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Abstract

Background

Notified cases of hepatitis E have increased 40-fold in the past 10 years in Germany. Food safety is a major concern as hepatitis E virus (HEV) RNA has been detected in ready-to-eat retail-level food products. The objective of this case–control study was to assess risk factors for autochthonous symptomatic hepatitis E and explore reasons for delays in diagnosis. Demographic, clinical and exposure data from notified hepatitis E cases and individually matched population controls were collected in semi-standardised telephone interviews. Conditional logistic regression analysis was used to calculate matched odds ratios (mOR) and population attributable fractions (PAF). In total, 270 cases and 1,159 controls were included (mean age 53 years, 61% men in both groups). Associated with disease were: consumption of undercooked pork liver, pork, wild boar meat, frankfurters, liver sausage and raw vegetables; contact with waste water (occupational) and various host factors (mORs between 1.9 and 34.1, p value < 0.03). PAF for frankfurters and liver sausage were 17.6%, and 23.6%, respectively. There were statistically significant differences in the clinical presentation and hospitalisation proportion of acute hepatitis E in men and women. Diagnosis was preceded by more invasive procedures in 29.2% of patients, suggesting that hepatitis E was not immediately considered as a common differential diagnosis. Our study suggests that there are indeed sex-specific differences in disease development and lends important epidemiological evidence to specific ready-to-eat pork products as a major source for autochthonous hepatitis E. A review of existing consumer recommendations and production methods may be indicated.

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2018-05-10
2024-12-21
/content/10.2807/1560-7917.ES.2018.23.19.17-00469
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References

  1. 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 
  2. 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 
  3. Renou C, Roque-Afonso AM, Pavio N. Foodborne transmission of hepatitis E virus from raw pork liver sausage, France. Emerg Infect Dis. 2014;20(11):1945-7.  https://doi.org/10.3201/eid2011.140791  PMID: 25340356 
  4. Said B, Ijaz S, Chand MA, Kafatos G, Tedder R, Morgan D. Hepatitis E virus in England and Wales: indigenous infection is associated with the consumption of processed pork products. Epidemiol Infect. 2014;142(7):1467-75.  https://doi.org/10.1017/S0950268813002318  PMID: 24054519 
  5. Riveiro-Barciela M, Mínguez B, Gironés R, Rodriguez-Frías F, Quer J, Buti M. Phylogenetic demonstration of hepatitis E infection transmitted by pork meat ingestion. J Clin Gastroenterol. 2015;49(2):165-8.  https://doi.org/10.1097/MCG.0000000000000113  PMID: 24637729 
  6. 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 
  7. Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, et al. Hepatitis E Incident Investigation Team. Hepatitis E outbreak on cruise ship. Emerg Infect Dis. 2009;15(11):1738-44.  https://doi.org/10.3201/eid1511.091094  PMID: 19891860 
  8. Galiana C, Fernández-Barredo S, García A, Gómez MT, Pérez-Gracia MT. Occupational exposure to hepatitis E virus (HEV) in swine workers. Am J Trop Med Hyg. 2008;78(6):1012-5. PMID: 18541786 
  9. Krumbholz A, Mohn U, Lange J, Motz M, Wenzel JJ, Jilg W, et al. Prevalence of hepatitis E virus-specific antibodies in humans with occupational exposure to pigs. Med Microbiol Immunol (Berl). 2012;201(2):239-44.  https://doi.org/10.1007/s00430-011-0210-5  PMID: 21773797 
  10. Rutjes SA, Lodder WJ, Lodder-Verschoor F, van den Berg HH, Vennema H, Duizer E, et al. Sources of hepatitis E virus genotype 3 in The Netherlands. Emerg Infect Dis. 2009;15(3):381-7.  https://doi.org/10.3201/eid1503.071472  PMID: 19239749 
  11. Boxall E, Herborn A, Kochethu G, Pratt G, Adams D, Ijaz S, et al. Transfusion-transmitted hepatitis E in a ‘nonhyperendemic’ country. Transfus Med. 2006;16(2):79-83.  https://doi.org/10.1111/j.1365-3148.2006.00652.x  PMID: 16623913 
  12. Zhang S, Chen C, Peng J, Li X, Zhang D, Yan J, et al. Investigation of underlying comorbidities as risk factors for symptomatic human hepatitis E virus infection. Aliment Pharmacol Ther. 2017;45(5):701-13.  https://doi.org/10.1111/apt.13938  PMID: 28078736 
  13. Poggensee G, Benzler J, Eckmanns T, Krause Gund die Mitarbeiter der Abteilung für Infektionsepidemiologie. [On the 2007 edition of case definitions for the surveillance of notifiable infectious diseases in Germany]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2006;49(12):1189-94.  https://doi.org/10.1007/s00103-006-0088-3  PMID: 17149664 
  14. Robert Koch Institute. SurvStat@RKI 2.0. [Accessed Mar 2018]. Available from: https://survstat.rki.de/
  15. Faber MS, Wenzel JJ, Jilg W, Thamm M, Höhle M, Stark K. Hepatitis E virus seroprevalence among adults, Germany. Emerg Infect Dis. 2012;18(10):1654-7.  https://doi.org/10.3201/eid1810.111756  PMID: 23018055 
  16. Faber M, Willrich N, Schemmerer M, Rauh C, Kuhnert R, Stark K, et al. Hepatitis E virus seroprevalence, seroincidence and seroreversion in the German adult population. J Viral Hepat. 2018;00:1-7. Available from: https://doi.org/10.1111/jvh.12868 PMID: 29377436 
  17. Barnaud E, Rogée S, Garry P, Rose N, Pavio N. Thermal inactivation of infectious hepatitis E virus in experimentally contaminated food. Appl Environ Microbiol. 2012;78(15):5153-9.  https://doi.org/10.1128/AEM.00436-12  PMID: 22610436 
  18. Szabo K, Trojnar E, Anheyer-Behmenburg H, Binder A, Schotte U, Ellerbroek L, et al. Detection of hepatitis E virus RNA in raw sausages and liver sausages from retail in Germany using an optimized method. Int J Food Microbiol. 2015;215:149-56.  https://doi.org/10.1016/j.ijfoodmicro.2015.09.013  PMID: 26433460 
  19. Newson R. PUNAFCC: Stata module to compute population attributable fractions for case-control and survival studies. Stata J. 2012;13:st0314.
  20. Tsarev SA, Tsareva TS, Emerson SU, Yarbough PO, Legters LJ, Moskal T, et al. Infectivity titration of a prototype strain of hepatitis E virus in cynomolgus monkeys. J Med Virol. 1994;43(2):135-42.  https://doi.org/10.1002/jmv.1890430207  PMID: 8083660 
  21. Kuniholm MH, Purcell RH, McQuillan GM, Engle RE, Wasley A, Nelson KE. Epidemiology of hepatitis E virus in the United States: results from the Third National Health and Nutrition Examination Survey, 1988-1994. J Infect Dis. 2009;200(1):48-56.  https://doi.org/10.1086/599319  PMID: 19473098 
  22. Mykytczuk O, Harlow J, Bidawid S, Corneau N, Nasheri N. Prevalence and Molecular Characterization of the Hepatitis E Virus in Retail Pork Products Marketed in Canada. Food Environ Virol. 2017;9(2):208-18.  https://doi.org/10.1007/s12560-017-9281-9  PMID: 28197972 
  23. Wenzel JJ, Preiss J, Schemmerer M, Huber B, Plentz A, Jilg W. Detection of hepatitis E virus (HEV) from porcine livers in Southeastern Germany and high sequence homology to human HEV isolates. J Clin Virol. 2011;52(1):50-4.  https://doi.org/10.1016/j.jcv.2011.06.006  PMID: 21742549 
  24. Yapa CM, Furlong C, Rosewell A, Ward KA, Adamson S, Shadbolt C, et al. First reported outbreak of locally acquired hepatitis E virus infection in Australia. Med J Aust. 2016;204(7):274.  https://doi.org/10.5694/mja15.00955  PMID: 27078603 
  25. Riveiro-Barciela M, Buti M, Homs M, Campos-Varela I, Cantarell C, Crespo M, et al. Cirrhosis, liver transplantation and HIV infection are risk factors associated with hepatitis E virus infection. PLoS One. 2014;9(7):e103028.  https://doi.org/10.1371/journal.pone.0103028  PMID: 25068388 
  26. Dalton HR, Bendall RP, Rashid M, Ellis V, Ali R, Ramnarace R, et al. Host risk factors and autochthonous hepatitis E infection. Eur J Gastroenterol Hepatol. 2011;23(12):1200-5.  https://doi.org/10.1097/MEG.0b013e32834ca4da  PMID: 21941192 
  27. Singh KK, Panda SK, Shalimar, Acharya SK. Patients with Diabetes Mellitus are Prone to Develop Severe Hepatitis and Liver Failure due to Hepatitis Virus Infection. J Clin Exp Hepatol. 2013;3(4):275-80.  https://doi.org/10.1016/j.jceh.2013.11.003  PMID: 25755514 
  28. Faber MS, Stark K, Behnke SC, Schreier E, Frank C. Epidemiology of hepatitis A virus infections, Germany, 2007-2008. Emerg Infect Dis. 2009;15(11):1760-8.  https://doi.org/10.3201/eid1511.090214  PMID: 19891863 
  29. Lhomme S, Marion O, Abravanel F, Chapuy-Regaud S, Kamar N, Izopet J. Pathogenesis. Viruses. 2016;8(8):8.  https://doi.org/10.3390/v8080212  PMID: 27527210 
  30. Vollmer T, Diekmann J, Eberhardt M, Knabbe C, Dreier J. Monitoring of Anti-Hepatitis E Virus Antibody Seroconversion in Asymptomatically Infected Blood Donors: Systematic Comparison of Nine Commercial Anti-HEV IgM and IgG Assays. Viruses-Basel. 2016;8.
  31. Worm HC, van der Poel WH, Brandstätter G. Hepatitis E: an overview. Microbes Infect. 2002;4(6):657-66.  https://doi.org/10.1016/S1286-4579(02)01584-8  PMID: 12048035 
  32. Doting MHE, Weel J, Niesters HGM, Riezebos-Brilman A, Brandenburg A. The added value of hepatitis E diagnostics in determining causes of hepatitis in routine diagnostic settings in the Netherlands. Clin Microbiol Infect. 2017;23(9):667-71.  https://doi.org/10.1016/j.cmi.2017.02.026  PMID: 28285979 
  33. 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 
  34. Pischke S, Gisa A, Suneetha PV, Wiegand SB, Taubert R, Schlue J, et al. Increased HEV seroprevalence in patients with autoimmune hepatitis. PLoS One. 2014;9(1):e85330.  https://doi.org/10.1371/journal.pone.0085330  PMID: 24465537 
Case-control study on risk factors for acute hepatitis E in Germany, 2012 to 2014
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Mirko+Faber&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Faber Mirko</a>, <a href="/search?value1=Mona+Askar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Askar Mona</a>, <a href="/search?value1=Klaus+Stark&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Stark Klaus</a></span>. Case-control study on risk factors for acute hepatitis E in Germany, 2012 to 2014. <a href="/content/ecdc">Euro Surveill.</a> 2018;23(19):pii=17-00469. <a href="https://doi.org/10.2807/1560-7917.ES.2018.23.19.17-00469" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2018.23.19.17-00469</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 11 Jul 2017;&nbsp;&nbsp; <span class="generated">Accepted</span>: 02 Jan 2018 </span> </p>
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