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Open AccessReview

The Current Host Range of Hepatitis E Viruses

Food Animal Health Research Program, Department of Veterinary Preventive Medicine, The Ohio State University College of Veterinary Medicine, Wooster, OH 44691, USA
Viruses 2019, 11(5), 452; https://doi.org/10.3390/v11050452
Received: 24 April 2019 / Revised: 8 May 2019 / Accepted: 14 May 2019 / Published: 17 May 2019
(This article belongs to the Special Issue Hepatitis E Virus)

Abstract

Hepatitis E virus (HEV) is an emerging zoonotic pathogen transmitting both human to human via the fecal oral route and from animals to humans through feces, direct contact, and consumption of contaminated meat products. Understanding the host range of the virus is critical for determining where potential threats to human health may be emerging from and where potential reservoirs for viral persistence in the environment may be hiding. Initially thought to be a human specific disease endemic to developing countries, the identification of swine as a primary host for genotypes 3 and 4 HEV in industrialized countries has begun a long journey of discovering novel strains of HEV and their animal hosts. As we continue identifying new strains of HEV in disparate animal species, it is becoming abundantly clear that HEV has a broad host range and many of these HEV strains can cross between differing animal species. These cross-species transmitting strains pose many unique challenges to human health as they are often unrecognized as sources of viral transmission.
Keywords: hepatitis E virus; HEV; host range; zoonosis; animals; virus transmission hepatitis E virus; HEV; host range; zoonosis; animals; virus transmission

1. Introduction

Hepatitis E virus (HEV) is a single-stranded positive-sense RNA virus thought to be the leading cause of acute viral hepatitis in humans throughout the world [1]. The exact host range of HEV remains muddled, primarily due to the discrete nature of HEV infections. HEV often presents undetectable pathology in infected organisms. Replication levels are typically low and shedding of the virus is sporadic, making the technical and cost to benefit aspects involved in the extensive screening necessary for detecting HEV RNA in all potential host species prohibitive. A single virus serotype among all known strains makes distinguishing infection by differing strains difficult. However, recent data showing newly discovered HEV homologues in fish [2], amphibians [3], moose [4], kestrels [5], and other diverse species suggests the family Hepeviridae might possess a host range with similarity to the Herpesvirales order which include numerous viruses infecting humans and almost all animal species, including insects, fish, mollusks, reptiles, birds, and mammals [6]. The unique aspects of HEV infection might simply hide its full prevalence. As we continue to evolve more efficient and advanced methods to screen for RNA virus populations and expand our HEV phylogenetic trees, we will inevitably find even more members of the Hepeviridae family and their host species, increasing the known host range of the virus.

2. Background and Significance

HEV is a substantial human pathogen. In areas where adequate sanitation and clean water are lacking, such as in the developing world or in areas with geopolitical conflicts, there have been numerous instances of large-scale HEV outbreaks involving tens of thousands of individuals [7,8,9]. As our understanding of HEV has expanded, it is now recognized as an emerging zoonotic disease prevalent throughout the world [10,11]. HEV is increasingly being recognized as a threat to immunocompromised populations, including patients receiving organ transplantations [12,13], infected with human immunodeficiency virus [14], battling cancer [15], among others. Understanding the host range of HEV is critical to identifying potential transmission routes to humans, species that serve as reservoirs of viral persistence in the environment, and as potential hosts where HEV can mutate and become even more virulent.

3. Hepatitis E Virus Host Range

3.1. Factors Determining HEV Host Range

Viral host range is determined by many different factors, both intrinsic and extrinsic. Intrinsic factors to the virus, such as genetic traits encoding advantageous viral proteins, determine its fitness in individual hosts [16]. Intrinsic factors contributing to the host range of HEV include its ability to bind and enter host cells, successful interfacing with the host cell replication machinery, presence of negative regulatory factors, and ability to overcome the host’s innate immune defenses. The ability of HEV to exist as both lipid-associated and naked virus particles likely plays a role in immune system avoidance (enveloped virions) while maintaining stability in the environment (naked virions). The host receptor for HEV remains elusive, possibly complicated by differing entry mechanisms between envelope-associated and naked virions [17]. Without knowing a definitive entry receptor or set of receptors, predicting susceptible hosts through in silico modeling is impossible. Host factors necessary for efficient viral replication remain understudied owing to a lack of robust cell culture systems across differing strains [18]. From a mix of in vitro and in vivo data numerous host cellular proteins are known to be altered during HEV infection. These include host proteins involved in metabolism, cholesterol/lipid metabolism, inflammatory/immune responses, and cytoskeleton/trafficking [19]. HEV is reliant upon the host transcription and translational machinery to replicate and efficiently make viral protein [20]. How open reading frame 1(ORF1)—host protein interactions differ between host cells of differing species has not been studied. Unlike known negative host restriction factors in human immunodeficiency virus replication, such as apolipoprotein B mRNA-editing enzyme 3G (APOBEC-3G) or tripartite motif-containing protein 5 (TRIM 5α) and others [21,22,23], similar restriction factors have yet to be assessed for HEV but may contribute to host range. Finally, the host immune response, both innate and adaptive, likely play roles in limiting the host range of HEV. Species capable of mounting functional and lasting immune responses are less likely to serve as reservoir host species, as HEV appears to be particularly susceptible to host-mediated viral clearance with >98% of human cases self-resolving [24]. Extrinsic factors relating to ecology and epidemiology also play significant roles in HEV host range [16]. Examples of extrinsic factors altering HEV host range include the geographic distribution of HEV isolates. Genotype 1 HEV is predominantly spread throughout Africa, Asia, and the Middle East. Genotype 2 is limited to Africa and Mexico. Genotype 3 is the predominant strain circulating in North America, South America, and Europe but also has been found overlapping with genotype 4 in southern and eastern Asia. Genotype 4 HEV is primarily found in Asia with some overlap in Europe. This geographic limitation is also likely a product of immunological cross-protection by predominant circulating strains. For example, if a region has endemic genotype 1 HEV circulating that region is less likely to find genotype 3 or 4 HEV isolates. This phenomenon is likely due to the timing and probability of initial strain exposure coupled with generation of a cross-protective immune response slowing introduction of different strains to that region [25].

3.2. Serological Detection

When searching for HEV in new animal species there are two primary methods used for detecting hosts exposed to the virus. Serological testing entails searching for host specific antibodies to the HEV capsid protein utilizing methods such as enzyme linked immunosorbent assays (ELISAs). These assays are thought to work well for broad detection of previous or ongoing HEV infections as there has only been a single serotype attributed to HEV [26,27]. Serological analyses have indicated infections with HEV or HEV-related viruses in a broad range of different animal species. Besides humans, HEV antibodies have been detected in farmed domestic animals, companion animals, laboratory animals, wild animals, and even animals from zoological parks. Serological data does require careful interpretation and should be accompanied by corroborating evidence such as detection of RNA. The presence of only a single serotype of HEV does not allow for designation of the HEV strain to which the animal was exposed without further confirmatory tests. Data presented based solely on seropositivity suggests HEV exposure but is not conclusive. Additionally, HEV ELISA assays have been developed independently in many labs with noted variability between lab groups making data difficult to compare between research groups. Finally, there have been reports of HEV positive ELISA results with the serum containing HEV neutralizing antibodies in the apparent absence of HEV genomes throughout the animal’s life [28]. These results suggest the existence of unknown etiological agents that can generate cross-reacting, HEV-neutralizing antibodies in the absence of HEV infection [28]. Finally, the genetic heterogeneity of HEV does not exclude the possibility that divergent strains may have developed a different serotype that has yet to be detected.

3.3. RNA Detection

Utilization of reverse transcription polymerase chain reaction (RT-PCR) to directly detect HEV viral genomes is a critical step to diagnosing HEV infections. RT-PCR coupled with DNA sequencing allows the investigator to distinguish between HEV species and strains by genotyping. Simply detecting HEV RNA in fecal or whole organismal samples is also not a definitive indicator of host range or susceptibility. This is evidenced by detection of genotype 3 HEV RNA in mollusks and from vegetables [29,30]. These organisms are not thought to be true hosts for HEV replication but can become contaminated and harbor infectious virus as a potential pass through vector. The ability to detect HEV RNA in host plasma rather than in fecal samples or coupling RNA positive fecal data with HEV antibody seropositivity is a stronger indicator that a host is indeed susceptible to HEV replication. The only three definitive ways to show an organism is truly susceptible to HEV are to look for negative-stranded RNA replication intermediates in infected tissues, to show cell lines derived from the suspect species are capable of replicating HEV, or via experimental infection by showing viremia and virus shedding can persist longer than initial inoculum passing through the host. Many of these methods are very intrusive to the host species rendering them unable to be performed in totality. Hurdles such as necessary tissue samples being difficult to obtain, cell lines unavailable for many animal species, suspect animals themselves are rare and unavailable for experimental infection, and for other reasons. This leads to most of our knowledge relying on the combination of RNA and antibody detection to suggest a species is potentially a host for HEV infection. Frequent and continuous detection of specific HEV types in the same species crossing different geographical areas clearly indicates a true animal reservoir as exemplified by domestic pigs, wild boars, chickens, and rats. In other animal species where HEV is detected sparsely, this suggests spillover infections rather than a true reservoir host. For many animal species, no systematic studies on HEV infections are available, making many of the animals listed throughout Table 1 potential HEV hosts rather than true hosts. A combination of serology, RNA detection, experimental infection, confirmation of viral replication, and multiple detections of HEV in a specified host should be carefully considered before declaring the animal a true host.

3.4. Orthohepevirus A

3.4.1. Genotypes 1 and 2 Are Believed to Be Restricted to Higher Primates and Thought to Have Adapted Specifically within Humans

Primate species including rhesus monkeys (Macaca mulatta), cynomolgus monkeys (Macaca cynomolgus), chimpanzees (Pan troglodytes), squirrel monkeys (Saimiri sciureus), patas monkeys (Erythrocebus patas), Eastern owl monkeys (Aotus trivergatus), moustached tamarins (Saguinus mystax mystax), and vervet monkeys (Chlorocebus pygerythrus) are susceptible to experimental infection with the Sar-55 (genotype 1) and/or Mex-14 (genotype 2) (Table 1). Genotype 1 HEV is seen as the primary circulating HEV strain causing human disease in the developing world with many full-length viral sequences being deposited in Genbank [31]. However, genotype 2 HEV does currently remain in circulation as a threat to human health having been detected in a recent outbreak in Nigeria [32]. How genotypes 1 and 2 HEV remain endemic in the absence of non-primate animal reservoirs remains unknown. To date, only a single report of genotype 1 HEV infecting outside of a primate species exists. Horses (Equus caballus ferus) in Egypt had an HEV antibody seroprevalence of 13% and 4% of screened samples were HEV RNA positive. Phylogenetic comparison of a 253-bp gene fragment sequence placed these HEV strains within the genotype 1 lineage [33]. Until more thorough analysis of potential secondary host susceptibility is undertaken, genotypes 1 and 2 HEV appear to be limited to higher primates, except in potentially rare instances where close contact of humans with domesticated animals may lead to some crossover exposure and ability of the virus to pass through hosts, such as horses.

3.4.2. Genotype 3

Genotype 3 is the most well-studied strain of zoonotic HEV. The initial discovery of genotype-3 HEV infecting swine (Sus scrofa domestica) within the commercial pork industry completely reshaped the idea of HEV as a solely human pathogen found only infecting humans in underdeveloped countries. Our current understanding of HEV is both as an endemic human pathogen in developing countries and as a zoonotic pathogen spread throughout both the developing and developed world [63,114]. For almost a decade after the discovery of genotype 3 HEV in swine, very few animal hosts were identified. The HEV field focused primarily on primates and porcine hosts as animal reservoirs and as models for studying the disease. Only occasional hints that the HEV host range could potentially span into other species would arise in that decade, such as the serology data for rats [115], dogs (Canis lupis familiaris), cattle (Bos Taurus primigenius), and rodents [44]. The discovery of an ever-increasing range of potential hosts has begun to emerge as our general understanding of HEV has progressed to its consideration as a serious zoonotic pathogen and the technology to detect HEV infections has grown. Genotype 3 strains cross a significant range of mammalian species from the original identification in domestic pigs (Sus scrofa domestica) [63], to a number of species for which humans rely on as agriculturally important species including goats (Capra hircus aegagrus) [68,69], sheep (Ovis aries orientalis) [41,68], rabbits (Oryctologus cuniculus) [66,89,90,91], and horses (Equus caballus ferus) [73]. Genotype 3 strains have also been detected in many wild animal game species such as the wild boar (Sus scrofa) [102,116], deer, including sika deer (Cervus nippon nippon) [102], Yezo deer (Cervus nippon yesoensis) [102,113], Roe deer (Capreolus capreolus) [97,99], red deer (Cervus elaphus) [96,97], and in wild hares such as the European brown hare (Lepus europaeus) [66]. Genotype 3 species have even been noted in such exotic species as the Javan mongoose (Herpestes javanicus) [80,81,82] and even bottlenose dolphins (Tursiops truncatus) [40].
The recent findings that a genotype 3 HEV has been attributed to infection of a bird, the Himalayan griffon (Gyps himalayensis), which was coinfected with Aspergillus [72] suggests that given the right host conditions, genotype 3 HEV can become an opportunistic pathogen even infecting across classes such as Mammalia to Aves. Furthermore, in vitro evidence suggests the hypervariable region within the ORF 1 gene contributes to host range optimization [117]. Additionally, naturally occurring host protein insertions enhance HEV replication in cell lines derived from diverse species [118]. These two pieces of evidence suggest that the actual host range of genotype 3 HEV might be very broad if given the opportunity to infect under the right conditions. As our ability and interest to efficiently screen the viromes of differing species increases, so will the known host range for genotype 3 HEV. Scenarios such as the discovery of genotype 3 rabbit HEV in 2009, proceeding from initial discovery, to recognition as a zoonotic pathogen, and finally development into a beneficial animal model in a short amount of time, may become more commonplace [119]. A current listing of animal species shown to be associated with HEV infection are listed throughout Table 1.

3.4.3. Genotype 4 HEV

Genotye 4 is similar to genotype 3 in that it has proven to be a significant zoonotic pathogen.Unlike genotype 3, genotype 4 HEV primarily appears to be contained to Asia and more recently cases have appeared throughout Europe [120]. Like genotype 3 HEV, genotype 4 was initially discovered in domestic pigs and wild boars which serve as a primary reservoir [116]. Recent work out of China suggests cattle, including yellow cattle (Bos Taurus primigenius) [45], Holstein Frisian cattle (Bos Taurus primigenius) [46], sheep (Ovis aries orientalis) [101], and goats (Capra hircus aegagrus) [71,121] can be infected by genotype 4 HEV and that infectious virus can potentially be inserted into the human food chain through meat and milk from these animals. In addition to these domestic animals, tufted deer (Elaphodus cephalophus) [73], Reeves’ muntjac (Muntiacus reevesi), clouded leopard (Neofilis nebulosa) [73], and the Asiatic black bear (Ursus thibetanus) [36] have tested positive for genotype 4 HEV. In addition to these mammalian species, genotype 4 HEV was detected in two birds in a zoo setting, the crowned crane (Balearica regulorum) and silver pheasant (Lophura nycthemera) [36]. Like genotype 3 HEV, genotype 4 appears to have a broad host range and may infect many different hosts given appropriate opportunity.

3.4.4. Genotypes 5 and 6 HEV

Genotypes 5 and 6 were isolated from wild boar samples in Japan [108,122]. Recent studies have shown that the virus derived from a genotype 5 infectious clone could cause infections in cynomolgus monkeys that were seronegative for HEV [59]. This research suggests that at least genotype 5 HEV is likely a zoonotic threat to humans and suggests genotype 6 should be evaluated for its ability to infect primates.Human screening is also necessary to confirm their susceptibility. The relatively low circulation of the genotype 5 and 6 virus and geographic seclusion to Japan currently makes transmission to humans a rare occurrence.

3.4.5. Genotypes 7 and 8 HEV

Genotypes 7 and 8 are recently discovered HEV strains whose natural reservoirs are dromedary (Camelus dromedaries) and bactrian (Camelus bactrianus) camels, respectively [123]. The discovery of genotype 7 HEV chronically infecting a human liver transplant patient demonstrates the ability of this virus to infect humans [77]. Additionally, genotype 8 HEV positive samples were used to infect cynomolgus macaques which were susceptible to both acute and chronic infection [60]. Genotypes 7 and 8 should therefore be considered potential human pathogens with studies screening for genotype 8 in humans still necessary.

3.5. Orthohepevirus B

Orthohepevirus B, or avian HEV, isolates were first identified as causing hepatic splenomegaly syndrome or big liver and spleen disease in chickens [124]. The avian HEV genome shares ~48% identity with mammalian HEVs [124]. At least four different genotypes of avian HEV have been identified from chickens worldwide: genotype 1 from chickens in Australia, genotype 2 from chickens in the USA, genotype 3 from chickens in Europe and China, and genotype 4 from chickens in Hungary and Taiwan [124,125,126,127,128,129]. An infectious clone of genotype 2 avian HEV was created [130] and has served as an important in vivo animal model system for dissecting mechanisms contributing to HEV replication and immunology and to empirically test host susceptibility. Studies with genotype 2 avian HEV showed it could infect turkeys (Meleagris gallopavo) but not rhesus monkeys or pigs [131]. A recent publication shows that in addition to turkeys; ducks, geese, and rabbits in mixed housing could be infected by genotype 3 avian HEV, raising concerns that some avian HEV strains could cross into mammalian hosts [132]. Of great concern to the commercial poultry industry is discovery of avian HEV strains that appear to correlate with enhanced pathology in chicks causing hepatic hemorrhage rupture syndrome in China [133]. More avian strains of HEV are continuing to be discovered in expanded bird species. Avian HEV isolates have now been discovered in the little egret (Egretta garzetta) with 60–70% identity to genotype 1 avian HEV, the little owl (Athene noctua), song thrush (Turdus philomelos) [134] and feral pigeon (Columba livia domestica) [135]. Even in the United States a sparrow HEV was discovered and showed higher similarity to chicken HEV strains (71–78% and 80% identity) than to little egret HEV (55% and 68% identity) [136]. The host range of Orthohepevirus B remains an emerging field. Currently reported susceptible hosts are listed in Table 2. With more thorough testing of differing avian species potentially many more avian HEV strains and hosts will be discovered.

3.6. Orthohepevirus C

Orthohepevirus C HEV strains were initially detected around the same time as the discovery of swine HEV in 1999 when it was observed that more than 50% of rats within the United States tested positive for anti HEV antibodies [115,138], however, none tested positive for RNA. Lack of HEV RNA was likely due to PCR primer designs based on known Orthohepevirus A sequences and due to the sequence divergence of Orthohepevirus C from Orthohepevirus A strains. More thorough detection methods with broad spectrum PCR primers allowed for detection and eventually sequencing of full-length viral isolates of rat HEV [139,140]. These isolates had approximately 50% or less sequence identity to human and avian HEV strains. Since the discovery of the first sequences of rat HEV, Orthohepevirus C strains have been isolated from many different rat species [139,140,141], mice [142,143], greater bandicoot [134], Asian musk shrews [144], ferrets [145], voles [142,146], and mink [67,147] (Table 3). RNA from Orthohepevirus C-like strains have also been detected in feces from a red fox (Vulpes vulpes) [148], the common kestrel (Falco tinnunculus), and red-footed falcon (Falco vespertinus) [5]. Whether the fox, kestrel, or falcon-associated Orthohepevirus C HEV strains truly infect these host animals or simply pass through from consumed prey, remains debatable. Originally thought as unlikely to pose a threat to infection of higher ordered primates and humans, the recent discovery of a rat HEV strain causing chronic liver disease in a human liver transplant patient [149] greatly increases the urgency to understand this emerging human pathogen. The discovery of zoonotic potential for Orthohepevirus C, which had previously not been able to infect rhesus monkeys [150] experimentally, suggests that greater care is necessary to fully vet infectious potential of newly discovered HEV strains and advocates for revisiting potential host ranges of previously tested HEV strains.

3.7. Orthohepevirus D

Bat hepatitis E virus shares approximately 57.4–64.2% identity to human HEV genotypes 1–4 [156,157]. Bat HEV has been detected in bats from the Hipposideridae, Phyllostomidae, and Vespertilionidae families [156,157,158] (Table 4). Although one full-length bat HEV sequence exists (JQ001749), no infectious clones currently exist. Bat HEV is not thought to transmit to humans due to its sequence divergence from human infecting strains. In addition, over 93,000 pooled human blood donations screened negative for bat HEV antibodies or RNA [157]. Further research, including an infectious clone coupled with experimental animal infections, is necessary to determine the full host range of bat HEV.

3.8. Piscihepevirus

To date the most divergent strain of HEV, cutthroat trout virus (CTV), shares approximately 40% nucleotide identity with genotype 1 HEV, necessitating phylogenetic classification into its own genus, Piscihepevirus, in the Hepeviridae family [2]. CTV has been found in Cutthroat trout (Oncorhynchus clarkii), rainbow trout (Oncorhynchus mykiss), brown trout (Salmo trutta), brook trout (Salvelinus fontinalis), golden trout (Oncorhynchus aguabonita), apache trout (Oncorhynchus apache), and gila trout (Oncorhynchus gilae) and in a single Atlantic salmon (Salmo salar) [160]. Propagation in the CHSE-214 Chinook salmon embryo cell line suggests other salmon and fish species may harbor CTV or related Hepeviruses. The ability of CTV to infect species outside of fish is thought to be unlikely but has not been directly assessed.

4. Conclusions

The host range of HEV is broad and continues to expand as technology and funding allows scientists to continually scan new species for this elusive RNA virus. Careful examination of HEV serological data and correlation of results with confirmatory tests such as viremia, presence of negative-strand RNA replication intermediates, or experimental infection studies should all be considered best practice approaches to identifying true hosts for HEV infection rather than suboptimal or pass-through vector hosts.

Funding

The Ohio State University Discovery Themes Initiative, Infectious Diseases Institute, and Food Animal Health Research Program start up funds.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Teshale, E.H.; Hu, D.J. Hepatitis E: Epidemiology and prevention. World J. Hepatol. 2011, 3, 285–291. [Google Scholar] [CrossRef]
  2. Batts, W.; Yun, S.; Hedrick, R.; Winton, J. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res. 2011, 158, 116–123. [Google Scholar] [CrossRef] [PubMed][Green Version]
  3. Reuter, G.; Boros, A.; Toth, Z.; Kapusinszky, B.; Delwart, E.; Pankovics, P. Detection of a novel RNA virus with hepatitis E virus-like non-structural genome organization in amphibian, agile frog (Rana dalmatina) tadpoles. Infect. Genet. Evol. 2018, 65, 112–116. [Google Scholar] [CrossRef]
  4. Lin, J.; Karlsson, M.; Olofson, A.S.; Belak, S.; Malmsten, J.; Dalin, A.M.; Widen, F.; Norder, H. High prevalence of hepatitis E virus in Swedish moose--a phylogenetic characterization and comparison of the virus from different regions. PLoS ONE 2015, 10, e0122102. [Google Scholar] [CrossRef] [PubMed]
  5. Reuter, G.; Boros, A.; Matics, R.; Kapusinszky, B.; Delwart, E.; Pankovics, P. Divergent hepatitis E virus in birds of prey, common kestrel (Falco tinnunculus) and red-footed falcon (F. vespertinus), Hungary. Infect. Genet. Evol. 2016, 43, 343–346. [Google Scholar] [CrossRef] [PubMed]
  6. Wozniakowski, G.; Samorek-Salamonowicz, E. Animal herpesviruses and their zoonotic potential for cross-species infection. Ann. Agric. Env. Med. 2015, 22, 191–194. [Google Scholar] [CrossRef]
  7. Thomson, K.; Dvorzak, J.; Lagu, J.; Laku, R.; Dineen, B.; Schilperoord, M.; Muita, M.; Gikunju, S.; Waiboci, L.; Fields, B.; et al. Investigation of Hepatitis E Outbreak Among Refugees -- Upper Nile, South Sudan, 2012–2013. MMWR: Morb. Mortal. Wkly. Rep. 2013, 62, 581–586. [Google Scholar]
  8. Spina, A.; Lenglet, A.; Beversluis, D.; de Jong, M.; Vernier, L.; Spencer, C.; Andayi, F.; Kamau, C.; Vollmer, S.; Hogema, B.; et al. A large outbreak of Hepatitis E virus genotype 1 infection in an urban setting in Chad likely linked to household level transmission factors, 2016-2017. PLoS ONE 2017, 12, e0188240. [Google Scholar] [CrossRef]
  9. Teo, C.G. Fatal outbreaks of jaundice in pregnancy and the epidemic history of hepatitis E. Epidemiol. Infect. 2012, 140, 767–787. [Google Scholar] [CrossRef] [PubMed]
  10. Nan, Y.; Wu, C.; Zhao, Q.; Zhou, E.M. Zoonotic Hepatitis E Virus: An Ignored Risk for Public Health. Front. Microbiol. 2017, 8, 2396. [Google Scholar] [CrossRef]
  11. Meng, X.J. Expanding Host Range and Cross-Species Infection of Hepatitis E Virus. PLoS Pathog. 2016, 12, e1005695. [Google Scholar] [CrossRef]
  12. Kamar, N.; Selves, J.; Mansuy, J.M.; Ouezzani, L.; Peron, J.M.; Guitard, J.; Cointault, O.; Esposito, L.; Abravanel, F.; Danjoux, M.; et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N. Engl. J. Med. 2008, 358, 811–817. [Google Scholar] [CrossRef] [PubMed]
  13. Fang, S.Y.; Han, H. Hepatitis E viral infection in solid organ transplant patients. Curr. Opin. Organ. Transpl. 2017, 22, 351–355. [Google Scholar] [CrossRef]
  14. Shrestha, A.; Adhikari, A.; Bhattarai, M.; Rauniyar, R.; Debes, J.D.; Boonstra, A.; Lama, T.K.; Al Mahtab, M.; Butt, A.S.; Akbar, S.M.F.; et al. Prevalence and risk of hepatitis E virus infection in the HIV population of Nepal. Virol. J. 2017, 14, 228. [Google Scholar] [CrossRef][Green Version]
  15. Bai, M.J.; Zhou, N.; Dong, W.; Li, G.X.; Cong, W.; Zhu, X.Q. Seroprevalence and risk factors of hepatitis E virus infection in cancer patients in eastern China. Int. J. Infect. Dis. 2018, 71, 42–47. [Google Scholar] [CrossRef]
  16. McLeish, M.J.; Fraile, A.; Garcia-Arenal, F. Ecological Complexity in Plant Virus Host Range Evolution. Adv. Virus Res. 2018, 101, 293–339. [Google Scholar] [CrossRef] [PubMed]
  17. Yin, X.; Ambardekar, C.; Lu, Y.; Feng, Z. Distinct Entry Mechanisms for Nonenveloped and Quasi-Enveloped Hepatitis E Viruses. J. Virol. 2016, 90, 4232–4242. [Google Scholar] [CrossRef] [PubMed][Green Version]
  18. Meister, T.L.; Bruening, J.; Todt, D.; Steinmann, E. Cell culture systems for the study of hepatitis E virus. Antivir. Res. 2019, 163, 34–49. [Google Scholar] [CrossRef]
  19. Rogee, S.; Le Gall, M.; Chafey, P.; Bouquet, J.; Cordonnier, N.; Frederici, C.; Pavio, N. Quantitative proteomics identifies host factors modulated during acute hepatitis E infection in swine model. J. Virol. 2014. [Google Scholar] [CrossRef] [PubMed]
  20. Subramani, C.; Nair, V.P.; Anang, S.; Mandal, S.D.; Pareek, M.; Kaushik, N.; Srivastava, A.; Saha, S.; Shalimar; Nayak, B.; et al. Host-Virus Protein Interaction Network Reveals the Involvement of Multiple Host Processes in the Life Cycle of Hepatitis E Virus. mSystems 2018, 3. [Google Scholar] [CrossRef]
  21. Stremlau, M.; Owens, C.M.; Perron, M.J.; Kiessling, M.; Autissier, P.; Sodroski, J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427, 848–853. [Google Scholar] [CrossRef]
  22. Neil, S.; Bieniasz, P. Human immunodeficiency virus, restriction factors, and interferon. J. Interferon Cytokine Res. 2009, 29, 569–580. [Google Scholar] [CrossRef] [PubMed]
  23. Ghimire, D.; Rai, M.; Gaur, R. Novel host restriction factors implicated in HIV-1 replication. J. Gen. Virol. 2018, 99, 435–446. [Google Scholar] [CrossRef]
  24. Aggarwal, R. Hepatitis E: Clinical presentation in disease-endemic areas and diagnosis. Semin. Liver Dis. 2013, 33, 30–40. [Google Scholar] [CrossRef]
  25. Sanford, B.J.; Dryman, B.A.; Huang, Y.W.; Feagins, A.R.; Leroith, T.; Meng, X.J. Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res. 2011, 159, 17–22. [Google Scholar] [CrossRef][Green Version]
  26. Guo, H.; Zhou, E.M.; Sun, Z.F.; Meng, X.J.; Halbur, P.G. Identification of B-cell epitopes in the capsid protein of avian hepatitis E virus (avian HEV) that are common to human and swine HEVs or unique to avian HEV. J. Gen. Virol. 2006, 87, 217–223. [Google Scholar] [CrossRef][Green Version]
  27. Meng, X.J. Hepatitis E virus: Animal reservoirs and zoonotic risk. Vet. Microbiol. 2010, 140, 256–265. [Google Scholar] [CrossRef]
  28. Yugo, D.M.; Cossaboom, C.M.; Heffron, C.L.; Huang, Y.W.; Kenney, S.P.; Woolums, A.R.; Hurley, D.J.; Opriessnig, T.; Li, L.; Delwart, E.; et al. Evidence for an unknown agent antigenically related to the hepatitis E virus in dairy cows in the United States. J. Med. Virol. 2019, 91, 677–686. [Google Scholar] [CrossRef] [PubMed]
  29. Brassard, J.; Gagne, M.J.; Genereux, M.; Cote, C. Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl. Environ. Microbiol. 2012, 78, 3763–3766. [Google Scholar] [CrossRef] [PubMed]
  30. Crossan, C.; Baker, P.J.; Craft, J.; Takeuchi, Y.; Dalton, H.R.; Scobie, L. Hepatitis E virus genotype 3 in shellfish, United Kingdom. Emerg. Infect. Dis. 2012, 18, 2085–2087. [Google Scholar] [CrossRef]
  31. Krain, L.J.; Nelson, K.E.; Labrique, A.B. Host immune status and response to hepatitis E virus infection. Clin. Microbiol. Rev. 2014, 27, 139–165. [Google Scholar] [CrossRef]
  32. Wang, B.; Akanbi, O.A.; Harms, D.; Adesina, O.; Osundare, F.A.; Naidoo, D.; Deveaux, I.; Ogundiran, O.; Ugochukwu, U.; Mba, N.; et al. A new hepatitis E virus genotype 2 strain identified from an outbreak in Nigeria, 2017. Virol. J. 2018, 15, 163. [Google Scholar] [CrossRef]
  33. Saad, M.D.; Hussein, H.A.; Bashandy, M.M.; Kamel, H.H.; Earhart, K.C.; Fryauff, D.J.; Younan, M.; Mohamed, A.H. Hepatitis E virus infection in work horses in Egypt. Infect. Genet. Evol. 2007, 7, 368–373. [Google Scholar] [CrossRef]
  34. Doceul, V.; Bagdassarian, E.; Demange, A.; Pavio, N. Zoonotic Hepatitis E Virus: Classification, Animal Reservoirs and Transmission Routes. Viruses 2016, 8, 270. [Google Scholar] [CrossRef]
  35. Dong, C.; Meng, J.; Dai, X.; Liang, J.H.; Feagins, A.R.; Meng, X.J.; Belfiore, N.M.; Bradford, C.; Corn, J.L.; Cray, C.; et al. Restricted enzooticity of hepatitis E virus genotypes 1 to 4 in the United States. J. Clin. Microbiol. 2011, 49, 4164–4172. [Google Scholar] [CrossRef]
  36. Zhang, W.; Shen, Q.; Mou, J.; Yang, Z.B.; Yuan, C.L.; Cui, L.; Zhu, J.G.; Hua, X.G.; Xu, C.M.; Hu, J. Cross-species infection of hepatitis E virus in a zoo-like location, including birds. Epidemiol. Infect. 2008, 136, 1020–1026. [Google Scholar] [CrossRef]
  37. Woo, P.C.; Lau, S.K.; Teng, J.L.; Tsang, A.K.; Joseph, M.; Wong, E.Y.; Tang, Y.; Sivakumar, S.; Xie, J.; Bai, R.; et al. New hepatitis E virus genotype in camels, the Middle East. Emerg. Infect. Dis. 2014, 20, 1044–1048. [Google Scholar] [CrossRef]
  38. Rasche, A.; Saqib, M.; Liljander, A.M.; Bornstein, S.; Zohaib, A.; Renneker, S.; Steinhagen, K.; Wernery, R.; Younan, M.; Gluecks, I.; et al. Hepatitis E Virus Infection in Dromedaries, North and East Africa, United Arab Emirates, and Pakistan, 1983-2015. Emerg. Infect. Dis. 2016, 22, 1249–1252. [Google Scholar] [CrossRef]
  39. Arankalle, V.A.; Goverdhan, M.K.; Banerjee, K. Antibodies against hepatitis E virus in Old World monkeys. J. Viral Hepat. 1994, 1, 125–129. [Google Scholar] [CrossRef]
  40. Montalvo Villalba, M.C.; Cruz Martinez, D.; Ahmad, I.; Rodriguez Lay, L.A.; Bello Corredor, M.; Guevara March, C.; Martinez, L.S.; Martinez-Campo, L.S.; Jameel, S. Hepatitis E virus in bottlenose dolphins Tursiops truncatus. Dis. Aquat. Organ. 2017, 123, 13–18. [Google Scholar] [CrossRef][Green Version]
  41. El-Tras, W.F.; Tayel, A.A.; El-Kady, N.N. Seroprevalence of hepatitis E virus in humans and geographically matched food animals in Egypt. Zoonoses Public Health 2013, 60, 244–251. [Google Scholar] [CrossRef]
  42. Liang, H.; Chen, J.; Xie, J.; Sun, L.; Ji, F.; He, S.; Zheng, Y.; Liang, C.; Zhang, G.; Su, S.; et al. Hepatitis E virus serosurvey among pet dogs and cats in several developed cities in China. PLoS ONE 2014, 9, e98068. [Google Scholar] [CrossRef] [PubMed]
  43. Mochizuki, M.; Ouchi, A.; Kawakami, K.; Ishida, T.; Li, T.C.; Takeda, N.; Ikeda, H.; Tsunemitsu, H. Epidemiological study of hepatitis E virus infection of dogs and cats in Japan. Vet. Rec. 2006, 159, 853–854. [Google Scholar]
  44. Arankalle, V.A.; Joshi, M.V.; Kulkarni, A.M.; Gandhe, S.S.; Chobe, L.P.; Rautmare, S.S.; Mishra, A.C.; Padbidri, V.S. Prevalence of anti-hepatitis E virus antibodies in different Indian animal species. J. Viral Hepat. 2001, 8, 223–227. [Google Scholar] [CrossRef]
  45. Yan, B.; Zhang, L.; Gong, L.; Lv, J.; Feng, Y.; Liu, J.; Song, L.; Xu, Q.; Jiang, M.; Xu, A. Hepatitis E Virus in Yellow Cattle, Shandong, Eastern China. Emerg. Infect. Dis. 2016, 22, 2211–2212. [Google Scholar] [CrossRef][Green Version]
  46. Huang, F.; Li, Y.; Yu, W.; Jing, S.; Wang, J.; Long, F.; He, Z.; Yang, C.; Bi, Y.; Cao, W.; et al. Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis. Hepatology 2016, 64, 350–359. [Google Scholar] [CrossRef] [PubMed][Green Version]
  47. Yu, C.; Boon, D.; McDonald, S.L.; Myers, T.G.; Tomioka, K.; Nguyen, H.; Engle, R.E.; Govindarajan, S.; Emerson, S.U.; Purcell, R.H. Pathogenesis of hepatitis E virus and hepatitis C virus in chimpanzees: Similarities and differences. J. Virol. 2010, 84, 11264–11278. [Google Scholar] [CrossRef]
  48. Arankalle, V.A.; Ticehurst, J.; Sreenivasan, M.A.; Kapikian, A.Z.; Popper, H.; Pavri, K.M.; Purcell, R.H. Aetiological association of a virus-like particle with enterically transmitted non-A, non-B hepatitis. Lancet 1988, 1, 550–554. [Google Scholar] [CrossRef]
  49. Meng, X.J.; Halbur, P.G.; Shapiro, M.S.; Govindarajan, S.; Bruna, J.D.; Mushahwar, I.K.; Purcell, R.H.; Emerson, S.U. Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J. Virol. 1998, 72, 9714–9721. [Google Scholar] [PubMed]
  50. Yugo, D.M.; Cossaboom, C.M.; Meng, X.J. Naturally occurring animal models of human hepatitis E virus infection. ILAR J. 2014, 55, 187–199. [Google Scholar] [CrossRef] [PubMed]
  51. Zhou, C.; Li, W.; Yang, S. Analysis of hepatitis e virus-like sequence in chimpanzee. Hepat. Mon. 2014, 14, e19473. [Google Scholar] [CrossRef] [PubMed]
  52. Spahr, C.; Knauf-Witzens, T.; Vahlenkamp, T.; Ulrich, R.G.; Johne, R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health 2018, 65, 11–29. [Google Scholar] [CrossRef]
  53. Li, T.C.; Miyamura, T.; Takeda, N. Detection of hepatitis E virus RNA from the bivalve Yamato-Shijimi (Corbicula japonica) in Japan. Am. J. Trop. Med. Hyg. 2007, 76, 170–172. [Google Scholar] [CrossRef] [PubMed]
  54. Balayan, M.S.; Andjaparidze, A.G.; Savinskaya, S.S.; Ketiladze, E.S.; Braginsky, D.M.; Savinov, A.P.; Poleschuk, V.F. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 1983, 20, 23–31. [Google Scholar]
  55. Tsarev, S.A.; Tsareva, T.S.; Emerson, S.U.; Govindarajan, S.; Shapiro, M.; Gerin, J.L.; Purcell, R.H. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc. Natl. Acad. Sci. USA 1994, 91, 10198–10202. [Google Scholar] [CrossRef]
  56. Bradley, D.W.; Krawczynski, K.; Cook, E.H., Jr.; McCaustland, K.A.; Humphrey, C.D.; Spelbring, J.E.; Myint, H.; Maynard, J.E. Enterically transmitted non-A, non-B hepatitis: Serial passage of disease in cynomolgus macaques and tamarins and recovery of disease-associated 27- to 34-nm viruslike particles. Proc. Natl. Acad. Sci. USA 1987, 84, 6277–6281. [Google Scholar] [CrossRef] [PubMed]
  57. Aggarwal, R.; Kamili, S.; Spelbring, J.; Krawczynski, K. Experimental studies on subclinical hepatitis E virus infection in cynomolgus macaques. J. Infect. Dis. 2001, 184, 1380–1385. [Google Scholar] [CrossRef]
  58. de Carvalho, L.G.; Marchevsky, R.S.; dos Santos, D.R.; de Oliveira, J.M.; de Paula, V.S.; Lopes, L.M.; Van der Poel, W.H.; Gonzalez, J.E.; Munne, M.S.; Moran, J.; et al. Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis. BMC Infect. Dis. 2013, 13, 495. [Google Scholar] [CrossRef]
  59. Li, T.C.; Bai, H.; Yoshizaki, S.; Ami, Y.; Suzaki, Y.; Doan, Y.H.; Takahashi, K.; Mishiro, S.; Takeda, N.; Wakita, T. Genotype 5 Hepatitis E Virus Produced by a Reverse Genetics System Has the Potential for Zoonotic Infection. Hepatol. Commun. 2019, 3, 160–172. [Google Scholar] [CrossRef]
  60. Wang, L.; Teng, J.L.; Lau, S.K.P.; Sridhar, S.; Fu, H.; Gong, W.; Li, M.; Xu, Q.; He, Y.; Zhuang, H.; et al. Transmission of A Novel Genotype Hepatitis E Virus from Bactrian Camels to Cynomolgus Macaques. J. Virol. 2019. [Google Scholar] [CrossRef]
  61. Liu, J.; Zhang, W.; Shen, Q.; Yang, S.; Huang, F.; Li, P.; Guo, X.; Yang, Z.; Cui, L.; Zhu, J.; et al. Prevalence of antibody to hepatitis E virus among pet dogs in the Jiang-Zhe area of China. Scand. J. Infect. Dis. 2009, 41, 291–295. [Google Scholar] [CrossRef]
  62. McElroy, A.; Hiraide, R.; Bexfield, N.; Jalal, H.; Brownlie, J.; Goodfellow, I.; Caddy, S.L. Detection of Hepatitis E Virus Antibodies in Dogs in the United Kingdom. PLoS ONE 2015, 10, e0128703. [Google Scholar] [CrossRef]
  63. Meng, X.J.; Purcell, R.H.; Halbur, P.G.; Lehman, J.R.; Webb, D.M.; Tsareva, T.S.; Haynes, J.S.; Thacker, B.J.; Emerson, S.U. A novel virus in swine is closely related to the human hepatitis E virus. Proc. Natl. Acad. Sci. USA 1997, 94, 9860–9865. [Google Scholar] [CrossRef][Green Version]
  64. Garcia-Bocanegra, I.; Rivero, A.; Caballero-Gomez, J.; Lopez-Lopez, P.; Cano-Terriza, D.; Frias, M.; Jimenez-Ruiz, S.; Risalde, M.A.; Gomez-Villamandos, J.C.; Rivero-Juarez, A. Hepatitis E virus infection in equines in Spain. Transbound. Emerg. Dis. 2019, 66, 66–71. [Google Scholar] [CrossRef]
  65. Ticehurst, J.; Rhodes, L.L., Jr.; Krawczynski, K.; Asher, L.V.; Engler, W.F.; Mensing, T.L.; Caudill, J.D.; Sjogren, M.H.; Hoke, C.H., Jr.; LeDuc, J.W.; et al. Infection of owl monkeys (Aotus trivirgatus) and cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus from Mexico. J. Infect. Dis. 1992, 165, 835–845. [Google Scholar] [CrossRef]
  66. Hammerschmidt, F.; Schwaiger, K.; Dahnert, L.; Vina-Rodriguez, A.; Hoper, D.; Gareis, M.; Groschup, M.H.; Eiden, M. Hepatitis E virus in wild rabbits and European brown hares in Germany. Zoonoses Public Health 2017, 64, 612–622. [Google Scholar] [CrossRef]
  67. Xie, X.T.; Macdonald, R.E.; Tapscott, B.; Nagy, E.; Turner, P.V. Detection of Astrovirus, Rotavirus C, and Hepatitis E Viral RNA in Adult and Juvenile Farmed Mink (Neovison vison). Front. Vet. Sci 2018, 5, 132. [Google Scholar] [CrossRef]
  68. Peralta, B.; Casas, M.; de Deus, N.; Martin, M.; Ortuno, A.; Perez-Martin, E.; Pina, S.; Mateu, E. Anti-HEV antibodies in domestic animal species and rodents from Spain using a genotype 3-based ELISA. Vet. Microbiol. 2009, 137, 66–73. [Google Scholar] [CrossRef][Green Version]
  69. Sanford, B.J.; Emerson, S.U.; Purcell, R.H.; Engle, R.E.; Dryman, B.A.; Cecere, T.E.; Buechner-Maxwell, V.; Sponenberg, D.P.; Meng, X.J. Serological evidence for a hepatitis e virus-related agent in goats in the United States. Transbound. Emerg. Dis. 2013, 60, 538–545. [Google Scholar] [CrossRef]
  70. Di Martino, B.; Di Profio, F.; Melegari, I.; Sarchese, V.; Robetto, S.; Marsilio, F.; Martella, V. Detection of hepatitis E virus (HEV) in goats. Virus Res. 2016, 225, 69–72. [Google Scholar] [CrossRef]
  71. Li, S.; Liu, M.; Cong, J.; Zhou, Y.; Miao, Z. Detection and Characterization of Hepatitis E Virus in Goats at Slaughterhouse in Tai’an Region, China. BioMed Res. Int. 2017, 2017, 3723650. [Google Scholar] [CrossRef]
  72. Li, H.; Zhu, R.; She, R.; Zhang, C.; Shi, R.; Li, W.; Du, F.; Wu, Q.; Hu, F.; Zhang, Y.; et al. Case Report Associated with Aspergillosis and Hepatitis E Virus Coinfection in Himalayan Griffons. BioMed Res. Int. 2015, 2015, 287315. [Google Scholar] [CrossRef]
  73. Zhang, W.; Shen, Q.; Mou, J.; Gong, G.; Yang, Z.; Cui, L.; Zhu, J.; Ju, G.; Hua, X. Hepatitis E virus infection among domestic animals in eastern China. Zoonoses Public Health 2008, 55, 291–298. [Google Scholar] [CrossRef]
  74. Arankalle, V.A.; Paranjape, S.; Emerson, S.U.; Purcell, R.H.; Walimbe, A.M. Phylogenetic analysis of hepatitis E virus isolates from India (1976-1993). J. Gen. Virol. 1999, 80, 1691–1700. [Google Scholar] [CrossRef]
  75. Huang, C.C.; Nguyen, D.; Fernandez, J.; Yun, K.Y.; Fry, K.E.; Bradley, D.W.; Tam, A.W.; Reyes, G.R. Molecular cloning and sequencing of the Mexico isolate of hepatitis E virus (HEV). Virology 1992, 191, 550–558. [Google Scholar] [CrossRef]
  76. Hsieh, S.Y.; Meng, X.J.; Wu, Y.H.; Liu, S.T.; Tam, A.W.; Lin, D.Y.; Liaw, Y.F. Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus. J. Clin. Microbiol. 1999, 37, 3828–3834. [Google Scholar]
  77. Lee, G.H.; Tan, B.H.; Teo, E.C.; Lim, S.G.; Dan, Y.Y.; Wee, A.; Aw, P.P.; Zhu, Y.; Hibberd, M.L.; Tan, C.K.; et al. Chronic Infection With Camelid Hepatitis E Virus in a Liver Transplant Recipient Who Regularly Consumes Camel Meat and Milk. Gastroenterology 2016, 150, 355–357.e353. [Google Scholar] [CrossRef] [PubMed]
  78. Yamamoto, H.; Suzuki, J.; Matsuda, A.; Ishida, T.; Ami, Y.; Suzaki, Y.; Adachi, I.; Wakita, T.; Takeda, N.; Li, T.C. Hepatitis E virus outbreak in monkey facility, Japan. Emerg. Infect. Dis. 2012, 18, 2032–2034. [Google Scholar] [CrossRef]
  79. Xia, J.; Zeng, H.; Liu, L.; Zhang, Y.; Liu, P.; Geng, J.; Wang, L.; Wang, L.; Zhuang, H. Swine and rabbits are the main reservoirs of hepatitis E virus in China: Detection of HEV RNA in feces of farmed and wild animals. Arch. Virol. 2015, 160, 2791–2798. [Google Scholar] [CrossRef]
  80. Li, T.C.; Saito, M.; Ogura, G.; Ishibashi, O.; Miyamura, T.; Takeda, N. Serologic evidence for hepatitis E virus infection in mongoose. Am. J. Trop. Med. Hyg. 2006, 74, 932–936. [Google Scholar] [CrossRef]
  81. Nakamura, M.; Takahashi, K.; Taira, K.; Taira, M.; Ohno, A.; Sakugawa, H.; Arai, M.; Mishiro, S. Hepatitis E virus infection in wild mongooses of Okinawa, Japan: Demonstration of anti-HEV antibodies and a full-genome nucleotide sequence. Hepatol. Res. 2006, 34, 137–140. [Google Scholar] [CrossRef]
  82. Nidaira, M.; Takahashi, K.; Ogura, G.; Taira, K.; Okano, S.; Kudaka, J.; Itokazu, K.; Mishiro, S.; Nakamura, M. Detection and phylogenetic analysis of hepatitis E viruses from mongooses in Okinawa, Japan. J. Vet. Med. Sci. 2012, 74, 1665–1668. [Google Scholar] [CrossRef] [PubMed]
  83. Liu, T.; Xiao, P.; Li, R.; She, R.; Tian, J.; Wang, J.; Mao, J.; Yin, J.; Shi, R. Increased Mast Cell Activation in Mongolian Gerbils Infected by Hepatitis E Virus. Front. Microbiol 2018, 9, 2226. [Google Scholar] [CrossRef]
  84. O’Hara, Z.; Crossan, C.; Craft, J.; Scobie, L. First Report of the Presence of Hepatitis E Virus in Scottish-Harvested Shellfish Purchased at Retail Level. Food Env. Virol. 2018, 10, 217–221. [Google Scholar] [CrossRef][Green Version]
  85. Krog, J.S.; Larsen, L.E.; Schultz, A.C. Enteric porcine viruses in farmed shellfish in Denmark. Int. J. Food Microbiol. 2014, 186, 105–109. [Google Scholar] [CrossRef][Green Version]
  86. Diez-Valcarce, M.; Kokkinos, P.; Soderberg, K.; Bouwknegt, M.; Willems, K.; de Roda-Husman, A.M.; von Bonsdorff, C.H.; Bellou, M.; Hernandez, M.; Maunula, L.; et al. Occurrence of human enteric viruses in commercial mussels at retail level in three European countries. Food Env. Virol. 2012, 4, 73–80. [Google Scholar] [CrossRef]
  87. Kanai, Y.; Miyasaka, S.; Uyama, S.; Kawami, S.; Kato-Mori, Y.; Tsujikawa, M.; Yunoki, M.; Nishiyama, S.; Ikuta, K.; Hagiwara, K. Hepatitis E virus in Norway rats (Rattus norvegicus) captured around a pig farm. BMC Res. Notes 2012, 5, 4. [Google Scholar] [CrossRef]
  88. Lack, J.B.; Volk, K.; Van Den Bussche, R.A. Hepatitis E virus genotype 3 in wild rats, United States. Emerg. Infect. Dis. 2012, 18, 1268–1273. [Google Scholar] [CrossRef]
  89. Cossaboom, C.M.; Cordoba, L.; Dryman, B.A.; Meng, X.J. Hepatitis E virus in rabbits, Virginia, USA. Emerg. Infect. Dis. 2011, 17, 2047–2049. [Google Scholar] [CrossRef]
  90. Izopet, J.; Dubois, M.; Bertagnoli, S.; Lhomme, S.; Marchandeau, S.; Boucher, S.; Kamar, N.; Abravanel, F.; Guerin, J.L. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis. 2012, 18, 1274–1281. [Google Scholar] [CrossRef]
  91. Caruso, C.; Modesto, P.; Prato, R.; Scaglione, F.E.; De Marco, L.; Bollo, E.; Acutis, P.L.; Masoero, L.; Peletto, S. Hepatitis E Virus: First Description in a Pet House Rabbit. A New Transmission Route for Human? Transbound. Emerg. Dis. 2015, 62, 229–232. [Google Scholar] [CrossRef] [PubMed]
  92. Birke, L.; Cormier, S.A.; You, D.; Stout, R.W.; Clement, C.; Johnson, M.; Thompson, H. Hepatitis E antibodies in laboratory rabbits from 2 US vendors. Emerg. Infect. Dis. 2014, 20, 693–696. [Google Scholar] [CrossRef] [PubMed]
  93. Zhao, C.; Ma, Z.; Harrison, T.J.; Feng, R.; Zhang, C.; Qiao, Z.; Fan, J.; Ma, H.; Li, M.; Song, A.; et al. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J. Med. Virol. 2009, 81, 1371–1379. [Google Scholar] [CrossRef] [PubMed]
  94. Geng, J.; Wang, L.; Wang, X.; Fu, H.; Bu, Q.; Zhu, Y.; Zhuang, H. Study on prevalence and genotype of hepatitis E virus isolated from Rex Rabbits in Beijing, China. J. Viral Hepat. 2011, 18, 661–667. [Google Scholar] [CrossRef] [PubMed]
  95. Dahnert, L.; Conraths, F.J.; Reimer, N.; Groschup, M.H.; Eiden, M. Molecular and serological surveillance of Hepatitis E virus in wild and domestic carnivores in Brandenburg, Germany. Transbound. Emerg. Dis. 2018, 65, 1377–1380. [Google Scholar] [CrossRef]
  96. Forgach, P.; Nowotny, N.; Erdelyi, K.; Boncz, A.; Zentai, J.; Szucs, G.; Reuter, G.; Bakonyi, T. Detection of hepatitis E virus in samples of animal origin collected in Hungary. Vet. Microbiol. 2010, 143, 106–116. [Google Scholar] [CrossRef] [PubMed]
  97. Anheyer-Behmenburg, H.E.; Szabo, K.; Schotte, U.; Binder, A.; Klein, G.; Johne, R. Hepatitis E Virus in Wild Boars and Spillover Infection in Red and Roe Deer, Germany, 2013-2015. Emerg. Infect. Dis. 2017, 23, 130–133. [Google Scholar] [CrossRef] [PubMed]
  98. Huang, F.; Yu, W.; Hua, X.; Jing, S.; Zeng, W.; He, Z. Seroepidemiology and molecular characterization of hepatitis E Virus in Macaca mulatta from a village in Yunnan, China, where infection with this virus is endemic. Hepat. Mon. 2011, 11, 745–749. [Google Scholar] [CrossRef]
  99. Reuter, G.; Fodor, D.; Forgach, P.; Katai, A.; Szucs, G. Characterization and zoonotic potential of endemic hepatitis E virus (HEV) strains in humans and animals in Hungary. J. Clin. Virol. 2009, 44, 277–281. [Google Scholar] [CrossRef]
  100. Sarchese, V.; Di Profio, F.; Melegari, I.; Palombieri, A.; Sanchez, S.B.; Arbuatti, A.; Ciuffetelli, M.; Marsilio, F.; Martella, V.; Di Martino, B. Hepatitis E virus in sheep in Italy. Transbound. Emerg. Dis. 2019. [Google Scholar] [CrossRef] [PubMed]
  101. Wu, J.; Si, F.; Jiang, C.; Li, T.; Jin, M. Molecular detection of hepatitis E virus in sheep from southern Xinjiang, China. Virus Genes 2015, 50, 410–417. [Google Scholar] [CrossRef] [PubMed][Green Version]
  102. Sonoda, H.; Abe, M.; Sugimoto, T.; Sato, Y.; Bando, M.; Fukui, E.; Mizuo, H.; Takahashi, M.; Nishizawa, T.; Okamoto, H. Prevalence of hepatitis E virus (HEV) Infection in wild boars and deer and genetic identification of a genotype 3 HEV from a boar in Japan. J. Clin. Microbiol. 2004, 42, 5371–5374. [Google Scholar] [CrossRef] [PubMed]
  103. Lin, J.; Norder, H.; Uhlhorn, H.; Belak, S.; Widen, F. Novel hepatitis E like virus found in Swedish moose. J. Gen. Virol. 2014, 95, 557–570. [Google Scholar] [CrossRef]
  104. De Deus, N.; Peralta, B.; Pina, S.; Allepuz, A.; Mateu, E.; Vidal, D.; Ruiz-Fons, F.; Martin, M.; Gortazar, C.; Segales, J. Epidemiological study of hepatitis E virus infection in European wild boars (Sus scrofa) in Spain. Vet. Microbiol. 2008, 129, 163–170. [Google Scholar] [CrossRef] [PubMed]
  105. Adlhoch, C.; Wolf, A.; Meisel, H.; Kaiser, M.; Ellerbrok, H.; Pauli, G. High HEV presence in four different wild boar populations in East and West Germany. Vet. Microbiol. 2009, 139, 270–278. [Google Scholar] [CrossRef] [PubMed][Green Version]
  106. Wiratsudakul, A.; Sariya, L.; Prompiram, P.; Tantawet, S.; Suraruangchai, D.; Sedwisai, P.; Sangkachai, N.; Suksai, P.; Ratanakorn, P. Detection and phylogenetic characterization of hepatitis E virus genotype 3 in a captive wild boar in Thailand. J. Zoo Wildl Med. 2012, 43, 640–644. [Google Scholar] [CrossRef]
  107. Kaci, S.; Nockler, K.; Johne, R. Detection of hepatitis E virus in archived German wild boar serum samples. Vet. Microbiol. 2008, 128, 380–385. [Google Scholar] [CrossRef][Green Version]
  108. Takahashi, M.; Nishizawa, T.; Sato, H.; Sato, Y.; Jirintai; Nagashima, S.; Okamoto, H. Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J. Gen. Virol. 2011, 92, 902–908. [Google Scholar] [CrossRef][Green Version]
  109. Takahashi, M.; Nishizawa, T.; Nagashima, S.; Jirintai, S.; Kawakami, M.; Sonoda, Y.; Suzuki, T.; Yamamoto, S.; Shigemoto, K.; Ashida, K.; et al. Molecular characterization of a novel hepatitis E virus (HEV) strain obtained from a wild boar in Japan that is highly divergent from the previously recognized HEV strains. Virus Res. 2014, 180, 59–69. [Google Scholar] [CrossRef]
  110. Larska, M.; Krzysiak, M.K.; Jablonski, A.; Kesik, J.; Bednarski, M.; Rola, J. Hepatitis E virus antibody prevalence in wildlife in Poland. Zoonoses Public Health 2015, 62, 105–110. [Google Scholar] [CrossRef]
  111. Carpentier, A.; Chaussade, H.; Rigaud, E.; Rodriguez, J.; Berthault, C.; Boue, F.; Tognon, M.; Touze, A.; Garcia-Bonnet, N.; Choutet, P.; et al. High hepatitis E virus seroprevalence in forestry workers and in wild boars in France. J. Clin. Microbiol. 2012, 50, 2888–2893. [Google Scholar] [CrossRef]
  112. Xu, F.; Pan, Y.; Baloch, A.R.; Tian, L.; Wang, M.; Na, W.; Ding, L.; Zeng, Q. Hepatitis E virus genotype 4 in yak, northwestern China. Emerg. Infect. Dis. 2014, 20, 2182–2184. [Google Scholar] [CrossRef] [PubMed]
  113. Tomiyama, D.; Inoue, E.; Osawa, Y.; Okazaki, K. Serological evidence of infection with hepatitis E virus among wild Yezo-deer, Cervus nippon yesoensis, in Hokkaido, Japan. J. Viral Hepat. 2009, 16, 524–528. [Google Scholar] [CrossRef]
  114. Meng, X.J. Novel strains of hepatitis E virus identified from humans and other animal species: Is hepatitis E a zoonosis? J. Hepatol. 2000, 33, 842–845. [Google Scholar] [CrossRef]
  115. Kabrane-Lazizi, Y.; Fine, J.B.; Elm, J.; Glass, G.E.; Higa, H.; Diwan, A.; Gibbs, C.J., Jr.; Meng, X.J.; Emerson, S.U.; Purcell, R.H. Evidence for widespread infection of wild rats with hepatitis E virus in the United States. Am. J. Trop. Med. Hyg. 1999, 61, 331–335. [Google Scholar] [CrossRef]
  116. Pavio, N.; Meng, X.J.; Renou, C. Zoonotic hepatitis E: Animal reservoirs and emerging risks. Vet. Res. 2010, 41, 46. [Google Scholar] [CrossRef] [PubMed]
  117. Pudupakam, R.S.; Kenney, S.P.; Cordoba, L.; Huang, Y.W.; Dryman, B.A.; Leroith, T.; Pierson, F.W.; Meng, X.J. Mutational analysis of the hypervariable region of hepatitis E virus reveals its involvement in the efficiency of viral RNA replication. J. Virol. 2011, 85, 10031–10040. [Google Scholar] [CrossRef] [PubMed]
  118. Shukla, P.; Nguyen, H.T.; Torian, U.; Engle, R.E.; Faulk, K.; Dalton, H.R.; Bendall, R.P.; Keane, F.E.; Purcell, R.H.; Emerson, S.U. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc. Natl. Acad. Sci. USA 2011, 108, 2438–2443. [Google Scholar] [CrossRef] [PubMed]
  119. Wang, L.; Liu, L.; Wang, L. An overview: Rabbit hepatitis E virus (HEV) and rabbit providing an animal model for HEV study. Rev. Med. Virol. 2018, 28. [Google Scholar] [CrossRef] [PubMed]
  120. Forni, D.; Cagliani, R.; Clerici, M.; Sironi, M. Origin and dispersal of Hepatitis E virus. Emerg. Microbes Infect 2018, 7, 11. [Google Scholar] [CrossRef]
  121. Long, F.; Yu, W.; Yang, C.; Wang, J.; Li, Y.; Li, Y.; Huang, F. High prevalence of hepatitis E virus infection in goats. J. Med. Virol. 2017, 89, 1981–1987. [Google Scholar] [CrossRef] [PubMed]
  122. Takahashi, M.; Tamura, K.; Hoshino, Y.; Nagashima, S.; Yazaki, Y.; Mizuo, H.; Iwamoto, S.; Okayama, M.; Nakamura, Y.; Kajii, E.; et al. A nationwide survey of hepatitis E virus infection in the general population of Japan. J. Med. Virol. 2010, 82, 271–281. [Google Scholar] [CrossRef]
  123. Sridhar, S.; Teng, J.L.L.; Chiu, T.H.; Lau, S.K.P.; Woo, P.C.Y. Hepatitis E Virus Genotypes and Evolution: Emergence of Camel Hepatitis E Variants. Int. J. Mol. Sci. 2017, 18, 869. [Google Scholar] [CrossRef] [PubMed]
  124. Haqshenas, G.; Shivaprasad, H.L.; Woolcock, P.R.; Read, D.H.; Meng, X.J. Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States. J. Gen. Virol. 2001, 82, 2449–2462. [Google Scholar] [CrossRef] [PubMed]
  125. Banyai, K.; Toth, A.G.; Ivanics, E.; Glavits, R.; Szentpali-Gavaller, K.; Dan, A. Putative novel genotype of avian hepatitis E virus, Hungary, 2010. Emerg. Infect. Dis. 2012, 18, 1365–1368. [Google Scholar] [CrossRef] [PubMed]
  126. Bilic, I.; Jaskulska, B.; Basic, A.; Morrow, C.J.; Hess, M. Sequence analysis and comparison of avian hepatitis E viruses from Australia and Europe indicate the existence of different genotypes. J. Gen. Virol. 2009, 90, 863–873. [Google Scholar] [CrossRef][Green Version]
  127. Hsu, I.W.; Tsai, H.J. Avian hepatitis E virus in chickens, Taiwan, 2013. Emerg. Infect. Dis. 2014, 20, 149–151. [Google Scholar] [CrossRef] [PubMed]
  128. Marek, A.; Bilic, I.; Prokofieva, I.; Hess, M. Phylogenetic analysis of avian hepatitis E virus samples from European and Australian chicken flocks supports the existence of a different genus within the Hepeviridae comprising at least three different genotypes. Vet. Microbiol. 2010, 145, 54–61. [Google Scholar] [CrossRef]
  129. Zhao, Q.; Zhou, E.M.; Dong, S.W.; Qiu, H.K.; Zhang, L.; Hu, S.B.; Zhao, F.F.; Jiang, S.J.; Sun, Y.N. Analysis of avian hepatitis E virus from chickens, China. Emerg. Infect. Dis. 2010, 16, 1469–1472. [Google Scholar] [CrossRef]
  130. Huang, F.F.; Pierson, F.W.; Toth, T.E.; Meng, X.J. Construction and characterization of infectious cDNA clones of a chicken strain of hepatitis E virus (HEV), avian HEV. J. Gen. Virol. 2005, 86, 2585–2593. [Google Scholar] [CrossRef][Green Version]
  131. Sun, Z.F.; Larsen, C.T.; Huang, F.F.; Billam, P.; Pierson, F.W.; Toth, T.E.; Meng, X.J. Generation and infectivity titration of an infectious stock of avian hepatitis E virus (HEV) in chickens and cross-species infection of turkeys with avian HEV. J. Clin. Microbiol. 2004, 42, 2658–2662. [Google Scholar] [CrossRef] [PubMed]
  132. Liu, B.; Fan, M.; Zhang, B.; Chen, Y.; Sun, Y.; Du, T.; Nan, Y.; Zhou, E.M.; Zhao, Q. Avian hepatitis E virus infection of duck, goose, and rabbit in northwest China. Emerg. Microbes Infect. 2018, 7, 76. [Google Scholar] [CrossRef]
  133. Su, Q.; Li, Y.; Meng, F.; Cui, Z.; Chang, S.; Zhao, P. Hepatic rupture hemorrhage syndrome in chickens caused by a novel genotype avian hepatitis E virus. Vet. Microbiol. 2018, 222, 91–97. [Google Scholar] [CrossRef]
  134. Li, W.; Guan, D.; Su, J.; Takeda, N.; Wakita, T.; Li, T.C.; Ke, C.W. High prevalence of rat hepatitis E virus in wild rats in China. Vet. Microbiol. 2013, 165, 275–280. [Google Scholar] [CrossRef] [PubMed]
  135. Zhang, X.; Bilic, I.; Troxler, S.; Hess, M. Evidence of genotypes 1 and 3 of avian hepatitis E virus in wild birds. Virus Res. 2017, 228, 75–78. [Google Scholar] [CrossRef] [PubMed]
  136. Yang, C.; Wang, L.; Shen, H.; Zheng, Y.; Gauger, P.C.; Chen, Q.; Zhang, J.; Yoon, K.J.; Harmon, K.M.; Main, R.G.; et al. Detection and genomic characterization of new avian-like hepatitis E virus in a sparrow in the United States. Arch. Virol. 2018, 163, 2861–2864. [Google Scholar] [CrossRef]
  137. Reuter, G.; Boros, A.; Matics, R.; Kapusinszky, B.; Delwart, E.; Pankovics, P. A novel avian-like hepatitis E virus in wild aquatic bird, little egret (Egretta garzetta), in Hungary. Infect. Genet. Evol. 2016, 46, 74–77. [Google Scholar] [CrossRef]
  138. Easterbrook, J.D.; Kaplan, J.B.; Vanasco, N.B.; Reeves, W.K.; Purcell, R.H.; Kosoy, M.Y.; Glass, G.E.; Watson, J.; Klein, S.L. A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiol. Infect. 2007, 135, 1192–1199. [Google Scholar] [CrossRef] [PubMed][Green Version]
  139. Johne, R.; Plenge-Bonig, A.; Hess, M.; Ulrich, R.G.; Reetz, J.; Schielke, A. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J. Gen. Virol. 2010, 91, 750–758. [Google Scholar] [CrossRef] [PubMed]
  140. Johne, R.; Heckel, G.; Plenge-Bonig, A.; Kindler, E.; Maresch, C.; Reetz, J.; Schielke, A.; Ulrich, R.G. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg. Infect. Dis. 2010, 16, 1452–1455. [Google Scholar] [CrossRef]
  141. Li, T.C.; Yoshizaki, S.; Ami, Y.; Suzaki, Y.; Yasuda, S.P.; Yoshimatsu, K.; Arikawa, J.; Takeda, N.; Wakita, T. Susceptibility of laboratory rats against genotypes 1, 3, 4, and rat hepatitis E viruses. Vet. Microbiol. 2013, 163, 54–61. [Google Scholar] [CrossRef]
  142. Wang, B.; Li, W.; Zhou, J.H.; Li, B.; Zhang, W.; Yang, W.H.; Pan, H.; Wang, L.X.; Bock, C.T.; Shi, Z.L.; et al. Chevrier’s Field Mouse (Apodemus chevrieri) and Pere David’s Vole (Eothenomys melanogaster) in China Carry Orthohepeviruses that form Two Putative Novel Genotypes Within the Species Orthohepevirus C. Virol. Sin. 2018, 33, 44–58. [Google Scholar] [CrossRef]
  143. de Souza, W.M.; Romeiro, M.F.; Sabino-Santos, G., Jr.; Maia, F.G.M.; Fumagalli, M.J.; Modha, S.; Nunes, M.R.T.; Murcia, P.R.; Figueiredo, L.T.M. Novel orthohepeviruses in wild rodents from Sao Paulo State, Brazil. Virology 2018, 519, 12–16. [Google Scholar] [CrossRef]
  144. Guan, D.; Li, W.; Su, J.; Fang, L.; Takeda, N.; Wakita, T.; Li, T.C.; Ke, C. Asian musk shrew as a reservoir of rat hepatitis E virus, China. Emerg. Infect. Dis. 2013, 19, 1341–1343. [Google Scholar] [CrossRef]
  145. Raj, V.S.; Smits, S.L.; Pas, S.D.; Provacia, L.B.; Moorman-Roest, H.; Osterhaus, A.D.; Haagmans, B.L. Novel hepatitis E virus in ferrets, the Netherlands. Emerg. Infect. Dis. 2012, 18, 1369–1370. [Google Scholar] [CrossRef]
  146. Kurucz, K.; Hederics, D.; Bali, D.; Kemenesi, G.; Horvath, G.; Jakab, F. Hepatitis E virus in Common voles (Microtus arvalis) from an urban environment, Hungary: Discovery of a Cricetidae-specific genotype of Orthohepevirus C. Zoonoses Public Health 2019, 66, 259–263. [Google Scholar] [CrossRef]
  147. Krog, J.S.; Breum, S.O.; Jensen, T.H.; Larsen, L.E. Hepatitis E virus variant in farmed mink, Denmark. Emerg. Infect. Dis. 2013, 19, 2028–2030. [Google Scholar] [CrossRef]
  148. Bodewes, R.; van der Giessen, J.; Haagmans, B.L.; Osterhaus, A.D.; Smits, S.L. Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J. Virol. 2013, 87, 7758–7764. [Google Scholar] [CrossRef]
  149. Sridhar, S.; Yip, C.C.Y.; Wu, S.; Cai, J.; Zhang, A.J.; Leung, K.H.; Chung, T.W.H.; Chan, J.F.W.; Chan, W.M.; Teng, J.L.L.; et al. Rat Hepatitis E Virus as Cause of Persistent Hepatitis after Liver Transplant. Emerg. Infect. Dis. 2018, 24, 2241–2250. [Google Scholar] [CrossRef]
  150. Purcell, R.H.; Engle, R.E.; Rood, M.P.; Kabrane-Lazizi, Y.; Nguyen, H.T.; Govindarajan, S.; St Claire, M.; Emerson, S.U. Hepatitis E virus in rats, Los Angeles, California, USA. Emerg. Infect. Dis. 2011, 17, 2216–2222. [Google Scholar] [CrossRef]
  151. Mulyanto; Suparyatmo, J.B.; Andayani, I.G.; Khalid; Takahashi, M.; Ohnishi, H.; Jirintai, S.; Nagashima, S.; Nishizawa, T.; Okamoto, H. Marked genomic heterogeneity of rat hepatitis E virus strains in Indonesia demonstrated on a full-length genome analysis. Virus Res. 2014, 179, 102–112. [Google Scholar] [CrossRef]
  152. Ryll, R.; Bernstein, S.; Heuser, E.; Schlegel, M.; Dremsek, P.; Zumpe, M.; Wolf, S.; Pepin, M.; Bajomi, D.; Muller, G.; et al. Detection of rat hepatitis E virus in wild Norway rats (Rattus norvegicus) and Black rats (Rattus rattus) from 11 European countries. Vet. Microbiol. 2017, 208, 58–68. [Google Scholar] [CrossRef] [PubMed]
  153. He, W.; Wen, Y.; Xiong, Y.; Zhang, M.; Cheng, M.; Chen, Q. The prevalence and genomic characteristics of hepatitis E virus in murine rodents and house shrews from several regions in China. BMC Vet. Res. 2018, 14, 414. [Google Scholar] [CrossRef] [PubMed]
  154. Johne, R.; Dremsek, P.; Kindler, E.; Schielke, A.; Plenge-Bonig, A.; Gregersen, H.; Wessels, U.; Schmidt, K.; Rietschel, W.; Groschup, M.H.; et al. Rat hepatitis E virus: Geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect. Genet. Evol. 2012, 12, 947–956. [Google Scholar] [CrossRef] [PubMed]
  155. Widen, F.; Ayral, F.; Artois, M.; Olofson, A.S.; Lin, J. PCR detection and analysis of potentially zoonotic Hepatitis E virus in French rats. Virol. J. 2014, 11, 90. [Google Scholar] [CrossRef]
  156. Johne, R.; Dremsek, P.; Reetz, J.; Heckel, G.; Hess, M.; Ulrich, R.G. Hepeviridae: An expanding family of vertebrate viruses. Infect. Genet. Evol. 2014, 27, 212–229. [Google Scholar] [CrossRef]
  157. Drexler, J.F.; Seelen, A.; Corman, V.M.; Fumie Tateno, A.; Cottontail, V.; Melim Zerbinati, R.; Gloza-Rausch, F.; Klose, S.M.; Adu-Sarkodie, Y.; Oppong, S.K.; et al. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J. Virol. 2012, 86, 9134–9147. [Google Scholar] [CrossRef] [PubMed]
  158. Kobayashi, T.; Murakami, S.; Yamamoto, T.; Mineshita, K.; Sakuyama, M.; Sasaki, R.; Maeda, K.; Horimoto, T. Detection of bat hepatitis E virus RNA in microbats in Japan. Virus Genes 2018, 54, 599–602. [Google Scholar] [CrossRef]
  159. Wang, B.; Yang, X.L.; Li, W.; Zhu, Y.; Ge, X.Y.; Zhang, L.B.; Zhang, Y.Z.; Bock, C.T.; Shi, Z.L. Detection and genome characterization of four novel bat hepadnaviruses and a hepevirus in China. Virol. J. 2017, 14, 40. [Google Scholar] [CrossRef] [PubMed]
  160. Kibenge, F.S.; Whyte, S.K.; Hammell, K.L.; Rainnie, D.; Kibenge, M.T.; Martin, C.K. A dual infection of infectious salmon anaemia (ISA) virus and a togavirus-like virus in ISA of Atlantic salmon Salmo salar in New Brunswick, Canada. Dis. Aquat. Organ. 2000, 42, 11–15. [Google Scholar] [CrossRef][Green Version]
Table 1. Host Range for Orthohepevirus A.
Table 1. Host Range for Orthohepevirus A.
Animals Susceptible to Orthohepevirus A Infection
Animal SpeciesScientific NameGenotypeSerology/Genome DetectionaInfection TypeReferences
Order
African green monkeyChlorocebus sabaeusHEV 1-2+/NDExperimentalDoceul et al. [34]
Primate
American bisonBison bison?b+/-NaturalDong et al. [35]
Artiodactyla
Asiatic black bearUrsus thibetanusHEV 4ND/+NaturalZhang et al. [36]
Perissodactyla
Bactrian camelCamelus bactrianusHEV 8+/+NaturalWoo et al. [37], Rasche et al. [38]
Artiodactyla
Bonnet macaqueMacaca radiataHEV 1+/+NaturalArankalle et al. [39]
Primate
Bottlenose dolphinTursiops truncatusHEV 3+/+NaturalMontalvo Villalba et al. [40]
Cetacea
Cape buffaloSyncerus caffer? b+/NDNaturalEl-Tras et al. [41]
Artiodactyla
CatFelis catus silvestris? b+/-NaturalLiang et al. [42], Mochizuki et al. [43]
Carnivora
Dairy cattle, yellow, Holstein Frisian Bos Taurus primigeniusHEV 4, ? b+/+NaturalArankalle et al. [44], El-Tras et al. [41], Yan et al. [45], Huang et al. [46]
Artiodactyla
ChimpanzeePan troglodytesHEV 1-4+/+Experimental
Natural
Yu et al. [47], Arankalle et al. [48], Meng et al. [49], Yugo et al. [50], Zhou et al. [51], Spahr et al. [52]
Primate
Clams (Yamato-shijimi)Corbicula japonicaHEV 3ND/+NaturalLi et al. [53]
Veneroida
Clouded leopard Neofelis nebulosaHEV 4ND/+NaturalZhang et al. [36]
Carnivora
Crowned craneBalearica regulorumHEV 4ND/+NaturalZhang et al. [36]
Gruiformes
Cynomolgus macaqueMacaca fascicularisHEV 1-5, 8+/+Experimental
Natural
Balayan et al. [54], Tsarev et al. [55], Bradley et al. [56], Aggarwal et al. [57], de Carvalho et al. [58], Li et al. [59], Wang et al. [60]
Primate
DogCanis lupis familiarisHEV 4? b+/-NaturalLiu et al. [61], Liang et al. [42], McElroy et al. [62], Arankalle et al. [44]
Carnivora
Domestic PigSus scrofa domesticaHEV 3, 4+/+Experimental
Natural
Meng et al. [63],
Artiodactyla
DonkeyEquus africanusHEV 3ND/+NaturalGarcia-Bocanegra et al. [64]
Perissodactyla
Dromedary camelCamelua dromedariusHEV 7+/+NaturalWoo et al. [37], Rasche et al. [38]
Artiodactyla
Eastern owl monkeyAotus trivirgatusHEV 1, 2+/+ExperimentalYugo et al. [40], Ticehurst et al. [65]
Primate
European brown hareLepus europaeusHEV 3? b+/-NaturalHammershmidt et al. [66]
Lagomorpha
Farmed minkNeovison visonHEV 3ND/+NaturalXie et al. [67]
Carnivora
GoatCapra hircus aegagrusHEV 3, 4+/+NaturalPeralta et al. [68], El-Tras et al. [41], Sanford et al. [69], Di Martina et al. [70], Li et al. [71], Long et al. [70]
Artiodactyla
Gray langurSemnoppithecus entellusHEV 1+/+NaturalArankalle et al. [39]
Primate
Himalayan griffonGyps himalayensisHEV 3ND/+NaturalLi et al. [72]
Accipitriformes
HorseEquus caballus ferusHEV 1,3+/+NaturalSaad et al. [33], Zhang et al. [73]
Perissodactyla
HumanHomo sapiensHEV 1-4, 7+/+Natural
Experimental
Balayan et al. [54], Arankalle et al. [74], Huang et al. [75], Meng et al. [63], Hsieh et al. [76], Lee et al. [77]
Primate
Japanese macaqueMacaca fuscataHEV 3+/+NaturalYamamoto et al. [78]
Primate
Japanese white rabbitOryctologus cuniculus domesticusHEV 3ND/+Experimental NaturalXia et al. [79]
Lagomorpha
Javan mongooseHerpestes javanicusHEV 3+/+NaturalLi et al. [80], Nakamura et al. [81], Nidaira et al. [82]
Carnivora
Mongolian gerbilMeriones unguiculatusHEV 4+/+ExperimentalLiu et al. [83]
Rodentia
Moustached tamarinSaguinus mystax mystaxHEV 1,2+/+ExperimentalBradley et al. [56]
Primate
Mussels (Blue mussel, Mediterranean mussel, Pacific mussel), Mytilus edulis, Mytilus galloprovincialis, Crassostrea gigasHEV 3ND/+NaturalO’Hara et al. [84], Krog et al. [85], Diez-Valcarce et al. [86], Crossan et al. [30]
Ostreoida
Norwegian ratRattus norvegicusHEV 3+/+NaturalKanai et al. [87], Lack et al. [88]
Rodentia
Patas monkeyErythrocebus patasHEV 1, 2ND/+ExperimentalYugo et al. [50]
Primate
Rabbit
New Zealand White, Rex, Japanese White
Oryctolagus cuniculus
domesticus
HEV 3+/+Experimental
Natural
Cossaboom et al. [89], Izopet et al. [90], Carusoet al. [91], Hammerschmidt et al. [66], Birke et al, [92], Zhao et al. [93], Genget al. [94], Xia et al. [79]
Lagomorpha
RaccoonProcyon lotor? b+/-NaturalDähnert et al. [95]
Carnivora
Raccoon dogNyctereutes procyonoides? b+/-NaturalDähnert et al. [95]
Carnivora
Red deerCervus elaphusHEV 3-/+NaturalForgách [96] et al, Anheyer-Behmenburg et al. [97]
Artiodactyla
Reeves’ muntjacMuntiacus reevesiHEV 4ND/+NaturalZhang et al. [73]
Artiodactyla
Rhesus macaqueMacaca mulattaHEV 1-4+/+Experimental
Natural
Arankalle et al. [39], Yamamoto et al. [78], Meng et al. [49], Huang et al. [98]
Primate
Roe deerCapreolus capreolusHEV 3-/+NaturalReuter et al. [99], Forgách et al. [96] 2010, Anheyer-Behmenburg et al. [97]
Artiodactyla
SheepOvis aries orientalisHEV 3, 4+/+NaturalEl-Tras et al. [41], Peralta et al. [68], Sarchese et al. [100], Wu et al. [101]
Artiodactyla
Sika deerCervus nippon nipponHEV 3,4+/+NaturalSonoda et al. [102], Zhang et al. [73]
Artiodactyla
Silver pheasantLophura nycthemeraHEV 4ND/+NaturalZhang et al. [36]
Galliformes
Squirrel monkeySaimiri sciureusHEV 1,2+/+ExperimentalTsarev et al. [55]
Primate
Swedish mooseAlces alcesHEV ? c+/+NaturalLin et al. [103], Lin et al. [4]
Artiodactyla
Tufted deerElaphodus cephalophusHEV 4ND/+NaturalZhang et al. [73]
Artiodactyla
Vervet monkeyChlorocebus pygerythrusHEV 1,2ND/+ExperimentalTsarev et al. [55]
Primate
Wild boarSus scrofaHEV 3,4,5,6+/+NaturalSonoda et al. [102], Martelli et al, De Deus et al. [104], Adlhoch et al. [105], Wiratsudakulet al. [106], Kaci et al. [107], Dong et al. [35], Takahashi et al. [108], Takahashi et al. [109], Larska et al. [110], Carpentier et al. [111], Anheyer-Behmenburg et al. [97]
Artiodactyla
YakBos grunniensHEV 4+/+NaturalXu et al. [112]
Artiodactyla
Yezo deerCervus nippon yesoensisHEV 3 or 4? b+/-NaturalSonoda et al. [102], Tomiyama et al. [113]
Artiodactyla
Table 1. Animals known to be associated with Orthohepevirus A infection. Text in bold indicates taxonomic order. For serology/genome detection “+” is any reported positive result, “-“ indicates assays were performed and results were negative, “ND indicates test was not performed (Not Done).” a Serology and genomic RNA detection are a summary of all published data. Individual articles may have only included serology, only genomic RNA detection, or both. b Data presented as only serological data suggest animals were exposed to HEV but a definitive strain could not be assigned due to the single serotype of all HEV strains. c Swedish moose HEV strain has not been assigned to a current HEV genotype and appears to cluster between Orthohepevirus A and Orthohepevirus C strains.
Table 2. Host range of Orthohepevirus B.
Table 2. Host range of Orthohepevirus B.
Animals Susceptible to Orthohepevirus B
Animal SpeciesScientific NameSpeciesSerology/Genome
Detection
Infection TypeReferences
Order
ChickenGallus gallusOrtho B+/+Natural ExperimentalHaqshenas et al. [124] Liu et al. [132]
Galliformes
Common buzzardButeo buteoOrtho BND/+NaturalZhang et al. [135]
Accipitriformes
DucksAnas platyrhynchosaOrtho B+/+NaturalLiu et al. [132]
Anseriformes
Feral pigeonColumba livia domesticaOrtho BND/+NaturalZhang et al. [135]
Columbiformes
GeeseAnser anser domesticusaOrtho B+/+NaturalLiu et al. [132]
Anseriformes
Little egretEgretta garzettaOrtho BND/+NaturalReuter et al. [137]
Pelicaniformes
Little owlAthene noctuaOrtho BND/+NaturalZhang et al. [135]
Strigiformes
Rabbit
New Zealand White
Oryctolagus cuniculusOrtho B+/+Natural
Experimental
Liu et al. [132]
Lagomorpha
Song thrushTurdus philomelosOrtho BND/+NaturalZhang et al. [135]
Passeriformes
SparrowPasser domesticusOrtho BND/+NaturalYang et al. [136]
Passeriformes
TurkeyMeleagris gallopavoOrtho B+/+ExperimentalSun et al. [131]
Galliformes
Table 2 Animals associated with Orthohepevirus B infection. Names in bold represent taxonomic order. Under serology/genome detection “+” indicates any positive report for that assay within the literature, “-“ represents the test being performed with negative results, ND indicates the test was not performed (Not Done). a Exact species names are uncertain as tested animals were simply identified as duck and goose. E-mails to corresponding authors requesting clarification were not returned.
Table 3. Host range of Orthohepevirus C.
Table 3. Host range of Orthohepevirus C.
Animals Susceptible to Orthohepevirus C
Animal SpeciesScientific NameSpeciesSerology/Genome
Detectiona
Infection TypeReferences
Order
Asian musk shrewSuncus murinusOrtho C+/+NaturalGuan et al. [144]
Eulipotyphla
Black RatRattus rattus
Rattus rattus hainanus
Ortho C+/+NaturalLi et al. [134], Mulyanto et al. [151], Ryll et al. [152]
Rodentia
Chevrier’s Field MouseApodemus chevrieriOrtho CND/+NaturalWang et al. [142]
Rodentia
Common voleMicrotus arvalisOrtho CND/+NaturalKurucz et al. [146]
Rodentia
Delicate vesper mouseCalomys tenerOrtho CND/+Naturalde Souza et al. [143]
Rodentia
European ferretMustela putoriusOrtho C+/+NaturalRaj et al. [145]
Carnivora
European minkMustelo lutreolaOrtho CND/+NaturalKrog et al. [147]
Carnivora
Farmed minkNeovison visonOrtho CND/+Natural Xie et al. [67]
Carnivora
Greater bandicoot ratBandicota indicaOrtho C+/+NaturalLi et al. [134]
Rodentia
Hairy-tailed bolo mouseNecromys lasiurusOrtho CND/+Naturalde Souza et al. [143]
Rodentia
House ShrewSuncus murinusOrtho CND/+NaturalHe et al. [153]
Eulipotyphla
HumanHomo sapiensOrtho C+/+NaturalSridhar et al. [149]
Primate
Norway RatRattus norvegicusOrtho C+/+Natural
Experimental
Kabrane-Lazizi et al. [115], Easterbrook et al. [138], Johne et al. [140], Johne et al. [154], Purcell et al. [150], Widen et al. [155], He et al. [153]
Rodentia
Peré David’s VoleEothenomys melanogasterOrtho CND/+ Wang et al. [142]
Rodentia
Red foxVulpes vulpesOrtho CND/+NaturalBodewes et al. [148]
Carnivora
Taiwan ratRattus rattoides loseaOrtho C+/+NaturalLi et al. [134], He et al. [153]
Rodentia
Tanezumi rat
(Asian rat)
Rattus tanezumiOrtho CND/+NaturalHe et al. [153]
Rodentia
Yellow-breasted ratRattus flavipectusOrtho C+/+NaturalLi et al. [134]
Rodentia
Table 3 Species reported to be infected with Orthohepevirus C strains of HEV. Names in bold represent taxonomic order. Under serology/genome detection “+” indicates any positive report for that assay within the literature, “-“ represents the test being performed with negative results, ND indicates the test was not performed (Not Done). a Serology/Genome Detection summarizes findings from all literature, some article may have only shown serology positive, genome positive, or both.
Table 4. Host range of Orthohepevirus D.
Table 4. Host range of Orthohepevirus D.
Animals Susceptible to Orthohepevirus D
Animal SpeciesScientific NameSpeciesSerology/Genome DetectionInfection TypeReferences
Order
Aba roundleaf batHipposideros abaeOrtho DND/+NaturalDrexler et al. [157]
Chiroptera
Bechstein’s batMyotis bechsteiniiOrtho DND/+NaturalDrexler et al. [157]
Chiroptera
Brown long-eared batPlecotus sacrimontisOrtho DND/+NaturalKobayashi et al. [158]
Chiroptera
Daubenton’s batMyotis daubentoniiOrtho DND/+NaturalDrexler et al. [157]
Chiroptera
Great stripe-faced batVampyrodes caraccioliOrtho DND/+NaturalDrexler et al. [157]
Chiroptera
Japanese short-tailed batEptesicus japonensisOrtho DND/+NaturalKobayashi et al. [158]
Chiroptera
Serotine batEptesicus serotinusOrtho D ND/+NaturalDrexler et al. [157]
Chiroptera
Whiskered batMyotis davidiiOrtho DND/+NaturalWang et al. [159]
Chiroptera
Table 4 Species susceptible to Orthohepevirus D infection. Names in bold represent taxonomic order. Under serology/genome detection “+” indicates any positive report for that assay within the literature and “ND” indicates the test was not performed (Not Done).
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