Food and Environmental Virology

, Volume 9, Issue 3, pp 304–313 | Cite as

Relative Abundance of Human Bocaviruses in Urban Sewage in Greater Cairo, Egypt

  • Hazem Hamza
  • Mats Leifels
  • Michael Wilhelm
  • Ibrahim Ahmed Hamza
Original Paper


Human bocavirus (HBoV) is predominantly found in the respiratory tract infections and in the stool of patients with gastroenteritis symptoms. However, data on the prevalence of HBoV genotypes in environmental samples are limited. Here we addressed the prevalence of HBoV in sewage collected from three different wastewater treatment plants in Egypt. HBoV-1, HBoV-2, and HBoV-3 were detected, whereas none of the samples were positive for HBoV-4. The median concentration of HBoV in influent samples was 8.5 × 103 GC/l for HBoV-1, 3.0 × 104 GC/l for HBoV-2, and 2.5 × 104 GC/l for HBoV-3. The concentration was reduced but not completely removed in the effluent samples. The median concentration in the outlet samples was 2.9 × 103 GC/l for HBoV-1, 4.1 × 103 GC/l for HBoV-2, and 2.1 × 103 GC/l for HBoV-3. Moreover, no seasonality pattern of HBoVs was found. The high incidence of HBoV in sewage samples provided an evidence of its circulation in the local population. Although the role of HBoV in respiratory or gastro-intestinal infections still remains to be fully elucidated, the risk of infection via contaminated water should be taken into consideration.


Human bocavirus Wastewater qPCR Contamination 



This work was conducted within a short-term fellowship funded by the Egyptian Ministry of Higher Education and Scientific Research.


  1. Abdel-Moneim, A. S., El-Fol, H. A., Kamel, M. M., Soliman, A. S. A., Mahdi, E. A., El-Gammal, A. S., et al. (2016a). Screening of human bocavirus in surgically excised cancer specimens. Archives of Virology, 161(8), 2095–2102.CrossRefPubMedGoogle Scholar
  2. Abdel-Moneim, A. S., Kamel, M. M., Hamed, D. H., Hassan, S. S., Soliman, M. S., Al-Quraishy, S. A., et al. (2016b). A novel primer set for improved direct gene sequencing of human bocavirus genotype-1 from clinical samples. Journal of Virological Methods, 228, 108–113.CrossRefPubMedGoogle Scholar
  3. Ali, M. A., Al-Herrawy, A. Z., & El-Hawaary, S. E. (2004). Detection of enteric viruses, Giardia and Cryptosporidium in two different types of drinking water treatment facilities. Water Research, 38(18), 3931–3939.CrossRefPubMedGoogle Scholar
  4. Allander, T., Tammi, M. T., Eriksson, M., Bjerkner, A., Tiveljung-Lindell, A., & Andersson, B. (2005). Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proceedings of the National Academy of Sciences USA, 102(36), 12891–12896.CrossRefGoogle Scholar
  5. Arthur, J. L., Higgins, G. D., Davidson, G. P., Givney, R. C., & Ratcliff, R. M. (2009). A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathogens, 5(4), e1000391.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blinkova, O., Rosario, K., Li, L., Kapoor, A., Slikas, B., Bernardin, F., et al. (2009). Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States. Journal of Clinical Microbiology, 47(11), 3507–3513.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Broccolo, F., Falcone, V., Esposito, S., & Toniolo, A. (2015). Human bocaviruses: possible etiologic role in respiratory infection. Journal of Clinical Virology, 72, 75–81.CrossRefPubMedGoogle Scholar
  8. Cashman, O., & O’Shea, H. (2012). Detection of human bocaviruses 1, 2 and 3 in Irish children presenting with gastroenteritis. Archives of Virology, 157(9), 1767–1773.CrossRefPubMedGoogle Scholar
  9. Choi, E. H., Lee, H. J., Kim, S. J., Eun, B. W., Kim, N. H., Lee, J. A., et al. (2006). The association of newly identified respiratory viruses with lower respiratory tract infections in Korean children, 2000-2005. Clinical Infectious Diseases, 43(5), 585–592.CrossRefPubMedGoogle Scholar
  10. Chow, B. D., Huang, Y. T., & Esper, F. P. (2008). Evidence of human bocavirus circulating in children and adults, Cleveland, Ohio. Journal of Clinical Virology, 43(3), 302–306.CrossRefPubMedGoogle Scholar
  11. Dijkman, R., Koekkoek, S. M., Molenkamp, R., Schildgen, O., & van der Hoek, L. (2009). Human Bocavirus Can Be Cultured in Differentiated Human Airway Epithelial Cells. Journal of Virology, 83(15), 7739–7748.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fong, T. T., & Lipp, E. K. (2005). Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiology and Molecular Biology Reviews, 69(2), 357–371.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hamza, I. A., Jurzik, L., Uberla, K., & Wilhelm, M. (2011). Methods to detect infectious human enteric viruses in environmental water samples. International Journal of Hygiene and Environmental Health, 214(6), 424–436.CrossRefPubMedGoogle Scholar
  14. Hamza, I. A., Jurzik, L., Wilhelm, M., & Uberla, K. (2009). Detection and quantification of human bocavirus in river water. Journal of General Virology, 90(11), 2634–2637.CrossRefPubMedGoogle Scholar
  15. Huang, Q., Deng, X., Yan, Z., Cheng, F., Luo, Y., Shen, W., et al. (2012). Establishment of a Reverse Genetics System for Studying Human Bocavirus in Human Airway Epithelia. PLoS Pathogens, 8(8), e1002899.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Iaconelli, M., Divizia, M., Della Libera, S., Di Bonito, P., & La Rosa, G. (2016). Frequent detection and genetic diversity of human bocavirus in urban sewage samples. Food and Environmental Virology, 8, 289–295.CrossRefPubMedGoogle Scholar
  17. Jartti, T., Hedman, K., Jartti, L., Ruuskanen, O., Allander, T., & Soderlund-Venermo, M. (2012). Human bocavirus-the first 5 years. Reviews in Medical Virology, 22(1), 46–64.CrossRefPubMedGoogle Scholar
  18. Kamel, A. H., Ali, M. A., El-Nady, H. G., Aho, S., Pothier, P., & Belliot, G. (2010). Evidence of the co-circulation of enteric viruses in sewage and in the population of Greater Cairo. Journal of Applied Microbiology, 108(5), 1620–1629.CrossRefPubMedGoogle Scholar
  19. Kantola, K., Sadeghi, M., Antikainen, J., Kirveskari, J., Delwart, E., Hedman, K., et al. (2010). Real-time quantitative PCR detection of four human bocaviruses. Journal of Clinical Microbiology, 48(11), 4044–4050.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kapoor, A., Hornig, M., Asokan, A., Williams, B., Henriquez, J. A., & Lipkin, W. I. (2011). Bocavirus episome in infected human tissue contains non-identical termini. PLoS ONE, 6(6), e21362.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kapoor, A., Simmonds, P., Slikas, E., Li, L., Bodhidatta, L., Sethabutr, O., et al. (2010). Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. Journal of Infectious Diseases, 201(11), 1633–1643.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kapoor, A., Slikas, E., Simmonds, P., Chieochansin, T., Naeem, A., Shaukat, S., et al. (2009). A newly identified bocavirus species in human stool. Journal of Infectious Diseases, 199(2), 196–200.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Koseki, N., Teramoto, S., Kaiho, M., Gomi-Endo, R., Yoshioka, M., Takahashi, Y., et al. (2012). Detection of human bocaviruses 1 to 4 from nasopharyngeal swab samples collected from patients with respiratory tract infections. Journal of Clinical Microbiology, 50(6), 2118–2121.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Myrmel, M., Lange, H., & Rimstad, E. (2015). A 1-year quantitative survey of noro-, adeno-, human boca-, and Hepatitis E Viruses in raw and secondarily treated sewage from two plants in Norway. Food and Environmental Virology, 7(3), 213–223.CrossRefPubMedGoogle Scholar
  25. Nawaz, S., Allen, D. J., Aladin, F., Gallimore, C., & Iturriza-Gomara, M. (2012). Human bocaviruses are not significantly associated with gastroenteritis: results of retesting archive DNA from a case control study in the UK. PLoS ONE, 7(7), e41346.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Neske, F., Blessing, K., Tollmann, F., Schubert, J., Rethwilm, A., Kreth, H. W., et al. (2007). Real-time PCR for diagnosis of human bocavirus infections and phylogenetic analysis. Journal of Clinical Microbiology, 45(7), 2116–2122.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ong, D. S., Schuurman, R., & Heikens, E. (2016). Human bocavirus in stool: a true pathogen or an innocent bystander? Journal of Clinical Virology, 74, 45–49.CrossRefPubMedGoogle Scholar
  28. Pintó, R. M., Alegre, D., Dominguez, A., El-Senousy, W. M., Sanchez, G., Villena, C., et al. (2007). Hepatitis A virus in urban sewage from two Mediterranean countries. Epidemiology and Infection, 135(2), 270–273.CrossRefPubMedGoogle Scholar
  29. Proenca-Modena, J. L., Martinez, M., Amarilla, A. A., EspÍNola, E. E., Galeano, M. E., FariÑA, N., et al. (2013). Viral load of human bocavirus-1 in stools from children with viral diarrhoea in Paraguay. Epidemiology and Infection, 141(12), 2576–2580.CrossRefPubMedGoogle Scholar
  30. Rasanen, S., Lappalainen, S., Kaikkonen, S., Hamalainen, M., Salminen, M., & Vesikari, T. (2010). Mixed viral infections causing acute gastroenteritis in children in a waterborne outbreak. Epidemiology and Infection, 138(9), 1227–1234.CrossRefPubMedGoogle Scholar
  31. Santos, N., Peret, T. C., Humphrey, C. D., Albuquerque, M. C., Silva, R. C., Benati, F. J., et al. (2010). Human bocavirus species 2 and 3 in Brazil. Journal of Clinical Virology, 48(2), 127–130.CrossRefPubMedGoogle Scholar
  32. Schildgen, O. (2013). Human bocavirus: lessons learned to date. Pathogens, 2(1), 1–12.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Smits, S. L., Osterhaus, A. D., & Koopmans, M. P. (2016). Newly identified viruses in human gastroenteritis: pathogens or not? Pediatric Infectious Disease Journal, 35(1), 104–107.PubMedGoogle Scholar
  34. Song, J. R., Jin, Y., Xie, Z. P., Gao, H. C., Xiao, N. G., Chen, W. X., et al. (2010). Novel human bocavirus in children with acute respiratory tract infection. Emerging Infectious Diseases, 16(2), 324–327.CrossRefPubMedPubMedCentralGoogle Scholar
  35. USEPA (2001). Manual of methods for virology. EPA/600/4-84/013. USEPA, Cincinnati, USA: 6–62.Google Scholar
  36. Vicente, D., Cilla, G., Montes, M., Perez-Yarza, E. G., & Perez-Trallero, E. (2007). Human bocavirus, a respiratory and enteric virus. Emerging Infectious Diseases, 13(4), 636–637.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Villena, C., El-Senousy, W. M., Abad, F. X., Pinto, R. M., & Bosch, A. (2003). Group A rotavirus in sewage samples from Barcelona and Cairo: emergence of unusual genotypes. Applied and Environment Microbiology, 69(7), 3919–3923.CrossRefGoogle Scholar
  38. Wang, K., Wang, W., Yan, H., Ren, P., Zhang, J., Shen, J., et al. (2010). Correlation between bocavirus infection and humoral response, and co-infection with other respiratory viruses in children with acute respiratory infection. Journal of Clinical Virology, 47(2), 148–155.CrossRefPubMedGoogle Scholar
  39. Zhang, D. M., Ma, M. M., Wen, W. T., Zhu, X., Xu, L., He, Z. J., et al. (2015). Clinical epidemiology and molecular profiling of human bocavirus in faecal samples from children with diarrhoea in Guangzhou, China. Epidemiology and Infection, 143(11), 2315–2329.CrossRefPubMedGoogle Scholar
  40. Zhao, H., Zhao, L., Sun, Y., Qian, Y., Liu, L., Jia, L., et al. (2012). Detection of a bocavirus circular genome in fecal specimens from children with acute diarrhea in Beijing, China. PLoS One, 7(11), e48980.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Hazem Hamza
    • 1
    • 2
  • Mats Leifels
    • 2
  • Michael Wilhelm
    • 2
  • Ibrahim Ahmed Hamza
    • 1
  1. 1.Environmental Virology Laboratory, Department of Water Pollution ResearchNational Research CentreCairoEgypt
  2. 2.Department of Hygiene, Social- and Environmental MedicineRuhr-University BochumBochumGermany

Personalised recommendations