Sero-molecular epidemiology of hepatitis E virus in pigs and human contacts in Ghana.
Infectious disease reservoirs
Livestock
One health
Viral hepatitis
Zoonoses
Journal
One health outlook
ISSN: 2524-4655
Titre abrégé: One Health Outlook
Pays: England
ID NLM: 101769253
Informations de publication
Date de publication:
22 Jun 2021
22 Jun 2021
Historique:
received:
07
01
2021
accepted:
21
04
2021
entrez:
22
6
2021
pubmed:
23
6
2021
medline:
23
6
2021
Statut:
epublish
Résumé
Hepatitis E virus (HEV) is among the leading causes of viral hepatitis in most developing countries. Zoonotic acquisition of HEV genotype 3 from swine has come into focus more recently. Available studies on HEV in Ghana and other countries in the region do not provide enough information towards understanding the epidemiology of HEV in human and animal populations. Towards this end, we conducted a comparative cross-sectional study to determine the seroprevalence and risk factors associated with HEV exposure, both in swine and humans working on pig farms in typical local settings. The presence of viral RNA in human and swine samples was also evaluated, along with classification of viral sequences from HEV-positive samples. Structured questionnaires soliciting information on pigs reared, as well as socio-demographic information including age, sex and educational background of humans was collected. A total of 10 ml and 5 ml of whole blood was collected from pigs and human participants respectively. ELISA and real-time RT-PCR were performed on the sera for the qualitative detection of IgG antibodies to hepatitis E virus and viral RNA, respectively. Five hundred and forty-four (544) human participants including 264 swine contacts and 280 swine non-contacts were enrolled in the study. Although the proportion of HEV IgG antibodies was higher in contact groups (114; 54.3%) than non-contact groups (96; 45.7%), a multivariate analysis did not show any significant difference. No HEV RNA was detected in human samples. Similarly, 720 pigs were sampled from 18 farms located in five regions in Ghana. Twenty-three (23) of the pigs (3.2, 95%CI = 2.0-4.8) were positive for HEV RNA by real-time RT-PCR testing. Sequences obtained from HEV-positive samples were found to share high sequence identities with each other and clustered with other genotype 3 viruses indicating the existence of circulating zoonotic genotype 3 viruses on farms. Although we did not find evidence of pig to human transmission of HEV genotype 3, the presence of this genotype in pigs shows the potential for possible zoonotic transmission in African farm settings and buttresses the importance of active surveillance for the infection among at risk populations.
Sections du résumé
BACKGROUND
BACKGROUND
Hepatitis E virus (HEV) is among the leading causes of viral hepatitis in most developing countries. Zoonotic acquisition of HEV genotype 3 from swine has come into focus more recently. Available studies on HEV in Ghana and other countries in the region do not provide enough information towards understanding the epidemiology of HEV in human and animal populations. Towards this end, we conducted a comparative cross-sectional study to determine the seroprevalence and risk factors associated with HEV exposure, both in swine and humans working on pig farms in typical local settings. The presence of viral RNA in human and swine samples was also evaluated, along with classification of viral sequences from HEV-positive samples.
METHODS
METHODS
Structured questionnaires soliciting information on pigs reared, as well as socio-demographic information including age, sex and educational background of humans was collected. A total of 10 ml and 5 ml of whole blood was collected from pigs and human participants respectively. ELISA and real-time RT-PCR were performed on the sera for the qualitative detection of IgG antibodies to hepatitis E virus and viral RNA, respectively.
RESULTS
RESULTS
Five hundred and forty-four (544) human participants including 264 swine contacts and 280 swine non-contacts were enrolled in the study. Although the proportion of HEV IgG antibodies was higher in contact groups (114; 54.3%) than non-contact groups (96; 45.7%), a multivariate analysis did not show any significant difference. No HEV RNA was detected in human samples. Similarly, 720 pigs were sampled from 18 farms located in five regions in Ghana. Twenty-three (23) of the pigs (3.2, 95%CI = 2.0-4.8) were positive for HEV RNA by real-time RT-PCR testing. Sequences obtained from HEV-positive samples were found to share high sequence identities with each other and clustered with other genotype 3 viruses indicating the existence of circulating zoonotic genotype 3 viruses on farms. Although we did not find evidence of pig to human transmission of HEV genotype 3, the presence of this genotype in pigs shows the potential for possible zoonotic transmission in African farm settings and buttresses the importance of active surveillance for the infection among at risk populations.
Identifiants
pubmed: 34154674
doi: 10.1186/s42522-021-00043-w
pii: 10.1186/s42522-021-00043-w
pmc: PMC8218416
doi:
Types de publication
Journal Article
Langues
eng
Pagination
13Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : DR 772/12-1
Références
Van der Poel W, Verschoor F, van der Heide R, Herrera M-I, Vivo A, Kooreman M, et al. Hepatitis E virus sequences in swine related to sequences in humans, The Netherlands. Emerg Infect Dis. 2001;7(6):970–6. https://doi.org/10.3201/eid0706.010608 .
doi: 10.3201/eid0706.010608
pubmed: 11747723
pmcid: 2631914
Purcell RH, Emerson SU. Hidden danger: the raw facts about hepatitis E virus. J Infect Dis. 2010;202(6):819–21. https://doi.org/10.1086/655900 .
doi: 10.1086/655900
pubmed: 20695795
Pauli G, Aepfelbacher M, Bauerfeind U, Blümel J, Burger R, Gärtner B, et al. Hepatitis E virus. Transfus Med Hemother. 2015;42(4):247–65. https://doi.org/10.1159/000431191 .
doi: 10.1159/000431191
pubmed: 26557817
pmcid: 4569202
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. https://doi.org/10.4269/ajtmh.2008.78.1012 .
doi: 10.4269/ajtmh.2008.78.1012
pubmed: 18541786
Adjei A, Aviyase J, Tettey Y, Adu-Gyamfi C, Mingle J, Ayeh-Kumi P, et al. Heatitis E virus infection among pig handlers in Accra, Ghana. East Afr Med J. 2009;86(8):359–63.
pubmed: 20575309
Balayan MS, Andjaparidze AG, Savinskaya SS, Ketiladze ES, Braginsky DM, Savinov AP, et al. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology. 1983;20(1):23–31. https://doi.org/10.1159/000149370 .
doi: 10.1159/000149370
pubmed: 6409836
Vasickova P, Psikal I, Kralik P, Widen F, Hubalek Z, Pavlik I. Hepatitis E virus: a review. Vet Med Praha. 2007;52(9):365.
doi: 10.17221/1999-VETMED
Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2012;380(9859):2095–128.
doi: 10.1016/S0140-6736(12)61728-0
Tsega E, Krawczynski K, Hansson B, Nordenfelt E. Hepatitis E virus infection in pregnancy in Ethiopia. Ethiop Med J. 1993;31(3):173–81.
pubmed: 8404882
Pérez-Gracia MT, García M, Suay B, Mateos-Lindemann ML. Current knowledge on hepatitis E. J Clin Transl Hepatol. 2015;3(2):117–26. https://doi.org/10.14218/JCTH.2015.00009 .
doi: 10.14218/JCTH.2015.00009
pubmed: 26355220
pmcid: 4548356
Ankcorn M, Tedder R. Hepatitis E: the current state of play. Transfus Med. 2017;27(2):84–95. https://doi.org/10.1111/tme.12405 .
doi: 10.1111/tme.12405
pubmed: 28382704
Tei S, Kitajima N, Takahashi K, Mishiro S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet. 2003;362(9381):371–3. https://doi.org/10.1016/S0140-6736(03)14025-1 .
doi: 10.1016/S0140-6736(03)14025-1
pubmed: 12907011
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 .
doi: 10.1016/j.ijfoodmicro.2014.10.005
pubmed: 25462920
Dalton HR, van Eijk JJ, Cintas P, Madden RG, Jones C, Webb GW, et al. Hepatitis E virus infection and acute non-traumatic neurological injury: a prospective multicentre study. J Hepatol. 2017;67(5):925–32. https://doi.org/10.1016/j.jhep.2017.07.010 .
doi: 10.1016/j.jhep.2017.07.010
pubmed: 28734938
Kamar N, Bendall RP, Peron JM, Cintas P, Prudhomme L, Mansuy JM, et al. Hepatitis E virus and neurologic disorders. Emerg Infect Dis. 2011;17(2):173–9. https://doi.org/10.3201/eid1702.100856 .
doi: 10.3201/eid1702.100856
pubmed: 21291585
pmcid: 3298379
Shao Z-j, Li J-h, Zheng Y-j, Zhang J-x, Ma Y-h, Ma W-t, et al. Epidemiological screening for hepatitis E virus in bile specimens from livestock in Northwest China. J Clin Microbiol. 2009;47(3):814–6.
doi: 10.1128/JCM.01309-08
Meng X-J, Halbur PG, Shapiro MS, Govindarajan S, Bruna JD, Mushahwar IK, et al. Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol. 1998;72(12):9714–21. https://doi.org/10.1128/JVI.72.12.9714-9721.1998 .
doi: 10.1128/JVI.72.12.9714-9721.1998
pubmed: 9811705
pmcid: 110481
Halbur P, Kasorndorkbua C, Gilbert C, Guenette D, Potters M, Purcell R, et al. Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol. 2001;39(3):918–23. https://doi.org/10.1128/JCM.39.3.918-923.2001 .
doi: 10.1128/JCM.39.3.918-923.2001
pubmed: 11230404
pmcid: 87850
Yugo DM, Meng X-J. Hepatitis E virus: foodborne, waterborne and zoonotic transmission. Int J Environ Res Public Health. 2013;10(10):4507–33. https://doi.org/10.3390/ijerph10104507 .
doi: 10.3390/ijerph10104507
pubmed: 24071919
pmcid: 3823334
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. https://doi.org/10.1128/JCM.01686-17 .
Zhang Y, Wang L, Zeng H, Gong W, Wang L, Zhuang H. Development and validation of a new serum standard for the measurement of anti-HEV antibodies in animals. J Med Virol. 2017;89(3):497–501. https://doi.org/10.1002/jmv.24651 .
doi: 10.1002/jmv.24651
pubmed: 27487450
Van der Poel W, Pavio N, Van der Goot J, Van Es M, Martin M, Engel B. Development and validation of a genotype 3 recombinant protein-based immunoassay for hepatitis E virus serology in swine. Braz J Med Biol Res. 2014;47(4):334–9. https://doi.org/10.1590/1414-431X20133249 .
doi: 10.1590/1414-431X20133249
pubmed: 24676472
pmcid: 4075298
Krumbholz A, Joel S, Neubert A, Dremsek P, Dürrwald R, Johne R, et al. Age-related and regional differences in the prevalence of hepatitis E virus-specific antibodies in pigs in Germany. Vet Microbiol. 2013;167(3–4):394–402. https://doi.org/10.1016/j.vetmic.2013.10.001 .
doi: 10.1016/j.vetmic.2013.10.001
pubmed: 24238666
Ijaz S, Arnold E, Banks M, Bendall RP, Cramp ME, Cunningham R, et al. Non–travel-associated hepatitis E in England and wales: demographic, clinical, and molecular epidemiological characteristics. J Infect Dis. 2005;192(7):1166–72. https://doi.org/10.1086/444396 .
doi: 10.1086/444396
pubmed: 16136458
Dalton HR, Stableforth W, Thurairajah P, Hazeldine S, Remnarace R, Usama W, et al. Autochthonous hepatitis E in Southwest England: natural history, complications and seasonal variation, and hepatitis E virus IgG seroprevalence in blood donors, the elderly and patients with chronic liver disease. Eur J Gastroenterol Hepatol. 2008;20(8):784–90. https://doi.org/10.1097/MEG.0b013e3282f5195a .
doi: 10.1097/MEG.0b013e3282f5195a
pubmed: 18617784
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 .
doi: 10.1002/jmv.20206
pubmed: 15368508
Mitsui T, Tsukamoto Y, Hirose A, Suzuki S, Yamazaki C, Masuko K, et al. Distinct changing profiles of hepatitis A and E virus infection among patients with acute hepatitis, patients on maintenance hemodialysis and healthy individuals in Japan. J Med Virol. 2006;78(8):1015–24. https://doi.org/10.1002/jmv.20657 .
doi: 10.1002/jmv.20657
pubmed: 16789007
Mansuy JM, Legrand-Abravanel F, Calot JP, Peron JM, Alric L, Agudo S, et al. High prevalence of anti-hepatitis E virus antibodies in blood donors from south West France. J Med Virol. 2008;80(2):289–93. https://doi.org/10.1002/jmv.21056 .
doi: 10.1002/jmv.21056
pubmed: 18098159
Hewitt J, Harte D, Sutherland M, Croucher D, Fouche L, Flanagan P, et al. Prevalence of hepatitis E virus antibodies and infection in New Zealand blood donors. N Z Med J. 2018;131(1469):38–43.
pubmed: 29389927
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 .
doi: 10.1016/j.jcv.2016.06.010
pubmed: 27393938
Adjei AA, Aviyase JT, Tettey Y, Adu-Gyamfi C, Mingle JA, Ayeh-Kumi PF, et al. Hepatitis E virus infection among pig handlers in Accra, Ghana. East Afr Med J. 2009;86(8):359–63.
pubmed: 20575309
Adjei AA, Tettey Y, Aviyase JT, Adu-Gyamfi C, Mingle JA, Nartey ET. Unexpected elevated alanine aminotransferase, aspartate aminotransferase levels and hepatitis E virus infection among persons who work with pigs in Accra, Ghana. Virol J. 2010;7(1):1–9.
doi: 10.1186/1743-422X-7-336
Adjei AA, Tettey Y, Aviyase JT, Adu-Gyamfi C, Obed S, Mingle JA, et al. Hepatitis E virus infection is highly prevalent among pregnant women in Accra, Ghana. Virol J. 2009;6(1):1–5.
doi: 10.1186/1743-422X-6-108
Tettey Y, Adjei A, Ayivase J, Adu-Gyamfi C, Mingle J, Nartey E, et al. Serological evidence of hepatitis E virus infection among volunteer blood donors at the Accra area blood transfusion center, Accra, Ghana. J Ghana Sci Assoc. 2011;13(2):64–73.
Martinson FE, Marfo VY, Degraaf J. Hepatitis E virus seroprevalence in children living in rural Ghana. West Afr J Med. 1999;18(2):76–9.
pubmed: 10504860
Feldt T, Sarfo FS, Zoufaly A, Phillips RO, Burchard G, van Lunzen J, et al. Hepatitis E virus infections in HIV-infected patients in Ghana and Cameroon. J Clin Virol. 2013;58(1):18–23. https://doi.org/10.1016/j.jcv.2013.05.004 .
doi: 10.1016/j.jcv.2013.05.004
pubmed: 23743346
Ofosu-Appiah L, Boney J, Adiku T, Barnor J, Odoom J. Serological and molecular evidence of hepatitis E infection among patients with suspected viral hepatitis seen at Korle-Bu teaching hospital, Accra. J Sci Res Rep. 2016;10(1):1–10.
Meldal B, Sarkodie F, Owusu-Ofori S, Allain JP. Hepatitis E virus infection in Ghanaian blood donors–the importance of immunoassay selection and confirmation. Vox Sang. 2013;104(1):30–6. https://doi.org/10.1111/j.1423-0410.2012.01637.x .
doi: 10.1111/j.1423-0410.2012.01637.x
pubmed: 22845878
Bonney JHK, Osei-Kwasi M, Adiku TK, Barnor JS, Amesiya R, Kubio C, et al. Hospital-based surveillance for viral hemorrhagic fevers and hepatitides in Ghana. PLoS Negl Trop Dis. 2013;7(9):e2435. https://doi.org/10.1371/journal.pntd.0002435 .
doi: 10.1371/journal.pntd.0002435
pubmed: 24069490
pmcid: 3777898
Bonney JHK, Kwame-Aryee RA, Obed S, Tamatey AA, Barnor JS, Armah NB, et al. Fatal hepatitis E viral infection in pregnant women in Ghana: a case series. BMC Res Notes. 2012;5(1):478.
doi: 10.1186/1756-0500-5-478
Shirazi R, Pozzi P, Wax M, Bar-Or I, Asulin E, Lustig Y, et al. Hepatitis E in pigs in Israel: seroprevalence, molecular characterisation and potential impact on humans. Euro Surveill. 2018;23(49):1800067.
doi: 10.2807/1560-7917.ES.2018.23.49.1800067
Cannon R, Roe R. Livestock disease surveys: a field manualforveterinarians. Canberra: Australia Australian Gvt Publishing Service; 1982.
Zhang Z, Zhang H, Liu T. Study on body temperature detection of pig based on infrared technology: a review. Artif Intell Agric. 2019;1:14–26. https://doi.org/10.1016/j.aiia.2019.02.002 .
doi: 10.1016/j.aiia.2019.02.002
Olsen B, Axelsson-Olsson D, Thelin A, Weiland O. Unexpected high prevalence of IgG-antibodies to hepatitis E virus in Swedish pig farmers and controls. Scand J Infect Dis. 2006;38(1):55–8. https://doi.org/10.1080/00365540500321470 .
doi: 10.1080/00365540500321470
pubmed: 16338839
Wenzel JJ, Preiss J, Schemmerer M, Huber B, Jilg W. Test performance characteristics of anti-HEV IgG assays strongly influence hepatitis E seroprevalence estimates. J Infect Dis. 2012;207(3):497–500. https://doi.org/10.1093/infdis/jis688 .
doi: 10.1093/infdis/jis688
pubmed: 23148290
Yan Q, Du H-l, Wang Y-b, Ge S-x, Huang S-j, Jiang L, et al. Comparison of two diagnostic reagents to detect anti-hepatitis E virus IgG antibodies. Chin J Zoonoses. 2008;24:1087–9.
Capai L, Falchi A, Charrel R. Meta-analysis of human IgG anti-HEV seroprevalence in industrialized countries and a review of literature. Viruses. 2019;11(1):84. https://doi.org/10.3390/v11010084 .
doi: 10.3390/v11010084
pmcid: 6357031
Bohm K, Strömpl J, Krumbholz A, Zell R, Krause G, Sievers C. Establishment of a highly sensitive assay for detection of hepatitis E virus-specific immunoglobulins. J Clin Microbiol. 2020;58(2):e01029–19.
doi: 10.1128/JCM.01029-19
Caruso C, Modesto P, Bertolini S, Peletto S, Acutis P, Dondo A, et al. Serological and virological survey of hepatitis E virus in wild boar populations in northwestern Italy: detection of HEV subtypes 3e and 3f. Arch Virol. 2015;160(1):153–60. https://doi.org/10.1007/s00705-014-2246-5 .
doi: 10.1007/s00705-014-2246-5
pubmed: 25283611
Drexler JF, Seelen A, Corman VM, Fumie Tateno A, Cottontail V, Melim Zerbinati R, et al. Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae. J Virol. 2012;86(17):9134–47. https://doi.org/10.1128/JVI.00800-12 .
doi: 10.1128/JVI.00800-12
pubmed: 22696648
pmcid: 3416139
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754–5. https://doi.org/10.1093/bioinformatics/17.8.754 .
doi: 10.1093/bioinformatics/17.8.754
pubmed: 11524383
pmcid: 11524383
El-Duah P, Dei D, Binger T, Sylverken A, Wollny R, Tasiame W, et al. Detection and genomic characterization of hepatitis E virus genotype 3 from pigs in Ghana, Africa. One Health Outlook. 2020;2(1):1–9.
doi: 10.1186/s42522-020-00018-3
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 .
doi: 10.1099/jgv.0.000393
pubmed: 26743685
pmcid: 5588893
El-Esnawy N. Examination for hepatitis E virus in wastewater treatment plants and workers by nested RT-PCR and ELISA. J Egypt Public Health Assoc. 2000;75(1–2):219–31.
pubmed: 17219857
Stoszek SK, Abdel-Hamid M, Saleh DAA, Kafrawy SE, Narooz S, Hawash Y, et al. High prevalence of hepatitis E antibodies in pregnant Egyptian women. Trans R Soc Trop Med Hyg. 2006;100(2):95–101. https://doi.org/10.1016/j.trstmh.2004.12.005 .
doi: 10.1016/j.trstmh.2004.12.005
pubmed: 16257426
Owusu M, Bonney JK, Annan AA, Mawuli G, Okyere K, Mutocheluh M, et al. Aetiology of viral hepatitis among jaundiced patients presenting to a tertiary hospital in Ghana. PLoS One. 2018;13(9):e0203699. https://doi.org/10.1371/journal.pone.0203699 .
doi: 10.1371/journal.pone.0203699
pubmed: 30208084
pmcid: 6135398
Adjei AA, Tettey Y, Aviyase JT, Adu-Gyamfi C, Mingle JA, Nartey ET. Unexpected elevated alanine aminotransferase, asparte aminotransferase levels and hepatitis E virus infection among persons who work with pigs in Accra, Ghana. Virol J. 2010;7(1):336. https://doi.org/10.1186/1743-422X-7-336 .
doi: 10.1186/1743-422X-7-336
pubmed: 21092196
pmcid: 2995795
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 .
doi: 10.1016/j.vetmic.2009.03.017
pubmed: 19361937
Christensen PB, Engle RE, Hjort C, Homburg KM, Vach W, Georgsen J, et al. Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. Clin Infect Dis. 2008;47(8):1026–31. https://doi.org/10.1086/591970 .
doi: 10.1086/591970
pubmed: 18781880
Pavio N, Doceul V, Bagdassarian E, Johne R. Recent knowledge on hepatitis E virus in Suidae reservoirs and transmission routes to human. Vet Res. 2017;48(1):78. https://doi.org/10.1186/s13567-017-0483-9 .
doi: 10.1186/s13567-017-0483-9
pubmed: 29157309
pmcid: 5696788
Meng X, Wiseman B, Elvinger F, Guenette D, Toth T, Engle R, et al. 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. 2002;40(1):117–22. https://doi.org/10.1128/JCM.40.1.117-122.2002 .
doi: 10.1128/JCM.40.1.117-122.2002
pubmed: 11773103
pmcid: 120098
Kaufmann A, Kenfak-Foguena A, Andre C, Canellini G, Bürgisser P, Moradpour D, et al. Hepatitis E virus seroprevalence among blood donors in Southwest Switzerland. PLoS One. 2011;6(6):e21150. https://doi.org/10.1371/journal.pone.0021150 .
doi: 10.1371/journal.pone.0021150
pubmed: 21701586
pmcid: 3118806
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. 2012;201(2):239–44. https://doi.org/10.1007/s00430-011-0210-5 .
doi: 10.1007/s00430-011-0210-5
pubmed: 21773797
Taus K, Schmoll F, El-Khatib Z, Auer H, Holzmann H, Aberle S, et al. Occupational swine exposure and hepatitis E virus, Leptospira, Ascaris suum seropositivity and MRSA colonization in Austrian veterinarians, 2017–2018—a cross-sectional study. Zoonoses Public Health. 2019;66(7):842–51. https://doi.org/10.1111/zph.12633 .
doi: 10.1111/zph.12633
pubmed: 31419070
pmcid: 6851874
Silva SMT, Oliveira JM, Vitral CL, Vieira KA, Pinto MA, Souto FJD. Prevalence of hepatitis E virus antibodies in individuals exposed to swine in Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2012;107(3):338–41. https://doi.org/10.1590/S0074-02762012000300007 .
doi: 10.1590/S0074-02762012000300007
pubmed: 22510828
Temmam S, Besnard L, Andriamandimby SF, Foray C, Rasamoelina-Andriamanivo H, Héraud J-M, et al. High prevalence of hepatitis E in humans and pigs and evidence of genotype-3 virus in swine, Madagascar. Am J Trop Med Hyg. 2013;88(2):329–38. https://doi.org/10.4269/ajtmh.2012.12-0615 .
doi: 10.4269/ajtmh.2012.12-0615
pubmed: 23208879
pmcid: 3583326
Ukuli AQ, Mugimba KK. Seroprevalence of hepatitis E in swine abattoir workers. Afr Health Sci. 2017;17(4):1022–8. https://doi.org/10.4314/ahs.v17i4.9 .
doi: 10.4314/ahs.v17i4.9
pubmed: 29937872
pmcid: 5870292
Corwin A, Putri M, Winarno J, Lubis I, Suparmanto S, Sumardiati A, et al. Epidemic and sporadic hepatitis E virus transmission in West Kalimantan (Borneo), Indonesia. Am J Trop Med Hyg. 1997;57(1):62–5. https://doi.org/10.4269/ajtmh.1997.57.62 .
doi: 10.4269/ajtmh.1997.57.62
pubmed: 9242320
Arankalle VA, Tsarev SA, Chadha MS, Alling DW, Emerson SU, Banerjee K, et al. Age-specific prevalence of antibodies to hepatitis A and E viruses in Pune, India, 1982 and 1992. J Infect Dis. 1995;171(2):447–50. https://doi.org/10.1093/infdis/171.2.447 .
doi: 10.1093/infdis/171.2.447
pubmed: 7844387
Rapicetta M, Kondili LA, Pretolani S, Stroffolini T, Chionne P, Villano U, et al. Seroprevalence and anti-HEV persistence in the general population of the Republic of San Marino. J Med Virol. 1999;58(1):49–53. https://doi.org/10.1002/(SICI)1096-9071(199905)58:1<49::AID-JMV7>3.0.CO;2-C .
doi: 10.1002/(SICI)1096-9071(199905)58:1<49::AID-JMV7>3.0.CO;2-C
pubmed: 10223545