Zoonotic Viruses Associated with Illegally Imported Wildlife Products

et al. (2012) Zoonotic Viruses Associated with Illegally Imported Wildlife Products. PLoS ONE 7(1): e29505. doi:10.1371/journal.pone.0029505 Zoonotic Viruses Associated with Illegally Imported Wildlife Products Kristine M. Smith 0 1 Simon J. Anthony 0 1 William M. Switzer 0 1 Jonathan H. Epstein 0 1 Tracie Seimon 0 1 Hongwei Jia 0 1 Maria D. Sanchez 0 1 Thanh Thao Huynh 0 1 G. Gale Galland 0 1 Sheryl E. Shapiro 0 1 Jonathan M. Sleeman 0 1 Denise McAloose 0 1 Margot Stuchin 0 1 George Amato 0 1 Sergios-Orestis Kolokotronis 0 1 W. Ian Lipkin 0 1 William B. Karesh 0 1 Peter Daszak 0 1 Nina Marano 0 1 Bradley S. Schneider, Global Viral Forecasting Initiative, United States of America 0 Current address: EcoHealth Alliance , New York, New York , United States of America 1 1 Wildlife Conservation Society, Bronx, New York, United States of America , 2 EcoHealth Alliance, New York , New York, United States of America, 3 Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 4 Columbia University , New York , New York, United States of America, 5 Cummings School of Veterinary Medicine, Tufts University , North Grafton , Massachusetts, United States of America, 6 United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, United States of America, 7 Sackler Institute for Comparative Genomics, American Museum of Natural History , New York, New York , United States of America The global trade in wildlife has historically contributed to the emergence and spread of infectious diseases. The United States is the world's largest importer of wildlife and wildlife products, yet minimal pathogen surveillance has precluded assessment of the health risks posed by this practice. This report details the findings of a pilot project to establish surveillance methodology for zoonotic agents in confiscated wildlife products. Initial findings from samples collected at several international airports identified parts originating from nonhuman primate (NHP) and rodent species, including baboon, chimpanzee, mangabey, guenon, green monkey, cane rat and rat. Pathogen screening identified retroviruses (simian foamy virus) and/or herpesviruses (cytomegalovirus and lymphocryptovirus) in the NHP samples. These results are the first demonstration that illegal bushmeat importation into the United States could act as a conduit for pathogen spread, and suggest that implementation of disease surveillance of the wildlife trade will help facilitate prevention of disease emergence. - Funding: Funding for this study was supplied by the V. Kann Rasmussen Foundation, the Consortium for Conservation Medicine, the New York Community Trust, and the Eppley Foundation for Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. . These authors contributed equally to this work. No adequate estimate of numbers of wildlife traded throughout the world exists given the large size and covert nature of the business. Beyond the threats to conservation, the intermingling of wildlife, domestic animals and humans during the process of wildlife extraction, consumption, and trade can serve as a vessel for pathogen exchange [1]. Nearly 75% of emerging infectious diseases in humans are of zoonotic origin, the majority of which originate in wildlife [2,3]. Therefore infectious diseases acquired from contact with wildlife, such as occurs via the wildlife trade, are increasingly of concern to global public health. Trade in live animals and animal products has led to the emergence of several zoonotic pathogens, of which RNA viruses are the most common. SARS emerged as a respiratory and gastrointestinal disease in southwest China and within months had spread to 29 other countries, eventually leading to 8,098 cases and 774 deaths. Masked palm civets (Paguma larvata) traded in the markets of Guangdong were found to be infected and a large proportion of the early cases were restaurant workers who bought and butchered wildlife from these markets [4]. The United States is one of the worlds largest consumers of imported wildlife and wildlife products [5]. Between 2000 and 2006, approximately 1.5 billion live wild animals (around 120,000,000 per year) were legally imported into the United States nearly 90% of which were destined for the pet industry [6], and an average of over 25 million kilograms of non-live wildlife enter the United States each year [5]. New York is the most frequently used port of entry into the United States, and in combination with Los Angeles and Miami accounts for more than half of all known wildlife imports. Imports most often refused entry (i.e., deemed to be illegal) into the United States included those from China, Philippines, Hong Kong, Thailand, and Nigeria [5] countries with endemic pathogens such as highly pathogenic H5N1 influenza virus, Nipah virus, and simian retroviruses. Health risks to the US public, agricultural industry, and native wildlife posed by the wildlife trade have generally not been quantified due to minimal surveillance of live animal imports and the absence of surveillance of wildlife product imports. Despite this, known examples of disease introductions to the United States via the wildlife trade have included pathogens of risk to wildlife, livestock and public health such as amphibian chytridiomycosis, exotic Newcastles disease, and monkeypox, respectively. The monkeypox outbreak showed that a single shipment of infected animals can result in serious impact on public health, highlighting the challenges faced by agencies attempting to regulate both legal and illegal wildlife trade. The USDA regulates certain exotic ruminant species, some birds, some fish, a few species of tortoise, hedgehogs, tenrecs, and brushtail possums for specific foreign animal diseases to protect agricultural health. In general, there is no current remit for USDA to regulate species as potential threats to wildlife or public health. Species restricted by Centers for Disease Control and Prevention (CDC) include certain turtles, NHPs, bats, civets, and African rodents. Hunting and butchering of bushmeat (for the purpose of this paper to be defined according to Oxford Dictionary as the meat of African wild animals) has been increasingly recognized as a source of disease emergence. Harvest of NHP bushmeat and exposure to NHPs in captivity have resulted in cross-species transmission of several retroviruses to humans including simian immunodeficiency virus (SIV), simian T-lymphotropic virus (STLV), and simian foamy virus (SFV) [7,8]. While SIV and STLV adapted to humans and spread to become the global pathogens human immunodeficiency virus (HIV) and human T-lymphotropic virus (HTLV), less is known about the distribution and public health consequences of SFV infection [7]. Much of the bushmeat smuggled i (...truncated)