This paper overviews several examples of important public health impacts by marine microbes and directs readers to the extensive literature germane to these maladies. These examples include three types of dinoflagellates (Gambierdiscus spp., Karenia brevis, and Alexandrium fundyense), BMAA-producing cyanobacteria, and infectious microbes. The dinoflagellates are responsible for ciguatera fish poisoning, neurotoxic shellfish poisoning, and paralytic shellfish poisoning, respectively, that have plagued coastal populations over time. Research interest on the potential for marine cyanobacteria to contribute BMAA into human food supplies has been derived by BMAA's discovery in cycad seeds and subsequent implication as the putative cause of amyotrophic lateral sclerosis/parkinsonism dementia complex among the Chamorro people of Guam. Recent UPLC/MS analyses indicate that recent reports that BMAA is prolifically distributed among marine cyanobacteria at high concentrations may be due to analyte misidentification in the analytical protocols being applied for BMAA. Common infectious microbes (including enterovirus, norovirus, Salmonella, Campylobacter, Shigella, Staphylococcus aureus, Cryptosporidium, and Giardia) cause gastrointestinal and skin-related illness. These microbes can be introduced from external human and animal sources, or they can be indigenous to the marine environment. 1. Introduction The health and welfare of humans residing in the coastal zone and in island communities are inextricably linked to the oceans and its foodwebs. The multitude of relationships between human societies and the oceans has led to many human dimensions of ocean issues and processes. The effects of climate change, pollution, population increases, and the myriad of anthropogenic effects attendant increasing population are all related in various ways to the microbial organisms that are at the base of marine ecosystems. In 2004, the National Science Foundation and the National Institutes of Environmental Health Sciences initiated collaborative funding of four centers for oceans and human health, and in the same year, the National Oceanic and Atmospheric Administration launched its Oceans and Human Health Initiative. One of the important accomplishments of these centers has been the cross-discipline synergistic collaboration of scientists within and between centers. This paper summarizes five areas of this research focusing on the oceans and human health. 2. Gambierdiscus spp. and Ciguatera Fish Poisoning Gambierdiscus spp., a genus of dinoflagellates (division Phyrophyta),
References
[1]
P. K. Bienfang, M. L. Parsons, R. R. Bidigare, E. A. Laws, and P. D. R. Moeller, “Ciguatera fish poisoning: a synopsis from ecology to toxicity,” in Oceans and Human Health: Risks and Remedies from the Sea, P. J. Walsh, S. L. Smith, L. E. Fleming, H. Solo-Gabriele, and W. H. Gerwick, Eds., pp. 257–270, Elsevier, New York, NY, USA, 2008.
[2]
R. W. Dickey, “Ciguatera toxins: chemistry, toxicology and detection,” in Seafood and Freshwater Toxins: Pharmacology, Physiology, and Detection, L. M. Botana, Ed., pp. 479–500, CRC Press, Boca Raton, Fla, USA; Taylor & Francis, London, UK, 2nd edition, 2008.
[3]
R. W. Dickey and S. M. Plakas, “Ciguatera: a public health perspective,” Toxicon, vol. 56, no. 2, pp. 123–136, 2010.
[4]
P. Helfrich, “Fish poisoning in Hawaii,” Hawaii Medical Journal, vol. 22, pp. 361–372, 1964.
[5]
B. W. Halstead, Poisonous and Venomous Marine Animals of the World, vol. 2, U. S. Government Printing Office, 1967.
[6]
J. P. Quod and J. Turquet, “Ciguatera in Reunion Island (SW Indian ocean): epidemiology and clinical patterns,” Toxicon, vol. 34, no. 7, pp. 779–785, 1996.
[7]
R. J. Lewis, “The changing face of ciguatera,” Toxicon, vol. 39, no. 1, pp. 97–106, 2001.
[8]
J. Pearn, “Neurology of ciguatera,” Journal of Neurology, vol. 70, no. 1, pp. 4–8, 2001.
[9]
P. Arena, B. Levin, L. E. Fleming, M. A. Friedman, and D. Blythe, “A pilot study of the cognitive and psychological correlates of chronic ciguatera poisoning,” Harmful Algae, vol. 3, no. 1, pp. 51–60, 2004.
[10]
N. D. Lewis, “Disease and development: coguatera fish poisoning,” Social Science and Medicine, vol. 23, no. 10, pp. 983–993, 1986.
[11]
W. R. Lange, “Ciguatera fish poisoning,” American Family Physician, vol. 50, no. 3, pp. 579–584, 1994.
[12]
L. E. Fleming, D. Katz, J. A. Bean, and R. Hammond, “Epidemiology of seafood poisoning,” in Foodborne Disease Handbook, Y. H. Hui, D. Kitts, and P. Standfield, Eds., pp. 287–310, 2001.
[13]
L. E. Fleming, D. G. Baden, J. A. Bean, R. Weisman, and D. G. Blythe, “Seafood toxin diseases: issues in epidemiology and community outreach,” in Harmful Algae. Zunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, B. Reguera, J. Blanco, M. L. Fernandez, and T. Wyatt, Eds., pp. 245–248, 1998.
[14]
J. Cameron, A. E. Flowers, and M. F. Capra, “Electrophysiological studies on ciguatera poisoning in man (Part II),” Journal of the Neurological Sciences, vol. 101, no. 1, pp. 93–97, 1991.
[15]
E. Benoit, P. Juzans, A. M. Legrand, and J. Molgo, “Reversal of Pacific ciguatoxin-1B effects on myelinated axons by agents used in ciguatera treatment,” Cybium, vol. 24, no. 3, pp. 33–40, 2000.
[16]
M. A. Friedman, L. E. Fleming, M. Fernandez et al., “Ciguatera fish poisoning: treatment, prevention and management,” Marine Drugs, vol. 6, no. 3, pp. 456–479, 2008.
[17]
T. Yasumoto, I. Nakajima, R. Bagnis, and R. Adachi, “Finding of a dinoflagellate as a likely culprit of ciguatera,” Bulletin of the Japanese Society for the Science of Fish, vol. 43, pp. 1021–1026, 1977.
[18]
T. Yasumoto, A. Inoue, and R. Bagnis, “Ecological survey of a toxic dinoflagellate associated with ciguatera,” in Toxic Dinoflagellate Blooms, D. L. Taylor and H. Seliger, Eds., pp. 221–224, Elsevier, New York, Ny, USA, 1979.
[19]
T. Yasumoto, Y. Oshima, Y. Murakami, I. Nakajima, R. Bagnis, and Y. Fukuyo, “Toxicity of benthic dinoflagellates,” Bulletin of the Japanese Society for the Science of Fish, vol. 46, pp. 327–331, 1980.
[20]
R. Adachi and Y. Fukuyo, “The thecal structure of a marine toxic dinoflagellate Gambierdiscus toxicus gen. et sp. nov. collected in a ciguatera endemic area,” Bulletin of the Japanese Society for the Science of Fish, vol. 45, pp. 67–71, 1979.
[21]
M. A. Faust, “Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species,” Journal of Phycology, vol. 31, no. 6, pp. 996–1003, 1995.
[22]
M. J. Holmes, “Gambierdiscus yasumotoi sp. nov. (Dinophyceae), a toxic benthic dinoflagellate from Southeastern Asia,” Journal of Phycology, vol. 34, no. 4, pp. 661–668, 1998.
[23]
M. Chinain, M. A. Faust, and S. Pauillac, “Morphology and molecular analyses of three toxic species of Gambierdiscus (Dinophyceae): G. pacificus, sp. nov., G. australes, sp. nov., and G. polynesiensis, sp. nov,” Journal of Phycology, vol. 35, no. 6, pp. 1282–1296, 1999.
[24]
M. L. Richlen, S. L. Morton, P. H. Barber, and P. S. Lobel, “Phylogeography, morphological variation and taxonomy of the toxic dinoflagellate Gambierdiscus toxicus (Dinophyceae),” Harmful Algae, vol. 7, no. 5, pp. 614–629, 2008.
[25]
R. W. Litaker, M. W. Vandersea, M. A. Faust et al., “Taxonomy of Gambierdiscus including four new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales, Dinophyceae),” Phycologia, vol. 48, no. 5, pp. 344–390, 2009.
[26]
K. A. Steidinger and D. G. Baden, “Toxic marine dinoflagellates,” in Dinoflagellates, D. L. Spector, Ed., pp. 210–261, Academic Press, Orlando, Fla, USA, 1985.
[27]
H. Kite-Powell, “Public health and economic implications of oceans and human health research,” in Proceedings of Oceans and Human Health Symposium & Workshop, Washington, DC, USA, April 2010.
[28]
M.-L. Chateau-Degat, M. Chinain, N. Cerf, S. Gingras, B. Hubert, and é. Dewailly, “Seawater temperature, Gambierdiscus spp. variability and incidence of ciguatera poisoning in French Polynesia,” Harmful Algae, vol. 4, no. 6, pp. 1053–1062, 2005.
[29]
J. L. Perez-Arellano, O. P. Luzardo, A. Perez Brito, et al., “First report of ciguatera fish poisoning in West-African coast: a public health concern in the Canary Islands (Spain),” Emerging Infectious Diseases, vol. 11, pp. 1981–1982, 2005.
[30]
T. A. Villareal, S. Hanson, S. Qualia, E. L. E. Jester, H. R. Granade, and R. W. Dickey, “Petroleum production platforms as sites for the expansion of ciguatera in the northwestern Gulf of Mexico,” Harmful Algae, vol. 6, no. 2, pp. 253–259, 2007.
[31]
P. Bienfang, B. Oben, S. Defelice et al., “Ciguatera: the detection of neurotoxins in carnivorous reef fish from the coast of Cameroon, West Africa,” African Journal of Marine Science, vol. 30, no. 3, pp. 533–540, 2008.
[32]
P. A. Tester and K. A. Steidinger, “Gymnodinium breve red tide blooms: initiation, transport, and consequences of surface circulation,” Limnology and Oceanography, vol. 42, no. 5, pp. 1039–1051, 1998.
[33]
K. M. Kusek, G. Vargo, and K. Steidinger, “Gymnodinium breve in the field, in the lab, and in the newspaper—a scientific and journalistic analysis of Florida red tides,” Contributions in Marine Science, vol. 34, pp. 1–229, 1999.
[34]
C. C. Davis, “Gymnodinium brevis sp. nov., a cause of discolored water and animal mortality in the Gulf of Mexico,” Botany Gaz, vol. 109, pp. 358–360, 1948.
[35]
C. A. Heil, Vertical migration of ptychodiscus brevis (Davis) steidinger, M.S. thesis, University of South Florida, St. Petersburg, Fla, USA, 1986.
[36]
D. Kamykowski, E. J. Milligan, and R. E. Reed, “Relationships between geotaxis/phototaxis and diei vertical migration in autotrophic dinoflagellates,” Journal of Plankton Research, vol. 20, no. 9, pp. 1781–1796, 1998.
[37]
K. A. Steidinger, G. A. Vargo, P. A. Tester, and C. R. Tomas, “Bloom dynamics and physiology of Gymnodinium breve with emphasis on the Gulf of Mexic,” in Physiological Ecology of Harmful Algal Blooms, D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff, Eds., pp. 133–153, Springer, Heidelberg, Germany, 1998.
[38]
K. A. Steidinger, “Implications of dinoflagellate life cycles on initiation of Gymnodinium breve red tides,” Environmental Letters, vol. 9, no. 2, pp. 129–139, 1975.
[39]
M. Geesey and P. A. Tester, “Gymnodinium breve: ubiquitous in Gulf of Mexico waters,” in Toxic Phytoplankton Blooms in the Sea, T. J. Smayda and Y. Shimizu, Eds., pp. 251–255, Elsevier, New York, NY, USA, 1993.
[40]
L. E. Brand and A. Compton, “Long-term increase in Karenia brevis abundance along the Southwest Florida Coast,” Harmful Algae, vol. 6, no. 2, pp. 232–252, 2007.
[41]
P. A. Tester, R. P. Stumpf, F. M. Vukovich, P. K. Fowler, and J. T. Turner, “An expatriate red tide bloom: transport, distribution, and persistence,” Limnology & Oceanography, vol. 36, no. 5, pp. 1053–1061, 1991.
[42]
M. J. Olascoaga, I. I. Rypina, M. G. Brown et al., “Persistent transport barrier on the West Florida Shelf,” Geophysical Research Letters, vol. 33, no. 22, Article ID L22603, 2006.
[43]
G. Gunter, R. H. Williams, C. C. Davis, and F. G. Walton Smith, “Catastrophic mass mortality of marine animals and coincident phytoplankton bloom on the west coast of Florida, November 1946-August 1947,” Ecological Monographs, vol. 18, pp. 309–324, 1947.
[44]
G. A. Rounsefell and W. R. Nelson, “Red-tide research summarized to 1964 including an annotated bibliography,” U.S. Fish and Wildlife. Service Special Scientific Report—Fisheries, no. 535, p. 85, 1966.
[45]
L. K. Dixon and K. A. Steidinger, “Correlation of Karenia brevis presence in the eastern Gulf of Mexico and with rainfall and riverine flow,” in Harmful Algae, K. A. Steidinger, J. H. Landsberg, C. R. Tomas, and G. A. Vargo, Eds., pp. 29–31, 2004.
[46]
J. M. Lenes, B. P. Darrow, C. Cattrall et al., “Iron fertilization and the Trichodesmium response on the West Florida shelf,” Limnology and Oceanography, vol. 46, no. 6, pp. 1261–1277, 2001.
[47]
J. J. Walsh and K. A. Steidinger, “Saharan dust and Florida red tides: the cyanophyte connection,” Journal of Geophysical Research C: Oceans, vol. 106, no. 6, pp. 11.597–11.612, 2001.
[48]
J. J. Walsh, J. K. Jolliff, B. P. Darrow et al., “Red tides in the Gulf of Mexico: where, when, and why?” Journal of Geophysical Research C: Oceans, vol. 111, no. 11, Article ID C11003, 2006.
[49]
C. Hu, F. E. Muller-Karger, and P. W. Swarzenski, “Hurricanes, submarine groundwater discharge, and Florida's red tides,” Geophysical Research Letters, vol. 33, no. 11, Article ID L11601, 2006.
[50]
G. A. Vargo, C. A. Heil, K. A. Fanning et al., “Nutrient availability in support of Karenia brevis blooms on the central West Florida Shelf: what keeps Karenia blooming?” Continental Shelf Research, vol. 28, no. 1, pp. 73–98, 2008.
[51]
D. G. Baden, A. J. Bourdelais, H. Jacocks, S. Michelliza, and J. Naar, “Natural and derivative brevetoxins: historical background, multiplicity, and effects,” Environmental Health Perspectives, vol. 113, no. 5, pp. 621–625, 2005.
[52]
J. H. Landsberg, “The effects of harmful algal blooms on aquatic organisms,” Reviews in Fisheries Science, vol. 10, no. 2, pp. 113–390, 2002.
[53]
S. M. Watkins, A. Reich, L. E. Fleming, and R. Hammond, “Neurotoxic shellfish poisoning,” Marine Drugs, vol. 6, no. 3, pp. 431–455, 2008.
[54]
P. A. Tester, J. T. Turner, and D. Shea, “Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish,” Journal of Plankton Research, vol. 22, no. 1, pp. 47–61, 2000.
[55]
L. J. Flewelling, J. P. Naar, J. P. Abbott et al., “Brevetoxicosis: red tides and marine mammal mortalities,” Nature, vol. 435, no. 7043, pp. 755–756, 2005.
[56]
J. P. Naar, L. J. Flewelling, A. Lenzi et al., “Brevetoxins, like ciguatoxins, are potent ichthyotoxic neurotoxins that accumulate in fish,” Toxicon, vol. 50, no. 5, pp. 707–723, 2007.
[57]
L. C. Backer, L. E. Fleming, A. Rowan et al., “Recreational exposure to aerosolized brevetoxins during Florida red tide events,” Harmful Algae, vol. 2, no. 1, pp. 19–28, 2003.
[58]
B. Kirkpatrick, L. E. Fleming, D. Squicciarini et al., “Literature review of Florida red tide: implications for human health effects,” Harmful Algae, vol. 3, no. 2, pp. 99–115, 2004.
[59]
L. E. Fleming, L. C. Backer, and D. G. Baden, “Overview of aerosolized Florida red tide toxins: exposures and effects,” Environmental Health Perspectives, vol. 113, no. 5, pp. 618–620, 2005.
[60]
W. M. Abraham and D. G. Baden, “Aerosolized Florida red tide toxins and human health effects,” Oceanography, vol. 19, pp. 107–109, 2006.
[61]
B. Kirkpatrick, L. E. Fleming, L. C. Backer et al., “Environmental exposures to Florida red tides: effects on emergency room respiratory diagnoses admissions,” Harmful Algae, vol. 5, no. 5, pp. 526–533, 2006.
[62]
L. E. Fleming, B. Kirkpatrick, L. C. Backer et al., “Aerosolized red-tide toxins (brevetoxins) and asthma,” Chest, vol. 131, no. 1, pp. 187–194, 2007.
[63]
F. Alcock, “An assessment of Florida red tide,” Tech. Rep. 1190, Mote Marine Laboratory, Sarasota, Fla, USA, 2007.
[64]
M. Gantar and Z. Svir？ev, “Microalgae and cyanobacteria: food for thought,” Journal of Phycology, vol. 44, no. 2, pp. 260–268, 2008.
[65]
P. B. Nunn and P. O'Brien, “The interaction of β-N-methylamino-L-alanine with bicarbonate: an 1H-NMR study,” FEBS Letters, vol. 251, no. 1-2, pp. 31–35, 1989.
[66]
T. G. Myers and S. D. Nelson, “Neuroactive carbamate adducts of β-N-methylamino-L-alanine and ethylenediamine. Detection and quantitation under physiological conditions by 13C NMR,” Journal of Biological Chemistry, vol. 265, no. 18, pp. 10193–10195, 1990.
[67]
A. Vega and E. A. Bell, “α-amino-β-methylaminopropionic acid, a new amino acid from seeds of Cycas circinalis,” Phytochemistry, vol. 6, no. 5, pp. 759–762, 1967.
[68]
P. S. Spencer, P. B. Nunn, and J. Hugon, “Guam amyotrophic lateral sclerosis-Parkinsonism-dementia linked to a plant excitant neurotoxin,” Science, vol. 237, no. 4814, pp. 517–522, 1987.
[69]
U. Beckman Sundh, C. Andersson, J. Rosén, F. Fonnum, I. Knudsen, and S. Sippola, “Analysis, occurrence, and toxicity of -methylaminoalanine (BMAA): a risk for the consumer?” TemaNord, vol. 516, p. 128, 2007.
[70]
P. A. Cox, S. A. Banack, and S. J. Murch, “Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 23, pp. 13380–13383, 2003.
[71]
P. A. Cox, S. A. Banack, S. J. Murch et al., “Diverse taxa of cyanobacteria produce β-N-methylamino-L-alanine, a neurotoxic amino acid,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 14, pp. 5074–5078, 2005.
[72]
R. Rippka, J. Deruelles, J. B. Waterbury, M. Herdman, and R. Y. Stanier, “Generic assignments, strain histories and properties of pure cultures of cyanobacteria,” Journal of General Microbiology, vol. 111, no. 1, pp. 1–61, 1979.
[73]
B. M. Kuehn, “Environmental neurotoxin may pose health threat,” Journal of the American Medical Association, vol. 293, no. 20, pp. 2460–2462, 2005.
[74]
P. G. Ince and G. A. Codd, “Return of the cycad hypothesis—does the amyotrophic lateral sclerosis/parkinsonism dementia complex (ALS/PDC) of Guam have new implications for global health?” Neuropathology and Applied Neurobiology, vol. 31, no. 4, pp. 345–353, 2005.
[75]
M. Esterhuizen and T. G. Downing, “β-N-methylamino-l-alanine (BMAA) in novel South African cyanobacterial isolates,” Ecotoxicology and Environmental Safety, vol. 71, no. 2, pp. 309–313, 2008.
[76]
J. H. Weiss and D. W. Choi, “ -N-methylamino-L-alanine neurotoxicity: requirement for bicarbonate as a cofactor,” Science, vol. 241, no. 4868, pp. 973–975, 1988.
[77]
S. D. Rao, S. A. Banack, P. A. Cox, and J. H. Weiss, “BMAA selectively injures motor neurons via AMPA/kainate receptor activation,” Experimental Neurology, vol. 201, no. 1, pp. 244–252, 2006.
[78]
D. Lobner, P. M. T. Piana, A. K. Salous, and R. W. Peoples, “β-N-methylamino-l-alanine enhances neurotoxicity through multiple mechanisms,” Neurobiology of Disease, vol. 25, no. 2, pp. 360–366, 2007.
[79]
R. R. Bidigare, S. J. Christensen, S. B. Wilde, and S. A. Banack, “Cyanobacteria and BMAA: possible linkage with avian vacuolar myelinopathy (AVM) in the south-eastern United States,” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 71–73, 2009.
[80]
E. J. Faassen, F. Gillissen, H. A. J. Zweers, and M. Lrling, “Determination of the neurotoxins BMAA (β-N-methylamino-L-alanine) and DAB (α-,γ-diaminobutyric acid) by LC-MSMS in Dutch urban waters with cyanobacterial blooms,” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 79–84, 2009.
[81]
H. E. Johnson, S. R. King, S. A. Banack, C. Webster, W. J. Callanaupa, and P. A. Cox, “Cyanobacteria (Nostoc commune) used as a dietary item in the Peruvian highlands produce the neurotoxic amino acid BMAA,” Journal of Ethnopharmacology, vol. 118, no. 1, pp. 159–165, 2008.
[82]
J. S. Metcalf, S. A. Banack, J. Lindsay, L. F. Morrison, P. A. Cox, and G. A. Codd, “Co-occurrence of β-N-methylamino-l-alanine, a neurotoxic amino acid with other cyanobacterial toxins in British waterbodies, 1990–2004,” Environmental Microbiology, vol. 10, no. 3, pp. 702–708, 2008.
[83]
T. A. Caller, J. W. Doolin, J. F. Haney et al., “A cluster of amyotrophic lateral sclerosis in New Hampshire: a possible role for toxic cyanobacteria blooms,” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 101–108, 2009.
[84]
P. A. Cox, R. Richer, J. S. Metcalf, S. A. Banack, G. A. Codd, and W. G. Bradley, “Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans,” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 109–117, 2009.
[85]
D. Craighead, J. S. Metcalf, S. A. Banack, L. Amgalan, H. V. Reynolds, and M. Batmunkh, “Presence of the neurotoxic amino acids β-N-methylamino-L-alanine (BMAA) and 2,4-diamino-butyric acid (DAB) in shallow springs from the Gobi Desert,” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 96–117, 2009.
[86]
B. R. Roney, L. Renhui, S. A. Banack, S. Murch, R. Honegger, and P. A. Cox, “Consumption of fa cai Nostoc soup: a Potential for BMAA exposure from Nostoc cyanobacteria in China?” Amyotrophic Lateral Sclerosis, vol. 10, supplement 2, pp. 44–49, 2009.
[87]
S. Jonasson, J. Eriksson, L. Berntzon et al., “Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 20, pp. 9252–9257, 2010.
[88]
Z. Spácil, J. Eriksson, S. Jonasson, U. Rasmussen, L. L. Ilag, and B. Bergman, “Analytical protocol for identification of BMAA and DAB in biological samples,” Analyst, vol. 135, no. 1, pp. 127–132, 2010.
[89]
P. M. Scott, B. Niedzwiadek, D. F. K. Rawnben, and P.-Y. Lau, “Liquid chromatographic determination of the cyanobacterial toxin β-N-methylamino-l-alanine in algae food supplements, freshwater fish, and bottled water,” Journal of Food Protection, vol. 72, no. 8, pp. 1769–1773, 2009.
[90]
T. Kubo, N. Kato, K. Hosoya, and K. Kaya, “Effective determination method for a cyanobacterial neurotoxin, β-N-methylamino-l-alanine,” Toxicon, vol. 51, no. 7, pp. 1264–1268, 2008.
[91]
J. Rosén and K.-E. Hellen？s, “Determination of the neurotoxin BMAA (β-N-methylamino-L-alanine) in cycad seed and cyanobacteria by LC-MS/MS (liquid chromatography tandem mass spectrometry),” Analyst, vol. 133, no. 12, pp. 1785–1789, 2008.
[92]
T. Krüger, B. M？nch, S. Oppenh？user, and B. Luckas, “LC-MS/MS determination of the isomeric neurotoxins BMAA (β-N-methylamino-l-alanine) and DAB (2,4-diaminobutyric acid) in cyanobacteria and seeds of Cycas revoluta and Lathyrus latifolius,” Toxicon, vol. 55, no. 2-3, pp. 547–557, 2010.
[93]
C. Y. Kao, “Paralytic shellfish poisoning,” in Algal Toxins in Seafood and Drinking Water, I. R. Falconer, Ed., pp. 75–86, Academic Press, London, UK, 1993.
[94]
A. Prakash, J. Medcof, and A. Tennant, Paralytic Shellfish Poisoning in Eastern Canada, Fisheries Research Board of Canada, no. 177, Fisheries Research Board of Canada, Ottawa, Canada, 1971.
[95]
D. M. Anderson, D. M. Kulis, Y.-Z. Qi, L. Zheng, S. Lu, and Y.-T. Lin, “Paralytic shellfish poisoning in Southern China,” Toxicon, vol. 34, no. 5, pp. 579–590, 1996.
[96]
M. E. E. Popkiss, D. A. Horstman, and D. Harpur, “Paralytic shellfish poisoning. A report of 17 cases in Cape Town,” South African Medical Journal, vol. 55, no. 25, pp. 1017–1023, 1979.
[97]
B. W. Halstead and E. Shantz, Paralytic Shellfish Poisoning, WHO Offset Publication, no. 79, World Health Organization, Geneva, Switzerland, 1984.
[98]
D. M. Anderson, B. A. Keafer, D. J. McGillicuddy et al., “Initial observations of the 2005 Alexandrium fundyense bloom in southern New England: general patterns and mechanisms,” Deep-Sea Research II, vol. 52, no. 19-21, pp. 2856–2876, 2005.
[99]
D. J. McGillicuddy Jr., D. M. Anderson, D. R. Lynch, and D. W. Townsend, “Mechanisms regulating large-scale seasonal fluctuations in Alexandrium fundyense populations in the Gulf of Maine: results from a physical-biological model,” Deep-Sea Research II, vol. 52, no. 19-21, pp. 2698–2714, 2005.
[100]
L. C. Backer and D. J. McGillicuddy, “Harmful Algal Blooms: at the interface between coastal oceanography and human health,” Oceanography, vol. 19, no. 2, pp. 94–106, 2006.
[101]
D. M. Anderson, J. J. Sullivan, and B. Reguera, “Paralytic shellfish poisoning in northwest Spain: the toxicity of the dinoflagellate Gymnodinium catenatum,” Toxicon, vol. 27, no. 6, pp. 665–674, 1989.
[102]
D. G. Baden, “Marine food-borne dinoflagellate toxins,” International Review of Cytology, vol. 82, pp. 99–150, 1983.
[103]
D. M. Anderson and D. Wall, “Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms,” Journal of Phycology, vol. 14, no. 2, pp. 224–234, 1978.
[104]
D. W. Townsend, N. R. Pettigrew, and A. C. Thomas, “Offshore blooms of the red tide dinoflagellate, Alexandrium sp., in the Gulf of Maine,” Continental Shelf Research, vol. 21, no. 4, pp. 347–369, 2001.
[105]
P. J. S. Franks and D. M. Anderson, “Toxic phytoplankton blooms in the southwestern Gulf of Maine: testing hypotheses of physical control using historical data,” Marine Biology, vol. 112, no. 1, pp. 165–174, 1992.
[106]
R. M. Luerssen, A. C. Thomas, and J. Hurst, “Relationships between satellite-measured thermal features and Alexandrium-imposed toxicity in the Gulf of Maine,” Deep-Sea Research II, vol. 52, no. 19–21, pp. 2656–2673, 2005.
[107]
C. A. Stock, D. J. McGillicuddy, A. R. Solow, and D. M. Anderson, “Evaluating hypotheses for the initiation and development of Alexandrium fundyense blooms in the western Gulf of Maine using a coupled physical-biological model,” Deep-Sea Research II, vol. 52, no. 19-21, pp. 2715–2744, 2005.
[108]
C. A. Stock, D. J. McGillicuddy Jr., D. M. Anderson, A. M. Solow, and R. P. Signell, “Blooms of the toxic dinoflagellate Alexandrium fundyense in the western Gulf of Maine in 1993 and 1994: a comparative modeling study,” Continental Shelf Research, vol. 27, no. 19, pp. 2486–2512, 2007.
[109]
R. He and D. J. McGillicuddy Jr., “Historic 2005 toxic bloom of Alexandrium fundyense in the west Gulf of Maine: 1. In situ observations of coastal hydrography and circulation,” Journal of Geophysical Research C: Oceans, vol. 113, no. 7, Article ID C07039, 2008.
[110]
R. He, D. J. McGillicuddy Jr., B. A. Keafer, and D. M. Anderson, “Historic 2005 toxic bloom of Alexandrium fundyense in the western Gulf of Maine: 2. Coupled biophysical numerical modeling,” Journal of Geophysical Research C: Oceans, vol. 113, no. 7, Article ID C07040, 2008.
[111]
J. Zaias, L. C. Backer, and L. E. Fleming, “Harmful algal blooms (HABs),” in Human-Animal Medicine: A Clinical Guide to Toxins, Zoonoses, and Other Shared Health Risks, P. Rabinowitz and L. Conti, Eds., pp. 91–104, Elsevier Science, New York, NY, USA, 2010.
[112]
C. N. Haas, J. B. Rose, and C. P. Gerba, Quantitative Microbial Risk Assessment, John Wiley & Sons, New York, NY, USA, 1999.
[113]
L. C. Backer, J. K. Kish, H. M. Solo-Gabriele, and L. E. Fleming, “Naturally-occurring water pollutants,” in Water and Sanitation Related Diseases and the Environment: Challenges, Interventions and Preventive Measures, J. Selendy, Ed., Horizon International, Yale University, 2010.
[114]
H. Shuval, “Estimating the global burden of thalassogenic diseases: human infectious diseases caused by wastewater pollution of the marine environment,” Journal of Water and Health, vol. 1, no. 2, pp. 53–64, 2003.
[115]
National Research Defense Council (NRDC), “NRDC testing the waters,” 2009, http://www.nrdc.org/water/oceans/ttw/titinx.asp.
[116]
U.S. Food and Drug Administration (U.S. FDA), “National Shellfish Registry,” U.S. Food and Drug Administration and the Interstate Shellfish Sanitation Conference, The National Shellfish Register, 1995, http://seaserver.nos.noaa.gov/projects/95register.
[117]
S. Given, L. H. Pendleton, and A. B. Boehm, “Regional public health cost estimates of contaminated coastal waters: a case study of gastroenteritis at southern California beaches,” Environmental Science and Technology, vol. 40, no. 16, pp. 4851–4858, 2006.
[118]
J. S. Yoder, M. C. Hlavsa, G. F. Craun, et al., “Surveillance for waterborne disease and outbreaks assoicated with recreational water use and other aquatic facility-associated health events—United States, 2005-2006,” Morbidity and Mortality Weekly Report, vol. 58, no. 57/SS-9, pp. 1–38, 2008.
[119]
M. Iwamoto, T. Ayers, B. E. Mahon, and D. L. Swerdlow, “Epidemiology of seafood-associated infections in the United States,” Clinical Microbiology Reviews, vol. 23, no. 2, pp. 399–411, 2010.
[120]
S. Nithiuthai, M. T. Anantaphruti, J. Waikagul, and A. Gajadhar, “Waterborne zoonotic helminthiases,” Veterinary Parasitology, vol. 126, no. 1-2, pp. 167–193, 2004.
[121]
C. D. Heaney, E. Sams, S. Wing et al., “Contact with beach sand among beachgoers and risk of illness,” American Journal of Epidemiology, vol. 170, no. 2, pp. 164–172, 2009.
[122]
I. Paquet-Durand, J. Hernández, G. Dolz, J. J. R. Zu？iga, T. Schnieder, and C. Epe, “Prevalence of Toxocara spp., Toxascaris leonina and ancylostomidae in public parks and beaches in different climate zones of Costa Rica,” Acta Tropica, vol. 104, no. 1, pp. 30–37, 2007.
[123]
C. Vogel, A. Rogerson, S. Schatz, H. Laubach, A. Tallman, and J. Fell, “Prevalence of yeasts in beach sand at three bathing beaches in South Florida,” Water Research, vol. 41, no. 9, pp. 1915–1920, 2007.
[124]
L. C. Backer, J. K. Kish, H. M. Solo-Gabriele, and L. E. Fleming, “Naturally-occurring water pollutants,” in Water and Sanitation Related Diseases and the Environment: Challenges, Interventions and Preventive Measures, J. Selendy, Ed., John Wiley & Sons, New York, NY, USA, 2010.
[125]
D. W. Griffin, K. A. Donaldson, J. H. Paul, and J. B. Rose, “Pathogenic human viruses in coastal waters,” Clinical Microbiology Reviews, vol. 16, no. 1, pp. 129–143, 2003.
[126]
S. E. Henrickson, T. Wong, P. Allen, T. Ford, and P. R. Epstein, “Marine swimming-related illness: implications for monitoring and environmental policy,” Environmental Health Perspectives, vol. 109, no. 7, pp. 645–650, 2001.
[127]
R. Girones, S. Bofill-Mass, M. D. Furones, and C. Rodgers, “Foodborne infectious diseases and monitoring of marine food resources,” in Oceans and Human Health: Risks and Remedies from the Sea, P. J. Walsh, S. L. Smith, L. E. Fleming, H. Solo-Gabriele, and W. H. Gerwick, Eds., pp. 359–380, Elsevier Science, New York, NY, USA, 2008.
[128]
J. W. Santo Domingo and J. Hansel, “Waterborne diseases and microbial quality monitoring for recreational water bodies using regulatory methods,” in Oceans and Human Health: Risks and Remedies from the Sea, P. J. Walsh, S. L. Smith, L. E. Fleming, H. Solo-Gabriele, and W. H. Gerwick, Eds., pp. 337–357, Elsevier Science, New York, NY, USA, 2008.
[129]
L.-A. H. Krometis, G. W. Characklis, P. N. Drummey, and M. D. Sobsey, “Comparison of the presence and partitioning behavior of indicator organisms and Salmonella spp. in an urban watershed,” Journal of Water and Health, vol. 8, no. 1, pp. 44–59, 2010.
[130]
E. K. Lipp, R. Kurz, R. Vincent, C. Rodriguez-Palacios, S. R. Farrah, and J. B. Rose, “The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary,” Estuaries, vol. 24, no. 2, pp. 266–276, 2001.
[131]
C. Ortega, H. M. Solo-Gabriele, A. Abdelzaher, M. Wright, Y. Deng, and L. M. Stark, “Correlations between microbial indicators, pathogens, and environmental factors in a subtropical Estuary,” Marine Pollution Bulletin, vol. 58, no. 9, pp. 1374–1381, 2009.
[132]
A. B. Boehm, N. J. Ashbolt, J. M. Colford Jr. et al., “A sea change ahead for recreational water quality criteria,” Journal of Water and Health, vol. 7, no. 1, pp. 9–20, 2009.
[133]
M. Wong, L. Kumar, T. M. Jenkins, I. Xagoraraki, M. S. Phanikumar, and J. B. Rose, “Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker,” Water Research, vol. 43, no. 4, pp. 1137–1149, 2009.
[134]
R. M. Gersberg, M. A. Rose, R. Robles-Sikisaka, and A. K. Dhar, “Quantitative detection of hepatitis A virus and enteroviruses near the United States-Mexico border and correlation with levels of fecal indicator bacteria,” Applied and Environmental Microbiology, vol. 72, no. 12, pp. 7438–7444, 2006.
[135]
D. W. Griffin, C. J. Gibson III, E. K. Lipp, K. Riley, J. H. Paul III, and J. B. Rose, “Detection of viral pathogens by reverse transcriptase PCR and of microbial indicators by standard methods in the canals of the Florida Keys,” Applied and Environmental Microbiology, vol. 65, no. 9, pp. 4118–4125, 1999.
[136]
F. A. Aulicino, P. Orsini, M. Carere, and A. Mastrantonio, “Bacteriological and virological quality of seawater bathing areas along the Tyrrhenian coast,” International Journal of Environmental Health Research, vol. 11, no. 1, pp. 5–11, 2001.
[137]
J. L. Alonso and M. A. Alonso, “Presence of campylobacter in marine waters of Valencia, Spain,” Water Research, vol. 27, no. 10, pp. 1559–1562, 1993.
[138]
A. M. Gonzalez, R. Paranhos, and M. S. Lutterbach, “Relationships between fecal indicators and pathogenic microorganisms in a tropical lagoon in Rio de Janeiro, Brazil,” Environmental Monitoring and Assessment, vol. 164, no. 1–4, pp. 207–219, 2010.
[139]
K. D. Goodwin and M. Pobuda, “Performance of CHROMagarTM Staph aureus and CHROMagarTM MRSA for detection of Staphylococcus aureus in seawater and beach sand—comparison of culture, agglutination, and molecular analyses,” Water Research, vol. 43, no. 19, pp. 4802–4811, 2009.
[140]
C. D. Sinigalliano, M. L. Gidley, T. Shibata et al., “Impacts of Hurricanes Katrina and Rita on the microbial landscape of the New Orleans area,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 21, pp. 9029–9034, 2007.
[141]
A. L. Lang, Y.-L. Tsai, C. L. Mayer, K. C. Patton, and C. J. Palmer, “Multiplex PCR for detection of the heat-labile toxin gene and shiga-like toxin I and II genes in Escherichia coli isolated from natural waters,” Applied and Environmental Microbiology, vol. 60, no. 9, pp. 3145–3149, 1994.
[142]
S. Ishii, T. Yan, D. A. Shively, M. N. Byappanahalli, R. L. Whitman, and M. J. Sadowsky, “Cladophora (Chlorophyta) spp. harbor human bacterial pathogens in nearshore water of Lake Michigan,” Applied and Environmental Microbiology, vol. 72, no. 7, pp. 4545–4553, 2006.
[143]
T. K. Graczyk, D. Sunderland, L. Tamang, F. E. Lucy, and P. N. Breysse, “Bather density and levels of Cryptosporidium, Giardia, and pathogenic microsporidian spores in recreational bathing water,” Parasitology Research, vol. 101, no. 6, pp. 1729–1731, 2007.
[144]
D. P. Keymer, L. H. Lam, and A. B. Boehm, “Biogeographic patterns in genomic diversity among a large collection of vibrio cholerae isolates,” Applied and Environmental Microbiology, vol. 75, no. 6, pp. 1658–1666, 2009.
[145]
T. Scholz, H. H. Garcia, R. Kuchta, and B. Wicht, “Update on the human broad tapeworm (genus diphyllobothrium), including clinical relevance,” Clinical Microbiology Reviews, vol. 22, no. 1, pp. 146–160, 2009.
[146]
A. C. Wright, R. T. Hill, J. A. Johnson, M.-C. Roghman, R. R. Colwell, and J. G. Morris Jr., “Distribution of Vibrio vulnificus in the Chesapeake Bay,” Applied and Environmental Microbiology, vol. 62, no. 2, pp. 717–724, 1996.
[147]
K. R. O'Neill, S. H. Jones, and D. J. Grimes, “Seasonal incidence of Vibrio vulnificus in the Great Bay estuary of New Hampshire and Maine,” Applied and Environmental Microbiology, vol. 58, no. 10, pp. 3257–3262, 1992.
[148]
A. M. Zimmerman, A. DePaola, J. C. Bowers et al., “Variability of total and pathogenic vibrio parahaemolyticus densities in Northern Gulf of Mexico water and oysters,” Applied and Environmental Microbiology, vol. 73, no. 23, pp. 7589–7596, 2007.
[149]
R. R. Colwell, “Global climate and infectious disease: the cholera paradigm,” Science, vol. 274, no. 5295, pp. 2025–2031, 1996.
[150]
M. L. Tamplin, A. L. Gauzens, A. Huq, D. A. Sack, and R. R. Colwell, “Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters,” Applied and Environmental Microbiology, vol. 56, no. 6, pp. 1977–1980, 1990.
[151]
D. P. Keymer and A. B. Boehm, “Recombination shapes the structure of an environmental Vibrio cholerae population,” submitted.
[152]
S. W. Joseph, R. R. Colwell, and J. B. Kaper, “Vibrio parahaemolyticus and related halophilic Vibrios,” Critical Reviews in Microbiology, vol. 10, no. 1, pp. 77–124, 1982.
[153]
C. Pruzzo, A. Huq, R. R. Colwell, and G. Donelli, “Pathogenic Vibrio species in the marine and estuarine environment,” in Oceans and Health: Pathogens in the Marine Environment, S. Belkin and R. Colwell, Eds., Springer Science, New York, NY, USA, 2006.
[154]
J. D. Oliver, “Vibrio vulnificus,” in Oceans and Health: Pathogens in the Marine Environment, S. Belkin and R. Colwell, Eds., Springer Science, New York, NY, USA, 2006.
[155]
R. M. Maier, I. L. Pepper, and C. P. Gerba, Environmental Microbiology, Academic Press, New York, NY, USA, 2nd edition, 2008.
[156]
U.S. Environmental Protection Agency, Ambient Water Quality Criteria for Bacteria, Office of Water Regulations and Standards, Washington, DC, USA, 1986, EPA 440/5-84-002.
[157]
T. J. Wade, N. Pai, J. N. S. Eisenberg, and J. M. Colford Jr., “Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis,” Environmental Health Perspectives, vol. 111, no. 8, pp. 1102–1109, 2003.
[158]
U.S. Food and Drug Administration, Guide for the Control of Molluscan Shellfish—Section IV, chapter 2, 2007, Growing Areas .01 Total Coliform Standards, http://www.issc.org/.
[159]
C. P. Gerba, “Assessment of enteric pathogen shedding by bathers during recreational activity and its impact on water quality,” Quantitative Microbiology, vol. 2, no. 1, pp. 55–68, 2000.
[160]
N. Charoena and R. S. Fujioka, “Assessment of staphylococcus bacteria in Hawaii's marine recreational waters,” Water Science and Technology, vol. 27, no. 3-4, pp. 283–289, 1993.
[161]
J. M. Fleisher, L. E. Fleming, H. M. Solo-Gabriele, et al., “The BEACHES study: health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters,” International Journal of Epidemiology. In press.
[162]
C. D. Sinigalliano, J. M. Fleisher, M. L. Gidley et al., “Traditional and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters,” Water Research, vol. 44, no. 13, pp. 3763–3772, 2010.
[163]
R. T. Noble and J. A. Fuhrman, “Enteroviruses detected by reverse transcriptase polymerase chain reaction from the coastal waters of Santa Monica Bay, California: low correlation to bacterial indicator levels,” Hydrobiologia, vol. 460, pp. 175–184, 2001.
[164]
A. B. Boehm, K. M. Yamahara, D. C. Love, B. M. Peterson, K. Mcneill, and K. L. Nelson, “Covariation and photoinactivation of traditional and novel indicator organisms and human viruses at a sewage-impacted marine beach,” Environmental Science and Technology, vol. 43, no. 21, pp. 8046–8052, 2009.
[165]
A. M. Abdelzaher, M. E. Wright, C. Ortega et al., “Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach,” Applied and Environmental Microbiology, vol. 76, no. 3, pp. 724–732, 2010.
[166]
A. B. Boehm, S. B. Grant, J. H. Kim et al., “Decadal and shorter period variability of surf zone water quality at Huntington Beach, California,” Environmental Science and Technology, vol. 36, no. 18, pp. 3885–3892, 2002.
[167]
R. W. Haile, J. S. Witte, M. Gold et al., “The health effects of swimming in ocean water contaminated by storm drain runoff,” Epidemiology, vol. 10, no. 4, pp. 355–363, 1999.
[168]
A. M. Abdelzaher, H. M. Solo-Gabriele, C. J. Palmer, and T. M. Scott, “Simultaneous concentration of enterococci and coliphage from marine waters using a dual layer filtration system,” Journal of Environmental Quality, vol. 38, no. 6, pp. 2468–2473, 2009.
[169]
K. D. Goodwin and R. W. Litaker, “Emerging technologies for monitoring recreational waters for bacteria and viruses,” in Oceans and Human Health: Risks and Remedies from the Sea, P. J. Walsh, S. L. Smith, L. E. Fleming, H. Solo-Gabriele, and W. H. Gerwick, Eds., pp. 381–404, Elsevier Science, New York, NY, USA, 2008.
[170]
M. B. Nevers and R. L. Whitman, “Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan,” Water Research, vol. 39, no. 20, pp. 5250–5260, 2005.
[171]
C. J. Palmer, J. A. Bonilla, T. D. Bonilla, et al., “The future of microbial ocean water quality monitoring,” in Oceans and Human Health: Risks and Remedies from the Sea, P. J. Walsh, S. L. Smith, L. E. Fleming, H. Solo-Gabriele, and W. H. Gerwick, Eds., pp. 405–421, Elsevier Science, New York, NY, USA, 2008.
