Animal models of BMAA neurotoxicity: A critical review

Life Sciences

Volumn 82, Issue 5-6, 2008, Pages 233-246

  Karamyan, Vardan T ^a   Speth, Robert C ^a,b  

^a UNIVERSITY OF MISSISSIPPI   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Amyotrophic lateral sclerosis (ALS); Beta methylamino alanine (BMAA); Ecotoxins; Guam disease; Neurodegeneration; Neurological disorders

Indexed keywords

2 AMINO 3 METHYLAMINOPROPIONIC ACID;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; BODY WEIGHT; CARCINOGENESIS; CLINICAL FEATURE; CONTROLLED STUDY; DIETARY INTAKE; DISEASE COURSE; FLOUR; IN VITRO STUDY; IN VIVO STUDY; MONKEY; NERVE DEGENERATION; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; OUTCOME ASSESSMENT; PARKINSONISM; REVIEW;

AMINO ACIDS, DIAMINO; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENVIRONMENTAL EXPOSURE; EXCITATORY AMINO ACID ANTAGONISTS; FOOD CHAIN; FOOD CONTAMINATION; GUAM; MEAT; NEUROTOXINS; PARKINSON DISEASE, SECONDARY; PLANTS, EDIBLE;

ANIMALIA; CYCADOPSIDA; PTEROPODIDAE;

EID: 38349089902     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2007.11.020     Document Type: Review

References (103)

1. Banack S.A., and Cox P.A. Biomagnification of cycad neurotoxins in flying foxes: implications for ALS-PDC in Guam. Neurology 61 3 (2003) 387-389
2. Banack S.A., Murch S.J., and Cox P.A. Neurotoxic flying foxes as dietary items for the Chamorro people, Marianas Islands. Journal of Ethnopharmacology 106 1 (2006) 97-104
3. Boxenbaum H., and DiLea C. First-time-in-human dose selection: allometric thoughts and perspectives. Journal of Clinical Pharmacology 35 10 (1995) 957-966
4. Brown Jr. L.T. Projections and termination of the corticospinal tract in rodents. Experimental Brain Research 13 4 (1971) 432-450
5. Buenz E.J., and Howe C.L. Beta-methylamino-alanine (BMAA) injures hippocampal neurons in vivo. Neurotoxicology 28 3 (2007) 702-704
6. Calabrese E.J., Beck B.D., and Chappell W.R. Does the animal-to-human uncertainty factor incorporate interspecies differences in surface area?. Regulatory Toxicology and Pharmacology 15 2 Pt 1 (1992) 172-179
7. Chade A.R., Kasten M., and Tanner C.M. Nongenetic causes of Parkinson's disease. Journal of Neural Transmission, Supplementum 70 (2006) 147-151
8. Chang Y.C., Chiu S.J., and Kao K.P. Beta-N-methylamino-l-alanine (l-BMAA) decreases brain glutamate receptor number and induces behavioral changes in rats. Chinese Journal of Physiology 36 2 (1993) 79-84
9. Chen K.M., Craig U.K., Lee C.T., and Haddock R. Cycad neurotoxin, consumption of flying foxes, and ALS/PDC disease in Guam. Neurology 59 10 (2002) 1664
10. Copani A., Canonico P.L., and Nicoletti F. Beta-N-methylamino-l-alanine (l-BMAA) is a potent agonist of 'metabolotropic' glutamate receptors. European Journal of Pharmacology 181 3 (1990) 327-328
11. Cox P.A., Banack S., Murch S., Bell A., Nunn P., Bradley W., Mash D., Papapetropoulos S., Pablo J., Ronnevi L.-O., Conradi S., Bergman B., Rasmussen U., Bidigare R., Codd G.A., Metcalf J.S., Johnson H., Speth R., and Weiss J.H. Correspondence to: lack of β-methylamino-l-alanine in brain from controls, AD, or Chamorros with PDC. Neurology (2005). http://www.neurology.org/cgi/eletters/65/5/768 (published online, 22 December) http://www.neurology.org/cgi/eletters/65/5/768
12. Cox P.A., Banack S.A., Murch S.J., Rasmussen U., Tien G., Bidigare R.R., Metcalf J.S., Morrison L.F., Codd G.A., and Bergman B. Diverse taxa of cyanobacteria produce beta-N-methylamino-l-alanine, a neurotoxic amino acid. Proceedings of the National Academy of Sciences of the United States of America 102 14 (2005) 5074-5078
13. Cox P.A., Banack S., Murch S., and Sacks O. Commentary on: 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 32 6 (2006) 679-682
14. Cox P.A., Banack S.A., and Murch S.J. 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 100 23 (2003) 13380-13383
15. Cox P.A., and Sacks O.W. Cycad neurotoxin, consumption of flying foxes, and ALS/PDC disease in Guam. Neurology 59 10 (2002) 1664-1665
16. Cox P.A., and Sacks O.W. Cycad neurotoxins, consumption of flying foxes, and ALS-PDC disease in Guam. Neurology 58 6 (2002) 956-959
17. Cruz-Aguado R., Winkler D., and Shaw C.A. Lack of behavioral and neuropathological effects of dietary beta-methylamino-l-alanine (BMAA) in mice. Pharmacology, Biochemistry and Behavior 84 2 (2006) 294-299
18. Dawson Jr. R., Marschall E.G., Chan K.C., Millard W.J., Eppler B., and Patterson T.A. Neurochemical and neurobehavioral effects of neonatal administration of beta-N-methylamino-l-alanine and 3,3'-iminodipropionitrile. Neurotoxicology and Teratology 20 2 (1998) 181-192
19. Duncan M.W., Kopin I.J., Garruto R.M., Lavine L., and Markey S.P. 2-Amino-3 (methylamino)-propionic acid in cycad-derived foods is an unlikely cause of amyotrophic lateral sclerosis/parkinsonism. Lancet 2 8611 (1988) 631-632
20. Duncan M.W., Steele J.C., Kopin I.J., and Markey S.P. 2-Amino-3-(methylamino)-propanoic acid (BMAA) in cycad flour: an unlikely cause of amyotrophic lateral sclerosis and parkinsonism-dementia of Guam. Neurology 40 5 (1990) 767-772
21. Duncan M.W., Villacreses N.E., Pearson P.G., Wyatt L., Rapoport S.I., Kopin I.J., Markey S.P., and Smith Q.R. 2-Amino-3-(methylamino)-propanoic acid (BMAA) pharmacokinetics and blood-brain barrier permeability in the rat. Journal of Pharmacology and Experimental Therapeutics 258 1 (1991) 27-35
22. Easton N., and Marsden C.A. Ecstasy: are animal data consistent between species and can they translate to humans?. Journal of Psychopharmacology 20 2 (2006) 194-210
23. Fornai F., Vaglini F., Maggio R., Bonuccelli U., and Corsini G.U. Species differences in the role of excitatory amino acids in experimental parkinsonism. Neuroscience and Biobehavioral Reviews 21 4 (1997) 401-415
24. Garruto R.M., Yanagihara R., and Gajdusek D.C. Cycads and amyotrophic lateral sclerosis/parkinsonism dementia. Lancet 2 8619 (1988) 1079
25. Gunnell G.F., and Simmons N.B. Fossil evidence and the origin of bats. Journal of Mammalian Evolution 12 1-2 (2005) 209-246
26. Gurney M.E. The use of transgenic mouse models of amyotrophic lateral sclerosis in preclinical drug studies. Journal of the Neurological Sciences 152 Suppl 1 (1997) S67-S73
27. Gwiazda R., Lucchini R., and Smith D. Adequacy and consistency of animal studies to evaluate the neurotoxicity of chronic low-level manganese exposure in humans. Journal of Toxicology and Environmental Health. Part A 70 7 (2007) 594-605
28. Ince P.G., and Codd G.A. 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 31 4 (2005) 345-353
29. Ivorra M.D., D'Ocon M.P., Paya M., and Villar A. Antihyperglycemic and insulin-releasing effects of beta-sitosterol 3-beta-d-glucoside and its aglycone, beta-sitosterol. Archives Internationales de Pharmacodynamie et de Therapie 296 (1988) 224-231
30. Jakowec M.W., and Petzinger G.M. 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned model of Parkinson's disease, with emphasis on mice and nonhuman primates. Comparative Medicine 54 5 (2004) 497-513
31. Jenner P., and Marsden C.D. The actions of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in animals as a model of Parkinson's disease. Journal of Neural Transmission. Supplementum 20 (1986) 11-39
32. Jimenez-Escrig A., Santos-Hidalgo A.B., and Saura-Calixto F. Common sources and estimated intake of plant sterols in the Spanish diet. Journal of Agricultural and Food Chemistry 54 9 (2006) 3462-3471
33. Johnson K., Ryan L., Davis J., Elmore A., Guenther B., Marcus J., and Maronpot R.R. Application of magnetic resonance imaging in developmental neurotoxicity testing: a pilot study. Neurotoxicology 27 5 (2006) 846-851
34. Khabazian I., Bains J.S., Williams D.E., Cheung J., Wilson J.M., Pasqualotto B.A., Pelech S.L., Andersen R.J., Wang Y.T., Liu L., Nagai A., Kim S.U., Craig U.K., and Shaw C.A. Isolation of various forms of sterol beta-d-glucoside from the seed of Cycas circinalis: neurotoxicity and implications for ALS-parkinsonism dementia complex. Journal of Neurochemistry 82 3 (2002) 516-528
35. Kisby G.E., Ellison M., and Spencer P.S. Content of the neurotoxins cycasin (methylazoxymethanol beta-d-glucoside) and BMAA (beta-N-methylamino-l-alanine) in cycad flour prepared by Guam Chamorros. Neurology 42 7 (1992) 1336-1340
36. Kisby G.E., Kabel H., Hugon J., and Spencer P. Damage and repair of nerve cell DNA in toxic stress. Drug Metabolism Reviews 31 3 (1999) 589-618
37. Kurland L.T., and Mulder D.W. Epidemiologic investigations of amyotrophic lateral sclerosis. I. Preliminary report on geographic distribution, with special reference to the Mariana Islands, including clinical and pathologic observations. Neurology 4 5 (1954) 355-378
38. Kuypers H.G.J.M., 1981. Anatomy of the descending pathways. In the Handbook of Physiology - the Nervous System II (eds. J.M. Brookhart and V.B. Mountcastle). American Physiological Society, Bethesda, Maryland. In: Brookhart J.M., Mountcastle V.B. (Eds.), Handbook of Physiology - The Nervous System II. pp. 597-666.
39. Laqueur G.L., Mickelsen O., Whiting M.G., and Kurland L.T. Carcinogenic properties of nuts from Cycas circinalis l. indigenous to Guam. Journal of the National Cancer Institute 31 (1963) 919-951
40. Levene C.I., Duban S., and Hughes R.H. Effects of cycasin and cycad meal. Federation Proceedings 23 (1964) 1366-1367
41. Leyton S.S.F., and Sherrington C.S. Observations on the excitable cortex of the chimpanzee, orangutan and gorilla. Quarterly Journal of Experimental Physiology 11 (1917) 135-222
42. Lindstrom H., Luthman J., Mouton P., Spencer P., and Olson L. Plant-derived neurotoxic amino acids (beta-N-oxalylamino-l-alanine and beta-N-methylamino-l-alanine): effects on central monoamine neurons. Journal of Neurochemistry 55 3 (1990) 941-949
43. Ling W.H., and Jones P.J. Dietary phytosterols: a review of metabolism, benefits and side effects. Life Science 57 3 (1995) 195-206
44. Lobner D., Piana P.M., Salous A.K., and Peoples R.W. Beta-N-methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiology of Disease 25 2 (2007) 360-366
45. Ludolph A.C., Hugon J., Dwivedi M.P., Schaumburg H.H., and Spencer P.S. Studies on the aetiology and pathogenesis of motor neuron diseases. 1. Lathyrism: clinical findings in established cases. Brain 110 Pt 1 (1987) 149-165
46. Ludolph A.C., and Spencer P.S. Toxic models of upper motor neuron disease. Journal of the Neurological Sciences 139 (1996) 53-59 Suppl
47. Ly P.T., Singh S., and Shaw C.A. Novel environmental toxins: steryl glycosides as a potential etiological factor for age-related neurodegenerative diseases. Journal of Neuroscience Research 85 2 (2007) 231-237
48. Mahmood I. Interspecies scaling of biliary excreted drugs: a comparison of several methods. Journal of Pharmaceutical Sciences 94 4 (2005) 883-892
49. Mahmood I., Martinez M., and Hunter R.P. Interspecies allometric scaling. Part I: prediction of clearance in large animals. Journal of Veterinary Pharmacology and Therapeutics 29 5 (2006) 415-423
50. Marler T.E., Lee V., and Shaw C.A. Storage does not influence steryl glucoside concentration in Cycas micronesica seeds. HortScience 42 3 (2007) 626-628
51. Martinez M., Mahmood I., and Hunter R.P. Interspecies allometric scaling: prediction of clearance in large animal species: part II: mathematical considerations. Journal of Veterinary Pharmacology and Therapeutics 29 5 (2006) 425-432
52. Matsuoka Y., Rakonczay Z., Giacobini E., and Naritoku D. l-beta-methylamino-alanine-induced behavioral changes in rats. Pharmacology, Biochemistry and Behavior 44 3 (1993) 727-734
53. Mettler F.A., and Stern G.M. Observations on the toxic effects of yellow star thistle. Journal of Neuropathology and Experimental Neurology 22 (1963) 164-169
54. Mickelsen O., Campbell E., Yang M., Mugera G., and Whitehair C.K. Studies with cycad. Federation Proceedings 23 (1964) 1363-1365
55. Montine T.J., Li K., Perl D.P., and Galasko D. Lack of beta-methylamino-l-alanine in brain from controls, AD, or Chamorros with PDC. Neurology 65 5 (2005) 768-769
56. Murch S.J., Cox P.A., and Banack S.A. A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proceedings of the National Academy of Sciences of the United States of America 101 33 (2004) 12228-12231
57. Murch S.J., Cox P.A., Banack S.A., Steele J.C., and Sacks O.W. Occurrence of beta-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurologica Scandinavica 110 4 (2004) 267-269
58. Nunn P.B., Seelig M., Zagoren J.C., and Spencer P.S. Stereospecific acute neuronotoxicity of 'uncommon' plant amino acids linked to human motor-system diseases. Brain Reseacrch 410 2 (1987) 375-379
59. Papapetropoulos S. Is there a role for naturally occurring cyanobacterial toxins in neurodegeneration? The beta-N-methylamino-l-alanine (BMAA) paradigm. Neurochemistry International 50 7-8 (2007) 998-1003
60. Peng L., Kawagoe Y., Hogan P., and Delmer D. Sitosterol-beta-glucoside as primer for cellulose synthesis in plants. Science 295 5552 (2002) 147-150
61. Perry T.L., Bergeron C., Biro A.J., and Hansen S. Beta-N-methylamino-l-alanine. Chronic oral administration is not neurotoxic to mice. Journal of the Neurological Sciences 94 1-3 (1989) 173-180
62. Phillips K.M., Ruggio D.M., and Ashraf-Khorassani M. Analysis of steryl glucosides in foods and dietary supplements by solid-phase extraction and gas chromatography. Journal of Food Lipids 12 (2005) 124-140
63. Phillips K.M., Ruggio D.M., and Ashraf-Khorassani M. Phytosterol composition of nuts and seeds commonly consumed in the United States. Journal of Agricultural and Food Chemistry 53 24 (2005) 9436-9445
64. Piironen V., Lindsay D.G., Miettinen T.A., Toivo J., and Lampi A.M. Plant sterols: biosynthesis, biological function and their importance to human nutrition. Journal of the Science of Food and Agriculture 80 (2000) 939-966
65. Plat J., and Mensink R.P. Effects of plant sterols and stanols on lipid metabolism and cardiovascular risk. Nutrition Metabolism and Cardiovascular Diseases 11 1 (2001) 31-40
66. Polsky F.I., Nunn P.B., and Bell E.A. Distribution and toxicity of alpha-amino-beta-methylaminopropionic acid. Federation Proceedings 31 5 (1972) 1473-1475
67. Porter R., and Lemon R. Anatomical substrates for movement performance: cerebral cortex and the corticospinal tract. Monographs of the Physiological Society, 45. Oxford Science Publications. Monographs of the Physiological Society 45 (1993) 36-89
68. Price D.L., Koliatsos V.E., Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Cleveland D.W., Griffin J.W., Hoffman P.N., Cork L.C., and Sisodia S.S. Motor neuron disease and model systems: aetiologies, mechanisms and therapies. Ciba Foundation Symposium 196 (1996) 3-13
69. Rakonczay Z., Matsuoka Y., and Giacobini E. Effects of l-beta-N-methylamino-l-alanine (l-BMAA) on the cortical cholinergic and glutamatergic systems of the rat. Journal of Neuroscience Research 29 1 (1991) 121-126
70. Rao S.D., Banack S.A., Cox P.A., and Weiss J.H. BMAA selectively injures motor neurons via AMPA/kainate receptor activation. Experimental Neurology 201 1 (2006) 244-252
71. Rice D., and Barone Jr. S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental Health Perspectives 108 Suppl 3 (2000) 511-533
72. Ross S.M., Roy D.N., and Spencer P.S. Beta-N-oxalylamino-l-alanine action on glutamate receptors. Journal of Neurochemistry 53 3 (1989) 710-715
73. Ross S.M., and Spencer P.S. Specific antagonism of behavioral action of "uncommon" amino acids linked to motor-system diseases. Synapse 1 3 (1987) 248-253
74. Santiago M., Matarredona E.R., Machado A., and Cano J. Acute perfusion of BMAA in the rat's striatum by in vivo microdialysis. Toxicology Letters 167 1 (2006) 34-39
75. Seawright A.A., Brown A.W., Nolan C.C., and Cavanagh J.B. Selective degeneration of cerebellar cortical neurons caused by cycad neurotoxin, l-beta-methylaminoalanine (l-BMAA), in rats. Neuropathology and Applied Neurobiology 16 2 (1990) 153-169
76. Shaw C.A., and Wilson J.M. Analysis of neurological disease in four dimensions: insight from ALS-PDC epidemiology and animal models. Neuroscience and Biobehavioral Reviews 27 6 (2003) 493-505
77. Sieber S.M., Correa P., Dalgard D.W., McIntire K.R., and Adamson R.H. Carcinogenicity and hepatotoxicity of cycasin and its aglycone methylazoxymethanol acetate in nonhuman primates. Journal of the National Cancer Institute 65 1 (1980) 177-189
78. Sillevis Smitt P.A., and de Jong J.M. Animal models of amyotrophic lateral sclerosis and the spinal muscular atrophies. Journal of the Neurological Sciences 91 3 (1989) 231-258
79. Simmons N.B., Conway T. Chiroptera. Bats. http://tolweb.org/Chiroptera/15966/1997.01.01; Wund M., Myers P., 2005. "Chiroptera" (On-line), Animal Diversity Web. Accessed July 07, 2007 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Chiropte ra.html. 1997.
80. Smith Q.R., Nagura H., Takada Y., and Duncan M.W. Facilitated transport of the neurotoxin, beta-N-methylamino-l-alanine, across the blood-brain barrier. Journal of Neurochemistry 58 4 (1992) 1330-1337
81. Smith S.E., and Meldrum B.S. Receptor site specificity for the acute effects of beta-N-methylamino-alanine in mice. European Journal of Pharmacology 187 1 (1990) 131-134
82. Spencer P.S., Allen R.G., Kisby G.E., and Ludolph A.C. Excitotoxic disorders. Science 248 4952 (1990) 144
83. Spencer P.S., Hugon J., Ludolph A., Nunn P.B., Ross S.M., Roy D.N., and Schaumburg H.H. Discovery and partial characterization of primate motor-system toxins. Ciba Foundation Symposium 126 (1987) 221-238
84. Spencer P.S., Nunn P.B., Hugon J., Ludolph A.C., Ross S.M., Roy D.N., and Robertson R.C. Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science 237 4814 (1987) 517-522
85. Spencer P.S., Kisby G.E., Ross S.M., Roy D.N., Hugon J., Ludolph A.C., and Nunn P.B. Guam ALS-PDC: possible causes. Science 262 5135 (1993) 825-826
86. Spencer P.S., Nunn P.B., Hugon J., Ludolph A., and Roy D.N. Motorneurone disease on Guam: possible role of a food neurotoxin. Lancet 1 8487 (1986) 965
87. Spencer P.S., Roy D.N., Ludolph A., Hugon J., Dwivedi M.P., and Schaumburg H.H. Lathyrism: evidence for role of the neuroexcitatory aminoacid BOAA. Lancet 2 8515 (1986) 1066-1067
88. Stone R. Guam: deadly disease dying out. Science 261 5120 (1993) 424-426
89. Thewissen J.G.M., and Babcock S.K. The origin of flight in bats. BioScience 42 5 (1992) 340-345
90. Torres G., Meeder B.A., Hallas B.H., Spernyak J.A., Mazurchuk R., Jones C., Gross K.W., and Horowitz J.M. Ventricular size mapping in a transgenic model of schizophrenia. Brain Research and Developmental Brain Research 154 1 (2005) 35-44
91. Vega A., Bell E.A., and Nunn P.B. The preparation of l- and d-alpha-amino-beta-methylaminopropionic acids and the identification of the compound isolated from Cycas circinalis as the L-isomer. Phytochemistry 7 (1968) 1885-1887
92. Weber N. Metabolism of sitosteryl beta-d-glucoside and its nutritional effects in rats. Lipids 23 1 (1988) 42-47
93. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences (1988), The Third World Medical Research Foundation, New York ii-vi
94. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Fifth Cycad Conference. 1967 (1988), Third World Medical Research Foundation, New York XV-1-XV-21
95. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Fifth Cycad Conference. 1967 (1988), Third World Medical Research Foundation, New York XI-1-XI-7
96. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The First Cycad Conference: 1962 (1988), Third World Medical Research Foundation, New York 1-17
97. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Fourth Cycad Conference. 1965 (1988), Third World Medical Research Foundation, New York 39-43
98. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Fourth Cycad Conference. 1965 (1988), Third World Medical Research Foundation, New York 2-16
99. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Second Cycad Conference (1988), Third World Medical Research Foundation, New York 12-23
100. Whiting M.G. Toxicity of cycads: implications for neurodegenerative diseases and cancer. Transcripts of Four Cycad Conferences. The Third Cycad Conference. 1964 (1988), Third World Medical Research Foundation, New York 1363-1365 1988., New York
101. Wilson J., and Shaw C.A. Commentary on: 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 32 3 (2006) 341-343
102. Wilson J.M., Khabazian I., Wong M.C., Seyedalikhani A., Bains J.S., Pasqualotto B.A., Williams D.E., Andersen R.J., Simpson R.J., Smith R., Craig U.K., Kurland L.T., and Shaw C.A. Behavioral and neurological correlates of ALS-parkinsonism dementia complex in adult mice fed washed cycad flour. NeuroMolecular Medicine 1 3 (2002) 207-221
103. Wund M., Myers P. "Chiroptera" (On-line), Animal Diversity Web. Accessed July 07, 2007 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Chiropte ra.html. 2005.