Skip to main content

Advertisement

SpringerLink
Log in

Hepatitis E virus genotypes 1 and 3 in wastewater samples in Tunisia

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Hepatitis E represents an important public-health concern throughout the world. It is one of the leading causes of hepatitis in North Africa, Asia and the Middle East. In Tunisia, the true burden of HEV infection is still unknown. The objectives of the present study were to assess the occurrence of hepatitis E virus in Tunisia through the monitoring of urban sewage and to characterize the strains identified using molecular assays. A total of 150 sewage samples (raw and treated) were collected from three wastewater treatment plants located in the regions of Monastir and Mahdia and analyzed by nested RT-PCR using a qualitative assay targeting the methyltransferase gene in ORF1. Of these, only three samples (2 %) were found to be positive for HEV, one belonging to genotype 1 and two to genotype 3. The results of the present study indicate a low level of virus excretion among the Tunisian population. Both genotypes 1 and 3 are circulating in this country, however, possibly causing sporadic infections. The presence of the zoonotic genotype 3, known to be transmitted to humans mainly by swine and demonstrated in Tunisia for the first time in this work, raises the question of possible reservoir species, since pork products are not consumed in this country, pigs are not bred, and wild boar is not endemic. Further studies will be needed to gather information on the occurrence and diversity of HEV strains circulating among humans and animals in Tunisia, and on possible animal reservoirs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Teo CG (2010) Much meat, much malady: changing perceptions of the epidemiology of hepatitis E. Clin Microbiol Infect 16:24–32

    Article  CAS  PubMed  Google Scholar 

  2. Yugo DM, Meng XJ (2013) Hepatitis E virus: foodborne, waterborne and zoonotic transmission. Int J Environ Res Public Health 10:4507–4533

    Article  PubMed Central  PubMed  Google Scholar 

  3. Li X, Kamili S, Krawczynski K (2006) Quantitative detection of hepatitis E virus RNA and dynamics of viral replication in experimental infection. J Viral Hepat 13:835–839

    Article  CAS  PubMed  Google Scholar 

  4. Nikiema J, Figoli A, Weissenbacher N, Langergraber G, Marrot B, Moulin P (2013) Wastewater treatment practices in Africa—experiences from seven countries. Sustain Sanit Pract 14(2013):26–34

    Google Scholar 

  5. Gharbi-Khelifi H, Sdiri K, Ferre V, Harrath R, Berthome M, Billaudel S, Aouni M (2007) A 1-year study of the epidemiology of hepatitis A virus in Tunisia. Clin Microbiol Infect 13:25–32

    Article  CAS  PubMed  Google Scholar 

  6. Muscillo M, Fratini M, Graffeo R, Sanguinetti M, Martella V, Green KY, Della Libera S, La Rosa G (2013) GIV noroviruses in wastewaters and in stool specimens from hospitalized patients. Food Environ Virol 5(4):194–202

  7. Fogeda M, Avellon A, Cilla CG, Echevarria JM (2009) Imported and autochthonous hepatitis E virus strains in Spain. J Med Virol 81:1743–1749

    Article  CAS  PubMed  Google Scholar 

  8. La Rosa G, Muscillo M, Spuri V, Garbuglia AR, La Scala P, Capobianchi MR (2011) Hepatitis E virus in Italy: molecular analysis of travel-related and autochthonous cases. J Gen Virol 92:1617–1626

    Article  CAS  PubMed  Google Scholar 

  9. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, Toth TE, Meng XJ (2002) Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol 40:1326–1332

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H (2006) Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods 137:325–333

    Article  CAS  PubMed  Google Scholar 

  11. La Rosa G, Fratini M, Muscillo M, Iaconelli M, Taffon S, Equestre M, Chionne P, Madonna E, Pisani G, Bruni R, Ciccaglione AR (2014) Molecular characterisation of human hepatitis E virus from Italy: comparative analysis of five reverse transcription-PCR assays. Virol J 11:72

    Article  PubMed Central  PubMed  Google Scholar 

  12. Kmush B, Wierzba T, Krain L, Nelson K, Labrique AB (2013) Epidemiology of hepatitis E in low- and middle-income countries of Asia and Africa. Semin Liver Dis 33:15–29

    Article  PubMed  Google Scholar 

  13. Houcine N, Jacques R, Salma F, Anne-Gaelle D, Amin S, Mohsen H, Hamadi B, Christophe R, Patrice A, Mahjoub A, Caroline S (2012) Seroprevalence of hepatitis E virus infection in rural and urban populations, Tunisia. Clin Microbiol Infect 18:E119–E121

    Article  PubMed  Google Scholar 

  14. Kamal SM, Mahmoud S, Hafez T, El-Fouly R (2010) Viral hepatitis a to e in South mediterranean countries. Mediterr J Hematol Infect Dis 2:e2010001

    PubMed Central  PubMed  Google Scholar 

  15. Hassine M, Sdiri K, Riabi S, Beji A, Aouni Z, Aouni M (2010) Detection of enteric viruses in wastewater of Monastir region by RT-PCR method. Tunis Med 88:70–75

    PubMed  Google Scholar 

  16. Chatterjee R, Tsarev S, Pillot J, Coursaget P, Emerson SU, Purcell RH (1997) African strains of hepatitis E virus that are distinct from Asian strains. J Med Virol 53:139–144

    Article  CAS  PubMed  Google Scholar 

  17. Beji-Hamza A, Khelifi-Gharbi H, Hassine-Zaafrane M, Della Libera S, Iaconelli M, Muscillo M, Petricca S, Ciccaglione AR, Bruni R, Taffon S, Equestre M, Aouni M, La Rosa G (2014) Qualitative and quantitative assessment of hepatitis A virus in wastewaters in Tunisia. Food Environ Virol. doi:10.1007/s12560-014-9163-3

  18. La Rosa G, Pourshaban M, Iaconelli M, Spuri Vennarucci V, Muscillo M (2010) Molecular detection of hepatitis E virus in sewage samples. Appl Environ Microbiol 76:5870–5873

    Article  PubMed Central  PubMed  Google Scholar 

  19. Kokkinos PA, Ziros PG, Mpalasopoulou A, Galanis A, Vantarakis A (2011) Molecular detection of multiple viral targets in untreated urban sewage from Greece. Virol J 8:195

    Article  PubMed Central  PubMed  Google Scholar 

  20. Vivek R, Zachariah UG, Ramachandran J, Eapen CE, Rajan DP, Kang G (2013) Characterization of hepatitis E virus from sporadic hepatitis cases and sewage samples from Vellore, south India. Trans R Soc Trop Med Hyg 107:363–367

    Article  CAS  PubMed  Google Scholar 

  21. Ippagunta SK, Naik S, Sharma B, Aggarwal R (2007) Presence of hepatitis E virus in sewage in Northern India: frequency and seasonal pattern. J Med Virol 79:1827–1831

    Article  CAS  PubMed  Google Scholar 

  22. Ahmad T, Waheed Y, Tahir S, Safi SZ, Fatima K, Afzal MS, Farooqi ZU, Qadri I (2010) Frequency of HEV contamination in sewerage waters in Pakistan. J Infect Dev Ctries 4:842–845

    PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor Herbert W. Virgin, Washington University (St. Louis, Missouri, United States) for providing the murine NoV stain used as sample process control.

The research leading to these results has received funding from the Italian National Centre for the Prevention and Control of Diseases (CCM), project – Hepatitis E Surveillance in Italy: an emerging disease in industrialized countries, and from the European Union’s Seventh Framework Programme for Research, Technological Development and Demonstration under Grant Agreement no. 278433-PREDEMICS.

Author information

Authors and Affiliations

  1. Laboratory of Transmissible Diseases and Biological Active Substances, Faculty of Pharmacy, University of Monastir, Monastir, Tunisia

    A. Béji-Hamza, M. Hassine-Zaafrane, H. Khélifi-Gharbi & M. Aouni

  2. Department of Environment and Primary Prevention, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161, Rome, Italy

    S. Della Libera, M. Iaconelli, M. Muscillo, S. Petricca & G. La Rosa

  3. Department of Infectious, Parasitic and Immune-Mediated Diseases, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161, Rome, Italy

    A. R. Ciccaglione, R. Bruni & S. Taffon

Authors
  1. A. Béji-Hamza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Hassine-Zaafrane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Khélifi-Gharbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Della Libera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Iaconelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Muscillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Petricca
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. R. Ciccaglione
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. R. Bruni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. S. Taffon
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M. Aouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. G. La Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. La Rosa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Béji-Hamza, A., Hassine-Zaafrane, M., Khélifi-Gharbi, H. et al. Hepatitis E virus genotypes 1 and 3 in wastewater samples in Tunisia. Arch Virol 160, 183–189 (2015). https://doi.org/10.1007/s00705-014-2251-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-014-2251-8

Keywords

Search

Navigation