding HPAI [H5N1 abroad] to ensure that the threat to human health is being adequately addressed through animal control measures. If necessary, CDC can take measures to control a human health threat based upon its authority to prevent the introduction, transmission, or spread of communicable diseases from foreign countries into the United States. (CDC, 2009) Rodents The emergence of human monkeypox in the Western Hemisphere in May and June 2003 is a vivid reminder of why we are, and should continue to be, concerned about the importation of wild animals into the United States. Monkey-pox is a zoonotic disease endemic to Central and West Africa. African rodents are considered to be the natural hosts of the virus which, in humans, causes rashes similar to smallpox, fever, chills, and headache (CDC, 2004c; Khodakevich et al., 1988). Human infections during the 2003 outbreak were traced back and were determined to have resulted from contact with pet prairie dogs that contracted monkeypox from diseased African rodents imported for the commercial pet trade (CDC, 2003; Hutson et al., 2007; Reed et al., 2004) (Figure 3-1). The shipment of mammals imported from Ghana contained more than six species and a total of 762 African rodents, some of which were confirmed to be infected with monkey-pox. The monkeypox outbreak resulted in 72 human cases, with 37 of those cases being laboratory-confirmed (CDC, 2003). Most patients had direct or close contact with the infected prairie dogs, including 28 children at a day care center and veterinary clinic staff (Reynolds et al., 2007).
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Infectious Disease Movement in a Borderless World: Workshop Summary FIGURE 3-1 Movement of imported African rodents to animal distributors and distribution of prairie dogs from an animal distributor associated with human cases of monkeypox, 11 states, as of July 8, 2003: Illinois (IL), Indiana (IN), Iowa (IA), Kansas (KS), Michigan (MI), Minnesota (MN), Missouri (MO), New Jersey (NJ), South Carolina (SC), Texas (TX), and Wisconsin (WI). Japan is included among sites having received shipments of rodents implicated in this outbreak. Does not include one probable human case from Ohio; investigation is ongoing. Includes two persons who were employees at IL-1. aDate of shipment unknown. bIdentified as distributor C in MMWR 2003; 52:561-564. cIdentified as distributor D in MMWR 2003; 52:561-564. dIdentified as distributor B in MMWR 2003; 52:561-564. SOURCE: CDC (2003). On June 11, 2003, the CDC and the Food and Drug Administration (FDA) pursuant to 42 CFR § 70.2 and 21 CFR § 1240.30, respectively, issued a joint order prohibiting, until further notice, the transportation or offering of transportation in interstate commerce, or the sale, offering for sale, or offering for any other type of commercial or public distribution, including release into the environment, of prairie dogs and the six implicated species of African rodents (FDA, 2003; Gerberding and McClellan, 2003). In addition, pursuant to 42 CFR § 71.32(b), the CDC implemented an immediate embargo on the importation of all rodents (order Rodentia) from Africa. This emergency order was superseded on November 4,
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Infectious Disease Movement in a Borderless World: Workshop Summary 2003, when the two agencies issued an interim final rule creating two complementary regulations restricting both domestic trade and importation, intended to prevent the further introduction, establishment, and spread of the monkeypox virus in the United States. We are also concerned about rodents that originate outside of Africa, from other parts of the world such as Asia, Europe, and South America. We recently conducted an analysis of the numbers and origins of rodents imported to the United States since our African rodent ban was instituted in 2003. We analyzed data from the U.S. Fish and Wildlife Service’s Law Enforcement Management Information System (LEMIS) database, which records the entry of wildlife species to the United States. Since 2003, our ban has effectively limited legal importation of African rodents; the number of different rodent species entering the United States has decreased by 31 percent (Table 3-2). This decrease appears to be due to the restrictions on importation of African-origin rodents. However, the commercial pet market has found a new niche in rodents from other parts of the world, as the number of rodents from Asia, Europe, and South America has increased by 223 percent. Rodents harbor hantaviruses, [resulting in] more than 100,000 hospitalized cases of hemorrhagic fevers in Europe and Asia (McKee et al., 1991). Rodents are also associated with rickettsial diseases. (CDC, 2008e) Scrub typhus and murine typhus cause hundreds of thousands of cases annually; up to 50 percent of some human populations in Asia have antibodies to R. typhus (Azad, 1990). Outbreaks of Salmonella Typhimurium (CDC, 2005) and lymphocytic choriomeningitis (CDC, 2008a) have been associated with pet rodents in recent years. Since they are easier to care for than a dog or cat, these “pocket pets” are considered good choices for children. Because children interact with their pets in a closer and more intimate manner than they do with other animals, they may be at a heightened risk of infection. Table 3-3 provides a listing of pathogens in rodents that meet the following qualifications: they are zoonotic; nonindigenous; capable of causing significant human illness; and, if vector-borne, the vector is present in the United States (Acha and Szyfres, 2003; Eremeeva and Dasch, 2008; Heymann, 2008; Hugh-Jones et al., 1995). Rodents, once established, have several traits that make them ideal hosts for zoonotic diseases. They reproduce rapidly, and, unlike many other species of larger wild mammals, can be found in our gardens, storage buildings, and homes. Insectivorous Mammals Another potential concern for CDC may be insectivorous mammals, as there is some new evidence for hantaviruses being associated with shrews. We do not know whether these shrew-associated hantaviruses are human pathogens, and
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Infectious Disease Movement in a Borderless World: Workshop Summary pathogens in habitats where we only have a limited understanding of what we are actually looking for. Stage Two: Crossover Transmission The second stage in “successful” disease emergence occurs when a pathogen is transmitted between its reservoir host and a novel host species. This is both a rare event and one whose outcome is often missed. In most cases, the novel host’s immune system will overcome the pathogen’s arrival, or more commonly the pathogen will be unable to survive in the novel host species. The host may only suffer mild discomfort and we are only likely to detect the event if the host is human or if a domestic species monitored during routine slaughter is checked before entering the human food chain. Don Burke has called these events “viral chatter”31—they occur all the time, but only a tiny subset gives rise to cases where the virus (not forgetting bacteria, protozoa, fungi, prions, and the parasitic helminthes) is able to infect the host and reproduce in a way that leads to transmission to other members of the novel host species. In many cases, these initial “stuttering chains” of transmission will be broken by rapid intervention or, more often, because the new host is not a particularly good environment for the pathogen (for example, the index case may be an immunologically compromised host, whereas subsequent hosts with healthy immune systems can withstand infection). Analysis of the risks involved at this stage need to focus on the circumstances that caused increased contact between the reservoir host and the novel host species. Changes in the environment are particularly important here. In the case of Nipah virus in Malaysia, for example, deforestation had removed the natural habitat of fruit bats. Their populations were increasingly concentrated in the remaining areas of habitat with fruit trees. Unfortunately, fruit trees were often left around pig farms as they provided shade for the pigpens and an additional source of revenue for pig farmers. Because of the weight constraints of flight, bats only partially eat fruit by sucking out the juices and then regurgitating the seeds and fruit pith below the fruit tree where they have been feeding (Dobson, 2005). The regurgitated fruit can then be eaten by pigs at a time when it is covered by saliva that may be contaminated by Nipah virus. Similar spatial mechanisms are likely to occur as the reservoir hosts of other pathogens become increasingly contained in the fragmented patches of natural habitat that remain when humans have converted the rest of the landscape into agricultural land, shopping malls, and golf courses. If the patches of land contain too few resources to support wildlife, the reservoir hosts may well develop ways of exploiting food resources that are more closely associated with humans, thus increasing the risk of disease transmission to humans. 31 See http://magazine.jhsph.edu/2005/Fall/features/page_4.cfm.
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Infectious Disease Movement in a Borderless World: Workshop Summary Analogous effects occur during the build-up of mice populations in small forest fragments in the eastern United States; these help amplify the spread of Lyme disease (Ostfeld and LoGiudice, 2003). Considerably lower abundances of small mammals occur in large continuous forests where their abundance is reduced by predatory species that cannot survive on the more limited food resources in smaller forest fragments. Similarly, increased populations of domestic livestock will lead to increased contact between these species and remaining populations of wildlife. A potential disease transmission event can occur just as easily when a cow or sheep breaks through a fence and enters a wood or grassland nature reserve, as when an infected sparrow finds its way into a chicken barn. Most of the novel disease events that occur in livestock will also go undetected and rapidly fade out. The tiny subset that does initiate an epidemic outbreak can usually be stopped by culling all infected hosts along with those in which they have been in contact. However, this requires significant vigilance on the part of animal health inspection services and also assumes that farmers will not try to sell or move their livestock before movement restriction orders are put in place. Unfortunately, this assumes all farmers are honest; in Malaysia (during the Nipah outbreak) and in the United Kingdom during the 2001 foot-and-mouth outbreak (Ferguson et al., 2001; Keeling et al., 2001), farmers illegally moved infected livestock into previously uncontaminated areas and initiated new outbreaks that considerably increased the spatial scale of the outbreak and the number of livestock that ultimately had to be destroyed. The economic theory of “crime and punishment” provides important insights here (Becker, 1968; Sutinen and Anderson, 1985); ultimately, detecting the pathogen at the earliest stage of the epidemic and detecting illegal movement of potentially infected livestock will be much more effective in minimizing the size of the epidemic outbreak than will retrospectively imposed large fines or long prison sentences on the small subset of farmers eventually found guilty of illegally moving livestock. Stage Three: Outbreak Detecting infected individuals is crucial if the initial stuttering chains begin to give rise to a sustained epidemic. Two factors are crucial here: (1) the rate of transmission between infectious and susceptible hosts and (2) the ratio of the duration of time before symptoms appear to the duration of time before the hosts can transmit the disease (Fraser et al., 2004). If symptoms appear before transmission is efficient, then control of the outbreak can be achieved by isolation of infected individuals and their primary contacts, particularly when combined with relatively low transmission rates. This is primarily why it was relatively straightforward to contain the SARS outbreak (Anderson et al., 2004). In contrast, when symptoms do not appear until long after transmission has been established, the pathogen can spread and infect a significant number of hosts; HIV is the classic example.
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Infectious Disease Movement in a Borderless World: Workshop Summary Once an outbreak has been established and is spreading, the direct and indirect costs will start to increase faster than the exponential spread of the pathogen between hosts. Stories in the media have dynamics that are similar to epidemics; their transmission rates are much more efficient and their impact is often out of scale from the actual risk involved. The economic cost of the SARS epidemic in Southeast Asia was huge given the small number of people who actually became sick or died (McLean et al., 2005). The economic cost of the foot-and-mouth epidemic in the United Kingdom far exceeded the cost of all the cattle slaughtered due to the large indirect impact on tourism and movement restrictions in rural areas. Searching for novel pathogens and understanding their potential threat and risk of crossing over will require considerable capacity-building in areas that are woefully underfunded. The world has less than 100 people trained to understand the ecology and population dynamics of infectious diseases; this is roughly comparable to the number of knee specialists in New Jersey. Ultimately, this lack of intellectual capacity at the population level within the National Institutes of Health (NIH) has led to the current underestimate of the scale and impact of the H1N1 influenza epidemic in the United States. Equally disconcerting is that the annual meeting of the Wildlife Disease Association attracts less than 400 people and more than 80 percent of them are interested graduate students who are training as veterinarians. The scariest and most intriguing thing about their annual meetings is that each seems to provide an example of a novel pathogen that no one has heard about before and that requires a paradigm shift in the thinking and of people working in the discipline. This year it was white-nose syndrome in bats; last year Tasmanian Devil facial tumors; the year before that, highly pathogenic avian influenza. It is hard to think of another scientific society where a major paradigm shift occurs on an annual basis. Summary The past 25 years have seen major advances in our understanding of the mathematical population dynamic processes that underlie the movement of pathogens within and between host species (Anderson and May, 1991; Grenfell and Dobson, 1995). Over the past 25 years, this whole intellectual enterprise has moved beyond its origins as an area of applied mathematics to one that provides central quantitative insights into public health response to infectious disease outbreaks (Smith et al., 2005). This quantitative ecological-based understanding is central to our understanding of emerging disease dynamics. Any discussion of these problems in the absence of a quantititative mathematical framework are arguably best left in the cocktail reception. The spatial and temporal scales at which epidemic outbreaks occur requires the use of this mathematical machinery; attempting to understand disease dynamics in its absence is equivalent to attempting pathology without a microscope.
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Infectious Disease Movement in a Borderless World: Workshop Summary Unfortunately, levels of funding and training within the United States are considerably below adequate. It is thus likely to be an area where the United States will be increasingly dependent upon talent trained overseas. This is ironic because of the considerable pool of people in the United States trained in physics and mathematics who could make a huge contribution to this area, particularly when coupled into the U.S. domination of the world’s microcomputers, which will increasingly be needed to understand the dynamics of pathogens in populations and communities with complex spatial and temporal connections to each other. Detecting and preventing new pathogens from entering populations of humans and domestic livestock is an important initiative that can potentially tell a lot about the diversity of pathogens that currently inhabit the planet. Even an initial survey of what is out there suggests that there are hundreds of thousands of potentially pathogenic microorganisms already sharing the planet with us. While this is disconcerting, it makes me totally unconcerned about novel ones that might arrive from other planets—the pathetically thin arguments for these “alien pathogens” strike me as little more than a further plea from the National Aeronautics and Space Administration (NASA) for some form of relevance to studies of life on Earth. But, if we are worried about the emergence of new pathogens, early detection will always be significantly less costly than later prevention. If nothing else, there are no indirect costs associated with early detection, and everything to be gained. MARANO ET AL. REFERENCES Acha, P. N., and B. Szyfres. 1987. Zoonoses and communicable diseases common to man and animals. Washington, DC: Pan American Health Organization and World Health Organization. ———. 2003. Zoonoses and communicable diseases common to man and animals. Washington, DC: Pan American Health Organization and World Health Organization. Azad, A. F. 1990. Epidemiology of murine typhus. Annual Review of Entomology 35:553-569. Calisher, C. H., J. E. Childs, H. E. Field, K. V. Holmes, and T. Schountz. 2006. Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19(3):531-545. Castrodale, L., V. Walker, J. Baldwin, J. Hofmann, and C. Hanlon. 2008. Rabies in a puppy imported from India to the USA, March 2007. Zoonoses and Public Health 55(8-10):427-430. CDC (Centers for Disease Control and Prevention). 1990. Update: Ebola-related filovirus infection in nonhuman primates and interim guidelines for handling nonhuman primates during transit and quarantine. Morbidity and Mortality Weekly Report 39(2):22-24, 29-30. ———. 1993. Tuberculosis in imported nonhuman primates—United States, June 1990-May 1993. Morbidity and Mortality Weekly Report 42(29):572-576. ———. 2003. Update: multistate outbreak of monkeypox—Illinois, Indiana, Kansas, Missouri, Ohio, and Wisconsin, 2003. Morbidity and Mortality Weekly Report 52(27):642-646. ———. 2004a. Notice of embargo of civets, http://www.cdc.gov/ncidod/sars/pdf/order_civet_ban_011304.pdf (accessed April 8, 2009). ———. 2004b. Rescission of February 4, 2004, order and subsequent amendments prohibiting the importation of birds and bird products from specified countries, http://edocket.access.gpo.gov/2009/E9-1029.htm (accessed April 8, 2009).
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