The ALSFRS as an outcome measure in therapeutic trials and its relationship to symptom onset

References

• Turner MR, Hardiman O, Benatar M, Brooks BR, Chio A, de Carvalho M, et al. Controversies and priorities in amyotrophic lateral sclerosis. Lancet Neurol. 2013;12:310–22.
   PubMed Web of Science ®Google Scholar
• Jablecki CK, Berry C, Leach J. Survival prediction in amyotrophic lateral sclerosis. Muscle Nerve. 1989;12: 833–41.
   PubMed Web of Science ®Google Scholar
• Kihira T, Yoshida S, Okamoto K, Kazimoto Y, Ookawa M, Hama K, et al. Survival rate of patients with amyotrophic lateral sclerosis in Wakayama Prefecture, Japan, 1966 to 2005. J Neurol Sci. 2008;268:95–101.
   PubMed Web of Science ®Google Scholar
• Pupillo E, Messina P, Logroscino G, Beghi E. Long-term survival in amyotrophic lateral sclerosis: a population based study. Ann Neurol. 2014;75:287–97.
   PubMed Web of Science ®Google Scholar
• Kaufmann P, Levy G, Thompson JLP, Delbene ML, Battista V, Gordon PH, et al. The ALSFRS-R predicts survival time in an ALS clinic population. Neurology. 2005;64:38–43.
   PubMed Web of Science ®Google Scholar
• Watanabe H, Atsuta N, Nakamura R, Hirakawa A, Watanabe H, Ito M, et al. Factors affecting longitudinal functional decline and survival in amyotrophic lateral sclerosis patients. Amyotroph Lateral Scler Frontal Degener. 2015;16:230–6.
   PubMed Web of Science ®Google Scholar
• Mandrioli J, Biguzzi S, Guidi C, Sette E, Terlizzi E, Ravasio A, et al. Heterogeneity in ALSFRS-R decline and survival: a population based study in Italy. Neurol Sci. 2015. doi:10.1007/s10072-015-2343-6.
   PubMed Web of Science ®Google Scholar
• Turner MRM, Scaber J, Goodfellow JJ, Lord ME, Marsden R, Talbot K. The diagnostic pathway and prognosis in bulbar-onset amyotrophic lateral sclerosis. J Neurol Sci. 2010;294:81–5.
   PubMed Web of Science ®Google Scholar
• Andersen PM, Nilsson P, Keränen ML, Forsgren L, Hägglund J, Karlsborg M, et al. Phenotypic heterogeneity in motor neuron disease patients with Cu/Zn-superoxide dismutase mutations in Scandinavia. Brain. 1997;120 (Pt 1:1723–37).
   PubMed Web of Science ®Google Scholar
• Simón-Sánchez J, Dopper EGP, Cohn-Hokke PE, Hukema RK, Nicolaou N, Seelaar H, et al. The clinical and pathological phenotype of C9orf72 hexanucleotide repeat expansions. Brain. 2012;135:723–35.
   PubMed Web of Science ®Google Scholar
• Bowser R, Turner MR, Shefner J. Biomarkers in amyotrophic lateral sclerosis: opportunities and limitations. Nat Rev Neurol. 2011;7:631–8.
   PubMed Web of Science ®Google Scholar
• Appel V, Stewart SS, Smith G, Appel SH. A rating scale for amyotrophic lateral sclerosis: description and preliminary experience. Ann Neurol. 1987;22:328–33.
   PubMed Web of Science ®Google Scholar
• Armon C, Graves MC, Moses D, Forté DK, Sepulveda L, Darby SM, et al. Linear estimates of disease progression predict survival in patients with amyotrophic lateral sclerosis. Muscle Nerve. 2000;23:874–82.
   PubMed Web of Science ®Google Scholar
• Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999;169:13–21.
   PubMed Web of Science ®Google Scholar
• Gordon PH, Cheng B, Salachas F, Pradat P-F, Bruneteau G, Corcia P, et al. Progression in ALS is not linear but is curvilinear. J Neurol. 2010;257:1713–17.
   PubMed Web of Science ®Google Scholar
• Chio A, Mora G, Leone M, Mazzini L, Cocito D, Giordana MT, et al. Early symptom progression rate is related to ALS outcome: a prospective population based study. Neurology. 2002;59:99–103.
   PubMed Web of Science ®Google Scholar
• Gomeni R, Fava M. Amyotrophic lateral sclerosis disease progression model. Amyotroph Lateral Scler Frontotemporal Degener. 2014;15:119–29.
   PubMed Web of Science ®Google Scholar
• Kollewe K, Mauss U, Krampfl K, Petri S, Dengler R, Mohammadi B. ALSFRS-R score and its ratio: a useful predictor for ALS progression. J Neurol Sci. 2008;275:69–73.
   PubMed Web of Science ®Google Scholar
• Kimura F, Fujimura C, Ishida S, Nakajima H, Furutama D, Uehara H, et al. Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology 2006;66:265–7.
   PubMed Web of Science ®Google Scholar
• Traynor BJ, Zhang H, Shefner JM, Schoenfeld D, Cudkowicz ME. Functional outcome measures as clinical trial endpoints in ALS. Neurology. 2004;63:1933–5.
   PubMed Web of Science ®Google Scholar
• Czaplinski A, Yen AA, Appel SH. Forced vital capacity (FVC) as an indicator of survival and disease progression in an ALS clinic population. J Neurol Neurosurg Psychiatry. 2006;77:390–2.
   PubMed Web of Science ®Google Scholar
• Bensimon G, Lacomblez L, Meininger V, Iso H. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med 1994;330:585–91.
   PubMed Web of Science ®Google Scholar
• Stambler N, Charatan M, Cedarbaum JM. Prognostic indicators of survival in ALS. ALS CNTF Treatment Study Group. Neurology. 1998;50:66–72.
   PubMed Web of Science ®Google Scholar
• Qureshi MM, Hayden D, Urbinelli L, Ferrante K, Newhall K, Myers D, et al. Analysis of factors that modify susceptibility and rate of progression in amyotrophic lateral sclerosis (ALS). Amyotroph Lateral Scler. 2006;7:173–82.
   PubMed Web of Science ®Google Scholar
• Atassi N, Berry J, Shui A, Zach N, Sherman A, Sinani E, et al. The PRO-ACT database: design, initial analyses, and predictive features. Neurology 2014;83:1719–25.
   PubMed Web of Science ®Google Scholar
• Haverkamp LJ, Appel V, Appel SH. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain. 1995;118 (Pt 3:707–19).
   PubMed Web of Science ®Google Scholar
• Wicks P, Massagli MP, Wolf C, Heywood J. Measuring function in advanced ALS: Validation of ALSFRS-EX extension items. Eur J Neurol. 2009;16:353–9.
   PubMed Web of Science ®Google Scholar
• Ward NS, Hill NS. Pulmonary function testing in neuromuscular disease. Clin Chest Med. 2001;22:769–81.
   PubMed Web of Science ®Google Scholar
• Berry JD, Miller R, Moore DH, Cudkowicz ME, van den Berg LH, Kerr D A, et al. The Combined Assessment of Function and Survival (CAFS): a new endpoint for ALS clinical trials. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:162–8.
   PubMed Web of Science ®Google Scholar
• Kondo K, Hemmi I. Clinical Statistics in 515 Fatal Cases of Motor Neuron Disease. Determinants of Course. Neuroepidemiology. 1984;3:139–48.
   Google Scholar
• Chiò A, Logroscino G, Hardiman O, Swingler R, Mitchell D, Beghi E, et al. Prognostic factors in ALS: a critical review. Amyotroph Lateral Scler. 2009;10:310–23.
   PubMed Web of Science ®Google Scholar
• Creemers H, Grupstra H, Nollet F, van den Berg LH, Beelen A. Prognostic factors for the course of functional status of patients with ALS: a systematic review. J Neurol. 2014:1407–23.
   PubMed Web of Science ®Google Scholar
• Küffner R, Zach N, Norel R, Hawe J, Schoenfeld D, Wang L, et al. Crowdsourced analysis of clinical trial data to predict amyotrophic lateral sclerosis progression. Nat Biotechnol. 2015 Jan;33(1):51–7.
   Web of Science ®Google Scholar
• Lee CT-C, Chiu Y-W, Wang K-C, Hwang C-S, Lin K-H, Lee I-T, et al. 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. 2013;23:35–40.
   PubMed Web of Science ®Google Scholar
• Jennum P, Ibsen R, Pedersen SW, Kjellberg J. Mortality, health, social and economic consequences of amyotrophic lateral sclerosis: a controlled national study. J Neurol. 2013;260:785–93.
   PubMed Web of Science ®Google Scholar
• Labra J, Menon P, Byth K, Morrison S, Vucic S. Rate of disease progression: a prognostic biomarker in ALS. J Neurol Neurosurg Psychiatry. 2015:jnnp – 2015–310998. doi:10.1136/jnnp-2015-310998.
   PubMed Web of Science ®Google Scholar
• Tramacere I, Dalla Bella E, Chio A, Mora G, Filippini G, Lauria G, et al. The MITOS system predicts long-term survival in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2015:1–6.
   PubMed Web of Science ®Google Scholar
• Franchignoni F, Mandrioli J, Giordano A, Ferro S. A further Rasch study confirms that ALSFRS-R does not conform to fundamental measurement requirements. Amyotroph Lateral Scler Front Degener. 2015:1–7.
   Web of Science ®Google Scholar
• Voustianiouk A, Seidel G, Panchal J, Sivak M, Czaplinski A, Yen A, et al. ALSFRS and Appel ALS scores: discordance with disease progression. Muscle Nerve. 2008;37:668–72.
   PubMed Web of Science ®Google Scholar
• Goldstein LH, Abrahams S. Changes in cognition and behaviour in amyotrophic lateral sclerosis: nature of impairment and implications for assessment. Lancet Neurol. 2013;12:368–80.
   PubMed Web of Science ®Google Scholar
• Mantovan MC, Baggio L, Dalla Barba G, Smith P, Pegoraro E, Soraru’ G, et al. Memory deficits and retrieval processes in ALS. Eur J Neurol. 2003;10:221–7.
   PubMed Web of Science ®Google Scholar
• Machts J, Bittner V, Kasper E, Schuster C, Prudlo J, Abdulla S, et al. Memory deficits in amyotrophic lateral sclerosis are not exclusively caused by executive dysfunction: a comparative neuropsychological study of amnestic mild cognitive impairment. BMC Neurosci. 2014;15:83.
   PubMed Web of Science ®Google Scholar
• Roche JC, Rojas-Garcia R, Scott KM, Scotton W, Ellis CE, Burman R, et al. A proposed staging system for amyotrophic lateral sclerosis. Brain. 2012;135:847–52.
   PubMed Web of Science ®Google Scholar
• Felice KJ. A longitudinal study comparing thenar motor unit number estimates to other quantitative tests in patients with amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:179–85.
   PubMed Web of Science ®Google Scholar
• Pinto S, Geraldes R, Vaz N, Pinto A, de Carvalho M. Changes of the phrenic nerve motor response in amyotrophic lateral sclerosis: longitudinal study. Clin Neurophysiol. 2009;120:2082–5.
   PubMed Web of Science ®Google Scholar
• Fitting JW, Paillex R, Hirt L, Aebischer P, Schluep M. Sniff nasal pressure: a sensitive respiratory test to assess progression of amyotrophic lateral sclerosis. Ann Neurol. 1999;46:887–93.
   PubMed Web of Science ®Google Scholar
• Capozzo R, Quaranta VN, Pellegrini F, Fontana A, Copetti M, Carratù P, et al. Sniff nasal inspiratory pressure as a prognostic factor of tracheostomy or death in amyotrophic lateral sclerosis. J Neurol. 2014;262:593–603.
   PubMed Web of Science ®Google Scholar
• Lyall RA, Donaldson N, Polkey MI, Leigh PN, Moxham J. Respiratory muscle strength and ventilatory failure in amyotrophic lateral sclerosis. Brain. 2001;124:2000–13.
   PubMed Web of Science ®Google Scholar
• Chaudri MB, Liu C, Watson L, Jefferson D, Kinnear WJ. Sniff nasal inspiratory pressure as a marker of respiratory function in motor neuron disease. Eur Respir J. 2000;15:539–42.
   PubMed Web of Science ®Google Scholar
• Leonardis L, Dolenc Grošelj L, Vidmar G. Factors related to respiration influencing survival and respiratory function in patients with amyotrophic lateral sclerosis: a retrospective study. Eur J Neurol. 2012;19:1518–24.
   PubMed Web of Science ®Google Scholar
• Turner MR, Benatar M. Ensuring continued progress in biomarkers for amyotrophic lateral sclerosis. Muscle Nerve. 2015, Vol 51, Issue 1, Pages 14–8. doi:10.1002/mus.24470.
   Web of Science ®Google Scholar