The El Escorial criteria: Strengths and weaknesses

References

• Brooks BR. El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial ‘Clinical limits of amyotrophic lateral sclerosis’ workshop contributors. J Neurol Sci. 1994;124:96–107.
   PubMed Web of Science ®Google Scholar
• Brooks BR, Miller RG, Swash M, Munsat TL. World Federation of Neurology Research Group on Motor Neuron Disease. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:293–9.
   PubMed Web of Science ®Google Scholar
• de Carvalho M, Swash M. Awaji diagnostic algorithm increases sensitivity of El Escorial criteria for ALS diagnosis. Amyotroph Lateral Scler. 2009;10:53–7.
   PubMed Web of Science ®Google Scholar
• Costa J, Swash M, de Carvalho M. Awaji criteria for the diagnosis of amyotrophic lateral sclerosis: a systematic review. Arch Neurol. 2012;69:1410–6.
   PubMed Web of Science ®Google Scholar
• Cellura E, Spataro R, Taiello AC, La Bella V. Factors affecting the diagnostic delay in amyotrophic lateral sclerosis. Clin Neurol Neurosurg. 2012;114:550–4.
   PubMed Web of Science ®Google Scholar
• Davenport RJ, Swingler RJ, Chancellor AM, Warlow CP. Avoiding false-positive diagnoses of motor neuron disease: lessons from the Scottish Motor Neuron Disease Register. J Neurol Neurosurg Psychiatry. 1996;60:147–51.
   PubMed Web of Science ®Google Scholar
• Mitchell JD, Callagher P, Gardham J, Mitchell C, Dixon M, Addison-Jones R, et al. Timelines in the diagnostic evaluation of people with suspected amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND) – a 20-year review: can we do better? Amyotroph Lateral Scler. 2010;11:537–41.
   PubMed Web of Science ®Google Scholar
• Chiò A, Borghero G, Calvo A, Capasso M, Caponnetto C, Corbo M, et al. Lithium carbonate in amyotrophic lateral sclerosis: lack of efficacy in a dose-finding trial. Neurology. 2010;75:619–25.
   PubMed Web of Science ®Google Scholar
• Chiò A, Mora G, La Bella V, Caponnetto C, Mancardi G, Sabatelli M, et al. Repeated courses of granulocyte colony-stimulating factor in amyotrophic lateral sclerosis: clinical and biological results from a prospective multicenter study. Muscle Nerve. 2011;43:189–95.
   PubMed Web of Science ®Google Scholar
• Gordon PH, Moore DH, Miller RG, Florence JM, Verheijde JL, Doorish C, et al. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomized trial. Lancet Neurol. 2007;6:1045–53.
   PubMed Web of Science ®Google Scholar
• Kaufmann P, Thompson JL, Levy G, Buchsbaum R, Shefner J, Krivickas LS, et al. Phase II trial of CoQ10 for ALS finds insufficient evidence to justify phase III. Ann Neurol. 2009;66:235–44.
   PubMed Web of Science ®Google Scholar
• Miller RG, Petajan JH, Bryan WW, Armon C, Barohn RJ, Goodpasture JC, et al. A placebo-controlled trial of recombinant human ciliary neurotrophic (rhCNTF) factor in amyotrophic lateral sclerosis. rhCNTF ALS Study Group. Ann Neurol. 1996;39:256–60.
   PubMed Web of Science ®Google Scholar
• Miller RG, Moore DH 2nd, Gelinas DF, Dronsky V, Mendoza M, Barohn RJ, et al. Phase III randomized trial of gabapentin in patients with amyotrophic lateral sclerosis. Neurology. 2001;56:843–8.
   PubMed Web of Science ®Google Scholar
• Miller R, Bradley W, Cudkowicz M, Hubble J, Meininger V, Mitsumoto H, et al. Phase II/III randomized trial of TCH346 in patients with ALS. Neurology. 2007;69:776–84.
   PubMed Web of Science ®Google Scholar
• Pascuzzi RM, Shefner J, Chappell AS, Bjerke JS, Tamura R, Chaudhry V, et al. A phase II trial of talampanel in subjects with amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2010;11:266–71.
   PubMed Web of Science ®Google Scholar
• Shefner JM, Cudkowicz ME, Schoenfeld D, Conrad T, Taft J, Chilton M, et al. A clinical trial of creatine in ALS. Neurology. 2004;63:1656–61.
   PubMed Web of Science ®Google Scholar
• Aggarwal SP, Zinman L, Simpson E, McKinley J, Jackson KE, Pinto H, et al. Safety and efficacy of lithium in combination with riluzole for treatment of amyotrophic lateral sclerosis: a randomized, double-blind, placebo-controlled trial. Lancet Neurol. 2010;9:481–8.
   PubMed Web of Science ®Google Scholar
• Cudkowicz M, Bozik ME, Ingersoll EW, Miller R, Mitsumoto H, Shefner J, et al. The effects of dexpramipexole (KNS-760704) in individuals with amyotrophic lateral sclerosis. Nat Med. 2011;17:1652–6.
   PubMed Web of Science ®Google Scholar
• Byrne S, Bede P, Elamin M, Kenna K, Lynch C, McLaughlin R, et al. Proposed criteria for familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2011;12:157–9.
   PubMed Web of Science ®Google Scholar
• Turner MR, Bakker M, Sham P, Shaw CE, Leigh PN, Al-Chalabi A. Prognostic modelling of therapeutic interventions in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2002;3:15–21.
   PubMed Web of Science ®Google Scholar
• Chiò 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
• Wijesekera LC, Mathers S, Talman P, Galtrey C, Parkinson MH, Ganesalingam J, et al. Natural history and clinical features of the flail arm and flail leg ALS variants. Neurology. 2009;72:1087–94.
   PubMed Web of Science ®Google Scholar
• Ince PG, Evans J, Knopp M, Forster G, Hamdalla HH, Wharton SB, et al. Corticospinal tract degeneration in the progressive muscular atrophy variant of ALS. Neurology. 2003;60:1252–8.
   PubMed Web of Science ®Google Scholar
• Chen A, Weimer L, Brannagan T 3rd, Colin M, Andrews J, Mitsumoto H, et al. Experience with the Awaji Island modifications to the ALS diagnostic criteria. Muscle Nerve. 2010;42:831–2.
   PubMed Web of Science ®Google Scholar
• Okita T, Nodera H, Shibuta Y, Nodera A, Asanuma K, Shimatani Y, et al. Can Awaji ALS criteria provide earlier diagnosis than the revised El Escorial criteria? J Neurol Sci. 2001;302:29–32.
   Google Scholar
• Schrooten M, Smetcoren C, Robberecht W, van Damme P. Benefit of the Awaji diagnostic algorithm for amyotrophic lateral sclerosis: a prospective study. Ann Neurol. 2011; l70:79–83.
   Google Scholar
• Filippi M, Agosta F, Abrahams S, Fazekas F, Grosskreutz J, Kalra S, et al. EFNS guidelines on the use of neuroimaging in the management of motor neuron diseases. Eur J Neurol. 2010;17:520–6.
   Google Scholar
• Turner MR, Agosta F, Bede P, Govind V, Lule D, Verstraete E. Neuroimaging in ALS. Biomarkers in Medicine. Biomark Med. 2012;6:319–37.
   PubMed Web of Science ®Google Scholar
• McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement. 2011;7:263–9.
   PubMed Web of Science ®Google Scholar
• Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, et al.Sensitivity of revised diagnostic criteria for the behavioral variant of frontotemporal dementia. Brain. 2011;134:2456–77.
   PubMed Web of Science ®Google Scholar
• Agosta F, Valsasina P, Riva N, Copetti M, Messina MJ, Prelle A, et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One 2012;7:e42816.
   PubMed Web of Science ®Google Scholar
• Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, et al. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 2004;127:340–50.
   PubMed Web of Science ®Google Scholar
• van der Graaff MM, Sage CA, Caan MW, Akkerman EM, Lavini C, Majoie CB, et al. Upper and extramotor neuron involvement in early motor neuron disease: a diffusion tensor imaging study. Brain. 2011;134:1211–28.
   PubMed Web of Science ®Google Scholar
• Agosta F, Pagani E, Petrolini M, Sormani MP, Caputo D, Perini M, et al. MRI predictors of long-term evolution in amyotrophic lateral sclerosis. Eur J Neurosci. 2010;32: 1490–6.
   PubMed Web of Science ®Google Scholar
• Menke RA, Abraham I, Thiel CS, Filippini N, Knight S, Talbot K, et al. Fractional Anisotropy in the Posterior Limb of the Internal Capsule and Prognosis in Amyotrophic Lateral Sclerosis. Arch Neurol. 2012;69:1493–9.
   PubMedGoogle Scholar
• Raaphorst J, de Visser M, van Tol MJ, Linssen WHJP, van der Kooi AJ, de Haan RJ, et al. Cognitive dysfunction in lower motor neuron disease: executive and memory deficits in progressive muscular atrophy. J Neurol Neurosurg Psych. 2011;82:170–5.
   PubMed Web of Science ®Google Scholar
• van Blitterswijk M, Vlam L, van Es MA, van der Pol WL, Hennekam EA, Dooijes D, et al. Genetic overlap between apparently sporadic motor neuron diseases. PLoS One 2012; 7:e48983.
   Google Scholar
• van den Berg-Vos RM, Visser J, Franssen H, de Visser M, de Jong JMBV, Kalmijn S, et al. Sporadic lower motor neuron disease with adult onset: classification of subtypes. Brain. 2003;126:1036–47.
   PubMed Web of Science ®Google Scholar
• van den Berg-Vos RM, Visser J, Kalmijn S, Fischer K, de Visser M, de Jong JMBV, et al. A long-term prospective study of the natural course of sporadic adult-onset lower motor neuron syndromes. Arch Neurol. 2009;66:751–7.
   PubMedGoogle Scholar
• Van Rheenen W, van Blitterswijk M, Huisman MH, Vlam L, van Doormaal PT, Seelen M, et al. Hexanucleotide repeat expansions in C9orf72 in the spectrum of motor neuron diseases. Neurology. 2012:79:878–82.
   PubMed Web of Science ®Google Scholar
• Visser J, van den Berg RM, Franssen H, van den Berg LH, Wokke JHJ, de Jong JMBV, et al. Disease course and prognostic factors of progressive muscular atrophy. Arch Neurol. 2007;64:522–8.
   PubMedGoogle Scholar
• Visser J, van den Berg-Vos RM, Franssen H, van den Berg LH, Vogels OJ, Wokke JHJ, et al. Mimic syndromes in sporadic cases of progressive spinal muscular atrophy. Neurology. 2002;58:1593–6.
   PubMed Web of Science ®Google Scholar
• Guennoc AM, Camu W, Corcia P. Awaji criteria: new diagnostic criteria for amyotrophic lateral sclerosis. Rev Neurol. 2013;169:470–5.
   Google Scholar
• Hanby MF, Scott KM, Scotton W, Wijesekera L, Mole T, Ellis CE, et al. The risk to relatives of patients with sporadic amyotrophic lateral sclerosis. Brain. 2011;134:3454–7.
   PubMed Web of Science ®Google Scholar
• Al-Chalabi A, Lewis CM. Modeling the effects of penetrance and family size on rates of sporadic and familial disease. Human Heredity. 2011;71:281–8.
   PubMed Web of Science ®Google Scholar
• Byrne S, Heverin M, Elamin M, Bede P, Lynch C, Kenna K, et al. Aggregation of neurologic and neuropsychiatric disease in amyotrophic lateral sclerosis kindreds: a population based case-control cohort study of familial and sporadic amyotrophic lateral sclerosis. Ann Neurol. 2013;74:699–708.
   PubMed Web of Science ®Google Scholar
• DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, et al. Expanded GGGGCC hexanucleotide repeat in non-coding region of C9orf72 causes chromosome 9p-linked FTD and ALS. Neuron. 2011;72:245–56.
   PubMed Web of Science ®Google Scholar
• Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet. 2008;40:572–4.
   PubMed Web of Science ®Google Scholar
• Johnson JO, Mandrioli J, Benatar M, Abramzon Y, van Deerlin VM, Trojanowski JQ, et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron. 2010;68:857–64.
   PubMed Web of Science ®Google Scholar
• Dornblüth O. Anatomische Untersuchung eines Falles von amyotropher Lateralsklerose. Neurologisches Centralblatt. 1889;23:377–86.
   Google Scholar
• Elamin M, Phukan J, Bede P, Jordan N, Byrne S, Pender N, et al. Executive dysfunction is a negative prognostic indicator in patients with ALS without dementia. Neurology. 2011; 76:1263–9.
   PubMed Web of Science ®Google Scholar
• Elamin M, Bede P, Byrne S, Jordan N, Gallagher L, Wynne B, et al. Cognitive changes predict functional decline in ALS: a population based longitudinal study. Neurology. 2013;80:1590–7.
   PubMed Web of Science ®Google Scholar
• Phukan J, Elamin M, Bede P, Jordan N, Gallagher L, Byrne S, et al. The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry. 2012;83:102–8.
   PubMed Web of Science ®Google Scholar
• Bede P, Elamin M, Byrne S, McLaughlin RL, Kenna K, Vajda A, Pender N, et al. Basal ganglia involvement in amyotrophic lateral sclerosis. Neurology. 2013;81: 2107–15.
   PubMed Web of Science ®Google Scholar
• Brettschneider J, del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol. 2013;74: 20–38.
   PubMed Web of Science ®Google Scholar
• Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, et al. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioral syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2009;10:131–46.
   PubMed Web of Science ®Google Scholar
• Abrahams S, Newton J, Niven E, Foley J, Bak TH. Screening for cognition and behavior changes in ALS. Amyotroph Lateral Scler Frontotemporal Degener. 2014; 15:9–14.
   PubMed Web of Science ®Google Scholar