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Identification of Multiple Novel Viruses, Including a Parvovirus and a Hepevirus, in Feces of Red Foxes
Open accessAbstract
Red foxes ( Vulpes vulpes ) are the most widespread members of the order of Carnivora . Since they often live in (peri)urban areas, they are a potential reservoir of viruses that transmit from wildlife to humans or domestic animals. Here we evaluated the fecal viral microbiome of 13 red foxes by random PCR in combination with next-generation sequencing. Various novel viruses, including a parvovirus, bocavirus, adeno-associated virus, hepevirus, astroviruses, and picobirnaviruses, were identified.
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“We discovered viral transcripts with some sequence similarity to the Hepeviridae that cause hepatitis E in mammals, which has already been isolated from various domestic and wild animals including foxes in the Netherlands (Meng 2010; Bodewes et al. 2013).”
From Red fox viromes in urban and rural landscapes (2020) · cites this paper as Bodewes et al. 2013
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“In contrast, the hepevirus detected here was phylogenetically distinct from the fox hepatitis E virus previously detected (Bodewes et al. 2013) and instead was more closely related to hepeviruses detected in freshwater mussels and a house mouse.”
From Red fox viromes in urban and rural landscapes (2020) · cites this paper as Bodewes et al. 2013
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Cites
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Cited by
Sorted by citations
Consensus proposals for classification of the family Hepeviridae
Smith, D. B., Simmonds, P., Jameel, S., Emerson, S., Harrison, T., Meng, X.-J., Okamoto, H., van der Poel, W., & Purdy, M. (2014) · Journal of General Virology · doi:10.1099/vir.0.068429-0 · Cited by 658
“Both schemes are out-of-date in light of the recent publication of sequences from divergent variants isolated from moose (Lin et al. , 2014), mink (Krog et al. , 2013), fox (Bodewes et al. , 2013), ferret (Li et al. , 2014), wild boar (Takahashi et al. , 2014) and camel (Woo et al. , 2014).”
BackgroundZoonotic Hepatitis E Virus: Classification, Animal Reservoirs and Transmission Routes
Doceul, V., Bagdassarian, E., Demange, A., & Pavio, N. (2016) · Viruses · doi:10.3390/v8100270 · Cited by 236
“Partial sequences with the highest homology to rat HEV have also been detected in foxes [31].”
BackgroundPorcine circoviruses: current status, knowledge gaps and challenges
Opriessnig, T., Karuppannan, A. K., de Castro, A. M. M. G., & Xiao, C. (2020) · Virus Research · doi:10.1016/j.virusres.2020.198044 · Cited by 211
Zoonotic origin of hepatitis E.
Pavio, N., Meng, X.-J., & Doceul, V. (2015) · Current Opinion in Virology · doi:10.1016/j.coviro.2014.12.006 · Cited by 178
Faecal virome of cats in an animal shelter
Zhang, W., Li, L., Deng, X., Kapusinszky, B., Pesavento, P. A., & Delwart, E. (2014) · Journal of General Virology · doi:10.1099/vir.0.069674-0 · Cited by 215
“The tree based on the RdRp region showed that FAstV-D1 was more closely related to the fox astrovirus (GenBank accession number KC692365) (Bodewes et al., 2013) (Fig.”
BackgroundHepeviridae: an expanding family of vertebrate viruses.
Johne, R., Dremsek, P., Reetz, J., Heckel, G., Hess, M., & Ulrich, R. (2014) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2014.06.024 · Cited by 137
Hjelmsø, M. H., Hellmér, M., Fernández-Cassi, X., Timoneda, N., Lukjančenko, O., Seidel, M., Elsäßer, D., Aarestrup, F. M., Löfström, C., Bofill-Mas, S., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170199 · Cited by 150
“Metagenomic sequencing of the virus associated nucleic acids is considered to be an unbiased approach enabling the detection of all known viral species, as well as the discovery of novel and emergent species [10].”
BackgroundHepatitis E virus and related viruses in wild, domestic and zoo animals: A review
Spahr, C., Knauf-Witzens, T., Vahlenkamp, T. W., Ulrich, R. G., & Johne, R. (2018) · Zoonoses and Public Health · doi:10.1111/zph.12405 · Cited by 115
“…+ − HEV- 4 Liu et al. (2009) + n.d. n.d. Liang et al. (2014) + − n.d. McElroy et al. (2015) + n.d. n.d. Arankalle et al. (2001) Red fox Vulpes vulpes n.d. + HEV- C2 Bodewes et al. (2013) Asiatic black bear Ursus thibetanus n.d. + HEV- 4 Zhang, Shen, Mou, Gong, et al. (2008) and Zhang, Shen, Mou,…”
Exploring the Potential of Next-Generation Sequencing in Detection of Respiratory Viruses
Prachayangprecha, S., Schapendonk, C., Koopmans, M., Osterhaus, A., Schürch, A., Pas, S., van der Eijk, A. A., Poovorawan, Y., Haagmans, B., & Smits, S. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.01641-14 · Cited by 114
Self-citationNew Viruses in Idiopathic Human Diarrhea Cases, the Netherlands
Smits, S., Schapendonk, C., van Beek, J., Vennema, H., Schürch, A., Schipper, D., Bodewes, R., Haagmans, B., Osterhaus, A., & Koopmans, M. (2014) · Emerging Infectious Diseases · doi:10.3201/eid2007.140190 · Cited by 97
“Samples were analyzed by using a viral metagenomics approach and 169,305 trimmed reads were characterized according to BLAST searches as described (5).”
MethodSelf-citationGenetic Variability and Evolution of Hepatitis E Virus
Primadharsini, P. P., Nagashima, S., & Okamoto, H. (2019) · Viruses · doi:10.3390/v11050456 · Cited by 93
“Several other related viruses are yet to be classified, including those from moose [99,100], fox [101], little egret [102], tree shrew (GenBank accession number KR905549) (Figure 1), sparrow [103] and agile frog [104].”
BackgroundSchlosser, J., Eiden, M., Vina-Rodriguez, A., Fast, C., Dremsek, P., Lange, E., Ulrich, R., & Groschup, M. (2014) · Veterinary Research · doi:10.1186/s13567-014-0121-8 · Cited by 93
“Recently, novel HEV-related viruses were identified in carnivores such as ferret [14] and fox [15], different bat species [16], moose”
BackgroundThe Current Host Range of Hepatitis E Viruses
Kenney, S. P. (2019) · Viruses · doi:10.3390/v11050452 · Cited by 92
Classification and Genomic Diversity of Enterically Transmitted Hepatitis Viruses.
Smith, D. B., & Simmonds, P. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a031880 · Cited by 91
“3), have been described from moose (Lin et al. 2014), fox (Bodewes et al. 2013), kestrel (Reuter et al. 2016a), and little egret (Reuter et al. 2016b), although these have yet to be formally classified into individual species.”
BackgroundKraberger, S., Argüello-Astorga, G., Greenfield, L. G., Galilee, C., Law, D., Martin, D. P., & Varsani, A. (2015) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2015.01.001 · Cited by 86
Parvovirus Family Conundrum: What Makes a Killer?
Kailasan, S., Agbandje‐McKenna, M., & Parrish, C. R. (2015) · Annual Review of Virology · doi:10.1146/annurev-virology-100114-055150 · Cited by 90
Ganesh, B., Masachessi, G., & Mladenova, Z. (2014) · VirusDisease · doi:10.1007/s13337-014-0207-y · Cited by 79
“, pigs [2, 4, 16, 31, 34, 50, 56, 67], calves [10, 15, 35, 53, 54, 61, 77, 79], rabbits and guinea pigs [25, 43, 52, 65], bats [86], red fox [8], avian such as chickens &”
Viral metagenomic analysis of feces of wild small carnivores
Bodewes, R., Ruiz-González, A., Schapendonk, C., van den Brand, J. V. D., Osterhaus, A., & Smits, S. (2014) · Virology Journal · doi:10.1186/1743-422x-11-89 · Cited by 78
“In addition, in spite of their relevance as potential carriers of pathogens, only a few recent studies have conducted thorough metagenomic analysis of fecal material on wild carnivore species [9,14,50].”
InfluentialSelf-citationNovel myco-like DNA viruses discovered in the faecal matter of various animals.
Sikorski, A., Massaro, M., Kraberger, S., Young, L., Smalley, D., Martin, D. P., & Varsani, A. (2013) · Virus Research · doi:10.1016/j.virusres.2013.08.008 · Cited by 76
“…cows (Kim et al., 2012), rodents (Phan et al., 56 2011), bats (Ge et al., 2011; Li et al., 2010b), badgers (van den Brand et al., 2012), foxes 57 (Bodewes et al., 2013), New Zealand fur seal (Sikorski et al., 2013b) and pigs (Sachsenröder et al., 58 2012; Shan et al., 2011; Sikorski et al.,…”
BackgroundWoo, P. C. Y., Lau, S., Teng, J. L. L., Tsang, A. K. L., Joseph, M., Wong, E. Y. M., Tang, Y., Sivakumar, S., Bai, R., Wernery, R., et al. (2014) · Virology · doi:10.1016/j.virol.2014.09.020 · Cited by 74
“…results obtained from metagenomic studies for fecal samples of other animals, in which mainly genogroup I picobirnavirus sequences were observed (Bodewes et al., 2013; Cheung et al., 2013; Lager et al., 2012; Li et al., 2011b; Phan et al., 2011; Sachsenroder et al., 2012; Sachsenroder et al.,…”
BackgroundResultHan, J.-Q., Lei, Y.-X., Liu, L., Liu, P., Xia, J., Zhang, Y.-L., Zeng, H., Wang, L., Wang, L., & Zhuang, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099861 · Cited by 73
Small but mighty: old and new parvoviruses of veterinary significance
Jager, M. C., Tomlinson, J., López-Astacio, R. A., Parrish, C., & van de Walle, G. (2021) · Virology Journal · doi:10.1186/s12985-021-01677-y · Cited by 72
RECENT CHANGES IN INFECTIOUS DISEASES IN EUROPEAN WILDLIFE
Yon, L., Duff, J. P., Ågren, E. O., Erdélyi, K., Ferroglio, E., Godfroid, J., Hars, J., Hestvik, G., Horton, D. L., Kuiken, T., et al. (2018) · Journal of Wildlife Diseases · doi:10.7589/2017-07-172 · Cited by 91
“Hepatitis E virus has also been detected in feces of red foxes (Bodewes et al. 2013b) in the Netherlands, but it is unclear whether it was a true infection or if the virus originated from ingestion and subsequent excretion of infected prey.”
BackgroundDetection of Circovirus in Foxes with Meningoencephalitis, United Kingdom, 2009–2013
Bexton, S., Wiersma, L., Getu, S., van Run, P., Verjans, G. M. G. M., Schipper, D., Schapendonk, C., Bodewes, R., Oldroyd, L., Haagmans, B., et al. (2015) · Emerging Infectious Diseases · doi:10.3201/eid2107.150228 · Cited by 67
Self-citationOrthohepevirus C: An Expanding Species of Emerging Hepatitis E Virus Variants
Wang, B., Harms, D., Yang, X.-L., & Bock, C. (2020) · Pathogens · doi:10.3390/pathogens9030154 · Cited by 65
“Even though a short (362 nucleotide) partial ORF1 sequence was identified in a red fox (species Vulpes vulpes, family Canidae), classification into Orthohepevirus C requires comparisons based upon complete genome sequences, as recommended by the International Committee on the Taxonomy of Viruses (ICTV) Hepeviridae Stu…”
MethodHepatitis E Virus Variant in Farmed Mink, Denmark
Krog, J. S., Breum, S., Jensen, T. H., & Larsen, L. (2013) · Emerging Infectious Diseases · doi:10.3201/eid1912.130614 · Cited by 60
Novel canine bocavirus strain associated with severe enteritis in a dog litter
Bodewes, R., Lapp, S., Hahn, K., Habierski, A., Förster, C., König, M., Wohlsein, P., Osterhaus, A., & Baumgärtner, W. (2014) · Veterinary Microbiology · doi:10.1016/j.vetmic.2014.08.025 · Cited by 56
Self-citationBorm, S. V., Belák, S., Freimanis, G., Fusaro, A., Granberg, F., Höper, D. W., King, D. P., Monne, I., Orton, R. J., & Rosseel, T. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-2004-4_30 · Cited by 62
Sasaki, M., Orba, Y., Ueno, K., Ishii, A., Moonga, L., Hang'ombe, B., Mweene, A., Ito, K., & Sawa, H. (2015) · Journal of General Virology · doi:10.1099/vir.0.071209-0 · Cited by 49
“…of mammals, including nonhuman primates, bats, pigs, rodents, cats, sea lions, martens, badgers, foxes, ferrets and pigeons (Baker et al. , 2013; Bodewes et al. , 2013; Dacheux et al. , 2014; Donaldson et al. , 2010; Ge et al. , 2012; Handley et al. , 2012; Li et al. , 2011b; Li et al. , 2010b;…”
Antigenic and genetic characterization of a divergent African virus, Ikoma lyssavirus
Horton, D., Banyard, A., Marston, D., Wise, E., Selden, D., Núñez, A., Hicks, D., Lembo, T., Cleaveland, S., Peel, A., et al. (2014) · Journal of General Virology · doi:10.1099/vir.0.061952-0 · Cited by 48
“These include metagenomic studies of the viral flora of healthy animals aimed at predicting transmission risks to other species, and the detection of pathogens in clinical samples and excreta for diagnosis (Bodewes et al., 2013; Ge et al., 2012; Li et al., 2011; Phan et al., 2011; van den Brand et al., 2012).”
BackgroundRed fox viromes in urban and rural landscapes
Campbell, S. J., Ashley, W., Gil-Fernandez, M., Newsome, T. M., Di Giallonardo, F., Ortiz-Baez, A. S., Mahar, J. E., Towerton, A. L., Gillings, M., Holmes, E. C., et al. (2020) · Virus Evolution · doi:10.1093/ve/veaa065 · Cited by 47
False-positive results in metagenomic virus discovery: a strong case for follow-up diagnosis.
Rosseel, T., Pardon, B., Clercq, K. D., Ozhelvaci, O., & van Borm, S. (2014) · Transboundary and Emerging Diseases · doi:10.1111/tbed.12251 · Cited by 44
“…et al., 2011), well-known disorders presumed to be of multifactorial aetiology (Cox-Foster et al., 2007; Blomstr€om et al., 2009; Granberg et al., 2013), and reservoir species and vectors (Bishop-Lilly et al., 2010; Li et al., 2010; Blomstr€om et al., 2012; Ge et al., 2012; Bodewes et al., 2013).”
BackgroundHepatitis E Virus and Related Viruses in Animals
Thiry, D., Mauroy, A., Pavio, N., Purdy, M., Rose, N., Thiry, E., & de Oliveira-Filho, E. D. (2015) · Transboundary and Emerging Diseases · doi:10.1111/tbed.12351 · Cited by 43
“…Li et al, 2014 Japan C2 Li et al, 2014 Mink Country Genotype Reference Denmark / Krog et al, 2013 Fox Country Genotype Reference The Netherlands / Bodewes et al, 2013 Mongoose Country Genotype HEV- Reference Japan 3 Nakamura et al, 2006 Bat Country Genotype Reference Germany / Drexler et al,…”
Hjelmsø, M. H., Mollerup, S., Jensen, R. H., Pietroni, C., Lukjančenko, O., Schultz, A. C., Aarestrup, F. M., & Hansen, A. J. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210368 · Cited by 43
“Metagenomics is an unbiased detection technique allowing for both the detection of known pathogens as well as the discovery of novel viruses [22,23].”
Evolutionary Origins of Enteric Hepatitis VirusesPreprint
Sander, A., Corman, V. M., Lukashev, A. N., & Drexler, J. F. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a031690 · Cited by 40
“Unique hepeviruses from fox and mink were not included in B because they are only partially sequenced (Bodewes et al. 2013; Krog et al. 2013).”
BackgroundFecal virome analysis of three carnivores reveals a novel nodavirus and multiple gemycircularviruses
Conceição-Neto, N., Zeller, M., Heylen, E., Lefrère, H., Mesquita, J., & Matthijnssens, J. (2015) · Virology Journal · doi:10.1186/s12985-015-0305-5 · Cited by 37
The Expanding Field of Mammalian Astroviruses: Opportunities and Challenges in Clinical Virology.
Boujon, C. L., Koch, M., & Seuberlich, T. (2017) · Advances in Virus Research · doi:10.1016/bs.aivir.2017.07.002 · Cited by 37
Faecal virome of red foxes from peri-urban areas
Lojkić, I., Biđin, M., Prpić, J., Šimić, I., Krešić, N., & Bedeković, T. (2016) · Comparative Immunology, Microbiology & Infectious Diseases · doi:10.1016/j.cimid.2016.01.005 · Cited by 36
Feline Virome—A Review of Novel Enteric Viruses Detected in Cats
Martino, B. D., Profio, F. D., Melegari, I., & Marsilio, F. (2019) · Viruses · doi:10.3390/v11100908 · Cited by 35
“Furthermore, mamastroviruses more genetically closest in the RdRp region to AstVs previously found in foxes [155] have occasionally been identified in fecal samples collected from healthy cats [17, 156] .”
BackgroundFerret hepatitis E virus infection induces acute hepatitis and persistent infection in ferrets.
Li, T.-C., Yang, T.-T., Yoshizaki, S., Ami, Y., Suzaki, Y., Ishii, K., Kishida, N., Shirakura, M., Asanuma, H., Takeda, N., et al. (2016) · Veterinary Microbiology · doi:10.1016/j.vetmic.2015.11.014 · Cited by 33
Duraisamy, R., Akiana, J., Davoust, B., Mediannikov, O., Michelle, C., Robert, C., Parra, H., Raoult, D., Biagini, P., & Desnues, C. (2018) · Virus genes · doi:10.1007/s11262-018-1543-6 · Cited by 32
Rabbit and human hepatitis E virus strains belong to a single serotype.
Wang, S., Cheng, X.-F., Dai, X., Dong, C., Xu, M.-J., Liang, J.-H., Dong, M., Purdy, M., & Meng, J. (2013) · Virus Research · doi:10.1016/j.virusres.2013.05.013 · Cited by 32
Woo, P. C. Y., Teng, J. L. L., Bai, R., Tang, Y., Wong, A. Y. P., Li, K. S., Lam, C. S. F., Fan, R. Y. Y., Lau, S., & Yuen, K. Y. (2019) · Viruses · doi:10.3390/v11060574 · Cited by 31
“Although genogroup I PBVs have been found in different kinds of animals [2, 3, [7] [8] [9] [10] 13, [17] [18] [19] [20] [21] [39] [40] [41] [42] [43] [44] [45] , genogroup II PBVs have only been reported in humans [5, 46] , monkeys [47] , pigs [36] , a cattle calf [44] , and a cat [19] .”
BackgroundInfluentialPonterio, E., Bartolo, I. D., Orrù, G., Liciardi, M., Ostanello, F., & Ruggeri, F. (2014) · BMC Veterinary Research · doi:10.1186/1746-6148-10-133 · Cited by 30
“[9], foxes [10] and bats [11], but the current HEV classification has not been modified yet.”
BackgroundA novel astrovirus from dromedaries in the Middle East.
Woo, P. C. Y., Lau, S., Teng, J. L. L., Tsang, A. K. L., Joseph, S., Xie, J., Jose, S., Fan, R. Y. Y., Wernery, U., & Yuen, K. Y. (2015) · Journal of General Virology · doi:10.1099/jgv.0.000233 · Cited by 29
“On the other hand, for the mammalian AstVs found in sea lions, bottlenose dolphins, bats, mice, rats, foxes, wild boar, porcupines and cattle, there is so far no data on whether they are associated with gastroenteritis, although these viruses were found in the faecal samples of the animals (Bodewes et al., 2013; Chu e…”
BackgroundKraberger, S., Waits, K., Ivan, J. S., Newkirk, E. S., VandeWoude, S., & Varsani, A. (2018) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2018.06.001 · Cited by 28
High Diversity of Genogroup I Picobirnaviruses in Mammals
Woo, P. C. Y., Teng, J. L. L., Bai, R., Wong, A. Y. P., Martelli, P., Hui, S.-W., Tsang, A. K. L., Lau, C. C., Ahmed, S. S., Yip, C. C. Y., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01886 · Cited by 26
“…birds and environmental water samples (Fregolente et al., 2009; Ghosh et al., 2009; Symonds et al., 2009; Martinez et al., 2010; Ganesh et al., 2011a; Malik et al., 2011; Wang et al., 2012; Bodewes et al., 2013; Gillman et al., 2013; Ng et al., 2014; Ribeiro et al., 2014; Zhang et al., 2014).”
BackgroundInfluentialSchürch, A. C., Schipper, D., Bijl, M., Dau, J., Beckmen, K. B., Schapendonk, C. M. E., Raj, V. S., Osterhaus, A. D. M. E., Haagmans, B. L., Tryland, M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105227 · Cited by 22
“Metagenome sequencing Depletion of host nucleic acids, isolation of viral nucleic acids, sequence-independent amplification and next-generation of sequencing with a 454GS Junior (Roche) was carried out as previously described [6,23,24].”
MethodSelf-citationMetagenomic analysis of Sichuan takin fecal sample viromes reveals novel enterovirus and astrovirus.
Guan, T.-P., Teng, J. L. L., Yeong, K., You, Z.-Q., Liu, H., Wong, S. S., Lau, S., & Woo, P. C. Y. (2018) · Virology · doi:10.1016/j.virol.2018.05.027 · Cited by 22
Porea, D., Răileanu, C., Crivei, L., Gotu, V., Savuța, G., & Pavio, N. (2023) · Viruses · doi:10.3390/v15061337 · Cited by 21
“Strains related to ferrets and rat hepeviruses have also been detected in foxes in The Netherlands and Germany [9,10].”
BackgroundZhou, X., Kataoka, M., Liu, Z., Takeda, N., Wakita, T., & Li, T.-C. (2015) · Virus Research · doi:10.1016/j.virusres.2015.06.022 · Cited by 21
“In addition to humans, other animals such as chickens, bats, rats, rabbits, mongooses, foxes, moose, minks, ferrets, and even fish also harbor HEVs, including a number of genetically distant strains (Batts et al., 2011; Bodewes et al., 2013; Drexler et al., 2012; Haqshenas et al., 2001; Jay Lin et al., 2014; Johne et…”
Restoring Ciliary Function: Gene Therapeutics for Primary Ciliary Dyskinesia
Keiser, N. W., Cant, E., Sitaraman, S., Shoemark, A., & Limberis, M. P. (2023) · Human Gene Therapy · doi:10.1089/hum.2023.102 · Cited by 21
Leopardi, S., Milani, A., Cocchi, M., Bregoli, M., Schivo, A., Leardini, S., Festa, F., Pastori, A., de Zan, G., Gobbo, F., et al. (2022) · Viruses · doi:10.3390/v14122612 · Cited by 20
“8% prevalence of FPV in red foxes in other areas of Italy [13] and might be due to the fox susceptibility to Carnivore protoparvovirus 4 species, of which the prototype virus has been identified in a red fox [29].”
BackgroundPicobirnaviruses: prevalence, genetic diversity, detection methods
Kashnikov, A., Epifanova, N. V., & Novikova, N. (2020) · Vavilovskii zhurnal genetiki i selektsii · doi:10.18699/vj20.660 · Cited by 20
Han, J.-Q., Zeng, H., Wang, L., Liu, P., Liu, L., Xia, J., Zhang, Y.-L., Wang, L., & Zhuang, H. (2014) · Journal of Medical Virology · doi:10.1002/jmv.24003 · Cited by 20
“…species, including chickens, deer, mongooses, foxes, ferrets, rats, bats, wild boars, and trout [Haqshenas et al., 2001; Nakamura et al., 2006; Tomiyama et al., 2009; Johne et al., 2010; Batts et al., 2011; Takahashi et al., 2011; Drexler et al., 2012; Raj et al., 2012; Bodewes et al., 2013].”
BackgroundVlaanderen, F., Uiterwijk, M., Cuperus, T., Keur, I., Rosa, M. D., Rozendaal, H., Koene, M., Schreurs, H., Nijsse, R., Nielen, M., et al. (2011) · doi:10.21945/rivm-2020-0130 · Cited by 20
Small Animal Models of Hepatitis E Virus Infection.
Li, T.-C., & Wakita, T. (2019) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a032581 · Cited by 19
“…chickens, bats, and cutthroat trout (Haqshenas et al. 2001; Zhao et al. 2009; Johne et al. 2010a; Batts et al. 2011; Drexler et al. 2012; Raj et al. 2012; Yamamoto et al. 2012; Bodewes et al. 2013; Krog et al. 2013; Lin et al. 2014; Takahashi et al. 2014; Woo et al. 2014; Reuter et al. 2016).”
BackgroundVeterinary Infection Biology: Molecular Diagnostics and High-Throughput Strategies
Cunha, M. V., & Inácio, J. (2015) · Methods in Molecular Biology · doi:10.1007/978-1-4939-2004-4 · Cited by 19
Mietzsch, M., Hull, J. A., Makal, V., Ybargollin, A. J., Yu, J. C., McKissock, K., Bennett, A. D., Pénzes, J. J., Lins, B., Yu, Q., et al. (2022) · Journal of Virology · doi:10.1128/jvi.00335-22 · Cited by 19
“(3), cow (4), goat (5), pig (6), sea lion (7), fox (8), rodents (9), and bat (10).”
Eiden, M., Dähnert, L., Spoerel, S., Vina-Rodriguez, A., Schröder, R., Conraths, F., & Groschup, M. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00115 · Cited by 18
Monkeys and Rats Are Not Susceptible to Ferret Hepatitis E Virus Infection
Li, T.-C., Yoshizaki, S., Ami, Y., Suzaki, Y., Yang, T.-T., Takeda, N., & Wakita, T. (2015) · Intervirology · doi:10.1159/000373891 · Cited by 18
A broadly cross-reactive monoclonal antibody against hepatitis E virus capsid antigen
Kubickova, B., Schenk, J., Ramm, F., Markuškienė, K., Reetz, J., Dremsek, P., Tamošiunas, P. L., Cepulyte, L., Trinh, H., Scholz, J., et al. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11342-7 · Cited by 17
“In addition to human pathogenic HEV, related viruses have been identified in fowl, rats, bats, carnivores and even in fish (Batts et al. 2011; Bodewes et al. 2013; Drexler et al. 2012; Johne et al. 2010a, b; Krog et al. 2013; Raj et al. 2012).”
BackgroundStructural characterization of a bat Adeno-associated virus capsid
Mietzsch, M., Li, Y., Kurian, J. J., Smith, J. K., Chipman, P. R., McKENNA, R. V., Yang, L., & Agbandje‐McKenna, M. (2020) · Journal of Structural Biology · doi:10.1016/j.jsb.2020.107547 · Cited by 17
Rat hepatitis E virus (Rocahepevirus ratti) exposure in cats and dogs, Hong Kong
Shun, E. H. K., Situ, J.-W., Tsoi, J. Y. H., Wu, S.-S., Cai, J.-P., Lo, K. H.-Y., Chew, N., Li, Z., Poon, R., Teng, J. L., et al. (2024) · Emerging Microbes and Infections · doi:10.1080/22221751.2024.2337671 · Cited by 16
“Red foxes, also members of the family Canidae , have been putatively linked to a Rocahepevirus -like HEV variant that is distantly related to vole HEV ( Rocahepevirus eothenomi ) [44,45].”
BackgroundCanuti, M., Pénzes, J., & Lang, A. S. (2022) · Virus Evolution · doi:10.1093/ve/veac056 · Cited by 16
Novel orthohepeviruses in wild rodents from São Paulo State, Brazil
de Souza, W. M., Romeiro, M. F., Sabino-Santos, G., Maia, F. G. M., Fumagalli, M., Modha, S., Nunes, M., Murcia, P., & Figueiredo, L. T. (2018) · Virology · doi:10.1016/j.virol.2018.03.025 · Cited by 16
“In this novel clade, the orthohepevirus identified in fecal samples of fox (Vulpes vulpes) in Netherlands, suggests that this virus could be derived from their prey (e.g., rats) (Bodewes et al., 2013).”
BackgroundStructural and antigenic characterization of the avian adeno-associated virus capsid
Hsi, J., Mietzsch, M., Chipman, P. R., Afione, S. A., Zeher, A., Huang, R. K., Chiorini, J. A., & McKENNA, R. V. (2023) · Journal of Virology · doi:10.1128/jvi.00780-23 · Cited by 14
Du, H., Zhang, L., Zhang, X., Yun, F., Chang, Y., Tuersun, A., Aisaiti, K., & Ma, Z. (2022) · Viruses · doi:10.3390/v14020356 · Cited by 15
Kurucz, K., Hederics, D., Bali, D., Kemenesi, G., Horváth, G., & Jakab, F. (2018) · Zoonoses and Public Health · doi:10.1111/zph.12543 · Cited by 15
Ferret hepatitis E virus infection in Japan.
Li, T.-C., Yonemitsu, K., Terada, Y., Takeda, N., Wakita, T., & Maeda, K. (2015) · Japanese journal of infectious diseases (Print) · doi:10.7883/yoken.jjid.2014.169 · Cited by 15
Sarchese, V., Fruci, P., Palombieri, A., Profio, F. D., Robetto, S., Ercolini, C., Orusa, R., Marsilio, F., Martella, V., & Martino, B. D. (2021) · Animals · doi:10.3390/ani11123465 · Cited by 14
“Since then, carnivore-derived HEV-C2 strains have been detected in liver and faecal specimens from farmed American minks in Denmark [13] and in faeces of red foxes in the Netherlands, Germany, and Hungary [12,15,16].”
BackgroundGallagher, C., Navarro, R., Cruz, K., Aung, M. S., Ng, A., Bajak, E., Beierschmitt, A., Lawrence, M., Dore, K. M., Ketzis, J., et al. (2017) · Virus Research · doi:10.1016/j.virusres.2016.12.021 · Cited by 14
Yonemitsu, K., Terada, Y., Kuwata, R., Nguyễn, D., Shiranaga, N., Tono, S., Matsukane, T., Yokoyama, M., Suzuki, K., Shimoda, H., et al. (2016) · Journal of Virological Methods · doi:10.1016/j.jviromet.2016.07.030 · Cited by 13
“…wild boars, rats (Rattus spp.), rabbits, ferrets (Mustela putorius furo), minks (Neovison vison), foxes (Vulpes vulpes) and bats (Chiroptera spp.) (Bodewes et al., 2013; Drexler et al., 2012; Johne et al., 2010a, 2010b; Krog et al., 2013; Lhomme et al., 2013; Raj et al., 2012; Takahashi et al.,…”
BackgroundIdentification of further diversity among posaviruses
Sano, K., Naoi, Y., Kishimoto, M., Masuda, T., Tanabe, H., Ito, M., Niira, K., Haga, K., Asano, K., Tsuchiaka, S., et al. (2016) · Archives of Virology · doi:10.1007/s00705-016-3048-8 · Cited by 13
Prevalence of Astroviruses in Different Animal Species in Poland
Kuczera, K., Orłowska, A., Smreczak, M., Frant, M., Trębas, P., & Rola, J. (2024) · Viruses · doi:10.3390/v16010080 · Cited by 12
“Metagenomics studies performed on rodents in China and red foxes in the Netherlands revealed novel rodent and fox astroviruses, respectively [31,32].”
BackgroundIdentification of Hepatitis E Virus in the Feces of Red Foxes (Vulpes vulpes)
Lanszki, Z., Kurucz, K., Zeghbib, S., Kemenesi, G., Lanszki, J., & Jakab, F. (2020) · Animals · doi:10.3390/ani10101841 · Cited by 12
“Furthermore, it showed a lower nucleotide similarity (85%) to Fox Hepatitis E virus described previously in fecal samples of the red fox (KC692370) from the Netherlands [8].”
BackgroundResultEndemic Skunk amdoparvovirus in free-ranging striped skunks (Mephitis mephitis) in California.
Glueckert, E., Clifford, D., Brenn-White, M., Ochoa, J., Gabriel, M., Wengert, G. M., & Foley, J. (2019) · Transboundary and Emerging Diseases · doi:10.1111/tbed.13272 · Cited by 12
Detection of anti-viral antibodies from meat juice of wild boars
Yonemitsu, K., Minami, S., Noguchi, K., Kuwata, R., Shimoda, H., & Maeda, K. (2018) · Journal of Veterinary Medical Science · doi:10.1292/jvms.18-0576 · Cited by 12
A surveillance study of hepatitis E virus infection in household cats.
Capozza, P., Martella, V., Lanave, G., Beikpour, F., Profio, F. D., Palombieri, A., Sarchese, V., Marsilio, F., Rosa, G. L., Suffredini, E., et al. (2021) · Research in Veterinary Science · doi:10.1016/j.rvsc.2021.04.022 · Cited by 11
Molecular characterization of a novel picobirnavirus in a chicken
Pankovics, P., Boros, Á., Nemes, C., Kapusinszky, B., Delwart, E., & Reuter, G. (2018) · Archives of Virology · doi:10.1007/s00705-018-4012-6 · Cited by 11
Detection and evolutionary analysis of picobirnaviruses in treated wastewater
Zhang, S., Bai, R., Feng, R., Zhang, H.-X., & Liu, L. (2014) · Microbial Biotechnology · doi:10.1111/1751-7915.12239 · Cited by 11
“…of hosts, including humans (Smits et al., 2012), rabbits (Ludert et al., 1995; Green et al., 1999), pigs (Martínez et al., 2010; Smits et al., 2011), cattle (Ghosh et al., 2009), horses (Ganesh et al., 2011), birds (Chandra, 1997), monkeys (Wang et al., 2007; 2012) and foxes (Bodewes et al., 2013).”
BackgroundUllah, K., Mehmood, A., Chen, X., Dar, M., Yang, S.-X., & Zhang, W. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198624 · Cited by 9
The amazing AAV capsids: Into the structure-verse
Hsi, J., Mietzsch, M., & McKENNA, R. V. (2025) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2025.101629 · Cited by 9
Gallagher, M. D., Matějusová, I., Ruane, N. M., & Macqueen, D. J. (2020) · Aquaculture · doi:10.1016/j.aquaculture.2020.735117 · Cited by 14
Isolating Natural Adeno-Associated Viruses from Primate Tissues with a High-Fidelity Polymerase
Wang, Q., Nambiar, K., & Wilson, J. M. (2021) · Human Gene Therapy · doi:10.1089/hum.2021.055 · Cited by 8
“18,19 Using PCR to amplify AAV is a straightforward and effective means for discovering novel AAV capsid sequences.”
Trends and Challenges in the Detection and Environmental Surveillance of the Hepatitis E Virus
Elois, M., Pavi, C. P., Jempierre, Y. F. S. H., Pilati, G. V. T., Zanchetta, L., Grisard, H. B. D. S., García, N., Rodríguez-Lázaro, D., & Fongaro, G. (2025) · Microorganisms · doi:10.3390/microorganisms13050998 · Cited by 6
“…[156–158], ferrets [159], camels [160–162], musks [163], rats [164–175], mice [176,177], voles [176,178], minks [179,180], shrews [171], foxes [181], bats [182–184], monkeys [185–188], bisons [189], bears [190], macaques [1,188,191–199], cats [200,201], chimpanzees [186,198,202–205], leopards…”
Newlavirus, a Novel, Highly Prevalent, and Highly Diverse Protoparvovirus of Foxes (Vulpes spp.)
Canuti, M., Bouchard, É., Rodrigues, B., Whitney, H., Hopson, M., Gilroy, C., Stenson, G., Dufour, S., Lang, A. S., & Verhoeven, J. (2021) · Viruses · doi:10.3390/v13101969 · Cited by 6
“The genus Protoparvovirus currently includes 17 species, 15 official and two proposed [1,2,13,35], five of which are viruses of carnivores including three detected at least once in foxes [8,9,15].”
BackgroundKaiser, F., de le Roi, M., Jo, W., Gerhauser, I., Molnár, V., Osterhaus, A., Baumgärtner, W., & Ludlow, M. (2023) · Viruses · doi:10.3390/v15051087 · Cited by 5
Self-citationNovel bisegmented virus (picobirnavirus) of animals, birds and humans.
Mondal, A., & Majee, S. (2014) · doi:10.1016/s2222-1808(14)60333-9 · Cited by 5
Prpić, J., Kunić, A., Keros, T., Lojkić, I., Brnić, D., & Jemeršić, L. (2023) · Microorganisms · doi:10.3390/microorganisms11040834 · Cited by 4
High Prevalence of Genogroup I and Genogroup II Picobirnaviruses in Dromedary Camels
Teng, J. L., Wernery, U., Wong, P.-C., Chan, E., Lee, H. H., Joseph, S., Bai, R., Tang, Y., Wong, E. Y. M., Lau, S., et al. (2021) · Viruses · doi:10.3390/v13030430 · Cited by 4
“Consistent with the organization of segment 1 of other genogroup I PBVs [18,35,36], a short ORF was observed upstream of the capsid protein, with complete sequences of 136 to 225 amino acids determined from 15C, 17C, and 78C (Table 2).”
BackgroundHepatitis A and E in South America: New Challenges Toward Prevention and Control
Pinto, M., de Oliveira, J. D., & González, J. (2017) · doi:10.1007/978-3-319-54567-7_7 · Cited by 3
Metagenomic Analysis of the Fecal Virome in Wild Mammals Hospitalized in Pisa, Italy
Pacini, M. I., Forzan, M., Sgorbini, M., Cingottini, D., & Mazzei, M. (2025) · Veterinary Sciences · doi:10.3390/vetsci12090820 · Cited by 2
“…encompass both targeted investigations—employing classical molecular methods to detect specific pathogens within selected species [33,38,39,41,42]—and broader surveys aiming to characterize the fecal virome of wildlife using next-generation sequencing (NGS)-based metagenomics [9,34–37, 41, 43 ].”
Wang, Y., Guo, X., Chang, S., Zhao, L., Li, A., Liu, X.-B., Ma, H., & Li, Y.-D. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.137366 · Cited by 2
Detection at high prevalence of newlavirus (protoparvovirus) in the carcasses of red foxes
Lanave, G., Ndiana, L. A., Pellegrini, F., Diakoudi, G., Martino, B. D., Sgroi, G., Alessio, N. D., Vasinioti, V., Camero, M., Canuti, M., et al. (2022) · Virus Research · doi:10.1016/j.virusres.2022.198971 · Cited by 2
Genomics and Foodborne Viral Infections
Smits, S., & Koopmans, M. (2017) · Applied Genomics of Foodborne Pathogens · doi:10.1007/978-3-319-43751-4_9 · Cited by 2
“Four major genotypes are discerned and novel lineages of hepatitis E viruses have been identified in rabbits, rats, wild boar, ferrets and possibly foxes more recently [78] [79] [80] [81] [82] [83] [84] .”
BackgroundSelf-citationHepatitis E virus infection: a zoonotic threat.
Saxena, V., & Arora, S. (2014) · doi:10.14737/journal.aavs/2014/2.10.582.591 · Cited by 2
“Fox Bodewes et al. (2013), in their attempt to study viral microbiome in red foxes (Vulpes vulpes), evaluated fecal samples of 13 red foxes by random PCR and sequencing.”
Pacini, M. I., Forzan, M., & Mazzei, M. (2025) · Animals · doi:10.3390/ani15233378 · Cited by 1
“…viral diversity across taxa and geographical regions: novel members of the Parvoviridae and Hepeviridae family in red foxes in the Netherlands [12], diverse Astroviridae members in wild boars and cervids [18–20], and novel Picornaviridae and Picobirnaviridae in small carnivores and rodents…”
InfluentialDiversity of viral communities in faecal samples of farmed red foxes
Zhang, D., Wang, Y., Chen, X., He, Y., Zhao, M., Lü, X., Lü, J., Ji, L., Shen, Q., Wang, X., et al. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e12826 · Cited by 1
Red fox viromes across an urban-rural gradientPreprint
Campbell, S. J., Ashley, W., Gil-Fernández, M., Newsome, T., Giallonardo, F. D., Ortiz-Baez, A., Mahar, J., Towerton, A. L., Gillings, M., Holmes, E., et al. (2020) · bioRxiv · doi:10.1101/2020.06.15.153858 · Cited by 1
“95 Although red foxes are known to harbour a diversity of viruses (27, 28), it is unknown whether urban and 96 rural foxes have different viral compositions.”
BackgroundResultInfluential
Metadata
- Authors
- Bodewes, R., van der Giessen, J., Haagmans, B. L., Osterhaus, A. D. M. E., & Smits, S. L.
- Affiliations
- Erasmus MC (NL)
- National Institute for Public Health and the Environment (NL)
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2013-07
- Volume
- 87
- Issue
- 13
- Pages
- 7758-7764
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC3700315
- OpenAlex
- W2016522317
- Cited by
- 117
- References
- 56
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 7 · 2022: 6 · 2021: 8 · 2020: 12 · 2019: 7 · 2018: 12 · 2017: 9 · 2016: 5 · 2015: 13 · 2014: 21 · 2013: 5
- FWCI
- 24.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Rivm Repository (Netherlands National Institute for Public Health and the Environment) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
- Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
- Keywords
- red fox, novel virus, parvovirus, bocavirus, adeno-associated virus, astrovirus, wildlife reservoirs, zoonotic transmission, viral metagenomics
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Disease Reservoirs, Feces, Foxes, Models, Genetic, Molecular Sequence Data, Phylogeny, Species Specificity, Likelihood Functions, Polymerase Chain Reaction, Sequence Analysis, DNA, Parvovirus, Picobirnavirus, Astroviridae, Hepevirus, Metagenome
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