Presence of Hepatitis E Virus in a RED Deer (Cervus elaphus) Population in Central Italy

Transboundary and Emerging Diseases

Volumn 64, Issue 1, 2017, Pages 137-143

  Di Bartolo, I ^a   Ponterio, E ^a   Angeloni, G ^a   Morandi, F ^b   Ostanello, F ^c   Nicoloso, S ^d   Ruggeri, F M ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Servizio gestione del territorio e sviluppo sostenibile   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d DREAM Italia ^*  (Italy)

Author keywords

anti HEV IgG; genotype 3; hepatitis E; red deer; Zoonoses

Indexed keywords

HEPATITIS ANTIBODY; IMMUNOGLOBULIN G;

ANIMAL; BLOOD; DEER; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEPATITIS E; HEPATITIS E VIRUS; IMMUNOLOGY; ITALY; MALE; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; VETERINARY; VIROLOGY;

ANIMALS; DEER; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEPATITIS ANTIBODIES; HEPATITIS E; HEPATITIS E VIRUS; IMMUNOGLOBULIN G; ITALY; MALE; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; SEQUENCE ANALYSIS, DNA;

EID: 84928139226     PISSN: 18651674     EISSN: 18651682     Source Type: Journal    
DOI: 10.1111/tbed.12353     Document Type: Article

References (35)

1. Boadella, M., M. Casas, M. Martin, J. Vicente, J. Segales, J. de la Fuente, and C. Gortazar, 2010: Increasing contact with hepatitis E virus in red deer, Spain. Emerg. Infect. Dis. 16, 1994–1996.
2. Carpentier, A., H. Chaussade, E. Rigaud, J. Rodriguez, C. Berthault, F. Boue, M. Tognon, A. Touze, N. Garcia-Bonnet, P. Choutet, and P. Coursaget, 2012: High hepatitis E virus seroprevalence in forestry workers and in wild boars in France. J. Clin. Microbiol. 50, 2888–2893.
3. Caruso, C., P. Modesto, S. Bertolini, S. Peletto, P. L. Acutis, A. Dondo, S. Robetto, W. Mignone, R. Orusa, G. Ru, and L. Masoero, 2014: Serological and virological survey of hepatitis E virus in wild boar populations in northwestern Italy: detection of HEV subtypes 3e and 3f. Arch. Virol. 160, 153–160.
4. Colson, P., P. Borentain, B. Queyriaux, M. Kaba, V. Moal, P. Gallian, L. Heyries, D. Raoult, and R. Gerolami, 2010: Pig liver sausage as a source of hepatitis E virus transmission to humans. J. Infect. Dis. 202, 825–834.
5. Di Bartolo, I., F. Martelli, N. Inglese, M. Pourshaban, A. Caprioli, F. Ostanello, and F. M. Ruggeri, 2008: Widespread diffusion of genotype 3 hepatitis E virus among farming swine in Northern Italy. Vet. Microbiol. 132, 47–55.
6. Di Bartolo, I., E. Ponterio, L. Castellini, F. Ostanello, and F. M. Ruggeri, 2011: Viral and antibody HEV prevalence in swine at slaughterhouse in Italy. Vet. Microbiol. 149, 330–338.
7. Di Bartolo, I., M. Diez-Valcarce, P. Vasickova, P. Kralik, M. Hernandez, G. Angeloni, F. Ostanello, M. Bouwknegt, D. Rodriguez-Lazaro, I. Pavlik, and F. M. Ruggeri, 2012: Hepatitis E virus in pork production chain in Czech Republic, Italy, and Spain, 2010. Emerg. Infect. Dis. 18, 1282–1289.
8. Di Bartolo, I., G. Angeloni, E. Ponterio, F. Ostanello, and F. M. Ruggeri, 2015: Detection of hepatitis E virus in pork liver sausages. Int. J. Food Microbiol. 193, 29–33.
9. Forgach, P., N. Nowotny, K. Erdelyi, A. Boncz, J. Zentai, G. Szucs, G. Reuter, and T. Bakonyi, 2010: Detection of hepatitis E virus in samples of animal origin collected in Hungary. Vet. Microbiol. 143, 106–116.
10. Garbuglia, A. R., P. Scognamiglio, N. Petrosillo, C. M. Mastroianni, P. Sordillo, D. Gentile, P. La Scala, E. Girardi, and M. R. Capobianchi, 2013: Hepatitis e virus genotype 4 outbreak, Italy, 2011. Emerg. Infect. Dis. 19, 110–114.
11. Gyarmati, P., N. Mohammed, H. Norder, J. Blomberg, S. Belak, and F. Widen, 2007: Universal detection of hepatitis E virus by two real-time PCR assays: TaqMan and Primer-Probe Energy Transfer. J. Virol. Methods 146, 226–235.
12. Huang, F. F., G. Haqshenas, D. K. Guenette, P. G. Halbur, S. K. Schommer, F. W. Pierson, T. E. Toth, and X. J. Meng, 2002: Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J. Clin. Microbiol. 40, 1326–1332.
13. Izopet, J., M. Dubois, S. Bertagnoli, S. Lhomme, S. Marchandeau, S. Boucher, N. Kamar, F. Abravanel, and J. L. Guerin, 2012: Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis. 18, 1274–1281.
14. Johne, R., P. Dremsek, J. Reetz, G. Heckel, M. Hess, and R. G. Ulrich, 2014: Hepeviridae: an expanding family of vertebrate viruses. Infect. Genet. Evol. 27C, 212–229.
15. Kamar, N., R. Bendall, F. Legrand-Abravanel, N. S. Xia, S. Ijaz, J. Izopet, and H. R. Dalton, 2012: Hepatitis E. Lancet 379, 2477–2488.
16. Kukielka, D., V. Rodriguez-Prieto, J. Vicente, and J. M. Sanchez-Vizcaino, 2016: Constant hepatitis E virus (HEV) circulation in wild boar and red deer in Spain: an increasing concern source of HEV Zoonotic transmission. Transbound. Emerg. Dis. 63, e360–e368.
17. La Rosa, G., M. Muscillo, V. S. Vennarucci, A. R. Garbuglia, P. La Scala, and M. R. Capobianchi, 2011: Hepatitis E virus in Italy: molecular analysis of travel-related and autochthonous cases. J. Gen. Virol. 92, 1617–1626.
18. Martelli, F., A. Caprioli, M. Zengarini, A. Marata, C. Fiegna, I. Di Bartolo, F. M. Ruggeri, M. Delogu, and F. Ostanello, 2008: Detection of hepatitis E virus (HEV) in a demographic managed wild boar (Sus scrofa scrofa) population in Italy. Vet. Microbiol. 126, 74–81.
19. Martinelli, N., E. Pavoni, D. Filogari, N. Ferrari, M. Chiari, E. Canelli, and G. Lombardi, 2015: Hepatitis E Virus in Wild Boar in the Central Northern Part of Italy. Transbound. Emerg. Dis. 62, 217–222.
20. Matsuura, Y., M. Suzuki, K. Yoshimatsu, J. Arikawa, I. Takashima, M. Yokoyama, H. Igota, K. Yamauchi, S. Ishida, D. Fukui, G. Bando, M. Kosuge, H. Tsunemitsu, C. Koshimoto, K. Sakae, M. Chikahira, S. Ogawa, T. Miyamura, N. Takeda, and T. C. Li, 2007: Prevalence of antibody to hepatitis E virus among wild sika deer, Cervus nippon, in Japan. Arch. Virol. 152, 1375–1381.
21. Meng, X. J., 2013: Zoonotic and foodborne transmission of hepatitis E virus. Semin. Liver Dis. 33, 41–49.
22. Monne, I., L. Ceglie, D. I. M. G, A. Natale, S. Zamprogna, A. Morreale, E. Rampazzo, G. Cattoli, and L. Bonfanti, 2015: Hepatitis E virus genotype 4 in a pig farm, Italy, 2013. Epidemiol. Infect., 143, 529–533.
23. Nicoloso, S., Viliani M., Mattioli S., and Riga F., 2010: Analisi consultiva stagioni faunistico-venatorie dal 2005-06 al 2009-10 e programma annuale operativo di gestione del cervo 2010–2011. Available at: http://agricoltura.regione.emilia-romagna.it/caccia/temi/ungulati/documenti-ungulati/acater-centrale/relazioni-consuntive-dal-2005-6-al-2009-10-e-programma-annuale-operativo-2010-2011/view
24. Pavio, N., X. J. Meng, and C. Renou, 2010: Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet. Res. 41, 46.
25. Ponterio, E., I. Di Bartolo, G. Orru, M. Liciardi, F. Ostanello, and F. M. Ruggeri, 2014: Detection of serum antibodies to hepatitis E virus in domestic pigs in Italy using a recombinant swine HEV capsid protein. BMC Vet. Res. 10, 133.
26. Romano, L., S. Paladini, C. Tagliacarne, M. Canuti, S. Bianchi, and A. R. Zanetti, 2011: Hepatitis E in Italy: a long-term prospective study. J. Hepatol. 54, 34–40.
27. Ruggeri, F. M., I. Di Bartolo, E. Ponterio, G. Angeloni, M. Trevisani, and F. Ostanello, 2013: Zoonotic transmission of hepatitis E virus in industrialized countries. New Microbiol. 36, 331–344.
28. Rutjes, S. A., F. Lodder-Verschoor, W. J. Lodder, J. van der Giessen, H. Reesink, M. Bouwknegt, and A. M. de Roda Husman, 2010: Seroprevalence and molecular detection of hepatitis E virus in wild boar and red deer in The Netherlands. J. Virol. Methods 168, 197–206.
29. Scobie, L., V. Padler-Karavani, S. Le Bas-Bernardet, C. Crossan, J. Blaha, M. Matouskova, R. D. Hector, E. Cozzi, B. Vanhove, B. Charreau, G. Blancho, L. Bourdais, M. Tallacchini, J. M. Ribes, H. Yu, X. Chen, J. Kracikova, L. Broz, J. Hejnar, P. Vesely, Y. Takeuchi, A. Varki, and J. P. Soulillou, 2013: Long-term IgG response to porcine Neu5Gc antigens without transmission of PERV in burn patients treated with porcine skin xenografts. J. Immunol. 191, 2907–2915.
30. Smith, D. B., P. Simmonds, S. Jameel, S. U. Emerson, T. J. Harrison, X. J. Meng, H. Okamoto, W. H. Van der Poel, and M. A. Purdy, 2014: Consensus proposals for classification of the family Hepeviridae. J. Gen. Virol. 95, 2223–2232.
31. Sonoda, H., M. Abe, T. Sugimoto, Y. Sato, M. Bando, E. Fukui, H. Mizuo, M. Takahashi, T. Nishizawa, and H. Okamoto, 2004: 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. 42, 5371–5374.
32. Tamura, K., G. Stecher, D. Peterson, A. Filipski, and S. Kumar, 2013: MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.
33. Tei, S., N. Kitajima, K. Takahashi, and S. Mishiro, 2003: Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362, 371–373.
34. Wang, Y., R. Ling, J. C. Erker, H. Zhang, H. Li, S. Desai, I. K. Mushahwar, and T. J. Harrison, 1999: A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J. Gen. Virol. 80(Pt 1), 169–177.
35. Zakhour, M., H. Maalouf, I. Di Bartolo, L. Haugarreau, F. S. Le Guyader, N. Ruvoen-Clouet, J. C. Le Saux, F. M. Ruggeri, M. Pommepuy, and J. Le Pendu, 2010: Bovine norovirus: carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters. Appl. Environ. Microbiol. 76, 6404–6411.