Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Mini-Review Article

Mycotoxins and Amyotrophic Lateral Sclerosis: Food Exposure, Nutritional Implications and Dietary Solutions

Author(s): Umberto Manera*, Enrico Matteoni, Antonio Canosa, Stefano Callegaro, Federico Casale, Daniela Marchis, Rosario Vasta, Cristina Moglia, Adriano Chiò and Andrea Calvo

Volume 23, Issue 5, 2024

Published on: 31 August, 2023

Page: [562 - 572] Pages: 11

DOI: 10.2174/1871527323666230817145434

Price: $65

Abstract

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder determined by a combination of both genetic and environmental factors. Despite wide investigations, the role of chronic exposure to environmental pollutants is still rather unknown. Among natural toxins, the mycotoxins have received major attention only in the last few years, due to both technical and scientific achievements that allowed to disentangle many important features of the complex fungal biology. Whereas the effects of acute and high-dose mycotoxin exposure are well known, the potential effects of chronic and low-dose exposure on neurodegeneration have not been broadly elucidated. In this review, we have summarized all the studies concerning environmental exposure to unknown substances that caused ALS outbreaks all over the world, reinterpreting in light of the new scientific acquisitions and highlighting the potential and neglected role of mycotoxins. Then, we focused on recent papers about food exposure to mycotoxin, mycobiome and fungal infections in ALS and other neurodegenerative diseases. We analyzed the gaps of current literature that lead to an undervaluation of mycotoxins as detrimental molecules. By listing all the most important mycotoxins and analyzing all the biological pathways that they can affect, we explained the reasons why they need to be considered in the next epidemiological studies on ALS and other neurodegenerative and neuroinflammatory diseases. In conclusion, after suggesting some possible solutions to mitigate mycotoxin exposure risk, we affirm that future collaborations between scientists and policymakers are important to develop sustainable interventions and promote health through dietary diversity.

Graphical Abstract

[1]
Masrori P, Van Damme P. Amyotrophic lateral sclerosis: A clinical review. Eur J Neurol 2020; 27(10): 1918-29.
[http://dx.doi.org/10.1111/ene.14393] [PMID: 32526057]
[2]
Chiò A, Logroscino G, Traynor BJ, et al. Global epidemiology of amyotrophic lateral sclerosis: A systematic review of the published literature. Neuroepidemiology 2013; 41(2): 118-30.
[http://dx.doi.org/10.1159/000351153] [PMID: 23860588]
[3]
Andrew A, Zhou J, Gui J, et al. Pesticides applied to crops and amyotrophic lateral sclerosis risk in the U.S. Neurotoxicology 2021; 87: 128-35.
[http://dx.doi.org/10.1016/j.neuro.2021.09.004] [PMID: 34562505]
[4]
Limongi D, Baldelli S. Redox imbalance and viral infections in neurodegenerative diseases. Oxid Med Cell Longev 2016; 2016
[http://dx.doi.org/10.1155/2016/6547248]
[5]
Park S, Lim W, You S, Song G. Ochratoxin A exerts neurotoxicity in human astrocytes through mitochondria-dependent apoptosis and intracellular calcium overload. Toxicol Lett 2019; 313: 42-9.
[http://dx.doi.org/10.1016/j.toxlet.2019.05.021] [PMID: 31154016]
[6]
Scafuri B, Varriale A, Facchiano A, D’Auria S, Raggi ME, Marabotti A. Binding of mycotoxins to proteins involved in neuronal plasticity: A combined in silico/wet investigation. Sci Rep 2017; 7(1): 15156.
[http://dx.doi.org/10.1038/s41598-017-15148-4] [PMID: 29123130]
[7]
Nakajima Y, Iguchi H, Kamisuki S, Sugawara F, Furuichi T, Shinoda Y. Low doses of the mycotoxin citrinin protect cortical neurons against glutamate-induced excitotoxicity. J Toxicol Sci 2016; 41(2): 311-9.
[http://dx.doi.org/10.2131/jts.41.311] [PMID: 26961616]
[8]
Marin B, Logroscino G, Boumédiene F, et al. Clinical and demographic factors and outcome of amyotrophic lateral sclerosis in relation to population ancestral origin. Eur J Epidemiol 2016; 31(3): 229-45.
[http://dx.doi.org/10.1007/s10654-015-0090-x] [PMID: 26458931]
[9]
Al-Chalabi A, Calvo A, Chio A, et al. Analysis of amyotrophic lateral sclerosis as a multistep process: A population-based modelling study. Lancet Neurol 2014; 13(11): 1108-13.
[http://dx.doi.org/10.1016/S1474-4422(14)70219-4] [PMID: 25300936]
[10]
Reed DM, Brody JA. Amyotrophic lateral sclerosis and parkinsonism-dementia on guam. Am J Epidemiol 1975; 101(4): 287-301.
[http://dx.doi.org/10.1093/oxfordjournals.aje.a112097] [PMID: 1124759]
[11]
Gajdusek DC, Salazar AM. Amyotrophic lateral sclerosis and parkinsonian syndromes in high incidence among the Auyu and Jakai people of West New Guinea. Neurology 1982; 32(2): 107-26.
[http://dx.doi.org/10.1212/WNL.32.2.107] [PMID: 7198738]
[12]
Kaji R, Izumi Y, Adachi Y, Kuzuhara S. ALS-Parkinsonism-Dementia complex of Kii and other related diseases in Japan. Parkinsonism Relat Disord 2012; 18 (Suppl. 1): S190-1.
[http://dx.doi.org/10.1016/S1353-8020(11)70059-1] [PMID: 22166431]
[13]
Spencer PS, Palmer VS, Kihira T, et al. Kampō medicine and muro disease (amyotrophic lateral sclerosis and parkinsonism-dementia complex). eNeurologicalSci 2020; 18: 100230.
[http://dx.doi.org/10.1016/j.ensci.2020.100230] [PMID: 32090178]
[14]
Spencer PS, Palmer VS, Kisby GE. Seeking environmental causes of neurodegenerative disease and envisioning primary prevention. Neurotoxicology 2016; 56: 269-83.
[http://dx.doi.org/10.1016/j.neuro.2016.03.017] [PMID: 27050202]
[15]
Spencer PS, Palmer VS, Ludolph AC. On the decline and etiology of high-incidence motor system disease in west papua (Southwest New Guinea) 2005. Available From: https://movementdisorders.onlinelibrary.wiley.com/doi/10.1002/mds.20552 (Accessed on 2022 Dec 26)
[16]
Ishiura H, Takahashi Y, Mitsui J, et al. C9ORF72 repeat expansion in amyotrophic lateral sclerosis in the Kii peninsula of Japan. Arch Neurol 2012; 69(9): 1154-8.
[http://dx.doi.org/10.1001/archneurol.2012.1219] [PMID: 22637429]
[17]
Hendley AG. Lathyrism. Ind Med Gaz 1893; 28(9): 300-2. Available From: https://pubmed-ncbi-nlm-nih-gov.bibliopass.unito.it/29001151/ (Accessed on 2022 Dec 27).
[PMID: 29001151]
[18]
Rao SLN, Adiga PR, Sarma Biochemistry PS, Sarma PS. The isolation and characterization of j-IV-Oxalyl-L-a-Diaminopropionic acid: A neurotoxin from the seeds of lathyrus sativus. Available From: https://pubs.acs.org/sharingguidelines (Accessed on 2022 Dec 27)
[19]
Murch SJ, Cox PA, Banack SA, Steele JC, Sacks OW. Occurrence of β-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol Scand 2004; 110(4): 267-9.
[http://dx.doi.org/10.1111/j.1600-0404.2004.00320.x] [PMID: 15355492]
[20]
Bradley WG. The john walton muscular dystrophy research centre in the university of newcastle and the BMAA theory of motor neuron disease. J Neuromuscul Dis 2015; 2(s2): S77-81.
[http://dx.doi.org/10.3233/JND-150090] [PMID: 27858760]
[21]
Borenstein AR, Mortimer JA, Schofield E, et al. Cycad exposure and risk of dementia, MCI, and PDC in the chamorro population of guam. Neurology 2007; 68(21): 1764-71.
[http://dx.doi.org/10.1212/01.wnl.0000262027.31623.b2] [PMID: 17515538]
[22]
Symposium on mycotoxins in human health. Symposium on Mycotoxins in Human Health 1971.
[23]
Kasarskis EJ, Lindquist JH, Coffman CJ, et al. Clinical aspects of ALS in Gulf War veterans. Amyotroph Lateral Scler 2009; 10(1): 35-41.
[http://dx.doi.org/10.1080/17482960802351029] [PMID: 18792848]
[24]
Sava V, Reunova O, Velasquez A, Sanchez-Ramos J. Can low level exposure to ochratoxin-A cause parkinsonism? J Neurol Sci 2006; 249(1): 68-75.
[http://dx.doi.org/10.1016/j.jns.2006.06.006] [PMID: 16844142]
[25]
Spencer PS, McCauley LA, Joos SK, et al. U.S. Gulf War Veterans: Service periods in theater, differential exposures, and persistent unexplained illness. Toxicol Lett 1998; 102-103: 515-21.
[http://dx.doi.org/10.1016/S0378-4274(98)00258-6] [PMID: 10022305]
[26]
Heyndrickx A, Sookvanichsilp N, Van den Heede M. Detection of trichothecene mycotoxins (yellow rain) in blood, urine and faeces of Iranian soldiers treated as victims of a gas attack. Arch Belges 1984; (Suppl.)143-6.
[PMID: 6535464]
[27]
Research Advisory Committee on Gulf War Veterans’ Illnesses. Gulf War Illness and the Health of Gulf War Veterans Scientific Findings and Recommendations. D.C.: Washington 2008.
[28]
Horner RD, Kamins KG, Feussner JR, et al. Occurrence of amyotrophic lateral sclerosis among Gulf War veterans. Neurology 2003; 61(6): 742-9.
[http://dx.doi.org/10.1212/01.WNL.0000069922.32557.CA] [PMID: 14504315]
[29]
Horner RD, Grambow SC, Coffman CJ, et al. Amyotrophic lateral sclerosis among 1991 Gulf War veterans: evidence for a time-limited outbreak. Neuroepidemiology 2008; 31(1): 28-32.
[http://dx.doi.org/10.1159/000136648] [PMID: 18535397]
[30]
Wang MD, Little J, Gomes J, Cashman NR, Krewski D. Identification of risk factors associated with onset and progression of amyotrophic lateral sclerosis using systematic review and meta-analysis. Neurotoxicology 2017; 61: 101-30.
[http://dx.doi.org/10.1016/j.neuro.2016.06.015] [PMID: 27377857]
[31]
McKay KA, Smith KA, Smertinaite L, Fang F, Ingre C, Taube F. Military service and related risk factors for amyotrophic lateral sclerosis. Acta Neurol Scand. In: Blackwell Publishing Ltd 2021; pp. 39-50.
[32]
Neilson S, Robinson I, Rose FC. Ecological correlates of motor neuron disease mortality: A hypothesis concerning an epidemiological association with radon gas and gamma exposure. J Neurol 1996; 243(4): 329-36.
[http://dx.doi.org/10.1007/BF00868407] [PMID: 8965106]
[33]
Schwartz GG, Klug MG. Motor neuron disease mortality rates in U.S. states are associated with well water use. Amyotroph Lateral Scler Frontotemporal Degener 2016; 17(7-8): 528-34.
[http://dx.doi.org/10.1080/21678421.2016.1195409] [PMID: 27324739]
[34]
Schwartz GG, Rundquist BC, Simon IJ, Swartz SE. Geographic distributions of motor neuron disease mortality and well water use in U.S. counties. Amyotroph Lateral Scler Frontotemporal Degener 2017; 18(3-4): 279-83.
[http://dx.doi.org/10.1080/21678421.2016.1264975] [PMID: 28019106]
[35]
Vinceti M, Bonvicini F, Rothman KJ, Vescovi L, Wang F. The relation between amyotrophic lateral sclerosis and inorganic selenium in drinking water: A population-based case-control study. Environ Health 2010; 9(1): 77.
[http://dx.doi.org/10.1186/1476-069X-9-77] [PMID: 21134276]
[36]
Das K, Nag C, Ghosh M. Familial, environmental, and occupational risk factors in development of amyotrophic lateral sclerosis. N Am J Med Sci 2012; 4(8): 350-5.
[http://dx.doi.org/10.4103/1947-2714.99517] [PMID: 22912943]
[37]
Oliveira BR, Mata AT, Ferreira JP, Barreto Crespo MT, Pereira VJ, Bronze MR. Production of mycotoxins by filamentous fungi in untreated surface water. Environ Sci Pollut Res Int 2018; 25(18): 17519-28.
[http://dx.doi.org/10.1007/s11356-018-1952-z] [PMID: 29663293]
[38]
Oliveira BR, Barreto Crespo MT, San Romão MV, Benoliel MJ, Samson RA, Pereira VJ. New insights concerning the occurrence of fungi in water sources and their potential pathogenicity. Water Res 2013; 47(16): 6338-47.
[http://dx.doi.org/10.1016/j.watres.2013.08.004] [PMID: 24011405]
[39]
Shittu OB, Iwaloye OF, Oloyede AR, et al. Water safety, antifungal-resistant aflatoxigenic aspergillus flavus and other pathogenic fungi in a community hand-dug wells. J Appl Microbiol 2022; 133(2): 673-82.
[http://dx.doi.org/10.1111/jam.15559] [PMID: 35368141]
[40]
Babič MN, Gunde-Cimerman N, Vargha M, Tischner Z, Magyar D, Veríssimo C, et al. Fungal contaminants in drinking water regulation? A tale of ecology, exposure, purification and clinical relevance. Int J Environ Res Public Health 2017; 14(6): 636.
[41]
Al-Gabr HM, Zheng T, Yu X. Fungi contamination of drinking water. Rev Environ Contam Toxicol 2014; 228: 121-39.
[PMID: 24162095]
[42]
French P, Ludowyke R, Guillemin G. Fungal-contaminated grass and well water and sporadic amyotrophic lateral sclerosis. Neural Regen Res 2019; 14(9): 1490-3.
[http://dx.doi.org/10.4103/1673-5374.255959] [PMID: 31089037]
[43]
Bozzoni V, Pansarasa O, Diamanti L, Nosari G, Cereda C, Ceroni M. Amyotrophic lateral sclerosis and environmental factors. Funct Neurol 2016; 31(1): 7-19.
[PMID: 27027889]
[44]
Krewski D, Barakat-Haddad C, Donnan J, et al. Determinants of neurological disease: Synthesis of systematic reviews. Neurotoxicology 2017; 61: 266-89.
[http://dx.doi.org/10.1016/j.neuro.2017.04.002] [PMID: 28410962]
[45]
Goldman SM. Environmental toxins and Parkinson’s disease. Annu Rev Pharmacol Toxicol 2014; 54(1): 141-64.
[http://dx.doi.org/10.1146/annurev-pharmtox-011613-135937] [PMID: 24050700]
[46]
Vinceti M, Bottecchi I, Fan A, Finkelstein Y, Mandrioli J. Are environmental exposures to selenium, heavy metals, and pesticides risk factors for amyotrophic lateral sclerosis? Rev Environ Health 2012; 27(1): 19-41.
[http://dx.doi.org/10.1515/reveh-2012-0002] [PMID: 22755265]
[47]
Malek AM, Barchowsky A, Bowser R, Youk A, Talbott EO. Pesticide exposure as a risk factor for amyotrophic lateral sclerosis: A meta-analysis of epidemiological studies. Environ Res 2012; 117: 112-9.
[http://dx.doi.org/10.1016/j.envres.2012.06.007] [PMID: 22819005]
[48]
Kamel F, Umbach DM, Bedlack RS, et al. Pesticide exposure and amyotrophic lateral sclerosis. Neurotoxicology 2012; 33(3): 457-62.
[http://dx.doi.org/10.1016/j.neuro.2012.04.001] [PMID: 22521219]
[49]
Costello S, Cockburn M, Bronstein J, Zhang X, Ritz B. Parkinson’s disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of california. Am J Epidemiol 2009; 169(8): 919-26.
[http://dx.doi.org/10.1093/aje/kwp006] [PMID: 19270050]
[50]
Jones RR, Yu CL, Nuckols JR, et al. Farm residence and lymphohematopoietic cancers in the Iowa Women׳s Health Study. Environ Res 2014; 133: 353-61.
[http://dx.doi.org/10.1016/j.envres.2014.05.028] [PMID: 25038451]
[51]
Govoni V, Granieri E, Fallica E, Casetta I. Amyotrophic lateral sclerosis, rural environment and agricultural work in the Local Health District of Ferrara, Italy, in the years 1964–1998. J Neurol 2005; 252(11): 1322-7.
[http://dx.doi.org/10.1007/s00415-005-0859-z] [PMID: 15995797]
[52]
Mandrioli J, Biguzzi S, Guidi C, et al. Epidemiology of amyotrophic lateral sclerosis in Emilia Romagna Region (Italy): A population based study. Amyotroph Lateral Scler Frontotemporal Degener 2014; 15(3-4): 262-8.
[http://dx.doi.org/10.3109/21678421.2013.865752] [PMID: 24863640]
[53]
Vinceti M, Filippini T, Violi F, et al. Pesticide exposure assessed through agricultural crop proximity and risk of amyotrophic lateral sclerosis. Environ Health 2017; 16(1): 91.
[http://dx.doi.org/10.1186/s12940-017-0297-2] [PMID: 28851431]
[54]
Mehta P, Kaye W, Raymond J, et al. Prevalence of amyotrophic lateral sclerosis: United States, 2015. MMWR Morb Mortal Wkly Rep 2018; 67(46): 1285-9.
[http://dx.doi.org/10.15585/mmwr.mm6746a1] [PMID: 30462626]
[55]
Waśkiewicz A, Gromadzka K, Bocianowski J, Pluta P, Goliński P. Zearalenone contamination of the aquatic environment as a result of its presence in crops. Arh Hig Rada Toksikol 2012; 63(4): 429-35.
[http://dx.doi.org/10.2478/10004-1254-63-2012-2229] [PMID: 23334037]
[56]
Hartmann N, Erbs M, Wettstein FE, Hoerger CC, Schwarzenbach RP, Bucheli TD. Quantification of zearalenone in various solid agroenvironmental samples using D6-zearalenone as the internal standard. J Agric Food Chem 2008; 56(9): 2926-32.
[http://dx.doi.org/10.1021/jf8002448] [PMID: 18412358]
[57]
Gromadzka K, Waśkiewicz A, Goliński P, Świetlik J. Occurrence of estrogenic mycotoxin: Zearalenone in aqueous environmental samples with various NOM content. Water Res 2009; 43(4): 1051-9.
[http://dx.doi.org/10.1016/j.watres.2008.11.042] [PMID: 19084253]
[58]
Hartmann N, Erbs M, Wettstein FE, Schwarzenbach RP, Bucheli TD. Quantification of estrogenic mycotoxins at the ng/L level in aqueous environmental samples using deuterated internal standards. J Chromatogr A 2007; 1138(1-2): 132-40.
[http://dx.doi.org/10.1016/j.chroma.2006.10.045] [PMID: 17084850]
[59]
Waśkiewicz A, Bocianowski J, Perczak A, Goliński P. Occurrence of fungal metabolites: Fumonisins at the ng/L level in aqueous environmental samples. Sci Total Environ 2015; 524-525: 394-9.
[http://dx.doi.org/10.1016/j.scitotenv.2015.03.015] [PMID: 25920071]
[60]
Voss KA, Riley RT, Snook ME, Waes JG. Reproductive and sphingolipid metabolic effects of fumonisin B(1) and its alkaline hydrolysis product in LM/Bc mice: Hydrolyzed fumonisin B(1) did not cause neural tube defects. Toxicol Sci 2009; 112(2): 459-67.
[http://dx.doi.org/10.1093/toxsci/kfp215] [PMID: 19783636]
[61]
Hartmann N, Erbs M, Forrer HR, et al. Occurrence of zearalenone on fusarium graminearum infected wheat and maize fields in crop organs, soil, and drainage water. Environ Sci Technol 2008; 42(15): 5455-60.
[http://dx.doi.org/10.1021/es8007326] [PMID: 18754460]
[62]
Fazekas B, Tar A, Kovács M. Ochratoxin A content of urine samples of healthy humans in Hungary. Acta Vet Hung 2005; 53(1): 35-44.
[http://dx.doi.org/10.1556/avet.53.2005.1.4] [PMID: 15782657]
[63]
De Santis B, Debegnach F, Toscano P, Crisci A, Battilani P, Brera C. Overall exposure of european adult population to mycotoxins by statistically modelled biomonitoring data. Toxins 2021; 13(10): 695.
[http://dx.doi.org/10.3390/toxins13100695] [PMID: 34678988]
[64]
Pupillo E, Bianchi E, Chiò A, et al. Amyotrophic lateral sclerosis and food intake. Amyotroph Lateral Scler Frontotemporal Degener 2018; 19(3-4): 267-74.
[http://dx.doi.org/10.1080/21678421.2017.1418002] [PMID: 29268633]
[65]
Paterson RRM, Venâncio A, Lima N, Guilloux-Bénatier M, Rousseaux S. Predominant mycotoxins, mycotoxigenic fungi and climate change related to wine. Food Res Int 2018; 103: 478-91.
[http://dx.doi.org/10.1016/j.foodres.2017.09.080] [PMID: 29389638]
[66]
Liew WPP, Mohd-Redzwan S. Mycotoxin: Its impact on gut health and microbiota. Front Cell Infect Microbiol 2018; 8: 60.
[http://dx.doi.org/10.3389/fcimb.2018.00060] [PMID: 29535978]
[67]
Persoon IF, Buijs MJ, Özok AR, et al. The mycobiome of root canal infections is correlated to the bacteriome. Clin Oral Investig 2017; 21(5): 1871-81.
[http://dx.doi.org/10.1007/s00784-016-1980-3] [PMID: 27771826]
[68]
De Santis B, Brera C, Mezzelani A, et al. Role of mycotoxins in the pathobiology of autism: A first evidence. Nutr Neurosci 2019; 22(2): 132-44.
[http://dx.doi.org/10.1080/1028415X.2017.1357793] [PMID: 28795659]
[69]
French PW, Ludowyke R, Guillemin GJ. Fungal neurotoxins and sporadic amyotrophic lateral sclerosis. Neurotox Res 2019; 35(4): 969-80.
[http://dx.doi.org/10.1007/s12640-018-9980-5] [PMID: 30515715]
[70]
Akbari P, Braber S, Varasteh S, Alizadeh A, Garssen J, Fink-Gremmels J. The intestinal barrier as an emerging target in the toxicological assessment of mycotoxins. Arch Toxicol 2017; 91(3): 1007-29.
[http://dx.doi.org/10.1007/s00204-016-1794-8] [PMID: 27417439]
[71]
Bertero A, Augustyniak J, Buzanska L, Caloni F. Species-specific models in toxicology: In vitro epithelial barriers. Environ Toxicol Pharmacol 2019; 70: 103203.
[http://dx.doi.org/10.1016/j.etap.2019.103203] [PMID: 31176950]
[72]
Kolf-Clauw M, Sassahara M, Lucioli J, et al. The emerging mycotoxin, enniatin B1, down-modulates the gastrointestinal toxicity of T-2 toxin in vitro on intestinal epithelial cells and ex vivo on intestinal explants. Arch Toxicol 2013; 87(12): 2233-41.
[http://dx.doi.org/10.1007/s00204-013-1067-8] [PMID: 23649843]
[73]
Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9(11): 799-809.
[http://dx.doi.org/10.1038/nri2653] [PMID: 19855405]
[74]
Gao Y, Meng L, Liu H, Wang J, Zheng N. The compromised intestinal barrier induced by mycotoxins. Toxins. In: Basel MDPI AG. 2020.
[75]
Poirier AA, Aubé B, Côté M, Morin N, Di Paolo T, Soulet D. Gastrointestinal dysfunctions in Parkinson’s disease: Symptoms and treatments. Parkinsons Dis. In: Hindawi Publishing Corporation. 2016; 2016: p. 6762528.
[76]
Nübling GS, Mie E, Bauer RM, et al. Increased prevalence of bladder and intestinal dysfunction in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2014; 15(3-4): 174-9.
[http://dx.doi.org/10.3109/21678421.2013.868001] [PMID: 24479577]
[77]
Bodukam V, Hays RD, Maranian P, et al. Association of gastrointestinal involvement and depressive symptoms in patients with systemic sclerosis. Rheumatology 2011; 50(2): 330-4.
[http://dx.doi.org/10.1093/rheumatology/keq296] [PMID: 20884655]
[78]
Pellegrini C, Antonioli L, Colucci R, Blandizzi C, Fornai M. Interplay among gut microbiota, intestinal mucosal barrier and enteric neuro-immune system: A common path to neurodegenerative diseases? Acta Neuropathol. In: Springer Verlag. 2018; pp. 345-61.
[79]
Tremlett H, Bauer KC, Appel-Cresswell S, Finlay BB, Waubant E. The gut microbiome in human neurological disease: A review. Ann Neurol 2017; 81(3): 369-82.
[http://dx.doi.org/10.1002/ana.24901] [PMID: 28220542]
[80]
Fang X, Wang X, Yang S, et al. Evaluation of the microbial diversity in amyotrophic lateral sclerosis using high-throughput sequencing. Front Microbiol 2016; 7: 1479.
[http://dx.doi.org/10.3389/fmicb.2016.01479] [PMID: 27703453]
[81]
Bonfili L, Cecarini V, Berardi S, et al. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sci Rep 2017; 7(1): 2426.
[http://dx.doi.org/10.1038/s41598-017-02587-2] [PMID: 28546539]
[82]
Cryan JF, Dinan TG. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13(10): 701-12.
[http://dx.doi.org/10.1038/nrn3346] [PMID: 22968153]
[83]
Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 2017; 20(2): 145-55.
[http://dx.doi.org/10.1038/nn.4476] [PMID: 28092661]
[84]
Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson’s disease. Mov Disord 2015; 30(10): 1351-60.
[http://dx.doi.org/10.1002/mds.26307] [PMID: 26179554]
[85]
Alonso R, Pisa D, Marina AI, et al. Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int J Biol Sci 2015; 11(5): 546-58.
[http://dx.doi.org/10.7150/ijbs.11084] [PMID: 25892962]
[86]
Pisa D, Alonso R, Rábano A, Carrasco L. Corpora amylacea of brain tissue from neurodegenerative diseases are stained with specific antifungal antibodies. Front Neurosci 2016; 10: 86.
[http://dx.doi.org/10.3389/fnins.2016.00086] [PMID: 27013948]
[87]
Taniwaki MH, Pitt JI. Mycotoxins. Food Microbiology: Fundamentals and Frontiers 2019; 16: 587-608.
[88]
Dutton MF. Fumonisins, mycotoxins of increasing importance: Their nature and their effects. Pharmacol Ther 1996; 70(2): 137-61.
[http://dx.doi.org/10.1016/0163-7258(96)00006-X] [PMID: 8843466]
[89]
Peraica M. Radić B, Lucić A, Pavlović M. Toxic effects of mycotoxins in humans. Bull World Health Organ 1999; 77(9): 754-66.
[PMID: 10534900]
[90]
Wang J, Fitzpatrick DW, Wilson JR. Effect of dietary T-2 toxin on biogenic monoamines in discrete areas of the rat brain. Food Chem Toxicol 1993; 31(3): 191-7.
[http://dx.doi.org/10.1016/0278-6915(93)90093-E] [PMID: 8473003]
[91]
Wang J, Fitzpatrick DW, Wilson JR. Effects of the trichothecene mycotoxin T-2 toxin on neurotransmitters and metabolites in discrete areas of the rat brain. Food Chem Toxicol 1998; 36(11): 947-53.
[http://dx.doi.org/10.1016/S0278-6915(98)00078-7] [PMID: 9771557]
[92]
Mavrommatis A, Giamouri E, Tavrizelou S, et al. Impact of mycotoxins on animals’ oxidative status. Antioxidants 2021; 10(2): 214.
[http://dx.doi.org/10.3390/antiox10020214] [PMID: 33535708]
[93]
Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29(3-4): 323-33.
[http://dx.doi.org/10.1016/S0891-5849(00)00302-6] [PMID: 11035261]
[94]
Doi K, Uetsuka K. Mechanisms of mycotoxin-induced neurotoxicity through oxidative stress-associated pathways. Int J Mol Sci 2011; 12(8): 5213-37.
[http://dx.doi.org/10.3390/ijms12085213] [PMID: 21954354]
[95]
Lee HJ, Ryu D. JFS special issue: 75 years of advancing food science, and preparing for the next 75: Advances in mycotoxin research: Public health perspectives. J Food Sci 2015; 80(12): T2970-83.
[http://dx.doi.org/10.1111/1750-3841.13156] [PMID: 26565730]
[96]
Gallo M, Ferrara L, Calogero A, Montesano D, Naviglio D. Relationships between food and diseases: What to know to ensure food safety Food research international. In: Elsevier Ltd 2020; p. 109414.
[97]
De Ruyck K, Huybrechts I, Yang S, et al. Mycotoxin exposure assessments in a multi-center European validation study by 24-hour dietary recall and biological fluid sampling. Environ Int 2020; 137: 105539.
[http://dx.doi.org/10.1016/j.envint.2020.105539] [PMID: 32035364]
[98]
Li Q, Dong Z, Lian W, et al. Ochratoxin A causes mitochondrial dysfunction, apoptotic and autophagic cell death and also induces mitochondrial biogenesis in human gastric epithelium cells. Arch Toxicol 2019; 93(4): 1141-55.
[http://dx.doi.org/10.1007/s00204-019-02433-6] [PMID: 30903243]
[99]
Klarić MŠ, Želježić D, Rumora L, Peraica M, Pepeljnjak S, Domijan AM. A potential role of calcium in apoptosis and aberrant chromatin forms in porcine kidney PK15 cells induced by individual and combined ochratoxin A and citrinin. Arch Toxicol 2012; 86(1): 97-107.
[http://dx.doi.org/10.1007/s00204-011-0735-9] [PMID: 21739216]
[100]
Sundstøl Eriksen G, Pettersson H, Lundh T. Comparative cytotoxicity of deoxynivalenol, nivalenol, their acetylated derivatives and de-epoxy metabolites. Food Chem Toxicol 2004; 42(4): 619-24.
[http://dx.doi.org/10.1016/j.fct.2003.11.006] [PMID: 15019186]
[101]
Riley RT, Merrill AH Jr. Ceramide synthase inhibition by fumonisins: A perfect storm of perturbed sphingolipid metabolism, signaling, and disease. J Lipid Res 2019; 60(7): 1183-9.
[http://dx.doi.org/10.1194/jlr.S093815] [PMID: 31048407]
[102]
Stockmann-Juvala H, Mikkola J, Naarala J, Loikkanen J, Elovaara E, Savolainen K. Oxidative stress induced by fumonisin B1 in continuous human and rodent neural cell cultures. Free Radic Res 2004; 38(9): 933-42.
[http://dx.doi.org/10.1080/10715760412331273205] [PMID: 15621711]
[103]
Shifrin VI, Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem 1999; 274(20): 13985-92.
[http://dx.doi.org/10.1074/jbc.274.20.13985] [PMID: 10318810]
[104]
Kamp H, Eisenbrand G, Schlatter J, Würth K, Janzowski C, Ochratoxin A. Ochratoxin A: induction of (oxidative) DNA damage, cytotoxicity and apoptosis in mammalian cell lines and primary cells. Toxicology 2005; 206(3): 413-25.
[http://dx.doi.org/10.1016/j.tox.2004.08.004] [PMID: 15588931]
[105]
Mally A, Pepe G, Ravoori S, et al. Ochratoxin a causes DNA damage and cytogenetic effects but no DNA adducts in rats. Chem Res Toxicol 2005; 18(8): 1253-61.
[http://dx.doi.org/10.1021/tx049650x] [PMID: 16097798]
[106]
Bódi V, Csikós V, Rátkai EA, et al. Short-term neuronal effects of fumonisin B1 on neuronal activity in rodents. Neurotoxicology 2020; 80: 41-51.
[http://dx.doi.org/10.1016/j.neuro.2020.06.007] [PMID: 32561249]
[107]
Stevens VL, Tang J. Fumonisin B1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J Biol Chem 1997; 272(29): 18020-5.
[http://dx.doi.org/10.1074/jbc.272.29.18020] [PMID: 9218430]
[108]
Marasas WFO, Riley RT, Hendricks KA, et al. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: A potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 2004; 134(4): 711-6.
[http://dx.doi.org/10.1093/jn/134.4.711] [PMID: 15051815]
[109]
Zhang X, Boesch-Saadatmandi C, Lou Y, Wolffram S, Huebbe P, Rimbach G. Ochratoxin A induces apoptosis in neuronal cells. Genes Nutr 2009; 4(1): 41-8.
[http://dx.doi.org/10.1007/s12263-008-0109-y] [PMID: 19148691]
[110]
Shankar J. Food habit associated mycobiota composition and their impact on human health. Front Nutr 2021; 8: 773577. Available From: https://pubmed-ncbi-nlm-nih-gov.bibliopass.unito.it/34881282/
[http://dx.doi.org/10.3389/fnut.2021.773577] [PMID: 34881282]
[111]
Swash M, Eisen A. Hypothesis: amyotrophic lateral sclerosis and environmental pollutants. Muscle Nerve 2020; 62(2): 187-91.
[http://dx.doi.org/10.1002/mus.26855] [PMID: 32134532]
[112]
Adegbeye MJ, Reddy PRK, Chilaka CA, Balogun OB, Elghandour MMMY, Rivas-Caceres RR, et al. Mycotoxin toxicity and residue in animal products: Prevalence, consumer exposure and reduction strategies – A review Toxicon. In: Elsevier Ltd 2020; pp. 96-108.
[113]
Carballo D, Tolosa J, Ferrer E, Berrada H. Dietary exposure assessment to mycotoxins through total diet studies A review food and chemical toxicology. In: Elsevier Ltd 2019; pp. 8-20.
[114]
Saha Turna N, Wu F. Aflatoxin M1 in milk: A global occurrence, intake, & exposure assessment Trends Food Sci Technol. In: Elsevier Ltd 2021; pp. 183-92.
[115]
Biasucci G, Calabrese G, Carrara G, Colombo F, Mandelli B. The presence of ochratoxin A in cord serum and in human milk and its correspondence with maternal dietary habits. Eur J Nutr 2011; 50(3): 211-8.
[116]
Galvano F, Pietri A, Bertuzzi T, et al. Maternal dietary habits and mycotoxin occurrence in human mature milk. Mol Nutr Food Res 2008; 52(4): 496-501. Available From: https://onlinelibrary-wiley-com.bibliopass.unito.it/doi/full/10.1002/mnfr.200700266
[http://dx.doi.org/10.1002/mnfr.200700266] [PMID: 18338407]
[117]
Thuvander A, Paulsen JE, Axberg K, Johansson N, Vidnes A, Enghardt-Barbieri H, et al. Levels of ochratoxin A in blood from Norwegian and Swedish blood donors and their possible correlation with food consumption Available From: www.elsevier.com/locate/foodchemtox
[http://dx.doi.org/10.1016/S0278-6915(01)00080-1]
[118]
Di Giuseppe R, Bertuzzi T, Rossi F, Rastelli S, Mulazzi A, Capraro J. Plasma ochratoxin A levels, food consumption, and risk biomarkers of a representative sample of men and women from the Molise region in Italy. Eur J Nutr 51(7): 851-60.
[http://dx.doi.org/10.1007/s00394-011-0265-5]
[119]
Wu F, Mitchell NJ, Male D, Kensler TW. Reduced foodborne toxin exposure is a benefit of improving dietary diversity. Toxicological Sciences 2014; 141: 329.
[http://dx.doi.org/10.1093/toxsci/kfu137]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy