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The association between marine bathing and infectious diseases– a review

Published online by Cambridge University Press:  19 January 2016

Nicholas Young*
Affiliation:
University of Bristol, Bristol, UK Public Health England, Exeter, UK
*
Correspondence should be addressed to:N. Young, University of Bristol, Bristol, UK email: [email protected]

Abstract

Worldwide, infectious diseases represent a leading cause of death and disability. Exposure to the ocean, whether through recreation or occupation, represents a potentially significant, but poorly understood, source of infectious diseases in man. This review describes the potential mechanisms whereby marine bathing could lead to infectious diseases in man. Sources of pathogens in the marine environment are described, including human sewage, animal sources, fellow bathers and indigenous marine organisms. The epidemiological evidence for the association between marine bathing and infectious disease is presented, including a consideration of the differing relationship between faecal indicator bacteria levels and illness at point source compared with non-point source settings. Estimating the burden of infectious disease is reliant on public health surveillance, both formal and informal, which is described from a UK perspective in this review. Potential emerging threats at the marine–human interface are discussed, including infections caused by Shewanella and Vibrio bacteria, and the presence of human pathogens in the marine environment that are resistant to antimicrobials.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Aigbivbalu, L. and Maraqa, N. (2009) Photobacterium damsela wound infection in a 14-year-old surfer. South Medical Journal 102, 425426.CrossRefGoogle Scholar
Andersson, Y. and Ekdahl, K. (2006) Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006. Euro Surveillance 11, E060803E060802.Google ScholarPubMed
Arnold, B.F., Schiff, K.C., Griffith, J.F., Gruber, J.S., Yau, V., Wright, C.C., Wade, T.J., Burns, S., Hayes, J.M., McGee, C., Gold, M., Cao, Y., Weisberg, S.B. and ColfordJ.M., Jr. J.M., Jr. (2013) Swimmer illness associated with marine water exposure and water quality indicators: impact of widely used assumptions. Epidemiology 24, 845853.CrossRefGoogle ScholarPubMed
Baker-Austin, C., Stockley, L., Rangdale, R. and Martinez-Urtaza, J. (2010) Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environmental Microbiology Reports 2, 718.CrossRefGoogle ScholarPubMed
Balarajan, R., Soni Raleigh, V., Yuen, P., Wheeler, D., Machin, D. and Cartwright, R. (1991) Health risks associated with bathing in sea water. British Medical Journal 303, 14441445.CrossRefGoogle ScholarPubMed
Beversdorf, L.J., Bornstein-Forst, S.M. and McLellan, S.L. (2007) The potential for beach sand to serve as a reservoir for Escherichia coli and the physical influences on cell die-off. Journal of Applied Microbiology 102, 13721381.CrossRefGoogle ScholarPubMed
Bradley, G. and Hancock, C. (2003) Increased risk of non-seasonal and body immersion recreational marine bathers contacting indicator microorganisms of sewage pollution. Marine Pollution Bulletin 46, 791794.CrossRefGoogle ScholarPubMed
Brinks, M.V., Dwight, R.H., Osgood, N.D., Sharavanakumar, G., Turbow, D.J., El-Gohary, M., Caplan, J.S., Semenza, J.C. (2008) Health risk of bathing in Southern California coastal waters. Archives of Environmental and Occupational Health 63, 123135.CrossRefGoogle ScholarPubMed
Charoenca, N. and Fujioka, R. (1995) Association of staphylococcal skin infections and swimming. Water Science and Technology 31, 1117.CrossRefGoogle Scholar
Cheung, J.P., Fung, B., Wong, S.S. and Ip, W.Y. (2010) Review article: Mycobacterium marinum infection of the hand and wrist. Journal of Orthopaedic Surgery (Hong Kong) 18, 98103.CrossRefGoogle ScholarPubMed
Colford, J.M. Jr, Wade, T.J., Schiff, K.C., Wright, C.C., Griffith, J.F., Sandhu, S.K., Burns, S., Sobsey, M., Lovelace, G. and Weisberg, S.B. (2007) Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology 18, 2735.CrossRefGoogle ScholarPubMed
Corbett, S.J., Rubin, G.L., Curry, G.K. and Kleinbaum, D.G. (1993) The health effects of swimming at Sydney beaches. The Sydney Beach Users Study Advisory Group. American Journal of Public Health 83, 17011706.CrossRefGoogle ScholarPubMed
Dallman, T.J., Byrne, L., Ashton, P.M., Cowley, L.A., Perry, N.T., Adak, G., Petrovska, L., Ellis, R.J., Elson, R. and Underwood, A. (2015) Whole-genome sequencing for national surveillance of shiga toxin–producing Escherichia coli O157. Clinical Infectious Diseases 61, 305312.CrossRefGoogle ScholarPubMed
Depledge, M.H. and Bird, W.J. (2009) The blue gym: health and wellbeing from our coasts. Marine Pollution Bulletin 58, 947948.CrossRefGoogle ScholarPubMed
Dominguez, H., Vogel, B.F., Gram, L., Hoffmann, S. and Schaebel, S. (1996) Shewanella alga bacteremia in two patients with lower leg ulcers. Clinical Infectious Diseases 22, 10361039.CrossRefGoogle ScholarPubMed
Efstratiou, M.A. and Tsirtsis, G. (2009) Do 2006/7/EC European Union Bathing Water Standards exclude the risk of contact with Salmonella or Candida albicans? Marine Pollution Bulletin 58, 10391044.CrossRefGoogle ScholarPubMed
Elliot, A., Hughes, H., Hughes, T., Locker, T., Brown, R., Sarran, C., Clewlow, Y., Murray, V., Bone, A. and Catchpole, M. (2013) The impact of thunderstorm asthma on emergency department attendances across London during July 2013. Emergency Medicine Journal 31, 675678. doi: 10.1136/emermed-2013-203122.CrossRefGoogle ScholarPubMed
Elmir, S.M., Wright, M.E., Abdelzaher, A., Solo-Gabriele, H.M., Fleming, L.E., Miller, G., Rybolowik, M., Peter, Shih M.T., Pillai, S.P., Cooper, J.A. and Quaye, E.A. (2007) Quantitative evaluation of bacteria released by bathers in a marine water. Water Research 41, 310.CrossRefGoogle Scholar
Elmir, S.M., Shibata, T., Solo-Gabriele, H.M., Sinigalliano, C.D., Gidley, M.L., Miller, G., Plano, L.R., Kish, J., Withum, K. and Fleming, L.E. (2009) Quantitative evaluation of enterococci and Bacteroidales released by adults and toddlers in marine water. Water Research 43, 46104616.CrossRefGoogle ScholarPubMed
Environment Agency, UK (2014) Tough action to protect England's beaches and £3.6bn seaside economy – Press releases [Internet]. Available at https://www.gov.uk/government/news/tough-action-to-protect-englands-beaches-and-36bn-seaside-economy (accessed 25 October 2015).Google Scholar
Fayer, R., Graczyk, T.K., Lewis, E.J., Trout, J.M. and Farley, C.A. (1998) Survival of infectious Cryptosporidium parvum oocysts in seawater and eastern oysters (Crassostrea virginica) in the Chesapeake Bay. Applied and Environmental Microbiology 64, 10701074.CrossRefGoogle ScholarPubMed
Fleisher, J.M., Kay, D., Salmon, R.L., Jones, F., Wyer, M.D. and Godfree, A.F. (1996) Marine waters contaminated with domestic sewage: nonenteric illnesses associated with bather exposure in the United Kingdom. American Journal of Public Health 86, 12281234.CrossRefGoogle ScholarPubMed
Fleisher, J.M., Fleming, L.E., Solo-Gabriele, H.M., Kish, J.K., Sinigalliano, C.D., Plano, L., Elmir, S.M., Wang, J.D., Withum, K., Shibata, T., Gidley, M.L., Abdelzaher, A., He, G., Ortega, C., Zhu, X., Wright, M., Hollenbeck, J. and Backer, L.C. (2010) The BEACHES Study: health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters. International Journal of Epidemiology 39, 12911298.CrossRefGoogle ScholarPubMed
Frank, C., Littman, M., Alpers, K. and Hallauer, J. (2006) Vibrio vulnificus wound infections after contact with the Baltic Sea, Germany. Euro Surveillance 11, E060817E060811.Google ScholarPubMed
Fujioka, R.S. and Unutoa, T.M. (2006) Comparative stability and growth requirements of S. aureus and faecal indicator bacteria in seawater. Water Science and Technology 54, 169175.CrossRefGoogle ScholarPubMed
Gomez, J.M., Fajardo, R., Patino, J.F. and Arias, C.A. (2003) Necrotizing fasciitis due to Vibrio alginolyticus in an immunocompetent patient. Journal of Clinical Microbiology 41, 34273429.CrossRefGoogle Scholar
Goyal, R., Kaur, N. and Thakur, R. (2011) Human soft tissue infection by the emerging pathogen Shewanella algae. Journal of Infection in Developing Countries 5, 310312.CrossRefGoogle ScholarPubMed
Harder-Lauridsen, N.M., Kuhn, K.G., Erichsen, A.C., Mølbak, K. and Ethelberg, S. (2013) Gastrointestinal illness among triathletes swimming in non-polluted versus polluted seawater affected by heavy rainfall, Denmark, 2010–2011. PLoS ONE 8, e78371.CrossRefGoogle Scholar
Heaney, C.D., Sams, E., Dufour, A.P., Brenner, K.P., Haugland, R.A., Chern, E., Wing, S., Marshall, S., Love, D.C., Serre, M., Noble, R. and Wade, T.J. (2012) Fecal indicators in sand, sand contact, and risk of enteric illness among beachgoers. Epidemiology 23, 95106.CrossRefGoogle ScholarPubMed
Heymann, D.L. (2008) Control of communicable diseases manual. Washington, DC: American Public Health Association.Google Scholar
Heymann, D.L. and Rodier, G. (2004) Global surveillance, national surveillance, and SARS. Emerging Infectious Diseases 10, 173175.CrossRefGoogle ScholarPubMed
Holt, H.M., Gahrn-Hansen, B. and Bruun, B. (2005) Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics. Clinical Microbiology and Infection 11, 347352.CrossRefGoogle ScholarPubMed
Holt, H.M., Sogaard, P. and Gahrn-Hansen, B. (1997) Ear infections with Shewanella alga: a bacteriologic, clinical and epidemiologic study of 67 cases. Clinical Microbiology and Infection 3, 329334.CrossRefGoogle ScholarPubMed
Huq, A., Colwell, R.R., Rahman, R., Ali, A., Chowdhury, M., Parveen, S., Sack, D. and Russek-Cohen, E. (1990) Detection of Vibrio cholerae O1 in the aquatic environment by fluorescent-monoclonal antibody and culture methods. Applied and Environmental Microbiology 56, 23702373.CrossRefGoogle ScholarPubMed
Ihekweazu, C., Barlow, M., Roberts, S., Christensen, H., Guttridge, B., Lewis, D. and Paynter, S. (2005) Outbreak of E. coli O157 infection in the south west of the UK: risks from streams crossing seaside beaches. Euro Surveillance 11, 128130.Google Scholar
Janda, J.M. and Abbott, S.L. (2014) The genus Shewanella: from the briny depths below to human pathogen. Critical Reviews in Microbiology 40, 293312.CrossRefGoogle ScholarPubMed
Jiang, S., Noble, R. and Chu, W. (2001) Human adenoviruses and coliphages in urban runoff-impacted coastal waters of Southern California. Applied and Environmental Microbiology 67, 179184.CrossRefGoogle ScholarPubMed
Jiang, S.C. and Chu, W. (2004) PCR detection of pathogenic viruses in southern California urban rivers. Journal of Applied Microbiology 97, 1728.CrossRefGoogle ScholarPubMed
Kay, D., Fleisher, J.M., Salmon, R.L., Jones, F., Wyer, M.D., Godfree, A.F., Zelenauch-Jacquotte, Z. and Shore, R. (1994) Predicting likelihood of gastroenteritis from sea bathing: results from randomised exposure. Lancet 344, 905909.CrossRefGoogle ScholarPubMed
Keller, M., Blench, M., Tolentino, H., Freifeld, C.C., Mandl, K.D., Mawudeku, A., Eysenbach, G. and Brownstein, J.S. (2009) Use of unstructured event-based reports for global infectious disease surveillance. Emerging Infectious Diseases 15, 689.CrossRefGoogle ScholarPubMed
Khan, N.H., Ahsan, M., Taylor, W.D. and Kogure, K. (2010) Culturability and survival of marine, freshwater and clinical Pseudomonas aeruginosa. Microbes and Environments 25, 266274.CrossRefGoogle ScholarPubMed
Kushawaha, A., Mobarakai, N., Cooper, M., Rose, K. and Awasum, M. (2010) Necrotising fasciitis with Vibrio vulnificus: a limb threatening dermatologic complication following exposure to marine life. British Medical Journal Case Reports. doi: 10.1136/bcr.11.2009.2478.Google ScholarPubMed
Leonard, A.F., Zhang, L., Balfour, A.J., Garside, R. and Gaze, W.H. (2015) Human recreational exposure to antibiotic resistant bacteria in coastal bathing waters. Environment International 82, 92100. doi: 10.1016/j.envint.2015.02.013.CrossRefGoogle ScholarPubMed
Lepesteur, M., McComb, A.J. and Moore, S.A. (2006) Do we all face the same risk when bathing in the estuary? Water Research 40, 27872795.CrossRefGoogle ScholarPubMed
Measures, L.N. and Olson, M. (1999) Giardiasis in pinnipeds from eastern Canada. Journal of Wildlife Diseases 35, 779782.CrossRefGoogle ScholarPubMed
Oliver, D.M., van, Niekerk M., Kay, D., Heathwaite, A.L., Porter, J., Fleming, L.E., Kinzelman, J.L., Connolly, E., Cummins, A. and McPhail, C. (2014) Opportunities and limitations of molecular methods for quantifying microbial compliance parameters in EU bathing waters. Environment International 64, 124128.CrossRefGoogle ScholarPubMed
Papastergiou, P., Mouchtouri, V., Pinaka, O., Katsiaflaka, A., Rachiotis, G. and Hadjichristodoulou, C. (2012) Elevated bathing-associated disease risks despite certified water quality: a cohort study. International Journal of Environmental Research and Public Health 9, 15481565.CrossRefGoogle ScholarPubMed
Park, K.H., Jung, S.I., Jung, Y.S., Shin, J.H. and Hwang, J.H. (2009) Marine bacteria as a leading cause of necrotizing fasciitis in coastal areas of South Korea. American Journal of Tropical Medicine and Hygiene 80, 646650.CrossRefGoogle ScholarPubMed
Pina, S., Puig, M., Lucena, F., Jofre, J. and Girones, R. (1998) Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Applied and Environmental Microbiology 64, 33763382.CrossRefGoogle ScholarPubMed
Plano, L.R., Garza, A.C., Shibata, T., Elmir, S.M., Kish, J., Sinigalliano, C.D., Gidley, M.L., Miller, G., Withum, K., Fleming, L.E. and Solo-Gabriele, H.M. (2011) Shedding of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from adult and pediatric bathers in marine waters. BMC Microbiology 11, 5.CrossRefGoogle ScholarPubMed
Plano, L.R., Shibata, T., Garza, A.C., Kish, J., Fleisher, J.M., Sinigalliano, C.D., Gidley, M.L., Withum, K., Elmir, S.M. and Hower, S. (2013) Human-associated methicillin-resistant Staphylococcus aureus from a subtropical recreational marine beach. Microbial Ecology 65, 10391051.CrossRefGoogle ScholarPubMed
Powell, A., Baker-Austin, C., Wagley, S., Bayley, A. and Hartnell, R. (2013) Isolation of pandemic Vibrio parahaemolyticus from UK water and shellfish produce. Microbial Ecology 65, 924927.CrossRefGoogle ScholarPubMed
Prieto, M.D., Lopez, B., Juanes, J.A., Revilla, J.A., Llorca, J. and Delgado-Rodriguez, M. (2001) Recreation in coastal waters: health risks associated with bathing in sea water. Journal of Epidemiology and Community Health 55, 442447.CrossRefGoogle ScholarPubMed
Public Health England (2014a) Vero cytotoxin-producing Escherichia coli (VTEC): guidance, data and analysis [Internet]. Available at https://www.gov.uk/government/collections/vero-cytotoxin-producing-escherichia-coli-vtec-guidance-data-and-analysis (accessed 25 October 2015).Google Scholar
Public Health England (2014b) Syndromic surveillance: systems and analyses [Internet]. Available at https://www.gov.uk/government/collections/syndromic-surveillance-systems-and-analyses (accessed 25 October 2015).Google Scholar
Rusinol, M., Fernandez-Cassi, X., Hundesa, A., Vieira, C., Kern, A., Eriksson, I., Ziros, P., Kay, D., Miagostovich, M. and Vargha, M. (2014) Application of human and animal viral microbial source tracking tools in fresh and marine waters from five different geographical areas. Water Research 59, 119129.CrossRefGoogle ScholarPubMed
Saliba, L.J. and Helmer, R. (1990) Health risks associated with pollution of coastal bathing waters. World Health Stat Q 43, 177187.Google ScholarPubMed
Schets, F., Van den Berg, H., Demeulmeester, A., Van Dijk, E., Rutjes, S., van Hooijdonk, H. and de Roda Husman, A. (2006) Vibrio alginolyticus infections in the Netherlands after swimming in the North Sea. Euro Surveillance 11, 3077.Google ScholarPubMed
Schets, F.M., van den Berg, H.H., Marchese, A., Garbom, S. and de Roda Husman, A.M. (2011) Potentially human pathogenic vibrios in marine and fresh bathing waters related to environmental conditions and disease outcome. International Journal of Hygiene and Environmental Health 214, 399406.CrossRefGoogle ScholarPubMed
Schijven, J. and de Roda Husman, A.M. (2006) A survey of diving behaviour and accidental water ingestion among Dutch occupational and sport divers to assess the risk of infection with waterborne pathogenic microorganisms. Environmental Health Perspectives 114, 712717.CrossRefGoogle ScholarPubMed
Scholthof, K.-B.G. (2007) The disease triangle: pathogens, the environment and society. Nature Reviews Microbiology 5, 152156.CrossRefGoogle ScholarPubMed
Solo-Gabriele, H.M., Wolfert, M.A., Desmarais, T.R. and Palmer, C.J. (2000) Sources of Escherichia coli in a coastal subtropical environment. Applied Environmental Microbiology 66, 230237.CrossRefGoogle Scholar
Spicer, W.J. (2008) Clinical microbiology and infectious diseases, 2nd edn.Edinburgh: Churchill Livingstone/Elsevier.Google Scholar
Srinivas, J., Pillai, M., Vinod, V. and Dinesh, R.K. (2015) Skin and soft tissue infections due to Shewanella algae–an emerging pathogen. Journal of Clinical and Diagnostic Research 9, DC16.Google Scholar
Tam, C.C., Rodrigues, L.C., Viviani, L., Dodds, J.P., Evans, M.R., Hunter, P.R., Gray, J.J., Letley, L.H., Rait, G. and Tompkins, D.S. (2012) Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut 61, 6977.CrossRefGoogle ScholarPubMed
Thomas, D. and Bowers, D.G. (2012) Introducing oceanography. Edinburgh: Dunedin Academic Press.Google Scholar
Tolba, O., Loughrey, A., Goldsmith, C.E., Millar, B.C., Rooney, P.J. and Moore, J.E. (2008) Survival of epidemic strains of healthcare (HA-MRSA) and community-associated (CA-MRSA) methicillin-resistant Staphlycoccus aureus (MRSA) in river-, sea- and swimming pool water. International Journal of Hygiene and Environmental Health 211, 398402.CrossRefGoogle Scholar
Turbow, D.J., Kent, E.E. and Jiang, S.C. (2008) Web-based investigation of water associated illness in marine bathers. Environ Research 106, 101109.CrossRefGoogle ScholarPubMed
United States Centers for Disease Control & Prevention (2005) Vibrio illnesses after Hurricane Katrina – multiple states, August – September 2005. Morbidity and Mortality Weekly Report 54 (Dispatch), 14.Google Scholar
United States Centers for Disease Control & Prevention (2014) Background and goals [Internet]. Available at http://wwwnc.cdc.gov/eid/page/background-goals (accessed 25 October 2015).Google Scholar
United States Centers for Disease Control & Prevention (2015) Principles of epidemiology: lesson 1, section 10|self-study course [Internet]. Available at http://www.cdc.gov/ophss/csels/dsepd/ss1978/lesson1/section10.html (accessed 25 October 2015).Google Scholar
Victoria, M., Rigotto, C., Moresco, V., De Abreu Corrêa, A., Kolesnikovas, C., Leite, J.P.G., Miagostovich, M.P. and Barardi, C.R.M. (2010) Assessment of norovirus contamination in environmental samples from Florianopolis City, Southern Brazil. Journal of Applied Microbiology 109, 231238.CrossRefGoogle ScholarPubMed
Vignier, N., Barreau, M., Olive, C., Baubion, E., Theodose, R., Hochedez, P. and Cabie, A. (2013) Human infection with Shewanella putrefaciens and S. algae: report of 16 cases in Martinique and review of the literature. American Journal of Tropical Medicine and Hygiene 89, 151156.CrossRefGoogle ScholarPubMed
Wade, T.J., Pai, N., Eisenberg, J.N. and Colford, J.M. Jr (2003) Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environmental Health Perspectives 111, 11021109.CrossRefGoogle ScholarPubMed
Wade, T.J., Calderon, R.L., Brenner, K.P., Sams, E., Beach, M., Haugland, R., Wymer, L. and Dufour, A.P. (2008) High sensitivity of children to swimming-associated gastrointestinal illness: results using a rapid assay of recreational water quality. Epidemiology 19, 375383.CrossRefGoogle ScholarPubMed
Wade, T.J., Sams, E., Brenner, K.P., Haugland, R., Chern, E., Beach, M., Wymer, L., Rankin, C.C., Love, D. and Li, Q. (2010) Rapidly measured indicators of recreational water quality and swimming-associated illness at marine beaches: a prospective cohort study. Environmental Health 9, 114.CrossRefGoogle ScholarPubMed
Wade, T.J., Sams, E.A., Beach, M.J., Collier, S.A. and Dufour, A.P. (2013) The incidence and health burden of earaches attributable to recreational swimming in natural waters: a prospective cohort study. Environmental Health 12, 67.CrossRefGoogle ScholarPubMed
Wang, J.D., Solo-Gabriele, H.M., Abdelzaher, A.M. and Fleming, L.E. (2010) Estimation of enterococci input from bathers and animals on a recreational beach using camera images. Marine Pollution Bulletin 60, 12701278.CrossRefGoogle ScholarPubMed
World Health Organization (2014) The top ten causes of death [Internet]. Available at http://www.who.int/mediacentre/factsheets/fs310/en/ (accesed 25 October 2015).Google Scholar
World Health Organization (2015a) Water-related disease [Internet]. Available at http://www.who.int/water_sanitation_health/diseases/diarrhoea/en/ (accessed 25 October 2015).Google Scholar
World Health Organization (2015b) Public health surveillance [Internet]. Available at http://www.who.int/topics/public_health_surveillance/en/ (accessed 25 October 2015).Google Scholar
World Health Organization (2015c) Antimicrobial resistance [Internet]. Available at http://www.who.int/mediacentre/factsheets/fs194/en/ (accessed 25 October 2015).Google Scholar
Yamahara, K.M., Layton, B.A., Santoro, A.E. and Boehm, A.B. (2007) Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters. Environmental Science and Technology 41, 45154521.CrossRefGoogle ScholarPubMed
Yau, V.M., Schiff, K.C., Arnold, B.F., Griffith, J.F., Gruber, J.S., Wright, C.C., Wade, T.J., Burns, S., Hayes, J.M. and McGee, C. (2014) Effect of submarine groundwater discharge on bacterial indicators and swimmer health at Avalon Beach, CA, USA. Water Research 59, 2336.CrossRefGoogle ScholarPubMed