Figures
Abstract
Background
Research regarding zoonotic diseases often focuses on infectious diseases animals have given to humans. However, an increasing number of reports indicate that humans are transmitting pathogens to animals. Recent examples include methicillin-resistant Staphylococcus aureus, influenza A virus, Cryptosporidium parvum, and Ascaris lumbricoides. The aim of this review was to provide an overview of published literature regarding reverse zoonoses and highlight the need for future work in this area.
Methods
An initial broad literature review yielded 4763 titles, of which 4704 were excluded as not meeting inclusion criteria. After careful screening, 56 articles (from 56 countries over three decades) with documented human-to-animal disease transmission were included in this report.
Findings
In these publications, 21 (38%) pathogens studied were bacterial, 16 (29%) were viral, 12 (21%) were parasitic, and 7 (13%) were fungal, other, or involved multiple pathogens. Effected animals included wildlife (n = 28, 50%), livestock (n = 24, 43%), companion animals (n = 13, 23%), and various other animals or animals not explicitly mentioned (n = 2, 4%). Published reports of reverse zoonoses transmission occurred in every continent except Antarctica therefore indicating a worldwide disease threat.
Interpretation
As we see a global increase in industrial animal production, the rapid movement of humans and animals, and the habitats of humans and wild animals intertwining with great complexity, the future promises more opportunities for humans to cause reverse zoonoses. Scientific research must be conducted in this area to provide a richer understanding of emerging and reemerging disease threats. As a result, multidisciplinary approaches such as One Health will be needed to mitigate these problems.
Citation: Messenger AM, Barnes AN, Gray GC (2014) Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals. PLoS ONE 9(2): e89055. https://doi.org/10.1371/journal.pone.0089055
Editor: Bradley S. Schneider, Metabiota, United States of America
Received: September 24, 2013; Accepted: November 4, 2013; Published: February 28, 2014
Copyright: © 2014 Messenger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the US Armed Forces Health Surveillance Center - Global Emerging Infections Surveillance Operations (multiple grants to GCG) and a supplement from the National Institute of Allergy and Infectious Diseases (R01 AI068803 to GCG). 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.
Introduction
With today's rapid transport systems, modern public health problems are growing increasingly complex. A pathogen that emerges today in one country can easily be transported unnoticed in people, animals, plants, or food products to distant parts of the world in less than 24 hours [1]. This high level of mobility makes tracking and designing interventions against emerging pathogens exceedingly difficult, requiring close international and interdisciplinary collaborations. Fundamental to these efforts is an understanding of the ecology of emerging diseases. Published works often cite the large proportion of human emerging pathogens that originate in animals [2], [3], [4], [5]. However, scientific reports seldom mention human contributions to the variety of emerging diseases that impact animals. The focus of this review is to examine and summarize the scientific literature regarding such zoonoses transmission. A comprehensive table of the results is included in this document.
Methods
For the purpose of this review several terms require definitions. Despite the fact that the term “zoonosis” usually refers to a disease that is transmitted from animals to humans (also called “anthropozoonosis”) [6], in this paper, “zoonosis” was defined as any disease that is transmitted from animals to humans, or vice versa [6], There are two related terms (“zooanthroponosis” and “reverse zoonosis”) that refer to any pathogen normally reservoired in humans that can be transmitted to other vertebrates [6]. Acknowledging that the terms “reverse zoonosis” or “zooanthroponosis” are seldom used, and that the term “zoonosis” can have several meanings, search methods were designed to include all of these terms in an effort to capture the widest possible subset of publications with documented human-to-animal transmission.
Literature search
In June 2012, we searched PubMed in addition to several databases within Web of Knowledge and ProQuest to find articles documenting reverse zoonoses transmission. Search terms included: reverse zoonosis, bidirectional zoonosis, anthroponosis, zooanthroponosis, anthropozoonosis, and human-to-animal disease transmission. Articles were limited to clinical and observational type studies and were restricted to English only. Review articles were not included as they did not demonstrate a specific account of transmission. Letters to editors or similar correspondence were also excluded. Only publications with documented human-to-animal transmission were included. No time period was stipulated.
Four search strings were used for the PubMed database: ((bidirectional OR reverse) AND (zoono* or “disease transmission”)) OR anthropono* OR “human-to-animal”), ((bidirectional OR reverse OR “human-to-animal”) AND (zoono* or “disease transmission”)) OR anthropono*), (“reverse zoonoses” OR “ bidirectional zoonoses” OR “reverse zoonosis” OR “ bidirectional zoonosis” OR “reverse zoonotic” OR “ bidirectional zoonotic” OR anthropono* OR (“human-to-animal” AND disease* AND transmi*)), and (((bidirectional OR reverse OR “human-to-animal”) AND (zoonoses[majr] OR “Disease Transmission, Infectious”[majr] OR zoonosis[tiab] OR zoonoses[tiab] OR zoonotic[tiab])) OR Anthroponos*[tiab] OR Zooanthroponos*[tiab] OR Anthropozoonos*[tiab]). In the ProQuest and Web of Knowledge databases, we only used one string: ((bidirectional OR reverse) AND (zoonosis OR zoonoses OR zoonotic)) OR anthropono* OR Zooanthropono* OR anthropozoono* OR “human-to-animal” OR “human to animal”). The lack of additional search strings for the latter databases was due to less comprehensive search capabilities. Duplicate articles were removed.
Literature analyses
Titles and abstracts were reviewed and articles were retained when there was evidence of disease transmission from humans to animals. During full text review, some citations proved straightforward in distinguishing transmission from humans to animals (e.g. via direct contact), while others were selected based on strong author suggestion or research implications toward reverse zoonotic transmission. In an effort to highlight trends in an otherwise diverse set of articles, citations were grouped by pathogen type and year of publication. To further clarify relationships, we also pictorially displayed the study locations and animal types discussed in the various articles.
Results
This comprehensive literature review yielded 4763 titles, 2507 of which were excluded as duplicates (Figure 1). During the review of abstracts, 2091 studies were excluded due to a lack of evidence of human-to-animal disease transmission. After consideration of the 165 eligible for full text review, 109 studies were excluded based on full texts being written in a language other than English, absence of human-to-animal disease transmission, or full texts being unavailable. After all exclusions, 56 articles were considered for this review (Table 1).
Included reports were based in 56 different countries. Although the reports spanned three decades, there seems to be an increasing number of studies published in recent years (Figure 2). Twenty eight percent of the studies were conducted in the United States (n = 16), 14% in Canada (n = 8), and 13% in Uganda (n = 7) (Figure 3). Within the study results, 21 publications discussed human-to-animal transmission of bacterial pathogens (38%); 16 studies discussed viral pathogens (29%); 12 studies discussed human parasites (21%); and seven studies discussed transmission of fungi, other pathogens, or diseases of multiple etiologies (13%). Bacterial pathogen reports were centered in North America and Europe. Viral studies were well-distributed globally. Parasitic disease reports were conducted chiefly in Africa. Fungal studies were conducted almost exclusively in India (Figure 4).
Note: Many reports identified several countries therefore each country in this figure does not necessarily represent a single corresponding publication.
A. Proportion of reverse zoonoses scientific reports as illustrated by study location and pathogen type; B. Proportion of reverse zoonoses scientific reports on bacterial pathogens as illustrated by study location; C. Proportion of reverse zoonoses scientific reports on viral pathogens as illustrated by study location; D. Proportion of reverse zoonoses scientific reports on parasitic pathogens as illustrated by study location; E. Proportion of reverse zoonoses scientific reports on fungal pathogens as illustrated by study location.
Animals with reported infection or inoculation with human diseases included wildlife (n = 28, 50%), livestock (n = 24, 43%), companion animals (n = 13, 23%), and other animals or animals not explicitly mentioned (n = 2, 4%). The majority of companion and livestock animals were studied in North America and Europe, while wildlife studies were most prevalent in Africa (Table 1, Figure 5). Typically, diagnostic specimens were collected at veterinary hospitals (n = 15, 27%), national parks (n = 8, 14%) and livestock farms (n = 8, 14%). Direct contact was the suggested transmission route 71% of the time (n = 40). Other transmission routes included fomite, oral contact, aerosols, and inoculation.
A. Proportion of reverse zoonoses scientific reports as illustrated by study location and animal(s) infected; B. Proportion of reverse zoonoses scientific reports on companion animals as illustrated by study location; C. Proportion of reverse zoonoses scientific reports on livestock as illustrated by study location; D. Proportion of reverse zoonoses scientific reports on wildlife as illustrated by study location.
As early as 1988, zoonoses research focusing on fungal pathogens was being conducted. Initial studies implied human transmission of Microsporum (n = 2) and Trichophyton (n = 2) to various animal species, with a later article centered on Candida albicans (n = 1) (Figure 2). These publications were set in India (n = 2) and the United States (n = 1).
Since 1988, research with implications of reverse zoonoses has been largely focused on infections of bacterial origin, beginning in 1995. The majority of articles in this review focused on methicillin-resistant Staphylococcus aureus (MRSA) (n = 9) and Mycobacterium tuberculosis (n = 5). Reports regarding these bacteria were primarily conducted in the United States (n = 8) among livestock (n = 10) or companion animals (n = 9).
Viruses were the second most common pathogen associated with human-to-animal transmission. Reverse zoonoses reports regarding viral pathogens began in 1998 and have since been focused primarily on influenza with great interest surrounding the 2009 H1N1 pandemic (n = 9). These studies were conducted largely in the United States (n = 6) in livestock (n = 8) and wildlife (n = 8).
Studies suggestive of transmission of human parasites to animals were first published in 2000. The most commonly reported parasitic agents to be transmitted from humans to animals were Giardia duodenalis (n = 6) and Cryptosporidium parvum (n = 4). Parasitic research has been carried out most frequently in Uganda (n = 4) and Canada (n = 2). The authors investigated human parasitic infections chiefly in wildlife (n = 10) and livestock (n = 5).
Human-to-animal transmission is plausible for a large number of diseases because the pathogens concerned are known to infect multiple species [3]. For instance, 77.3% of the pathogens infecting livestock are considered “multiple species pathogens [3].” However, this review only found 24 reports which considered reverse zoonoses disease transmission as a potential threat to livestock, underscoring a need for further research in this area [3]. Similarly, in companion animals this review found even fewer studies (n = 13) that implied reverse zoonoses as a possible cause of infection, despite the fact that 90% of known pathogens for domestic carnivores are recognized as “multiple species pathogens [3].” The majority of publications in this reverse zoonoses review involved studies documenting human-to-wildlife transmission (n = 28). Unfortunately, they too were severely lacking in comparison to the research need. Each type of animal- livestock, companion, or wildlife, represents a unique set of risk factors for reverse zoonoses through their specific routes of human contact.
Discussion
Human and animal relationships are likely to continue to intensify worldwide over the next several decades due in part to animal husbandry practices, the growth of the companion animal market, climate change and ecosystem disruption, anthropogenic development of habitats, and global travel and commerce [2]. As the human-animal connection escalates, so does the threat for pathogen spread [1], [63]. This review notes a number of factors that influence the risk of disease transmission from humans to animals.
For instance, human population growth and expansion encourages different species to interact in ways and at rates previously not encountered, and to do so in novel geographical areas [4]. The term “pathogen pollution” refers to the process of bringing a foreign disease into a new locality due to human involvement [64]. In the case of the endangered African painted dog, wild dogs have been infected with human strains of Giardia duodenalis, leading researchers to believe that pathogen pollution occurred through open defecation in and around national parks by tourists and local residents [53]. Anthropogenic changes in the ecosystem increase the amount of shared habitats between humans and animals thus exposing both to new pathogens. Researchers discovered the human strain of pandemic Escherichia coli strain 025:H4-ST131 CTX-M-15 in many different species of animals indicating inter-species transmission from humans to pets and livestock [23]. This particular human strain found to be infecting animals was documented across Europe.
In addition to habitat change, growth, and/or destruction, there is the ever-increasing global movement of products and travelers that extends to both humans and animals. During the pandemic of 2009 H1N1 influenza, the novel virus was able to travel across the globe and from humans to swine in less than two months [32]. One driving force behind the movement of animals and animal products is the worldwide shipment of meat. This phenomenon is a relatively new event as developing countries adjust their diets to include more meat- and dairy-based products [4]. While food and animal safety guidelines attempt to keep up with the speed of global trade, international efforts appear to be outpaced by product demand. For example, it has been estimated that five tons of illegal bushmeat pass through Paris' main Roissy-Charles de Gaulle airport each week in personal luggage [65]. However, overt retail systems of animal and animal products can also contribute to the danger of zoonoses and reverse zoonoses transmission. Many animals are sold in markets which allow humans and a myriad of animal species to interact in conditions that are known to trigger emerging diseases [66]. Specifically, this is true for live animal markets and warehouses for exotic pets [4].
The pet industry is an enormous global business that now expands from domestic to exotic animals. A 2011–2012 national pet owners survey found that in the United States alone, 72.9 million homes or 62% of the population have a pet [67]. Of these pets, the majority of animals are dogs (78.2 million) or cats (86.4 million), but a large number of pets are birds (16.2 million), reptiles (13 million), or small animals (16 million) [67]. As pet ownership seems to be increasing worldwide and more exotic pets are being introduced to private homes, the potential for disease transmission between humans and animals will continue to increase. Veterinarians must more fervently protect animals under their care from human disease threats [68]. Adopting a One Health strategy for emerging disease surveillance and reporting will benefit both humans and animals and produce a more collaborative response plan.
Veterinarians, animal health workers, and public health professionals are not the only ones who should recognize the threat of reverse zoonoses. Increased awareness must also be communicated to the general public. Worldwide, there are 1,300 zoos and aquariums that sustain more than 700 million visitors each year [69]. The potential for pathogen spread to animals can come from a visitor with an illness, contamination of a shared environment or food, and the spread of disease through relocation of animals for captivity or educational purposes. In Tanzania, a fatal outbreak of human metapneumovirus in wild chimpanzees is believed to be the result of researchers and visitors viewing the animals in a national park that was once the great apes' territory [30]. Public education and awareness should be augmented to include the potential health threats inflicted on a susceptible animal by an unhealthy human.
This report has limitations. As demonstrated in this review paper, the trend for reporting pathogen spread of human-to-animal is increasing. However the route of human transmission to animal disease manifestation is often unknown in these reports and not well documented in this review. Also the report did not examine articles that did not document human-to-animal transmission. We acknowledge that many additional works that have recorded the existence of human pathogens in animals were not evaluated. However, this review was designed to summarize only the publications that document reverse zoonotic transmission.
Many common and dangerous pathogens have not, to the authors' knowledge, been researched as reverse zoonoses threats to animals representing a significant gap in the scientific literature. Future investigations of reverse zoonoses should take into account both transmission routes and disease prevalence. Prospective research should also include a wider variety of etiological agents and animal species. Scientific literature must document the presence and transmission of human diseases in animals such that the wealth of literature on this subject will become defined and accessible across multiple disciplines. A wider knowledge and understanding of reverse zoonoses should be sought for a successful One Health response. We recommend that future research be conducted on how human disease can, and does, affect the animals around us.
Acknowledgments
The authors especially thank Nancy Schaffer and Jennifer Lyon from the University of Florida Library Sciences for their research assistance.
References
- 1. Wilson ME (2003) The traveller and emerging infections: sentinel, courier, transmitter. J Appl Microbiol 94 Suppl: 1S–11S.
- 2.
Worldbank (2010) People, pathogens and our planet: Volume 1: Towards a one health approach for controlling zoonotic diseases.
- 3. Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc Lond B Biol Sci 356: 991–999.
- 4. Brown C (2004) Emerging zoonoses and pathogens of public health significance–an overview. Rev Sci Tech 23: 435–442.
- 5.
World Health Organization (2010) The FAO-OIE-WHO Collaboration: Tripartite Concept Note: Sharing responsibilities and coordinating global activities to address health risks at the animal-human-ecosystems interfaces. Food and Agriculture Organization, World Organization for Animal Health, World Health Organization.
- 6. Hubalek Z (2003) Emerging human infectious diseases: anthroponoses, zoonoses, and sapronoses. Emerg Infect Dis 9: 403–404.
- 7. Cosivi O, Meslin FX, Daborn CJ, Grange JM (1995) Epidemiology of Mycobacterium bovis infection in animals and humans, with particular reference to Africa. Rev Sci Tech 14: 733–746.
- 8. Seguin JC, Walker RD, Caron JP, Kloos WE, George CG, et al. (1999) Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. J Clin Microbiol 37: 1459–1463.
- 9. Donnelly TM, Behr MJ, Nims LJ (2000) What's your diagnosis? Septicemia in La Mancha goat kids - Apparent reverse zoonotic transmission of Streptococcus pneumoniae. Lab Animal 29: 23–25.
- 10. Nizeyi JB, Innocent RB, Erume J, Kalema G, Cranfield MR, et al. (2001) Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. J Wildl Dis 37: 239–244.
- 11. Michel AL, Venter L, Espie IW, Coetzee ML (2003) Mycobacterium tuberculosis infections in eight species at the National Zoological Gardens of South Africa, 1991–2001. J Zoo Wildl Med 34: 364–370.
- 12. Hackendahl NC, Mawby DI, Bemis DA, Beazley SL (2004) Putative transmission of Mycobacterium tuberculosis infection from a human to a dog. J Am Vet Med Assoc 225: 1573–1577.
- 13. Erwin PC, Bemis DA, Mawby DI, McCombs SB, Sheeler LL, et al. (2004) Mycobacterium tuberculosis transmission from human to canine. Emerg Infect Dis 10: 2258–2210.
- 14. Prasad HK, Singhal A, Mishra A, Shah NP, Katoch VM, et al. (2005) Bovine tuberculosis in India: potential basis for zoonosis. Tuberculosis (Edinb) 85: 421–428.
- 15. Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, et al. (2006) Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol 115: 148–155.
- 16. Morris DO, Mauldin EA, O'Shea K, Shofer FS, Rankin SC (2006) Clinical, microbiological, and molecular characterization of methicillin-resistant Staphylococcus aureus infections of cats. Am J Vet Res 67: 1421–1425.
- 17. Kwon N, Park K, Jung W, Youn H, Lee Y, et al. (2006) Characteristics of methicillin resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet Microbiol 117: 304–312.
- 18. Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol 22: 1600–1607.
- 19. Hsieh J, Chen R, Tsai T, Pan T, Chou C (2008) Phylogenetic analysis of livestock oxacillin-resistant Staphylococcus aureus. Vet Microbiol 126: 234–242.
- 20. Berg S, Firdessa R, Habtamu M, Gadisa E, Mengistu A, et al. (2009) The Burden of Mycobacterial Disease in Ethiopian Cattle: Implications for Public Health. PLoS One 4: e5068–e5068.
- 21. Heller J, Kelly L, Reid SWJ, Mellor DJ (2010) Qualitative Risk Assessment of the Acquisition of Methicillin-Resistant Staphylococcus aureus in Pet Dogs. Risk Anal 30: 458–472.
- 22. Kottler S, Middleton JR, Perry J, Weese JS, Cohn LA (2010) Prevalence of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus Carriage in Three Populations. J Vet Intern Med 24: 132–139.
- 23. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, et al. (2010) Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta-lactamase-producing Escherichia coli among companion animals. J Antimicrob Chemother 65: 651–660.
- 24. Every AL, Selwood L, Castano-Rodriguez N, Lu W, Windsor HM, et al. (2011) Did transmission of Helicobacter pylori from humans cause a disease outbreak in a colony of Stripe-faced Dunnarts (Sminthopsis macroura)? Vet Res 42: 26.
- 25. Lin Y, Barker E, Kislow J, Kaldhone P, Stemper ME, et al. (2011) Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States. Clin Med Res 9: 7–16.
- 26. Rubin JEJ, Chirino-Trejo MM (2011) Antimicrobial susceptibility of canine and human Staphylococcus aureus collected in Saskatoon, Canada. Zoonoses Public Health 58: 454–462.
- 27. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, et al. (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 3.
- 28. Meng X, Halbur PG, Shapiro MS, Sugantha G, Bruna JD, et al. (1998) Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72: 9714–9721.
- 29. Willy ME, Woodward RA, Thornton VB, Wolff AV, Flynn BM, et al. (1999) Management of a measles outbreak among Old World nonhuman primates. Lab Anim Sci 49: 42–48.
- 30. Kaur T, Singh J, Tong SX, Humphrey C, Clevenger D, et al. (2008) Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, western Tanzania. Am J Primatol 70: 755–765.
- 31. Feagins AR, Opriessnig T, Huang YW, Halbur PG, Meng XJ (2008) Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus. J Med Virol 80: 1379–1386.
- 32. Song M, Lee J, Pascua PNQ, Baek Y, Kwon H, et al. (2010) Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J Clin Microbiol 48: 3204–3211.
- 33. Swenson SL, Koster LG, Jenkins-Moore M, Killian ML, DeBess EE, et al. (2010) Natural cases of 2009 pandemic H1N1 Influenza A virus in pet ferrets. J Vet Diagn Invest 22: 784–788.
- 34. Tischer BK, Osterrieder N (2010) Herpesviruses–a zoonotic threat? Vet Microbiol 140: 266–270.
- 35. Abe M, Yamasaki A, Ito N, Mizoguchi T, Asano M, et al. (2010) Molecular characterization of rotaviruses in a Japanese raccoon dog (Nyctereutes procyonoides) and a masked palm civet (Paguma larvata) in Japan. Vet Microbiol 146: 253–259.
- 36. Berhane Y, Ojkic D, Neufeld J, Leith M, Hisanaga T, et al. (2010) Molecular characterization of pandemic H1N1 influenza viruses isolated from turkeys and pathogenicity of a human pH1N1 isolate in turkeys. Avian Dis 54: 1275–1285.
- 37. Poon LL, Mak PW, Li OT, Chan KH, Cheung CL, et al. (2010) Rapid detection of reassortment of pandemic H1N1/2009 influenza virus. Clin Chem 56: 1340–1344.
- 38. Forgie SE, Keenliside J, Wilkinson C, Webby R, Lu P, et al. (2011) Swine outbreak of pandemic influenza A virus on a Canadian research farm supports human-to-swine transmission. Clin Infect Dis 52: 10–18.
- 39. Holyoake PK, Kirkland PD, Davis RJ, Arzey KE, Watson J, et al. (2011) The first identified case of pandemic H1N1 influenza in pigs in Australia. Aust Vet J 89: 427–431.
- 40. Scotch M, Brownstein JS, Vegso S, Galusha D, Rabinowitz P (2011) Human vs. animal outbreaks of the 2009 swine-origin H1N1 influenza A epidemic. Ecohealth 8: 376–380.
- 41. Trevennec K, Leger L, Lyazrhi F, Baudon E, Cheung CY, et al. (2011) Transmission of pandemic influenza H1N1 (2009) in Vietnamese swine in 2009–2010. Influenza Other Respi Viruses
- 42. Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, et al. (2011) Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 85: 10774–10784.
- 43. Crossley B, Hietala S, Hunt T, Benjamin G, Martinez M, et al. (2012) Pandemic (H1N1) 2009 in captive cheetah. Emerg Infect Dis 18: 315–317.
- 44. Sleeman JM, Meader LL, Mudakikwa AB, Foster JW, Patton S (2000) Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J Zoo Wildl Med 31: 322–328.
- 45. Graczyk TK, DaSilva AJ, Cranfield MR, Nizeyi JB, Kalema G, et al. (2001) Cryptosporidium parvum Genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitol Res 87: 368–370.
- 46. Graczyk TK, Bosco-Nizeyi J, da Silva AJ, Moura IN, Pieniazek NJ, et al. (2002) A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol Res 88: 926–931.
- 47. Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RCA, Read C, et al. (2002) Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda. J Parasitol 88: 905–909.
- 48. Guk S, Yong T, Park S, Park J, Chai J (2004) Genotype and animal infectivity of a human isolate of Cryptosporidium parvum in the Republic of Korea. Korean J Parasitol 42: 85–89.
- 49. Noel C, Dufernez F, Gerbod D, Edgcomb VP, Delgado-Viscogliosi P, et al. (2005) Molecular phylogenies of Blastocystis isolates from different hosts: implications for genetic diversity, identification of species, and zoonosis. J Clin Microbiol 43: 348–355.
- 50. Coklin T, Farber J, Parrington L, Dixon B (2007) Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario, Canada. Vet Parasitol 150: 297–305.
- 51. Adejinmi OJ, Ayinmode AB (2008) Preliminary investigation of zooanthroponosis in a Nigerian Zoological Garden. Vet Res (Pakistan) 2: 38–41.
- 52. Teichroeb JA, Kutz SJ, Parkar U, Thompson RCA, Sicotte P (2009) Ecology of the Gastrointestinal Parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: Possible Anthropozoonotic Transmission. Am J Phys Anthropol 140: 498–507.
- 53. Ash A, Lymbery A, Lemon J, Vitali S, Thompson RCA (2010) Molecular epidemiology of Giardia duodenalis in an endangered carnivore - The African painted dog. Vet Parasitol 174: 206–212.
- 54. Johnston AR, Gillespie TR, Rwego IB, McLachlan TL, Kent AD, et al. (2010) Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis 4: e683.
- 55. Dixon B, Parrington L, Cook A, Pintar K, Pollari F, et al. (2011) The potential for zoonotic transmission of Giardia duodenalis and Cryptosporidium spp. from beef and dairy cattle in Ontario, Canada. Vet Parasitol 175: 20–26.
- 56. Jacobs PHP (1988) Dermatophytes that infect animals and humans. Cutis; cutaneous medicine for the practitioner 42: 330–331.
- 57. Pal M, Matsusaka N, Chauhan P (1997) Zooanthroponotic significance of Trichophyton rubrum in a rhesus monkey (Macaca mulatta). Verh. ber. Erkrg. Zootiere 38: 355–358.
- 58. Wrobel L, Whittington JK, Pujol C, Oh S-H, Ruiz MO, et al. (2008) Molecular Phylogenetic Analysis of a Geographically and Temporally Matched Set of Candida albicans Isolates from Humans and Nonmigratory Wildlife in Central Illinois. Eukaryot Cell 7: 1475–1486.
- 59. Sharma DK, Gurudutt J, Singathia R, Lakhotia RL (2009) Zooanthroponosis of Microsporum gypseum infection. Haryana Veterinarian 48: 108–109.
- 60. Epstein JH, Price JT (2009) The significant but understudied impact of pathogen transmission from humans to animals. Mt Sinai J Med 76: 448–455.
- 61. Guyader Fl, Haugarreau L, Miossec L, Dubois E, Pommepuy M (2000) Three-year study to assess human enteric viruses in shellfish. Appl Environ Microbiol 66: 3241–3248.
- 62. Muehlenbein MP, Martinez LA, Lemke AA, Ambu L, Nathan S, et al. (2010) Unhealthy travelers present challenges to sustainable primate ecotourism. Travel Med Infect Dis 8: 169–175.
- 63. DeHart RL (2003) Health issues of air travel. Annu Rev Public Health 24: 133–151.
- 64. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287: 443–449.
- 65. Chaber A-L, Allebone-Webb S, Lignereux Y, Cunningham AA, Marcus Rowcliffe J (2010) The scale of illegal meat importation from Africa to Europe via Paris. Conservation Letters 3: 317–321.
- 66. Fournie G, Pfeiffer DU (2013) Monitoring and controlling disease spread through live animal market networks. Vet J 195: 8–9.
- 67.
American Pet Products Association Pet Industry Market Size & Ownership Statistics.
- 68. Leighton FA (2004) Veterinary medicine and the lifeboat test: a perspective on the social relevance of the veterinary profession in the 21st century. Can Vet J 45: 259–263.
- 69.
World Association of Zoos and Aquariums (2013) Zoos and Aquariums of the World.