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The increasing importance of environmental conditions in amyotrophic lateral sclerosis

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Abstract

Amyotrophic lateral sclerosis (ALS) is the most common neurodegenerative disease affecting motor neurons (MNs). Although a small percentage of ALS has a familial origin, the vast majority of cases are sporadic in which genetic factors and environment interact with each other leading to disease onset in genetically predisposed individuals. In the current model of the disease, each individual has a determined genetic load, some degree of cell degeneration related to age and several risky environmental exposures. In this scenario, MN degeneration would occur when the sum of these factors reach a certain threshold. To date, an extensive list of environmental factors has been associated to ALS, including different categories, such as exposure to heavy metals and other toxicants, cyanotoxins or infectious agents. In addition, in recent years, lifestyle and other demographic parameters are gaining relevance in the genesis of the disease. Among them, physical activity, nutrition, body mass index, cardiovascular risk factors, autoimmune diseases and cancer are some of the conditions which have been related to the disease. In this review, we will discuss the potential mechanisms of environmental conditions in motor neuron degeneration. Understanding the role of each one of these factors as well as their interactions appears as a crucial step in order to develop new preventive, diagnostic and therapeutic approaches for ALS patients.

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References

  • Abhinav K, Al Chalabi A, Hortobagyi T, Leigh PN (2007) Electrical injury and amyotrophic lateral sclerosis: a systematic review of the literature. J Neurol Neurosurg Psychiatry 78:450–453

    Article  Google Scholar 

  • Adams CR, Ziegler DK, Lin JT (1983) Mercury intoxication simulating amyotrophic lateral sclerosis. JAMA 250:642–643

    Article  CAS  Google Scholar 

  • Al Chalabi A, Hardiman O (2013) The epidemiology of ALS: a conspiracy of genes, environment and time. Nat Rev Neurol 9:617–628

    Article  CAS  Google Scholar 

  • Al Chalabi A, Fang F, Hanby MF, Leigh PN, Shaw CE, Ye W, Rijsdijk F (2010) An estimate of amyotrophic lateral sclerosis heritability using twin data. J Neurol Neurosurg Psychiatry 81:1324–1326

    Article  Google Scholar 

  • Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15:539–553

    Article  CAS  Google Scholar 

  • Alonso A, Logroscino G, Hernan MA (2010) Smoking and the risk of amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 81:1249–1252

    Article  Google Scholar 

  • Alonso R, Pisa D, Marina AI, Morato E, Rabano A, Rodal I, Carrasco L (2015) Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int J Biol Sci 11:546–558

    Article  CAS  Google Scholar 

  • Barbeito AG, Martinez-Palma L, Vargas MR, Pehar M, Manay N, Beckman JS, Barbeito L, Cassina P (2010) Lead exposure stimulates VEGF expression in the spinal cord and extends survival in a mouse model of ALS. Neurobiol Dis 37:574–580

    Article  CAS  Google Scholar 

  • Bassett T, Bach P, Chan HM (2012) Effects of methylmercury on the secretion of pro-inflammatory cytokines from primary microglial cells and astrocytes. Neurotoxicology 33:229–234

    Article  CAS  Google Scholar 

  • Bjornstad P, Snell-Bergeon JK, McFann K, Wadwa RP, Rewers M, Rivard CJ, Jalal D, Chonchol MB, Johnson RJ, Maahs DM (2014) Serum uric acid and insulin sensitivity in adolescents and adults with and without type 1 diabetes. J Diabetes Complicat 28:298–304

    Article  Google Scholar 

  • Boccia S, Sayed-Tabatabaei FA, Persiani R, Gianfagna F, Rausei S, Arzani D, La Greca A, D'Ugo D, La Torre G, van Duijn CM, Ricciardi G (2007) Polymorphisms in metabolic genes, their combination and interaction with tobacco smoke and alcohol consumption and risk of gastric cancer: a case-control study in an Italian population. BMC Cancer 7:206

    Article  CAS  Google Scholar 

  • Bradley WG (2015) The John Walton Muscular Dystrophy Research Centre in the University of Newcastle and the BMAA theory of motor neuron disease. J Neuromuscul Dis 2:S77–S81

    Article  Google Scholar 

  • Buee-Scherrer V, Buee L, Hof PR, Leveugle B, Gilles C, Loerzel AJ, Perl DP, Delacourte A (1995) Neurofibrillary degeneration in amyotrophic lateral sclerosis/parkinsonism-dementia complex of Guam. Immunochemical characterization of tau proteins=. Am J Pathol 146:924–932

    CAS  Google Scholar 

  • Caller TA, Chipman JW, Field NC, Stommel EW (2013) Spatial analysis of amyotrophic lateral sclerosis in northern New England, USA, 1997-2009. Muscle Nerve 48:235–241

    Article  Google Scholar 

  • Casteignau A, Fontan A, Morillo A, Oliveros JA, Segales J (2006) Clinical, pathological and toxicological findings of a iatrogenic selenium toxicosis case in feeder pigs. J Vet Med A Physiol Pathol Clin Med 53:323–326

    Article  CAS  Google Scholar 

  • Daneman D (2006) Type 1 diabetes. Lancet 367:847–858

    Article  CAS  Google Scholar 

  • Desport JC, Preux PM, Truong TC, Vallat JM, Sautereau D, Couratier P (1999) Nutritional status is a prognostic factor for survival in ALS patients. Neurology 53:1059–1063

    Article  CAS  Google Scholar 

  • Dormann D, Haass C (2013) Fused in sarcoma (FUS): an oncogene goes awry in neurodegeneration. Mol Cell Neurosci 56:475–486

    Article  CAS  Google Scholar 

  • Douville R, Liu J, Rothstein J, Nath A (2011) Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol 69:141–151

    Article  CAS  Google Scholar 

  • Driver JA, Beiser A, Au R, Kreger BE, Splansky GL, Kurth T, Kiel DP, Lu KP, Seshadri S, Wolf PA (2012) Inverse association between cancer and Alzheimer’s disease: results from the Framingham Heart Study. BMJ 344:e1442

    Article  Google Scholar 

  • Dupuis L, Corcia P, Fergani A, Gonzalez De Aguilar JL, Bonnefont-Rousselot D, Bittar R, Seilhean D, Hauw JJ, Lacomblez L, Loeffler JP, Meininger V (2008) Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology 70:1004–1009

    Article  CAS  Google Scholar 

  • Dupuis L, Pradat PF, Ludolph AC, Loeffler JP (2011) Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol 10:75–82

    Article  CAS  Google Scholar 

  • Eaglehouse YL, Talbott EO, Chang Y, Kuller LH (2016) Participation in physical activity and risk for amyotrophic lateral sclerosis mortality among postmenopausal women. JAMA Neurol 73:329–336

    Article  Google Scholar 

  • Estevez AO, Mueller CL, Morgan KL, Szewczyk NJ, Teece L, Miranda-Vizuete A, Estevez M (2012) Selenium induces cholinergic motor neuron degeneration in Caenorhabditis elegans. Neurotoxicology 33:1021–1032

    Article  CAS  Google Scholar 

  • Falone S, Mirabilio A, Carbone MC, Zimmitti V, Di Loreto S, Mariggio MA, Mancinelli R, Di Ilio C, Amicarelli F (2008) Chronic exposure to 50Hz magnetic fields causes a significant weakening of antioxidant defence systems in aged rat brain. Int J Biochem Cell Biol 40:2762–2770

    Article  CAS  Google Scholar 

  • Fang X (2016) Potential role of gut microbiota and tissue barriers in Parkinson's disease and amyotrophic lateral sclerosis. Int J Neurosci 126:771–776

    Article  CAS  Google Scholar 

  • Fang F, Kwee LC, Allen KD, Umbach DM, Ye W, Watson M, Keller J, Oddone EZ, Sandler DP, Schmidt S, Kamel F (2010) Association between blood lead and the risk of amyotrophic lateral sclerosis. Am J Epidemiol 171:1126–1133

    Article  Google Scholar 

  • Fang F, Al Chalabi A, Ronnevi LO, Turner MR, Wirdefeldt K, Kamel F, Ye W (2013) Amyotrophic lateral sclerosis and cancer: a register-based study in Sweden. Amyotroph Lateral Scler Frontotemporal Degener 14:362–368

    Article  Google Scholar 

  • Fang F, Hallmarker U, James S, Ingre C, Michaelsson K, Ahlbom A, Feychting M (2016) Amyotrophic lateral sclerosis among cross-country skiers in Sweden. Eur J Epidemiol 31:247–253

    Article  Google Scholar 

  • Feddermann-Demont N, Junge A, Weber KP, Weller M, Dvorak J, Tarnutzer AA (2017) Prevalence of potential sports-associated risk factors in Swiss amyotrophic lateral sclerosis patients. Brain Behav 7:e00630

    Article  Google Scholar 

  • Field NC, Metcalf JS, Caller TA, Banack SA, Cox PA, Stommel EW (2013) Linking beta-methylamino-L-alanine exposure to sporadic amyotrophic lateral sclerosis in Annapolis, MD. Toxicon 70:179–183

    Article  CAS  Google Scholar 

  • Fitzgerald KC, O'Reilly EJ, Fondell E, Falcone GJ, McCullough ML, Park Y, Kolonel LN, Ascherio A (2013) Intakes of vitamin C and carotenoids and risk of amyotrophic lateral sclerosis: pooled results from 5 cohort studies. Ann Neurol 73:236–245

    Article  CAS  Google Scholar 

  • Freedman DM, Curtis RE, Daugherty SE, Goedert JJ, Kuncl RW, Tucker MA (2013) The association between cancer and amyotrophic lateral sclerosis. Cancer Causes Control 24:55–60

    Article  Google Scholar 

  • Freedman DM, Wu J, Daugherty SE, Kuncl RW, Enewold LR, Pfeiffer RM (2014) The risk of amyotrophic lateral sclerosis after cancer in U.S. elderly adults: a population-based prospective study. Int. J Cancer 135:1745–1750

    Article  CAS  Google Scholar 

  • Gajdusek DC, Salazar AM (1982) Amyotrophic lateral sclerosis and Parkinsonian syndromes in high incidence among the Auyu and Jakai people of west New Guinea. Neurology 32:107–126

    Article  CAS  Google Scholar 

  • Gallo V, Bueno-De-Mesquita HB, Vermeulen R, Andersen PM, Kyrozis A, Linseisen J, Kaaks R, Allen NE, Roddam AW, Boshuizen HC, Peeters PH, Palli D, Mattiello A, Sieri S, Tumino R, Jimenez-Martin JM, Diaz MJ, Suarez LR, Trichopoulou A, Agudo A, Arriola L, Barricante-Gurrea A, Bingham S, Khaw KT, Manjer J, Lindkvist B, Overvad K, Bach FW, Tjonneland A, Olsen A, Bergmann MM, Boeing H, Clavel-Chapelon F, Lund E, Hallmans G, Middleton L, Vineis P, Riboli E (2009) Smoking and risk for amyotrophic lateral sclerosis: analysis of the EPIC cohort. Ann Neurol 65:378–385

    Article  Google Scholar 

  • Gallo V, Wark PA, Jenab M, Pearce N, Brayne C, Vermeulen R, Andersen PM, Hallmans G, Kyrozis A, Vanacore N, Vahdaninia M, Grote V, Kaaks R, Mattiello A, Bueno-De-Mesquita HB, Peeters PH, Travis RC, Petersson J, Hansson O, Arriola L, Jimenez-Martin JM, Tjonneland A, Halkjaer J, Agnoli C, Sacerdote C, Bonet C, Trichopoulou A, Gavrila D, Overvad K, Weiderpass E, Palli D, Quiros JR, Tumino R, Khaw KT, Wareham N, Barricante-Gurrea A, Fedirko V, Ferrari P, Clavel-Chapelon F, Boutron-Ruault MC, Boeing H, Vigl M, Middleton L, Riboli E, Vineis P (2013) Prediagnostic body fat and risk of death from amyotrophic lateral sclerosis: the EPIC cohort. Neurology 80:829–838

    Article  Google Scholar 

  • Gallo V, Vanacore N, Bueno-De-Mesquita HB, Vermeulen R, Brayne C, Pearce N, Wark PA, Ward HA, Ferrari P, Jenab M, Andersen PM, Wennberg P, Wareham N, Katzke V, Kaaks R, Weiderpass E, Peeters PH, Mattiello A, Pala V, Barricante A, Chirlaque MD, Travier N, Travis RC, Sanchez MJ, Pessah-Rasmussen H, Petersson J, Tjonneland A, Tumino R, Quiros JR, Trichopoulou A, Kyrozis A, Oikonomidou D, Masala G, Sacerdote C, Arriola L, Boeing H, Vigl M, Claver-Chapelon F, Middleton L, Riboli E, Vineis P (2016) Physical activity and risk of amyotrophic lateral sclerosis in a prospective cohort study. Eur J Epidemiol 31:255–266

    Article  Google Scholar 

  • Geser F, Winton MJ, Kwong LK, Xu Y, Xie SX, Igaz LM, Garruto RM, Perl DP, Galasko D, Lee VM, Trojanowski JQ (2008) Pathological TDP-43 in Parkinsonism-dementia complex and amyotrophic lateral sclerosis of Guam. Acta Neuropathol 115:133–145

    Article  CAS  Google Scholar 

  • Gibson SB, Abbott D, Farnham JM, Thai KK, McLean H, Figueroa KP, Bromberg MB, Pulst SM, Cannon-Albright L (2016) Population-based risks for cancer in patients with ALS. Neurology 87:289–294

    Article  Google Scholar 

  • Goldman SM, Tanner CM, Oakes D, Bhudhikanok GS, Gupta A, Langston JW (2006) Head injury and Parkinson’s disease risk in twins. Ann Neurol 60:65–72

    Article  Google Scholar 

  • Gotkine M, Friedlander Y, Hochner H (2014) Triathletes are over-represented in a population of patients with ALS. Amyotroph Lateral Scler Frontotemporal Degener 15:534–536

    Article  Google Scholar 

  • Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 29:173–178

    Article  CAS  Google Scholar 

  • Hamidou B, Couratier P, Besancon C, Nicol M, Preux PM, Marin B (2014) Epidemiological evidence that physical activity is not a risk factor for ALS. Eur J Epidemiol 29:459–475

    Article  Google Scholar 

  • Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865–877

    Article  CAS  Google Scholar 

  • Ishiura H, Takahashi Y, Mitsui J, Yoshida S, Kihira T, Kokubo Y, Kuzuhara S, Ranum LP, Tamaoki T, Ichikawa Y, Date H, Goto J, Tsuji S (2012) C9ORF72 repeat expansion in amyotrophic lateral sclerosis in the Kii peninsula of Japan. Arch Neurol 69:1154–1158

    Article  Google Scholar 

  • Janssen PH, Mandrekar J, Mielke MM, Ahlskog JE, Boeve BF, Josephs K, Savica R (2017) High School Football and Late-Life Risk of Neurodegenerative Syndromes, 1956-1970. Mayo Clin Proc 92:66–71

    Article  Google Scholar 

  • Johnson FO, Atchison WD (2009) The role of environmental mercury, lead and pesticide exposure in development of amyotrophic lateral sclerosis. Neurotoxicology 30:761–765

    Article  CAS  Google Scholar 

  • Kamel F, Umbach DM, Hu H, Munsat TL, Shefner JM, Taylor JA, Sandler DP (2005) Lead exposure as a risk factor for amyotrophic lateral sclerosis. Neurodegener Dis 2:195–201

    Article  CAS  Google Scholar 

  • Kamel F, Umbach DM, Bedlack RS, Richards M, Watson M, Alavanja MC, Blair A, Hoppin JA, Schmidt S, Sandler DP (2012) Pesticide exposure and amyotrophic lateral sclerosis. Neurotoxicology 33:457–462

    Article  CAS  Google Scholar 

  • Kilness AW, Hichberg FH (1977) Amyotrophic lateral sclerosis in a high selenium environment. JAMA 237:2843–2844

    Article  CAS  Google Scholar 

  • Kioumourtzoglou MA, Rotem RS, Seals RM, Gredal O, Hansen J, Weisskopf MG (2015) Diabetes mellitus, obesity, and diagnosis of amyotrophic lateral sclerosis: a population-based study. JAMA Neurol 72:905–911

    Article  Google Scholar 

  • Kuwahara S, Sato Y (2013) Retired American football players have a four times higher chance of getting Alzheimer disease or amyotrophic lateral sclerosis. Brain Nerve 65:996–997

    Google Scholar 

  • Kuzuhara S (2011) Muro disease: amyotrophic lateral sclerosis/Parkinsonism-dementia complex in Kii peninsula of Japan. Brain Nerve 63:119–129

    Google Scholar 

  • Kuzuhara S, Kokubo Y (2005) Atypical Parkinsonism of Japan: amyotrophic lateral sclerosis-Parkinsonism-dementia complex of the Kii peninsula of Japan (Muro disease): an update. Mov Disord 20(Suppl 12):S108–S113

    Article  Google Scholar 

  • Lannuzel A, Mecharles S, Tressieres B, Demoly A, Alhendi R, Hedreville-Tablon MA, Alecu C (2015) Clinical varieties and epidemiological aspects of amyotrophic lateral sclerosis in the Caribbean island of Guadeloupe: a new focus of ALS associated with Parkinsonism. Amyotroph Lateral Scler Frontotemporal Degener 16:216–223

    Article  CAS  Google Scholar 

  • Leese GP, Wang J, Broomhall J, Kelly P, Marsden A, Morrison W, Frier BM, Morris AD (2003) Frequency of severe hypoglycemia requiring emergency treatment in type 1 and type 2 diabetes: a population-based study of health service resource use. Diabetes Care 26:1176–1180

    Article  Google Scholar 

  • Li W, Lee MH, Henderson L, Tyagi R, Bachani M, Steiner J, Campanac E, Hoffman DA, von Geldern G, Johnson K, Maric D, Morris HD, Lentz M, Pak K, Mammen A, Ostrow L, Rothstein J, Nath A (2015) Human endogenous retrovirus-K contributes to motor neuron disease. Sci Transl Med 7:307ra153

    Article  Google Scholar 

  • Lo RY, Tanner CM, Van Den Eeden SK, Albers KB, Leimpeter AD, Nelson LM (2010) Comorbid cancer in Parkinson’s disease. Mov Disord 25:1809–1817

    Article  Google Scholar 

  • MacGowan DJ, Scelsa SN, Imperato TE, Liu KN, Baron P, Polsky B (2007) A controlled study of reverse transcriptase in serum and CSF of HIV-negative patients with ALS. Neurology 68:1944–1946

    Article  CAS  Google Scholar 

  • Malek AM, Barchowsky A, Bowser R, Youk A, Talbott EO (2012) Pesticide exposure as a risk factor for amyotrophic lateral sclerosis: a meta-analysis of epidemiological studies: pesticide exposure as a risk factor for ALS. Environ Res 117:112–119

    Article  CAS  Google Scholar 

  • Maraldi T, Riccio M, Zambonin L, Vinceti M, De Pol A, Hakim G (2011) Low levels of selenium compounds are selectively toxic for a human neuron cell line through ROS/RNS increase and apoptotic process activation. Neurotoxicology 32:180–187

    Article  CAS  Google Scholar 

  • Masseret E, Banack S, Boumediene F, Abadie E, Brient L, Pernet F, Juntas-Morales R, Pageot N, Metcalf J, Cox P, Camu W (2013) Dietary BMAA exposure in an amyotrophic lateral sclerosis cluster from southern France. PLoS One 8:e83406

    Article  CAS  Google Scholar 

  • Morahan JM, Yu B, Trent RJ, Pamphlett R (2007) Genetic susceptibility to environmental toxicants in ALS. Am J Med Genet B Neuropsychiatr Genet 144B:885–890

    Article  CAS  Google Scholar 

  • Murch SJ, Cox PA, Banack SA (2004a) A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc Natl Acad Sci U S A 101:12228–12231

    Article  CAS  Google Scholar 

  • Murch SJ, Cox PA, Banack SA, Steele JC, Sacks OW (2004b) Occurrence of beta-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol Scand 110:267–269

    Article  CAS  Google Scholar 

  • Nelson LM, McGuire V, Longstreth WT Jr, Matkin C (2000) Population-based case-control study of amyotrophic lateral sclerosis in western Washington state. I Cigarette smoking and alcohol consumption. Am J Epidemiol 151:156–163

    Article  CAS  Google Scholar 

  • Nicoletti A, Vasta R, Venti V, Mostile G, Lo FS, Patti F, Scillieri R, De Cicco D, Volanti P, Marziolo R, Maimone D, Fiore M, Ferrante M, Zappia M (2016) The epidemiology of amyotrophic lateral sclerosis in the Mount Etna region: a possible pathogenic role of volcanogenic metals. Eur J Neurol 23:964–972

    Article  CAS  Google Scholar 

  • Nie CL, Wang XS, Liu Y, Perrett S, He RQ (2007) Amyloid-like aggregates of neuronal tau induced by formaldehyde promote apoptosis of neuronal cells. BMC Neurosci 8:9

    Article  CAS  Google Scholar 

  • Nieves JW, Gennings C, Factor-Litvak P, Hupf J, Singleton J, Sharf V, Oskarsson B, Fernandes Filho JA, Sorenson EJ, D'Amico E, Goetz R, Mitsumoto H (2016) Association between dietary intake and function in amyotrophic lateral sclerosis. JAMA Neurol 73:1425–1432

    Article  Google Scholar 

  • Noristani HN, Sabourin JC, Gerber YN, Teigell M, Sommacal A, Vivanco M, Weber M, Perrin FE (2015) Brca1 is expressed in human microglia and is dysregulated in human and animal model of ALS. Mol Neurodegener 10:34

    Article  CAS  Google Scholar 

  • Okamoto K, Kihira T, Kondo T, Kobashi G, Washio M, Sasaki S, Yokoyama T, Miyake Y, Sakamoto N, Inaba Y, Nagai M (2007) Nutritional status and risk of amyotrophic lateral sclerosis in Japan. Amyotroph Lateral Scler 8:300–304

    Article  Google Scholar 

  • Pamphlett R, Waley P (1998) Mercury in human spinal motor neurons. Acta Neuropathol 96:515–519

    Article  CAS  Google Scholar 

  • Pearce N, Gallo V, McElvenny D (2015) Head trauma in sport and neurodegenerative disease: an issue whose time has come? Neurobiol Aging 36:1383–1389

    Article  Google Scholar 

  • Pinkerton LE, Hein MJ, Meyers A, Kamel F (2013) Assessment of ALS mortality in a cohort of formaldehyde-exposed garment workers. Amyotroph Lateral Scler Frontotemporal Degener 14:353–355

    Article  Google Scholar 

  • Plassman BL, Williams JW Jr, Burke JR, Holsinger T, Benjamin S (2010) Systematic review: factors associated with risk for and possible prevention of cognitive decline in later life. Ann Intern Med 153:182–193

    Article  Google Scholar 

  • Potgieter M, Bester J, Kell DB, Pretorius E (2015) The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol Rev 39:567–591

    Article  Google Scholar 

  • Poulletier DG, Ruffie G, Taxile M, Ladeveze E, Hurtier A, Haro E, Duleu S, Charlet DS, Billaudel B, Geffard M, Veyret B, Lagroye I (2009) Amyotrophic lateral sclerosis (ALS) and extremely-low frequency (ELF) magnetic fields: a study in the SOD-1 transgenic mouse model. Amyotroph Lateral Scler 10:370–373

    Article  Google Scholar 

  • Praline J, Guennoc AM, Limousin N, Hallak H, de Toffol B, Corcia P (2007) ALS and mercury intoxication: a relationship? Clin Neurol Neurosurg 109:880–883

    Article  Google Scholar 

  • Reed DM, Brody JA (1975) Amyotrophic lateral sclerosis and Parkinsonism-dementia on Guam, 1945-1972. I Descriptive epidemiology. Am J Epidemiol 101:287–301

    Article  CAS  Google Scholar 

  • Reed D, Plato C, Elizan T, Kurland LT (1966) The amyotrophic lateral sclerosis/Parkinsonism-dementia complex: a ten-year follow-up on Guam. I Epidemiologic studies. Am J Epidemiol 83:54–73

    Article  CAS  Google Scholar 

  • Riancho J (2016) Retinoids and PPAR agonists: promising partners in neurodegenerative diseases? Free Radic Biol Med 97:616–617

    Article  CAS  Google Scholar 

  • Riancho J, Ruiz-Soto M, Berciano MT, Berciano J, Lafarga M (2015) Neuroprotective effect of bexarotene in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Front Cell Neurosci 9:250

    Article  CAS  Google Scholar 

  • Riancho J, Berciano MT, Berciano J, Lafarga M (2016a) Relaunching an old drug: the potential role of bexarotene in neurodegenerative diseases. J Neurol 263:177–178

    Article  Google Scholar 

  • Riancho J, Berciano MT, Ruiz-Soto M, Berciano J, Landreth G, Lafarga M (2016b) Retinoids and motor neuron disease: potential role in amyotrophic lateral sclerosis. J Neurol Sci 360:115–120

    Article  CAS  Google Scholar 

  • Riancho J, Gonzalo I, Ruiz-Soto M, Berciano J (2016c) Why do motor neurons degenerate? Actualization in the pathogenesis of amyotrophic lateral sclerosis. Neurologia

  • Riancho J, Lozano-Cuesta P, Santurtun A, Sanchez-Juan P, Lopez-Vega JM, Berciano J, Polo JM (2016d) Amyotrophic lateral sclerosis in northern Spain 40 years later: what has changed? Neurodegener Dis 16:337–341

    Article  Google Scholar 

  • Roberts AL, Johnson NJ, Cudkowicz ME, Eum KD, Weisskopf MG (2015) Job-related formaldehyde exposure and ALS mortality in the USA. J Neurol Neurosurg Psychiatry

  • Roberts AL, Johnson NJ, Chen JT, Cudkowicz ME, Weisskopf MG (2016) Race/ethnicity, socioeconomic status, and ALS mortality in the United States. Neurology 87:2300–2308

    Article  Google Scholar 

  • Rooney J (2011) Further thoughts on mercury, epigenetics, genetics and amyotrophic lateral sclerosis. Neurodegener Dis 8:523–524

    Article  Google Scholar 

  • Rooney J, Vajda A, Heverin M, Elamin M, Crampsie A, McLaughlin R, Staines A, Hardiman O (2015a) Spatial cluster analysis of population amyotrophic lateral sclerosis risk in Ireland. Neurology 84:1537–1544

    Article  Google Scholar 

  • Rooney JP, Tobin K, Crampsie A, Vajda A, Heverin M, McLaughlin R, Staines A, Hardiman O (2015b) Social deprivation and population density are not associated with small area risk of amyotrophic lateral sclerosis. Environ Res 142:141–147

    Article  CAS  Google Scholar 

  • Rothman KJ, Lash TL, Greenland S (2008) Modern epidemiology. Lippincott Williams & Wilkins

  • Santurtun A, Villar A, Delgado-Alvarado M, Riancho J (2016a) Trends in motor neuron disease: association with latitude and air lead levels in Spain. Neurol Sci

  • Santurtun A, Villar A, Lopez-Delgado L, Riancho J (2016b) Amyotrophic lateral sclerosis and richness: a correlation study across Spain. J Neurol Sci 367:380–381

    Article  Google Scholar 

  • Satizabal CL, Beiser AS, Chouraki V, Chene G, Dufouil C, Seshadri S (2016) Incidence of dementia over three decades in the Framingham heart study. N Engl J Med 374:523–532

    Article  CAS  Google Scholar 

  • Schmidt ML, Lee VM, Saido T, Perl D, Schuck T, Iwatsubo T, Trojanowski JQ (1998) Amyloid plaques in Guam amyotrophic lateral sclerosis/Parkinsonism-dementia complex contain species of a beta similar to those found in the amyloid plaques of Alzheimer’s disease and pathological aging. Acta Neuropathol 95:117–122

    Article  CAS  Google Scholar 

  • Schmidt S, Kwee LC, Allen KD, Oddone EZ (2010) Association of ALS with head injury, cigarette smoking and APOE genotypes. J Neurol Sci 291:22–29

    Article  CAS  Google Scholar 

  • Schwarz S, Husstedt I, Bertram HP, Kuchelmeister K (1996) Amyotrophic lateral sclerosis after accidental injection of mercury. J Neurol Neurosurg Psychiatry 60:698

    Article  CAS  Google Scholar 

  • Sebeo J, Hof PR, Perl DP (2004) Occurrence of alpha-synuclein pathology in the cerebellum of Guamanian patients with Parkinsonism-dementia complex. Acta Neuropathol 107:497–503

    Article  CAS  Google Scholar 

  • Seelen M, van Doormaal PT, Visser AE, Huisman MH, Roozekrans MH, de Jong SW, van der Kooi AJ, de Visser M, Voermans NC, Veldink JH, van den Berg LH (2014) Prior medical conditions and the risk of amyotrophic lateral sclerosis. J Neurol 261:1949–1956

    Article  CAS  Google Scholar 

  • Shah PP, Lockwood WW, Saurabh K, Kurlawala Z, Shannon SP, Waigel S, Zacharias W, Beverly LJ (2015) Ubiquilin1 represses migration and epithelial-to-mesenchymal transition of human non-small cell lung cancer cells. Oncogene 34:1709–1717

    Article  CAS  Google Scholar 

  • Sieh W, Choi Y, Chapman NH, Craig UK, Steinbart EJ, Rothstein JH, Oyanagi K, Garruto RM, Bird TD, Galasko DR, Schellenberg GD, Wijsman EM (2009) Identification of novel susceptibility loci for Guam neurodegenerative disease: challenges of genome scans in genetic isolates. Hum Mol Genet 18:3725–3738

    Article  CAS  Google Scholar 

  • Spencer PS, Palmer VS, Ludolph AC (2005) On the decline and etiology of high-incidence motor system disease in West Papua (southwest New Guinea). Mov Disord 20(Suppl 12):S119–S126

    Article  Google Scholar 

  • Steele AJ, Al Chalabi A, Ferrante K, Cudkowicz ME, Brown RH Jr, Garson JA (2005) Detection of serum reverse transcriptase activity in patients with ALS and unaffected blood relatives. Neurology 64:454–458

    Article  CAS  Google Scholar 

  • Sutedja NA, Fischer K, Veldink JH, van der Heijden GJ, Kromhout H, Heederik D, Huisman MH, Wokke JJ, van den Berg LH (2009) What we truly know about occupation as a risk factor for ALS: a critical and systematic review. Amyotroph Lateral Scler 10:295–301

    Article  Google Scholar 

  • Talbott EO, Malek AM, Lacomis D (2016) The epidemiology of amyotrophic lateral sclerosis. Handb Clin Neurol 138:225–238

    Article  CAS  Google Scholar 

  • Tanaka H, Hoshino Y, Watanabe Y, Sakurai K, Takekawa H, Hirata K (2012) A case of strategic-infarct mild cognitive impairment. Neurologist 18:211–213

    Article  Google Scholar 

  • TORRES J, IRIARTE LL, Kurland LT (1957) Amyotrophic lateral sclerosis among Guamanians in California. Calif Med 86:385–388

    CAS  Google Scholar 

  • Tremlett H, Bauer KC, Appel-Cresswell S, Finlay BB, Waubant E (2017) The gut microbiome in human neurological disease: a review. Ann Neurol 81:369–382

    Article  Google Scholar 

  • Trias E, Ibarburu S, Barreto-Nunez R, Babdor J, Maciel TT, Guillo M, Gros L, Dubreuil P, Diaz-Amarilla P, Cassina P, Martinez-Palma L, Moura IC, Beckman JS, Hermine O, Barbeito L (2016) Post-paralysis tyrosine kinase inhibition with masitinib abrogates neuroinflammation and slows disease progression in inherited amyotrophic lateral sclerosis. J Neuroinflammation 13:177

    Article  CAS  Google Scholar 

  • Turner MR, Abisgold J, Yeates DG, Talbot K, Goldacre MJ (2010) Head and other physical trauma requiring hospitalisation is not a significant risk factor in the development of ALS. J Neurol Sci 288:45–48

    Article  Google Scholar 

  • Turner MR, Goldacre R, Ramagopalan S, Talbot K, Goldacre MJ (2013) Autoimmune disease preceding amyotrophic lateral sclerosis: an epidemiologic study. Neurology 81:1222–1225

    Article  CAS  Google Scholar 

  • Turner MR, Goldacre R, Talbot K, Goldacre MJ (2016) Cerebrovascular injury as a risk factor for amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 87:244–246

    Article  Google Scholar 

  • Vaisman N, Lusaus M, Nefussy B, Niv E, Comaneshter D, Hallack R, Drory VE (2009) Do patients with amyotrophic lateral sclerosis (ALS) have increased energy needs? J Neurol Sci 279:26–29

    Article  Google Scholar 

  • Van Den HC, Thornton E, Vink R (2007) Traumatic brain injury and Alzheimer’s disease: a review. Prog Brain Res 161:303–316

    Article  CAS  Google Scholar 

  • Vinceti M, Guidetti D, Pinotti M, Rovesti S, Merlin M, Vescovi L, Bergomi M, Vivoli G (1996) Amyotrophic lateral sclerosis after long-term exposure to drinking water with high selenium content. Epidemiology 7:529–532

    Article  CAS  Google Scholar 

  • Visser AE, Seelen M, Hulsbergen A, de Graaf J, van der Kooi AJ, Raaphorst J, Veldink JH, van den Berg LH (2017a) Exploring the fitness hypothesis in ALS: a population-based case-control study of parental cause of death and lifespan. J Neurol Neurosurg Psychiatry

  • Visser AE, Verduyn Lunel FM, Veldink JH, van den Berg LH (2017b) No association between Borrelia burgdorferi antibodies and amyotrophic lateral sclerosis in a case-control study. Eur J Neurol 24:227–230

    Article  CAS  Google Scholar 

  • Watanabe Y, Watanabe T (2017) Meta-analytic evaluation of the association between head injury and risk of amyotrophic lateral sclerosis. Eur J Epidemiol 32:867–879

    Article  Google Scholar 

  • Weisskopf MG, Morozova N, O'Reilly EJ, McCullough ML, Calle EE, Thun MJ, Ascherio A (2009) Prospective study of chemical exposures and amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 80:558–561

    Article  CAS  Google Scholar 

  • Zhang YG, Wu S, Yi J, Xia Y, Jin D, Zhou J, Sun J (2017) Target intestinal microbiota to alleviate disease progression in amyotrophic lateral sclerosis. Clin Ther 39:322–336

    Article  Google Scholar 

  • Zhou H, Chen G, Chen C, Yu Y, Xu Z (2012) Association between extremely low-frequency electromagnetic fields occupations and amyotrophic lateral sclerosis: a meta-analysis. PLoS One 7:e48354

    Article  CAS  Google Scholar 

  • Zufiria M, Gil-Bea FJ, Fernandez-Torron R, Poza JJ, Munoz-Blanco JL, Rojas-Garcia R, Riancho J, de Munain AL (2016) ALS: a bucket of genes, environment, metabolism and unknown ingredients. Prog Neurobiol 142:104–129

    Article  CAS  Google Scholar 

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The authors declare that they have no competing interests.

Funding

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

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Authors and Affiliations

  1. Service of Neurology, Hospital Sierrallana, Institute of Research Valdecilla (IDIVAL), Torrelavega, Spain

    Javier Riancho

  2. Department of Medicine, University of Cantabria, Santander, Spain

    Javier Riancho

  3. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, CIBERNED, Instituto Carlos III, Ministry of Economy and Competitiveness, Madrid, Spain

    Javier Riancho, Mónica Povedano & Adolfo López de Munaín

  4. Service of Neurology, University Hospital Marques de Valdecilla, Santander, Spain

    Pilar Bosque-Varela & Sara Perez-Pereda

  5. Service of Neurology-Motor Neuron Unit, IDIBELL, Bellvitge University Hospital, Barcelona, Spain

    Mónica Povedano

  6. ALS Multidisciplinary Unit, Hospital Donostia- Neuroscience Area, Donostia Health Research Institute, San Sebastián, Spain

    Adolfo López de Munaín

  7. Toxicology Unit, Physiology and Farmacology Department, University of Cantabria-IDIVAL, Santander, Spain

    Ana Santurtun

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  1. Javier Riancho
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  2. Pilar Bosque-Varela
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  3. Sara Perez-Pereda
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  4. Mónica Povedano
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  5. Adolfo López de Munaín
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Correspondence to Javier Riancho.

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Riancho, J., Bosque-Varela, P., Perez-Pereda, S. et al. The increasing importance of environmental conditions in amyotrophic lateral sclerosis. Int J Biometeorol 62, 1361–1374 (2018). https://doi.org/10.1007/s00484-018-1550-2

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  • DOI: https://doi.org/10.1007/s00484-018-1550-2

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