Detection of serum antibodies to hepatitis E virus in domestic pigs in Italy using a recombinant swine HEV capsid protein

BMC Veterinary Research

Volumn 10, Issue , 2014, Pages

  Ponterio, Eleonora ^a   Di Bartolo, Ilaria ^a   Orrù, Ginevra ^b   Liciardi, Manuel ^b   Ostanello, Fabio ^c   Ruggeri, Franco M ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA SARDEGNA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

ELISA; Hepatitis E virus; ORF2; Swine; Western blotting

Indexed keywords

CAPSID PROTEIN; RECOMBINANT PROTEIN; VIRUS ANTIBODY;

ANIMAL; BLOOD; CELL LINE; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; GENOTYPE; HEPATITIS E; HEPATITIS E VIRUS; IMMUNOLOGY; METABOLISM; MOTH; PIG; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SWINE DISEASE; VETERINARY; VIROLOGY;

ANIMALS; ANTIBODIES, VIRAL; CAPSID PROTEINS; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENOTYPE; HEPATITIS E; HEPATITIS E VIRUS; MOTHS; RECOMBINANT PROTEINS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SWINE; SWINE DISEASES;

EID: 84903475290     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-10-133     Document Type: Article

References (43)

1. Garbuglia AR, Scognamiglio P, Petrosillo N, Mastroianni CM, Sordillo P, Gentile D, La Scala P, Girardi E, Capobianchi MR. Hepatitis E virus genotype 4 outbreak, Italy, 2011. Emerg Infect Dis 2013, 19(1):110-114. 10.3201/eid1901.120983, 3558000, 23260079.
2. Dalton HR, Stableforth W, Thurairajah P, Hazeldine S, Remnarace R, Usama W, Farrington L, Hamad N, Sieberhagen C, Ellis V, Mitchell J, Hussaini SH, Banks M, Ijaz S, Bendall RP. Autochthonous hepatitis E in Southwest England: natural history, complications and seasonal variation, and hepatitis E virus IgG seroprevalence in blood donors, the elderly and patients with chronic liver disease. Eur J Gastroenterol Hepatol 2008, 20(8):784-790. 10.1097/MEG.0b013e3282f5195a, 18617784.
3. Ijaz S, Vyse AJ, Morgan D, Pebody RG, Tedder RS, Brown D. Indigenous hepatitis E virus infection in England: more common than it seems. J Clin Virol 2009, 44(4):272-276. 10.1016/j.jcv.2009.01.005, 19217345.
4. Colson P, Romanet P, Moal V, Borentain P, Purgus R, Benezech A, Motte A, Gerolami R. Autochthonous infections with hepatitis E virus genotype 4, France. Emerg Health Serv Rev 2012, 18(8):1361-1364.
5. Emerson SU AA, Arankalle XJ, Meng XJ, Purdy M, Schlauder GG, Tsarev SA. Hepevirus. Virus Taxonomy, VIIth Report of the ICTV 2004, 851-855. London: Elsevier/Academic Press, CM Fauquet MM, Maniloff J, Desselberg U, Ball LA.
6. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K, Nagashima S, Tanaka T, Okamoto H. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J Gen Virol 2009, 90(Pt 8):1880-1891.
7. Meng XJ. Zoonotic and foodborne transmission of hepatitis E virus. Semin Liver Dis 2013, 33(1):41-49.
8. Johne R, Heckel G, Plenge-Bonig A, Kindler E, Maresch C, Reetz J, Schielke A, Ulrich RG. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 2010, 16(9):1452-1455. 10.3201/eid1609.100444, 3294985, 20735931.
9. Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H, Osterhaus AD, Haagmans BL. Novel hepatitis E virus in ferrets, the Netherlands. Emerg Infect Dis 2012, 18(8):1369-1370. 10.3201/eid1808.111659, 3414025, 22840220.
10. Bodewes R, van der Giessen J, Haagmans BL, Osterhaus AD, Smits SL. Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J Virol 2013, 87(13):7758-7764. 10.1128/JVI.00568-13, 3700315, 23616657.
11. Drexler JF, Seelen A, Corman VM, Fumie Tateno A, Cottontail V, Melim Zerbinati R, Gloza-Rausch F, Klose SM, Adu-Sarkodie Y, Oppong SK, Kalko EK, Osterman A, Rasche A, Adam A, Müller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 2012, 86(17):9134-9147. 10.1128/JVI.00800-12, 3416139, 22696648.
12. Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU. A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A 1997, 94(18):9860-9865. 10.1073/pnas.94.18.9860, 23282, 9275216.
13. Schlauder GG, Dawson GJ, Erker JC, Kwo PY, Knigge MF, Smalley DL, Rosenblatt JE, Desai SM, Mushahwar IK. The sequence and phylogenetic analysis of a novel hepatitis E virus isolated from a patient with acute hepatitis reported in the United States. J Gen Virol 1998, 79(Pt 3):447-456.
14. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, Toth TE, Meng XJ. 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 2002, 40(4):1326-1332. 10.1128/JCM.40.4.1326-1332.2002, 140370, 11923352.
15. Mansuy JM, Peron JM, Abravanel F, Poirson H, Dubois M, Miedouge M, Vischi F, Alric L, Vinel JP, Izopet J. Hepatitis E in the south west of France in individuals who have never visited an endemic area. J Med Virol 2004, 74(3):419-424. 10.1002/jmv.20206, 15368508.
16. Di Bartolo I, Ponterio E, Castellini L, Ostanello F, Ruggeri FM. Viral and antibody HEV prevalence in swine at slaughterhouse in Italy. Vet Microbiol 2011, 149(3-4):330-338.
17. Colson P, Borentain P, Queyriaux B, Kaba M, Moal V, Gallian P, Heyries L, Raoult D, Gerolami R. Pig liver sausage as a source of hepatitis E virus transmission to humans. J Infect Dis 2010, 202(6):825-834. 10.1086/655898, 20695796.
18. Di Bartolo I, Diez-Valcarce M, Vasickova P, Kralik P, Hernandez M, Angeloni G, Ostanello F, Bouwknegt M, Rodriguez-Lazaro D, Pavlik I, Ruggeri FM. Hepatitis E virus in pork production chain in Czech Republic, Italy, and Spain, 2010. Emerg Infect Dis 2012, 18(8):1282-1289. 3414029, 22840221.
19. Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ. Detection and characterization of infectious Hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J Gen Virol 2007, 88(Pt 3):912-917.
20. Choi JY, Lee JM, Jo YW, Min HJ, Kim HJ, Jung WT, Lee OJ, Yun H, Yoon YS. Genotype-4 hepatitis E in a human after ingesting roe deer meat in South Korea. Clin Mol Hepatol 2013, 19(3):309-314. 10.3350/cmh.2013.19.3.309, 3796682, 24133670.
21. Kanai Y, Tsujikawa M, Yunoki M, Nishiyama S, Ikuta K, Hagiwara K. Long-term shedding of hepatitis E virus in the feces of pigs infected naturally, born to sows with and without maternal antibodies. J Med Virol 2010, 82(1):69-76. 10.1002/jmv.21647, 19950246.
22. Panda SK, Thakral D, Rehman S. Hepatitis E virus. Rev Med Virol 2007, 17(3):151-180. 10.1002/rmv.522, 17051624.
23. Satou K, Nishiura H. Transmission dynamics of hepatitis E among swine: potential impact upon human infection. BMC Vet Res 2007, 3:9. 10.1186/1746-6148-3-9, 1885244, 17493260.
24. 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(1-2):66-73.
25. Rose N, Boutrouille A, Fablet C, Madec F, Eloit M, Pavio N. The use of Bayesian methods for evaluating the performance of a virus-like particles-based ELISA for serology of hepatitis E virus infection in swine. J Virol Methods 2010, 163(2):329-335. 10.1016/j.jviromet.2009.10.019, 19879297.
26. Casas M, Pujols J, Rosell R, de Deus N, Peralta B, Pina S, Casal J, Martin M. Retrospective serological study on hepatitis E infection in pigs from 1985 to 1997 in Spain. Vet Microbiol 2009, 135(3-4):248-252.
27. Hadgu A, Qu Y. A biomedical appication of latent class models with random effects. Appl Stat 1998, 47:603-616.
28. Jimenez de Oya N, Galindo I, Girones O, Duizer E, Escribano JM, Saiz JC. Serological immunoassay for detection of hepatitis E virus on the basis of genotype 3 open reading frame 2 recombinant proteins produced in Trichoplusia ni larvae. J Clin Microbiol 2009, 47(10):3276-3282. 10.1128/JCM.00750-09, 2756903, 19656986.
29. Engle RE, Yu C, Emerson SU, Meng XJ, Purcell RH. Hepatitis E virus (HEV) capsid antigens derived from viruses of human and swine origin are equally efficient for detecting anti-HEV by enzyme immunoassay. J Clin Microbiol 2002, 40(12):4576-4580. 10.1128/JCM.40.12.4576-4580.2002, 154628, 12454155.
30. Li TC, Yamakawa Y, Suzuki K, Tatsumi M, Razak MA, Uchida T, Takeda N, Miyamura T. Expression and self-assembly of empty virus-like particles of hepatitis E virus. J Virol 1997, 71(10):7207-7213. 192060, 9311793.
31. Li TC, Yoshimatsu K, Yasuda SP, Arikawa J, Koma T, Kataoka M, Ami Y, Suzaki Y, le Mai TQ, Hoa NT, Yamashiro T, Hasebe F, Takeda N, Wakita T. Characterization of self-assembled virus-like particles of rat hepatitis E virus generated by recombinant baculoviruses. J Gen Virol 2011, 92(Pt 12):2830-2837. 3352569, 21865442.
32. Li SW, Zhang J, Li YM, Ou SH, Huang GY, He ZQ, Ge SX, Xian YL, Pang SQ, Ng MH, Xia NS. A bacterially expressed particulate hepatitis E vaccine: antigenicity, immunogenicity and protectivity on primates. Vaccine 2005, 23(22):2893-2901. 10.1016/j.vaccine.2004.11.064, 15780738.
33. Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, Wang H, Yang CL, Jiang HM, Cai JP, Wang YJ, Ai X, Hu YM, Tang Q, Yao X, Yan Q, Xian YL, Wu T, Li YM, Miao J, Ng MH, Shih JW, Xia NS. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet 2010, 376(9744):895-902. 10.1016/S0140-6736(10)61030-6, 20728932.
34. Meng J, Dai X, Chang JC, Lopareva E, Pillot J, Fields HA, Khudyakov YE. Identification and characterization of the neutralization epitope(s) of the hepatitis E virus. Virology 2001, 288(2):203-211. 10.1006/viro.2001.1093, 11601892.
35. Lee WJ, Shin MK, Cha SB, Yoo HS. Development of a novel enzyme-linked immunosorbent assay to detect Anti-IgG against swine hepatitis E virus. J Vet Sci 2013, 14(4):467-472. 10.4142/jvs.2013.14.4.467, 3885741, 24421718.
36. Chaussade H, Rigaud E, Allix A, Carpentier A, Touze A, Delzescaux D, Choutet P, Garcia-Bonnet N, Coursaget P. Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals. J Clin Virol 2013, 58(3):504-508. 10.1016/j.jcv.2013.08.030, 24084601.
37. Shenyang G, Dandan L, Chen F, Shuliang W, Tiezhong Z. Design and evaluation of a recombinant multi-epitope-based ELISA for the serological surveillance of HEV infection in northern China. Arch Virol 2011, 156(9):1621-1626. 10.1007/s00705-011-1007-y, 21544544.
38. Herremans M, Bakker J, Duizer E, Vennema H, Koopmans MP. Use of serological assays for diagnosis of hepatitis E virus genotype 1 and 3 infections in a setting of low endemicity. Clin Vaccine Immunol 2007, 14(5):562-568. 10.1128/CVI.00231-06, 1865643, 17360853.
39. Fogeda M, de Ory F, Avellon A, Echevarria JM. Differential diagnosis of hepatitis E virus, cytomegalovirus and Epstein-Barr virus infection in patients with suspected hepatitis E. J Clin Virol 2009, 45(3):259-261. 10.1016/j.jcv.2009.05.022, 19505848.
40. Meng XJ. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 2010, 140(3-4):256-265. 2814965, 19361937.
41. Casas M, Cortes R, Pina S, Peralta B, Allepuz A, Cortey M, Casal J, Martin M. Longitudinal study of hepatitis E virus infection in Spanish farrow-to-finish swine herds. Vet Microbiol 2011, 148(1):27-34. 10.1016/j.vetmic.2010.08.010, 20863630.
42. Masia G, Orru G, Liciardi M, Desogus G, Coppola RC, Murru V, Argiolas M, Orru G. Evidence of hepatitis E virus (HEV) infection in human and pigs in Sardinia, Italy. J Prev Med Hyg 2009, 50(4):227-231.
43. Zakhour M, Maalouf H, Di Bartolo I, Haugarreau L, Le Guyader FS, Ruvoen-Clouet N, Le Saux JC, Ruggeri FM, Pommepuy M, Le Pendu J. Bovine norovirus: carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters. Appl Environ Microbiol 2010, 76(19):6404-6411. 10.1128/AEM.00671-10, 2950446, 20709837.