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Published in: Medical Microbiology and Immunology 4/2014

01-08-2014 | Original Investigation

Seroprevalence of hepatitis E virus (HEV) in humans living in high pig density areas of Germany

Authors: Andi Krumbholz, Sebastian Joel, Paul Dremsek, Anne Neubert, Reimar Johne, Ralf Dürrwald, Mario Walther, Thomas H. Müller, Detlef Kühnel, Jeannette Lange, Peter Wutzler, Andreas Sauerbrei, Rainer G. Ulrich, Roland Zell

Published in: Medical Microbiology and Immunology | Issue 4/2014

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Abstract

An increase in acute autochthonous hepatitis E virus (HEV) infections has been recorded in Germany. These are suspected to be zoonotically transmitted from wild boar, deer and domestic pig. The latter may represent a major reservoir for HEV. In this study, 537 sera from humans living in Westphalia and Lower Saxony, representing areas of high pig density in Germany, were tested for the presence of HEV-specific antibodies. Among them were 302 individuals with occupational, direct contact to pigs and 235 individuals without direct contact to pigs. Two commercial tests and one in-house assay were applied for the detection of HEV-specific immunoglobulin G (IgG) antibodies. Sera were also tested in an assay that detects all classes of HEV-specific antibodies. Depending on the test used, the seroprevalence ranged from 4.1 to 27.9 %. Exposition to pigs was found to be associated with a significantly higher seroprevalence in subjects with contact to pigs (13.2–32.8 %) compared with that in non-exposed humans (7.7–21.7 %). In particular, individuals younger than 40 years with occupational exposure exhibited a markedly higher HEV seroprevalence compared with non-exposed individuals of that age group. In general, HEV seroprevalence increased with age resulting in a similar prevalence level in the age group of ≥50 years for exposed and non-exposed individuals. Analysis of all sera by a commercial anti-HEV IgM ELISA revealed 35 positive and 25 borderline samples. However, only one positive serum could be confirmed by an IgM line assay. Selected samples from IgM and/or IgG as well as total HEV antibody-positive individuals were also tested for the presence of HEV RNA. In one of the 78 samples, the only IgM ELISA positive and IgM line assay confirmed sample, RNA of HEV genotype 3 was detected. This sequence has high similarity to HEV sequences obtained from wild boars and domestic pigs from Germany and The Netherlands. This study demonstrates that in addition to the consumption of raw or undercooked meat, direct contact to pigs has to be considered as an additional risk factor for HEV infection.
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Literature
1.
go back to reference Batts W, Yun S, Hedrick R, Winton J (2011) A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res 158:116–123PubMedCrossRef Batts W, Yun S, Hedrick R, Winton J (2011) A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res 158:116–123PubMedCrossRef
2.
go back to reference Payne CJ, Ellis TM, Plant SL, Gregory AR, Wilcox GE (1999) Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet Microbiol 68:119–125PubMedCrossRef Payne CJ, Ellis TM, Plant SL, Gregory AR, Wilcox GE (1999) Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet Microbiol 68:119–125PubMedCrossRef
3.
go back to reference Drexler JF, Seelen A, Corman VM, Tateno AF, Cottontail V, Melim Zerbinati R, Gloza-Rausch F, Klose SM, Adu-Sarkodie Y, Oppong SK, Kalko EK, Osterman A, Rasche A, Adam A, Muller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C (2012) Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 86:9134–9147PubMedCentralPubMedCrossRef Drexler JF, Seelen A, Corman VM, Tateno AF, Cottontail V, Melim Zerbinati R, Gloza-Rausch F, Klose SM, Adu-Sarkodie Y, Oppong SK, Kalko EK, Osterman A, Rasche A, Adam A, Muller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C (2012) Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 86:9134–9147PubMedCentralPubMedCrossRef
4.
go back to reference Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H, Osterhaus AD, Haagmans BL (2012) Novel hepatitis E virus in ferrets, The Netherlands. Emerg Infect Dis 18:1369–1370PubMedCentralPubMedCrossRef Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H, Osterhaus AD, Haagmans BL (2012) Novel hepatitis E virus in ferrets, The Netherlands. Emerg Infect Dis 18:1369–1370PubMedCentralPubMedCrossRef
5.
go back to reference Johne R, Plenge-Bonig A, Hess M, Ulrich RG, Reetz J, Schielke A (2010) Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 91:750–758PubMedCrossRef Johne R, Plenge-Bonig A, Hess M, Ulrich RG, Reetz J, Schielke A (2010) Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 91:750–758PubMedCrossRef
6.
go back to reference Johne R, Heckel G, Plenge-Bonig A, Kindler E, Maresch C, Reetz J, Schielke A, Ulrich RG (2010) Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 16:1452–1455PubMedCentralPubMedCrossRef Johne R, Heckel G, Plenge-Bonig A, Kindler E, Maresch C, Reetz J, Schielke A, Ulrich RG (2010) Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 16:1452–1455PubMedCentralPubMedCrossRef
7.
go back to reference Meng XJ, Anderson DA, Arankalle VA, Emerson SU, Harrison TJ, Jameel S, Okamoto H (2012) Hepeviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Elsevier, Amsterdam, pp 1021–1028 Meng XJ, Anderson DA, Arankalle VA, Emerson SU, Harrison TJ, Jameel S, Okamoto H (2012) Hepeviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Elsevier, Amsterdam, pp 1021–1028
8.
go back to reference Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C, Qiao Z, Fan J, Ma H, Li M, Song A, Wang Y (2009) A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol 81:1371–1379PubMedCrossRef Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C, Qiao Z, Fan J, Ma H, Li M, Song A, Wang Y (2009) A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol 81:1371–1379PubMedCrossRef
11.
go back to reference Aggarwal R (2011) Hepatitis E: historical, contemporary and future perspectives. J Gastroenterol Hepatol 26(Suppl 1):72–82PubMedCrossRef Aggarwal R (2011) Hepatitis E: historical, contemporary and future perspectives. J Gastroenterol Hepatol 26(Suppl 1):72–82PubMedCrossRef
12.
go back to reference Meng XJ (2011) From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res 161:23–30PubMedCentralPubMedCrossRef Meng XJ (2011) From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res 161:23–30PubMedCentralPubMedCrossRef
14.
go back to reference Wedemeyer H, Pischke S, Manns MP (2012) Pathogenesis and treatment of hepatitis E virus infection. Gastroenterology 142:1388–1397 e1381PubMedCrossRef Wedemeyer H, Pischke S, Manns MP (2012) Pathogenesis and treatment of hepatitis E virus infection. Gastroenterology 142:1388–1397 e1381PubMedCrossRef
15.
go back to reference Kamar N, Rostaing L, Izopet J (2013) Hepatitis E virus infection in immunosuppressed patients: natural history and therapy. Semin Liver Dis 33:62–70PubMedCrossRef Kamar N, Rostaing L, Izopet J (2013) Hepatitis E virus infection in immunosuppressed patients: natural history and therapy. Semin Liver Dis 33:62–70PubMedCrossRef
16.
go back to reference Arankalle VA, Lole KS, Deshmukh TM, Chobe LP, Gandhe SS (2007) Evaluation of human (genotype 1) and swine (genotype 4)-ORF2-based ELISAs for anti-HEV IgM and IgG detection in an endemic country and search for type 4 human HEV infections. J Viral Hepat 14:435–445PubMedCrossRef Arankalle VA, Lole KS, Deshmukh TM, Chobe LP, Gandhe SS (2007) Evaluation of human (genotype 1) and swine (genotype 4)-ORF2-based ELISAs for anti-HEV IgM and IgG detection in an endemic country and search for type 4 human HEV infections. J Viral Hepat 14:435–445PubMedCrossRef
17.
go back to reference Dremsek P, Wenzel JJ, Johne R, Ziller M, Hofmann J, Groschup MH, Werdermann S, Mohn U, Dorn S, Motz M, Mertens M, Jilg W, Ulrich RG (2012) Seroprevalence study in forestry workers from eastern Germany using novel genotype 3- and rat hepatitis E virus-specific immunoglobulin G ELISAs. Med Microbiol Immunol 201:189–200PubMedCrossRef Dremsek P, Wenzel JJ, Johne R, Ziller M, Hofmann J, Groschup MH, Werdermann S, Mohn U, Dorn S, Motz M, Mertens M, Jilg W, Ulrich RG (2012) Seroprevalence study in forestry workers from eastern Germany using novel genotype 3- and rat hepatitis E virus-specific immunoglobulin G ELISAs. Med Microbiol Immunol 201:189–200PubMedCrossRef
18.
go back to reference Meng XJ, Wiseman B, Elvinger F, Guenette DK, Toth TE, Engle RE, Emerson SU, Purcell RH (2002) Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J Clin Microbiol 40:117–122PubMedCentralPubMedCrossRef Meng XJ, Wiseman B, Elvinger F, Guenette DK, Toth TE, Engle RE, Emerson SU, Purcell RH (2002) Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J Clin Microbiol 40:117–122PubMedCentralPubMedCrossRef
19.
go back to reference Obriadina A, Meng JH, Ulanova T, Trinta K, Burkov A, Fields HA, Khudyakov YE (2002) A new enzyme immunoassay for the detection of antibody to hepatitis E virus. J Gastroenterol Hepatol 17(Suppl 3):S360–S364PubMedCrossRef Obriadina A, Meng JH, Ulanova T, Trinta K, Burkov A, Fields HA, Khudyakov YE (2002) A new enzyme immunoassay for the detection of antibody to hepatitis E virus. J Gastroenterol Hepatol 17(Suppl 3):S360–S364PubMedCrossRef
20.
go back to reference Peralta B, Casas M, de Deus N, Martin M, Ortuno A, Perez-Martin E, Pina S, Mateu E (2009) Anti-HEV antibodies in domestic animal species and rodents from Spain using a genotype 3-based ELISA. Vet Microbiol 137:66–73PubMedCrossRef Peralta B, Casas M, de Deus N, Martin M, Ortuno A, Perez-Martin E, Pina S, Mateu E (2009) Anti-HEV antibodies in domestic animal species and rodents from Spain using a genotype 3-based ELISA. Vet Microbiol 137:66–73PubMedCrossRef
21.
go back to reference Khudyakov Y, Kamili S (2011) Serological diagnostics of hepatitis E virus infection. Virus Res 161:84–92PubMedCrossRef Khudyakov Y, Kamili S (2011) Serological diagnostics of hepatitis E virus infection. Virus Res 161:84–92PubMedCrossRef
22.
go back to reference Aggarwal R (2013) Hepatitis E: clinical presentation in disease-endemic areas and diagnosis. Semin Liver Dis 33:30–40PubMedCrossRef Aggarwal R (2013) Hepatitis E: clinical presentation in disease-endemic areas and diagnosis. Semin Liver Dis 33:30–40PubMedCrossRef
23.
go back to reference Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bonig A, Gregersen H, Wessels U, Schmidt K, Rietschel W, Groschup MH, Guenther S, Heckel G, Ulrich RG (2012) Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect Genet Evol 12:947–956PubMedCrossRef Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bonig A, Gregersen H, Wessels U, Schmidt K, Rietschel W, Groschup MH, Guenther S, Heckel G, Ulrich RG (2012) Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect Genet Evol 12:947–956PubMedCrossRef
24.
go back to reference Wilhelm BJ, Rajic A, Greig J, Waddell L, Trottier G, Houde A, Harris J, Borden LN, Price C (2011) A systematic review/meta-analysis of primary research investigating swine, pork or pork products as a source of zoonotic hepatitis E virus. Epidemiol Infect 139:1127–1144PubMedCrossRef Wilhelm BJ, Rajic A, Greig J, Waddell L, Trottier G, Houde A, Harris J, Borden LN, Price C (2011) A systematic review/meta-analysis of primary research investigating swine, pork or pork products as a source of zoonotic hepatitis E virus. Epidemiol Infect 139:1127–1144PubMedCrossRef
25.
go back to reference Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J (2012) Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 50:2708–2713PubMedCentralPubMedCrossRef Vollmer T, Diekmann J, Johne R, Eberhardt M, Knabbe C, Dreier J (2012) Novel approach for detection of hepatitis E virus infection in German blood donors. J Clin Microbiol 50:2708–2713PubMedCentralPubMedCrossRef
26.
go back to reference Carpentier A, Chaussade H, Rigaud E, Rodriguez J, Berthault C, Boue F, Tognon M, Touze A, Garcia-Bonnet N, Choutet P, Coursaget P (2012) High hepatitis E virus seroprevalence in forestry workers and in wild boars in France. J Clin Microbiol 50:2888–2893PubMedCentralPubMedCrossRef Carpentier A, Chaussade H, Rigaud E, Rodriguez J, Berthault C, Boue F, Tognon M, Touze A, Garcia-Bonnet N, Choutet P, Coursaget P (2012) High hepatitis E virus seroprevalence in forestry workers and in wild boars in France. J Clin Microbiol 50:2888–2893PubMedCentralPubMedCrossRef
27.
go back to reference Krumbholz A, Mohn U, Lange J, Motz M, Wenzel JJ, Jilg W, Walther M, Straube E, Wutzler P, Zell R (2012) Prevalence of hepatitis E virus-specific antibodies in humans with occupational exposure to pigs. Med Microbiol Immunol 201:239–244PubMedCrossRef Krumbholz A, Mohn U, Lange J, Motz M, Wenzel JJ, Jilg W, Walther M, Straube E, Wutzler P, Zell R (2012) Prevalence of hepatitis E virus-specific antibodies in humans with occupational exposure to pigs. Med Microbiol Immunol 201:239–244PubMedCrossRef
28.
29.
go back to reference Bouwknegt M, Engel B, Herremans MM, Widdowson MA, Worm HC, Koopmans MP, Frankena K, de Roda Husman AM, De Jong MC, Van Der Poel WH (2008) Bayesian estimation of hepatitis E virus seroprevalence for populations with different exposure levels to swine in The Netherlands. Epidemiol Infect 136:567–576PubMedCentralPubMed Bouwknegt M, Engel B, Herremans MM, Widdowson MA, Worm HC, Koopmans MP, Frankena K, de Roda Husman AM, De Jong MC, Van Der Poel WH (2008) Bayesian estimation of hepatitis E virus seroprevalence for populations with different exposure levels to swine in The Netherlands. Epidemiol Infect 136:567–576PubMedCentralPubMed
30.
go back to reference Galiana C, Fernandez-Barredo S, Garcia A, Gomez MT, Perez-Gracia MT (2008) Occupational exposure to hepatitis E virus (HEV) in swine workers. Am J Trop Med Hyg 78:1012–1015PubMed Galiana C, Fernandez-Barredo S, Garcia A, Gomez MT, Perez-Gracia MT (2008) Occupational exposure to hepatitis E virus (HEV) in swine workers. Am J Trop Med Hyg 78:1012–1015PubMed
31.
go back to reference Drobeniuc J, Favorov MO, Shapiro CN, Bell BP, Mast EE, Dadu A, Culver D, Iarovoi P, Robertson BH, Margolis HS (2001) Hepatitis E virus antibody prevalence among persons who work with swine. J Infect Dis 184:1594–1597PubMedCrossRef Drobeniuc J, Favorov MO, Shapiro CN, Bell BP, Mast EE, Dadu A, Culver D, Iarovoi P, Robertson BH, Margolis HS (2001) Hepatitis E virus antibody prevalence among persons who work with swine. J Infect Dis 184:1594–1597PubMedCrossRef
32.
go back to reference Geng J, Wang L, Wang X, Fu H, Bu Q, Liu P, Zhu Y, Wang M, Sui Y, Zhuang H (2011) Potential risk of zoonotic transmission from young swine to human: seroepidemiological and genetic characterization of hepatitis E virus in human and various animals in Beijing, China. J Viral Hepat 18:e583–e590PubMedCrossRef Geng J, Wang L, Wang X, Fu H, Bu Q, Liu P, Zhu Y, Wang M, Sui Y, Zhuang H (2011) Potential risk of zoonotic transmission from young swine to human: seroepidemiological and genetic characterization of hepatitis E virus in human and various animals in Beijing, China. J Viral Hepat 18:e583–e590PubMedCrossRef
33.
go back to reference Pourpongporn P, Samransurp K, Rojanasang P, Wiwattanakul S, Srisurapanon S (2009) The prevalence of anti-hepatitis E in occupational risk groups. J Med Assoc Thai 92(Suppl 3):S38–S42PubMed Pourpongporn P, Samransurp K, Rojanasang P, Wiwattanakul S, Srisurapanon S (2009) The prevalence of anti-hepatitis E in occupational risk groups. J Med Assoc Thai 92(Suppl 3):S38–S42PubMed
35.
go back to reference Chaussade H, Rigaud E, Allix A, Carpentier A, Touze A, Delzescaux D, Choutet P, Garcia-Bonnet N, Coursaget P (2013) Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals. J Clin Virol 58:504–508PubMedCrossRef Chaussade H, Rigaud E, Allix A, Carpentier A, Touze A, Delzescaux D, Choutet P, Garcia-Bonnet N, Coursaget P (2013) Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals. J Clin Virol 58:504–508PubMedCrossRef
36.
go back to reference Anonymous (2014) Übermittelte Hepatitis E-Fälle nach Meldekategorie, Deutschland, Fälle entsprechend der Referenzdefinition des RKI. Robert Koch-Institut, Datenstand, 19 March 2014 Anonymous (2014) Übermittelte Hepatitis E-Fälle nach Meldekategorie, Deutschland, Fälle entsprechend der Referenzdefinition des RKI. Robert Koch-Institut, Datenstand, 19 March 2014
37.
38.
go back to reference Kaci S, Nockler K, Johne R (2008) Detection of hepatitis E virus in archived German wild boar serum samples. Vet Microbiol 128:380–385PubMedCrossRef Kaci S, Nockler K, Johne R (2008) Detection of hepatitis E virus in archived German wild boar serum samples. Vet Microbiol 128:380–385PubMedCrossRef
39.
go back to reference Adlhoch C, Wolf A, Meisel H, Kaiser M, Ellerbrok H, Pauli G (2009) High HEV presence in four different wild boar populations in East and West Germany. Vet Microbiol 139:270–278PubMedCrossRef Adlhoch C, Wolf A, Meisel H, Kaiser M, Ellerbrok H, Pauli G (2009) High HEV presence in four different wild boar populations in East and West Germany. Vet Microbiol 139:270–278PubMedCrossRef
40.
go back to reference Schielke A, Sachs K, Lierz M, Appel B, Jansen A, Johne R (2009) Detection of hepatitis E virus in wild boars of rural and urban regions in Germany and whole genome characterization of an endemic strain. Virol J 6:58PubMedCentralPubMedCrossRef Schielke A, Sachs K, Lierz M, Appel B, Jansen A, Johne R (2009) Detection of hepatitis E virus in wild boars of rural and urban regions in Germany and whole genome characterization of an endemic strain. Virol J 6:58PubMedCentralPubMedCrossRef
41.
go back to reference Wenzel JJ, Preiss J, Schemmerer M, Huber B, Plentz A, Jilg W (2011) Detection of hepatitis E virus (HEV) from porcine livers in Southeastern Germany and high sequence homology to human HEV isolates. J Clin Virol 52:50–54PubMedCrossRef Wenzel JJ, Preiss J, Schemmerer M, Huber B, Plentz A, Jilg W (2011) Detection of hepatitis E virus (HEV) from porcine livers in Southeastern Germany and high sequence homology to human HEV isolates. J Clin Virol 52:50–54PubMedCrossRef
42.
go back to reference Baechlein C, Seehusen F, Nathues H, Beilage E, Baumgartner W, Grummer B (2013) Molecular detection of hepatitis E virus in German domestic pigs. Berl Munch Tierarztl Wochenschr 126:25–31PubMed Baechlein C, Seehusen F, Nathues H, Beilage E, Baumgartner W, Grummer B (2013) Molecular detection of hepatitis E virus in German domestic pigs. Berl Munch Tierarztl Wochenschr 126:25–31PubMed
43.
go back to reference Baechlein C, Schielke A, Johne R, Ulrich RG, Baumgaertner W, Grummer B (2010) Prevalence of hepatitis E virus-specific antibodies in sera of German domestic pigs estimated by using different assays. Vet Microbiol 144:187–191PubMedCrossRef Baechlein C, Schielke A, Johne R, Ulrich RG, Baumgaertner W, Grummer B (2010) Prevalence of hepatitis E virus-specific antibodies in sera of German domestic pigs estimated by using different assays. Vet Microbiol 144:187–191PubMedCrossRef
44.
go back to reference Dremsek P, Joel S, Baechlein C, Pavio N, Schielke A, Ziller M, Durrwald R, Renner C, Groschup MH, Johne R, Krumbholz A, Ulrich RG (2013) Hepatitis E virus seroprevalence of domestic pigs in Germany determined by a novel in-house and two reference ELISAs. J Virol Methods 190:11–16PubMedCrossRef Dremsek P, Joel S, Baechlein C, Pavio N, Schielke A, Ziller M, Durrwald R, Renner C, Groschup MH, Johne R, Krumbholz A, Ulrich RG (2013) Hepatitis E virus seroprevalence of domestic pigs in Germany determined by a novel in-house and two reference ELISAs. J Virol Methods 190:11–16PubMedCrossRef
45.
go back to reference Krumbholz A, Joel S, Neubert A, Dremsek P, Durrwald R, Johne R, Hlinak A, Walther M, Lange J, Wutzler P, Sauerbrei A, Ulrich RG, Zell R (2013) Age-related and regional differences in the prevalence of hepatitis E virus-specific antibodies in pigs in Germany. Vet Microbiol 167:394–402PubMedCrossRef Krumbholz A, Joel S, Neubert A, Dremsek P, Durrwald R, Johne R, Hlinak A, Walther M, Lange J, Wutzler P, Sauerbrei A, Ulrich RG, Zell R (2013) Age-related and regional differences in the prevalence of hepatitis E virus-specific antibodies in pigs in Germany. Vet Microbiol 167:394–402PubMedCrossRef
47.
go back to reference Schnegg A, Burgisser P, Andre C, Kenfak-Foguena A, Canellini G, Moradpour D, Abravanel F, Izopet J, Cavassini M, Darling KE (2013) An analysis of the benefit of using HEV genotype 3 antigens in detecting anti-HEV IgG in a European population. PLoS One 8:e62980PubMedCentralPubMedCrossRef Schnegg A, Burgisser P, Andre C, Kenfak-Foguena A, Canellini G, Moradpour D, Abravanel F, Izopet J, Cavassini M, Darling KE (2013) An analysis of the benefit of using HEV genotype 3 antigens in detecting anti-HEV IgG in a European population. PLoS One 8:e62980PubMedCentralPubMedCrossRef
49.
go back to reference Krumbholz A, Lange J, Durrwald R, Walther M, Muller TH, Kuhnel D, Wutzler P, Sauerbrei A, Zell R (2014) Prevalence of antibodies to European porcine influenza viruses in humans living in high pig density areas of Germany. Med Microbiol Immunol 203:13–24PubMedCrossRef Krumbholz A, Lange J, Durrwald R, Walther M, Muller TH, Kuhnel D, Wutzler P, Sauerbrei A, Zell R (2014) Prevalence of antibodies to European porcine influenza viruses in humans living in high pig density areas of Germany. Med Microbiol Immunol 203:13–24PubMedCrossRef
50.
go back to reference Sauerbrei A, Langenhan T, Brandstadt A, Schmidt-Ott R, Krumbholz A, Girschick, Huppertz H, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Wutzler P (2014) Prevalence of antibodies against influenza A and B viruses in children in Germany, 2008 to 2010. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 19 Sauerbrei A, Langenhan T, Brandstadt A, Schmidt-Ott R, Krumbholz A, Girschick, Huppertz H, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Wutzler P (2014) Prevalence of antibodies against influenza A and B viruses in children in Germany, 2008 to 2010. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 19
51.
go back to reference Krumbholz A, Neubert A, Girschick H, Huppertz HI, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Sauerbrei A (2013) Prevalence of antibodies against hepatitis A virus among children and adolescents in Germany. Med Microbiol Immunol 202:417–424PubMedCrossRef Krumbholz A, Neubert A, Girschick H, Huppertz HI, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Sauerbrei A (2013) Prevalence of antibodies against hepatitis A virus among children and adolescents in Germany. Med Microbiol Immunol 202:417–424PubMedCrossRef
52.
go back to reference Kaufmann A, Kenfak-Foguena A, Andre C, Canellini G, Burgisser P, Moradpour D, Darling KE, Cavassini M (2011) Hepatitis E virus seroprevalence among blood donors in southwest Switzerland. PLoS One 6:e21150PubMedCentralPubMedCrossRef Kaufmann A, Kenfak-Foguena A, Andre C, Canellini G, Burgisser P, Moradpour D, Darling KE, Cavassini M (2011) Hepatitis E virus seroprevalence among blood donors in southwest Switzerland. PLoS One 6:e21150PubMedCentralPubMedCrossRef
53.
go back to reference Meader E, Thomas D, Salmon R, Sillis M (2010) Seroprevalence of hepatitis E virus in the UK farming population. Zoonoses Public Health 57:504–509PubMedCrossRef Meader E, Thomas D, Salmon R, Sillis M (2010) Seroprevalence of hepatitis E virus in the UK farming population. Zoonoses Public Health 57:504–509PubMedCrossRef
54.
go back to reference Myint KS, Endy TP, Gibbons RV, Laras K, Mammen MP Jr, Sedyaningsih ER, Seriwatana J, Glass JS, Narupiti S, Corwin AL (2006) Evaluation of diagnostic assays for hepatitis E virus in outbreak settings. J Clin Microbiol 44:1581–1583PubMedCentralPubMedCrossRef Myint KS, Endy TP, Gibbons RV, Laras K, Mammen MP Jr, Sedyaningsih ER, Seriwatana J, Glass JS, Narupiti S, Corwin AL (2006) Evaluation of diagnostic assays for hepatitis E virus in outbreak settings. J Clin Microbiol 44:1581–1583PubMedCentralPubMedCrossRef
55.
go back to reference Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR (2006) A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65–71PubMedCrossRef Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR (2006) A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65–71PubMedCrossRef
56.
go back to reference Herremans M, Vennema H, Bakker J, van der Veer B, Duizer E, Benne CA, Waar K, Hendrixks B, Schneeberger P, Blaauw G, Kooiman M, Koopmans MP (2007) Swine-like hepatitis E viruses are a cause of unexplained hepatitis in the Netherlands. J Viral Hepat 14:140–146PubMedCrossRef Herremans M, Vennema H, Bakker J, van der Veer B, Duizer E, Benne CA, Waar K, Hendrixks B, Schneeberger P, Blaauw G, Kooiman M, Koopmans MP (2007) Swine-like hepatitis E viruses are a cause of unexplained hepatitis in the Netherlands. J Viral Hepat 14:140–146PubMedCrossRef
57.
go back to reference Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRef Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRef
58.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRef Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRef
59.
go back to reference Landis JR, Koch GG (1977) An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 33:363–374PubMedCrossRef Landis JR, Koch GG (1977) An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 33:363–374PubMedCrossRef
60.
go back to reference Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174PubMedCrossRef Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174PubMedCrossRef
61.
go back to reference Abdi H (2007) Bonferroni and Sidak corrections for multiple comparisons. In: Salkind NJ (ed) Encyclopedia of measurement and statistics. Sage, Thousand Oaks Abdi H (2007) Bonferroni and Sidak corrections for multiple comparisons. In: Salkind NJ (ed) Encyclopedia of measurement and statistics. Sage, Thousand Oaks
62.
go back to reference Pas SD, Streefkerk RH, Pronk M, de Man RA, Beersma MF, Osterhaus AD, van der Eijk AA (2013) Diagnostic performance of selected commercial HEV IgM and IgG ELISAs for immunocompromised and immunocompetent patients. J Clin Virol 58:629–634PubMedCrossRef Pas SD, Streefkerk RH, Pronk M, de Man RA, Beersma MF, Osterhaus AD, van der Eijk AA (2013) Diagnostic performance of selected commercial HEV IgM and IgG ELISAs for immunocompromised and immunocompetent patients. J Clin Virol 58:629–634PubMedCrossRef
63.
go back to reference Reinheimer C, Allwinn R, Berger A (2012) Hepatitis E: are psychiatric patients on special risk? Med Microbiol Immunol 201:171–175PubMedCrossRef Reinheimer C, Allwinn R, Berger A (2012) Hepatitis E: are psychiatric patients on special risk? Med Microbiol Immunol 201:171–175PubMedCrossRef
64.
go back to reference Juhl D, Baylis SA, Blumel J, Gorg S, Hennig H (2014) Seroprevalence and incidence of hepatitis E virus infection in German blood donors. Transfusion 54:49–56PubMedCrossRef Juhl D, Baylis SA, Blumel J, Gorg S, Hennig H (2014) Seroprevalence and incidence of hepatitis E virus infection in German blood donors. Transfusion 54:49–56PubMedCrossRef
65.
go back to reference Krumbholz A, Neubert A, Joel S, Girschick H, Huppertz HI, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Zell R, Sauerbrei A (2014) Prevalence of hepatitis E virus antibodies in children in Germany. Pediatr Infect Dis J 33:258–262PubMedCrossRef Krumbholz A, Neubert A, Joel S, Girschick H, Huppertz HI, Kaiser P, Liese J, Streng A, Niehues T, Peters J, Sauerbrey A, Schroten H, Tenenbaum T, Wirth S, Zell R, Sauerbrei A (2014) Prevalence of hepatitis E virus antibodies in children in Germany. Pediatr Infect Dis J 33:258–262PubMedCrossRef
66.
go back to reference Wenzel JJ, Preiss J, Schemmerer M, Huber B, Jilg W (2013) Test performance characteristics of Anti-HEV IgG assays strongly influence hepatitis E seroprevalence estimates. J Infect Dis 207:497–500PubMedCrossRef Wenzel JJ, Preiss J, Schemmerer M, Huber B, Jilg W (2013) Test performance characteristics of Anti-HEV IgG assays strongly influence hepatitis E seroprevalence estimates. J Infect Dis 207:497–500PubMedCrossRef
67.
go back to reference Bendall R, Ellis V, Ijaz S, Ali R, Dalton H (2010) A comparison of two commercially available anti-HEV IgG kits and a re-evaluation of anti-HEV IgG seroprevalence data in developed countries. J Med Virol 82:799–805PubMedCrossRef Bendall R, Ellis V, Ijaz S, Ali R, Dalton H (2010) A comparison of two commercially available anti-HEV IgG kits and a re-evaluation of anti-HEV IgG seroprevalence data in developed countries. J Med Virol 82:799–805PubMedCrossRef
68.
go back to reference Pischke S, Heim A, Bremer B, Raupach R, Horn-Wichmann R, Ganzenmueller T, Klose B, Goudeva L, Wagner F, Oehme A, Manns MP, Wedemeyer H (2011) Hepatitis E: an emerging infectious disease in Germany? Z Gastroenterol 49:1255–1257PubMedCrossRef Pischke S, Heim A, Bremer B, Raupach R, Horn-Wichmann R, Ganzenmueller T, Klose B, Goudeva L, Wagner F, Oehme A, Manns MP, Wedemeyer H (2011) Hepatitis E: an emerging infectious disease in Germany? Z Gastroenterol 49:1255–1257PubMedCrossRef
69.
go back to reference Anonymous (2013) Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2012, Robert Koch-Institut, Berlin Anonymous (2013) Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2012, Robert Koch-Institut, Berlin
70.
go back to reference Veitt R, Reichardt M, Wenzel J, Jilg W (2011) Autochthonous hepatitis E-virus infection as cause of acute hepatitis in Germany—a case report. Z Gastroenterol 49:42–46PubMedCrossRef Veitt R, Reichardt M, Wenzel J, Jilg W (2011) Autochthonous hepatitis E-virus infection as cause of acute hepatitis in Germany—a case report. Z Gastroenterol 49:42–46PubMedCrossRef
71.
go back to reference Christensen PB, Engle RE, Hjort C, Homburg KM, Vach W, Georgsen J, Purcell RH (2008) Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. Clin Infect Dis Off Publ Infect Dis Soc Am 47:1026–1031CrossRef Christensen PB, Engle RE, Hjort C, Homburg KM, Vach W, Georgsen J, Purcell RH (2008) Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. Clin Infect Dis Off Publ Infect Dis Soc Am 47:1026–1031CrossRef
72.
go back to reference Renou C, Moreau X, Pariente A, Cadranel JF, Maringe E, Morin T, Causse X, Payen JL, Izopet J, Nicand E, Bourliere M, Penaranda G, Hardwigsen J, Gerolami R, Peron JM, Pavio N (2008) A national survey of acute hepatitis E in France. Aliment Pharmacol Ther 27:1086–1093PubMedCrossRef Renou C, Moreau X, Pariente A, Cadranel JF, Maringe E, Morin T, Causse X, Payen JL, Izopet J, Nicand E, Bourliere M, Penaranda G, Hardwigsen J, Gerolami R, Peron JM, Pavio N (2008) A national survey of acute hepatitis E in France. Aliment Pharmacol Ther 27:1086–1093PubMedCrossRef
73.
go back to reference Mansuy JM, Bendall R, Legrand-Abravanel F, Saune K, Miedouge M, Ellis V, Rech H, Destruel F, Kamar N, Dalton HR, Izopet J (2011) Hepatitis E virus antibodies in blood donors, France. Emerg Infect Dis 17:2309–2312PubMedCentralPubMedCrossRef Mansuy JM, Bendall R, Legrand-Abravanel F, Saune K, Miedouge M, Ellis V, Rech H, Destruel F, Kamar N, Dalton HR, Izopet J (2011) Hepatitis E virus antibodies in blood donors, France. Emerg Infect Dis 17:2309–2312PubMedCentralPubMedCrossRef
74.
go back to reference Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaaijer HL (2013) Silent hepatitis E virus infection in Dutch blood donors, 2011 to 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 18 Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaaijer HL (2013) Silent hepatitis E virus infection in Dutch blood donors, 2011 to 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 18
75.
go back to reference Zhang S, Tian D, Zhang Z, Xiong J, Yuan Q, Ge S, Zhang J, Xia N (2009) Clinical significance of anti-HEV IgA in diagnosis of acute genotype 4 hepatitis E virus infection negative for anti-HEV IgM. Dig Dis Sci 54:2512–2518PubMedCrossRef Zhang S, Tian D, Zhang Z, Xiong J, Yuan Q, Ge S, Zhang J, Xia N (2009) Clinical significance of anti-HEV IgA in diagnosis of acute genotype 4 hepatitis E virus infection negative for anti-HEV IgM. Dig Dis Sci 54:2512–2518PubMedCrossRef
76.
go back to reference Tian DY, Chen Y, Xia NS (2006) Significance of serum IgA in patients with acute hepatitis E virus infection. World J Gastroenterol 12:3919–3923PubMed Tian DY, Chen Y, Xia NS (2006) Significance of serum IgA in patients with acute hepatitis E virus infection. World J Gastroenterol 12:3919–3923PubMed
Metadata
Title
Seroprevalence of hepatitis E virus (HEV) in humans living in high pig density areas of Germany
Authors
Andi Krumbholz
Sebastian Joel
Paul Dremsek
Anne Neubert
Reimar Johne
Ralf Dürrwald
Mario Walther
Thomas H. Müller
Detlef Kühnel
Jeannette Lange
Peter Wutzler
Andreas Sauerbrei
Rainer G. Ulrich
Roland Zell
Publication date
01-08-2014
Publisher
Springer Berlin Heidelberg
Published in
Medical Microbiology and Immunology / Issue 4/2014
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-014-0336-3

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