Skip to main content
Top
Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Total coliforms as an indicator of human enterovirus presence in surface water across Tianjin city, China

Authors: Jing Miao, Xuan Guo, Weili Liu, Dong Yang, Zhiqiang Shen, Zhigang Qiu, Xiang Chen, Kunming Zhang, Hui Hu, Jing Yin, Zhongwei Yang, Junwen Li, Min Jin

Published in: BMC Infectious Diseases | Issue 1/2018

Login to get access

Abstract

Background

Enteric viruses in surface water pose considerable risk to morbidity in populations living around water catchments and promote outbreaks of waterborne diseases. However, due to poor understanding of the correlation between water quality and the presence of human enteric viruses, the failure to assess viral contamination through alternative viral indicators makes it difficult to control disease transmission.

Methods

We investigated the occurrence of Enteroviruses (EnVs), Rotaviruses (HRVs), Astroviruses (AstVs), Noroviruses GII (HuNoVs GII) and Adenoviruses (HAdVs) from Jinhe River over 4 years and analyzed their correlation with physicochemical and bacterial parameters in water samples.

Results

The findings showed that all target viruses were detected in water at frequencies of 91.7% for HAdVs, 81.3% for HuNoVs GII, 79.2% for EnVs and AstVs, and 70.8% for HRVs. These viruses had a seasonal pattern, which showed that EnVs were abundant in summer but rare in winter, while HAdVs, HRVs, AstVs, and HuNoVs GII exhibited opposite seasonal trends. Pearson correlation analysis showed that total coliforms (TC) was significantly positively correlated with EnVs concentrations while no consistent significant correlations were observed between bacterial indices and viruses that precipitate acute gastroenteritis.

Conclusions

Taken together, the findings provide insights into alternative viral indicators, suggesting that TC is a potentially promising candidate for assessment of EnVs contamination. However, it failed to predict the presence of HAdVs, HRVs, AstVs, and HuNoVs GΙΙ in surface water across the city of Tianjin.
Appendix
Available only for authorised users
Literature
1.
go back to reference Husman AMDR, Bartram J. Chapter 7 global supply of virus-safe drinking water. Persp Med Virol. 2007;17:127–62.CrossRef Husman AMDR, Bartram J. Chapter 7 global supply of virus-safe drinking water. Persp Med Virol. 2007;17:127–62.CrossRef
3.
go back to reference Gerba CP, Rose JB, Haas CN. Sensitive populations: who is at the greatest risk? Int J Food Microbiol. 1996;30(1–2):113.CrossRef Gerba CP, Rose JB, Haas CN. Sensitive populations: who is at the greatest risk? Int J Food Microbiol. 1996;30(1–2):113.CrossRef
4.
go back to reference Fong TT, Lipp EK. Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev. 2005;69(2):357–71.CrossRef Fong TT, Lipp EK. Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev. 2005;69(2):357–71.CrossRef
5.
go back to reference Clemens J. Evaluation of vaccines against enteric infections: a clinical and public health research agenda for developing countries. Philos Trans R Soc Lond Ser B Biol Sci. 2011;366(1579):2799–805.CrossRef Clemens J. Evaluation of vaccines against enteric infections: a clinical and public health research agenda for developing countries. Philos Trans R Soc Lond Ser B Biol Sci. 2011;366(1579):2799–805.CrossRef
6.
go back to reference Iaconelli M, Muscillo M, Della LS, Fratini M, Meucci L, De CM, Giacosa D, La RG. One-year surveillance of human enteric viruses in raw and treated wastewaters, Downstream River waters, and drinking waters. Food Environ Virol. 2016;9(1):1–10. Iaconelli M, Muscillo M, Della LS, Fratini M, Meucci L, De CM, Giacosa D, La RG. One-year surveillance of human enteric viruses in raw and treated wastewaters, Downstream River waters, and drinking waters. Food Environ Virol. 2016;9(1):1–10.
7.
go back to reference He X, Wei Y, Cheng L, Zhang D, Wang Z. Molecular detection of three gastroenteritis viruses in urban surface waters in Beijing and correlation with levels of fecal indicator bacteria. Environ Monit Assess. 2012;184(9):5563.CrossRef He X, Wei Y, Cheng L, Zhang D, Wang Z. Molecular detection of three gastroenteritis viruses in urban surface waters in Beijing and correlation with levels of fecal indicator bacteria. Environ Monit Assess. 2012;184(9):5563.CrossRef
8.
go back to reference Prevost B, Lucas FS, Goncalves A, Richard F, Moulin L, Wurtzer S. Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environ Int. 2015;79:42–50.CrossRef Prevost B, Lucas FS, Goncalves A, Richard F, Moulin L, Wurtzer S. Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environ Int. 2015;79:42–50.CrossRef
9.
go back to reference Kiulia NM, Netshikweta R, Page NA, Van Zyl WB, Kiraithe MM, Nyachieo A, Mwenda JM, Taylor MB. 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(3):818–28.CrossRef Kiulia NM, Netshikweta R, Page NA, Van Zyl WB, Kiraithe MM, Nyachieo A, Mwenda JM, Taylor MB. 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(3):818–28.CrossRef
10.
go back to reference Wynjones AP, Carducci A, Cook N, D'Agostino M, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C. Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res. 2011;45(3):1025–38.CrossRef Wynjones AP, Carducci A, Cook N, D'Agostino M, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C. Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res. 2011;45(3):1025–38.CrossRef
11.
go back to reference Gibson KE, Schwab KJ. 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(1):355.CrossRef Gibson KE, Schwab KJ. 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(1):355.CrossRef
12.
go back to reference Yang N, Qi H, Wong MM, Wu RS, Kong RY. Prevalence and diversity of norovirus genogroups I and II in Hong Kong marine waters and detection by real-time PCR. Mar Pollut Bull. 2012;64(1):164–8.CrossRef Yang N, Qi H, Wong MM, Wu RS, Kong RY. Prevalence and diversity of norovirus genogroups I and II in Hong Kong marine waters and detection by real-time PCR. Mar Pollut Bull. 2012;64(1):164–8.CrossRef
13.
go back to reference Montazeri N, Goettert D, Achberger EC, Johnson CN, Prinyawiwatkul W, Janes ME. Pathogenic enteric viruses and microbial indicators during secondary treatment of municipal wastewater. Appl Environ Microbiol. 2015;81(18):6436–45.CrossRef Montazeri N, Goettert D, Achberger EC, Johnson CN, Prinyawiwatkul W, Janes ME. Pathogenic enteric viruses and microbial indicators during secondary treatment of municipal wastewater. Appl Environ Microbiol. 2015;81(18):6436–45.CrossRef
14.
go back to reference Yezli S, Otter JA. Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment. Food Environ Virol. 2011;3(1):1–30. Yezli S, Otter JA. Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment. Food Environ Virol. 2011;3(1):1–30.
15.
go back to reference Jurzik L, Hamza IA, Puchert W, Überla K, Wilhelm M. Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water. Int J Hyg Envir Heal. 2010;213(3):210–6.CrossRef Jurzik L, Hamza IA, Puchert W, Überla K, Wilhelm M. Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water. Int J Hyg Envir Heal. 2010;213(3):210–6.CrossRef
16.
go back to reference Zhu H, Yuan F, Yuan Z, Liu R, Xie F, Huang L, Liu X, Jiang X, Wang J, Xu Q. Monitoring of Poyang lake water for sewage contamination using human enteric viruses as an indicator. Virol J. 2018;15(1):3.CrossRef Zhu H, Yuan F, Yuan Z, Liu R, Xie F, Huang L, Liu X, Jiang X, Wang J, Xu Q. Monitoring of Poyang lake water for sewage contamination using human enteric viruses as an indicator. Virol J. 2018;15(1):3.CrossRef
17.
go back to reference Walter WG. APHA standard methods for the examination of water and wastewater. Health Lab Sci. 1998;4(3):137. Walter WG. APHA standard methods for the examination of water and wastewater. Health Lab Sci. 1998;4(3):137.
18.
go back to reference Jin M, Guo X, Wang XW, Yang D, Shen ZQ, Qiu ZG, Chen ZL, Li JW. Development of a novel filter cartridge system with electropositive granule media to concentrate viruses from large volumes of natural surface water. Environ Sci Technol. 2014;48(12):6947.CrossRef Jin M, Guo X, Wang XW, Yang D, Shen ZQ, Qiu ZG, Chen ZL, Li JW. Development of a novel filter cartridge system with electropositive granule media to concentrate viruses from large volumes of natural surface water. Environ Sci Technol. 2014;48(12):6947.CrossRef
19.
go back to reference Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol. 2003;41(4):1548–57.CrossRef Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol. 2003;41(4):1548–57.CrossRef
20.
go back to reference Xagoraraki I, Kuo DH, Wong K, Wong M, Rose JB. Occurrence of human adenoviruses at two recreational beaches of the Great Lakes. Appl Environ Microbiol. 2007;73(24):7874.CrossRef Xagoraraki I, Kuo DH, Wong K, Wong M, Rose JB. Occurrence of human adenoviruses at two recreational beaches of the Great Lakes. Appl Environ Microbiol. 2007;73(24):7874.CrossRef
21.
go back to reference Le CP, Ranarijaona S, Monpoeho S, Le GF, Ferré V. Quantification of human astroviruses in sewage using real-time RT-PCR. Res Microbiol. 2004;155(1):11–5.CrossRef Le CP, Ranarijaona S, Monpoeho S, Le GF, Ferré V. Quantification of human astroviruses in sewage using real-time RT-PCR. Res Microbiol. 2004;155(1):11–5.CrossRef
22.
go back to reference Guo X, Wang S, Qiu ZG, Dou YL, Liu WL, Yang D, Shen ZQ, Chen ZL, Wang JF, Zhang B. Efficient replication of blood-borne hepatitis C virus in human fetal liver stem cells. Hepatology. 2017;66(4):1045–57.CrossRef Guo X, Wang S, Qiu ZG, Dou YL, Liu WL, Yang D, Shen ZQ, Chen ZL, Wang JF, Zhang B. Efficient replication of blood-borne hepatitis C virus in human fetal liver stem cells. Hepatology. 2017;66(4):1045–57.CrossRef
24.
go back to reference Wong K, Fong TT, Bibby K, Molina M. Application of enteric viruses for fecal pollution source tracking in environmental waters. Environ Int. 2012;45(1):151–64.CrossRef Wong K, Fong TT, Bibby K, Molina M. Application of enteric viruses for fecal pollution source tracking in environmental waters. Environ Int. 2012;45(1):151–64.CrossRef
25.
go back to reference Espinosa AC, Mazari-Hiriart M, Espinosa R, Maruri-Avidal L, Méndez E, Arias CF. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res. 2008;42(10–11):2618–28.CrossRef Espinosa AC, Mazari-Hiriart M, Espinosa R, Maruri-Avidal L, Méndez E, Arias CF. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res. 2008;42(10–11):2618–28.CrossRef
26.
go back to reference Ouyang Y, Ma H, Jin M, Wang X, Wang J, Xu L, Lin S, Shen Z, Chen Z, Qiu Z. Etiology and epidemiology of viral diarrhea in children under the age of five hospitalized in Tianjin, China. Arch Virol. 2012;157(5):881–7.CrossRef Ouyang Y, Ma H, Jin M, Wang X, Wang J, Xu L, Lin S, Shen Z, Chen Z, Qiu Z. Etiology and epidemiology of viral diarrhea in children under the age of five hospitalized in Tianjin, China. Arch Virol. 2012;157(5):881–7.CrossRef
27.
go back to reference Li W, Gao H, Zhang Q, Liu Y, Tao R, Cheng Y, Shu Q, Shang S. Large outbreak of herpangina in children caused by enterovirus in summer of 2015 in Hangzhou, China. Sci Rep. 2016;6:35388.CrossRef Li W, Gao H, Zhang Q, Liu Y, Tao R, Cheng Y, Shu Q, Shang S. Large outbreak of herpangina in children caused by enterovirus in summer of 2015 in Hangzhou, China. Sci Rep. 2016;6:35388.CrossRef
28.
go back to reference Am DRH, Lodder WJ, Rutjes SA, Schijven JF, Teunis PF. Long-term inactivation study of three enteroviruses in artificial surface and groundwaters, using PCR and cell culture. Appl Environ Microbiol. 2009;75(4):1050–7.CrossRef Am DRH, Lodder WJ, Rutjes SA, Schijven JF, Teunis PF. Long-term inactivation study of three enteroviruses in artificial surface and groundwaters, using PCR and cell culture. Appl Environ Microbiol. 2009;75(4):1050–7.CrossRef
29.
go back to reference Lodder WJ, HHJLvd B, Rutjes SA, Husman AMDR. Presence of enteric viruses in source waters for drinking water production in the Netherlands. Appl Environ Microbiol. 2010;76(17):5965–71.CrossRef Lodder WJ, HHJLvd B, Rutjes SA, Husman AMDR. Presence of enteric viruses in source waters for drinking water production in the Netherlands. Appl Environ Microbiol. 2010;76(17):5965–71.CrossRef
30.
go back to reference Gerba CP, Goyal SM, Labelle RL, Cech I, Bodgan GF. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health. 1979;69(11):1116–9.CrossRef Gerba CP, Goyal SM, Labelle RL, Cech I, Bodgan GF. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health. 1979;69(11):1116–9.CrossRef
31.
go back to reference Berg G. Indicators of viruses in water and food. Michigan: Ann Arbor Science; 1978. Berg G. Indicators of viruses in water and food. Michigan: Ann Arbor Science; 1978.
32.
go back to reference Winterbourn JB, Clements K, Lowther JA, Malham SK, Mcdonald JE, Jones DL. Use of Mytilus edulis biosentinels to investigate spatial patterns of norovirus and faecal indicator organism contamination around coastal sewage discharges. Water Res. 2016;105:241.CrossRef Winterbourn JB, Clements K, Lowther JA, Malham SK, Mcdonald JE, Jones DL. Use of Mytilus edulis biosentinels to investigate spatial patterns of norovirus and faecal indicator organism contamination around coastal sewage discharges. Water Res. 2016;105:241.CrossRef
33.
go back to reference Gamazo P, Victoria M, Schijven JF, Alvareda E, Tort LFL, Ramos J, Burutaran L, Olivera M, Lizasoain A, Sapriza G, et al. Evaluation of bacterial contamination as an Indicator of viral contamination in a sedimentary aquifer in Uruguay. Food Environ Virol. 2018;10(2):1867–0342.CrossRef Gamazo P, Victoria M, Schijven JF, Alvareda E, Tort LFL, Ramos J, Burutaran L, Olivera M, Lizasoain A, Sapriza G, et al. Evaluation of bacterial contamination as an Indicator of viral contamination in a sedimentary aquifer in Uruguay. Food Environ Virol. 2018;10(2):1867–0342.CrossRef
Metadata
Title
Total coliforms as an indicator of human enterovirus presence in surface water across Tianjin city, China
Authors
Jing Miao
Xuan Guo
Weili Liu
Dong Yang
Zhiqiang Shen
Zhigang Qiu
Xiang Chen
Kunming Zhang
Hui Hu
Jing Yin
Zhongwei Yang
Junwen Li
Min Jin
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3438-5

Other articles of this Issue 1/2018

BMC Infectious Diseases 1/2018 Go to the issue