Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 15, Number 3—March 2009

Sources of Hepatitis E Virus Genotype 3 in the Netherlands

Saskia A. RutjesComments to Author , Willemijn J. Lodder, Froukje Lodder-Verschoor, Harold H.J.L. van den Berg, Harry Vennema, Erwin Duizer, Marion Koopmans, and Ana Maria de Roda Husman
Author affiliations: National Institute for Public Health and the Environment, Bilthoven, the Netherlands

Main Article

Table 1

Detection of hepatitis E virus RNA by RT-PCR for the ORF2 region of the genome in environmental samples, the Netherlands*

Source Origin Sample type Sampling year Matrix No. samples ORF2 (nt 6298–6494)†
No. (%) PCR positive Sequence
Pig Pig farm Pooled 2005 Feces 97 51 (53) 36‡
Individual 2002 Feces 2 2 (100) 2
Slaughterhouse Individual 2006 Feces 50 7 (14) 7
Butcher shop/ supermarket§ Individual 2005 Liver 62 4 (6) 3
Wild boar National Park Individual 2005 Feces 26 1 (4) 1
Muskrat Southeast Individual 1998–1999 Feces 150 0 0
Water Meuse River Filtered 2004–2005 Concentrate 12 2 (17) 2

*RT-PCR, reverse transcription–PCR; ORF, open reading frame.
†Position in Burmese hepatitis E virus strain (GenBank accession no. M73218).
‡Obtained by direct sequencing.
§Obtained from Bouwknegt et al. (28).

Main Article

  1. Zaaijer  HL, Kok  M, Lelie  PN, Timmerman  RJ, Chau  K, van der Pal  HJ. Hepatitis E in the Netherlands: imported and endemic. Lancet. 1993;341:826. DOIPubMedGoogle Scholar
  2. Mast  EE, Kuramoto  IK, Favorov  MO, Schoening  VR, Burkholder  BT, Shapiro  CN, Prevalence of and risk factors for antibody to hepatitis E virus seroactivity among blood donors in northern California. J Infect Dis. 1997;176:3440. DOIPubMedGoogle Scholar
  3. Lu  L, Li  C, Hagedorn  CH. Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol. 2006;16:536. DOIPubMedGoogle Scholar
  4. Haqshenas  G, Shivaprasad  HL, Woolcock  PR, Read  DH, Meng  XJ. Genetic identification and characterisation of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States. J Gen Virol. 2001;82:244962.PubMedGoogle Scholar
  5. Billam  P, Sun  ZF, Meng  XJ. Analysis of the complete genomic sequence of an apparently avirulent strain of avian hepatitis E virus (avian HEV) identified major genetic differences compared with the prototype pathogenic strain of avian HEV. J Gen Virol. 2007;88:153844. DOIPubMedGoogle Scholar
  6. Meng  XJ, Purcell  RH, Halbur  PG, Lehman  JR, Webb  DM, Tsareva  TS, A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A. 1997;94:98605. DOIPubMedGoogle Scholar
  7. Okamoto  H. Genetic variability and evolution of hepatitis E virus. Virus Res. 2007;127:21628. DOIPubMedGoogle Scholar
  8. Wibawa  ID, Suryadarma  IGA, Mulyanto  TF, Matsumoto  Y, Ninomiya  M, Takahashi  M, Identification of genotype 4 hepatitis E virus strains from a patient with acute hepatitis E and farm pigs in Bali, Indonesia. J Med Virol. 2007;79:113846. DOIPubMedGoogle Scholar
  9. Mochizuki  M, Ouchi  A, Kawakami  K, Ishida  T, Li  TC, Ikeda  H, Epidemiological study of hepatitis E virus infection of dogs and cats in Japan. Vet Rec. 2006;159:8534.PubMedGoogle Scholar
  10. Vitral  CL, Pinto  MA, Lewis-Ximenez  LL, Khundyakov  YE, dos Santos  DR, Gaspar  AM. Serological evidence of hepatitis E virus infection in different animal species from the Southeast of Brazil. Mem Inst Oswaldo Cruz. 2005;100:11722. DOIPubMedGoogle Scholar
  11. Easterbrook  JD, Kaplan  JB, Vanasco  NB, Reevers  WK, Purcell  RH, Kosoy  MY, A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiol Infect. 2007;135:11929. DOIPubMedGoogle Scholar
  12. Li  TC, Saito  M, Ogura  G, Ishibashi  O, Miyamura  T, Takeda  N. Serologic evidence for hepatitis E virus infection in mongoose. Am J Trop Med Hyg. 2006;74:9326.PubMedGoogle Scholar
  13. Tei  S, Kitajima  N, Takakashi  K, Mishiro  S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet. 2003;362:3713. DOIPubMedGoogle Scholar
  14. Matsuda  H, Okada  K, Takahashi  K, Mishiro  S. Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J Infect Dis. 2003;188:944. DOIPubMedGoogle Scholar
  15. Takahashi  K, Kitajima  N, Abe  N, Mishiro  S. Complete or near-complete nucleotide sequence of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology. 2004;330:5015. DOIPubMedGoogle Scholar
  16. Widdowson  MA, Jaspers  WJ, van der Poel  WH, Verschoor  F, de Roda Husman  AM, Winter  HL, Cluster of cases of acute hepatitis associated with hepatitis E virus infection acquired in the Netherlands. Clin Infect Dis. 2003;36:2933. DOIPubMedGoogle Scholar
  17. Waar  K, Herremans  MM, Vennema  H, Koopmans  MP, Benne  CA. Hepatitis E is a cause of unexplained hepatitis in The Netherlands. J Clin Virol. 2005;33:1459. DOIPubMedGoogle Scholar
  18. Herremans  M, Vennema  H, Bakker  J, van der Veer  B, Duizer  E, Benne  CA, Swine-like hepatitis E viruses are a cause of unexplained hepatitis in the Netherlands. J Viral Hepat. 2007;14:1406. DOIPubMedGoogle Scholar
  19. Borgen  K, Herremans  T, Duizer  E, Vennema  H, Rutjes  S, Bosman  A, Non-travel related hepatitis E virus genotype 3 infections in the Netherlands; A case series 2004–2006. BMC Infect Dis. 2008;8:61 . DOIPubMedGoogle Scholar
  20. Rutjes  SA, Lodder  WJ, Bouwknegt  M, de Roda Husman  AM. Increased hepatitis E virus prevalence on Dutch pig farms from 33% to 55% by using appropriate internal quality controls for RT-PCR. J Virol Methods. 2007;143:1126. DOIPubMedGoogle Scholar
  21. Borgsteede  FH, Tippen  JH, van der Giessen  JW. The musk rat (Ondatra zibethicus) as intermediate host of cestodes in the Netherlands. Vet Parasitol. 2003;117:2936. DOIPubMedGoogle Scholar
  22. Rutjes  SA, Italiaander  R, van den Berg  HH, Lodder  WJ, de Roda Husman  AM. Isolation and detection of enterovirus RNA from large-volume water samples by using the NucliSens miniMAG system and real-time nucleic acid sequence-based amplification. Appl Environ Microbiol. 2005;71:373440. DOIPubMedGoogle Scholar
  23. Boom  R, Sol  CJ, Salimans  MM, Jansen  CL, Wertheim van Dillen  PM, van der Noordaa  JS. Rapid and simple method for purification of nucleic acids. J Clin Microbiol. 1990;28:495503.PubMedGoogle Scholar
  24. Schlauder  GG, Desai  SM, Zanetti  AR, Tassopoulos  NC, Mushahwar  IK. Novel hepatitis E virus (HEV) isolates from Europe: evidence for additional genotypes of HEV. J Med Virol. 1999;57:24351. DOIPubMedGoogle Scholar
  25. van der Poel  WH, Verschoor  F, van de Heide  R, Herrera  MI, Vivo  A, Kooreman  M, Hepatitis E virus sequences in swine related to sequences in humans, the Netherlands. Emerg Infect Dis. 2001;7:9706.PubMedGoogle Scholar
  26. Wang  Y, Ling  R, Erker  JC, Zhang  H, Li  H, Desai  S, A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol. 1999;80:16977.PubMedGoogle Scholar
  27. Westrell  T, Teunis  P, van den Berg  H, Lodder  W, Ketelaars  H, Stenström  TA, Short- and long-term variations of norovirus concentrations in the Meuse River during a 2-year study period. Water Res. 2006;40:261320. DOIPubMedGoogle Scholar
  28. Bouwknegt  M, Lodder-Verschoor  F, van der Poel  W, Rutjes  SA, de Roda Husman  AM. Detection of hepatitis E virus in commercial livers in The Netherlands. J Food Prot. 2007;70:288995.PubMedGoogle Scholar
  29. Takahashi  M, Nishizawa  T, Miyajima  H, Gotanda  Y, Lita  T, Tsuda  F, Swine hepatitis E virus strains in Japan from four phylogenetic clusters comparable with those of Japanese isolates of human hepatitis E virus. J Gen Virol. 2003;84:85162. DOIPubMedGoogle Scholar
  30. Meng  XJ, Wiseman  B, Elvinger  F, Guenette  DK, Toth  TE, Engle  RE, 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;40:11722. DOIPubMedGoogle Scholar
  31. Bouwknegt  M, Engel  B, Herremans  MM, Widdowson  MA, Worm  HC, Koopmans  MP, Bayesian estimation of hepatitis E virus seroprevalence for populations with different exposure levels to swine in the Netherlands. Epidemiol Infect. 2008;136:56776. DOIPubMedGoogle Scholar
  32. El-Esnawy  NA. Examination for hepatitis E virus in wastewater treatment plants and workers by nested RT-PCR and ELISA. J Egypt Public Health Assoc. 2000;75:21931.PubMedGoogle Scholar
  33. Feagins  AR, Opriessnig  T, Guenette  DK, Halbur  PG, Meng  X-J. Detection and characterization of infectious hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J Gen Virol. 2007;88:9127. DOIPubMedGoogle Scholar
  34. Feagins  AR, Opriessnig  T, Guenette  DK, Halbur  PG, Meng  X-J. Inactivation of infectious hepatitis E virus present in commercial pig livers sold in local grocery stores in the United States. Int J Food Microbiol. 2008;123:327. DOIPubMedGoogle Scholar
  35. Favorov  MO, Kosoy  MY, Tsarev  SA, Childs  JE, Margolis  HS. Prevalence of antibody to hepatiaits E virus among rodents in the United States. J Infect Dis. 2000;181:44955. DOIPubMedGoogle Scholar
  36. Clemente-Casares  P, Pina  S, Buti  M, Jardi  R, Martin  M, Bofill-Mas  S, Hepatitis E virus epidemiology in industrialized countries. Emerg Infect Dis. 2003;9:44854.PubMedGoogle Scholar
  37. Pina  S, Buti  M, Cotrina  M, Piella  J, Girones  R. HEV identified in serum from humans with acute hepatitis and in sewage of animal origin in Spain. J Hepatol. 2000;33:82633. DOIPubMedGoogle Scholar
  38. Emerson  SU, Arankalle  VA, Purcell  RH. Thermal stability of hepatitis E virus. J Infect Dis. 2005;192:9303. DOIPubMedGoogle Scholar
  39. Tanaka  T, Takahashi  M, Kusano  E, Okamoto  H. Development and evaluation of an efficient cell-culture system for Hepatitis E virus. J Gen Virol. 2007;88:90311. DOIPubMedGoogle Scholar
  40. Ossiboff  RJ, Sheh  A, Shoton  J, Pesavento  PA, Parker  SL. Feline caliciviruses (FCVs) isolated from cats with virulent systemic diseases possess in vitro phenotypes distinct from those of other FCV isolates. J Gen Virol. 2007;88:50617. DOIPubMedGoogle Scholar

Main Article

Page created: December 07, 2010
Page updated: December 07, 2010
Page reviewed: December 07, 2010
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.