Spatial clustering of amyotrophic lateral sclerosis and the potential role of BMAA

Amyotrophic Lateral Sclerosis

Volumn 13, Issue 1, 2012, Pages 25-32

  Caller, Tracie A ^a   Field, Nicholas C ^a   Chipman, Jonathan W ^b   Shi, Xun ^b   Harris, Brent T ^c   Stommel, Elijah W ^a  

^a DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^b Dartmouth College   (United States)

^c GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 3 METHYLAMINOPROPIONIC ACID; FORMALDEHYDE; HEAVY METAL; MICROCYSTIN; NEUROTOXIN; PESTICIDE; SELENIUM;

AEROSOL; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CYANOBACTERIUM; DEMENTIA; DEMOGRAPHY; DISEASE ASSOCIATION; ELECTROMAGNETIC RADIATION; ENVIRONMENTAL FACTOR; EPIDEMIOLOGICAL DATA; EUTROPHICATION; FOOD CONTAMINATION; FOOD INTAKE; GENETIC SUSCEPTIBILITY; GEOGRAPHIC INFORMATION SYSTEM; HEAD INJURY; HEALTH LITERACY; HUMAN; HUNTINGTON CHOREA; LIFESTYLE; MODIFIABLE AREAL UNIT PROBLEM; NEUROTOXICITY; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; REVIEW; TOBACCO;

AMINO ACIDS, DIAMINO; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CLUSTER ANALYSIS; CYANOBACTERIA; ENVIRONMENT; EPIDEMIOLOGIC STUDIES; EXCITATORY AMINO ACID AGONISTS; HUMANS; NEUROTOXINS; RISK FACTORS;

EID: 84855408969     PISSN: 17482968     EISSN: 1471180X     Source Type: Journal    
DOI: 10.3109/17482968.2011.621436     Document Type: Review

References (108)

1. Fang F, Valdimarsdottir U, Bellocco R, Ronnevi LO, Sparen P, Fall K, et al. Amyotrophic lateral sclerosis in Sweden, 1991-2005. Arch Neurol. 2009;66:515-9.
2. Noonan CW, White MC, Thurman D, Wong LY. Temporal and geographic variation in the United States motor neuron disease mortality, 1969-1998. Neurology. 2005;64: 1215-21.
3. Cronin S, Hardiman O, Traynor BJ. Ethnic variation in the incidence of als: a systematic review. Neurology. 2007;68: 1002-7. (Pubitemid 46569133)
4. Fang F, Kamel F, Lichtenstein P, Bellocco R, Sparen P, Sandler DP, et al. Familial aggregation of amyotrophic lateral sclerosis. Ann Neurol. 2009;66:94-9.
5. Banack SA, Cox PA. Biomagnification of cycad neurotox-ins in flying foxes: implications for ALS-PDC in Guam. Neurology. 2003;61:387-9. (Pubitemid 36975972)
6. Cox PA, Sacks OW. Cycad neurotoxins, consumption of flying foxes, and ALS-PDC disease in Guam. Neurology. 2002;58:956-9. (Pubitemid 34242075)
7. Spencer PS, Nunn PB, Hugon J, Ludolph A, Roy DN. Motor neuron disease on Guam: possible role of a food neurotoxin. Lancet. 1986;1:965. (Pubitemid 16143084)
8. Bradley WG, Cox PA. Beyond Guam: cyanobacteria, BMAA and sporadic amyotrophic lateral sclerosis. Amyo-troph Lateral Scler. 2009;10:5-6.
9. Waller LA. Statistical power and design of focused clustering studies. Stat Med. 1996;15:765-82. (Pubitemid 26128732)
10. Openshaw S. The Modifiable Areal Unit Problem. Norwich, UK: Geo Books; 1984.
11. Marin B, Gil J, Preux PM, Funalot B, Couratier P. Incidence of amyotrophic lateral sclerosis in the Limousin region of France, 1997-2007. Amyotroph Lateral Scler. 2009;10:216-20.
12. Waller LA, GotwayCA. Applied Spatial Statistics for Public Health Data. Hoboken, NJ: Wiley; 2004.
13. Jacquez GM, Greiling DA. Local clustering in breast, lung and colorectal cancer in Long Island, New York. Int J Health Geogr. 2003;2:3.
14. Garruto RM, Gajdusek C, Chen KM. Amyotrophic lateral sclerosis among Chamorro migrants from Guam. Ann Neurol. 1980;8:612-9. (Pubitemid 11213507)
15. Garruto RM, Gajdusek DC, Chen KM. Amyotrophic lateral sclerosis and Parkinsonism-dementia among Filipino migrants to Guam. Ann Neurol. 1981;10:341-50. (Pubitemid 11027071)
16. Sabel CE, Boyle PJ, Loytonen M, Gatrell AC, Jokelainen M, Flowerdew R, et al. Spatial clustering of amyotrophic lateral sclerosis in Finland at place of birth and place of death. Am J Epidemiol. 2003;157:898-905. (Pubitemid 36555049)
17. Logroscino G, Traynor BJ, Hardiman O, Chio A, Couratier P, Mitchell JD, et al. Descriptive epidemiology of amyo-trophic lateral sclerosis: new evidence and unsolved issues. J Neurol Neurosurg Psychiatry. 2008;79:6-11.
18. Chad D, Mitsumoto H, Adelman LS, Bradley WG, Munsat TL, Zieper I. Conjugal motor neuron disease. Neurology. 1982;32:306-7. (Pubitemid 12176883)
19. Maloo JC, Radhakrishnan K, Poddar SK, Thacker AK. Conjugal motor neuron disease. J Assoc Physicians India. 1987;35:303-4.
20. Maloo JC, Radhakrishnan K, Poddar SK, Thacker AK. Conjugal motor neuron disease. J Assoc Physicians India. 1989;37:789-90.
21. Corcia P, Jafari-Schluep HF, Lardillier D, Mazyad H, Giraud P, Clavelou P, et al. A clustering of conjugal amyo-trophic lateral sclerosis in south-eastern France. Arch Neu-rol. 2003;60:553-7. (Pubitemid 36432069)
22. Camu W, Cadilhac J, Billiard M. Conjugal amyotrophic lateral sclerosis: a report on two couples from southern France. Neurology. 1994;44:547-8. (Pubitemid 24098160)
23. Rachele MG, Mascia V, Tacconi P, Dessi N, Marrosu F, Giagheddu M. Conjugal amyotrophic lateral sclerosis: a report on a couple from Sardinia, Italy. Ital J Neurol Sci. 1998;19:97-100. (Pubitemid 128730529)
24. Gajdusek DC. Motor neuron disease in natives of New Guinea. N Engl J Med. 1963;268:474-6.
25. Kurland LT, Mulder DW. Epidemiologic investigations of amyotrophic lateral sclerosis. I. Preliminary report on geographic distribution and special reference to the Mariana Islands, including clinical and pathologic observations. Neurology. 1954;4:438-48.
26. Zimmerman HM, editor. Monthly report to the medical officer in command. United States Navy Medical Research Unit No 2; 1945.
27. Araki S, Iwahashi Y, Kuroiwa Y. Epidemiological study of amyotrophic lateral sclerosis and allied disorders in the Kii Peninsula (Japan). J Neurol Sci. 1967;4:279-87.
28. Reed DM, Brody JA. Amyotrophic lateral sclerosis and Parkinsonism- dementia on Guam, 1945-1972. I. Descriptive epidemiology. Am J Epidemiol. 1975;101:287-301.
29. Spencer PS, Hugon J, Ludolph A, Nunn PB, Ross SM, Roy DN, et al. Discovery and partial characterization of primate motor-system toxins. Ciba Found Symp. 1987;126: 221-38.
30. Yase Y. The pathogenetic role of metals in motor neuron disease: the participation of aluminum. Adv Exp Med Biol. 1987;209:89-96.
31. Kilness AW, Hichberg FH. Amyotrophic lateral sclerosis in a high selenium environment. JAMA. 1977;237:2843-4. (Pubitemid 8140819)
32. Melmed C, Krieger C. A cluster of amyotrophic lateral sclerosis. Arch Neurol. 1982;39:595-6. (Pubitemid 12048108)
33. Sanders M. Clustering of amyotrophic lateral sclerosis. JAMA. 1980;244:435.
34. Sienko DG, Davis JP, Taylor JA, Brooks BR. Amyotrophic lateral sclerosis. A case-control study following detection of a cluster in a small Wisconsin community. Arch Neurol. 1990;47:38-41. (Pubitemid 20024151)
35. Taylor JA, Davis JP. Evidence for clustering of amyo-trophic lateral sclerosis in Wisconsin. J Clin Epidemiol. 1989;42:569-75. (Pubitemid 19161021)
36. Kusui K. Epidemiological study on amyotrophic lateral sclerosis (ALS) and other neighboring motor neuron diseases in Kii Peninsula. Folia Psychiatr Neurol Jpn. 1962;64:85-99.
37. Spencer PS, Kisby GE, Ludolph AC. Slow toxins, biologic markers, and long-latency neurodegenerative disease in the western Pacific region. Neurology. 1991;41:62-6; discussion 6-8.
38. Kuzuhara S, Kokubo Y. Atypical Parkinsonism of Japan: amyotrophic lateral sclerosis-Parkinsonism-dementia complex of the Kii peninsula of Japan (Muro disease): an update. Mov Disord. 2005;20 (Suppl 12):S108-13. (Pubitemid 41419563)
39. Gunnarsson LG, Lygner PE, Veiga-Cabo J, de Pedro-Cuesta J. An epidemic-like cluster of motor neuron disease in a Swedish county during the period 1973-1984. Neu-roepidemiology. 1996;15:142-52. (Pubitemid 26157787)
40. Neilson S, Gunnarsson LG, Robinson I. Rising mortality from motor neuron disease in Sweden, 1961-1990: the relative role of increased population life expectancy and environmental factors. Acta Neurol Scand. 1994;90: 150-9. (Pubitemid 24305915)
41. Proctor SP, Feldman RG, Wolf PA, Brent B, Wartenberg D. A perceived cluster of amyotrophic lateral sclerosis cases in a Massachusetts community. Neuroepidemiology. 1992;11: 277-81. (Pubitemid 23044216)
42. Uccelli R, Binazzi A, Altavista P, Belli S, Comba P, Mas-trantonio M, et al. Geographic distribution of amyotrophic lateral sclerosis through motor neuron disease mortality data. Eur J Epidemiol. 2007;22:781-90. (Pubitemid 350105363)
43. Caller TA, Doolin JW, Haney JF, Murby AJ, West KG, Far-rar HE, et al. A cluster of amyotrophic lateral sclerosis in New Hampshire: a possible role for toxic cyanobacteria blooms. Amyotroph Lateral Scler. 2009;10 (Suppl 2):101-8.
44. Cox PA, Richer R, Metcalf JS, Banack SA, Codd GA, Bradley WG. Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans. Amyotroph Lateral Scler. 2009;10 (Suppl 2): 109-17.
45. Miranda ML, Alicia Overstreet Galeano M, Tassone E, Allen KD, Horner RD. Spatial analysis of the etiology of amyotrophic lateral sclerosis among 1991 Gulf War veterans. Neurotoxicology. 2008;29:964-70.
46. Scott KM, Abhinav K, Stanton BR, Johnston C, Turner MR, Ampong MA, et al. Geographical clustering of amyo-trophic lateral sclerosis in south-east England: a population study. Neuroepidemiology. 2009;32:81-8.
47. Kurtzke JF. On statistical testing of prevalence studies. J Chronic Dis. 1966;19:909-22.
48. Armon C, Daube JR, O'Brien PC, Kurland LT, Mulder DW. When is an apparent excess of neurologic cases epide-miologically significant? Neurology. 1991;41:1713-8.
49. Horner RD, Grambow SC, Coffman CJ, Lindquist JH, Oddone EZ, Allen KD, et al. Amyotrophic lateral sclerosis among 1991 Gulf War veterans: evidence for a time-limited outbreak. Neuroepidemiology. 2008;31:28-32. (Pubitemid 351957395)
50. Haley RW. Excess incidence of ALS in young Gulf War veterans. Neurology. 2003;61:750-6. (Pubitemid 37179884)
51. Coffman CJ, Horner RD, Grambow SC, Lindquist J. Estimating the occurrence of amyotrophic lateral sclerosis among Gulf War (1990-1991) veterans using capture-recapture methods. Neuroepidemiology. 2005;24:141-50. (Pubitemid 41094840)
52. Mitchell JD, Borasio GD. Amyotrophic lateral sclerosis. Lancet. 2007;369:2031-41.
53. McGuire V, Longstreth WT Jr, Nelson LM, Koepsell TD, Checkoway H, Morgan MS, et al. Occupational exposures and amyotrophic lateral sclerosis: a population-based case-control study. Am J Epidemiol. 1997;145:1076-88. (Pubitemid 27272937)
54. Johnson FO, Atchison WD. The role of environmental mercury, lead and pesticide exposure in development of amyotrophic lateral sclerosis. Neurotoxicology. 2009;30: 761-5.
55. Kamel F, Umbach DM, Hu H, Munsat TL, Shefner JM, Taylor JA, et al. Lead exposure as a risk factor for amyo-trophic lateral sclerosis. Neurodegener Dis. 2005;2: 195-201. (Pubitemid 43827921)
56. Kamel F, Umbach DM, Lehman TA, Park LP, Munsat TL, Shefner JM, et al. Amyotrophic lateral sclerosis, lead, and genetic susceptibility: polymorphisms in the delta-aminole-vulinic acid dehydratase and vitamin D receptor genes. Environ Health Perspect. 2003;111:1335-9. (Pubitemid 37021137)
57. Kamel F, Umbach DM, Munsat TL, Shefner JM, Hu H, Sandler DP. Lead exposure and amyotrophic lateral sclerosis. Epidemiology. 2002;13:311-9. (Pubitemid 34415852)
58. Kamel F, Umbach DM, Stallone L, Richards M, Hu H, Sandler DP. Association of lead exposure with survival in amyotrophic lateral sclerosis. Environ Health Perspect. 2008;116:943-7. (Pubitemid 351943903)
59. Morahan JM, Pamphlett R. Amyotrophic lateral sclerosis and exposure to environmental toxins: an Australian case-control study. Neuroepidemiology. 2006;27:130-5. (Pubitemid 44651432)
60. Weisskopf MG, Morozova N, O'Reilly EJ, McCullough ML, Calle EE, Thun MJ, et al. Prospective study of chemical exposures and amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2009;80:558-61.
61. Hakansson N, Gustavsson P, Johansen C, Floderus B. Neu-rodegenerative diseases in welders and other workers exposed to high levels of magnetic fields. Epidemiology. 2003;14:420-8.
62. Li CY, Sung FC. Association between occupational exposure to power frequency electromagnetic fields and amyo-trophic lateral sclerosis: a review. Am J Ind Med. 2003;43: 212-20.
63. Weisskopf MG, Ascherio A. Cigarettes and amyotrophic lateral sclerosis: only smoke or also fire? Ann Neurol. 2009;65:361-2.
64. Kamel F, Umbach DM, Munsat TL, Shefner JM, Sandler DP. Association of cigarette smoking with amyotrophic lateral sclerosis. Neuroepidemiology. 1999;18:194-202. (Pubitemid 29284080)
65. Alonso A, Logroscino G, Jick SS, Hernan MA. Association of smoking with amyotrophic lateral sclerosis risk and survival in men and women: a prospective study. BMC Neurol. 2010;10:6.
66. Armon C. Smoking may be considered an established risk factor for sporadic ALS. Neurology. 2009;73:1693-8.
67. Fang F, Ye W. Smoking may be considered an established risk factor for sporadic ALS. Neurology. 2010;74:1927; author reply 8-9.
68. Weisskopf MJ, Gallo V, O'Reilly EJ, Vineis P, Ascherio A. Smoking may be considered an established risk factor for sporadic ALS. Neurology. 2010;74:1927-8; author reply 8-9.
69. Gallo V, Bueno-De-Mesquita HB, Vermeulen R, Andersen PM, Kyrozis A, Linseisen J, et al. Smoking and risk for amyotrophic lateral sclerosis: analysis of the EPIC cohort. Ann Neurol. 2009;65:378-85.
70. Mulder DW, Kurland LT. Motor neuron disease: epide-miologic studies. Adv Exp Med Biol. 1987;209:325-32.
71. Plato CC, Garruto RM, Galasko D, Craig UK, Plato M, Gamst A, et al. Amyotrophic lateral sclerosis and Parkin-sonism-dementia complex of Guam: changing incidence rates during the past 60 years. Am J Epidemiol. 2003;157: 149-57. (Pubitemid 36077446)
72. Bradley WG, Mash DC. Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurode-generative diseases. Amyotroph Lateral Scler. 2009;10 (Suppl 2):7-20.
73. Marler TE, Snyder LR, Shaw CA. Cycas micronesica (Cycadales) plants devoid of endophytic cyanobacteria increase in beta-methylamino-L-alanine. Toxicon. 2010;56: 563-8.
74. Banack SA, Murch SJ, Cox PA. Neurotoxic flying foxes as dietary items for the Chamorro people, Marianas Islands. J Ethnopharmacol. 2006;106:97-104.
75. Murch SJ, Cox PA, Banack SA. A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc Natl Acad Sci USA. 2004;101:12228-31. (Pubitemid 39145425)
76. Pablo J, Banack SA, Cox PA, Johnson TE, Papapetropoulos S, Bradley WG, et al. Cyanobacterial neurotoxin BMAA in ALS and Alzheimer's disease. Acta Neurol Scand. 2009;120: 216-25.
77. Brand LE. Human exposure to cyanobacteria and BMAA. Amyotroph Lateral Scler. 2009;10 (Suppl 2):85-95.
78. Brand LE, Pablo J, Compton A, Hammerschlag N, Mash DC. Cyanobacterial blooms and the occurrence of the neu-rotoxin, beta-N-methylamino-L-alanine (BMAA), in South Florida aquatic food webs. Harmful Algae. 2010; doi:10.1016/j.hal.2010.05.002.
79. Jonasson S, Eriksson J, Berntzon L, Spacil Z, Ilag LL, Ron-nevi LO, et al. Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc Natl Acad Sci USA. 2010;107: 9252-7.
80. Bradley WG, Banack SA, Cox PA. The ALS/PDC syndrome of Guam and the cycad hypothesis. Neurology. 2009;72:473-4, 6; author reply 5-6.
81. Snyder LR, Cruz-Aguado R, Sadilek M, Galasko D, Shaw CA, Montine TJ. Parkinson-dementia complex and development of a new stable isotope dilution assay for BMAA detection in tissue. Toxicol Appl Pharmacol. 2009;240:180-8.
82. Snyder LR, Cruz-Aguado R, Sadilek M, Galasko D, Shaw CA, Montine TJ. Lack of cerebral BMAA in human cerebral cortex. Neurology. 2009;72:1360-1.
83. Shen WB, McDowell KA, Siebert AA, Clark SM, Dugger NV, Valentino KM, et al. Environmental neurotoxin-induced progressive model of Parkinsonism in rats. Ann Neurol. 2010;68:70-80.
84. Lincoln EP, Wilkie AC, French BT. Cyanobacterial process for renovating dairy wastewater. Biomass and Bioenergy. 1996;10:63-8. (Pubitemid 126663178)
85. Dionysiou D. Overview: harmful algal blooms and natural toxins in fresh and marine waters. Exposure, occurrence, detection, toxicity, control, management and policy. Toxi-con. 2010;55:907-8.
86. Aleksandrov S V. Biological production and eutrophication of Baltic Sea estuarine ecosystems: the Curonian and Vistula lagoons. Mar Pollut Bull. 2010;61:205-10.
87. Barros LS, de Souza FC, Tavares LH, Amaral LA. Micro-cystin-LR in Brazilian aquaculture production systems. Water Environ Res. 2010;82:240-8.
88. Nyenje PM, Foppen JW, Uhlenbrook S, Kulabako R, Muwanga A. Eutrophication and nutrient release in urban areas of sub-Saharan Africa: a review. Sci Total Environ. 2010;408:447-55.
89. Carpenter SR. Phosphorus control is critical to mitigating eutrophication. Proc Natl Acad Sci USA. 2008;105: 11039-40.
90. Jeppesen E, Kronvang B, Meerhoff M, Sondergaard M, Hansen KM, Andersen HE, et al. Climate change effects on run-off, catchment phosphorus loading and lake ecological state, and potential adaptations. J Environ Qual. 2009;38:1930-41.
91. Paul VJ. Global warming and cyanobacterial harmful algal blooms. Adv Exp Med Biol. 2008;619:239-57.
92. Maasilta P, Jokelainen M, Loytonen M, Sabel CE, Gatrell AC. Mortality from amyotrophic lateral sclerosis in Finland, 1986-1995. Acta Neurol Scand. 2001;104:232-5. (Pubitemid 32844270)
93. Seljeseth YM, Vollset SE, Tysnes OB. Increasing mortality from amyotrophic lateral sclerosis in Norway? Neurology. 2000;55:1262-6.
94. Tysnes OB, Vollset SE, Aarli JA. Epidemiology of amyo-trophic lateral sclerosis in Hordaland county, western Norway. Acta Neurol Scand. 1991;83:280-5.
95. Sabel CE, Gatrell AC, eds. Exploratory spatial data analysis of motor neuron disease in north-west England: beyond the address at diagnosis. Proceedings of the International Workshop on Geomedical Systems; 1998. Stutgartt: Teubner-Verlag.
96. Chi A, Magnani C, Schiffer D. Amyotrophic lateral sclerosis mortality in Italy, 1958-1987: a cross-sectional and cohort study. Neurology. 1993;43:927-30. (Pubitemid 23150563)
97. Lilienfeld DE, Chan E, Ehland J, Godbold J, Landrigan PJ, Marsh G, et al. Rising mortality from motor neuron disease in the USA, 1962-1984. Lancet. 1989;1:710-3. (Pubitemid 19089229)
98. Lilienfeld DE, Perl D P. Projected neurodegenerative disease mortality in the United States, 1990-2040. Neuroep-idemiology. 1993;12:219-28. (Pubitemid 23353340)
99. Fleming LE, Rivero C, Burns J, Williams C, Beana JA, Shea KA, et al. Blue-green algae (cyanobacterial) toxins, surface drinking water, and liver cancer in Florida. Harmful Algae. 2002;1:157-68. (Pubitemid 37379142)
100. Nishiwaki-Matsushima R, Ohta T, Nishiwaki S, Suganuma M, Kohyama K, Ishikawa T, et al. Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J Cancer Res Clin Oncol. 1992;118:420-4.
101. Svircev Z, Krstic S, Miladinov-Mikov M, Baltic V, Vidovic M. Freshwater cyanobacterial blooms and primary liver cancer epidemiological studies in Serbia. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2009; 27:36-55.
102. Yu SZ. Primary prevention of hepatocellular carcinoma. J Gastroenterol Hepatol. 1995;10:674-82.
103. Backer LC, McNeel SV, Barber T, Kirkpatrick B, Williams C, Irvin M, et al. Recreational exposure to microcystins during algal blooms in two California lakes. Toxicon. 2010;55:909-21.
104. Cheng YS, Zhou Y, Irvin CM, Kirkpatrick B, Backer LC. Characterization of aerosols containing microcystin. Mar Drugs. 2007;5:136-50.
105. Fleming LE, Kirkpatrick B, Backer LC, Bean JA, Wanner A, Reich A, et al. Aerosolized red-tide toxins (brevetoxins) and asthma. Chest. 2007;131:187-94. (Pubitemid 46122991)
106. Fleming LE, Bean JA, Kirkpatrick B, Cheng YS, Pierce R, Naar J, et al. Exposure and effect assessment of aerosolized red tide toxins (brevetoxins) and asthma. Environ Health Perspect. 2009;117:1095-100.
107. Neutra RR. Counterpoint from a cluster buster. Am J Epidemiol. 1990;132:1-8. (Pubitemid 20203296)
108. Carmichael W. A world overview: one hundred and twenty-seven years of research on toxic cyanobacteria: where do we go from here? Adv Exp Med Biol. 2008;619: 105-25.