Beach sand and the potential for infectious disease transmission: Observations and recommendations

Journal of the Marine Biological Association of the United Kingdom

Volumn 96, Issue 1, 2016, Pages 101-120

  Solo Gabriele, Helena M ^a,b   Harwood, Valerie J ^c   Kay, David ^d   Fujioka, Roger S ^e   Sadowsky, Michael J ^f   Whitman, Richard L ^g   Wither, Andrew ^h   Caniça, Manuela ^i,j   Da Fonseca, Rita Carvalho ⁱ   Duarte, Aida ^k   Edge, Thomas A ^l   Gargaté, Maria J ⁱ   Gunde Cimerman, Nina ^m   Hagen, Ferry ⁿ   Mclellan, Sandra L ^o   Da Silva, Alexandra Nogueira ^k   Babič, Monika Novak ^m   Prada, Susana ^p,q   Rodrigues, Raquel ⁱ   Romão, Daniela ⁱ   Sabino, Raquel ⁱ   Samson, Robert A ^r   Segal, Esther ^s   Staley, Christopher ^f   Taylor, Huw D ^t   Veríssimo, Cristina ⁱ   Viegas, Carla ^u   Barroso, Helena ^v   Brandão, João C ⁱ   more..

^a UNIVERSITY OF MIAMI   (United States)

^b University of Miami College of Engineering   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d ABERYSTWYTH UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF HAWAII   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g U S GEOLOGICAL SURVEY   (United States)

^h NATIONAL OCEANOGRAPHY CENTRE   (United Kingdom)

ⁱ NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^j UNIVERSITY OF PORTO   (Portugal)

^k RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^l ENVIRONMENT CANADA   (Canada)

^m UNIVERSITY OF LJUBLJANA   (Slovenia)

ⁿ CANISIUS WILHELMINA HOSPITAL   (Netherlands)

^o UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^p UNIVERSITY OF MADEIRA   (Portugal)

^q UNIVERSITY OF THE AZORES   (Portugal)

^r CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^s TEL AVIV UNIVERSITY   (Israel)

^t UNIVERSITY OF BRIGHTON   (United Kingdom)

^u INSTITUTO POLITÉCNICO DE LISBOA   (Portugal)

^v INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

more..

Author keywords

bacteria; Beach sand; fungi; microbes

Indexed keywords

BACTERIUM; BEACH MORPHOLOGY; DISEASE TRANSMISSION; ENVIRONMENTAL MONITORING; ETIOLOGY; FECAL PELLET; FUNGUS; HEALTH RISK; INFECTIOUS DISEASE; SAND; SANITATION; SPATIAL DISTRIBUTION;

BACTERIA (MICROORGANISMS); FUNGI;

EID: 84934300189     PISSN: 00253154     EISSN: 14697769     Source Type: Journal    
DOI: 10.1017/S0025315415000843     Document Type: Article

References (166)

1. Abdelzaher A., Solo-Gabriele H., Phillips M., Elmir S., and Fleming L. (2013) An alternative approach to water regulations for public health protection at bathing beaches. Journal of Environmental, and Public Health 2013, 1-9
2. Abdelzaher A., Wright M., Ortega C., Solo-Gabriele H.M., Miller G., Elmir S., Newman X., Shih P., Bonilla J.A., Bonilla T.D., Palmer C.J., Scott T., Lukasik J., Harwood V.J., McQuaig S., Sinigalliano C., Gidley M., Plano L.R.W., Zhu X., Wang J.D., and Fleming L.E. (2010) Presence of pathogens, and indicator microbes at a non-point source subtropical recreational marine beach. Applied, and Environmental Microbiology 76, 724-732
3. Alastruey-Izquierdo A., Cuenca-Estrella M., Monzón A., Mellado E., and Rodríguez-Tudela J.L. (2008) Antifungal susceptibility profile of clinical Fusarium spp. isolates identified by molecular methods. Epub 61, 805-809. doi: 10.1093/jac/dkn022
4. Alcazar-Fuoli L., Mellado E., Alastruey-Izquierdo A., Cuenca-Estrella M., and Rodriguez-Tudela J.L. (2008) Aspergillus section Fumigati: antifungal susceptibility patterns, and sequence-based identification. Antimicrobial Agents, and Chemotherapy 52, 1244-1251
5. Alm E.W., Burke J., and Spain A. (2003) Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Research 37, 3978-3982
6. Anderson J.H. (1979) In vitro survival of human pathogenic fungi in Hawaiian beach sand. Sabouraudia 17, 13-22
7. Ashbolt N.J., Amézquita A., Backhaus T., Borriello P., Brandt K.K., Collignon P., Coors A., Finley R., Gaze W.H., Heberer T., Lawrence J.R., Larsson D.G., McEwen S.A., Ryan J.J., Schönfeld J., Silley P., Snape J.R., Van den Eede C., and Topp E. (2013) Human Health Risk Assessment (HHRA) for environmental development, and transfer of antibiotic resistance. Environmental Health Perspectives 121, 993-1001
8. Aw T.G., and Rose J.B. (2012) Detection of pathogens in water: from phylochips to qPCR to pyrosequencing. Current Opinion in Biotechnology 23, 422-430
9. Badillet G. (1973) Les Dermatophytes: atlas clinique et biologique, 3 eme Ed. Paris: E'ditions Varia
10. Balajee S.A., Gribskov J.L., Hanley E., Nickle D., and Marr K.A. (2005) Aspergillus lentulus sp. nov., a new sibling species of A. fumigatus. Eukaryotic Cell 4, 625-632
11. Bik M.H., Halanych M., Sharma J., and Thomas K. (2012) Dramatic shifts in benthic microbial eukaryote communities following the deep water horizon oil spill. PLoS ONE 7, 1-6
12. Boehm A., Ashbolt N., Colford J. Jr, Dunbar L., Fleming L., Gold M., Hansel J., Hunter P., Ichida A., McGee C., Soller J., and Weisberg S. (2009a) A sea change ahead for recreational water quality criteria. Journal of Water, and Health 7, 9-20
13. Boehm A.B., Grant S.B., Kim J.H., Mowbray S.L., McGee C.D., Clark C.D., Foley D.M., and Wellman D.E. (2002) Decadal, and shorter period variability of surf-zone water quality at Huntington beach, California. Environmental Science, and Technology 36, 3885-3892
14. Boehm A.B., Griffith J., McGee C., Edge T.A., Solo-Gabriele H.M., Whitman R., Cao Y., Getrich M., Jay J.A., Ferguson D., Goodwin K.D., Lee C.M., Madison M., and Weisberg S.B. (2009b) Faecal indicator bacteria enumeration in beach sand: a comparison study of extraction methods in medium to coarse sands. Journal of Applied Microbiology 107, 1740-1750
15. Boehm A., and Sassoubre L. (2014) Enterococci as indicators of human faecal pollution. In Gilmore M.S., Clewell D.B., Ike Y., and Shankar N. (eds) Enterococci: from commensals to leading causes of drug resistant infection. Boston, MA: Massachusetts Eye, and Ear Infirmary
16. Boehm A.B., Shellenbarger G.G., and Paytan A. (2004) Groundwater discharge: potential association with faecal indicator bacteria in the surf zone. Environmental Science & Technology 38, 3558-3566
17. Bonde G.J. (1966) Bacteriological methods for estimation of water pollution. Health Laboratory Science 3, 124-128
18. Bonilla T.D., Nowosiellski K., Cuvelier M., Hartz A., Grenn M., Esiobu N., McCorquodale D.S., Fleisher J.M., and Rogerson A. (2007) Prevalence, and distribution of faecal indicator organisms in South Florida beach sand, and preliminary assessment of health effects associated with beach sand exposure. Marine Pollution Bulletin 54, 1472-1482
19. Brandão J., Wergikosky B., Rosado C., Noronha G., Verissimo C., Falcão M.L., Giraldes A., Simões M., and Rebelo H. (2002) Qualidade Microbiológica De areias De Praias Litoriais -Relatório Final. Alfragide: Instituto do Ambiente, Associac?ão Bandeira Azul da Europa. Available at: http://repositorio.insa.pt/handle/10400.18/232
20. Byappanahalli M.N., Nevers M.B., Whitman R.L., Ge Z., Spoljaric A., Shively D., and Przybyla-Kelly K. (2015) Wildlife, urban inputs, and landscape configuration are responsible for degraded swimming water quality at an embayed beach. Journal of Great Lakes Research 41, 156-163
21. Byappanahalli M.N., Shively D.A., Nevers M.B., Sadowsky M.J., and Whitman R.L. (2003) Growth, and survival of Escherichia coli, and enterococci populations in the macro-alga Cladophora (Chlorophyta) FEMS Microbiology Ecology 46, 203-211
22. Carneiro H.A., Coleman J.J., Restrepo A., and Mylonakis E. (2011) Fusarium infection in lung transplant patients: report of 6 cases, and review of the literature. Medicine (Baltimore) 90, 69-80
23. CDC (2013) Summary of notifiable diseases - United States, 2011. Morbidity, and Mortality Weekly Report 60 8-107
24. CDC 2014) Summary of notifiable diseases - United States, 2011. Morbidity, and Mortality Weekly Report 61 1-121
25. CDC (2015) Antifungal resistance. http://www.cdc.gov/fungal/antifungalresistance. html
26. Chowdhary A., Kathuria S., Xu J., and Meis J.F. (2013) Emergence of azole-resistant Aspergillus fumigatus strains due to agricultural azole use creates an increasing threat to human health. PLoS Pathogens 9, e1003633. doi: 10.1371/journal.ppat.1003633
27. 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, 27-35
28. Costa I., Bértolo E., Bagulho A., and Duarte A. (2009) Monitoring of fungi flora on beaches sand along the Estoril coast, Portugal. 4th Trends in Medical Mycology Meeting (TIMM), 18-21 October, Athens, Greece
29. Cui H., Yang K., Pagaling E., and Yan T. (2013) Spatial, and temporal variation in enterococcal abundance, and its relationship to the microbial community in Hawaii beach sand, and water. Applied, and Environmental Microbiology 79, 3601-3609
30. De Hoog G.S., Guarro J., Gene J., and Figueras M.J. (2009) Atlas of clinical fungi. Utrecht/Reus: Centra albureauVoor Schimmelcultures, Universitat Rovira I Virgili
31. De Kraker M.E., Davey P.G., Grundmann H., and BURDEN Study Group (2011) Mortality, and hospital stay associated with resistant Staphylococcus aureus, and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Medicine 8, e1001104
32. De Sieyes N.R., Yamahara K.M., Layton B.A., Joyce E.H., and Boehm A.B. (2008) Submarine discharge of nutrient-enriched fresh groundwater at Stinson Beach, California is enhanced during neap tides. Limnology, and Oceanography 53, 1434-1445
33. Diwan V., Stålsby L.C., and Tamhankar A.J. (2013) Seasonal, and temporal variation in release of antibiotics in hospital wastewater: estimation using continuous, and grab sampling. PLoS ONE 8, e68715
34. Dolenc-Voljc M. (2005) Dermatophyte infections in the Ljubljana region, Slovenia. Mycoses 48, 181-186
35. Dunhill I., Nicholson N., Long R., Porter J., and Rahman A. (2013) Faecal indicator organism populations in wrack piles. Bristol: Evidence Directorate, Environment Agency
36. Ebdon J., Muniesa M., and Taylor H.D. (2007) The application of a recently isolated strain of Bacteroides (GB-124) to identify human sources of faecal pollution in a temperate river catchment. Water Research 41, 3683-3690
37. Edge T.A., and Hill S. (2007) Multiple lines of evidence to identify the sources of fecal pollution at a freshwater beach in Hamilton Harbour, Lake Ontario. Water Research 41, 3585-3594
38. ECDC (2011a) Annual report of the Director 2011. Stockholm: European Centre for Disease Prevention, and Control. doi: 10.2900/25172, 71
39. ECDC (2011b) Annual report of the Director 2010. Stockholm: European Centre for Disease Prevention, and Control. doi: 10.2900/52932, 64
40. ECDC (2012) Annual report of the Director 2012. Stockholm: European Centre for Disease Prevention, and Control. doi: 10.2900/7911, 77
41. ECDC (2013) Antimicrobial resistance surveillance in Europe. Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) Stockholm: European Centre for Disease Prevention, and Control
42. ECDC (2014a) Annual epidemiological report 2014 - Food-and waterborne diseases, and zoonoses. Surveillance report. Stockholm: European Centre for Disease Prevention, and Control
43. ECDC (2014b) Annual epidemiological report 2014 - respiratory tract infections. Surveillance Report. Stockholm: European Centre for Disease Prevention, and Control
44. Efstratiou M., and Velegraki A. (2009) Recovery of melanised yeasts from Eastern Mediterranean beach sand associated with the prevailing geochemical, and marine flora patterns. Medical Mycology 48, 413-415
45. Elmir S.M., Shibata T., Solo-Gabriele H.M., Sinigalliano C.D., Gidley M.L., Miller G., Plano L., Kish J., Withum K., and Fleming L. (2009) Quantitative evaluation of enterococci, and Bacteroidales released by adults, and toddlers in marine water. Water Research 43, 4610-4616
46. Elmir S.M., Wright M.E., Solo-Gabriele H.M., Abdelzaher A., Fleming L.E., Miller G., Rybolowik M., Shih M.-T.P., 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, 3-10
47. Enns A.A., Vogel L.J., Abdelzaher A.M., Solo-Gabriele H.M., Plano L.R.W., Gidley M.L., Phillips M.C., Klaus J.S., Piggot A.M., Feng Z., Reniers A.J.H.M., Haus B.K., Elmir S.M., Zhang Y., Jimenez N.H., Abdel-Mottaleb N., Schoor M.E., Brown A., Khan S.Q., Dameron A.S., Salazar N.C., and Fleming L.E. (2012) Spatial, and temporal variation in indicator microbe sampling is influential in beach management decisions. Water Research 46, 2237-2246
48. Esiobu N., Mohammed R., Echeverry A., Green M., Bonilla T., Hartz A., McCorquodale D., and Rogerson A. (2004) The application of peptide nucleic acid probes for rapid detection, and enumeration of eubacteria, Staphylococcus aureus, and Pseudomonas aeruginosa in recreational beaches of S Florida. Journal of Microbiological Methods 57, 157-162
49. EU (2009) European Union FP6 Frame Work Virobathe Project reference 513648. Methods for the concentration, and detection of adenoviruses, and noroviruses in European bathing waters with reference to the revision of the Bathing Water Directive 76/160/EEC, accessible report. Brussels: European Union. http://cordis.europa.eu/publication/rcn/12840-en.html
50. EU 1976 Council Directive (1976) Council Directive of 8 December 1975 concerning the quality of bathing water (76/ 160/EEC) Brussels: European Communities
51. EU 2006 European Union (EU) (2006) Directive 2006/7/EC of the European Parliament, and of the Council of 15 February 2006 concerning the management of bathing water quality, and repealing directive 76/160/EEC. Official Journal of the European Union 64, 37-51
52. Feng Z., Reniers A., Haus B.K., and Solo-Gabriele H.M. (2013) Modeling sediment-related enterococci loading, transport, and inactivation at an embayed nonpoint source beach. Water Resources Research 49, 693-712
53. Finley R.L., Collignon P., Larsson D.G., McEwen S.A., Li X.Z., Gaze W.H., Reid-Smith R., Timinouni M., Graham D.W., and Topp E. (2013) The scourge of antibiotic resistance: the important role of the environment. Clinical Infectious Diseases 57, 704-710
54. Fleisher J.M., Fleming L.E., Solo-Gabriele H.M., Kish J.K., Sinigalliano C.D., Plano L.R.W., 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, 1291-1298
55. Fogarty L.R., Haack S.K., Wolcott M.J., and Whitman R.L. (2003) Abundance, and characteristics of the recreational water quality indicator bacteria Escherichia coli, and enterococci in gull faeces. Journal of Applied Microbiology 94, 865-878
56. Francino P.M. (2012) The ecology of bacterial genes, and the survival of the new. International Journal of Evolutionary Biology Art. ID 394026, 14 pages. http://dx.doi.org/10.1155/2012/394026
57. Fujioka R., and Shizumura L.K. (1985) Clostridium perfringens, a reliable indicator of stream water quality. Journal of the Water Pollution Control Federation 57, 986-992
58. Ge Z., Nevers M.B., Schwab D.J., and Whitman R.L. (2010) Coastal loading, and transport of Escherichia coli at an embayed beach in Lake Michigan. Environmental Science & Technology 44, 6731-6737
59. Gomes D.N.F., Cavalcanti M.A.Q., Fernandes M.J.S., Lima D.M.M., and Passavante J.Z.O. (2008) Filamentous fungi isolated from sand, and water of Bairro Novo, and Casa Caiada beaches. Brazilian Journal of Biology 68, 577-582
60. Gonzales M., Hanlin T.R., Herrera T., and Ulloa M. (2000) Fungi colonizing hair-bats from three coastal beaches of Mexico. Mycoscience 41, 259-262
61. Gooch-Moore J., Goodwin K., Doresey C., Ellender R., Mott J., Ornelas M., Sinigalliano C., Vincent B., Whiting D., and Wolfe S. (2011) New USEPA Water Quality criteria 2012. GOMA concerns, and recommendations. Journal of Water, and Health 9, 718-733
62. Halliday E., and Gast R.J. (2011) Bacteria in beach sands: an emerging challenge in protecting coastal water quality, and bather health. Environmental Science & Technology 45, 370-379
63. Halliday E., McLellan S.L., Amaral-Zettler L.A., Sogin M.L., and Gast R.J. (2014) Comparison of bacterial communities in sands, and water at beaches with bacterial water quality violations. PLoS ONE 9, e90815. doi: 10.1371/journal.pone.0090815
64. Harwood V.J., Staley C., Badgley B.D., Borges K., and Korajkic A. (2014) Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens, and human health outcomes. FEMS Microbiology Review 38, 1-40
65. Havelaar A.H., Van Olphen M., and Drost Y.C. (1993) F-specific RNA-bacteriophages are adequate model organisms for enteric viruses in fresh water. Applied, and Environmental Microbiology 59, 2956-2962
66. Health Canada (2012) Guidelines for Canadian Recreational Water Quality. 3rd edition. Ottawa: Water, Air, and Climate Change Bureau, Healthy Environments, and Consumer Safety Branch, Health Canada. (Catalogue No H129-15/2012E) http://www.hc-sc. gc.ca/ewh-semt/pubs/water-eau/guide-water-2012-guide-eau/indexeng. php#a9
67. 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) Faecal indicators in sand, sand contact, and risk of enteric illness among beachgoers. Epidemiology 23, 95-106
68. Heaney C., Sams E., Wing S., Marshall S., Brenner K., Dufour A.P., and Wade T.J. (2009) Contact with beach sand among beachgoers, and risk of illness. American Journal of Epidemiology 170, 164-172
69. Heikens E., Van Schaik W., Leavis H.L., Bonten M.J., and Willems R.J. (2008) Identification of a novel genomic island specific to hospitalacquired clonal complex 17 Enterococcus faecium isolates. Applied, and Environmental Microbiology 74, 7094-7097
70. Heim S., Del Mar Lleo M., Bonato B., Guzman C.A., and Canepari P. (2002) The viable but nonculturable state, and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. Journal of Bacteriology 184, 6739-6745
71. Hernandez R.J., Hernandez Y., Jimenez N.H., Piggot A.M., Klaus J.S., Feng Z., Reniers A., and Solo-Gabriele H.M. (2014) Effect of full-scale beach renovation on fecal indicator levels in shoreline sand, and water. Water Research 48, 579-591
72. Imamura G.J., Boehm A.B., Thompson R.S., and Jay J.A. (2011) Wrack promotes the persistence of fecal indicator bacteria in marine sands, and seawater. FEMS Microbiology Ecology 77, 40-49
73. Ishii S., Hansen D.L., Hicks R.E., and Sadowsky M.J. (2007) Beach sand, and sediments are temporal sinks, and sources of Escherichia coli in Lake Superior. Environmental Science & Technology 41, 2203-2209
74. Ishii S.T., Yan T., Shively D.A., Byappanahalli M.N., Whitman R.L., and Sadowsky M.J. (2006) Cladophora (Chlorophyta) spp. harbor human bacterial pathogens in nearshore water of Lake Michigan. Applied, and Environmental Microbiology 72, 4545-4553
75. International Organization for Standardization, and the International Electrotechnical Commission (ISO/IEC) (2005) 17025, General requirements for the competence of testing, and calibration laboratories, 2nd edn, 12 May 2005. ISBN : 0 580 34929 2
76. IWA (2011) Declaration adopted by a joint meeting of the International Water Association Health Related Microbiology, and Diffuse Pollution held at Rotorua, New Zealand, September. http://www.iwamicrobiology. org/uploadedFiles/Website-IWA-Microbiology/Newsletter/HRWM-Newsletter-February-2012
77. Jiang L., Hu X., Yin D., Zhang H., and Yu Z. (2011) Occurrence, distribution, and seasonal variation of antibiotics in the Huangpu River, Shanghai, China. Chemosphere 82, 822-828
78. Kaštelan M., Utješinović-Gudelj V., Prpić-Massari L., and Brajac I. (2014) Dermatophyte infections in Primorsko-Goranska County, Croatia: a 21 year survey. Acta Dermatovenerologica Croatica 22, 175-179
79. Kay D. (2015) Centre for Research into Environment, and Health, Aberystwyth University, UK. http://cadair.aber.ac.uk/dspace/handle/2160/12683?locale-attribute=cy. Last Accessed 18 March 2015
80. Kay D., Wyer M.D., Crowther J., and Fewtrell L. (1999) Faecal indicator impacts on recreational waters: budget studies, and diffuse source modeling. Journal of Applied Microbiology Symposium Supplement 85, 70S-82S.
81. Khiyama H.M., and Makemson J.C. (1973) Sand beach bacteria: enumeration, and characterization. Applied, and Environmental Microbiology 26, 293-297
82. Kinzelman J., and McLellan S. (2009) Success of science-based management practices in reducing swimming bans: a case study from Racine, WI, USA. Aquatic Ecosystems, and Health Management 12, 187-196
83. Kinzelman J., McLellan S., Daniels A., Cashin S., Singh A., Gradus S., and Bagley R. (2004) Non-point source pollution: determination of replication versus persistence of Escherichia coli in surface water, and sediments with correlation of levels to readily measurable environmental parameters. Journal of Water, and Health 2, 103-114
84. Kinzelman J.L., Whitman R.L., Byappanahalli M., Jackson E., and Bagley R.C. (2003) Evaluation of beach grooming techniques on Escherichia coli density in foreshore sand. Lake, and Reservoir Management 19, 349-354
85. Larrondo J.V., and Calvo M.A. (1989) Fungal density in the sands of the Mediterranean coast beaches. Mycopathologia 108, 185-193
86. 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. doi: 10.1016/j.envint.2015.02.013. [Epub ahead of print]
87. Lévesque B., Brousseau P., Simard P., Dewailly E., Meisels M., Ramsay D., and Joly J. (1993) Impact of the ring-billed gull (Larus delawarensis) on the microbiological quality of recreational water. Applied, and Environmental Microbiology 59, 1228-1230
88. Lleò M., Bonato B., Benedetti D., and Canepari P. (2005) Survival of enterococcal species in aquatic environments. FEMS Microbiology Ecology 54, 189-196
89. Lozupone C.A., and Knight R. (2007) Global patterns in bacterial diversity. Proceeding of the National Academy of Sciences USA 104, 11436-11440
90. Lu J., Hodon R., Hill S., Schoen M., Ashbolt N., Edge T.A., and Santo Domingo J. (2011) Distribution, and potential significance of a gull fecal marker in urban coastal, and riverine areas of southern Ontario, Canada. Water Research 45, 3960-3968
91. Luther K., and Fujioka R. (2004) Usefulness of monitoring tropical streams for male-specific RNA coliphages. Journal of Water, and Health 2, 171-181
92. Marzol M.V., Yanes A., Romero C., Brito De Azevedo E., Prada S., and Martins A. (2006a) Los riesgos De las lluvias torrenciales en las islas De la Macaronesia (Azores, Madeira, Canarias y Cabo Verde) In Cuadrat Prats J.M., Saz Sa'nchez M.A., Vicente Serrano S.M., Lanjeri S., De Luis Arrillaga M., and Gonza'lez-Hidalgo J.C. (eds) Clima, Sociedad y Medio Ambiente. Publicaciones De la Asociacio'n Española De Climatologi'a, Serie A, pp. 443-452
93. Marzol M.V., Yanes A., Romero C., Brito De Azevedo E., Prada S., and Martins A. (2006b) Caracte'ristiques des pre'cipitacions dans les îles De la Macaronesia (Ac?ores, Made're, Canaries et Cap Vert) Les Risques Liés au Temps et au climat. XIX Colloque De l'Association International De Climatologie (AIC), E' pernay, 415-420
94. McMinn B.R., Korajkic A., and Ashbolt N.J. (2014) Evaluation of Bacteroides fragilis GB-124 bacteriophages as novel human-associated faecal indicators in the United States. Letters in Applied Microbiology 59, 115-121
95. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., and Tauxe R.V. (1999) Food-related illness, and death in the United States. Emerging Infectious Diseases 5, 607
96. Migahed F. (2003) Distribution of fungi in the sandy soil of Egyptian beaches. Mycobiology 31, 61-67
97. Mortensen K.L., Mellado E., Lass-Florl C., Rodriguez-Tudela J.L., Johansen H.K., and Arendrup M.C. (2010) Environmental study of azole-resistant Aspergillus fumigatus, and other aspergilli in Austria, Denmark, and Spain. Antimicrobial Agents, and Chemotherapy 54, 4545-4549
98. Mudryk Z.J., Kosiorek A., and Perlinski P. (2013) In vitro antibiotic resistance of Vibrio-like organisms isolated from seawater, and sand of marine recreation beach in the southern Baltic Sea. Hydrobiologia 702, 141-150
99. NAS U.S. National Academy of Science (1972) Water Quality Criteria 1972, a report of the committee on water quality criteria, 549, National Academy of Sciences, National Technical Advisory Committee, Federal Water Pollution Administration, Department of the Interior, Washington DC.
100. Olapade O.A., Depas M.M., Jensen E.T., and McLellan S.L. (2006) Microbial communities, and faecal indicator bacteria associated with Cladophora mats on beach sites along Lake Michigan shores. Applied, and Environmental Microbiology 72, 1932-1938
101. Orozco A.S., Higginbotham L.M., Hitchcock C.A., Parkinson T., Falconer D., Ibrahim A.S., Ghannoum M.A., and Filler S.G. (1998) Mechanism of fluconazole resistance in Candida krusei. Antimicrobial Agents, and Chemotherapy 42, 2645-2649
102. Papadakis J.A., Mavridou A., Richardson S.C., Lampiri M., and Marcelou U. (1997) Bather-related microbial, and yeast populations in sand, and seawater. Water Research 31, 799-804
103. Pennak R.W. (1951) Comparative ecology of the interstitial fauna of fresh-water, and marine beaches. Annals of Biology 27, 449-480
104. Pereira E., Figueira C., Aguiar N., Vasconcelos R., Vasconcelos S., Silva M.G., Brandao J., and Prada S. (2013) Microbiological, and mycological beach sand quality in a volcanic environment: Madeira archipelago, Portugal. Science of the Total Environment 461-462, 469-479
105. Pfaller M.A., Moet G.J., Messer S.A., Jones R.N., and Castanheira M. (2011) Geographic variations in species distribution, and echinocandin, and azole antifungal resistance rates among Candida bloodstream infection isolates: report from the SENTRY Antimicrobial Surveillance Program (2008 to 2009) Journal of Clinical Microbiology 49, 396-399. doi: 10.1128/JCM.01398-10. pmid: 21068282
106. Phillips M.C., Feng Z., Vogel L.J., Reniers A.J.H.M., Haus B.K., Enns A.A., Zhang Y., Hernandez D.B., and Solo-Gabriele H.M. (2014) Microbial release from seeded beach sediments during wave conditions. Marine Pollution Bulletin 79, 114-122
107. Phillips M.C., Solo-Gabriele H.M., Piggot A.M., Klaus J.S., and Zhang Y. (2011a) Relationships between sand, and water quality at recreational beaches. Water Research 45, 6763-6769
108. Phillips M.C., Solo-Gabriele H.M., Reniers A.J.H.M., Wang J.D., Kiger R.T., and Abdel-Mottaleb N. (2011b) Pore water transport of enterococci out of beach sediments. Marine Pollution Bulletin 62, 2293-2298
109. Piggot A.M., Klaus J.S., Johnson S., Phillips M.C., and Solo-Gabriele H.M. (2012) Relationship between enterococcal levels, and sediment biofilms at recreational beaches in South Florida. Applied, and Environmental Microbiology 78, 5973-5982
110. Pinto K., Hachich E., Sato M., Di Bari M., Coelho M., Matté M., Lamparelli C., and Razzolini M. (2012a) Microbiological quality assessment of sand, and water from three selected beaches of South Coast, São Paulo State, Brazil. Water Science, and Technology 66, 2475-2482
111. Pinto D., Ruivo M., Vandamme P., and Lopes M.F.S. (2012b) Hospital-adapted clonal complex 17 Enterococcus faecium found among sand enterococcal isolates. Journal of Environmental Protection 3, 74-82
112. Plano L.R.W., 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, 1-10
113. Plano L.R.W., Shibata T., Garza A.C., Kish J., Fleisher J., Sinigalliano C.D., Gidley M.L., Withum K., Elmir S.M., Hower S., Jackson C.R., Barrett J.B., Cleary T., Davidson M., Davis J., Mukherjee S., Fleming L.E., and Solo-Gabriele H.M. (2013) Human-associated methicillin-resistant Staphylococcus aureus from a subtropical recreational marine beach. Microbial Ecology 65, 1039-1051
114. Rees R.J., Pinner W.R., Hajjeh A.R., Brandt E.M., and Reingold L.A. (1998) The epidemiological features of invasive mycotic infections in the San Francisco Bay Area, 1992-1993: results of population-based laboratory active surveillance. Clinical Infectious Diseases 27, 1138-1147
115. Roberts M.C., Olusegun O.S., and No D. (2013) Comparison of multidrug resistant environmental methicillin-resistant Staphylococcus aureus isolated from recreational beaches, and high touch surfaces in built environments. Frontiers in Microbiology 4, 1-8
116. Roll B.M., and Fujioka R.S. (1997) Sources of faecal indicator bacteria in a brackish, tropical stream, and their impact on recreational water quality. Water Science, and Technology 35, 179-186
117. Russell T.L., Sassoubre L.M., Wang D., Masuda S., Chen H., Soetjipto C., Hassaballah A., and Boehm A.B. (2013) A coupled modeling, and molecular biology approach to microbial source tracking at Cowell Beach, Santa Cruz, CA, United States. Environmental Science & Technology 47, 10231-10239
118. Sabino R., Rodrigues R., Costa I., Carneiro C., Cunha M., Duarte A., Faria N., Ferreira F.C., Gargaté M.J., Júlio C., Martins M.L., Nevers M.B., Oleastro M., Solo-Gabriele H., Veríssimo C., Viegas C., Whitman R.L., and Brandão J. (2014a) Routine screening of harmful microorganisms in beach sands: implications to public health. Science of the Total Environment 472, 1062-1069
119. Sabino R., Veríssimo C., Cunha M.A., Wergikoski B., Ferreira F.C., Rodrigues R., Parada H., Falcão L., Rosado L., Pinheiro C., Paixão E., and Brandão J. (2011) Pathogenic fungi: an unacknowledged risk at coastal resorts?. New insights on microbiological sand quality in Portugal. Marine Pollution Bulletin 62, 1506-1511
120. Sabino R., Veríssimo C., Parada H., Brandão J., Viegas C., Carolino E., Clemons K.V., and Stevens D.A. (2014b) Molecular screening of 246 Portuguese Aspergillus isolates among different clinical, and environmental sources. Medical Mycology 52, 519-529
121. Santiago-Rodriguez T.M., Marcos P., Monteiro S., Urdaneta M., Santos R., and Toranzos G.A. (2013) Evaluation of Enterococcus-infecting phages as indices of fecal pollution. Journal of Water, and Health 11, 51-63
122. Shah A., Abdelzaher A., Phillips M., Hernandez R., Solo-Gabriele H., Kish J., Scorzetti G., Fell J., Diaz M., Scott T., Lukasik J., Harwood V., McQuaig S., Sinigalliano C., Gidley M., Wanless D., Ager A., Lui J., Stewart J., Plano L., and Fleming L. (2011) Indicator microbes correlate with pathogenic bacteria, yeasts, and helminthes in sand at a subtropical recreational beach site. Journal of Applied Microbiology 110, 1571-1583
123. Shibata T., and Solo-Gabriele H. (2012) Quantitative microbial risk assessment of human illness from exposure to marine beach sand. Environmental Science & Technology 46, 2799-2805
124. Shibata T., Solo-Gabriele H.M., Fleming L., and Elmir S. (2004) Monitoring marine recreational water quality using multiple microbial indicators in an urban tropical environment. Water Research 38, 3119-3131
125. Sinigalliano C.D., Fleisher J.M., Gidley M.L., Solo-Gabriele H.M., Shibata T., Plano L.R.W., Elmir S.M., Wanless D., Bartkowiak J., Boiteau R., Withum K., Abdelzaher A.M., He G., Ortega C., Zhu X., Wright M.E., Kish J., Hollenbeck J., Scott T., Backer L.C., and Fleming L.E. (2010) Traditional, and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters. Water Research 44, 3763-3772
126. Sipsas N.V., Lewis R.E., Tarrand J., Hachem R., Rolston K.V., Raad I.I., and Kontoyiannis D.P. (2009) Candidemia in patients with hematologic malignancies in the era of new antifungal agents (2001-2007): stable incidence but changing epidemiology of a still frequently lethal infection. Cancer 115, 4745-4752
127. Snelders E., Van Der Lee A.L.H., Kuijpers J., Rijs J.M.M.A., Varga J., Samson R.A., Mellado E., Donders A.R.T., Melchers W.J.G., and Verweij P.E. (2008) Emergence of azole resistance in Aspergillus fumigatus, and spread of a single resistance mechanism. PLoS Medicine 5, e219
128. Soller A., Bartrand T., Ashbolt N.J., Ravenscroft J., and Wade T.J. (2010) Estimating the primary aetiologic agents in freshwater recreational waters impacted by human sources of faecal contamination. Water Research 44, 4473-4747
129. Soller J.A., Schoen M.E., Varghese A., Ichida A.M., Boehm A.B., Eftim S., Ashbolt N.J., and Ravenscroft J.E. (2014) Human health risk implications of multiple sources of faecal indicator bacteria in a recreational waterbody. Water Research 66, 254-264
130. Solo-Gabriele H.M., Neumeister S.M., Dubon J.M., and Palmer C.J. (1998) Occurrence of Cryptosporidium oocysts, and Giardia cysts in water supplies of San Pedro Sula, Honduras. Pan American Journal of Public Health 4, 398-400
131. Staley C., Gould T.J., Wang P., Phillips J., Cotner J.B., and Sadowsky M.J. (2015) Species sorting, and seasonal dynamics primarily shape bacterial communities in the Upper Mississippi River. Science of the Total Environment 505, 435-445
132. Stoeckel D.M., and Harwood V.J. (2007) Performance, design, and analysis in microbial source tracking studies. Applied, and Environmental Microbiology 73, 2405-2415
133. Suzuki S., and Hoa P.T. (2012) Distribution of quinolones, sulfonamides, tetracyclines in aquatic environment, and antibiotic resistance in Indochina. Frontiers in Microbiology 3, 67
134. The Fungal Research Trust (2011) How common are fungal diseases?. London: Fungal Research Trust 20th Anniversary Meeting
135. USEPA (1976) Quality criteria for water. Washington, DC: U.S. Environmental Protection Agency. PB-263 943. USEPA (1986) Ambient water quality criteria for bacteria - 1986
136. Washington, DC: U.S. Environmental Protection Agency, Office of Research, and Development, Microbiology, and Toxicology Division, and Office of Water Regulations, and Standards, Criteria, and Standards Division. EPA 440/5-84-002
137. USEPA (2005) Microbial source tracking guide document. Washington, DC: Office of Research, and Development. EPA-600/R-05/064. 131
138. USEPA (2012) Recreational water criteria. Washington, DC: US Environmental Protection Agency Office of Water. 820-F-12-058
139. Velonakis E., Dimitriadi D., Papadogiannakis E., and Vatopoulos A. (2014) Present status of effect of microorganisms from sand beach on public health. Journal of Coastal Life Medicine 2, 746-756
140. Verweij P.E., Snelders E., Kema G.J.H., Mellado E., and Melchers W.J.G. (2009) Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use?. Lancet Infectious Diseases 9, 789-795
141. Vicente V., Attili-Angelis D., Pie M.R., Queiroz-Telles F., Cruz L.M., Najafzadeh M.J., De Hoog G.S., Zhao J., and Pizzirani-Kleiner A. (2008) Environmental isolation of black yeast-like fungi involved in human infection. Studies in Mycology 61, 137-144
142. Vital M., Hammes F., and Egli T. (2008) Escherichia coli 0157 can grow in natural freshwaters at low carbon concentrations. Environmental Microbiology 10, 2387-2396
143. Vogel C., Rogerson A., Schatz S., Laubach H., Tallman A., and Fell J. (2007) Prevalence of yeast in beach sand at three bathing beaches in South Florida. Water Research 41, 1915-1920
144. Wang X., Singh P., Gao Z., Zhang X., Johnson I.Z., and Wang G. (2014) Distribution, and diversity of planktonic fungi in the West Pacific warm pool. PLoS ONE 9. doi: 10.1371/journal.pone.0101523. PLoS One. 2014 Jul 3; 9 (7): e101523. doi: 10.1371/journal.pone.0101523.eCollection 2014
145. Ward C. (2009) Do seaweeds play a part in the survival and/or growth of faecal indicator organisms which could affect counts on bathing beaches in UK waters?. Millport Marine Station: University of London
146. Weidhaas J.L., Li X., and Harwood V.J. (2014) Microbial Source Tracking (MST) Microarray for Advanced Pathogen Detection, and Source Identification in Environmental Systems. American Society for Microbiology General Meeting. 17-20, May. Boston, MA.
147. Wellington E.M.H., Boxall A.B.A., Cross P., Feil E.J., William H.G., Hawkey P.M., Johnson-Rollings A.S., Jones D.L., Lee N.M., Otten W., Thomas C.M. andWilliams A.P. (2013) The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infectious Diseases 13, 155-165
148. Wheeler J.G., Sethi D., Cowden J.M., Wall P.G., Rodrigues L.C., Tompkins D.S., Hudson M.J., and Roderick P.J. (1999) Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. The Infectious Intestinal Disease Study Executive. British Medical Journal 318, 1046-1050
149. Whitman R., Harwood V.J., Edge T.A., Nevers M., Byappanahalli M., Vijayavel K., Brandão J., Sadowsky M.J., Alm E.W., Crowe A., Ferguson D., Zhongfu G., Halliday E., Kinzelman G., Kleinheinz G., Przybyla-Kelly K., Staley C., Staley Z., and Solo-Gabriele H.M. (2014) Microbes in beach sands: integrating environment, ecology, and public health. Reviews in Environmental Science, and Biotechnology13, 329-368
150. Whitman R.L., Horvath T.G., Goodrich M.L., Nevers M.B., Wolcott M.J., and Haack S.K. (2001) Characterization of E. coli levels at 63rd Street Beach; City of Chicago, and the Chicago Park District, Chicago. http://www.onsetcomp.com/files/63rdStreetBeachReport. pdf
151. Whitman R.L., and Nevers M.B. (2003) Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Applied, and Environmental Microbiology 69, 5555-5562
152. Whitman R.L., Nevers M.B., and Byappanahalli M.N. (2006a) Examination of the watershed-wide distribution of Escherichia coli along Southern Lake Michigan: an integrated approach. Applied, and Environmental Microbiology 72, 7301-7310
153. Whitman R., Przybyla-Kelly K., Shively D., Nevers M., and Byappanahalli M. (2009) Hand-mouth transfer, and potential for exposure to E. coli, and F+ coliphage in beach sand, Chicago, Illinois. Journal of Water, and Health 7, 623-629
154. Whitman R., Shively D., Pawlik H., Nevers M., and Byappanahalli M. (2003) Occurrence of Escherichia coli, and enterococci in Cladophora (Chlorophyta) in nearshore water, and beach sand of Lake Michigan. Applied, and Environmental Microbiology 69, 4714-4719
155. Whitman R.L., Shively D., Ting W., Tseng C., and Nevers M. (2006b) Seasonal persistence, and population characteristics of Escherichia coli, and enterococci in deep backshore sand of two freshwater beaches. Journal of Water Health 4, 313-320
156. WHO (1999) Health-based monitoring of recreational waters: the feasibility of a new approach (the 'Annapolis Protocol') Report WHO/SDE/ WSH99.1. Geneva: World Health Organization
157. WHO (2003) Guidelines for safe recreational water environments. Volume 1: Coastal, and fresh waters. Geneva: World Health Organization
158. WHO (2009) Addendum to the WHO Guidelines for safe recreational water environments, Volume 1, Coastal, and fresh waters. WHO/HSE/WSH/10.04. Geneva: World Health Organization
159. WHO 2014) Antimicrobial - resistance: global report on surveillance. Geneva: http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748-eng.pdf
160. Wright M.E., Solo-Gabriele H.M., Elmir S., and Fleming L.E. (2009) Microbial load from animal faeces at a recreational beach. Marine Pollution Bulletin 58, 1649-1656
161. Wright M., Abdelzaher A., Solo-Gabriele H., Elmir S., and Fleming L. (2011) The inter-tidal zone is the pathway of input of enterococci to a subtropical recreational marine beach. Water Science, and Technology 63, 542-549
162. Wyer M., Wyn-Jones P., Kay D., Au-Yeung H., Gironés S., López-Pila J., De Roda Husman A., Rutjes S., and Schneider O. (2012) Relationships between human adenoviruses, and faecal indicator organisms in European recreational waters. Water Research 46, 4139-4141
163. Yaguchi T., Horie Y., Tanaka R., Matsuzawa T., Ito J., and Nishimura K. (2007) Molecular phylogenetics of multiple genes on Aspergillus section Fumigati isolated from clinical specimens in Japan. Japanese Journal of Medical Mycology 48, 37-46
164. Yamahara K.M., Sassoubre L.M., Goodwin K.D., and Boehm A.B. (2012) Occurrence, and persistence of bacterial pathogens, and indicator organisms in beach sand along the California coast. Applied, and Environmental Microbiology 78, 1733-1745
165. Yamahara K., Walters S., and Boehm A. (2009) Growth of enterococci in unaltered, unseeded beach sands subject to tidal wetting. Applied, and Environmental Microbiology 75, 1517-1524
166. Yates M.V. (2007) Classical indicators in the 21st century - far, and beyond coliform. Water Environment Research 79, 279-286