{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T01:14:27Z","timestamp":1792113267011,"version":"4.4.0"},"reference-count":37,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,9,9]],"date-time":"2021-09-09T00:00:00Z","timestamp":1631145600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Sciences"],"abstract":"<jats:p>In previous studies, a below-average, average, or above-average intelligence quotient (IQ) in children with SMA was detected but, aside from a severe physical disability, the cognitive performance of adult SMA patients has not yet been evaluated. The intelligence test used in this study, the Wechsler Adult Intelligence Scale, fourth edition (WAIS-IV), was used to measure major intelligence components of adult SMA patients. The WAIS-IV determines four index scores representing verbal comprehension, perceptual reasoning, working memory, and processing speed. Due to time-dependent demands on motor function, the processing speed index score was excluded. IQ index scores of 33 adult SMA patients did not differ from IQ index scores of the normal population. In SMA type-3 patients, the index scores for verbal comprehension, perceptual reasoning, and working memory did not differ from the normal population but showed a trend of IQ scores towards lower points. Patients with SMA type 2 had lower IQ index scores for working memory (90.33 \u00b1 12.95; p = 0.012) and perceptual reasoning (90.73 \u00b1 12.58; p = 0.013) than the normal population. This study provided further evidence that SMA is a multi-systemic disease and may refute the widespread hypothesis that SMA patients might improve their cognitive skills to compensate for their physical impairment.<\/jats:p>","DOI":"10.3390\/brainsci11091184","type":"journal-article","created":{"date-parts":[[2021,9,9]],"date-time":"2021-09-09T12:20:37Z","timestamp":1631190037000},"page":"1184","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Cognitive Impairment in Adult Patients with 5q-Associated Spinal Muscular Atrophy"],"prefix":"10.3390","volume":"11","author":[{"given":"Kathrin","family":"Kizina","sequence":"first","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yakup","family":"Akkaya","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Jokisch","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2774-067X","authenticated-orcid":false,"given":"Benjamin","family":"Stolte","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"Totzeck","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan","family":"Munoz-Rosales","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"Thimm","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saskia","family":"Bolz","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Svenja","family":"Brakemeier","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Refik","family":"Pul","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Derya","family":"Aslan","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jana","family":"Hackert","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Kleinschnitz","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3631-3450","authenticated-orcid":false,"given":"Tim","family":"Hagenacker","sequence":"additional","affiliation":[{"name":"Department of Neurology, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2120","DOI":"10.1016\/S0140-6736(08)60921-6","article-title":"Spinal muscular atrophy","volume":"371","author":"Lunn","year":"2008","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1186\/s13023-017-0671-8","article-title":"Prevalence, incidence and carrier frequency of 5q\u2013linked spinal muscular atrophy\u2014A literature review","volume":"12","author":"Verhaart","year":"2017","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"487","DOI":"10.3233\/JND-160177","article-title":"Type 0 Spinal Muscular Atrophy: Further Delineation of Prenatal and Postnatal Features in 16 Patients","volume":"3","author":"Grotto","year":"2016","journal-title":"J. Neuromuscul. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1186\/1750-1172-6-71","article-title":"Spinal muscular atrophy","volume":"6","author":"Mercuri","year":"2011","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1002\/ana.25930","article-title":"Yeo and Darras: Extraneuronal Phenotypes of Spinal Muscular Atrophy","volume":"89","author":"Yeo","year":"2020","journal-title":"Ann. Neurol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1136\/jnnp-2016-314292","article-title":"Association of motor milestones, SMN2 copy and outcome in spinal muscular atrophy types 0\u20134","volume":"88","author":"Wadman","year":"2017","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_7","first-page":"489","article-title":"Cognitive dysfunction and mild closed head injury in traumatic spinal cord injury","volume":"66","author":"Davidoff","year":"1985","journal-title":"Arch. Phys. Med. Rehabil."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1212\/WNL.0000000000006244","article-title":"Cognitive function after spinal cord injury","volume":"91","author":"Sachdeva","year":"2018","journal-title":"Neurology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1179\/2045772312Y.0000000056","article-title":"Decentralized cardiovascular autonomic control and cognitive deficits in persons with spinal cord injury","volume":"36","author":"Wecht","year":"2013","journal-title":"J. Spinal Cord Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1136\/jnnp.2009.183525","article-title":"Incidence of amyotrophic lateral sclerosis in Europe","volume":"81","author":"Logroscino","year":"2009","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1016\/S0140-6736(10)61156-7","article-title":"Amyotrophic lateral sclerosis","volume":"377","author":"Kiernan","year":"2011","journal-title":"Lancet"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1002\/mus.26201","article-title":"Social participation of adult patients with spinal muscular atrophy: Frequency, restrictions, satisfaction, and correlates","volume":"58","author":"Reenen","year":"2018","journal-title":"Muscle Nerve"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1186\/s13023-021-01701-y","article-title":"\u201cI have SMA, SMA doesn\u2019t have me\u201d: A qualitative snapshot into the challenges, successes, and quality of life of adolescents and young adults with SMA","volume":"16","author":"Mazzella","year":"2021","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/s13023-017-0613-5","article-title":"Cardiac pathology in spinal muscular atrophy: A systematic review","volume":"12","author":"Wijngaarde","year":"2017","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1111\/joa.12083","article-title":"Spinal muscular atrophy: A motor neuron disorder or a multi-organ disease?","volume":"224","author":"Shababi","year":"2013","journal-title":"J. Anat."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.pediatrneurol.2020.01.003","article-title":"Overturning the Paradigm of Spinal Muscular Atrophy as Just a Motor Neuron Disease","volume":"109","author":"Yeo","year":"2020","journal-title":"Pediatr. Neurol."},{"key":"ref_17","unstructured":"Hausmanowa-Petrusewicz, I. (1978). Spinal Muscular Atrophy\u2014Infantile and Juvenile Type."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/S0960-8966(01)00274-7","article-title":"Intelligence and cognitive function in children and adolescents with spinal muscular atrophy","volume":"12","author":"Zerres","year":"2002","journal-title":"Neuromuscul. Disord."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1590\/1980-57642018dn13-040011","article-title":"Cognitive performance of children with spinal muscular atrophy: A systematic review","volume":"13","author":"Polido","year":"2019","journal-title":"Dement. Neuropsychol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1016\/j.nmd.2017.01.017","article-title":"Matching pairs difficulty in children with spinal muscular atrophy type I","volume":"27","author":"Polido","year":"2017","journal-title":"Neuromuscul. Disord."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/S0960-8966(06)80008-8","article-title":"Cognitive functions in duchenne muscular dystrophy: A reappraisal and comparison with spinal muscular atrophy","volume":"2","author":"Billard","year":"1992","journal-title":"Neuromuscul. Disord."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e548","DOI":"10.1542\/peds.2004-0668","article-title":"Spinal Muscular Atrophy: Survival Pattern and Functional Status","volume":"114","author":"Chung","year":"2004","journal-title":"Pediatrics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1002\/ana.25549","article-title":"Severe brain involvement in 5q spinal muscular atrophy type 0","volume":"86","author":"Rocha","year":"2019","journal-title":"Ann. Neurol."},{"key":"ref_24","unstructured":"Kaufmann, A., and Lichtenberg, E. (2006). Assessing Adolescent and Adult Intelligence, Wiley. [3rd ed.]."},{"key":"ref_25","unstructured":"Petermann, F. (2012). Wechsler Adult Intelligence Scale (WAIS-IV) (Deutsche Ausgabe), Pearson Assessment."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Phelps, R.F. (2009). Chapter 1: Logical Fallacies Used to Dismiss the Evidence on Intelligence Testing. Washington (DC). Correcting Fallacies about Educational and Psychological Testing, American Psychological Association.","DOI":"10.1037\/11861-000"},{"key":"ref_27","first-page":"137","article-title":"The Psychological Methods of Testing Intelligence","volume":"13","author":"Gordon","year":"1916","journal-title":"J. Philos. Psychol. Sci. Methods"},{"key":"ref_28","unstructured":"(2021, May 20). Statistisches Bundesamt. Available online: https:\/\/www.destatis.de\/EN\/Themes\/Society-Environment\/Education-Research-Culture\/Schools\/Tables\/graduates-school-leavers-type-qualification-class.html."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1002\/mus.20535","article-title":"Cognitive impairment in neuromuscular disorders","volume":"34","author":"Bresolin","year":"2006","journal-title":"Muscle Nerve"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1748","DOI":"10.1007\/s12035-019-01845-w","article-title":"Dystrophin Dp71 and the Neuropathophysiology of Duchenne Muscular Dystrophy","volume":"57","author":"Naidoo","year":"2019","journal-title":"Mol. Neurobiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e1370","DOI":"10.1212\/WNL.0000000000006317","article-title":"ALS-specific cognitive and behavior changes associated with advancing disease stage in ALS","volume":"91","author":"Crockford","year":"2018","journal-title":"Neurology"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Osmanovic, A., Wieselmann, G., Mix, L., Siegler, H., Kumpe, M., Ranxha, G., Wurster, C., Steinke, A., Ludolph, A., and Kopp, B. (2020). Cognitive Performance of Patients with Adult 5q-Spinal Muscular Atrophy and with Amyotrophic Lateral Sclerosis. Brain Sci., 11.","DOI":"10.3390\/brainsci11010008"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1207\/S15326942DN2103_4","article-title":"Spatial Cognition in Young Children with Spinal Muscular Atrophy","volume":"21","author":"Riviere","year":"2002","journal-title":"Dev. Neuropsychol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1124\/jpet.113.212407","article-title":"Pharmacology of a Central Nervous System Delivered 2\u2032-O-Methoxyethyl\u2013Modified Survival of Motor Neuron Splicing Oligonucleotide in Mice and Nonhuman Primates","volume":"350","author":"Rigo","year":"2014","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4817","DOI":"10.1172\/JCI124120","article-title":"Age-dependent SMN expression in disease-relevant tissue and implications for SMA treatment","volume":"129","author":"Ramos","year":"2019","journal-title":"J. Clin. Investig."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"643","DOI":"10.3233\/JAD-180080","article-title":"The Montreal Cognitive Assessment: Normative Data from a German-Speaking Cohort and Comparison with International Normative Samples","volume":"64","author":"Thomann","year":"2018","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.12740\/PP\/45368","article-title":"Is the Montreal Cognitive Assessment (MoCA) test better suited than the Mini-Mental State Examination (MMSE) in mild cognitive impairment (MCI) detection among people aged over 60? Meta-analysis","volume":"50","author":"Ciesielska","year":"2016","journal-title":"Psychiatr. Polska"}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/11\/9\/1184\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:59:22Z","timestamp":1760165962000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/11\/9\/1184"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,9]]},"references-count":37,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["brainsci11091184"],"URL":"https:\/\/doi.org\/10.3390\/brainsci11091184","relation":{},"ISSN":["2076-3425"],"issn-type":[{"value":"2076-3425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,9]]}}}