Rapidly measured indicators of recreational water quality and swimming-associated illness at marine beaches: A prospective cohort study

Environmental Health: A Global Access Science Source

Volumn 9, Issue 1, 2010, Pages

  Wade, Timothy J ^a   Sams, Elizabeth ^a   Brenner, Kristen P ^b   Haugland, Richard ^b   Chern, Eunice ^b   Beach, Michael ^c   Wymer, Larry ^b   Rankin, Clifford C ^b   Love, David ^d   Li, Quanlin ^a   Noble, Rachel ^e   Dufour, Alfred P ^b  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRESH WATER; SEA WATER;

BEACH; BIOINDICATOR; COHORT ANALYSIS; FECAL COLIFORM; POLYMERASE CHAIN REACTION; RECREATIONAL ACTIVITY; SAMPLING; SEWAGE DISPOSAL; SPATIOTEMPORAL ANALYSIS; SWIMMING; WATER QUALITY;

ARTICLE; BACTERIUM; BACTEROIDALES; CLOSTRIDIUM PERFRINGENS; COHORT ANALYSIS; ENTEROCOCCUS; EYE DISEASE; FECES; GASTROINTESTINAL DISEASE; INDICATOR ORGANISM; MARINE ENVIRONMENT; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; RECREATION; RESPIRATORY TRACT DISEASE; SEASHORE; SEWAGE TREATMENT; SKIN DISEASE; SWIMMING; UNITED STATES; WATER QUALITY; WATER SAMPLING; ADOLESCENT; ADULT; CHILD; ENVIRONMENTAL MONITORING; FEMALE; HUMAN; INFANT; ISOLATION AND PURIFICATION; MALE; METHODOLOGY; MICROBIOLOGY; NEWBORN; PRESCHOOL CHILD; SEWAGE; STANDARD; STATISTICS;

ALABAMA; MISSISSIPPI; RHODE ISLAND; UNITED STATES;

BACTEROIDALES; BACTEROIDES; CLOSTRIDIUM PERFRINGENS; ENTEROCOCCUS;

ADOLESCENT; ADULT; BATHING BEACHES; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; ENTEROCOCCUS; ENVIRONMENTAL MONITORING; FECES; FEMALE; GASTROINTESTINAL DISEASES; HUMANS; INFANT; INFANT, NEWBORN; MALE; POLYMERASE CHAIN REACTION; PROSPECTIVE STUDIES; RECREATION; SEAWATER; SEWAGE; SWIMMING; UNITED STATES; YOUNG ADULT;

EID: 77958528995     PISSN: None     EISSN: 1476069X     Source Type: Journal    
DOI: 10.1186/1476-069X-9-66     Document Type: Article

References (52)

1. Indicator Microorganisms. CP Gerba, Environmental Microbiology San Diego, CA: Academic Press, Maier RM, Pepper IL, Gerba CP, 2000 491 503
2. Review of epidemiological studies on health effects from exposure to recreational water. A Pruss, Int J Epidemiol 1998 27 1 9 10.1093/ije/27.1.1 9563686
3. Do U.S. Environmental Protection Agency Water Quality Guidelines for Recreational Waters Prevent Gastrointestinal Illness? A Systematic Review and Meta-analysis. TJ Wade N Pai JN Eisenberg JMJ Colford, Environmental Health Perspectives 2003 111 1102 1109 12826481
4. Public Mis-Notification of Coastal Water Quality: A Probabilistic Evaluation of Posting Errors at Huntington Beach, California. JH Kim SB Grant, Environmental Science and Technology 2004 38 2497 2504 10.1021/es034382v 15180043
5. Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. RA Haugland SC Siefring LJ Wymer KP Brenner AP Dufour, Water Res 2005 39 559 568 10.1016/j.watres.2004.11.011 15707628
6. High sensitivity of children to swimming-associated gastrointestinal illness: results using a rapid assay of recreational water quality. TJ Wade RL Calderon KP Brenner E Sams M Beach R Haugland L Wymer AP Dufour, Epidemiology 2008 19 375 383 10.1097/EDE.0b013e318169cc87 18379427
7. Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. TJ Wade RL Calderon E Sams M Beach KP Brenner AH Williams AP Dufour, Environ Health Perspect 2006 114 24 28 10.1289/ehp.8273 16393653
8. Health effects criteria for fresh recreational waters. A Dufour, Tech Rep EPA-600-1-84-004, US Environmental Protection Agency 1984
9. Health effects criteria for marine recreational waters. V Cabelli, Tech Rep USEPA Report Number: EPA-600/1-80-031, US Environmental Protection Agency 1983
10. Viability of Escherichia coli in sea water. RF Vaccaro MP Briggs CL Carey BH Ketchum, Am J Public Health 1950 40 1257 1266 10.2105/AJPH.40.10.1257
11. Effect of sunlight on the infectivity of Cryptosporidium parvum in seawater. AM Nasser L Telser Y Nitzan, Can J Microbiol 2007 53 1101 1105 10.1139/W07-043 18026231
12. A population-based estimate of the burden of diarrhoeal illness in the United States: FoodNet, 1996-7. H Herikstad S Yang TJ Van Gilder D Vugia J Hadler P Blake V Deneen B Shiferaw FJ Angulo, Epidemiol Infect 2002 129 9 17 12211601
13. Burden of self-reported acute diarrheal illness in FoodNet surveillance areas, 1998-1999. B Imhoff D Morse B Shiferaw M Hawkins D Vugia S Lance-Parker J Hadler C Medus M Kennedy MR Moore T Van Gilder, Clin Infect Dis 2004 38 Suppl 3 219 226 10.1086/381590 15095193
14. Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. S Siefring M Varma E Atikovic L Wymer RA Haugland, Journal of Water Health 2008 6 225 237 10.2166/wh.2008.022 (Pubitemid 351772174)
15. Rapid QPCR-based assay for fecal Bacteroides spp. as a tool for assessing fecal contamination in recreational waters. RR Converse AD Blackwood M Kirs JF Griffith RT Noble, Water Res 2009 43 4828 4837 10.1016/j.watres.2009.06.036 19631958
16. Development of an extensive set of 16 S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. T Rinttilä A Kassinen E Malinen L Krogius A Palva, J Appl Microbiol 2004 97 1166 1177 10.1111/j.1365-2672.2004.02409.x 15546407
17. Simple and rapid F+ coliphage culture, latex agglutination, and typing assay to detect and source track fecal contamination. DC Love MD Sobsey, Appl Environ Microbiol 2007 73 4110 4118 10.1128/AEM.02546-06 17483282
18. Method 1601: Male-specific (F+) and Somatic Coliphage in Water by Two-step Enrichment Procedure. USEPA, Tech Rep EPA 821-R-01-030 2001
19. Method 1600: Membrane Filter Test for Enterococci in Water. USEPA, Tech Rep EPA-821-R-97-004, Office of Water 1997
20. User Bulletin 2: ABI PRISM 7700 Sequence Detection System. Biosystems Applied, Tech rep, Applied Biosystems Corporation 1997
21. Evaluation of a rapid, quantitative real-time PCR method for enumeration of pathogenic Candida cells in water. NE Brinkman RA Haugland LJ Wymer M Byappanahalli RL Whitman SJ vesper, Appl Environ Microbiol 2003 69 1775 1782 10.1128/AEM.69.3.1775-1782.2003 12620869
22. Comparison of Fecal Indicator Bacteria Densities in Marine Recreational Waters by QPCR. EC Chern KP Brenner L Wymer RA Haugland, Water Quality Exposure and Health 2009 1 203 214 10.1007/s12403-009-0019-2
23. The behavior of maximum likelihood estimates under non-standard conditions. P Huber, Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability Berkeley, CA: University of California Press 1967 1 221 233
24. A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. H White, Econometrica 1980 48 817 830 10.2307/1912934
25. Regression standard errors in clustered samples. W Rogers, Stata Technical Bulletin 1993 13 19 23
26. A note on robust variance estimation for cluster-correlated data. RL Williams, Biometrics 2000 56 645 6 10.1111/j.0006-341X.2000.00645.x 10877330
27. R Little D Rubin, Statistical Analysis with Missing Data New York: Wiley 2 2002
28. S Greenland KJ Rothman, Modern epidemiology Philadelphia, PA:: Lippincott-Raven 1998
29. Stata Statistical Software: Release 10.1. College Station, Texas: StataCorp LP. StataCorp, 2008
30. Ambient Water Quality for Bacteria-1986. USEPA, Tech Rep EPA-440/5-84-002, Office of Water Regulations and Standards 1986
31. More than obvious: better methods for interpreting nondetect data. DR Helsel, Environ Sci Technol 2005 39 419A 423A 10.1021/es053368a 16295833
32. Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. JM Colford TJ Wade KC Schi CC Wright JF Griffith SK Sandhu S Burns M Sobsey G Lovelace SB Weisberg, Epidemiology 2007 18 27 35 10.1097/01.ede.0000249425.32990.b9 17149140
33. Swimming-associated gastroenteritis and water quality. VJ Cabelli AP Dufour LJ McCabe MA Levin, American Journal of Epidemiology 1982 115 606 616 7072706
34. Traditional and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters. CD Sinigalliano JM Fleisher ML Gidley HM Solo-Gabriele T Shibata LR Plano SM Elmir D Wanless J Bartkowiak R Boiteau K Withum AM Abdelzaher G He C Ortega X Zhu ME Wright J Kish J Hollenbeck T Scott LC Backer LE Fleming, Water Research 2010 44 3763 3772 10.1016/j.watres.2010.04.026 20605185
35. Water and non-water-related risk factors for gastroenteritis among bathers exposed to sewage-contaminated marine waters. JM Fleisher F Jones D Kay R Stanwell-Smith M Wyer R Morano, International Journal of Epidemiology 1993 22 698 708 10.1093/ije/22.4.698 8225746
36. Modeling Enterococcus densities measured by quantitative polymerase chain reaction and membrane filtration using environmental conditions at four Great Lakes beaches. JW Telech KP Brenner R Haugland E Sams AP Dufour L Wymer TJ Wade, Water Res 2009 43 4947 4955 10.1016/j.watres.2009.07.002 19651425
37. Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters. SP Walters KM Yamahara AB Boehm, Water Res 2009 43 4929 4939 10.1016/j.watres.2009.05.047 19616273
38. Rapid decay of host-specific fecal Bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide. S Bae S Wuertz, Water Res 2009 43 4850 4859 10.1016/j.watres.2009.06.053 19656546
39. Faecal indicator bacteria enumeration in beach sand: a comparison study of extraction methods in medium to coarse sands. AB Boehm J Griffith C McGee TA Edge HM Solo-Gabriele R Whitman Y Cao M Getrich JA Jay D Ferguson KD Goodwin CM Lee M Madison SB Weisberg, J Appl Microbiol 2009 107 1740 1750 10.1111/j.1365-2672.2009.04440.x 19659700
40. Re: "epidemiology of salmonellosis in California, 1990-1999: morbidity, mortality, and hospitalization costs". ZD Mulla SR Cole, Am J Epidemiol 2004 159 104 10.1093/aje/kwh007 14693666
41. If we're so different, why do we keep overlapping? When 1 plus 1 doesn't make 2. R Wolfe J Hanley, CMAJ 2002 166 65 66 11800251
42. Monitoring coastal marine waters for spore-forming bacteria of faecal and soil origin to determine point from non-point source pollution. RS Fujioka, Water Sci Technol 2001 44 181 188 11724486
43. Bacteriophages are a better indicator of illness rates than bacteria amongst users of a white water course fed by a lowland river. JV Lee SR Dawson S Ward SB Surman KR Neal, Water Science and Technology 1997 35 165 170 10.1016/S0273-1223(97)00253-9 (Pubitemid 27395444)
44. Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination. JA Soller T Bartrand NJ Ashbolt J Ravenscroft TJ Wade, Water Res 2010 44 4736 4747 10.1016/j.watres. 2010.07.064 20728915
45. The BEACHES Study: health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters. JM Fleisher LE Fleming HM Solo-Gabriele JK Kish CD Sinigalliano L Plano D abd John SME Wang K Withum T Shibata ML Gidley A Abdelzaher G He C Ortega X Zhu M Wright J Hollenbeck LC Backer, International Journal of Epidemiology 2010 Advance Access published June 3, 2010 20522483
46. Tracking sources of bacterial contamination in stormwater discharges to Mission Bay, California. K Schiff P Kinney, Water Environment Research 2001 73 534 542 10.2175/106143001X139605 11765989
47. Mission Bay bacterial source identification study. SJ Gruber LM Kay R Kolb K Henry, Stormwater 2005 6 40 51
48. Monitoring coastal marine waters for spore-forming bacteria of faecal and soil origin to determine point from non-point source pollution. R Fujioka, Water Science & Technology 2001 44 181 188
49. Health effects of marine bathing in New Zealand. G McBride C Salmondo D Bandaranayake S Turner G Lewis D Till, International Journal of Environmental Health Research 1998 8 173 189 10.1080/09603129873462 (Pubitemid 28410304)
50. Association of gastrointestinal illness and recreational water exposure at an inland U.S. beach. JW Marion J Lee S Lemeshow TJ Buckley, Water Res 2010 44 4796 4804 10.1016/j.watres.2010.07.065 20723965
51. The health effects of swimming in ocean water contaminated by storm drain runoff. RW Haile JS Witte M Gold R Cressey C McGee RC Millikan A Glasser N Harawa C Ervin P Harmon J Harper J Dermand J Alamillo K Barrett M Nides G Wang, Epidemiology 1999 10 355 363 10.1097/00001648-199907000-00004 10401868
52. The health effects of swimming at Sydney beaches. The Sydney Beach Users Study Advisory Group. SJ Corbett GL Rubin GK Curry DG Kleinbaum, American Journal of Public Health 1993 83 1701 1706 10.2105/AJPH.83.12.1701 8259798