key: cord-304909-3wmrjlhy
authors: Wicker, L. V.; Canfield, P. J.; Higgins, D. P.
title: Potential Pathogens Reported in Species of the Family Viverridae and Their Implications for Human and Animal Health
date: 2016-06-30
journal: Zoonoses Public Health
DOI: 10.1111/zph.12290
sha: 
doc_id: 304909
cord_uid: 3wmrjlhy

The Viverridae is a family of nocturnal carnivores including civets, genets and African linsangs. While a list of known organisms isolated from a species is an essential tool for population management, this review represents the first attempt to collate published reports of organisms isolated from viverrids. A wide range of organisms, including 11 viruses, eight bacterial species, one internal arthropod species, representatives from eight genera of protozoan, 21 genera of nematode, seven genera of cestode, eight genera of trematode and six genera of external arthropod (mites, ticks and louse), have been reported in literature spanning over a century of research. Many of these are capable of infecting multiple hosts, including humans. This is of concern given the anthropogenic factors that bring humans and domestic species into close contact with viverrids, facilitating transmission and spillover of organisms between groups. These factors include trade in viverrids for human consumption, captive management in zoos, rescue centres or on commercial breeding farms, and the increasing overlap of free‐ranging viverrid distribution and human settlement.

The family Viverridae is a diverse group of small, nocturnal carnivores, including 34 species of civet, genet and African linsang distributed across Southern Europe, Africa and Asia (Wilson and Reeder, 2005) . Viverrids are commonly exploited for human consumption, being farmed and hunted for their fur, meat, 'civet' scent, to produce civet coffee, or to be kept as zoo animals or pets (Schreiber et al., 1989; Balakrishnan and Sreedevi, 2007; Shepherd and Shepherd, 2010; D'Cruze et al., 2014) . While habitat loss has contributed to historical population declines, hunting for human consumption is considered the most significant threat to their global conservation (Schreiber et al., 1989; Shepherd and Shepherd, 2010 ).

An inventory of organisms known to be associated with a particular species is considered essential baseline information for species management (Munson, 1991) . This information guides rational development of husbandry protocols for captive populations (Hope and Deem, 2006) , facilitates design of surveillance programmes to investigate change in species disease profiles over time (Lonsdorf et al., 2006) and highlights the threatening role infectious diseases might play in endangered species management (Gilbert et al., 2014) . Given the potential for transmission of diseases between wildlife, humans and livestock (Jones et al., 2008) , a complete list of pathogens and indigenous microflora also enables evidence-based risk assessment of human and animal contact with the species in question .

No attempt has yet been made to collate the current knowledge of potential pathogens detected from species within the family Viverridae (Shepherd, 2008; Bongiovanni et al., 2014) despite the family's long history of exploitation for human consumption (Abebe, 2003; Shepherd and Shepherd, 2010) , the management of threatened viverrids for conservation (Roberton et al., 2002) , the peri-urban habitation of many species within the family (King et al., 1993; Ninomiya et al., 2003; Sato et al., 2013) and their susceptibility to a number of important zoonotic pathogens including the novel coronavirus responsible for the outbreak of severe acute respiratory syndrome (SARS) (Guan et al., 2003; Tu, 2004) , rabies virus (Matsumoto et al., 2011) and highly pathogenic avian influenza H5N1 (HPAI H5N1) (Roberton et al., 2006) . While many organisms have been identified in a very wide range of viverrid species globally, this information is scattered throughout the scientific and grey literature. An accessible list of organisms isolated from viverrids does not currently exist.

This review represents the first collation of currently recognized organisms isolated from the Viverridae, derived from an extensive and intensive assessment of the literature. In doing so, it expands on our understanding of viverrid health and the key epidemiological factors of infectious disease involving free living and captive wildlife. More importantly, this review assesses the significance of isolation of organisms from viverrids in terms of the implications for public health. Anthropogenic factors including wildlife trade, the keeping of viverrids in captivity and land use change all encourage increased contact between viverrids and other species, thereby facilitating the transmission and spillover of these organisms between humans, viverrids and other animals.

A systematic review of the scientific literature resulted in this first collation of all organisms previously reported for species from the carnivorous family Viverridae. All available fields of the databases Google scholar, Web of Science, PubMed and Scopus were searched using all possible combinations of the following key terms: 'viverrid*' or 'civet' or 'linsang' or 'binturong' or 'genetta' (the scientific name for the genus Genetta was used to reduce the number of papers on 'genetics' returned by the search), AND 'disease' or 'pathogen' or 'vir*' (to locate both virus and viral) or 'bacteria*' (to locate both bacteria and bacterial) or 'parasit*' (to locate parasite or parasitic) or 'fung*' (to locate both fungus and fungal). No limitations were placed on date of publication. Additional papers were identified by scanning the reference lists and 'cited by' lists of selected papers. For all organisms, complete primary references describing original research were sought.

While this review resulted in important baseline information, a number of limitations are acknowledged. It is undoubtedly incomplete as many more reports are likely to exist in the medical records of zoos and rescue centres that hold viverrids, unavailable to a database literature review. Inaccuracies are also likely included due to the reliance on traditional approaches to identification, such as descriptions of morphology (Nadler and De Leon, 2011) . Increased availability of molecular methods has significantly improved accuracy in the detection and identification of organisms (Bhadury et al., 2008; Thompson et al., 2009) , resulting in a revision of numerous taxonomic trees (Brown-Elliott et al., 2006; Balajee et al., 2009) . Future research may find some organisms listed here no longer considered valid species, and advancing molecular techniques mean that future revision of this list of recognized organisms of Viverridae are inevitable.

A total of 98 peer-reviewed publications reported the identification of organisms from species within the family Viverridae. These included 10 viruses, eight bacterial species, a single internal arthropod species and representatives from 21 genera of nematode, seven genera of cestode, eight genera of trematode, six genera of external arthropod, and eight genera of protozoan, many of which were not identified to species level. These organisms are presented in detail in Tables 1-7. Of the ten viruses reported for Viverridae (Table 1) , three were zoonoses of considerable public health significance. These were the SARS coronavirus (SARS CoV) (Guan et al., 2003; Poon et al., 2005) ; HPAI H5N1 (Roberton et al., 2006; Wu et al., 2013 ) and a number of variants of the rabies virus (Enurah et al., 1988a; Wilde et al., 1991; Tremlett et al., 1994; Nel et al., 2005; Susetya et al., 2008; Pfukenyi et al., 2009; Matsumoto et al., 2011) . Three important viruses of domestic carnivores were also reported, including canine distemper virus (CDV) (Machida et al., 1992; Hur et al., 1999; Chandra et al., 2000; L opez-Peña et al., 2001; Hirama et al., 2004; Chen et al., 2007; Takayama et al., 2009) , feline parvovirus (caused by the feline panleukopenia virus, FPV) (Ikeda et al., 1999; Demeter et al., 2009) and canine parvovirus (CP) (Santos et al., 2009; Xiao-Ying et al., 2011; Duarte et al., 2013) . In more recent years, the use of advanced molecular techniques has enabled the identification of five novel viruses of uncertain significance. These were an orthoreovirus (mammalian reovirus MPC/04) isolated (Guan et al., 2003; Tu, 2004; Kan et al., 2005; Wu et al., 2005; Wang and Eaton, 2007) Family (Enurah et al., 1988a; Wilde et al., 1991; Tremlett et al., 1994; Nel et al., 2005; Susetya et al., 2008b; Pfukenyi et al., 2009; Matsumoto et al., 2011) Ikoma lyssavirus (Machida et al., 1992; Hur et al., 1999; Chandra et al., 2000; L opez-Peña et al., 2001; Hirama et al., 2004; Chen et al., 2007; Takayama et al., 2009; Techangamsuwan et al., 2014) Family from Masked palm civet (Paguma larvata) in China (Shao et al., 2008 (Shao et al., , 2010 ; the ikoma lyssavirus, a novel divergent lyssavirus (Marston et al., 2012) ; two picornaviruses (genet faecal theilovirus (GFTV) and a kobuvirus genotype); and a picobirnavirus (genet faecal picobirnavirus) (Bodewes et al., 2014; ) . Reports of eight bacterial species, all of which are multihost organisms with zoonotic potential, were found (Table 2 ). Nine serovars of Leptospira interrogans, including some known to cause leptospirosis in humans (Mill an et al., 2009) , were cultured (Smith et al., 1961; Tsai et al., 1973) or identified on serology (Mill an et al., 2009; Moinet et al., 2010) , and the gram-negative bacteria Bartonella henselae, responsible for cat scratch fever in humans, was isolated from a wild, peri-urban-dwelling Masked palm civet (Sato et al., 2013) . A number of reports also describe isolation of enteric bacteria from viverrids. These include Salmonella enterica serovar Glostrup (Falade and Durojaiye, 1976) ; Klebsiella pneumoniae (Enurah et al., 1988b) ; and Plesiomonas shigelloides (Bardon, 1999) , an Escherichia coli with a broad antibiotic resistance panel from a captive Masked palm civet (Ahmed et al., 2007) , and Salmonella enterica enterica (serovars Enteritidis, Nagoya and 4,12:I), Yersinia pseudotuberculosis and Campylobacter spp. from peri-urban, free-ranging Masked palm civets (Lee et al., 2011) .

Of the vectorborne protozoans recognized for viverrids (Table 4) , those carried by ticks include Hepatozoon canis (Laird, 1959) and six Babesia spp. (L eger and L eger, 1920; Heisch, 1952; Peenen et al., 1968; Tolosa and Regassa, 2007) . The trypanosomes, Trypanosoma brucei and T. congolense (Njiokou et al., 2006; Tolosa and Regassa, 2007) , and Leishmania donovani, the protozoan responsible for Visceral Leishmaniasis in humans, were reported (Hoogstraal and Heyneman, 1969) .

Species from four genera of non-vector-borne protozoan were reported (Table 4 ). These included the zoonotic intracellular protozoan Toxoplasma gondii (Janitschke and Werner, 1972; Lopes et al., 2011) ; the coccidian Isospora spp. (Colon and Patton, 2013; Su et al., 2013) ; Eimeria spp. (Colon and Patton, 2013) ; and three species of Giardia including Giardia dasi (Abraham, 1962) , G. hegneri (Chu, 1930) and the zoonotic G. duodenalis, one of the few organisms confirmed using molecular (polymerase chain reaction (PCR) on faeces of a captive Common palm civet, Paradoxurus hermaphroditus) rather than morphological techniques (Beck et al., 2011) .

Some of the earliest papers found during this review reported on nematode (roundworm) parasites. Over two centuries of research has reported on nematodes isolated from a very wide range of viverrid species (Table 5) . While many were not identified to species level, nematodes representing 21 genera from 16 families have been reported in 25 published papers. These included Toxocara spp. (Warren, 1972; Maung, 1975; Alvarez et al., 1990; Colon and Patton, 2013; Su et al., 2013) ; Ascaris spp. (Xavier et al., 2000; Ajibade et al., 2010; Pradhan et al., 2011) ; the hookworms Ancylostoma spp. and Uncinaria longespiculum (Baylis, 1933; Chowdhury and Schad, 1972; Coumaranem and Mohan, 2008; Colon and Patton, 2013; Su et al., 2013) ; Strongyloides sp. threadworms (Su et al., 2013) ; Crenosoma sp. lungworms and Viverrostrongylus brauni (Myers and Kuntz, 1969; Asakawa et al., 1986; Colon and Patton, 2013) ; Mammomonogamus sp. (Colon and Patton, 2013) ; Trichuris spp. whipworms (Colon and Patton, 2013; Su et al., 2013) ; Capillaria sp. (Colon and Patton, 2013; Su et al., 2013) ; Rictularia spp. (Baylis, 1928; Chen, 1937; Schmidt and Kuntz, 1967; Kumar et al., 2005; Mahali et al., 2010) , Spirura sp. (Casanova et al., 2000) ; Spirocera sp. and Cyathospirura seurati (Su et al., 2013) ; Physaloptera sp. (Casanova et al., 2000) ; Gnathostoma sp. (probably G. spinigerum) (Colon and Patton, 2013) ; Brugia spp. and Dirofilaria sp. (Edeson and Wilson, 1964; Masbar et al., 1981) ; and Trichinella spp. (Wang et al., 2012) . Nematodes were commonly identified by the examination of morphological features of adult worms, eggs, larvae or oocysts under light microscopy. Only a single reference described the use of molecular diagnostic techniques, in this case PCR and genetic sequencing to accurately identify zoonotic Trichinella spiralis in infected muscle tissue of a Masked palm civet in China (Wang et al., 2012) . Platyhelminthes (flatworms) from two classes (Cestoda and Trematoda), many of which have zoonotic potential, were also reported ( Table 6 ). Cestode tapeworms from four families included Echinococcus sp. and Taenia spp. (Mahannop et al., 1984; Ndiaye et al., 2002; Millan and Casanova, 2007; Lahmar et al., 2009 ); Diplopylidium spp. and Joyeuxiella pasqualei (Casanova et al., 2000; Millan and Casanova, 

Senegal genet (G. senegalensis) Not discussed Sudan (wild) (Hoogstraal and Heyneman, 1969) Z, zoonotic potential acknowledged; M, protozoan affects multiple hosts other than Viverridae. (Chu, 1930; Abraham, 1962; Beck et al., 2011) Z, zoonotic potential acknowledged; M, protozoan affects multiple hosts other than Viverridae. (Schrank et al., 1788; Warren, 1972; Maung, 1975; Alvarez et al., 1990; Casanova et al., 2000; Colon and Patton, 2013; Su et al., 2013) Family (Baylis, 1928; Chen, 1937; Schmidt and Kuntz, 1967; Casanova et al., 2000; Kumar et al., 2005; Mahali et al., 2010) Family (Casanova et al., 2000) 2007); Mesocestoides spp. (Casanova et al., 2000; Su et al., 2013) ; and Spirometra erinaceieuropaei and Diplobothrium sp. (Uchida et al., 2000; Xavier et al., 2000) . Flukes from the class Trematoda reported for viverrids included species from eight genera, in six families. These were as follows: Echinochasmus hangzhouensis and Artyfechinostomum sp. (Xida, 1990; Varadharajan and Kandasamy, 2000) ; Metagonimus yokagawai (Uchida et al., 2000) ; Opisthorchis viverrine and Metorchis albidus (Nicoll, 1927; Casanova et al., 2000) ; Schistosoma japonicum (Carney et al., 1978; He et al., 2001) ; Brachylaema spp. (Baugh, 1962; Casanova et al., 2000) ; and Paragonimus spp. in a wide range of civet species (Chen, 1959; Dissanaike and Paramananthan, 1961; Sachs et al., 1986; Gang et al., 1999; Aka et al., 2009; Colon and Patton, 2013; Su et al., 2013) . The vast majority of platyhelminthes reported for viverrids were identified by examining morphology of different stages within the parasite's life cycle. Only one paper cited the use of a molecular biochemical test, an enzyme-linked immunosorbent assay (ELISA), to identify Echinococcus sp. antigen in Common genet (Genetta genetta) faecal samples from Tunisia (Lahmar et al., 2009) .

Both external and internal arthropods from seven genera, in four families -Sarcoptidae (mites), Ixodidae (ticks), Trichodectidae (chewing lice) and Porocephalidae (pentostomes)were reported for viverrids (Table 7) . The sarcoptid mite, Notoedres cati, a common parasite of domestic and wild felids, was reported for urban-dwelling Masked palm civet in Japan (Ninomiya et al., 2003) . Many species of ixodid tick, most of which are themselves carriers of zoonotic pathogens, were also reported, including Amblyomma testudinarium (Grassman et al., 2004) ; Ixodes ovatus (Tanskul et al., 1983; Robbins et al., 1997) ; a number of Haemaphysalis spp. (Hoogstraal and Trapido, 1966; Hoogstraal, 1971; Tanskul et al., 1983; Tolosa and Regassa, 2007; Mediannikov et al., 2012) ; Rhipicephalus spp. (Grassman et al., 2004; Tolosa and Regassa, 2007) ; Dermacentor tawianensis (Hoogstraal et al., 1986) and D. auratus (Hoogstraal and Wassef, 1985) . The chewing louse, Felicola bengalensis was collected from a wild civet (Changbunjong et al., 2011) , and one internal arthropod parasite, the pentostome Armillifer moniliformis, was reported for a range of civet species (Stabler and Self, 1967; Krishnasamy et al., 1981) . Identification of arthropods was based on morphology of varying life cycle stages of the organisms collected from viverrids.

While previous authors have suggested that very little is known about the pathogens of viverrids (Williams and Thorne, 1996; Shepherd, 2008; Bongiovanni et al., 2014) , this review identified a wide range of viral, bacterial, 

Knowledge of the significance of isolation of an organism for animal health builds on the baseline information provided by a simple inventory of organisms for the species. Observation of clinical signs in infected individuals contributes to our understanding of pathogenicity. Detailed descriptions of clinical signs seen in viverrids were included in a small number of reports, including an investigation into morbidity or mortality in Viverridae (Roberton et al., 2006) , and the documentation of experimental infection of viverrids with SARS CoV (Wu et al., 2005) . However, most (Chen, 1959; Dissanaike and Paramananthan, 1961; Sachs et al., 1986; Gang et al., 1999; Aka et al., 2009; Colon and Patton, 2013; Su et al., 2013) Z, zoonotic potential acknowledged; M, platyhelminth affects multiple hosts other than Viverridae. (Hoogstraal and Trapido, 1966; Hoogstraal, 1971; Tanskul et al., 1983; Tolosa and Regassa, 2007; Mediannikov et al., 2012) Rhipicephalus (Hoogstraal and Wassef, 1985; Hoogstraal et al., 1986) Family (Stabler and Self, 1967; Krishnasamy et al., 1981) Z, zoonotic potential acknowledged; M, arthropod affects multiple hosts other than Viverridae.

reports listed here provide no information on the presence or absence of clinical signs associated with infection, as many document researches carried out on stored biological samples (Moinet et al., 2010) , on samples collected at necropsy (Santos et al., 2009; Duarte et al., 2013) , or on samples, such as faeces, collected opportunistically without seeing the individual animal (Colon and Patton, 2013; Su et al., 2013) . In other reports, including all reported nematodes in viverrids (Table 3) , clinical signs were simply not discussed. In these cases, it is not possible to elucidate whether isolation of these organisms from clinically unwell Viverridae explains the presence of disease, or whether it is simply an incidental finding.

Knowledge of the role a host plays in the life cycle of an organism provides further understanding of the significance of its isolation, and assists in the prevention or management of outbreaks of disease caused by the organism. Viverrids are understood to be infective hosts, capable of transmitting disease, for a small number of organisms. These include the SARS CoV, for which Masked palm civets were important amplification and transmission hosts in the epidemic of respiratory disease caused by the organism in southern China in 2003 (Guan et al., 2003) . Viverrids also transmit the infective life cycle stage of a number of macroparasites including the Sarcoptid mite, Notoedres cati (Ninomiya et al., 2003) and helminthes Toxocara genettae (Sanmartin et al., 1992) , Ancylostoma sp. (Coumaranem and Mohan, 2008) , Rictularia sp. (Schmidt and Kuntz, 1967; Kumar et al., 2005) , Taenia sp. (Mahannop et al., 1984; Millan and Casanova, 2007) and Diplopylidium monoophorum (Millan and Casanova, 2007) . However, for many more, the significance of viverrids as hosts is probably insignificant. For example, wild Common genets are dead end hosts for Leptospira interrogans serovars (Icterohemorragiae and Ballum) (Mill an et al., 2009) ; and Binturong (Arctictus binturong), Small-toothed palm civet (Arctogalidia trivirgata), Masked palm civet, Common palm civet and Otter civet (Cynogale bennettii) are believed to be accidental hosts for the pentostome Armillifer moniliformis (Stabler and Self, 1967; Krishnasamy et al., 1981; ) . In many other cases, the opportunistic identification of organisms from a small sample size, a recognized impediment to disease surveillance in wild species (Stitt et al., 2007) , hampers our ability to understand the role of Viverridae in the organism's life cycle. The amount of useful epidemiological information obtained is particularly limited where a multihost organism, such as the ixodid tick Amblyomma testudinarium, is identified from just one individual viverrid (Grassman et al., 2004) . Positive results obtained through opportunistic sampling of small numbers of individuals remain useful in that they provide information on the presence of potential new carriers for an organism, but further research is required to understand the role that viverrids play in the organism's life cycle, or their significance in the epidemiology of the diseases which they cause.

Some of the organisms listed in this review may be of significance for the conservation of threatened populations of viverrid or other wild carnivores. Canine distemper virus (CDV), feline panleukopenia virus (FPV) and canine parvovirus (CP) ( Table 1 ) are all highly contagious and cause significant morbidity and mortality in susceptible carnivore species. Infected carnivores shed a high viral load in faeces and other bodily secretions (Deem et al., 2000; Steinel et al., 2001) , facilitating environmental contamination and rapid spread of disease. Infection of susceptible animals does not require direct contact as transmission may be via inhalation of aerosolized respiratory secretions or ingestion of contaminated material from the environment (Deem et al., 2000; Steinel et al., 2001) . Spillover of canine distemper virus from the domestic dog has already impacted several wild carnivore populations, including African wild dogs (Lycaon pictus) (Fanshawe et al., 1991) , Santa Catalina Island foxes (Urocyon littoralis catalinae) (Timm et al., 2009) , Black-footed ferrets (Mustela nigripes) (Williams et al., 1988) and Lions (Panthera leo) (Roelke-Parker et al., 1996) , and has been implicated as a significant concern for the conservation of Amur tiger (Panthera tigris altaica) in Russia (Gilbert et al., 2014) . Multihost viruses such as those listed for Viverridae may pose a threat to the conservation of threatened wild viverrids where their distribution overlaps areas inhabited by unvaccinated domestic carnivores, and must be considered in population management, preventative health measures or in case of disease outbreak. Conversely, viverrids themselves may contribute to the maintenance and cycling of pathogens in an environment which, in turn, could threaten the conservation of other endangered species.

In addition to the potential significance for viverrid and other animal health, many of the organisms listed for Viverridae raise concerns for human health. Wild species are a common source or carrier of zoonotic pathogens (Wolfe et al., 2005; Jones et al., 2008) , and there is a growing interest in understanding the host, pathogen and external (environmental and anthropogenic) factors that facilitate their transmission from wild animals to people and other animals (Bengis et al., 2004; Woolhouse and Gowtage-Sequeria, 2005; Greger, 2007; Chomel, 2008; Rhyan and Spraker, 2010) . The vast majority of organisms reported here for viverrids have the capacity to infect a wide range of species a characteristic which, while common amongst pathogens in general -91% of all domestic carnivore pathogens infect more than one host (Cleaveland et al., 2001 )is of concern as it is a significant risk factor for outbreak of disease (Cleaveland et al., 2001; Greger, 2007) . Given the prevalence of multihost organisms reported for viverrids, particularly those with zoonotic potential, an examination of the factors bringing these forest dwelling mammals into unnaturally close proximity with humans is warranted. For the Viverridae, these include the trades (legal and illegal) in wildlife for human consumption, keeping of viverrids in captivity (wildlife farms, zoos or rescue centres), and human contact with free-ranging viverrids in areas where human and viverrid habitation overlap, or from human incursion into wild spaces.

The global wildlife trade is widely regarded as an interface where close contact between humans and wild animals creates an ecosystem favouring disease emergence and expression (Bengis et al., 2004; Kuiken et al., 2005; Karesh et al., 2007; Pavlin et al., 2009; Cutler et al., 2010; Bausch and Schwarz, 2014) . Stressed, sick and injured animals are transported in mixed-species shipments (Bell et al., 2004) to wet markets or other trade nodes where animals are kept in crowded, unhygienic conditions, exposed to both a wide range of other wild and domestic animals for sale (Kan et al., 2005; Woo et al., 2006) , and to potentially immunologically na€ ıve, urban-dwelling wildlife consumers (Swift et al., 2007) . This combination of conditions facilitates emergence, transmission and amplification of pathogens (Greger, 2007) .

Viverrids are frequently encountered in the wildlife trade in Africa and Asia (Shepherd, 2008; Nijman, 2009; Shepherd and Shepherd, 2010) where they are consumed for their meat (Bell et al., 2004; Yang et al., 2007; Van Song, 2008) or utilized in traditional medicines (Kumara and Singh, 2007; Ashwell and Walston, 2008; Tsegaye et al., 2008) . While the number of organisms reported for this animal source (refer to 'Country (source)' column, Tables 1-7) is low compared to other animal sources, this is likely due to the paucity of research in this area rather than a reliable indication of the health of viverrids in the trade, or the potential significance of this source as a concern for public health. In fact, although few in number, all organisms reported for viverrids sourced from the wildlife tradethe SARS coronavirus (Table 1) (Tu, 2004) , an ixodid tick (Table 7) (Robbins et al., 1997) , a Giardia sp. protozoan (Table 4) (Abraham, 1962) , the vectorborne parasite responsible for African sleeping sickness Trypanosoma brucei (Table 3 ) (Njiokou et al., 2006) and a trematode fluke of genus Paragonimus (Table 6) (Chen, 1959) are zoonotic, multihost organisms with the potential to cause considerable socio-economic impact Chan et al., 2013) . In fact, a viverrid played a central role in the pandemic of human respiratory disease caused by one of the most significant diseases to emerge from the wildlife trade system to datethe SARS CoV (Table 1) . Masked palm civets in this crowded, multispecies wet market in southern China were implicated as the main source of infection in humans via exposure to viral particles in bodily fluids aerosolized during slaughter and preparation for human consumption (Guan et al., 2003; WHO, 2004; Li, 2008; Chan et al., 2013) . The socioeconomic impact of this outbreak, which resulted in over 8000 human cases and a fatality rate of 10%, was considerable (Dong et al., 2007; Chan et al., 2013) .

This process of preparation of carcasses for human consumption presents a considerable risk for transmission of disease to and from viverrids (Wang, 2005; Woo et al., 2006) , a risk which is amplified by the illegal nature of much of the wildlife trade, meaning that slaughter and preparation for human consumption frequently occur outside government-regulated slaughterhouses, unbound by official hygiene standards (WCS, 2008) . Any one of the zoonotic pathogens reported for viverrids in this review may be transmitted to humans during this process, but the rabies virus, another significant viral zoonosis commonly reported for viverrids, is one for which this process is a documented transmission risk (Table 1 ). The broad tissue tropism of rabies (Carey and McLean, 1978) facilitates aerosolization and environmental contamination during the butchering of rabid animals, resulting in confirmed cases of transmission to people following slaughter of domestic dog and cat in China and Vietnam (Kureishi et al., 1992; Wertheim et al., 2009; Nguyen et al., 2011) . Given the conditions in which the wildlife trade currently operates, the considerable scale of trade in viverrids and their susceptibility to such a wide range of multihost organisms, it is likely that species from this family could again play a central role in the emergence, amplification and transmission of disease to people within this system (Dong et al., 2007) .

Maintenance of wild species in captivity provides another opportunity for unnatural human-wildlife proximity, facilitating interspecies sharing of organisms (Daszak et al., 2001) . Viverrids are kept in captivity in zoos (Cosson et al., 2007) , conservation breeding programmes for threatened species (Roberton et al., 2002) and, in far greater numbers, on commercial wildlife farms. Civets have traditionally been farmed for their fur (Shi and Hu, 2008) and to supply the demand for 'civet' scent (used in the production of perfume), a practice which drives farming of civets in Ethiopia (Tolosa and Regassa, 2007) and India (Balakrishnan and Sreedevi, 2007) . More recently, farming of civet in Asia has expanded to supply a growing demand for their meat in wildlife restaurants and markets (Patou et al., 2009) . While published data on wildlife farming are scant, the number of individual civets on farms is likely to be large by 2003, 40,000 individual civets were registered on farms in China (Patou et al., 2009) . Another growing industry is the production of civet coffee, where coffee beans are fed to civets and subsequently harvested, undigested, from their faeces. Traditionally collected from the faeces of free-ranging animals in the vicinity of coffee farms, coffee producers are increasingly turning to caged production to satisfy demand for this product, which has the dubious distinction of being the 'world's most expensive coffee' (D'Cruze et al., 2014; Techangamsuwan et al., 2014) .

A wide variety of zoonoses have been reported for captive viverrids (refer to 'Country (source)' columns, Tables 1-7), including the very high profile zoonotic virus HPAI H5N1 (Table 1) . This was confirmed on PCR and serology from a number of Owston's civets (Chrotogale owstoni) which died following an outbreak of respiratory and neurological diseases in a conservation breeding programme in Vietnam (Roberton et al., 2006) . While no evidence of viverrid-to-human transmission of HPAI H5N1 exists, isolation of pathogens with pandemic potential from any mammalian host is significant as it may provide conditions suitable for the virus to adapt to mammalian respiratory epithelial receptors, enabling efficient mammalto-human, and possibly also human-to-human, transmission, paving the way for a potentially devastating pandemic (Rimmelzwaan et al., 2006; Peiris et al., 2007) . Isolation of this virus from captive civets is also significant in that some countries with the highest number of human cases and fatalities due to HPAI H5N1, such as Indonesia, China and Vietnam (WHO, 2015) , overlap with those where civets are also farmed in the greatest numbers (Patou et al., 2009; D'Cruze et al., 2014) , a risk compounded by the poor standards of husbandry and lack of veterinary care reported for wildlife farms (WSPA, 1998; WCS, 2008) . Knowledge of susceptibility to zoonotic pathogens guides the development of appropriate quarantine and biosecurity protocols in captive institutions required to safeguard both human and animal health.

Understanding transmission routes of reported organisms also assists in identifying the practices associated with keeping viverrids in captivity which pose the greatest risk to public health. For many of the organisms reported here for captive civets, including the enterobacteriaceae Klebsiella pneumoniae and Salmonella enterica serovar Glostrup in Nigerian zoos (Falade and Durojaiye, 1976; Enurah et al., 1988b) and Escherichia coli in a Japanese zoo (Ahmed et al., 2007) , the faecal-oral transmission route is common. Appropriate hygiene and husbandry standards can reduce the spread of these organisms amongst animals, and between animals and humans, in captive environments. However, for those workers tasked with the collection of undigested coffee beans from civet faeces in the production of civet coffee (D'Cruze et al., 2014) , they present a significant, ongoing occupational hazard which must be addressed.

Captive viverrids have also been reported as hosts for a number of diseases listed by the World Health Organization (WHO) as 'neglected tropical diseases' (NTD), including rabies in an African civet which displayed neurological signs prior to death (Table 1) (Enurah et al., 1988a) , soiltransmitted helminthiasis (ascarid roundworms in Large Indian civet and Masked palm civets and ancylostome hookworms in Common palm civet and Small Indian civet, Table 5 ) (Baylis, 1933; Ajibade et al., 2010; Pradhan et al., 2011) and human African trypanosomiasis in a farmed African civet (Table 3 ) (Njiokou et al., 2006) . These pathogens are considered 'neglected' because they are poorly studied and commonly ignored by donors, policy makers and public health officials (Maudlin et al., 2009) ; however, they continue to cause widespread morbidity and mortality in the poorer regions of the world (Hotez et al., 2007; WHO, 2010) . Identification of the pathogens responsible for NTDs in captive viverrids contributes to our understanding of potential animal reservoirs for these diseases, knowledge which is vital to the development of interventions aimed at their control or elimination (Zinsstag et al., 2007) .

Ecotourism is a further anthropogenic factor which brings people into contact with free-ranging viverrids, facilitating the cycling of organisms between these groups. As ecotourism, and hence visitation to national parks, expands globally, an increase in human-wildlife contact has led to a corresponding increase in the risk of transmission of disease (Muehlenbein et al., 2008) , a risk which was illustrated in the Serengeti National Park in 2009 when an African civet, showing clinical signs consistent with rabies, bit a child in an unprovoked attack. A novel lyssavirus, the ikoma lyssavirus, was subsequently isolated from the civet (Marston et al., 2012) . Although the pathogenicity of Ikoma Lyssavirus to humans is unknown, and further research is required to understand its prevalence and distribution (Marston et al., 2012) , this case highlighted the risk of disease emergence when immunologically na€ ıve people come into close and unnatural proximity with wild animals.

As human populations expand, and wild spaces are lost, there is an increasing overlap between human habitation and the distribution of wild species, particularly for species which have adapted well to human settlement (Campbell, 2009) . Tolerance of human presence by some viverrids has led to high density urban and peri-urban populations, where they are frequently seen as pests, scavenging food from garbage bins, gardens and orchards, and living in the roofs and wall spaces of houses (Ninomiya et al., 2003; Campbell, 2009) . Direct contact between viverrids and people in an urban environment leading to disease transmission was reported in Japan, where cat scratch fever (caused by the gram-negative bacteria Bartonella henselae) was transmitted to a man via a scratch from a free-ranging Masked palm civet (Table 2) (Sato et al., 2013) . Peri-urban wildlife may also serve as sylvatic reservoirs for zoonotic disease (Weiss and McMichael, 2004) , as reported for African civet, believed to contribute to the maintenance and cycling of the mongoose biotype of the rabies virus (Sabeta et al., 2008) , and Masked palm civet, considered a maintenance host of the enteric pathogens Salmonella, Campylobacter spp. and Yersinia (Table 2) in Japan (Lee et al., 2011) .

While the list of known organisms for viverrids will grow as future work incorporates improved methodology and advanced molecular techniques, this review provides an important baseline inventory of organisms reported for species from the family Viverridae. A number of these have clear and serious implications for viverrid health, and as such, this information facilitates sensible health management of both wild and captive viverrids, and provides a knowledge base from which future research, surveillance programmes and disease outbreak investigations can be developed. As the vast majority of organisms listed here are also capable of infecting a wide range of hosts, including humans, many may also pose a risk to public health. This is of concern given the anthropogenic factors, including trade of viverrids for human consumption, keeping of viverrids in captivity, and land use changes which bring people and other animals into closer contact with the Viverridae than would naturally occur, facilitating transmission and spillover of organisms within and between these groups.

However, gaps remain in our understanding of the significance of isolation for many of the organisms reported for viverrids. Whether due to small sample numbers, or a failure to investigate factors which help to explain the epidemiology of the diseases they cause, we have very little appreciation of the importance of many of these organisms for viverrid, human and other animal health. Future research should utilize larger host sample sizes in a range of environmental settings (wild and captive), investigate the role of viverrids in the life cycle of the organism in question, and consider the significance of known and novel organisms for both human and animal health, rather than simply reporting their presence.

Sustainable Utilization of the African civet (Civettictis civetta) in Ethiopia

On two new species of Giardia parasitic in Indian mammals

Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes

Coprological survey and inventory of animals at Obafemi Awolowo University and University of Ibadan Zoological Gardens

Human paragonimiasis in Africa

New findings on the helminth fauna of the common European genet (Genetta genetta L.) first record of Toxocara genettae Warren, 1972 (Ascarididae) in Europe

Studies on the parasite fauna of Malaysia I. A redescription of Strongylus brauni linstow, 1897, and the establishment of a new genus

An Overview of the Use and Trade of Plants and Animals in Traditional Medicine Systems in Cambodia

Sequence-based identification of Aspergillus, Fusarium, and Mucorales species in the clinical mycology laboratory: where are we and where should we go from here?

Captive breeding of the Small Indian civet Viverricula indica ( E. Geoffroy Saint

Evaluation of the pathogenicity of strains of Plesiomonas shigelloides isolated in animals

Contributions to our knowledge of digenetic trematodes IV

Outbreak of Ebola virus disease in Guinea: where ecology meets economy

1928: LXXII. Some further parasitic worms from Sarawak

A new species of the nematode genus Uncinaria from a sea-lion, with some observations on related species

Prevalence and molecular typing of Giardia spp. in captive mammals at the zoo of Zagreb

Animal origins of SARS coronavirus: possible links with the international trade in small carnivores

The role of wildlife in emerging and re-emerging zoonoses

Evaluation of combined morphological and molecular techniques for marine nematode (Terschellingia spp.) identification

Viral metagenomic analysis of feces of wild small carnivores

Fatal hemorrhagic-necrotizing pancreatitis associated with pancreatic and hepatic lipidosis in an obese Asian palm civet (Paradoxurus hermaphroditus). Asian Pac

Clinical and laboratory features of the Nocardia spp. based on current molecular taxonomy

Proximity in a Ghanaian savanna: human reactions to the African palm civet Nandinia binotata

Rabies antibody prevalence and virus tissue tropism in wild carnivores in Virginia

A mammalian reservoir of Schistosoma japonicum in the Napu Valley

Faunistic and ecological trends on the helminthic community of Genetta genetta Linnaeus, 1758 (Carnivora: Viverridae) in the Iberian Peninsula

Interspecies transmission and emergence of novel viruses: lessons from bats and birds

Canine distemper virus infection in binturongs (Arctictis binturong)

A redescription of Felicola (Paradoxuroecus) bengalensis (Werneck, 1948) (Phthiraptera: Trichodectidae) from a Common palm civet (Paradoxurus hermaphroditus) in Thailand

Some parasitic nematodes from mammals of South China

The occurrence of a new type of Paragonimus and some clinical problems related to lung flukes in China (Annual report 1958)

The Status of Canine Distemper Virus in Wild Carnivore Community in Southern Taiwan

Chapter 11: wildlife zoonoses -emerging and re-emerging zoonoses from wildlife reservoirs

Ancylostoma Ceylanicum: a parasite of man in Calcutta and environs

Giardia hegneri sp. from a Philippine civet cat

Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence

a caprological survey

Genetic diversity of captive binturongs (Arctictis binturong, Viverridae, Carnivora): implications for conservation

Mixed parasitic infection in a captive toddy cat

Public health threat of new, reemerging, and neglected zoonoses in the industrialized world

Anthropogenic environmental change and the emergence of infectious diseases in wildlife

What is the true cost of the world's most expensive coffee?

Canine distemper in terrestrial carnivores: a review

Feline parvovirus infection in an Asian palm civet (Paradoxurus hermaphroditus)

Detection of a novel and highly divergent coronavirus from Asian leopard cats and Chinese ferret badgers in Southern

Snapshot of viral infections in wild carnivores reveals ubiquity of parvovirus and susceptibility of egyptian mongoose to feline panleukopenia virus

The epidemiology of filariasis due to Wuchereria Bancroft and Brugia Malayi

Rabies in a civet cat (Civettictis civetta) in the Jos Zoo, Nigeria

Klebsiella pneumoniae as a cause of pneumonia and septicemia in a civet kitten (Civettictis civetta) in the Jos Zoo

Salmonellae isolated from captive animals in Ibadan, western state of Nigeria

The wild dog-Africa's vanishing carnivore

Survey of natural focuses of paragonimiasis of Guangxi

Estimating the potential impact of Canine Distemper Virus on the Amur tiger population (Panthera tigris altaica) in Russia

Ticks (Acari: ixodidae) parasitizing wild carnivores in Phu Khieo Wildlife Sanctuary

The human/animal interface: emergence and resurgence of zoonotic infectious

Isolation and characterisation of viruses related to the SARS coronavirus from animals in southern China

Host-parasite relationships of Schistosoma japonicum in mammalian hosts

New piroplasms of a genet cat and a groundsquirrel from Kenya

Phylogenetic analysis of the hemagglutinin (H) gene of Canine Distemper Viruses isolated from wild Masked palm civets (Paguma larvata)

Identity, hosts, and distribution of Haemaphysalis (Rhipistoma) canestrinii (Supino) (resurrected), the postulated Asian progenitor of the African Leachi Complex (Ixodoidea: Ixodidae)

Leishmaniasis in the Sudan Republic: 30. Final epidemiologic report

Species described by Supino in 1897 from Burma, with special reference to H. (Rhipistoma) asiaticus

Dermacentor (Indocentor) auratus (Acari: Ixodoidea: Ixodidae): hosts, distribution, and medical importance in tropical Asia

Dermacentor (Indocentor) taiwanensis (Acari: Ixodoidea: Ixodidae): hosts and distribution in Taiwan and southern Japan

Retrospective study of morbidity and mortality of captive jaguars (Panthera onca) in North America

Control of neglected tropical diseases

Canine distemper virus infection in Binturongs (Arctictus binturong)

Serosurvey for selected virus infections of wild carnivores in Taiwan and Vietnam

Untersuchungen € uber die Wirtsspezifit€ at des geschlechtlichen Entwicklungszyklus von Toxoplasma gondii

Global trends in emerging infectious diseases

Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms

Implications of wildlife trade on the movement of Avian Influenza and other infectious diseases

Canid and viverrid rabies viruses in South Africa

The natural infection of wild animals in West Malaysia with nymphs of Armillifer moniliformis (Diesing 1934) Sambon 1922

Public health: Pathogen surveillance in animals

Rictularia sp

Small carnivores of Karnataka: distribution and sight records

Rabies in China: recommendations for control

Echinococcus in the wild carnivores and stray dogs of northern Tunisia: the results of a pilot survey

Malayan protozoa 2. Hepatozoon miller (Sporozoa: Coccidia), with an unusual host record for H.canis (James)

Prevalence of Salmonella, Yersinia and Campylobacter spp. in feral raccoons (Procyon lotor) and Masked palm civets (Paguma larvata) in Japan

Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections

Paragonimiasis: an important food-borne zoonosis in China

Using retrospective health data from the Gombe chimpanzee study to inform future monitoring efforts

High seroprevalence of antibodies to Toxoplasma gondii in wild animals from Portugal

Canine distemper in a genet (Gennetta gennetta), associated with endogenous lipid pneumonia

Canine distemper virus infection in a Masked palm civet (Paguma larvata)

Incidence and seasonal variation of gastro-intestinal parasitic infections in captive carnivores in Nandankanan zoological park

Survey of Intestinal Parasitism in the Exotic Animals at Dusit Zoo

2012: Ikoma lyssavirus, highly divergent novel lyssavirus in an African civet

Blood parasites of wild and domestic animals from South Kalimantan

Novel sylvatic rabies virus variant in endangered Golden palm civet

Neglected and endemic zoonoses

An ascaridoid nematode from a hippopotamus

Spotted fever group rickettsiae in ticks and fleas from the Democratic Republic of the Congo

Helminth parasites of the endangered Iberian lynx (Lynx pardinus) and sympatric carnivores

Leptospirosis in wild and domestic carnivores in natural areas in Andalusia. Spain. Vector Borne Zoonotic Dis

Leptospirosis in free-ranging endangered European Mink (Mustela lutreola) and other small carnivores (mustelidae, Viverridae) from Southwestern France

Perceived vaccination status in ecotourists and risks of anthropozoonoses

Strategies for integrating pathology into single species conservation programs

Nematode parasites of mammals (Dermoptera, Primates, Pholidota, Rodentia, Carnivora, and Artiodactyla) from North Borneo (Malaysia)

Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology

Ultrastructure of spermiogenseis and spermatozoa of Taenia parva Baer, 1926 (Cestoda, Cyclophyllidea, Taeniidae), a parasite of the Common genet (Genetta genetta)

Mongoose rabies in southern Africa: a re-evaluation based on molecular epidemiology

Molecular epidemiology of rabies virus in Vietnam

1927: A reference list of the trematode parasites of man and the primates

An overview of international wildlife trade from Southeast Asia

Notoedric mange in free-ranging Masked palm civets (Paguma larvata) in Japan

Wild fauna as a probable animal reservoir for Trypanosoma brucei gambiense in Cameroon

Low genetic diversity in the Masked palm civet Paguma larvata (Viverridae)

Risk of importing zoonotic diseases through wildlife trade, United States

Hematozoa from mammals of South Vietnam

Avian Influenza Virus (H5N1): a threat to human health

Babesiosis of wild carnivores and ungulates

A retrospective study of wildlife rabies in Zimbabwe

Identification of a novel coronavirus in bats

Preliminary investigation on the parasites of mammals at Padmaja Naidu Himalayan Zoological Park. Darjeeling

Emergence of diseases from wildlife reservoirs

Influenza A Virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts

Two noteworthy collections of ticks (Acari: Ixodida: Ixodidae) from endangered carnivores in the Lao People's Democratic Republic

Management Guidelines for Owston's palm civet, Chrotogale owstoni (Thomas, 1912)

Avian influenza H5N1 in viverrids: implications for wildlife health and conservation

A canine distemper virus epidemic in Serengeti lions (Panthera leo)

Mongoose rabies and the African civet in Zimbabwe

Prevalence of Paragonimus uterobilateralis infection in children in a Liberian village

A scanning electron microscope study of Toxocara genettae Warren 1972 (Ascaridae), with data on morphometric variation. Folia Parasitol

Serologic survey for canine distemper virus and canine parvovirus in free-ranging wild carnivores from Portugal

Small Indian mongooses and Masked palm civets serve as new reservoirs of Bartonella henselae and potential sources of infection for humans

Nematode parasites of Oceanica. II. Redescription of Rictularia whartoni Tubangui, 1931, and notes on other species from Palawan

Verzeichnis der bisher hinl€ anglich bekannten Eingeweidew€ urmer, nebst einer Abhandlung € uber ihre Anverwandtschaft

Weasels, Civets, Mongooses, and their Relatives: An Action Plan for the Conservation of Mustelids and Viverrids

Isolation and identification of a reovirus from Masked civet cats (Paguma Larvata)

Whole genome sequencing of mammalian orthoreovirus MPC/04 strain from Masked civet cats

) with notes on legal protection

The trade in Viverridae and Prionodontidae in Peninsular Malaysia with notes on conservation and legislation

A review of studies on animal reservoirs of the SARS coronavirus

Animal leptospirosis in Malaya: 1. methods, zoogeographical background, and broad analysis of results

The Binturong: a new host for the Nymphs of Armillifer moniliformis (Diesing, 1836)

Parvovirus infections in wild carnivores

Opportunities and obstacles to collecting wildlife disease data for public health purposes: results of a pilot study on Vancouver Island. British Columbia

Leaf swallowing and parasitic infection of the Chinese lesser civet Viverricula indica in northeastern Taiwan

Molecular epidemiology of rabies in Indonesia

Wildlife trade and the emergence of infectious diseases

Pathological and phylogenetic features of prevalent canine distemper viruses in wild Masked palm civets in Japan

A checklist of ticks of Thailand (Acari: Metastigmata: Ixodoidea)

Pathologic and Molecular Virologic Characterization of a Canine Distemper Outbreak in Farmed Civets

Parasite Zoonoses and wildlife: emerging issues

A suspected Canine Distemper epidemic as the cause of a catastrophic decline in Santa Catalina Islan Foxes (Urocyon littoralis catalinae)

The husbandry, welfare and health of captive African civets (Vivera civetica) in western Ethiopa

Disease risk analysis: a tool for primate conservation planning and decision making

Rabies virus typing-preliminary survey in Botswana

A team approach to a disease survey on an aboriginal island (Orchid Island, Taiwan). II. Leptospirosis in man and animals on Lan Yu

Scent-marking by the African civet Civettictis civetta in the Menagesha-Suba State Forest

Antibodies to SARS coronavirus in civets

New host records of Metagonimus yokogawai and Spirometra erinaceieuropaei from the Masked palm civet (Paguma larvata)

Wildlife trading in Vietnam: situation, causes, and solutions

A survey of gastrointestinal parasites of wild animals in captivity in the VOC Park and Mini Zoo. Coimbatore

SARS Co-V infection in a restaurant from a palm civet

Bats, civets and the emergence of SARS

Molecular identification and phylogenetic analysis of Trichinella isolates from different provinces in mainland China

Two new species of Toxocara from viverrid hosts

Commercial Wildlife Farms in Vietnam: A Problem or Solution for Conservation

Social and environmental risk factors in the emergence of infectious diseases

6, e1000044. WHO, 2004: WHO Guidelines for the Global Surveillance of Severe Acute Respiratory Syndrome (SARS)

First WHO Report on Neglected Tropical Diseases: Working to Overcome the Global Impact of Neglected Tropical Diseases

Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1)Reported to WHO

Infectious and parasitic diseases of captive carnivores, with special emphasis on the black-footed ferret (Mustela nigripes)

Canine distemper in Black-footed ferrets (Mustela nigripes) from Wyoming

Bushmeat hunting, deforestation, and prediction of zoonotic disease

Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections

WSPA Report -Civet Farming: An Ethiopian Investigation. World Society for the Protection of Animals

Civets Are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates

Genetic analysis and pathogenicity of an H5N1 avian influenza virus isolated from palm-civet

A coprological survey of parasites of seven mammal groups at Silent Valley National Park. Kerala

Genetic diversity of parvovirus isolates from dogs and wild animals in China

A new species of Echinochasmus parasitic in civet (Trematoda: Echinostomatidae)

Changes in attitudes toward wildlife and wildlife meats in Hunan Province, central China, before and after the severe acute respiratory syndrome outbreak

Human benefits of animal interventions for zoonosis control


