Misdiagnosis of amyotrophic lateral sclerosis in clinical practice in Europe and the USA: a patient chart review and physician survey

References

• Hardiman O, van den Berg LH, Kiernan MC. Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat Rev Neurol. 2011;7:639–49.
   PubMed Web of Science ®Google Scholar
• Brown RH, Al-Chalabi A. Amyotrophic lateral sclerosis. N Engl J Med. 2017;377:162–72.
   PubMed Web of Science ®Google Scholar
• Chiò A, Mazzini L, Mora G. Disease-modifying therapies in amyotrophic lateral sclerosis. Neuropharmacology. 2020;167:107986.
   PubMed Web of Science ®Google Scholar
• Mead RJ, Shan N, Reiser HJ, Marshall F, Shaw PJ. Amyotrophic lateral sclerosis: a neurodegenerative disorder poised for successful therapeutic translation. Nat Rev Drug Discov. 2023;22:185–212.
   PubMed Web of Science ®Google Scholar
• Genge A, Chiò A. The future of ALS diagnosis and staging: where do we go from here? Amyotroph Lateral Scler Frontotemporal Degener. 2023;24:165–74.
   PubMed Web of Science ®Google Scholar
• Kwak S, Kim DH, Boudier-Reveret M, MC C. Amyotrophic lateral sclerosis mimicking radiculopathy: a case series. Nagoya J Med Sci. 2021;83:877–81.
   PubMed Web of Science ®Google Scholar
• Storti B, Diamanti S, Tremolizzo L, Riva N, Lunetta C, Filippi M, et al. ALS mimics due to affection of the cervical spine: from common compressive myelopathy to rare CSF epidural collection. Case Rep Neurol. 2021;13:145–56.
   PubMed Web of Science ®Google Scholar
• Al-Chalabi A, Hardiman O, Kiernan MC, Chiò A, Rix-Brooks B, van den Berg LH. Amyotrophic lateral sclerosis: moving towards a new classification system. Lancet Neurol. 2016;15:1182–94.
   PubMed Web of Science ®Google Scholar
• Norris SP, Likanje MF, Andrews JA. Amyotrophic lateral sclerosis: update on clinical management. Curr Opin Neurol. 2020;33:641–8.
   PubMed Web of Science ®Google Scholar
• Roggenbuck J, Rich KA, Vicini L, Palettas M, Schroeder J, Zaleski C, et al. Amyotrophic lateral sclerosis genetic access program: paving the way for genetic characterization of ALS in the clinic. Neurol Genet. 2021;7:e615.
   PubMed Web of Science ®Google Scholar
• Vajda A, McLaughlin RL, Heverin M, Thorpe O, Abrahams S, Al-Chalabi A, et al. Genetic testing in ALS: a survey of current practices. Neurology. 2017;88:991–9.
   PubMed Web of Science ®Google Scholar
• Richards D, Morren JA, Pioro EP. Time to diagnosis and factors affecting diagnostic delay in amyotrophic lateral sclerosis. J Neurol Sci. 2020;417:117054.
   PubMed Web of Science ®Google Scholar
• Paganoni S, Macklin EA, Lee A, Murphy A, Chang J, Zipf A, et al. Diagnostic timelines and delays in diagnosing amyotrophic lateral sclerosis (ALS). Amyotroph Lateral Scler Frontotemporal Degener. 2014;15:453–6.
   PubMed Web of Science ®Google Scholar
• Morren JA, Rheaume C, Pioro EP. Self-reported factors contributing to delay in ALS diagnosis among primary care providers in a large Ohio-based US healthcare network. J Neurol Sci. 2023;445:120532.
   PubMed Web of Science ®Google Scholar
• Belsh JM, Schiffman PL. The amyotrophic lateral sclerosis (ALS) patient perspective on misdiagnosis and its repercussions. J Neurol Sci. 1996;139 Suppl:110–6.
   PubMed Web of Science ®Google Scholar
• Shefner JM, Al-Chalabi A, Baker MR, Cui LY, de Carvalho M, Eisen A, et al. A proposal for new diagnostic criteria for ALS. Clin Neurophysiol. 2020;131:1975–8.
   PubMed Web of Science ®Google Scholar
• Galvin M, Ryan P, Maguire S, Heverin M, Madden C, Vajda A, et al. The path to specialist multidisciplinary care in amyotrophic lateral sclerosis: a population-based study of consultations, interventions and costs. PLoS One. 2017;12:e0179796.
   PubMed Web of Science ®Google Scholar
• Anderson P, Benford M, Harris N, Karavali M, Piercy J. Real-world physician and patient behaviour across countries: disease-specific programmes – a means to understand. Curr Med Res Opin. 2008;24:3063–72.
   PubMed Web of Science ®Google Scholar
• Babineaux SM, Curtis B, Holbrook T, Milligan G, Piercy J. Evidence for validity of a national physician and patient-reported, cross-sectional survey in China and UK: the disease specific programme. BMJ Open. 2016;6:e010352.
   PubMed Web of Science ®Google Scholar
• Higgins V, Piercy J, Roughley A, Milligan G, Leith A, Siddall J, et al. Trends in medication use in patients with type 2 diabetes mellitus: a long-term view of real-world treatment between 2000 and 2015. Diabetes Metab Syndr Obes. 2016;9:371–80.
   PubMed Web of Science ®Google Scholar
• EPHMRA. Code of conduct/AER https://www.ephmra.org/code-conduct-aer. 2021. Accessed 14 September 2022.
   Google Scholar
• Strong MJ, Abrahams S, Goldstein LH, Woolley S, McLaughlin P, Snowden J, et al. Amyotrophic lateral sclerosis – frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener. 2017;18:153–74.
   PubMed Web of Science ®Google Scholar
• Muller HP, Gorges M, Del Tredici K, Ludolph AC, Kassubek J. The same cortico-efferent tract involvement in progressive bulbar palsy and in ‘classical’ ALS: a tract of interest-based MRI study. Neuroimage Clin. 2019;24:101979.
   PubMed Web of Science ®Google Scholar
• Rechtman L, Jordan H, Wagner L, Horton DK, Kaye W. Racial and ethnic differences among amyotrophic lateral sclerosis cases in the United States. Amyotroph Lateral Scler Frontotemporal Degener. 2015;16:65–71.
   PubMed Web of Science ®Google Scholar
• Falcão de Campos C, Gromicho M, Uysal H, Grosskreutz J, Kuzma-Kozakiewicz M, Oliveira Santos M, et al. Trends in the diagnostic delay and pathway for amyotrophic lateral sclerosis patients across different countries. Front Neurol. 2022;13:1064619.
   PubMed Web of Science ®Google Scholar
• Sennfalt S, Klappe U, Thams S, Samuelsson K, Press R, Fang F, et al. The path to diagnosis in ALS: delay, referrals, alternate diagnoses, and clinical progression. Amyotroph Lateral Scler Frontotemporal Degener. 2023;24:45–53.
   PubMed Web of Science ®Google Scholar
• Martínez-Molina M, Argente-Escrig H, Polo MF, Hervás D, Frasquet M, Cortés V, et al. Early referral to an ALS center reduces several months the diagnostic delay: a multicenter-based study. Front Neurol. 2020;11:604922.
   PubMed Web of Science ®Google Scholar
• Masrori P, Van Damme P. Amyotrophic lateral sclerosis: a clinical review. Eur J Neurol. 2020;27:1918–29.
   PubMed Web of Science ®Google Scholar
• Stegmann GM, Hahn S, Liss J, Shefner J, Rutkove S, Shelton K, et al. Early detection and tracking of bulbar changes in ALS via frequent and remote speech analysis. NPJ Digit Med. 2020;3:132.
   PubMed Web of Science ®Google Scholar
• Matharan M, Mathis S, Bonabaud S, Carla L, Soulages A, Le Masson G. Minimizing the diagnostic delay in amyotrophic lateral sclerosis: the role of nonneurologist practitioners. Neurol Res Int. 2020;2020:1473981.
   PubMed Web of Science ®Google Scholar
• Cronin S, Hardiman O, Traynor BJ. Ethnic variations in the incidence of ALS: a systematic review. Neurology. 2007;68:1002–7.
   PubMed Web of Science ®Google Scholar
• Abdullah AI. Invitae opens genetic testing to adults with ALS symptoms or family risk [Internet]. 2021. Available at: https://alsnewstoday.com/news/invitae-opens-free-als-genetic-testing-adults-als-risk/. Accessed April 28, 2023.
   Google Scholar
• Turner MR, Barnwell J, Al-Chalabi A, Eisen A. Young-onset amyotrophic lateral sclerosis: historical and other observations. Brain. 2012;135:2883–91.
   PubMed Web of Science ®Google Scholar
• Salmon K, Kiernan MC, Kim SH, Andersen PM, Chio A, van den Berg LH, et al. The importance of offering early genetic testing in everyone with amyotrophic lateral sclerosis. Brain. 2022;145:1207–10.
   PubMed Web of Science ®Google Scholar