Alternative fecal indicators and their empirical relationships with enteric viruses, Salmonella enterica, and Pseudomonas aeruginosa in surface waters of a tropical urban catchment

Applied and Environmental Microbiology

Volumn 81, Issue 3, 2015, Pages 850-860

  Liang, L ^a   Goh, S G ^a   Vergara, G G R V ^a   Fang, H M ^a   Rezaeinejad, S ^a   Chang, S Y ^b   Bayen, S ^c,d   Lee, W A ^c   Sobsey, M D ^e   Rose, J B ^f   Gin, K Y H ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b Water Quality Office Public Utilities Board (PUB)   (Singapore)

^c Sustainable Development and Water Alliance (SDWA)   (Singapore)

^d MCGILL UNIVERSITY   (Canada)

^e University of North Carolina at Chapel Hill   (United States)

^f MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CATCHMENTS; CONTAMINATION; DISSOLVED OXYGEN; ESCHERICHIA COLI; LINEAR REGRESSION; ORGANIC CARBON; PATHOGENS; RUNOFF; SEWAGE; SURFACE WATERS; VIRUSES; WATER POLLUTION;

ALTERNATIVE FECAL INDICATORS; BACTEROIDES THETAIOTAOMICRON; EMPIRICAL RELATIONSHIPS; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL PARAMETER; GEOGRAPHICAL LOCATIONS; MULTIPLE LINEAR REGRESSIONS; SIMULTANEOUS DETECTION;

SALMONELLA;

CATCHMENT; FECES; GENETIC MARKER; GEOGRAPHICAL REGION; MICROBIAL ACTIVITY; PATHOGEN; REGROWTH; SURFACE WATER; VIRUS; WATER QUALITY;

SINGAPORE [SOUTHEAST ASIA];

ADENOVIRIDAE; ASTROVIRIDAE; BACTEROIDES THETAIOTAOMICRON; ENTEROCOCCUS; ESCHERICHIA COLI; METHANOBREVIBACTER SMITHII; NOROVIRUS; POLYOMAVIRUS; PSEUDOMONAS AERUGINOSA; ROTAVIRUS; SALMONELLA; SALMONELLA ENTERICA;

BACTERIUM; FECES; HEALTH CARE QUALITY; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; SINGAPORE; URBAN POPULATION; VIROLOGY; VIRUS; WATER POLLUTION;

BACTERIA; FECES; HUMANS; QUALITY INDICATORS, HEALTH CARE; SINGAPORE; URBAN POPULATION; VIRUSES; WATER POLLUTION;

EID: 84921395805     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02670-14     Document Type: Article

References (49)

1. Jiang S, Noble R, Chu W. 2001. Human adenoviruses and coliphages in urban runoff-impacted coastal waters of Southern California. Appl Environ Microbiol 67:179-184. http://dx.doi.org/10.1128/AEM.67.1.179-184.2001.
2. Byappanahalli MN, Whitman RL, Shively DA, Ting WTE, Tseng CC, Nevers MB. 2006. Seasonal persistence and population characteristics of Escherichia coli and enterococci in deep backshore sand of two freshwater beaches. J Water Health 4:313-320.
3. Field KG, Samadpour M. 2007. Fecal source tracking, the indicator paradigm, and managing water quality. Water Res 41:3517-3538. http://dx.doi.org/10.1016/j.watres.2007.06.056.
4. Yampara-Iquise H, Zheng G, Jones JE, Carson CA. 2008. Use of a Bacteroides thetaiotaomicron-specific alpha-1-6, mannanase quantitative PCR to detect human faecal pollution in water. J Appl Microbiol 105: 1686-1693. http://dx.doi.org/10.1111/j.1365-2672.2008.03895.x.
5. McQuaig SM, Scott TM, Lukasik JO, Paul JH, Harwood VJ. 2009. Quantification of human polyomaviruses JC virus and BK virus by Taq-Man quantitative PCR and comparison to other water quality indicators in water and fecal samples. Appl Environ Microbiol 75:3379-3388. http://dx.doi.org/10.1128/AEM.02302-08.
6. Johnston C, Ufnar JA, Griffith JF, Gooch JA, Stewart JR. 2010. A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. J Appl Microbiol 109:1946-1956. http://dx.doi.org/10.1111/j.1365-2672.2010.04824.x.
7. McQuaig S, Griffith J, Harwood VJ. 2012. Association of fecal indicator bacteria with human viruses and microbial source tracking markers at coastal beaches impacted by nonpoint source pollution. Appl Environ Microbiol 78:6423-6432. http://dx.doi.org/10.1128/AEM.00024-12.
8. Walters SP, Yamahara KM, Boehm AB. 2009. Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters. Water Res 43: 4929-4939. http://dx.doi.org/10.1016/j.watres.2009.05.047.
9. Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A. 2014. Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev 38:1-40. http://dx.doi.org/10.1111/1574-6976.12031.
10. Viau EJ, Goodwin KD, Yamahara KM, Layton BA, Sassoubre LM, Burns SL, Tong HI, Wong SH, Lu Y, Boehm AB. 2011. Bacterial pathogens in Hawaiian coastal streams-associations with fecal indicators, land cover, and water quality. Water Res 45:3279-3290. http://dx.doi.org/10.1016/j.watres.2011.03.033.
11. Frahm E, Obst U. 2003. Application of the fluorogenic probe technique (TaqMan PCR) to the detection of Enterococcus spp. and Escherichia coli in water samples. J Microbiol Methods 52:123-131. http://dx.doi.org/10.1016/S0167-7012(02)00150-1.
12. Haugland RA, Siefring SC, Wymer LJ, Brenner KP, Dufour AP. 2005. Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. Water Res 39:559-568. http://dx.doi.org/10.1016/j.watres.2004.11.011.
13. Ufnar JA, Wang SY, Christiansen JM, Yampara-Iquise H, Carson CA, Ellender RD. 2006. Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101:44-52. http://dx.doi.org/10.1111/j.1365-2672.2006.02989.x.
14. Eaton AD, Franson MA. 2005. Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC.
15. U.S. Environmental Protection Agency. 2001. Method 1601: malespecific (F+) and somatic coliphage in water by two-step enrichment procedure. U.S. Environmental Protection Agency, Washington, DC.
16. Le Cann P, Ranarijaona S, Monpoeho S, Le Guyader F, Ferre V. 2004. Quantification of human astroviruses in sewage using real-time RT-PCR. Res Microbiol 155:11-15. http://dx.doi.org/10.1016/j.resmic.2003.09.013.
17. Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41:1548-1557. http://dx.doi.org/10.1128/JCM.41.4.1548-1557.2003.
18. Jothikumar N, Cromeans TL, Hill VR, Lu X, Sobsey MD, Erdman DD. 2005. Quantitative real-time PCR assays for detection of human adenoviruses and identification of serotypes 40 and 41. Appl Environ Microbiol 71:3131-3136. http://dx.doi.org/10.1128/AEM.71.6.3131-3136.2005.
19. Aw TG, Gin KY, Ean Oon LL, Chen EX, Woo CH. 2009. Prevalence and genotypes of human noroviruses in tropical urban surface waters and clinical samples in Singapore. Appl Environ Microbiol 75:4984-4992. http://dx.doi.org/10.1128/AEM.00489-09.
20. Zeng SQ, Halkosalo A, Salminen M, Szakal ED, Puustinen L, Vesikari T. 2008. One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. J Virol Methods 153:238-240. http://dx.doi.org/10.1016/j.jviromet.2008.08.004.
21. Zar JH. 2010. Biostatistical analysis, 5th ed. Pearson Education, Inc., Upper Saddle River, NJ.
22. Sinclair RG, Jones EL, Gerba CP. 2009. Viruses in recreational waterborne disease outbreaks: a review. J Appl Microbiol 107:1769-1780. http://dx.doi.org/10.1111/j.1365-2672.2009.04367.x.
23. Santiago-Rodriguez TM, Tremblay RL, Toledo-Hernandez C, Gonzalez-Nieves JE, Ryu H, Santo Domingo JW, Toranzos GA. 2012. Microbial quality of tropical inland waters and effects of rainfall events. Appl Environ Microbiol 78:5160-5169. http://dx.doi.org/10.1128/AEM.07773-11.
24. Calci KR, Burkhardt W III, Watkins WD, Rippey SR. 1998. Occurrence of male-specific bacteriophage in feral and domestic animal wastes, human feces, and human-associated wastewaters. Appl Environ Microbiol 64:5027-5029.
25. Ibarluzea JM, Santa Marina L, Moreno B, Serrano E, Larburu K, Maiztegi MJ, Yarzabal A. 2007. Somatic coliphages and bacterial indicators of bathing water quality in the beaches of Gipuzkoa, Spain. J Water Health 5:417-426. http://dx.doi.org/10.2166/wh.2007.037.
26. Ahmed W, Sidhu JP, Toze S. 2012. Evaluation of the nifH gene marker of Methanobrevibacter smithii for the detection of sewage pollution in environmental waters in Southeast Queensland, Australia. Environ Sci Technol 46:543-550. http://dx.doi.org/10.1021/es203372u.
27. Payment P, Locas A. 2011. Pathogens in water: value and limits of correlation with microbial indicators. Ground Water 49:4-11. http://dx.doi.org/10.1111/j.1745-6584.2010.00710.x.
28. Gin KYH, Ramaswamy U, Gopalakrishnan AP. 2011. Comparison of nutrient limitation in freshwater and estuarine reservoirs in tropical urban Singapore. J Environ Eng 137:913-919. http://dx.doi.org/10.1061/(ASCE)EE.1943-7870.0000397.
29. Wilkes G, Edge T, Gannon V, Jokinen C, Lyautey E, Medeiros D, Neumann N, Ruecker N, Topp E, Lapen DR. 2009. Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Res 43:2209-2223. http://dx.doi.org/10.1016/j.watres.2009.01.033.
30. Korajkic A, Brownell MJ, Harwood VJ. 2011. Investigation of human sewage pollution and pathogen analysis at Florida Gulf coast beaches. J Appl Microbiol 110:174-183. http://dx.doi.org/10.1111/j.1365-2672.2010.04869.x.
31. Yan T, Goto DK, Feng F. 2011. Concentration dynamics of fecal indicators in Hawaii's coastal and inland sand, soil, and water during rainfall events. Water Environment Research Foundation, Alexandria, VA.
32. Wu J, Long SC, Das D, Dorner SM. 2011. Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research J Water Health 9:265-278.
33. Ogorzaly L, Tissier A, Bertrand I, Maul A, Gantzer C. 2009. Relationship between F-specific RNA phage genogroups, faecal pollution indicators and human adenoviruses in river water. Water Res 43:1257-1264. http://dx.doi.org/10.1016/j.watres.2008.12.011.
34. Horman A, Rimhanen-Finne R, Maunula L, von Bonsdorff CH, Torvela N, Heikinheimo A, Hanninen ML. 2004. Campylobacter spp., Giardia spp., Cryptosporidium spp., noroviruses, and indicator organisms in surface water in Southwestern Finland, 2000-2001. Appl Environ Microbiol 70:87-95. http://dx.doi.org/10.1128/AEM.70.1.87-95.2004.
35. Schriewer A, Miller WA, Byrne BA, Miller MA, Oates S, Conrad PA, Hardin D, Yang HH, Chouicha N, Melli A, Jessup D, Dominik C, Wuertz S. 2010. Presence of Bacteroidales as a predictor of pathogens in surface waters of the central California coast. Appl Environ Microbiol 76:5802-5814. http://dx.doi.org/10.1128/AEM.00635-10.
36. McEgan R, Mootian G, Goodridge LD, Schaffner DW, Danyluk MD. 2013. Predicting Salmonella populations from biological, chemical, and physical indicators in Florida surface waters. Appl Environ Microbiol 79: 4094-4105. http://dx.doi.org/10.1128/AEM.00777-13.
37. Noble RT, Blackwood AD, Griffith JF, McGee CD, Weisberg SB. 2010. Comparison of rapid quantitative PCR-based and conventional culturebased methods for enumeration of Enterococcus spp. and Escherichia coli in recreational waters. Appl Environ Microbiol 76:7437-7443. http://dx.doi.org/10.1128/AEM.00651-10.
38. Wade TJ, Calderon RL, Brenner KP, Sams E, Beach M, Haugland R, Wymer L, Dufour AP. 2008. High sensitivity of children to swimmingassociated gastrointestinal illness: results using a rapid assay of recreational water quality. Epidemiology 19:375-383. http://dx.doi.org/10.1097/EDE.0b013e318169cc87.
39. Chalker RB, Blaser MJ. 1988. A review of human salmonellosis. III. Magnitude of Salmonella infection in the United States. Rev Infect Dis 10:111-124.
40. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309-317. http://dx.doi.org/10.1086/421946.
41. Janssen A. 2012. Prevention of norovirus infection in schools and child-care facilities. European Centre for Disease Prevention and Control, Stockholm, Sweden.
42. Edwards K, Thompson J, Paolini J, Wright P. 1985. Adenovirus infections in young children. J Am Acad Pediatr 76:420-424.
43. Anderson KL, Whitlock JE, Harwood VJ. 2005. Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71:3041-3048. http://dx.doi.org/10.1128/AEM.71.6.3041-3048.2005.
44. Fish JT, Pettibone GW. 1995. Influence of freshwater sediment on the survival of Escherichia coli and Salmonella sp. as measured by three methods of enumeration. Lett Appl Microbiol 20:277-281. http://dx.doi.org/10.1111/j.1472-765X.1995.tb00445.x.
45. Skraber S, Gassilloud B, Gantzer C. 2004. Comparison of coliforms and coliphages as tools for assessment of viral contamination in river water. Appl Environ Microbiol 70:3644-3649. http://dx.doi.org/10.1128/AEM.70.6.3644-3649.2004.
46. Ferguson AS, Layton AC, Mailloux BJ, Culligan PJ, Williams DE, Smartt AE, Sayler GS, Feighery J, McKay LD, Knappett PS, Alexandrova E, Arbit T, Emch M, Escamilla V, Ahmed KM, Alam MJ, Streatfield PK, Yunus M, van Geen A. 2012. Comparison of fecal indicators with pathogenic bacteria and rotavirus in groundwater. Sci Total Environ 431:314-322. http://dx.doi.org/10.1016/j.scitotenv.2012.05.060.
47. Lytle CD, Sagripanti J-L. 2005. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol 79:14244-14252. http://dx.doi.org/10.1128/JVI.79.22.14244-14252.2005.
48. Espinosa AC, Mazari-Hiriart M, Espinosa R, Maruri-Avidal L, Méndez E, Arias CF. 2008. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res 42:2618-2628. http://dx.doi.org/10.1016/j.watres.2008.01.018.
49. Savichtcheva O, Okayama N, Okabe S. 2007. Relationships between Bacteroides 16S rRNA genetic markers and presence of bacterial enteric pathogens and conventional fecal indicators. Water Res 41:3615-3628. http://dx.doi.org/10.1016/j.watres.2007.03.028.