Microbial source tracking markers for detection of fecal contamination in environmental waters: Relationships between pathogens and human health outcomes

FEMS Microbiology Reviews

Volumn 38, Issue 1, 2014, Pages 1-40

  Harwood, Valerie J ^a   Staley, Christopher ^a,b   Badgley, Brian D ^c   Borges, Kim ^d   Korajkic, Asja ^e  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MAINE   (United States)

^e U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Epidemiology; Fecalindicatorbacteria; MST; QPCR; Recreationalwater; Waterquality

Indexed keywords

BIOCHEMICAL MARKER; MITOCHONDRIAL DNA; RNA 16S;

BACTERIAL GENE; BACTEROIDALES; BIFIDOBACTERIUM; BIRD; COLIPHAGE; COMPARATIVE STUDY; COW; DISEASE ASSOCIATION; DOG; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; EVALUATION STUDY; FECES ANALYSIS; FECES MICROFLORA; FIELD STUDY; GENE TARGETING; GENOTYPE; HEALTH HAZARD; HOST PATHOGEN INTERACTION; HUMAN; INFECTION RISK; INVESTIGATIVE PROCEDURES; LABORATORY TEST; LACHNOSPIRACEAE; METHANOBREVIBACTER SMITHII; MICROBIAL SOURCE TRACKING; NONHUMAN; OUTCOME ASSESSMENT; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REVIEW; RISK ASSESSMENT; SURVIVAL; SWINE; VIRUS VIRULENCE; WASTE WATER MANAGEMENT; WATER CONTAMINATION;

ANIMALIA; BACTERIA (MICROORGANISMS);

EPIDEMIOLOGY; FECAL INDICATOR BACTERIA; MST; QPCR; RECREATIONAL WATER; WATER QUALITY;

ANIMALS; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; FECES; HEALTH; HUMANS; WATER MICROBIOLOGY;

EID: 84891630221     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/1574-6976.12031     Document Type: Review

References (195)

1. Abdelzaher AM, Wright ME, Ortega C et al. (2010) Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl Environ Microbiol 76: 724-732.
2. Ahmed W, Stewart J, Gardner T & Powell D (2008) A real-time polymerase chain reaction assay for quantitative detection of the human-specific enterococci surface protein marker in sewage and environmental waters. Environ Microbiol 10: 3255-3264.
3. Ahmed W, Goonetilleke A, Powell D & Gardner T (2009a) Evaluation of multiple sewage-associated Bacteroides PCR markers for sewage pollution tracking. Water Res 43: 4872-4877.
4. Ahmed W, Goonetilleke A, Powell D, Chauhan K & Gardner T (2009b) Comparison of molecular markers to detect fresh sewage in environmental waters. Water Res 43: 4908-4917.
5. Ahmed W, Yusuf R, Hasan I, Goonetilleke A & Gardner T (2010) Quantitative PCR assay of sewage-associated Bacteroides markers to assess sewage pollution in an urban lake in Dhaka, Bangladesh. Can J Microbiol 56: 838-845.
6. 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.
7. Albinana-Gimenez N, Clemente-Casares P, Calgua B, Huguet JM, Courtois S & Girones R (2009) Comparison of methods for concentrating human adenoviruses, polyomavirus JC and noroviruses in source waters and drinking water using quantitative PCR. J Virol Methods 158: 104-109.
8. Anderson KL, Whitlock JE, Harwood VJ & K, (2005) Persistence and differential survival of indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71: 3041-3048.
9. Arnone RD & Walling JP (2007) Waterborne pathogens in urban watersheds. J Water Health 5: 149-162.
10. Badgley BD, Thomas FI & Harwood VJ (2011) Quantifying environmental reservoirs of fecal indicator bacteria associated with sediment and submerged aquatic vegetation. Environ Microbiol 13: 932-942.
11. Bae S & Wuertz S (2009) Rapid decay of host-specific fecal Bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide. Water Res 43: 4850-4859.
12. Bae S & Wuertz S (2012) Survival of host-associated Bacteroidales cells and their relationship with Enterococcus spp., Campylobacter jejuni, Salmonella enterica serovar Typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR. Appl Environ Microbiol 78: 922-932.
13. Balleste E, Bonjoch X, Belanche LA & Blanch AR (2010) Molecular indicators used in the development of predictive models for microbial source tracking. Appl Environ Microbiol 76: 1789-1795.
14. Beekwilder J, Nieuwenhuizen R, Havelaar AH & van Duin J (1996) An oligonucleotide hybridization assay for the identification and enumeration of F-specific RNA phages in surface water. J Appl Bacteriol 80: 179-186.
15. Bernhard AE & Field KG (2000a) Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Appl Environ Microbiol 66: 1587-1594.
16. Bernhard AE & Field KG (2000b) A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA. Appl Environ Microbiol 66: 4571-4574.
17. Bernhard AE, Goyard T, Simonich MT & Field KG (2003) Application of a rapid method for identifying fecal pollution sources in a multi-use estuary. Water Res 37: 909-913.
18. Betancourt WQ & Fujioka RS (2006) Bacteroides spp. as reliable marker of sewage contamination in Hawaii's environmental waters using molecular techniques. Water Sci Technol 54: 101-107.
19. Boehm AB & Soller JA (2012) Recreational water risk: pathogens and fecal indicators. Encyclopedia of Sustainability, Science and Technology, (Meyers RA Ed), Chapter 16, pp. 441-459. Springer, New York, NY.
20. Boehm AB, Fuhrman JA, Mrse RD & Grant SB (2003) Tiered approach for identification of a human fecal pollution source at a recreational beach: Case study at Avalon Cay, Catalina Island, California. Environ Sci Technol 37: 673-680.
21. Boehm AB, Yamahara KM, Love DC, Peterson BM, McNeill K & Nelson KL (2009) Covariation and photoinactivation of traditional and novel indicator organisms and human viruses at a sewage-impacted marine beach. Environ Sci Technol 43: 8046-8052.
22. Boehm AB, Van De Werfhorst L, Griffith JF et al. (2013) Performance of forty-one microbial source tracking methods: a twenty-seven lab evaluation study. Water Res 47, in press.
23. Bofill-Mas S, Pina S & Girones R (2000) Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl Environ Microbiol 66: 238-245.
24. Bonadonna L, Briancesco R, Ottaviani M & Veschetti E (2002) Occurrence of Cryptosporidium oocysts in sewage effluents and correlation with microbial, chemical and physical water variables. Environ Monit Assess 75: 241-252.
25. Bonjoch X, Balleste E & Blanch AR (2004) Multiplex PCR with 16S rRNA gene-targeted primers of Bifidobacterium spp. to identify sources of fecal pollution. Appl Environ Microbiol 70: 3171-3175.
26. Bosch A (1998) Human enteric viruses in the water environment: a minireview. Int Microbiol 1: 191-196.
27. Bosch A, Lucena F, Diez JM, Gajardo R, Blasi M & Jofre J (1991) Waterborne viruses associated with hepatitis outbreak. J Am Water Works Assoc 83: 80-83.
28. Bower PA, Scopel CO, Jensen ET, Depas MM & McLellan SL (2005) Detection of genetic markers of fecal indicator bacteria in Lake Michigan and determination of their relationship to Escherichia coli densities using standard microbiological methods. Appl Environ Microbiol 71: 8305-8313.
29. Brownell MJ, Harwood VJ, Kurz RC, McQuaig SM, Lukasik J & Scott TM (2007) Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations. Water Res 41: 3747-3757.
30. Byappanahalli MN & Fujioka RS (1998) Evidence that tropical soil environment can support the growth of Escherichia coli. Water Sci Technol 38: 171-174.
31. Byappanahalli MN, Shively DA, Nevers MB, Sadowsky MJ & Whitman RL (2003) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46: 203-211.
32. Cabelli VJ, Dufour AP, McCabe LJ & Levin MA (1982) Swimming-associated gastroenteritis and water quality. Am J Epidemiol 115: 606-616.
33. Caldwell JM & Levine JF (2009) Domestic wastewater influent profiling using mitochondrial real-time PCR for source tracking animal contamination. J Microbiol Methods 77: 17-22.
34. Caldwell JM, Raley ME & Levine JF (2007) Mitochondrial multiplex real-time PCR as a source tracking method in fecal-contaminated effluents. Environ Sci Technol 41: 3277-3283.
35. Carson CA, Shear BL, Ellersieck MR & Asfaw A (2001) Identification of fecal Escherichia coli from humans and animals by ribotyping. Appl Environ Microbiol 67: 1503-1507.
36. Carson CA, Christiansen JM, Yampara-Iquise H et al. (2005) Specificity of a Bacteroides thetaiotaomicron marker for human feces. Appl Environ Microbiol 71: 4945-4949.
37. Cheung WH, Chang KC, Hung RP & Kleevens JW (1990) Health effects of beach water pollution in Hong Kong. Epidemiol Infect 105: 139-162.
38. Clermont O, Lescat M, O'Brien CL, Gordon DM, Tenaillon O & Denamur E (2008) Evidence for a human-specific Escherichia coli clone. Environ Microbiol 10: 1000-1006.
39. Colford JM, Wade TJ, Schiff KC, Wright C, Griffith JF, Sukhminder KS & Weisberg SB (2005) Recreational Water Contact and Illness in Mission Bay, California. pp. 430. Southern California Coastal Water Research Project, Westminster, CA.
40. Colford JM, Wade TJ, Schiff KC et al. (2007) Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology 18: 27-35.
41. Converse RR, Blackwood AD, Kirs M, Griffith JF & Noble RT (2009) Rapid QPCR-based assay for fecal Bacteroides spp. as a tool for assessing fecal contamination in recreational waters. Water Res 43: 4828-4837.
42. Deprez RHL, Fijnvandraat AC, Ruijter JM & Moorman AFM (2002) Sensitivity and accuracy of quantitative real-time polymerase chain reaction using SYBR green I depends on cDNA synthesis conditions. Anal Biochem 307: 63-69.
43. Dick LK & Field KG (2004) Rapid estimation of numbers of fecal Bacteroidetes by use of a quantitative PCR assay for 16S rRNA genes. Appl Environ Microbiol 70: 5695-5697.
44. Dick LK, Bernhard AE, Brodeur TJ, Santo Domingo JW, Simpson JM, Walters SP & Field KG (2005) Host distributions of uncultivated fecal Bacteroidales bacteria reveal genetic markers for fecal source identification. Appl Environ Microbiol 71: 3184-3191.
45. Dick LK, Stelzer EA, Bertke EE, Fong DL & Stoeckel DM (2010) Relative decay of Bacteroidales microbial source tracking markers and cultivated Escherichia coli in freshwater microcosms. Appl Environ Microbiol 76: 3255-3262.
46. Dombek PE, Johnson LK, Zimmerley ST & Sadowsky MJ (2000) Use of repetitive DNA sequences and the PCR to differentiate Escherichia coli isolates from human and animal sources. Appl Environ Microbiol 66: 2572-2577.
47. Dorai-Raj S, O'Grady J & Colleran E (2009) Specificity and sensitivity evaluation of novel and existing Bacteroidales and Bifidobacteria-specific PCR assays on feces and sewage samples and their application for microbial source tracking in Ireland. Water Res 43: 4980-4988.
48. Dridi B, Henry M, El Khechine A, Raoult D & Drancourt M (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS ONE 4: e7063.
49. Dwight RH, Baker DB, Semenza JC & Olson BH (2004) Health effects associated with recreational coastal water use: urban versus rural California. Am J Public Health 94: 565-567.
50. Edge TA, Hill S, Seto P & Marsalek J (2010) Library-dependent and library-independent microbial source tracking to identify spatial variation in faecal contamination sources along a Lake Ontario beach (Ontario, Canada). Water Sci Technol 62: 719-727.
51. Ferguson CM, Coote BG, Ashbolt NJ & Stevenson IM (1996) Relationships between indicators, pathogens and water quality in an estuarine system. Water Res 30: 2045-2054.
52. Field KG & Samadpour M (2007) Fecal source tracking, the indicator paradigm, and managing water quality. Water Res 41: 3517-3538.
53. Field KG, Chern EC, Dick LK et al. (2003) A comparative study of culture-independent, library-independent genotypic methods of fecal source tracking. J Water Health 1: 181-194.
54. Fleisher JM, Fleming LE, Solo-Gabriele HM et al. (2010) The BEACHES Study: health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters. Int J Epidemiol 39: 1291-1298.
55. Flood C, Ufnar J, Wang S, Johnson J, Carr M & Ellender R (2011) Lack of correlation between enterococcal counts and the presence of human specific fecal markers in Mississippi creek and coastal waters. Water Res 45: 872-878.
56. Fremaux B, Gritzfeld J, Boa T & Yost CK (2009) Evaluation of host-specific Bacteroidales 16S rRNA gene markers as a complementary tool for detecting fecal pollution in a prairie watershed. Water Res 43: 4838-4849.
57. Fremaux B, Boa T & Yost CK (2010) Quantitative real-time PCR assays for sensitive detection of Canada goose-specific fecal pollution in water sources. Appl Environ Microbiol 76: 4886-4889.
58. Gourmelon M, Caprais MP, Segura R, Le Mennec C, Lozach S, Piriou JY & Rince A (2007) Evaluation of two library-independent microbial source tracking methods to identify sources of fecal contamination in French estuaries. Appl Environ Microbiol 73: 4857-4866.
59. Gourmelon M, Caprais MP, Le Mennec C, Mieszkin S, Ponthoreau C & Gendronneau M (2010a) Application of library-independent microbial source tracking methods for identifying the sources of faecal contamination in coastal areas. Water Sci Technol 61: 1401-1409.
60. Gourmelon M, Caprais MP, Mieszkin S et al. (2010b) Development of microbial and chemical MST tools to identify the origin of the faecal pollution in bathing and shellfish harvesting waters in France. Water Res 44: 4812-4824.
61. Graves AK (2011) Food safety and implications for microbial source tracking. Microbial Source Tracking: Methods, Applications, and Case Studies (Hagedorn C, Blanch AR & Harwood VJ, eds), pp. 585-607. Springer, New York, NY.
62. Green HC, Dick LK, Gilpin B, Samadpour M & Field KG (2011a) Genetic markers for rapid PCR-based identification of gull, Canada goose, duck, and chicken fecal contamination in water. Appl Environ Microbiol 78: 503-510.
63. Green HC, Shanks OC, Sivaganesan M, Haugland RA & Field KG (2011b) Differential decay of human fecal Bacteroides in marine and freshwater. Environ Microbiol 13: 3235-3249.
64. Griffith JF, Weisberg SB & McGee CD (2003) Evaluation of microbial source tracking methods using mixed fecal sources in aqueous test samples. J Water Health 1: 141-151.
65. Griffith JF, Cao YP, McGee CD & Weisberg SB (2009) Evaluation of rapid methods and novel indicators for assessing microbiological beach water quality. Water Res 43: 4900-4907.
66. Hagedorn C, Robinson SL, Filtz JR, Grubbs SM, Angier TA & Reneau RB Jr (1999) Determining sources of fecal pollution in a rural Virginia watershed with antibiotic resistance patterns in fecal streptococci. Appl Environ Microbiol 65: 5522-5531.
67. Hammerum AM & Jensen LB (2002) Prevalence of esp, encoding the enterococcal surface protein, in Enterococcus faecalis and Enterococcus faecium isolates from hospital patients, poultry, and pigs in Denmark. J Clin Microbiol 40: 4396.
68. Hamza IA, Jurzik L, Uberla K & Wilhelm M (2011) Evaluation of pepper mild mottle virus, human picobirnavirus and Torque teno virus as indicators of fecal contamination in river water. Water Res 45: 1358-1368.
69. Harada T, Mito Y, Otsuki K & Murase T (2004) Resistance to gentamicin and vancomycin in enterococcal strains isolated from retail broiler chickens in Japan. J Food Prot 67: 2292-2295.
70. Harwood VJ & Stoeckel DM (2011) Performance criteria. Microbial Source Tracking: Methods, Applications, and Case Studies, (Hagedorn C, Blanch AR & Harwood VJ, eds), pp. 7-30. Springer, New York, NY.
71. Harwood VJ, Butler J, Parrish D & Wagner V (1999) Isolation of fecal coliform bacteria from the diamondback terrapin (Malaclemys terrapin centrata). Appl Environ Microbiol 65: 865-867.
72. Harwood VJ, Whitlock J & Withington V (2000) Classification of antibiotic resistance patterns of indicator bacteria by discriminant analysis: use in predicting the source of fecal contamination in subtropical waters. Appl Environ Microbiol 66: 3698-3704.
73. Harwood VJ, Wiggins B, Hagedorn C et al. (2003) Phenotypic library-based microbial source tracking methods: efficacy in the California collaborative study. J Water Health 1: 153-166.
74. Harwood VJ, Levine AD, Scott TM, Chivukula V, Lukasik J, Farrah SR & Rose JB (2005) Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl Environ Microbiol 71: 3163-3170.
75. Harwood VJ, Brownell M, Wang S et al. (2009) Validation and field testing of library-independent microbial source tracking methods in the Gulf of Mexico. Water Res 43: 4812-4819.
76. Harwood VJ, Gordon KV & Staley C (2011) Validation of Rapid Methods for Enumeration of Markers for Human Sewage Contamination in Recreational Water. Water Environment Research Foundation, Alexandria, VA. PATH3C09.
77. Harwood VJ, Boehm AB, Sassoubre LM et al. (2013) Performance of viruses and bacteriophages for fecal source determination in a Multi-laboratory, comparative Study. Water Res, 47, in press.
78. 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.
79. Haugland RA, Varma M, Sivaganesan M, Kelty C, Peed L & Shanks OC (2010) Evaluation of genetic markers from the 16S rRNA gene V2 region for use in quantitative detection of selected Bacteroidales species and human fecal waste by qPCR. Syst Appl Microbiol 33: 348-357.
80. Havelaar AH, Pot-Hogeboom WM, Furuse K, Pot R & Hormann MP (1990) F-specific RNA bacteriophages and sensitive host strains in faeces and wastewater of human and animal origin. J Appl Bacteriol 69: 30-37.
81. Heid CA, Stevens J, Livak KJ & Williams PM (1996) Real time quantitative PCR. Genome Res 6: 986-994.
82. Hopkins RS, Gaspard GB, Williams FP, Karlin RJ, Cukor G & Blacklow NR (1984) A community waterborne gastroenteritis outbreak - evidence for rotavirus as the agent. Am J Public Health 74: 263-265.
83. Hsu FC, Shieh YS, van Duin J, Beekwilder MJ & Sobsey MD (1995) Genotyping male-specific RNA coliphages by hybridization with oligonucleotide probes. Appl Environ Microbiol 61: 3960-3966.
84. Hundesa A, de Motes CM, Albinana-Gimenez N, Rodriguez-Manzano J, Bofill-Mas S, Sunen E & Girones RR (2009) Development of a qPCR assay for the quantification of porcine adenoviruses as an MST tool for swine fecal contamination in the environment. J Virol Methods 158: 130-135.
85. Ishii S, Ksoll WB, Hicks RE & Sadowsky MJ (2006) Presence and growth of naturalized Escherichia coli in temperate soils from lake superior watersheds. Appl Environ Microbiol 72: 612-621.
86. Jeng HWC, England AJ & Bradford HB (2005) Indicator organisms associated with stormwater suspended particles and estuarine sediment. J Environ Sci Health A Tox Hazard Subst Environ Eng 40: 779-791.
87. Jenkins MW, Tiwari S, Lorente M, Gichaba CM & Wuertz S (2009) Identifying human and livestock sources of fecal contamination in Kenya with host-specific Bacteroidales assays. Water Res 43: 4956-4966.
88. 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.
89. Jokinen CC, Schreier H, Mauro W et al. (2010) The occurrence and sources of Campylobacter spp., Salmonella enterica and Escherichia coli O157:H7 in the Salmon River, British Columbia, Canada. J Water Health 8: 374-386.
90. Kildare BJ, Leutenegger CM, McSwain BS, Bambic DG, Rajal VB & Wuertz S (2007) 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: a Bayesian approach. Water Res 41: 3701-3715.
91. King EL, Bachoon DS & Gates KW (2007) Rapid detection of human fecal contamination in estuarine environments by PCR targeting of Bifidobacterium adolescentis. J Microbiol Methods 68: 76-81.
92. Kinzelman JL & McLellan SL (2009) Success of science-based best management practices in reducing swimming bans - a case study from Racine, Wisconsin, USA. Aquat Ecosyst Health Manage 12: 187-196.
93. Kirs M & Smith DC (2007) Multiplex quantitative real-time reverse transcriptase PCR for F+-specific RNA coliphages: a method for use in microbial source tracking. Appl Environ Microbiol 73: 808-814.
94. 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.
95. Kreader CA (1998) Persistence of PCR-detectable Bacteroides distasonis from human feces in river water. Appl Environ Microbiol 64: 4103-4105.
96. Ksoll WB, Ishii S, Sadowsky MJ & Hicks RE (2007) Presence and sources of fecal coliform bacteria in epilithic periphyton communities of lake superior. Appl Environ Microbiol 73: 3771-3778.
97. Lamendella R, Santo Domingo JW, Kelty C & Oerther DB (2008) Bifidobacteria in feces and environmental waters. Appl Environ Microbiol 74: 575-584.
98. Layton A, McKay L, Williams D, Garrett V, Gentry R & Sayler G (2006) Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl Environ Microbiol 72: 4214-4224.
99. Layton BA, Walters SP & Boehm AB (2009) Distribution and diversity of the enterococcal surface protein (esp) gene in animal hosts and the Pacific coast environment. J Appl Microbiol 106: 1521-1531.
100. Leclerc H, Mossel DAA, Edberg SC & Struijk CB (2001) Advances in the bacteriology of the Coliform Group: their suitability as markers of microbial water safety. Annu Rev Microbiol 55: 201-234.
101. Lee CS & Lee J (2010) Evaluation of new gyrB-based real-time PCR system for the detection of B. fragilis as an indicator of human-specific fecal contamination. J Microbiol Methods 82: 311-318.
102. Lee DY, Weir SC, Lee H & Trevors JT (2010) Quantitative identification of fecal water pollution sources by TaqMan real-time PCR assays using Bacteroidales 16S rRNA genetic markers. Appl Microbiol Biotechnol 88: 1373-1383.
103. Lemarchand K & Lebaron P (2003) Occurrence of Salmonella spp. and Cryptosporidium spp. in a French coastal watershed: relationship with fecal indicators. FEMS Microbiol Lett 218: 203-209.
104. Leskinen SD, Brownell M, Lim DV & Harwood VJ (2010) Hollow-fiber ultrafiltration and PCR detection of human-associated genetic markers from various types of surface water in Florida. Appl Environ Microbiol 76: 4116-4117.
105. Litton RM, Ahn JH, Sercu B, Holden PA, Sedlak DL & Grant SB (2010) Evaluation of chemical, molecular, and traditional markers of fecal contamination in an effluent dominated urban stream. Environ Sci Technol 44: 7369-7375.
106. Lodder WJ, Vinje J, van de Heide R, Husman AMD, Leenen EJTM & Koopmans MPG (1999) Molecular detection of Norwalk-like caliciviruses in sewage. Appl Environ Microbiol 65: 5624-5627.
107. Lu JR, Santo Domingo JW, Lamendella R, Edge T & Hill S (2008) Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl Environ Microbiol 74: 3969-3976.
108. Lu J, Ryu H, Hill S, Schoen M, Ashbolt N, Edge TA & Domingo JS (2011) Distribution and potential significance of a gull fecal marker in urban coastal and riverine areas of southern Ontario, Canada. Water Res 45: 3960-3968.
109. Lund V (1996) Evaluation of E. coli as an indicator for the presence of Campylobacter jejuni and Yersinia enterocolitica in chlorinated and untreated oligotrophic lake water. Water Res 30: 1528-1534.
110. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM & Konstantinidis KT (2011) Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. P Natl Acad Sci USA 108: 7200-7205.
111. Martellini A, Payment P & Villemur R (2005) Use of eukaryotic mitochondrial DNA to differentiate human, bovine, porcine and ovine sources in fecally contaminated surface water. Water Res 39: 541-548.
112. Marti R, Zhang Y, Lapen DR & Topp E (2011) Development and validation of a microbial source tracking marker for the detection of fecal pollution by muskrats. J Microbiol Methods 87: 82-88.
113. Matsuki T, Watanabe K, Tanaka R & Oyaizu H (1998) Rapid identification of human intestinal bifidobacteria by 16S rRNA-targeted species- and group-specific primers. FEMS Microbiol Lett 167: 113-121.
114. McBride GB, Loftis JC & Adkins NC (1993) What do significance tests really tell us about the environment. Environ Manage 17: 423-432.
115. McLain JE, Ryu H, Kabiri-Badr L, Rock CM & Abbaszadegan M (2009) Lack of specificity for PCR assays targeting human Bacteroides 16S rRNA gene: cross-amplification with fish feces. FEMS Microbiol Lett 299: 38-43.
116. McQuaig SM (2009) The development of a human polyomavirus quantitative PCR assay to assess viral persistence, water quality, and human health risks Thesis. University of South Florida, Tampa, FL, USA.
117. McQuaig SM, Scott TM, Harwood VJ, Farrah SR & Lukasik JO (2006) Detection of human-derived fecal pollution in environmental waters by use of a PCR-based human polyomavirus assay. Appl Environ Microbiol 72: 7567-7574.
118. McQuaig SM, Scott TM, Lukasik JO, Paul JH & Harwood VJ (2009) Quantification of human polyomaviruses JC Virus and BK Virus by TaqMan quantitative PCR and comparison to other water quality indicators in water and fecal samples. Appl Environ Microbiol 75: 3379-3388.
119. McQuaig S, Griffith J & Harwood VJ (2012) The 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.
120. Mieszkin S, Furet JP, Corthier G & Gourmelon M (2009) Estimation of pig fecal contamination in a river catchment by real-time PCR using two pig-specific Bacteroidales 16S rRNA genetic markers. Appl Environ Microbiol 75: 3045-3054.
121. Moore DF, Harwood VJ, Ferguson DM, Lukasik J, Hannah P, Getrich M & Brownell M (2005) Evaluation of antibiotic resistance analysis and ribotyping for identification of faecal pollution sources in an urban watershed. J Appl Microbiol 99: 618-628.
122. Myoda SP, Carson CA, Fuhrmann JJ et al. (2003) Comparison of genotypic-based microbial source tracking methods requiring a host origin database. J Water Health 1: 167-180.
123. Newton RJ, Vandewalle J, Borchardt MA, Gorelick MH & McLellan SL (2011) Lachnospiraceae and Bacteroidales alternative fecal indicators reveal chronic human sewage contamination in an urban harbor. Appl Environ Microbiol 77: 6972-6981.
124. Noble RT, Allen SM, Blackwood AD et al. (2003) Use of viral pathogens and indicators to differentiate between human and non-human fecal contamination in a microbial source tracking comparison study. J Water Health 1: 195-207.
125. Noble RT, Griffith JF, Blackwood AD et al. (2006) Multitiered approach using quantitative PCR to track sources of fecal pollution affecting Santa Monica Bay, California. Appl Environ Microbiol 72: 1604-1612.
126. Okabe S, Okayama N, Savichtcheva O & Ito T (2007) Quantification of host-specific Bacteroides-Prevotella 16S rRNA genetic markers for assessment of fecal pollution in freshwater. Appl Microbiol Biotechnol 74: 890-901.
127. Parker JK, McIntyre D & Noble RT (2010) Characterizing fecal contamination in stormwater runoff in coastal North Carolina, USA. Water Res 44: 4186-4194.
128. Parveen S, Murphree RL, Edmiston L, Kaspar CW, Portier KM & Tamplin ML (1997) Association of multiple-antibiotic-resistance profiles with point and nonpoint sources of Escherichia coli in Apalachicola Bay. Appl Environ Microbiol 63: 2607-2612.
129. Parveen S, Portier KM, Robinson K, Edmiston L & Tamplin ML (1999) Discriminant analysis of ribotype profiles of Escherichia coli for differentiating human and nonhuman sources of fecal pollution. Appl Environ Microbiol 65: 3142-3147.
130. Pina S, Puig M, Lucena F, Jofre J & Girones R (1998) Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl Environ Microbiol 64: 3376-3382.
131. Prieto MD, Lopez B, Juanes JA, Revilla JA, Llorca J & Delgado-Rodriguez M (2001) Recreation in coastal waters: health risks associated with bathing in sea water. J Epidemiol Community Health 55: 442-447.
132. Reischer GH, Kasper DC, Steinborn R, Mach RL & Farnleitner AH (2006) Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in alpine karstic regions. Appl Environ Microbiol 72: 5610-5614.
133. Reischer GH, Kasper DC, Steinborn R, Farnleitner AH & Mach RL (2007) A quantitative real-time PCR assay for the highly sensitive and specific detection of human faecal influence in spring water from a large alpine catchment area. Lett Appl Microbiol 44: 351-356.
134. Reynolds KA, Mena KD & Gerba CP (2008) Risk of waterborne illness via drinking water in the United States. Rev Environ Contam Toxicol 192: 117-158.
135. Rosario K, Symonds EM, Sinigalliano C, Stewart J & Breitbart M (2009) Pepper mild mottle virus as an indicator of fecal pollution. Appl Environ Microbiol 75: 7261-7267.
136. Ryu H, Lu JR, Vogel J, Elk M, Chavez-Ramirez F, Ashbolt N & Domingo JS (2012a) Development and evaluation of a quantitative PCR assay targeting sandhill crane (Grus canadensis) fecal pollution. Appl Environ Microbiol 78: 4338-4345.
137. Ryu H, Griffith JF, Khan IU et al. (2012b) Comparison of gull feces-specific assays targeting the 16S rRNA genes of Catellicoccus marimammalium and Streptococcus spp. Appl Environ Microbiol 78: 1909-1916.
138. Santo Domingo JW & Sadowsky MJ (2007) Microbial Source Tracking. ASM Press, Washington, D.C.
139. Sauer EP, VandeWalle JL, Bootsma MJ & McLellan SL (2011) Detection of the human specific Bacteroides genetic marker provides evidence of widespread sewage contamination of stormwater in the urban environment. Water Res 45: 4081-4091.
140. 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.
141. Schill WB & Mathes MV (2008) Real-time PCR detection and quantification of nine potential sources of fecal contamination by analysis of mitochondrial cytochrome b targets. Environ Sci Technol 42: 5229-5234.
142. Schriewer A, Miller WA, Byrne BA et al. (2010) Presence of Bacteroidales as a predictor of pathogens in surface waters of the central California coast. Appl Environ Microbiol 76: 5802-5814.
143. Scott TM, Jenkins TM, Lukasik J & Rose JB (2005) Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ Sci Technol 39: 283-287.
144. Seurinck S, Defoirdt T, Verstraete W & Siciliano SD (2005) Detection and quantification of the human-specific HF183 Bacteroides 16S rRNA genetic marker with real-time PCR for assessment of human faecal pollution in freshwater. Environ Microbiol 7: 249-259.
145. Shanks OC, Santo Domingo JW, Lamendella R, Kelty CA & Graham JE (2006) Competitive metagenomic DNA hybridization identifies host-specific microbial genetic markers in cow fecal samples. Appl Environ Microbiol 72: 4054-4060.
146. Shanks OC, Domingo JW, Lu J, Kelty CA & Graham JE (2007) Identification of bacterial DNA markers for the detection of human fecal pollution in water. Appl Environ Microbiol 73: 2416-2422.
147. Shanks OC, Atikovic E, Blackwood AD et al. (2008) Quantitative PCR for detection and enumeration of genetic markers of bovine fecal pollution. Appl Environ Microbiol 74: 745-752.
148. Shanks OC, Kelty CA, Sivaganesan M, Varma M & Haugland RA (2009) Quantitative PCR for genetic markers of human fecal pollution. Appl Environ Microbiol 75: 5507-5513.
149. Shanks OC, White K, Kelty CA et al. (2010a) Performance of PCR-based assays targeting Bacteroidales genetic markers of human fecal pollution in sewage and fecal samples. Environ Sci Technol 44: 6281-6288.
150. Shanks OC, White K, Kelty CA et al. (2010b) Performance assessment PCR-based assays targeting Bacteroidales genetic markers of bovine fecal pollution. Appl Environ Microbiol 76: 1359-1366.
151. Shanks OC, Sivaganesan M, Peed L et al. (2012) Interlaboratory comparison of real-time PCR protocols for quantification of general fecal indicator bacteria. Environ Sci Technol 46: 945-953.
152. Shibata T, Solo-Gabriele HM, Sinigalliano CD et al. (2010) Evaluation of conventional and alternative monitoring methods for a recreational marine beach with nonpoint source of fecal contamination. Environ Sci Technol 44: 8175-8181.
153. Siefring S, Varma M, Atikovic E, Wymer L & Haugland RA (2008) Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. J Water Health 6: 225-237.
154. Silkie SS & Nelson KL (2009) Concentrations of host-specific and generic fecal markers measured by quantitative PCR in raw sewage and fresh animal feces. Water Res 43: 4860-4871.
155. Simpson JM, Santo Domingo JW & Reasoner DJ (2002) Microbial source tracking: state of the science. Environ Sci Technol 36: 5279-5288.
156. Sinigalliano CD, Fleisher JM, Gidley ML et al. (2010) Traditional and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters. Water Res 44: 3763-3772.
157. Sokolova E, Astrom J, Pettersson TJ, Bergstedt O & Hermansson M (2012) Decay of Bacteroidales genetic markers in relation to traditional fecal indicators for water quality modeling of drinking water sources. Environ Sci Technol 46: 892-900.
158. Solecki O, Jeanneau L, Jarde E, Gourmelon M, Marin C & Pourcher AM (2011) Persistence of microbial and chemical pig manure markers as compared to faecal indicator bacteria survival in freshwater and seawater microcosms. Water Res 45: 4623-4633.
159. Soller JA, Bartrand T, Ashbolt NJ, Ravenscroft J & Wade TJ (2010a) Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination. Water Res 44: 4736-4747.
160. Soller JA, Schoen ME, Bartrand T, Ravenscroft JE & Ashbolt NJ (2010b) Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44: 4674-4691.
161. Solo-Gabriele HM, Wolfert MA, Desmarais TR & Palmer CJ (2000) Sources of Escherichia coli in a coastal subtropical environment. Appl Environ Microbiol 66: 230-237.
162. Souza V, Rocha M, Valera A & Eguiarte LE (1999) Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl Environ Microbiol 65: 3373-3385.
163. Srinivasan S, Aslan A, Xagoraraki I, Alocilja E & Rose JB (2011) Escherichia coli, enterococci, and Bacteroides thetaiotaomicron qPCR signals through wastewater and septage treatment. Water Res 45: 2561-2572.
164. Stapleton CM, Kay D, Wyer MD et al. (2009) Evaluating the operational utility of a Bacteroidales quantitative PCR-based MST approach in determining the source of faecal indicator organisms at a UK bathing water. Water Res 43: 4888-4899.
165. Stewart JR, Boehm AB, Dubinsky EA et al. (2012) Recommendations following a multi-laboratory comparison of microbial source tracking methods. Water Res, 47, in press.
166. Stewart-Pullaro J, Daugomah JW, Chestnut DE, Graves DA, Sobsey MD & Scott GI (2006) F+ RNA coliphage typing for microbial source tracking in surface waters. J Appl Microbiol 101: 1015-1026.
167. Stoeckel DM & Harwood VJ (2007) Performance, design, and analysis in microbial source tracking studies. Appl Environ Microbiol 73: 2405-2415.
168. Taguchi F, Kajioka J & Miyamura T (1982) Prevalence rate and age of acquisition of antibodies against JC virus and BK virus in human sera. Microbiol Immunol 26: 1057-1064.
169. Tallon P, Magajna B, Lofranco C & Leung KT (2005) Microbial indicators of faecal contamination in water: a current perspective. Water Air Soil Pollut 166: 139-166.
170. Teaf CM, Garber MM & Harwood VJ(2011) Use of microbial source tracking in the legal arena: benefits and challenges. Microbial Source Tracking: Methods, Applications, and Case Studies (Hagedorn C, Blanch AR & Harwood VJ, eds), pp. 301-312. Springer, New York, NY.
171. Topp E, Welsh M, Tien YC, Dang A, Lazarovits G, Conn K & Zhu H (2003) Strain-dependent variability in growth and survival of Escherichia coli in agricultural soil. FEMS Microbiol Ecol 44: 303-308.
172. 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.
173. Varma M, Field R, Stinson M, Rukovets B, Wymer L & Haugland R (2009) Quantitative real-time PCR analysis of total and propidium monoazide-resistant fecal indicator bacteria in wastewater. Water Res 43: 4790-4801.
174. Viau EJ & Boehm AB (2011) Quantitative PCR-based detection of pathogenic Leptospira in Hawai'ian coastal streams. J Water Health 9: 637-646.
175. Viau EJ, Lee D & Boehm AB (2011) Swimmer risk of gastrointestinal illness from exposure to tropical coastal waters impacted by terrestrial dry-weather runoff. Environ Sci Technol 45: 7158-7165.
176. Wade TJ, Pai N, Eisenberg JNS & Colford JM (2003) Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environ Health Perspect 111: 1102-1109.
177. Wade TJ, Calderon RL, Sams E, Beach M, Brenner KP, Williams AH & Dufour AP (2006) Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ Health Perspect 114: 24-28.
178. Wade TJ, Calderon RL, Brenner KP et al. (2008) High sensitivity of children to swimming-associated gastrointestinal illness: results using a rapid assay of recreational water quality. Epidemiology 19: 375-383.
179. Wade TJ, Sams E, Brenner KP et al. (2010) Rapidly measured indicators of recreational water quality and swimming-associated illness at marine beaches: a prospective cohort study. Environ Health 9: 66.
180. Walker NJ (2002) A technique whose time has come. Science 296: 557-559.
181. Walters SP & Field KG (2009) Survival and persistence of human and ruminant-specific faecal Bacteroidales in freshwater microcosms. Environ Microbiol 11: 1410-1421.
182. Walters SP, Gannon VPJ & Field KG (2007) Detection of Bacteroidales fecal indicators and the zoonotic pathogens E. coli 0157:H7, Salmonella, and Campylobacter in river water. Environ Sci Technol 41: 1856-1862.
183. 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.
184. Wang RF, Cao WW, Campbell WL, Hairston L, Franklin W & Cerniglia CE (1994) The use of PCR to monitor the population abundance of 6 human intestinal bacterial species in an in-vitro semicontinuous culture system. FEMS Microbiol Lett 124: 229-237.
185. Weidhaas JL, Macbeth TW, Olsen RL, Sadowsky MJ, Norat D & Harwood VJ (2010) Identification of a Brevibacterium marker gene specific to poultry litter and development of a quantitative PCR assay. J Appl Microbiol 109: 334-347.
186. Whitman RL, Shively DA, Pawlik H, Nevers MB & Byappanahalli MN (2003) Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Appl Environ Microbiol 69: 4714-4719.
187. Whitman RL, Przybyla-Kelly K, Shively DA & Byappanahalli MN (2007) Incidence of the enterococcal surface protein (esp) gene in human and animal fecal sources. Environ Sci Technol 41: 6090-6095.
188. Wiggins BA (1996) Discriminant analysis of antibiotic resistance patterns in fecal streptococci, a method to differentiate human and animal sources of fecal pollution in natural waters. Appl Environ Microbiol 62: 3997-4002.
189. Wolf S, Hewitt J, Rivera-Aban M & Greening GE (2008) Detection and characterization of F+ RNA bacteriophages in water and shellfish: application of a multiplex real-time reverse transcription PCR. J Virol Methods 149: 123-128.
190. Wolf S, Hewitt J & Greening GE (2010) Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Appl Environ Microbiol 76: 1388-1394.
191. Wong M, Kumar L, Jenkins TM, Xagoraraki I, Phanikumar MS & Rose JB (2009) Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker. Water Res 43: 1137-1149.
192. Wyer MD, Kay D, Watkins J et al. (2010) Evaluating short-term changes in recreational water quality during a hydrograph event using a combination of microbial tracers, environmental microbiology, microbial source tracking and hydrological techniques: a case study in Southwest Wales, UK. Water Res 44: 4783-4795.
193. 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.
194. Zhang T, Breitbart M, Lee WH et al. (2006) RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol 4: 108-118.
195. Zmirou D, Pena L, Ledrans M & Letertre A (2003) Risks associated with the microbiological quality of bodies of fresh and marine water used for recreational purposes: summary estimates based on published epidemiological studies. Arch Environ Health 58: 703-711.