Quantitative RT-PCR detection of hepatitis A virus, rotaviruses and enteroviruses in the Buffalo River and source water dams in the Eastern Cape Province of South Africa

International Journal of Environmental Research and Public Health

Volumn 9, Issue 11, 2012, Pages 4017-4032

  Chigor, Vincent Nnamdigadi ^a   Okoh, Anthony Ifeanyi ^a  

^a UNIVERSITY OF FORT HARE   (South Africa)

Author keywords

Detection; Enteric RNA viruses; Enteroviruses; Hepatitis a virus; Quantification; Real time RT PCR; Rotaviruses; Surface waters

Indexed keywords

RIVER WATER; VIRUS RNA;

CONCENTRATION (COMPOSITION); DETECTION METHOD; DISEASE PREVALENCE; EPIDEMIOLOGY; HEALTH RISK; HEALTH STATUS; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RNA; SURFACE WATER; VIRUS; WATERBORNE DISEASE;

ADSORPTION; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELUTION; ENTERIC VIRUS; ENTEROVIRUS; HEALTH HAZARD; HEPATITIS A VIRUS; NONHUMAN; PREVALENCE; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIVER; RNA EXTRACTION; ROTAVIRUS; SOUTH AFRICA; VIRUS DETECTION; WATER SAMPLING; WATER SUPPLY;

ARKANSAS; BUFFALO RIVER; EASTERN CAPE; SOUTH AFRICA; UNITED STATES;

EID: 84870826526     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph9114017     Document Type: Article

References (77)

1. World Health Organization (WHO). World Health Statistics 2009; WHO Press: Geneva, Switzerland, 2009; pp. 1-149.
2. Gibson, K.E.; Schwab, K.J. Detection of bacterial indicators and human and bovine enteric viruses in surface water and groundwater sources potentially impacted by animal and human wastes in Lower Yakima Valley, Washington. Appl. Environ. Microbiol. 2011, 77, 355-362.
3. Pruss, A.; Kay, D.; Fewtrell, L.; Bartram, J. Estimating the burden of disease from water sanitation and hygiene at a global level. Environ. Health Perspect. 2002, 110, 537-542.
4. Boschi-Pinto, C.; Velebit, L.; Shibuya, K. Estimating child mortality due to diarrhoea in developing countries. Bull. World Health Organ. 2008, 86, 710-717.
5. World Health Organization (WHO) and UNICEF. Progress on Sanitation and Drinking-Water: 2010 Update; WHO Press: Geneva, Switzerland, 2010; pp. 1-60.
6. Muller, M.; Schreiner, B.; Smith, L.; van Koppen, B.; Sally, H.; Aliber, M.; Cousins, B.; Tapela, B.; van der Merwe-Botha, M.; Karar, E.; Pietersen, K. Water Security in South Africa; Development Planning Division DBSA: Midrand, South Africa, 2009.
7. Shuval, H.I. Wastewater Irrigation in Developing Countries: Health Effects and Technical Solutions; The World Bank: Washinton, DC, USA, 1990; pp.1-19.
8. Okoh, A.I.; Sibanda, T.; Gusha, S.S. Inadequately treated wastewater as a source of human enteric viruses in the environment. Int. J. Environ. Res. Pub. Health 2010, 7, 2620-2637.
9. Chigor, V.N.; Umoh, V.J.; Okuofu, C.A.; Ameh, J.B.; Igbinosa, E.O.; Okoh, A.I. Water quality assessment: Surface water sources used for drinking and irrigation in Zaria, Nigeria are a public health hazard. Environ. Monit. Assess. 2012, 184, 3389-3400.
10. Miagostovich, M.P.; Ferreira, F.F.M.; Guimaraes, F.R.; Fumian, T.M.; Diniz-Mendes, L.; Luz, S.L.B.; Silva, L.A.; Leite, J.P.G. Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, central Amazonia, Brazil. Appl. Environ. Microbiol. 2008, 74, 375-382.
11. Bosch, A.; Guix, S.; Sano, D.; Pinto, R.M. New tools for the study and direct surveillance of viral pathogens in water. Curr. Op. Biotechnol. 2008, 19, 1-7.
12. Fong, T.T.; Lipp, E.K. Enteric viruses of human and animals in aquatic environments: Heath risks, detection and potential water quality assessment tools. Appl. Environ. Microbiol. 2005, 69, 357-371.
13. Haramoto, E.; Katayama, H.; Utagawa, E.; Ohgaki, S. Development of sample storage methods for detecting enteric viruses in environmental water. J. Virol. Methods 2008, 151, 1-6.
14. Bosch, A. Human enteric viruses in the water environment: A minireview. Int. Microbiol. 1998, 1, 191-196.
15. Fauquet, C.M.; Mayo, M.A.; Maniloff, J.; Desselberger, U.; Ball, L.A. Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses; Elsevier Academic Press: San Diego, CA, USA, 2005; pp. 853-857.
16. Ward, R.L.; Bernstein, D.I.; Young, E.C.; Sherwood, J.R.; Knowlton, D.R.; Schiff, G.M. Human rotavirus studies in volunteers: Determination of infectious dose and serological response to infection. J. Infect. Dis. 1986, 154, 871-880.
17. Pusch, D.; Oh, D.Y.; Wolf, S.; Dumke, R.; Schroter-Bobsin, U.; Hohne, M.; Roske, I.; Schreier, E. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch. Virol. 2005, 150, 929-947.
18. Liu, J.; Kibiki, G.; Maro, V.; Maro, A.; Kumburu, H.; Swai, N.; Taniuchi, M.; Gratz, J.; Toney, D.; Kang, G.; Houpt, E. Multiplex reverse transcription PCR Luminex assay for detection and quantitation of viral agents of gastroenteritis. J. Clin. Virol. 2011, 50, 308-313.
19. Kittigul, L.; Uthaisin, A.; Ekchaloemkiet, S.; Utrarachkij, F.; Luksamijarulkul, P. Detection and characterization of hepatitis A virus in water samples in Thailand. J. Appl. Microbiol. 2006, 100, 1318-1323.
20. Colbere-Garapin, F.; Martin-Latil, S.; Blondel, B.; Mousson, L.; Pelletier, I.; Autret, A.; Francois, A.; Niborski, V.; Grompone, G.; Catonnet, G.; van de Moer, A. Prevention and treatment of enteric viral infections: Possible benefits of probiotic bacteria. Microb. Infect. 2007, 9, 1623-1631.
21. Roque-Afonso, A.M.; Desbois, D.; Dussaix, E. Hepatitis A virus: Serology and molecular diagnostics. Future Virol. 2010, 5, 233-242.
22. Taylor, M.B.; Cox, N.; Very, M.A.; Grabow, W.O.K. The occurrence of hepatitis A and astroviruses in selected river and dam waters in South Africa. Water Res. 2001, 35, 2653-2660.
23. Venter, J.M.E.; van Heerden, J.; Vivier, J.C.; Grabow, W.O.K.; Taylor, M.B. Hepatitis A virus in surface water in South Africa: What are the risks? J. Water Health 2007, 5, 229-240.
24. MacIntyre, U.E.; de Villiers, F.P.R. The Economic burden of diarrheal disease in a tertiary level hospital, Gauteng, South Africa. J. Infect. Dis. 2010, 202, S116-S125.
25. Mwenda, J.M.; Ntoto, K.M.; Abebe, A.; Enweronu-Laryea, C.; Amina, I.; Mchomvu, J.; Kisakye, A.; Mpabalwani, E.M.; Pazvakavambwa, I.; Armah, G.E.; Seheri, L.M.; Kiulia, N.M.; Page, N.; Widdowson, M.A.; Steele, A.D. Burden and epidemiology of rotavirus diarrhea in selected African countries: preliminary results from the African Rotavirus Surveillance Network. J. Infect. Dis. 2010, 202, S5-S11.
26. Patel, M.M.; Steele, D.; Gentsch, J.R.; Wecker, J.; Glass, R.I.; Parashar, U.D. Real-world impact of rotavirus vaccination. Pediat. Infect. Dis. J. 2011, 30, S1-S5.
27. Ramachandran, M.; Gentsch, J.R.; Parashar, U.D.; Jin, S.; Woods, P.A.; Holmes, J.L.; Kirkwood, C.D.; Bishop, R.F.; Greenberg, H.B.; Urasawa, S.; Gerna, G.; Coulson, B.S.; Taniguchi, K.; Bresee, J.S.; Glass, R.I. Detection and characterization of novel rotavirus strains in the United States. J. Clin. Microbiol. 1998, 36, 3223-3229.
28. Adah, M.; Wade, A.; Taniguchi, K. Molecular epidemiology of rotaviruses in Nigeria: Detection of unusual strains with G2P [6] and G8P [1] specificities. J. Clin. Microbiol. 2001, 39, 3969-3975.
29. Pinto, R.M.; Saiz, J.C. Enteric Hepatitis Viruses. In Human Viruses in Water; Bosch, A., Ed.; Elsevier: Amsterdam, The Netherlands, 2007; pp. 39-67.
30. Tallon, L.A.; Love, D.C.; Moore, Z.S.; Sobsey, M.D. Recovery and sequence analysis of hepatitis A virus from springwater implicated in an outbreak of acute viral hepatitis. Appl. Environ. Microbiol. 2008, 74, 6158-6160.
31. Taylor, M.B.; Schildhauer, C.I.; Parker, S.; Grabow, W.O.; Xi, J.; Estes, M.K. Two successive outbreaks of SRSV-associated gastroenteritis in South Africa. J. Med Virol. 1993, 41, 18-23.
32. Mans, J.; de Villiers, J.C.; du Plessis, N.M.; Avenant, T.; Taylor, M.B. Emerging norovirus GII.4 2008 variant detected in hospitalised paediatric patients in South Africa. J. Clin. Virol. 2010, 49, 258-264.
33. Rinaldi, M.; Brierley, E.; Bekker, A. Donor breastmilk saved infant lives during an outbreak of rotavirus in South Africa. Breastfeeding Medicine 2009, 4, 133-134.
34. Griffin, D.W.; Gibson, C.J.III; Lipp, E.K.; Riley, K.; Paul, J.H.III; Rose, J.B. Detection of viral pathogens by reverse transcriptase PCR and of microbial indicators by standard methods in the canals of the Florida Keys. Appl. Environ. Microbiol. 1999, 65, 4118-4125.
35. Grabow, W.O.K.; Taylor, M.B.; de Villiers, J.C. New methods for the detection of viruses: Call for review of drinking water quality guidelines. Water Sci. Technol. 2001, 43, 1-8.
36. Pina, S.; Buti, M.; Jardi, R.; Clemente-Casares, P.; Jofre, J.; Girones, R. Genetic analysis of hepatitis A virus strains recovered from the environment and from patients with acute hepatitis. J. Gen. Virol. 2001, 82, 2955-2963.
37. Castello, A.A.; Arguelles, M.H.; Rota, R.P.; Olthoff, A.; Jiang, B.; Glass, R.I.; Gentsch, J.R.; Glikmann, G. Molecular epidemiology of Group A rotavirus diarrhea among children in Buenos Aires, Argentina, from 1999 to 2003 and emergence of the infrequent genotype G12. J. Clin. Microbiol. 2006, 44, 2046-2050.
38. Gersberg, R.M.; Rose, M.A.; Robles-Sikisaka, R.; Dhar, A.K. Quantitative detection of hepatitis A virus and enteroviruses near the United States-Mexico border and correlation with levels of fecal indicator bacteria. Appl. Environ. Microbiol. 2006, 72, 7438-7444.
39. Meleg, E.; Banyai, K.; martella, V.; Jiang, B.; Kocsis, B.; Kisfali, P.; Melegh, B.; Szucs, G. Detection and quantification of group C rotaviruses in communal sewage. Appl. Environ. Microbiol. 2008,74, 3394-3399.
40. Cunliffe, N.A.; Ngwira, B.M.; Dove, W.; Nakagomi, O.; Nakagomi, T.; Perez, A.; Hart, C.A.; Kazembe, P.N.; Mwansambo, C.V. Serotype G12 rotaviruses, Lilongwe, Malawi. Emerg. Infect. Dis. 2009, 15, 87-90
41. Kiulia, N.M.; Netshikweta, R.N.A.; van Zyl, W.B.; Kiraithe, M.M.; Nyachieo, A.; Mwenda, J.M.; Taylor, M.B. The detection of enteric viruses in selected urban and rural river water and sewage in Kenya, with special reference to rotaviruses. J. Appl. Microbiol. 2010, 109, 818-828.
42. Grabow, W.O.K.; Taylor, M.B.; Wolfaardt, M. Research on Human Viruses in Diffuse Effluents and Related Water Environments; Water Research Commission: Pretoria, South Africa, 1996; pp. 1-25.
43. Vivier, J.C.; Clay, C.G.; Grabow, W.O. Detection and rapid differentiation of human enteroviruses in water sources by restriction enzyme analysis. Water Sci. Technol. 2001, 4, 209-212.
44. Pavlov, D.N. Poliovirus vaccine strains in sewage and river water in South Africa. Can. J. Microbiol. 2006, 52, 717-723.
45. Nadan, S.; Walter, J.E.; Grabow, W.O.K.; Mitchell, D.K.; Taylor, M.B. Molecular characterization of astroviruses by reverse transcriptase PCR and sequence analysis: Comparison of clinical and environmental isolates from South Africa. Appl. Environ. Microbiol. 2003, 69, 747-753.
46. Genthe, B.; Idema, G.K.; Kfir, R.; Grabow, W.O.K. Detection of rotavirus in South African waters: A comparison of a cytoimmunolabelling technique with commercially available immunoassays. Water Sci. Technol. 1991, 24, 241-244.
47. van Zyl, W.B.; Williams, P.J.; Grabow, W.O.; Taylor, M.B. Application of a molecular method for the detection of group A rotaviruses in raw and treated water. Water Sci. Technol. 2004, 50, 223-228.
48. Pourcher, A.M.; Picard-Bonnaud, F.P.B.; Agnieszka, V.F.; Vasilica, S.; Gerard, M. Survival of faecal indicators and enteroviruses in soil after land-spreading of municipal sewage sludge. Appl. Soil Ecol. 2007, 35, 473-479.
49. Muscillo, M.; Pourshaban, M.; Iaconelli, M.; Fontana, S.; Di Grazia, A.; Manzara, S.; Fadda, G.; Santangelo, R.; La Rosa, G. Detection and quantification of human adenoviruses in surface waters by nested PCR, TaqMan real-time PCR and cell culture assays. Water Air Soil Pollut. 2008, 191, 1-11.
50. Jurzik, L.; Hamza, I.A.; Puchert, W.; Überla, K.; Wilhelm, M. Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water. Int. J. Hygi. Environ. Health 2010, 213, 210-216.
51. Dahling, D. Detection and enumeration of enteric viruses in cell culture. CRC Rev. Environ. Contamin. 1991, 21, 237-263.
52. Schvoerer, E.; Bonneta, F.; Duboisa, V.; Cazauxb, G.; Serceauc, R.; Fleurya, H.J.A.; Lafona, M.E. PCR detection of human enteric viruses in bathing areas, waste waters and human stools in southwestern France. Res. Microbiol. 2000, 151, 693-701.
53. Griffin, D.W.; Donalson, K.A.; Paul, J.H.; Rose, J.B. Pathogenic human viruses in coastal waters. Clin.Microbiol. Rev. 2003, 16, 129-143.
54. de Paula, V.S.; Diniz-Mendes, L.; Villar, L.M.; Luz, S.L.B.; Silva, L.A.; Jesus, M.S.; da Silva, M.N.V.S.; Gaspar, A.S. Hepatitis A in environmental water samples from the Amazon Basin. Water Res. 2007, 41, 1169-1176.
55. Rodríguez, R.A.; Pepper, I.L.; Gerba, C.P. Application of PCR-based methods to assess the infectivity of enteric viruses in environmental samples. Appl. Environ. Microbiol. 2009, 75, 297-307.
56. Costafreda, M.I.; Bosch, A.; Pinto, R.M. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl. Environ. Microbiol. 2006, 72, 3846-3855.
57. Gregory, J.B.; Litaker, R.W.; Noble, R.T. Rapid one-step quantitative reverse transcriptase PCR Assay with competitive internal positive control for detection of enteroviruses in environmental samples. Appl. Environ. Microbiol. 2006, 72, 3960-3967.
58. Haramoto, E.; Katayama, H.; Oguma, K.; Ohgaki, S. Recovery of viral genomes in water by virus concentration methods. J. Virol. Methods 2007, 142, 169-173.
59. Jothikumar, N.; Kang, G.; Hill, V.R. Broadly reactive TaqMan assay for real-time RT-PCR detection of rotavirus in clinical and environmental samples. J. Virol. Methods 2009, 155, 126-131.
60. Zhang, M.; Zhao, H.; Yang, J.; Jiang, S.; Cai1, B. Detection and quantification of enteroviruses in coastal seawaters from Bohai Bay, Tianjin, China. J. Environ. Sci. 2010, 22, 150-154.
61. Hamza, I.A.; Jurzik, L.; Stang, A.; Sure, K.; Uberla, K.; Wilhelm, M. Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. Water Res. 2009, 43, 2657-2668.
62. Bofill-Mas, S.; Calgua, B.; Clemente-Casares, P.; La Rosa, G.; Iaconelli, M.; Muscillo, M.; Rutjes, S.; de Roda Husman, A.M.; Grunert, A.; Graber, I.; Verani, M.; Carducci, A.; Calvo, M.; Wyn-Jones, P.; Girones, R. Quantification of human adenoviruses in European recreational waters. Food Environ. Virol. 2010, 2, 101-109.
63. Donia, D.; Bonanni, E.; Diaco, L.; Divizia, M. Statistical correlation between enterovirus genome copy numbers and infectious viral particles in wastewater samples. Lett. Appl. Microbiol. 2010, 50, 237-240.
64. Parshionikar, S.; Laseke, I.; Fout, G.S. Use of propidium monoazide in reverse transcriptase PCR to distinguish between infectious and noninfectious enteric viruses in water samples. Appl. Environ. Microbiol. 2010, 76, 4318-4326.
65. River Health Programme (RHP). State-of-Rivers Report: Buffalo River System; Department of Water Affairs and Forestry: Pretoria, South Africa, 2004; pp. 1-41.
66. American Public Health Association (APHA). Standard Methods for the Examination of Water and Wastewater, 20th ed.; APHA: Washington DC, USA, 1998.
67. Haramoto, E.; Katayama, H.; Oguma, K.; Ohgaki, S. Application of cation-coated filters method to detection of noroviruses, enteroviruses, adenoviruses and torque teno viruses in the Tamagawa River in Japan. Appl. Environ. Microbiol. 2005, 71, 2403-2411.
68. Department of Water Affairs (DWAF). 2012 Green Drop Progress Report; Department of Water Affairs: Pretoria, South Africa, 2012.
69. Arankalle, V.A.; Ramakrishnan, J. Simian hepatitis A virus derived from a captive rhesus monkey in India is similar to the strain isolated from wild African green monkeys in Kenya. J. Viral Hepati.2009, 16, 214-218.
70. Amado, L.A.; Marchevsky, R.S.; de Paula, V.S.; Hooper, C.; Freire, M.D.S.; Gaspar, A.M.C.; Pinto, M.A. Experimental hepatitis A virus (HAV) infection in cynomolgus monkeys Macaca fascicularis: Evidence of active extrahepatic site of HAV replication. Int. J. Exp. Pathol. 2010, 91, 87-97.
71. Global Alert Response (GAR): Hepatitis A, 2012. World Health Organization (WHO). Available online: http://www.who.int/csr/disease/hepatitis/whocdscsredc2007/en/index3.html (accessed on 9 October 2012).
72. Lodder, W.J.; van den Berg, H.H.J.L.; Rutjes, S.A.; de Roda Husman, A.M. Presence of enteric viruses in source waters for drinking water production in the Netherlands. Appl. Environ Microbiol. 2010, 76, 5965-5971.
73. Steele, A.D.; Glass, R. Rotavirus in South Africa: From discovery to vaccine introduction. South Afri. J. Epidemiol.Infect. 2011, 26, 184-190.
74. Ehlers, M.M.; Grabow, W.O.K.; Pavlov, D.N. Detection of enteroviruses in untreated and treated drinking water supplies in South Africa. Water Res. 2005, 39, 2253-2258.
75. Harvala, H.; McIntyre, C.L.; Imai, N.; Clasper, L.; Djoko, C.F.; Lebreton, M.; Vermeulen, M.; Saville, A.; Mutapi, F.; Tamoufe, U. et al. High seroprevalence of enterovirus infections in apes and old world monkeys. Emerg. Infect. Dis. 2012, 18, 283-286.
76. Chen, C.H.; Hsu, B.M.; Wan, M.T. Detection of enteroviruses within brackish water from the Damshui River watershed, Taiwan. J. Environ. Engineer. 2008, 134, 486. doi: 10.1061/(ASCE) 0733-9372(2008)134:6(486).
77. Skraber, S.; Gassilloud, B.; Schwartzbrod, L.; Gantzer, C. Survival of infectious Poliovirus-1 in river water compared to the persistence of somatic coliphages, thermotolerant coliforms, and poliovirus-1 genome. Water Res. 2004, 38, 2927-2933.