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Abstract

Background

Hepatitis E virus (HEV) is an emerging zoonotic pathogen and an important cause of acute viral hepatitis in European countries. Corsica Island has been previously identified as a hyperendemic area for HEV.

Aim

Our aim was to characterise the prevalence and titres of IgG antibodies to HEV among blood donors on Corsica and establish a model of the annual force of infection.

Methods

Between September 2017 and January 2018, 2,705 blood donations were tested for anti-HEV IgG using the Wantai HEV IgG enzyme immunoassay.

Results

The overall seroprevalence was 56.1%. In multivariate analysis, seroprevalence was higher in men than in women (60.0% vs 52.2%; p < 0.01), increased with age and was significantly higher among donors born on Corsica (60.6% vs 53.2%; p < 0.01). No significant difference was observed between the five districts of the island. IgG anti-HEV titres were mostly low (70% of positive donors had titres < 3 IU/mL). In Corsican natives, increasing seroprevalence by age could be explained by models capturing a loss of immunity (annual probability of infection: 4.5%; duration of immunity: 55 years) or by age-specific probabilities of infection (3.8% for children, 1.3% for adults).

Conclusion

We confirmed the high HEV seroprevalence on Corsica and identified three aspects that should be further explored: (i) the epidemiology in those younger than 18 years, (ii) common sources of contamination, in particular drinking water, that may explain the wide exposure of the population, and (iii) the actual protection afforded by the low IgG titres observed and the potential susceptibility to secondary HEV infection.

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/content/10.2807/1560-7917.ES.2020.25.5.1900336
2020-02-06
2020-02-17
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2020.25.5.1900336
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References

  1. Kamar N, Bendall R, Legrand-Abravanel F, Xia NS, Ijaz S, Izopet J, et al. Hepatitis E. Lancet. 2012;379(9835):2477-88.  https://doi.org/10.1016/S0140-6736(11)61849-7  PMID: 22549046 
  2. Bradley DW. Enterically-transmitted non-A, non-B hepatitis. Br Med Bull. 1990;46(2):442-61.  https://doi.org/10.1093/oxfordjournals.bmb.a072409  PMID: 2116213 
  3. Emerson SU, Purcell RH. Hepatitis E virus. Rev Med Virol. 2003;13(3):145-54.  https://doi.org/10.1002/rmv.384  PMID: 12740830 
  4. Takahashi M, Tanaka T, Takahashi H, Hoshino Y, Nagashima S, Jirintai, et al. Hepatitis E Virus (HEV) strains in serum samples can replicate efficiently in cultured cells despite the coexistence of HEV antibodies: characterization of HEV virions in blood circulation. J Clin Microbiol. 2010;48(4):1112-25.  https://doi.org/10.1128/JCM.02002-09  PMID: 20107086 
  5. Chapuy-Regaud S, Dubois M, Plisson-Chastang C, Bonnefois T, Lhomme S, Bertrand-Michel J, et al. Characterization of the lipid envelope of exosome encapsulated HEV particles protected from the immune response. Biochimie. 2017;141:70-9.  https://doi.org/10.1016/j.biochi.2017.05.003  PMID: 28483690 
  6. Doceul V, Bagdassarian E, Demange A, Pavio N. Zoonotic hepatitis E virus: classification, animal reservoirs and transmission routes. Viruses. 2016;8(10):E270.  https://doi.org/10.3390/v8100270  PMID: 27706110 
  7. Pavio N, Meng XJ, Renou C. Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet Res. 2010;41(6):46.  https://doi.org/10.1051/vetres/2010018  PMID: 20359452 
  8. Dalton HR, Bendall R, Ijaz S, Banks M. Hepatitis E: an emerging infection in developed countries. Lancet Infect Dis. 2008;8(11):698-709.  https://doi.org/10.1016/S1473-3099(08)70255-X  PMID: 18992406 
  9. Aggarwal R. Clinical presentation of hepatitis E. Virus Res. 2011;161(1):15-22.  https://doi.org/10.1016/j.virusres.2011.03.017  PMID: 21458513 
  10. Guillois Y, Abravanel F, Miura T, Pavio N, Vaillant V, Lhomme S, et al. High proportion of asymptomatic infections in an outbreak of hepatitis E associated with a spit-roasted piglet, France, 2013. Clin Infect Dis. 2016;62(3):351-7.  https://doi.org/10.1093/cid/civ862  PMID: 26429341 
  11. Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, et al. Hepatitis E outbreak on cruise ship. Emerg Infect Dis. 2009;15(11):1738-44.  https://doi.org/10.3201/eid1511.091094  PMID: 19891860 
  12. Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS. Hepatitis E in pregnancy. Int J Gynaecol Obstet. 2004;85(3):240-4.  https://doi.org/10.1016/j.ijgo.2003.11.018  PMID: 15145258 
  13. Jilani N, Das BC, Husain SA, Baweja UK, Chattopadhya D, Gupta RK, et al. Hepatitis E virus infection and fulminant hepatic failure during pregnancy. J Gastroenterol Hepatol. 2007;22(5):676-82.  https://doi.org/10.1111/j.1440-1746.2007.04913.x  PMID: 17444855 
  14. de Niet A, Zaaijer HL, ten Berge I, Weegink CJ, Reesink HW, Beuers U. Chronic hepatitis E after solid organ transplantation. Neth J Med. 2012;70(6):261-6. PMID: 22859417 
  15. Gauss A, Wenzel JJ, Flechtenmacher C, Navid MH, Eisenbach C, Jilg W, et al. Chronic hepatitis E virus infection in a patient with leukemia and elevated transaminases: a case report. J Med Case Reports. 2012;6(1):334.  https://doi.org/10.1186/1752-1947-6-334  PMID: 23031738 
  16. Debing Y, Moradpour D, Neyts J, Gouttenoire J. Update on hepatitis E virology: Implications for clinical practice. J Hepatol. 2016;65(1):200-12.  https://doi.org/10.1016/j.jhep.2016.02.045  PMID: 26966047 
  17. Behrendt P, Steinmann E, Manns MP, Wedemeyer H. The impact of hepatitis E in the liver transplant setting. J Hepatol. 2014;61(6):1418-29.  https://doi.org/10.1016/j.jhep.2014.08.047  PMID: 25195557 
  18. Crossan CL, Simpson KJ, Craig DG, Bellamy C, Davidson J, Dalton HR, et al. Hepatitis E virus in patients with acute severe liver injury. World J Hepatol. 2014;6(6):426-34.  https://doi.org/10.4254/wjh.v6.i6.426  PMID: 25018853 
  19. Hoofnagle JH, Nelson KE, Purcell RH. Hepatitis E. N Engl J Med. 2012;367(13):1237-44.  https://doi.org/10.1056/NEJMra1204512  PMID: 23013075 
  20. Te HS, Drobeniuc J, Kamili S, Dong C, Hart J, Sharapov UM. Hepatitis E virus infection in a liver transplant recipient in the United States: a case report. Transplant Proc. 2013;45(2):810-3.  https://doi.org/10.1016/j.transproceed.2012.08.020  PMID: 23498824 
  21. Geng Y, Zhang H, Huang W, J Harrison T, Geng K, Li Z, et al. Persistent hepatitis e virus genotype 4 infection in a child with acute lymphoblastic leukemia. Hepat Mon. 2014;14(1):e15618. PMID: 24596581 
  22. Shrestha AC, Flower RL, Seed CR, Stramer SL, Faddy HM. A comparative study of assay performance of commercial hepatitis E virus enzyme-linked immunosorbent assay kits in australian blood donor samples. J Blood Transfus. 2016;2016:9647675.  https://doi.org/10.1155/2016/9647675  PMID: 27891290 
  23. Park HK, Jeong SH, Kim JW, Woo BH, Lee DH, Kim HY, et al. Seroprevalence of anti-hepatitis E virus (HEV) in a Korean population: comparison of two commercial anti-HEV assays. BMC Infect Dis. 2012;12(1):142.  https://doi.org/10.1186/1471-2334-12-142  PMID: 22726615 
  24. Hartl J, Otto B, Madden RG, Webb G, Woolson KL, Kriston L, et al. Hepatitis E seroprevalence in europe: a meta-analysis. Viruses. 2016;8(8):E211.  https://doi.org/10.3390/v8080211  PMID: 27509518 
  25. Yan Q, Du H, Wang Y. Comparison of two diagnostic reagents to detect anti-hepatitis E virus IgG antibodies. Chin J Zoonoses. 2008;24:1087-9.
  26. Abravanel F, Chapuy-Regaud S, Lhomme S, Miedougé M, Peron JM, Alric L, et al. Performance of anti-HEV assays for diagnosing acute hepatitis E in immunocompromised patients. J Clin Virol. 2013;58(4):624-8.  https://doi.org/10.1016/j.jcv.2013.10.003  PMID: 24183927 
  27. Wantai HEV-IgG ELISA. Beijing: Wantai Biological Pharmacy Enterprise Co, Ltd. Available from: http://www.ystwt.cn/IFU/HEV/HEV-IgG_CE.pdf
  28. Zhang J, Ge SX, Huang GY, Li SW, He ZQ, Wang YB, et al. Evaluation of antibody-based and nucleic acid-based assays for diagnosis of hepatitis E virus infection in a rhesus monkey model. J Med Virol. 2003;71(4):518-26.  https://doi.org/10.1002/jmv.10523  PMID: 14556264 
  29. Cleland A, Smith L, Crossan C, Blatchford O, Dalton HR, Scobie L, et al. Hepatitis E virus in Scottish blood donors. Vox Sang. 2013;105(4):283-9.  https://doi.org/10.1111/vox.12056  PMID: 23763589 
  30. Thom K, Gilhooly P, McGowan K, Malloy K, Jarvis LM, Crossan C, et al. Hepatitis E virus (HEV) in Scotland: evidence of recent increase in viral circulation in humans. Euro Surveill. 2018;23(12):17-00174.  https://doi.org/10.2807/1560-7917.ES.2018.23.12.17-00174  PMID: 29589577 
  31. Mansuy JM, Bendall R, Legrand-Abravanel F, Sauné K, Miédouge M, Ellis V, et al. Hepatitis E virus antibodies in blood donors, France. Emerg Infect Dis. 2011;17(12):2309-12.  https://doi.org/10.3201/eid1712.110371  PMID: 22172156 
  32. Mansuy JM, Gallian P, Dimeglio C, Saune K, Arnaud C, Pelletier B, et al. A nationwide survey of hepatitis E viral infection in French blood donors. Hepatology. 2016;63(4):1145-54.  https://doi.org/10.1002/hep.28436  PMID: 27008201 
  33. Marcontonio C, Pezzotti P, Bruni R, Taliani G, Chionne P, Madonna E, et al. Incidence of Hepatitis E virus infection among blood donors in a high endemic area of central Italy. J Viral Hepat. 2018;jvh.13049.  https://doi.org/10.1111/jvh.13049 
  34. Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaaijer HL. Silent hepatitis E virus infection in Dutch blood donors, 2011 to 2012. Euro Surveill. 2013;18(31):20550.  https://doi.org/10.2807/1560-7917.ES2013.18.31.20550  PMID: 23929229 
  35. Couturier E, Abravanel F, Figoni J, Van Cauteren D, Septfons A, Lhomme S, et al. Surveillance de l’hépatite E en France, 2002-2016. [Hepatitis E surveillance in France, 2002-2016]. Bulletin Epidémiologique Hebdomadaire. 2018;28:566-74. French. Available from: https://www.santepubliquefrance.fr/maladies-et-traumatismes/hepatites-virales/hepatite-e/documents/article/surveillance-de-l-hepatite-e-en-france-2002-2016
  36. Institut national de la statistique et des études Économiques (INSEE). Estimations de population par sexe et âge au 1er janvier 2019. [Estimate of the population by sex and age on 1 January 2019]. Montrouge: INSEE; 2019. French. Available from: https://www.insee.fr/fr/statistiques/2012692
  37. Li X, Kamili S, Krawczynski K. Quantitative detection of hepatitis E virus RNA and dynamics of viral replication in experimental infection. J Viral Hepat. 2006;13(12):835-9.  https://doi.org/10.1111/j.1365-2893.2006.00754.x  PMID: 17109683 
  38. Avellon A, Morago L, Garcia-Galera del Carmen M, Munoz M, Echevarría JM. Comparative sensitivity of commercial tests for hepatitis E genotype 3 virus antibody detection. J Med Virol. 2015;87(11):1934-9.  https://doi.org/10.1002/jmv.24251  PMID: 25959136 
  39. Abravanel F, Chapuy-Regaud S, Lhomme S, Miedougé M, Peron JM, Alric L, et al. Performance of anti-HEV assays for diagnosing acute hepatitis E in immunocompromised patients. J Clin Virol. 2013;58(4):624-8.  https://doi.org/10.1016/j.jcv.2013.10.003  PMID: 24183927 
  40. Abravanel F, Lhomme S, Chapuy-Regaud S, Mansuy JM, Muscari F, Sallusto F, et al. Hepatitis E virus reinfections in solid-organ-transplant recipients can evolve into chronic infections. J Infect Dis. 2014;209(12):1900-6.  https://doi.org/10.1093/infdis/jiu032  PMID: 24436450 
  41. Rookard LE, Edmondson O, Greenwell P. ABO reverse grouping: effect of varying concentrations of the enzyme bromelain. Br J Biomed Sci. 2009;66(2):93-7.  https://doi.org/10.1080/09674845.2009.11730251  PMID: 19637650 
  42. Hens N, Aerts M, Faes C, Shkedy Z, Lejeune O, Van Damme P, et al. Seventy-five years of estimating the force of infection from current status data. Epidemiol Infect. 2010;138(6):802-12.  https://doi.org/10.1017/S0950268809990781  PMID: 19765352 
  43. RStan: the R interface to Stan. R package version, 2(1). Vienna: Stan Development Team; 2019. Available from: https://cran.r-project.org/web/packages/rstan/vignettes/rstan.html
  44. Spiegelhalter DJ, Best NG, Carlin BR, van der Linde A. Bayesian measures of model complexity and fit. J R Stat Soc B. 2002;64(4):583-639.  https://doi.org/10.1111/1467-9868.00353 
  45. Colson P, Borentain P, Queyriaux B, Kaba M, Moal V, Gallian P, et al. Pig liver sausage as a source of hepatitis E virus transmission to humans. J Infect Dis. 2010;202(6):825-34.  https://doi.org/10.1086/655898  PMID: 20695796 
  46. Lucarelli C, Spada E, Taliani G, Chionne P, Madonna E, Marcantonio C, et al. High prevalence of anti-hepatitis E virus antibodies among blood donors in central Italy, February to March 2014. Euro Surveill. 2016;21(30):30299.  https://doi.org/10.2807/1560-7917.ES.2016.21.30.30299  PMID: 27494608 
  47. Heggelund JE, Varrot A, Imberty A, Krengel U. Histo-blood group antigens as mediators of infections. Curr Opin Struct Biol. 2017;44:190-200.  https://doi.org/10.1016/j.sbi.2017.04.001  PMID: 28544984 
  48. Politis C, Parara M, Kremastinou J, Hasapopoulou E, Iniotaki A, Siorenta A, et al. Associations of ABO, D, and Lewis blood groups and HLA Class I and Class II alleles with West Nile virus Lineage 2 disease outcome in Greece, 2010 to 2013. Transfusion. 2016;56(8):2115-21.  https://doi.org/10.1111/trf.13667  PMID: 27245377 
  49. Kaidarova Z, Bravo MD, Kamel HT, Custer BS, Busch MP, Lanteri MC. Blood group A and D negativity are associated with symptomatic West Nile virus infection. Transfusion. 2016;56(7):1699-706.  https://doi.org/10.1111/trf.13622  PMID: 27189860 
  50. Nordgren J, Svensson L. Genetic susceptibility to human norovirus infection: an update. Viruses. 2019;11(3):E226.  https://doi.org/10.3390/v11030226  PMID: 30845670 
  51. Servant-Delmas A, Abravanel F, Lefrère JJ, Lionnet F, Hamon C, Izopet J, et al. New insights into the natural history of hepatitis E virus infection through a longitudinal study of multitransfused immunocompetent patients in France. J Viral Hepat. 2016;23(7):569-75.  https://doi.org/10.1111/jvh.12531  PMID: 26990022 
  52. Marcantonio C, Pezzotti P, Bruni R, Taliani G, Chionne P, Madonna E, et al. Incidence of hepatitis E virus infection among blood donors in a high endemic area of Central Italy. J Viral Hepat. 2019;26(4):506-12. PMID: 30548124 
  53. Thiry D, Mauroy A, Pavio N, Purdy MA, Rose N, Thiry E, et al. Hepatitis E virus and related viruses in animals. Transbound Emerg Dis. 2017;64(1):37-52.  https://doi.org/10.1111/tbed.12351  PMID: 25919649 
  54. 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 
  55. Couturier E, Abravanel F, Figoni J, Van Cauteren D, Septfons A, Lhomme S, et al. Surveillance de l’hépatite E en France, 2002-2016. [Hepatitis E surveillance in France, 2002-2016]. Bull Epidémiol Hebd. 2018;(28):566-74. French. Available from: http://invs.santepubliquefrance.fr/beh/2018/28/2018_28_1.html
  56. Wang H, Kjellberg I, Sikora P, Rydberg H, Lindh M, Bergstedt O, et al. Hepatitis E virus genotype 3 strains and a plethora of other viruses detected in raw and still in tap water. Water Res. 2020;168:115141.  https://doi.org/10.1016/j.watres.2019.115141  PMID: 31590036 
  57. Bisseux M, Colombet J, Mirand A, Roque-Afonso AM, Abravanel F, Izopet J, et al. Monitoring human enteric viruses in wastewater and relevance to infections encountered in the clinical setting: a one-year experiment in central France, 2014 to 2015. Euro Surveill. 2018;23(7):17-00237.  https://doi.org/10.2807/1560-7917.ES.2018.23.7.17-00237  PMID: 29471623 
  58. Capai L, Maestrini O, Casabianca F, Villechenaud N, Masse S, Bosseur F, et al. Drastic decline of hepatitis E virus detection in domestic pigs after the age of 6 months, Corsica, France. Transbound Emerg Dis. 2019;66(6):2462-73.  https://doi.org/10.1111/tbed.13304  PMID: 31336031 
  59. Jori F, Laval M, Maestrini O, Casabianca F, Charrier F, Pavio N. Assessment of domestic pigs, wild boars and feral hybrid pigs as reservoirs of hepatitis E virus in Corsica, France. Viruses. 2016;8(8):E236.  https://doi.org/10.3390/v8080236  PMID: 27556478 
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