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Global variation in prevalence and incidence of amyotrophic lateral sclerosis: a systematic review and meta-analysis

  • Lu Xu
  • Tanxin Liu
  • Lili Liu
  • Xiaoying Yao
  • Lu Chen
  • Dongsheng Fan
  • Siyan ZhanEmail author
  • Shengfeng WangEmail author
Original Communication

Abstract

Background

Amyotrophic lateral sclerosis (ALS) is a global disease, which adversely affects the life quality of patients and significantly increases the burden of families and society. We aimed to assess the changing incidence, prevalence of ALS around the world.

Methods

We searched Medline, Embase, Web of Science, and Cochrane library to identify articles published until September 9, 2018. Each included study was independently reviewed for methodological quality by two reviewers. We used a random-effects model to summarize individual studies and assessed heterogeneity (I2) with the χ2 test on Cochrane’s Q statistic.

Results

We identified 124 studies that were eligible for final inclusion, including 110 studies of incidence and 58 studies of prevalence. The overall crude worldwide ALS prevalence and incidence were 4.42 (95% CI 3.92–4.96) per 1,00,000 population and 1.59 (95% CI 1.39–1.81) per 1,00,000 person-years, respectively. ALS prevalence and incidence increased by age until the age of 70–79. Since 1957, incidence has been significantly rising year by year, and this upward trend was weakened after standardization. The longest survival time were in Asia (ranging from 3.74 years in South Asia to 9.23 years in West Asia).

Conclusions

With the aggravation of population aging and the rapid growth of economy, developing regions following the development pattern of the developed regions may suffer rising ALS prevalence and incidence which may increase their disease burden as well. These data highlight the need for research into underlying mechanism and innovations in health-care systems.

Keywords

Amyotrophic lateral sclerosis Incidence Prevalence Meta-analysis 

Notes

Acknowledgements

The authors would like to thank Xuefeng Lai, Jinlang Lv, Junyou Yu, Wei Zhang, and Huan Yu for retrieving and managing articles as well as extracting data.

Funding

This study was funded by the National Natural Science Foundation (grant number 91646107).

The manuscript does not contain clinical studies or patient data.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

415_2019_9652_MOESM1_ESM.pdf (1.8 mb)
Supplementary file1 (PDF 1797 kb)

References

  1. 1.
    Brown RH, Al-Chalabi A (2017) Amyotrophic lateral sclerosis. N Engl J Med 377:162–172.  https://doi.org/10.1056/NEJMra1603471 CrossRefPubMedGoogle Scholar
  2. 2.
    Montuschi A, Iazzolino B, Calvo A, Moglia C, Lopiano L, Restagno G, Brunetti M, Ossola I, Lo Presti A, Cammarosano S, Canosa A, Chio A (2015) Cognitive correlates in amyotrophic lateral sclerosis: a population-based study in Italy. J Neurol Neurosurg Psychiatry 86:168–173.  https://doi.org/10.1136/jnnp-2013-307223 CrossRefPubMedGoogle Scholar
  3. 3.
    Phukan J, Elamin M, Bede P, Jordan N, Gallagher L, Byrne S, Lynch C, Pender N, Hardiman O (2012) The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry 83:102–108.  https://doi.org/10.1136/jnnp-2011-300188 CrossRefPubMedGoogle Scholar
  4. 4.
    Logroscino G, Piccininni M, Marin B, Nichols E, Abd-Allah F, Abdelalim A, Alahdab F, Asgedom SW, Awasthi A, Chaiah Y, Daryani A, Do HP, Dubey M, Elbaz A, Eskandarieh S, Farhadi F, Farzadfar F, Fereshtehnejad S-M, Fernandes E, Filip I, Foreman KJ, Gebre AK, Gnedovskaya EV, Hamidi S, Hay SI, Irvani SSN, Ji JS, Kasaeian A, Kim YJ, Mantovani LG, Mashamba-Thompson TP, Mehndiratta MM, Mokdad AH, Nagel G, Nguyen TH, Nixon MR, Olagunju AT, Owolabi MO, Piradov MA, Qorbani M, Radfar A, Reiner RC, Sahraian MA, Sarvi S, Sharif M, Temsah O, Tran BX, Truong NT, Venketasubramanian N, Winkler AS, Yimer EM, Feigin VL, Vos T, Murray CJL (2018) Global, regional, and national burden of motor neuron diseases 1990–2016: a systematic analysis for the global burden of disease study 2016. Lancet Neurol 17:1083–1097.  https://doi.org/10.1016/s1474-4422(18)30404-6 CrossRefGoogle Scholar
  5. 5.
    Baeza-Yates R, Sangal PM, Villoslada P (2017) Burden of neurological diseases in the US revealed by web searches. PLoS ONE 12:e0178019.  https://doi.org/10.1371/journal.pone.0178019 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Tysnes OB, Vollset SE, Aarli JA (1991) Epidemiology of amyotrophic lateral sclerosis in Hordaland county, western Norway. Acta Neurol Scand 83:280–285CrossRefGoogle Scholar
  7. 7.
    Benjaminsen E, Alstadhaug KB, Baloch F, Gulsvik M, Odeh F (2017) Amyotrophic lateral sclerosis in Nordland County, Norway 2000–2015. Eur J Neurol 24:28CrossRefGoogle Scholar
  8. 8.
    Tsai C-P, Wang K-C, Hwang C-S, Lee IT, Lee CT-C (2015) Incidence, prevalence, and medical expenditures of classical amyotrophic lateral sclerosis in Taiwan, 1999–2008. J Formos Med Assoc 114:612–619.  https://doi.org/10.1016/j.jfma.2013.01.008 CrossRefPubMedGoogle Scholar
  9. 9.
    McKenzie JE, Beller EM, Forbes AB (2016) Introduction to systematic reviews and meta-analysis. Respirology 21:626–637.  https://doi.org/10.1111/resp.12783 CrossRefPubMedGoogle Scholar
  10. 10.
    Marin B, Boumediene F, Logroscino G, Couratier P, Babron MC, Leutenegger AL, Copetti M, Preux PM, Beghi E (2017) Variation in worldwide incidence of amyotrophic lateral sclerosis: a meta-analysis. Int J Epidemiol 46:57–74.  https://doi.org/10.1093/ije/dyw061 CrossRefGoogle Scholar
  11. 11.
    Chio A, Logroscino G, Traynor BJ, Collins J, Simeone JC, Goldstein LA, White LA (2013) Global epidemiology of amyotrophic lateral sclerosis: a systematic review of the published literature. Neuroepidemiology 41:118–130.  https://doi.org/10.1159/000351153 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    D'Ovidio F, d'Errico A, Farina E, Calvo A, Costa G, Chio A (2016) Amyotrophic lateral sclerosis incidence and previous prescriptions of drugs for the nervous system. Neuroepidemiology 47:59–66.  https://doi.org/10.1159/000448618 CrossRefPubMedGoogle Scholar
  13. 13.
    Moura MC, Casulari LA, Carvalho Garbi Novaes MR (2016) Ethnic and demographic incidence of amyotrophic lateral sclerosis (ALS) in Brazil: a population based study. Amyotroph Lateral Scler Frontotemporal Degener 17:275–281.  https://doi.org/10.3109/21678421.2016.1140210 CrossRefGoogle Scholar
  14. 14.
    Scialo C, Novi G, Bandettini di Poggio M, Canosa A, Sormani MP, Mandich P, Origone P, Truffelli R, Mancardi GL, Caponnetto C (2016) Clinical epidemiology of amyotrophic lateral sclerosis in Liguria, Italy: an update of LIGALS register. Amyotroph Lateral Scler Frontotemporal Degener 17:535–542.  https://doi.org/10.1080/21678421.2016.1197942 CrossRefPubMedGoogle Scholar
  15. 15.
    Tesauro M, Consonni M, Filippini T, Mazzini L, Pisano F, Chio A, Esposito A, Vinceti M (2017) Incidence of amyotrophic lateral sclerosis in the province of Novara, Italy, and possible role of environmental pollution. Amyotroph Lateral Scler Frontotemporal Degener 18:284–290.  https://doi.org/10.1080/21678421.2017.1281961 CrossRefPubMedGoogle Scholar
  16. 16.
    Weil C, Zach N, Rishoni S, Shalev V, Chodick G (2016) Epidemiology of amyotrophic lateral sclerosis: a population-based study in Israel. Neuroepidemiology 47:76–81.  https://doi.org/10.1159/000448921 CrossRefPubMedGoogle Scholar
  17. 17.
    Demetriou CA, Hadjivasiliou PM, Kleopa KA, Christou YP, Leonidou E, Kyriakides T, Zamba-Papanicolaou E (2017) Epidemiology of amyotrophic lateral sclerosis in the Republic of Cyprus: a 25-year retrospective study. Neuroepidemiology 48:79–85.  https://doi.org/10.1159/000477126 CrossRefPubMedGoogle Scholar
  18. 18.
    Kahana E, Alter M, Feldman S (1976) Amyotrophic lateral sclerosis: a population study. J Neurol 212:205–213CrossRefGoogle Scholar
  19. 19.
    Okumiya K, Wada T, Fujisawa M, Ishine M, Garcia Del Saz E, Hirata Y, Kuzuhara S, Kokubo Y, Seguchi H, Sakamoto R, Manuaba I, Watofa P, Rantetampang AL, Matsubayashi K (2014) Amyotrophic lateral sclerosis and parkinsonism in Papua, indonesia: 2001–2012 survey results. BMJ open 4:e004353.  https://doi.org/10.1136/bmjopen-2013-004353 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Boyle MH (1998) Guidelines for evaluating prevalence studies. Evid Based Ment Health 1:37–39CrossRefGoogle Scholar
  21. 21.
    Loney PL, Chambers LW, Bennett KJ, Roberts JG, Stratford PW (1998) Critical appraisal of the health research literature: prevalence or incidence of a health problem. Chronic Dis Can 19:170–176PubMedGoogle Scholar
  22. 22.
    Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J, Pringsheim T, Lorenzetti DL, Jette N (2017) Prevalence and incidence of epilepsy: a systematic review and meta-analysis of international studies. Neurology 88:296–303.  https://doi.org/10.1212/wnl.0000000000003509 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Noubiap JJ, Bigna JJ, Nansseu JR, Nyaga UF, Balti EV, Echouffo-Tcheugui JB, Kengne AP (2018) Prevalence of dyslipidaemia among adults in Africa: a systematic review and meta-analysis. Lancet Glob Health 6:e998–e1007.  https://doi.org/10.1016/s2214-109x(18)30275-4 CrossRefPubMedGoogle Scholar
  24. 24.
    Noubiap JJ, Nansseu JR, Nyaga UF, Nkeck JR, Endomba FT, Kaze AD, Agbor VN, Bigna JJ (2019) Global prevalence of diabetes in active tuberculosis: a systematic review and meta-analysis of data from 2.3 million patients with tuberculosis. Lancet Glob Health 7:e448–e460.  https://doi.org/10.1016/s2214-109x(18)30487-x CrossRefPubMedGoogle Scholar
  25. 25.
    Etminan N, Chang HS, Hackenberg K, de Rooij NK, Vergouwen MDI, Rinkel GJE, Algra A (2019) Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: a systematic review and meta-analysis. JAMA neurol 76:588–597.  https://doi.org/10.1001/jamaneurol.2019.0006 CrossRefPubMedGoogle Scholar
  26. 26.
    Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, Panaccione R, Ghosh S, Wu JCY, Chan FKL, Sung JJY, Kaplan GG (2018) Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 390:2769–2778.  https://doi.org/10.1016/s0140-6736(17)32448-0 CrossRefPubMedGoogle Scholar
  27. 27.
    Freeman J, Hutchison GB (1980) Prevalence, incidence and duration. Am J Epidemiol 112:707–723.  https://doi.org/10.1093/oxfordjournals.aje.a113043 CrossRefPubMedGoogle Scholar
  28. 28.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558.  https://doi.org/10.1002/sim.1186 CrossRefGoogle Scholar
  29. 29.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634CrossRefGoogle Scholar
  30. 30.
    Marin B, Fontana A, Arcuti S, Copetti M, Boumediene F, Couratier P, Beghi E, Preux PM, Logroscino G (2018) Age-specific ALS incidence: a dose-response meta-analysis. Eur J Epidemiol 33:621–634.  https://doi.org/10.1007/s10654-018-0392-x CrossRefPubMedGoogle Scholar
  31. 31.
    Taskent RO, Gokcumen O (2017) The Multiple histories of Western Asia: perspectives from ancient and modern genomes. Hum Biol 89:107–117CrossRefGoogle Scholar
  32. 32.
    Anne MB, Judith RK, Joanna LM, Joan MH, Luciano C, Kenneth KK, Luca LC (1991) Drift, admixture, and selection in human evolution: a study with DNA polymorphisms. Proc Nati Acad Sci 88:839–843CrossRefGoogle Scholar
  33. 33.
    Luca LCS (1997) Genes, peoples, and languages. Proc Natl Acad Sci 94:7719–7724CrossRefGoogle Scholar
  34. 34.
    van Es MA, Veldink JH, Saris CG, Blauw HM, van Vught PW, Birve A, Lemmens R, Schelhaas HJ, Groen EJ, Huisman MH, van der Kooi AJ, de Visser M, Dahlberg C, Estrada K, Rivadeneira F, Hofman A, Zwarts MJ, van Doormaal PT, Rujescu D, Strengman E, Giegling I, Muglia P, Tomik B, Slowik A, Uitterlinden AG, Hendrich C, Waibel S, Meyer T, Ludolph AC, Glass JD, Purcell S, Cichon S, Nothen MM, Wichmann HE, Schreiber S, Vermeulen SH, Kiemeney LA, Wokke JH, Cronin S, McLaughlin RL, Hardiman O, Fumoto K, Pasterkamp RJ, Meininger V, Melki J, Leigh PN, Shaw CE, Landers JE, Al-Chalabi A, Brown RH Jr, Robberecht W, Andersen PM, Ophoff RA, van den Berg LH (2009) Genome-wide association study identifies 19p13.3 (UNC13A) and 9p21.2 as susceptibility loci for sporadic amyotrophic lateral sclerosis. Nat Genet 41:1083–1087.  https://doi.org/10.1038/ng.442 CrossRefPubMedGoogle Scholar
  35. 35.
    Diekstra FP, Saris CG, van Rheenen W, Franke L, Jansen RC, van Es MA, van Vught PW, Blauw HM, Groen EJ, Horvath S, Estrada K, Rivadeneira F, Hofman A, Uitterlinden AG, Robberecht W, Andersen PM, Melki J, Meininger V, Hardiman O, Landers JE, Brown RH Jr, Shatunov A, Shaw CE, Leigh PN, Al-Chalabi A, Ophoff RA, van den Berg LH, Veldink JH (2012) Mapping of gene expression reveals CYP27A1 as a susceptibility gene for sporadic ALS. PLoS ONE 7:e35333.  https://doi.org/10.1371/journal.pone.0035333 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Uyan O, Omur O, Agim ZS, Ozoguz A, Li H, Parman Y, Deymeer F, Oflazer P, Koc F, Tan E, Ozcelik H, Basak AN (2013) Genome-wide copy number variation in sporadic amyotrophic lateral sclerosis in the Turkish population: deletion of EPHA3 is a possible protective factor. PLoS ONE 8:e72381.  https://doi.org/10.1371/journal.pone.0072381 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Fogh I, Ratti A, Gellera C, Lin K, Tiloca C, Moskvina V, Corrado L, Soraru G, Cereda C, Corti S, Gentilini D, Calini D, Castellotti B, Mazzini L, Querin G, Gagliardi S, Del Bo R, Conforti FL, Siciliano G, Inghilleri M, Sacca F, Bongioanni P, Penco S, Corbo M, Sorbi S, Filosto M, Ferlini A, Di Blasio AM, Signorini S, Shatunov A, Jones A, Shaw PJ, Morrison KE, Farmer AE, Van Damme P, Robberecht W, Chio A, Traynor BJ, Sendtner M, Melki J, Meininger V, Hardiman O, Andersen PM, Leigh NP, Glass JD, Overste D, Diekstra FP, Veldink JH, van Es MA, Shaw CE, Weale ME, Lewis CM, Williams J, Brown RH, Landers JE, Ticozzi N, Ceroni M, Pegoraro E, Comi GP, D'Alfonso S, van den Berg LH, Taroni F, Al-Chalabi A, Powell J, Silani V (2014) A genome-wide association meta-analysis identifies a novel locus at 17q11.2 associated with sporadic amyotrophic lateral sclerosis. Hum Mol Genet 23:2220–2231.  https://doi.org/10.1093/hmg/ddt587 CrossRefPubMedGoogle Scholar
  38. 38.
    Du Y, Wen Y, Guo X, Hao J, Wang W, He A, Fan Q, Li P, Liu L, Liang X, Zhang F (2018) A Genome-wide expression association analysis identifies genes and pathways associated with amyotrophic lateral sclerosis. Cell Mol Neurobiol 38:635–639.  https://doi.org/10.1007/s10571-017-0512-2 CrossRefPubMedGoogle Scholar
  39. 39.
    Shatunov A, Mok K, Newhouse S, Weale ME, Smith B, Vance C, Johnson L, Veldink JH, van Es MA, van den Berg LH, Robberecht W, Van Damme P, Hardiman O, Farmer AE, Lewis CM, Butler AW, Abel O, Andersen PM, Fogh I, Silani V, Chio A, Traynor BJ, Melki J, Meininger V, Landers JE, McGuffin P, Glass JD, Pall H, Leigh PN, Hardy J, Brown RH Jr, Powell JF, Orrell RW, Morrison KE, Shaw PJ, Shaw CE, Al-Chalabi A (2010) Chromosome 9p21 in sporadic amyotrophic lateral sclerosis in the UK and seven other countries: a genome-wide association study. Lancet Neurol 9:986–994.  https://doi.org/10.1016/s1474-4422(10)70197-6 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Balendra R, Isaacs AM (2018) C9orf72-mediated ALS and FTD: multiple pathways to disease. Nat Rev Neurol 14:544–558.  https://doi.org/10.1038/s41582-018-0047-2 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lloyd-Sherlock P (1982) (2000) Population ageing in developed and developing regions: implications for health policy. Soc Sci Med 51:887–895CrossRefGoogle Scholar
  42. 42.
    A Chio G Mora C Moglia U Manera A Canosa S Cammarosano A Ilardi D Bertuzzo E Bersano P Cugnasco M Grassano F Pisano L Mazzini A Calvo VD Piemonte Register for ALS 2017 Secular trends of amyotrophic lateral sclerosis: the piemonte and valle d'aosta register, JAMA Neurol 74: 1097–1104 10.1001/jamaneurol.2017.1387CrossRefGoogle Scholar
  43. 43.
    Arthur KC, Calvo A, Price TR, Geiger JT, Chio A, Traynor BJ (2016) Projected increase in amyotrophic lateral sclerosis from 2015 to 2040. Nat Commun 7:12408.  https://doi.org/10.1038/ncomms12408 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Shahrizaila N, Sobue G, Kuwabara S, Kim SH, Birks C, Fan DS, Bae JS, Hu CJ, Gourie-Devi M, Noto Y, Shibuya K, Goh KJ, Kaji R, Tsai CP, Cui L, Talman P, Henderson RD, Vucic S, Kiernan MC (2016) Amyotrophic lateral sclerosis and motor neuron syndromes in Asia. J Neurol Neurosurg Psychiatry 87:821–830.  https://doi.org/10.1136/jnnp-2015-312751 CrossRefPubMedGoogle Scholar
  45. 45.
    Chen L, Zhang B, Chen R, Tang L, Liu R, Yang Y, Yang Y, Liu X, Ye S, Zhan S, Fan D (2015) Natural history and clinical features of sporadic amyotrophic lateral sclerosis in China. J Neurol Neurosurg Psychiatry 86:1075–1081.  https://doi.org/10.1136/jnnp-2015-310471 CrossRefPubMedGoogle Scholar
  46. 46.
    Dorst J, Chen L, Rosenbohm A, Dreyhaupt J, Hubers A, Schuster J, Weishaupt JH, Kassubek J, Gess B, Meyer T, Weyen U, Hermann A, Winkler J, Grehl T, Hagenacker T, Lingor P, Koch JC, Sperfeld A, Petri S, Grosskreutz J, Metelmann M, Wolf J, Winkler AS, Klopstock T, Boentert M, Johannesen S, Storch A, Schrank B, Zeller D, Liu XL, Tang L, Fan DS, Ludolph AC (2019) Prognostic factors in ALS: a comparison between Germany and China. J Neurol 266:1516–1525.  https://doi.org/10.1007/s00415-019-09290-4 CrossRefPubMedGoogle Scholar
  47. 47.
    Lee CT, Chiu YW, Wang KC, Hwang CS, Lin KH, Lee IT, Tsai CP (2013) Riluzole and prognostic factors in amyotrophic lateral sclerosis long-term and short-term survival: a population-based study of 1149 cases in Taiwan. J Epidemiol 23:35–40.  https://doi.org/10.2188/jea.je20120119 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Rabkin J, Ogino M, Goetz R, McElhiney M, Marziliano A, Imai T, Atsuta N, Morita M, Tateishi T, Matsumura T, Mitsumoto H (2013) Tracheostomy with invasive ventilation for ALS patients: neurologists' roles in the US and Japan. Amyotroph Lateral Scler Frontotemporal Degener 14:116–123.  https://doi.org/10.3109/17482968.2012.726226 CrossRefPubMedGoogle Scholar
  49. 49.
    Floeter MK, Traynor BJ, Farren J, Braun LE, Tierney M, Wiggs EA, Wu T (2017) Disease progression in C9orf72 mutation carriers. Neurology 89:234–241.  https://doi.org/10.1212/wnl.0000000000004115 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Trojsi F, Siciliano M, Femiano C, Santangelo G, Lunetta C, Calvo A, Moglia C, Marinou K, Ticozzi N, Ferro C, Scialo C, Soraru G, Conte A, Falzone YM, Tortelli R, Russo M, Sansone VA, Chio A, Mora G, Silani V, Volanti P, Caponnetto C, Querin G, Sabatelli M, Riva N, Logroscino G, Messina S, Fasano A, Monsurro MR, Tedeschi G, Mandrioli J (2019) Comparative analysis of C9orf72 and sporadic disease in a large multicenter als population: the effect of male sex on survival of C9orf72 positive patients. Front Neurosci 13:485.  https://doi.org/10.3389/fnins.2019.00485 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Al-Chalabi A, Hardiman O (2013) The epidemiology of ALS: a conspiracy of genes, environment and time. Nat Rev Neurol 9:617–628.  https://doi.org/10.1038/nrneurol.2013.203 CrossRefPubMedGoogle Scholar
  52. 52.
    Korner S, Kammeyer J, Zapf A, Kuzma-Kozakiewicz M, Piotrkiewicz M, Kuraszkiewicz B, Goszczynska H, Gromicho M, Grosskreutz J, Andersen PM, de Carvalho M, Petri S (2019) Influence of environment and lifestyle on incidence and progress of amyotrophic lateral sclerosis in A German ALS population. Aging Dis 10:205–216.  https://doi.org/10.14336/ad.2018.0327 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Beard JD, Steege AL, Ju J, Lu J, Luckhaupt SE, Schubauer-Berigan MK (2017) Mortality from amyotrophic lateral sclerosis and parkinson's disease among different occupation groups—United States, 1985–2011. MMWR Morb Mortal Wkly Rep 66:718–722.  https://doi.org/10.15585/mmwr.mm6627a2 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Mehta P, Kaye W, Raymond J, Punjani R, Larson T, Cohen J, Muravov O, Horton K (2018) Prevalence of amyotrophic lateral sclerosis—United States, 2015. MMWR Morb Mortal Wkly Rep 67:1285–1289.  https://doi.org/10.15585/mmwr.mm6746a1 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Epidemiology and Biostatistics, School of Public HealthPeking University Health Science CenterBeijingChina
  2. 2.Department of NeurologyPeking University Third HospitalBeijingChina
  3. 3.Center for Clinical EpidemiologyPeking University Third HospitalBeijingChina

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