1887
  1. Home
  2. Eurosurveillance
  3. Volume 23, Issue 49, 06/Dec/2018
  4. Article
Research article Open Access
Like 0
Download

Abstract

Introduction

The zoonotic hepatitis E virus (HEV) genotype 3 (HEV-G3) has become a common cause of acute and chronic hepatitis among humans worldwide. In Israel, while HEV-3 sequences have previously been detected in sewage, only the non-zoonotic HEV-G1 genotype has been found in samples from human patients.

Aim

In this pilot study, we aimed to assess the status of HEV in a sample of the swine population and among swine farm workers in Israel.

Methods

Pig blood (n = 141) and faecal samples (n = 39), pig farm sewage samples (n = 8) and blood from farm workers (n = 24) were collected between February 2016 and October 2017. Anti-HEV IgG was detected using the Wantai assay. HEV RNA was analysed with the RealStar HEV kit. HEV open reading frame 1 fragments amplified from representative HEV RNA-positive samples were used for phylogenetic analysis.

Results

Overall prevalence of HEV antibodies in pigs was 75.9% (107/141). HEV RNA was detected in plasma (2.1%, 3/141), faecal (22.8%, 18/79) and pig sewage (4/8) samples. Pig and sewage-derived viral sequences clustered with previously identified human sewage HEV-G3 sequences. Most pig farms workers (23 of 24) were HEV-seropositive; none was viraemic or reported previous clinical signs.

Conclusions

This study showed that domestic pigs in Israel are infected with HEV-G3. The high HEV seropositivity of the farm workers together with the previous identification of this virus in human sewage suggests circulation to humans. The clinical impact of these findings on public health should be further explored.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2018.23.49.1800067
2018-12-06
2024-12-30
/content/10.2807/1560-7917.ES.2018.23.49.1800067
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/23/49/eurosurv-23-49-2.html?itemId=/content/10.2807/1560-7917.ES.2018.23.49.1800067&mimeType=html&fmt=ahah

References

  1. Nimgaonkar I, Ding Q, Schwartz RE, Ploss A. Hepatitis E virus: advances and challenges. Nat Rev Gastroenterol Hepatol. 2018;15(2):96-110.  https://doi.org/10.1038/nrgastro.2017.150  PMID: 29162935 
  2. Pérez-Gracia MT, Suay-García B, Mateos-Lindemann ML. Hepatitis E and pregnancy: current state. Rev Med Virol. 2017;27(3):e1929.  https://doi.org/10.1002/rmv.1929  PMID: 28318080 
  3. Sridhar S, Teng JLL, Chiu TH, Lau SKP, Woo PCY. Hepatitis E virus genotypes and evolution: emergence of camel hepatitis E variants. Int J Mol Sci. 2017;18(4):E869.; Epub ahead of print.  https://doi.org/10.3390/ijms18040869  PMID: 28425927 
  4. Ahmed A, Ali IA, Ghazal H, Fazili J, Nusrat S. Mystery of hepatitis e virus: recent advances in its diagnosis and management. Int J Hepatol. 2015;2015:872431.  PMID: 25692043 
  5. Berto A, Grierson S, Hakze-van der Honing R, Martelli F, Johne R, Reetz J, et al. Hepatitis E virus in pork liver sausage, France. Emerg Infect Dis. 2013;19(2):264-6. d PMID: 23347828 
  6. Domanović D, Tedder R, Blümel J, Zaaijer H, Gallian P, Niederhauser C, et al. Hepatitis E and blood donation safety in selected European countries: a shift to screening? Euro Surveill. 2017;22(16):30514.  https://doi.org/10.2807/1560-7917.ES.2017.22.16.30514  PMID: 28449730 
  7. Lachish T, Tandlich M, Schwartz E. Acute hepatitis in israeli travelers. J Travel Med. 2013;20(4):232-6.  https://doi.org/10.1111/jtm.12039  PMID: 23809073 
  8. Ram D, Manor Y, Gozlan Y, Schwartz E, Ben-Ari Z, Mendelson E, et al. Hepatitis E virus genotype 3 in sewage and genotype 1 in acute hepatitis cases, Israel. Am J Trop Med Hyg. 2016;95(1):216-20.  https://doi.org/10.4269/ajtmh.15-0925  PMID: 27246446 
  9. García-Hernández ME, Cruz-Rivera M, Sánchez-Betancourt JI, Rico-Chávez O, Vergara-Castañeda A, Trujillo ME, et al. Seroprevalence of anti-hepatitis E virus antibodies in domestic pigs in Mexico. BMC Vet Res. 2017;13(1):289.  https://doi.org/10.1186/s12917-017-1208-z  PMID: 28934965 
  10. Pozzi SP, Aborali G, Cordioli P, Rosner A, Waner T. Investigation on swine influenza sub-types H1N1, H3N2, N1N2 in pigs population in Israel. Isr J Vet Med. 2010;65(1):11-4.
  11. Shulman LM, Hindiyeh M, Muhsen K, Cohen D, Mendelson E, Sofer D. Evaluation of four different systems for extraction of RNA from stool suspensions using MS-2 coliphage as an exogenous control for RT-PCR inhibition. PLoS One. 2012;7(7):e39455.  https://doi.org/10.1371/journal.pone.0039455  PMID: 22815706 
  12. Smith DB, Simmonds P, Izopet J, Oliveira-Filho EF, Ulrich RG, Johne R, et al. Proposed reference sequences for hepatitis E virus subtypes. J Gen Virol. 2016;97(3):537-42.  https://doi.org/10.1099/jgv.0.000393  PMID: 26743685 
  13. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-9.  https://doi.org/10.1093/molbev/mst197  PMID: 24132122 
  14. Ponterio E, Di Bartolo I, Orrù G, Liciardi M, Ostanello F, Ruggeri FM. Detection of serum antibodies to hepatitis E virus in domestic pigs in Italy using a recombinant swine HEV capsid protein. BMC Vet Res. 2014;10(1):133.  https://doi.org/10.1186/1746-6148-10-133  PMID: 24934984 
  15. Di Bartolo I, Angeloni G, Ponterio E, Ostanello F, Ruggeri FM. Detection of hepatitis E virus in pork liver sausages. Int J Food Microbiol. 2015;193:29-33.  https://doi.org/10.1016/j.ijfoodmicro.2014.10.005  PMID: 25462920 
  16. Peralta B, Mateu E, Casas M, de Deus N, Martín M, Pina S. Genetic characterization of the complete coding regions of genotype 3 hepatitis E virus isolated from Spanish swine herds. Virus Res. 2009;139(1):111-6.  https://doi.org/10.1016/j.virusres.2008.09.008  PMID: 18977254 
  17. dos Santos DR, Vitral CL, de Paula VS, Marchevsky RS, Lopes JF, Gaspar AM, et al. Serological and molecular evidence of hepatitis E virus in swine in Brazil. Vet J. 2009;182(3):474-80.  https://doi.org/10.1016/j.tvjl.2008.08.001  PMID: 18805029 
  18. Passos-Castilho AM, Reinaldo MR, Sena A, Granato CFH. High prevalence of hepatitis E virus antibodies in Sao Paulo, Southeastern Brazil: analysis of a group of blood donors representative of the general population. Braz J Infect Dis. 2017;21(5):535-9.  https://doi.org/10.1016/j.bjid.2017.05.004  PMID: 28606414 
  19. Meng XJ. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol. 2010;140(3-4):256-65.  https://doi.org/10.1016/j.vetmic.2009.03.017  PMID: 19361937 
  20. Takahashi M, Tanaka T, Azuma M, Kusano E, Aikawa T, Shibayama T, et al. Prolonged fecal shedding of hepatitis E virus (HEV) during sporadic acute hepatitis E: evaluation of infectivity of HEV in fecal specimens in a cell culture system. J Clin Microbiol. 2007;45(11):3671-9.  https://doi.org/10.1128/JCM.01086-07  PMID: 17728471 
  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.  https://doi.org/10.1002/jmv.21647  PMID: 19950246 
  22. Casas M, Cortés R, Pina S, Peralta B, Allepuz A, Cortey M, et al. Longitudinal study of hepatitis E virus infection in Spanish farrow-to-finish swine herds. Vet Microbiol. 2011;148(1):27-34.  https://doi.org/10.1016/j.vetmic.2010.08.010  PMID: 20863630 
  23. Mansuy JM, Peron JM, Abravanel F, Poirson H, Dubois M, Miedouge M, et al. Hepatitis E in the south west of France in individuals who have never visited an endemic area. J Med Virol. 2004;74(3):419-24.  https://doi.org/10.1002/jmv.20206  PMID: 15368508 
  24. Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H. Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods. 2006;137(2):325-33.  https://doi.org/10.1016/j.jviromet.2006.07.004  PMID: 16901555 
  25. Legrand-Abravanel F, Mansuy JM, Dubois M, Kamar N, Peron JM, Rostaing L, et al. Hepatitis E virus genotype 3 diversity, France. Emerg Infect Dis. 2009;15(1):110-4.  https://doi.org/10.3201/eid1501.080296  PMID: 19116067 
  26. Owolodun OA, Gerber PF, Giménez-Lirola LG, Kwaga JK, Opriessnig T. First report of hepatitis E virus circulation in domestic pigs in Nigeria. Am J Trop Med Hyg. 2014;91(4):699-704.  https://doi.org/10.4269/ajtmh.14-0144  PMID: 25002299 
  27. Tanaka Y, Takahashi K, Orito E, Karino Y, Kang JH, Suzuki K, et al. Molecular tracing of Japan-indigenous hepatitis E viruses. J Gen Virol. 2006;87(Pt 4):949-54.  https://doi.org/10.1099/vir.0.81661-0  PMID: 16528044 
  28. Mor O, Bassal R, Michaeli M, Wax M, Ram D, Cohen-Ezra O, et al. Prevalence of hepatitis E virus antibodies, Israel, 2009-2010. Emerg Infect Dis. 2015;21(4):692-4.  https://doi.org/10.3201/eid2104.140245  PMID: 25811302 
  29. Drobeniuc J, Meng J, Reuter G, Greene-Montfort T, Khudyakova N, Dimitrova Z, et al. Serologic assays specific to immunoglobulin M antibodies against hepatitis E virus: pangenotypic evaluation of performances. Clin Infect Dis. 2010;51(3):e24-7.  https://doi.org/10.1086/654801  PMID: 20578874 
  30. Mughini-Gras L, Angeloni G, Salata C, Vonesch N, D’Amico W, Campagna G, et al. Hepatitis E virus infection in North Italy: high seroprevalence in swine herds and increased risk for swine workers. Epidemiol Infect. 2017;145(16):3375-84.  https://doi.org/10.1017/S0950268817002485  PMID: 29145911 
  31. Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ. Inactivation of infectious hepatitis E virus present in commercial pig livers sold in local grocery stores in the United States. Int J Food Microbiol. 2008;123(1-2):32-7.  https://doi.org/10.1016/j.ijfoodmicro.2007.11.068  PMID: 18166239 
  32. Vered R. Prescribing pork in Israel. Gastronomica (Berkeley Calif). 2010;10(3):19-22.  PMID: 21542211 
  33. Salogni C, Lazzaro M, Giacomini E, Giovannini S, Zanoni M, Giuliani M, et al. Infectious agents identified in aborted swine fetuses in a high-density breeding area: a three-year study. J Vet Diagn Invest. 2016;28(5):550-4.  https://doi.org/10.1177/1040638716656024  PMID: 27400956 
  34. Lachish T, Erez O, Daudi N, Shouval D, Schwartz E. Acute hepatitis E virus in pregnant women in Israel and in other industrialized countries. J Clin Virol. 2015;73:20-4.  https://doi.org/10.1016/j.jcv.2015.10.011  PMID: 26521225 
Hepatitis E in pigs in Israel: seroprevalence, molecular characterisation and potential impact on humans
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Rachel+Shirazi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Shirazi Rachel</a>, <a href="/search?value1=Paolo+Pozzi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pozzi Paolo</a>, <a href="/search?value1=Marina+Wax&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wax Marina</a>, <a href="/search?value1=Itay+Bar-Or&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bar-Or Itay</a>, <a href="/search?value1=Efrat+Asulin&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Asulin Efrat</a>, <a href="/search?value1=Yaniv+Lustig&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lustig Yaniv</a>, <a href="/search?value1=Ella+Mendelson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mendelson Ella</a>, <a href="/search?value1=Ziv+Ben-Ari&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ben-Ari Ziv</a>, <a href="/search?value1=Eli+Schwartz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schwartz Eli</a>, <a href="/search?value1=Orna+Mor&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mor Orna</a></span>. Hepatitis E in pigs in Israel: seroprevalence, molecular characterisation and potential impact on humans. <a href="/content/ecdc">Euro Surveill.</a> 2018;23(49):pii=1800067. <a href="https://doi.org/10.2807/1560-7917.ES.2018.23.49.1800067" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2018.23.49.1800067</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 09 Feb 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 05 Jun 2018 </span> </p>
/content/10.2807/1560-7917.ES.2018.23.49.1800067
/content/10.2807/1560-7917.ES.2018.23.49.1800067
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error