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Risk of Importing Zoonotic Diseases Through Wildlife Trade, United States Boris I

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Risk of Importing Zoonotic Diseases Through Wildlife Trade, United States Boris I Risk of Importing Zoonotic Diseases through Wildlife Trade, United States Boris I. Pavlin, Lisa M. Schloegel, and Peter Daszak The United States is the world’s largest wildlife import- vidual animals during 2000–2004 (5). Little disease sur- er, and imported wild animals represent a potential source veillance is conducted for imported animals; quarantine is of zoonotic pathogens. Using data on mammals imported required for only wild birds, primates, and some ungulates during 2000–2005, we assessed their potential to host 27 arriving in the United States, and mandatory testing exists selected risk zoonoses and created a risk assessment for only a few diseases (psittacosis, foot and mouth dis- that could inform policy making for wildlife importation and ease, Newcastle disease, avian infl uenza). Other animals zoonotic disease surveillance. A total of 246,772 mam- mals in 190 genera (68 families) were imported. The most are typically only screened for physical signs of disease, widespread agents of risk zoonoses were rabies virus (in and pathogen testing is delegated to either the US Depart- 78 genera of mammals), Bacillus anthracis (57), Mycobac- ment of Agriculture (for livestock) or the importer (6). terium tuberculosis complex (48), Echinococcus spp. (41), The process of preimport housing and importation often and Leptospira spp. (35). Genera capable of harboring the involves keeping animals at high density and in unnatural greatest number of risk zoonoses were Canis and Felis (14 groupings of species, providing opportunities for cross- each), Rattus (13), Equus (11), and Macaca and Lepus (10 species transmission and amplifi cation of known and un- each). These fi ndings demonstrate the myriad opportunities known pathogens. Thus, imported wildlife remain a major for zoonotic pathogens to be imported and suggest that, public health threat, as exemplifi ed by the importation of to ensure public safety, immediate proactive changes are Ebola virus in primates from the Philippines (7), monkey- needed at multiple levels. pox from imported African rodents (8), and possibly HIV from chimpanzees in central Africa (9). Wildlife importa- ost emerging infectious diseases are caused by tion also poses a great threat to domestic wildlife and the Mzoonotic pathogens (1,2). The number and propor- US agriculture industry (5). tion of these diseases that originate in wild animals in par- To analyze the volume and diversity of live mammals ticular has increased substantially in the past few decades, that have been imported into the United States in recent even after accounting for increased reports of new emerg- years, we used data from the US Fish and Wildlife Service ing infectious diseases (1). This trend and recent pandem- Law Enforcement Management Information System. We ics of wildlife-origin infectious diseases (e.g., HIV, severe focused on mammals because of the frequency and sever- acute respiratory syndrome) suggest that targeted surveil- ity of previously reported mammal-borne zoonoses and lance efforts should focus on activities that bring humans because of the frequent close association between humans and wildlife in close contact (1,3). and many mammalian species (e.g., as pets). We then as- The United States is among the world’s largest import- sessed the zoonotic diseases that imported mammals are ers of live wild animals (4) and imported >1 billion indi- known to host. Our results may be used to inform policy decisions about wildlife importation and zoonotic disease Author affi liations: World Health Organization, Palikir, Federated surveillance and may alert clinicians to the broad range of States of Micronesia (B.I. Pavlin); and Wildlife Trust, New York, possible zoonoses that may be encountered in patients who New York, USA (L.M. Schloegel, P. Daszak) have been exposed to imported animals. DOI: 10.3201/eid1511.090467 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 11, November 2009 1721 PERSPECTIVE Methods the United States, or it must have the potential for new We used Freedom of Information Act requests to ob- epidemiology with regard to transmission (e.g., Yersinia tain records from the database of the US Fish and Wildlife pestis is presently found in wild rodents in the western Service Law Enforcement Management Information Sys- United States, but it is not expected to be found in animals tem. We obtained records for all wildlife shipments into sold as pets); and 5) if the pathogen uses an intermediate the United States during 2000–2005 through 14 of the 18 vector, competent vectors must exist in the United States. designated animal importation ports (Anchorage, Alaska; The resulting list comprised 30 risk zoonoses (20 viral Atlanta, Georgia; Baltimore, Maryland; Boston, Massachu- diseases, 9 bacterial diseases, and 1 helminthic disease); setts; Chicago, Illinois; Dallas, Texas; Honolulu, Hawaii; no fungal, protozoal, or prion diseases were on the list, Los Angeles, California; Miami, Florida; New Orleans, and thus they were not analyzed. Louisiana; New York, New York; Portland, Oregon; San Determination of the host range of the risk zoonoses Francisco, California; and Seattle, Washington). Data were was accomplished through systematic genus-driven and not available for Houston, Texas; Louisville, Kentucky; pathogen-driven searches of PubMed databases (www. Memphis, Tennessee; and Newark, New Jersey. For each pubmed.gov), the Google search engine (www.google. importation, we acquired information on the taxonomy, com), and references within published works. Confi rmed quantity, source (e.g., wild-caught, farmed), country of presence was defi ned as either isolation of the pathogen origin, intermediate port of call, port of entry, and declared from an animal or serologic evidence of past infection. purpose of all live specimens. Descriptive analyses were For all animals identifi ed in the literature as carrying a risk performed to determine the volume of trade from various zoonosis, genus and family were recorded. The host rang- regions of the world and the types of mammals imported. es of all of the risk zoonoses were then cross-referenced Individual importation events were then grouped into gen- against the imported genera to generate tables showing dis- era to determine the diversity of taxa imported. The phylo- eases found in each imported genus (affected genera). If genetic relationships and geographic ranges of host mam- the disease was found in a different genus within the same mals were determined by using the Animal Diversity Web family, this was also noted (potentially affected genera). at the University of Michigan Museum of Zoology (http:// The justifi cation for this expanded risk assessment is the animaldiversity.ummz.umich.edu/site/index.html). host nonspecifi city of many infectious diseases; lack of evi- We searched the literature to identify the zoonotic dence for the presence of a given disease in a given host pathogens known to occur in animals of each taxon in the should not be construed as evidence against its presence. database. Only data on live animal importations (as opposed to animal products) and importations for which the genus Results was known were retained for analysis. Statistical analyses During 2000–2005, a total of 4,067 shipment fractions were performed by using Intercooled Stata 9 (StataCorp, of mammals were imported (a shipment fraction is the sum College Station, TX, USA). In our fi nal risk assessment, we of all animals of a single species in a given shipment; a did not account for the origin of each specifi c importation single shipment may contain several shipment fractions), because of limitations in the database, likely caused by a totaling 246,772 individual mammals and representing 190 complicated system of exportation and reimportation. genera and 68 families. The average number of animals We created a list of relevant zoonotic diseases at risk per shipment fraction was 61 (range 1–8,000). The most for importation (hereafter referred to as risk zoonoses) by common declared purpose for importation was commercial searching the Centers for Disease Control and Prevention use (not classifi ed according to pet trade, food, traditional website (www.cdc.gov) and the World Health Organiza- medicine, etc.), accounting for 66% (163,760 individuals) tion website (www.who.int), reviewing the list of Select of the total. The second most common declared purpose Agents (agents with bioterrorism potential) of the US De- was biomedical research, accounting for 28% (69,986 in- partment of Health and Human Services (10), and con- dividuals) of the total. Only a small number of individu- sulting experts in the fi eld. To be on the list, diseases had als were imported for breeding, educational, zoo, personal, to meet the following 5 criteria: 1) the pathogen must be and other uses. Numbers of the most commonly imported zoonotic (there must be a recorded instance of infection of animals were 126,014 (>50% of all imported individuals) a human from an animal source); 2) the pathogen must be long-tailed macaques (Macaca fascicularis), 30,058 small capable of causing signifi cant illness or death (e.g., fungal desert hamsters (Phodopus sungorus), 19,724 rhesus ma- skin infections would not be on the list because although caques (Macaca mulatta), 19,537 raccoons (Procyon lo- they are extremely common zoonoses, their effects are tor), and 7,112 chinchillas (Chinchilla lanigera). Together, rarely debilitating); 3) the pathogen must be present in these 5 species accounted for 82% of all imported individu- animals in the wild (i.e., not only in experimental mod- als. By number of shipment fractions, the most common els); 4) the pathogen must not currently be widespread in animals were 1,343 M. fascicularis macaques, 332 Cal- 1722 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 11, November 2009 Importing Zoonotic Diseases through Wildlife Trade lithrix jacchus marmosets, 229 M. mulatta macaques, 165 Table 1. Risk zoonoses and their associated clinical syndromes C. lanigera chinchillas, and 107 Potos fl avus kinkajous.
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