1887
  1. Home
  2. Eurosurveillance
  3. Volume 27, Issue 23, 09/Jun/2022
  4. Article
Surveillance Open Access
Like 0
Download

Abstract

Background

Hepatitis E virus genotype 3 (HEV-3) is widely distributed throughout Europe, with incidence of infections increasing in many countries. Belgium, Bulgaria, France, Germany, Italy, the Netherlands and the United Kingdom have reported the distribution of HEV-3 subtypes in cohorts of patients with hepatic disease.

Aim

To describe the distribution of the HEV-3 subtypes in Spain at national and autonomous community (AC) levels between 2009 and 2019. The study was also extended to Andorra.

Methods

Of 5,197 samples received by the National Reference Laboratory during the study, 409 were HEV-RNA-positive. Among these, 294 (71.9%) were further typed based on an ORF2 sequence fragment, or, for a subset of 74, based on the full-coding genome sequence.

Results

HEV-3 was detected in 291 samples. The dominant subtype in Spain was HEV-3f (88.3%; 257/291), which occurred in all ACs, with no change in detection level over time. Within this subtype, three subclusters were characterised: HEV-3f-B, HEV-3f-A1 and HEV-3f-A2. The second most common HEV subtype was the recently described HEV-3m (7%; 21/291), with two subclusters identified: HEV-3m-A, which has been known since 2010, and HEV-3m-B, since 2014. The third most encountered subtype was HEV-3c (4.1%; 12/291), with a frequency not increasing over time, unlike observations in some European countries.

Conclusion

The importance of the surveillance of HEV-3 subtype and subcluster circulation is yet to be assessed. This surveillance together with the comprehensive epidemiological characterisation of clinical cases, could support the identification of sources of transmission and the establishment of control measures nationally and internationally.

© 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.2022.27.23.2100542
2022-06-09
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.23.2100542
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/27/23/eurosurv-27-23-2.html?itemId=/content/10.2807/1560-7917.ES.2022.27.23.2100542&mimeType=html&fmt=ahah

References

  1. Adlhoch C, Avellon A, Baylis SA, Ciccaglione AR, Couturier E, de Sousa R, et al. Hepatitis E virus: Assessment of the epidemiological situation in humans in Europe, 2014/15. J Clin Virol. 2016;82:9-16.  https://doi.org/10.1016/j.jcv.2016.06.010  PMID: 27393938 
  2. Purdy MA, Harrison TJ, Jameel S, Meng XJ, Okamoto H, Van der Poel WHM, et al. , Ictv Report Consortium. ICTV Virus Taxonomy Profile: Hepeviridae. J Gen Virol. 2017;98(11):2645-6.  https://doi.org/10.1099/jgv.0.000940  PMID: 29022866 
  3. 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 
  4. Spahr C, Knauf-Witzens T, Vahlenkamp T, Ulrich RG, Johne R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health. 2018;65(1):11-29.  https://doi.org/10.1111/zph.12405  PMID: 28944602 
  5. Ijaz S, Said B, Boxall E, Smit E, Morgan D, Tedder RS. Indigenous hepatitis E in England and wales from 2003 to 2012: evidence of an emerging novel phylotype of viruses. J Infect Dis. 2014;209(8):1212-8.  https://doi.org/10.1093/infdis/jit652  PMID: 24273173 
  6. Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C, Qiao Z, et al. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol. 2009;81(8):1371-9.  https://doi.org/10.1002/jmv.21536  PMID: 19551838 
  7. Miura M, Inoue J, Tsuruoka M, Nishizawa T, Nagashima S, Takahashi M, et al. Full-length genomic sequence analysis of new subtype 3k hepatitis E virus isolates with 99.97% nucleotide identity obtained from two consecutive acute hepatitis patients in a city in northeast Japan. J Med Virol. 2017;89(6):1116-20.  https://doi.org/10.1002/jmv.24743  PMID: 27922191 
  8. De Sabato L, Lemey P, Vrancken B, Bonfanti L, Ceglie L, Vaccari G, et al. Proposal for a new subtype of the zoonotic genotype 3 Hepatitis E virus: HEV-3l. Virus Res. 2018;248:1-4.  https://doi.org/10.1016/j.virusres.2018.02.010  PMID: 29452164 
  9. Smith DB, Izopet J, Nicot F, Simmonds P, Jameel S, Meng XJ, et al. Update: proposed reference sequences for subtypes of hepatitis E virus (species Orthohepevirus A). J Gen Virol. 2020;101(7):692-8.  https://doi.org/10.1099/jgv.0.001435  PMID: 32469300 
  10. Muñoz-Chimeno M, Forero JE, Echevarría JM, Muñoz-Bellido JL, Vázquez-López L, Morago L, et al. Full coding hepatitis E virus genotype 3 genome amplification method. J Virol Methods. 2016;230:18-23.  https://doi.org/10.1016/j.jviromet.2016.01.004  PMID: 26784284 
  11. Nicot F, Jeanne N, Roulet A, Lefebvre C, Carcenac R, Manno M, et al. Diversity of hepatitis E virus genotype 3. Rev Med Virol. 2018;28(5):e1987.  https://doi.org/10.1002/rmv.1987  PMID: 29939461 
  12. Nicot F, Dimeglio C, Migueres M, Jeanne N, Latour J, Abravanel F, et al. Classification of the Zoonotic Hepatitis E Virus Genotype 3 Into Distinct Subgenotypes. Front Microbiol. 2021;11:634430.  https://doi.org/10.3389/fmicb.2020.634430  PMID: 33584599 
  13. Subissi L, Peeters M, Lamoral S, Klamer S, Suin V, Van Gucht S. Subtype-specific differences in the risk of hospitalisation among patients infected with hepatitis E virus genotype 3 in Belgium, 2010-2018. Epidemiol Infect. 2019;147:e224.  https://doi.org/10.1017/S0950268819001122  PMID: 31364564 
  14. Suin V, Klamer SE, Hutse V, Wautier M, Jacques M, Abady M, et al. Epidemiology and genotype 3 subtype dynamics of hepatitis E virus in Belgium, 2010 to 2017. Euro Surveill. 2019;24(10):1800141.  https://doi.org/10.2807/1560-7917.ES.2019.24.10.1800141  PMID: 30862337 
  15. Bruni R, Villano U, Equestre M, Chionne P, Madonna E, Trandeva-Bankova D, et al. Hepatitis E virus genotypes and subgenotypes causing acute hepatitis, Bulgaria, 2013-2015. PLoS One. 2018;13(6):e0198045.  https://doi.org/10.1371/journal.pone.0198045  PMID: 29879148 
  16. Lhomme S, Abravanel F, Dubois M, Chapuy-Regaud S, Sandres-Saune K, Mansuy JM, et al. Temporal evolution of the distribution of hepatitis E virus genotypes in Southwestern France. Infect Genet Evol. 2015;35:50-5.  https://doi.org/10.1016/j.meegid.2015.07.028  PMID: 26218544 
  17. Wang B, Harms D, Papp CP, Niendorf S, Jacobsen S, Lütgehetmann M, et al. Comprehensive Molecular Approach for Characterization of Hepatitis E Virus Genotype 3 Variants. J Clin Microbiol. 2018;56(5):e01686-17.  https://doi.org/10.1128/JCM.01686-17  PMID: 29514938 
  18. Wichmann O, Schimanski S, Koch J, Kohler M, Rothe C, Plentz A, et al. Phylogenetic and case-control study on hepatitis E virus infection in Germany. J Infect Dis. 2008;198(12):1732-41.  https://doi.org/10.1086/593211  PMID: 18983248 
  19. De Sabato L, Di Bartolo I, Lapa D, Capobianchi MR, Garbuglia AR. Molecular Characterization of HEV Genotype 3 in Italy at Human/Animal Interface. Front Microbiol. 2020;11:137.  https://doi.org/10.3389/fmicb.2020.00137  PMID: 32117156 
  20. Garbuglia AR, Bruni R, Villano U, Vairo F, Lapa D, Madonna E, et al. , The Other Members Of The Hev Outbreak Working Group. Hepatitis E Outbreak in the Central Part of Italy Sustained by Multiple HEV Genotype 3 Strains, June-December 2019. Viruses. 2021;13(6):1159.  https://doi.org/10.3390/v13061159  PMID: 34204376 
  21. Koot H, Hogema BM, Koot M, Molier M, Zaaijer HL. Frequent hepatitis E in the Netherlands without traveling or immunosuppression. J Clin Virol. 2015;62:38-40.  https://doi.org/10.1016/j.jcv.2014.11.020  PMID: 25542468 
  22. Oeser C, Vaughan A, Said B, Ijaz S, Tedder R, Haywood B, et al. Epidemiology of Hepatitis E in England and Wales: A 10-Year Retrospective Surveillance Study, 2008-2017. J Infect Dis. 2019;220(5):802-10.  https://doi.org/10.1093/infdis/jiz207  PMID: 31107958 
  23. Fogeda M, Avellón A, Cilla CG, Echevarría JM. Imported and autochthonous hepatitis E virus strains in Spain. J Med Virol. 2009;81(10):1743-9.  https://doi.org/10.1002/jmv.21564  PMID: 19697406 
  24. Rivero-Juarez A, Aguado R, Lopez-Lopez P, Sanchez-Frias M, Frias M, Briceño J, et al. Prevalence of hepatitis E virus infection in liver donors in Spain. Clin Microbiol Infect. 2018;24(11):1218-9.  https://doi.org/10.1016/j.cmi.2018.06.030  PMID: 30017970 
  25. García N, Hernández M, Gutierrez-Boada M, Valero A, Navarro A, Muñoz-Chimeno M, et al. Occurrence of Hepatitis E Virus in Pigs and Pork Cuts and Organs at the Time of Slaughter, Spain, 2017. Front Microbiol. 2020;10:2990.  https://doi.org/10.3389/fmicb.2019.02990  PMID: 32047480 
  26. Caballero-Gómez J, Jiménez-Ruiz S, Lopez-Lopez P, Vicente J, Risalde MA, Cano-Terriza D, et al. Emergent subtype of hepatitis E virus genotype 3 in wild boar in Spain. Transbound Emerg Dis. 2019;66(5):1803-8.  https://doi.org/10.1111/tbed.13251  PMID: 31127865 
  27. Lhomme S, Abravanel F, Dubois M, Sandres-Saune K, Mansuy JM, Rostaing L, et al. Characterization of the polyproline region of the hepatitis E virus in immunocompromised patients. J Virol. 2014;88(20):12017-25.  https://doi.org/10.1128/JVI.01625-14  PMID: 25100839 
  28. Mulder AC, Kroneman A, Franz E, Vennema H, Tulen AD, Takkinen J, et al. , Members Of HEVnet. HEVnet: a One Health, collaborative, interdisciplinary network and sequence data repository for enhanced hepatitis E virus molecular typing, characterisation and epidemiological investigations. Euro Surveill. 2019;24(10):1800407.  https://doi.org/10.2807/1560-7917.ES.2019.24.10.1800407  PMID: 30862334 
  29. Lhomme S, Gallian P, Dimeglio C, Assal A, Abravanel F, Tiberghien P, et al. Viral load and clinical manifestations of hepatitis E virus genotype 3 infections. J Viral Hepat. 2019;26(9):1139-42.  https://doi.org/10.1111/jvh.13128  PMID: 31099059 
  30. Wang H, Castillo-Contreras R, Saguti F, López-Olvera JR, Karlsson M, Mentaberre G, et al. Genetically similar hepatitis E virus strains infect both humans and wild boars in the Barcelona area, Spain, and Sweden. Transbound Emerg Dis. 2019;66(2):978-85.  https://doi.org/10.1111/tbed.13115  PMID: 30597741 
  31. Said B, Usdin M, Warburton F, Ijaz S, Tedder RS, Morgan D. Pork products associated with human infection caused by an emerging phylotype of hepatitis E virus in England and Wales. Epidemiol Infect. 2017;145(12):2417-23.  https://doi.org/10.1017/S0950268817001388  PMID: 28756783 
Hepatitis E virus genotype 3 microbiological surveillance by the Spanish Reference Laboratory: geographic distribution and phylogenetic analysis of subtypes from 2009 to 2019
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Milagros+Mu%C3%B1oz-Chimeno&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Muñoz-Chimeno Milagros</a>, <a href="/search?value1=Silvia+Bart%C3%BAren&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bartúren Silvia</a>, <a href="/search?value1=Maira+Alejandra+Garc%C3%ADa-Lugo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">García-Lugo Maira Alejandra</a>, <a href="/search?value1=Lucia+Morago&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Morago Lucia</a>, <a href="/search?value1=%C3%81lvaro+Rodr%C3%ADguez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rodríguez Álvaro</a>, <a href="/search?value1=Juan+Carlos+Gal%C3%A1n&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Galán Juan Carlos</a>, <a href="/search?value1=Alfredo+P%C3%A9rez-Rivilla&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pérez-Rivilla Alfredo</a>, <a href="/search?value1=Mercedes+Rodr%C3%ADguez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rodríguez Mercedes</a>, <a href="/search?value1=Rosario+Mill%C3%A1n&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Millán Rosario</a>, <a href="/search?value1=Manuel+del+%C3%81lamo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">del Álamo Manuel</a>, <a href="/search?value1=Roberto+Alonso&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Alonso Roberto</a>, <a href="/search?value1=Laura+Molina&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Molina Laura</a>, <a href="/search?value1=Aitziber+Aguinaga&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Aguinaga Aitziber</a>, <a href="/search?value1=Ana+Avell%C3%B3n&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Avellón Ana</a></span>. Hepatitis E virus genotype 3 microbiological surveillance by the Spanish Reference Laboratory: geographic distribution and phylogenetic analysis of subtypes from 2009 to 2019. <a href="/content/ecdc">Euro Surveill.</a> 2022;27(23):pii=2100542. <a href="https://doi.org/10.2807/1560-7917.ES.2022.27.23.2100542" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2022.27.23.2100542</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 31 May 2021;&nbsp;&nbsp; <span class="generated">Accepted</span>: 21 Jan 2022 </span> </p>
/content/10.2807/1560-7917.ES.2022.27.23.2100542
/content/10.2807/1560-7917.ES.2022.27.23.2100542
Loading

Data & Media loading...

Supplementary data

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