Top

Open Access 08-04-2024 | Multiple Sclerosis | Review

The Prevalence of Cognitive Impairment in Relapsing-Remitting Multiple Sclerosis: A Systematic Review and Meta-analysis

Authors: Wendy Wu, Heather Francis, Abbie Lucien, Tyler-Ann Wheeler, Milena Gandy

Abstract

It is increasingly recognized that cognitive symptoms are a common sequelae of relapsing-remitting multiple sclerosis and are associated with adverse functional consequences. However, estimates of cognitive impairment (CIm) prevalence vary widely. This study aimed to determine the pooled prevalence of CIm among adults with RRMS and investigate moderators of prevalence rates. Following prospective registration (PROSPERO; CRD42021281815), electronic databases (Embase, Scopus, Medline, and PsycINFO) were searched from inception until March 2023. Eligible studies reported the prevalence of CIm among adults with RRMS, as determined through standardized neuropsychological testing and defined as evidence of reduced performance across at least two cognitive domains (e.g., processing speed, attention) relative to normative samples, healthy controls, or premorbid estimates. The electronic database search yielded 8695 unique records, of which 50 met selection criteria. The pooled prevalence of cognitive impairment was 32.5% (95% confidence interval 29.3–36.0%) across 5859 participants. Mean disease duration and age were significant predictors of cognitive impairment prevalence, with samples with longer disease durations and older age reporting higher prevalence rates. Studies which administered more extensive test batteries also reported significantly higher cognitive impairment prevalence. Approximately one third of adults with RRMS experience clinical levels of CIm. This finding supports the use of routine cognitive testing to enable early detection of CIm, and to identify individuals who may benefit from additional cognitive and functional support during treatment planning.

Available only for authorised users

Abdelnour, C., Rodríguez-Gómez, O., Alegret, M., Valero, S., Moreno-Grau, S., Sanabria, Á., Hernández, I., Rosende-Roca, M., Vargas, L., Mauleón, A., Sánchez, D., Espinosa, A., Ortega, G., Pérez-Cordón, A., Diego, S., Gailhajanet, A., Guitart, M., Sotolongo-Grau, Ó., Ruiz, A., … Boada, M. (2017). Impact of recruitment methods in subjective cognitive decline. Journal of Alzheimer’s Disease, 57, 625–632. https://doi.org/10.3233/JAD-160915CrossRefPubMed

Akbar, N., Lobaugh, N. J., O’Connor, P., Moradzadeh, L., Scott, C. J., & Feinstein, A. (2010). Diffusion tensor imaging abnormalities in cognitively impaired multiple sclerosis patients. Canadian Journal of Neurological Sciences, 37(5), 608–614. https://doi.org/10.1017/S0317167100010775CrossRef

Altieri, M., Fratino, M., Maestrini, I., Dionisi, C., Annecca, R., Vicenzini, E., & Di Piero, V. (2021). Cognitive performance in relapsing-remitting multiple sclerosis: At risk or impaired? Dementia and Geriatric Cognitive Disorders, 49(6), 539–543. https://doi.org/10.1159/000514674CrossRef

Amato, M., Hakiki, B., Goretti, B., Rossi, F., Stromillo, M., Giorgio, A., Roscio, M., Ghezzi, A., Guidi, L., Bartolozzi, M., Portaccio, E., & De Stefano, N. (2012). Association of MRI metrics and cognitive impairment in radiologically isolated syndromes. Neurology, 78(5), 309–314. https://doi.org/10.1212/wnl.0b013e31824528c9CrossRefPubMed

Amato, M., Bartolozzi, M., Zipoli, V., Portaccio, E., Mortilla, M., Guidi, L., Siracusa, G., Sorbi, S., Federico, A., & De Stefano, N. (2004). Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology, 63(1), 89–93. https://doi.org/10.1212/01.wnl.0000129544.79539.d5CrossRefPubMed

Amato, M., Portaccio, E., Stromillo, M., Goretti, B., Zipoli, V., Siracusa, G., Battaglini, M., Giorgio, A., Bartolozzi, M., Guidi, L., Sorbi, S., Federico, A., & De Stefano, N. (2008). Cognitive assessment and quantitative magnetic resonance metrics can help to identify benign multiple sclerosis. Neurology, 71(9), 632–638. https://doi.org/10.1212/01.wnl.0000324621.58447.00CrossRefPubMed

Amato, M. P., Portaccio, E., Goretti, B., Zipoli, V., Iudice, A., Della Pina, D., Malentacchi, G., Sabatini, S., Annunziata, P., Falcini, M., Mazzoni, M., Mortilla, M., Fonda, C., De Stefano, N., & Tu, S. S. G. (2010). Relevance of cognitive deterioration in early relapsing-remitting MS: a 3-year follow-up study. Multiple Sclerosis, 16(12), 1474–1482. https://doi.org/10.1177/1352458510380089CrossRefPubMed

Amato, M. P., Zipoli, V., & Portaccio, E. (2006). Multiple sclerosis-related cognitive changes: A review of cross-sectional and longitudinal studies. Journal of the Neurological Sciences, 245(1), 41–46. https://doi.org/10.1016/j.jns.2005.08.019CrossRefPubMed

Benedict, R. H., Amato, M. P., Boringa, J., Brochet, B., Foley, F., Fredrikson, S., Hamalainen, P., Hartung, H., Krupp, L., Penner, I., Reder, A. T., & Langdon, D. (2012). Brief International Cognitive Assessment for MS (BICAMS): International standards for validation. BMC Neurology, 12, 55. https://simsrad.net.ocs.mq.edu.au/login?url=http://ovidsp.ovid.com/ovidweb.cgi?T=JS&CSC=Y&NEWS=N&PAGE=fulltext&D=med9&AN=22799620https://libkey.io/libraries/590/openurl?sid=OVID:medline&id=pmid:22799620&id=doi:10.1186%2F1471-2377-12-55&issn=1471-2377&isbn=&volume=12&issue=1&spage=55&pages=55&date=2012&title=BMC+Neurology&atitle=Brief+International+Cognitive+Assessment+for+MS+%28BICAMS%29%3A+international+standards+for+validation.&aulast=Benedict

Benedict, R. H., Fischer, J. S., Archibald, C. J., Arnett, P. A., Beatty, W. W., Bobholz, J., Chelune, G. J., Fisk, J. D., Langdon, D. W., Caruso, L., Foley, F., LaRocca, N. G., Vowels, L., Weinstein, A., DeLuca, J., Rao, S. M., & Munschauer, F. (2002). Minimal neuropsychological assessment of MS patients: A consensus approach. The Clinical Neuropsychologist, 16(3), 381–397. https://doi.org/10.1076/clin.16.3.381.13859CrossRefPubMed

Bever, C. T., Jr., Grattan, L., Panitch, H. S., & Johnson, K. P. (1995). The brief repeatable battery of neuropsychological tests for multiple sclerosis: A preliminary serial study. Multiple Sclerosis Journal, 1(3), 165–169. https://doi.org/10.1177/135245859500100306CrossRefPubMed

Bisecco, A., Rocca, M., Pagani, E., Mancini, L., Enzinger, C., Gallo, A., Vrenken, H., Stromillo, M. L., Copetti, M., Thomas, D., Fazekas, F., Tedeschi, G., Barkhof, F., De Stefano, N., & Filippi, M. (2015). Connectivity-based parcellation of the thalamus in multiple sclerosis and its implications for cognitive impairment: A multicenter study. Human Brain Mapping, 36(7). https://doi.org/10.1002/hbm.22809

Bobholz, J. A., & Rao, S. M. (2003). Cognitive dysfunction in multiple sclerosis: A review of recent developments. Current Opinion in Neurology, 16(3), 283–288. https://doi.org/10.1097/01.wco.0000073928.19076.84CrossRefPubMed

Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2013). Comprehensive meta-analysis version 3. Biostat.

Broen, M. P., Braaksma, M. M., Patijn, J., & Weber, W. E. (2012). Prevalence of pain in Parkinson’s disease: A systematic review using the modified QUADAS tool. Movement Disorders, 27(4), 480–484. https://doi.org/10.1002/mds.24054CrossRefPubMed

Broen, M. P. G., Narayen, N. E., Kuijf, M. L., Dissanayaka, N. N. W., & Leentjens, A. F. G. (2016). Prevalence of anxiety in Parkinson’s disease: A systematic review and meta-analysis. Movement Disorders, 31(8), 1125–1133. https://doi.org/10.1002/mds.26643CrossRefPubMed

Bruce, J. M., Hancock, L. M., Arnett, P., & Lynch, S. (2010). Treatment adherence in multiple sclerosis: Association with emotional status, personality, and cognition. Journal of Behavioral Medicine, 33(3), 219–227. https://doi.org/10.1007/s10865-010-9247-yCrossRefPubMed

Caceres, F., Vanotti, S., Benedict, R. H., & RELACCEM Work Group. (2014). Cognitive and neuropsychiatric disorders among multiple sclerosis patients from Latin America: Results of the RELACCEM study. Multiple Sclerosis and Related Disorders, 3(3), 335–340. https://doi.org/10.1016/j.msard.2013.10.007CrossRefPubMed

Carotenuto, A., Valsasina, P., Schoonheim, M. M., Geurts, J. J. G., Barkhof, F., Gallo, A., Tedeschi, G., Tommasin, S., Pantano, P., Filippi, M., & Rocca, M. A. (2022). Investigating functional network abnormalities and associations with disability in multiple sclerosis. Neurology, 99(22), e2517–e2530. https://doi.org/10.1212/wnl.0000000000201264CrossRefPubMed

Clemens, L., & Langdon, D. (2018). How does cognition relate to employment in multiple sclerosis? A systematic review. Multiple Sclerosis and Related Disorders, 26, 183–191. https://doi.org/10.1016/j.msard.2018.09.018CrossRefPubMed

Conti, L., Preziosa, P., Meani, A., Vizzino, C., Riccitelli, G., Pagani, E., Valsasina, P., Marchesi, O., Filippi, M., & Rocca, M. A. (2021). Unraveling the substrates of cognitive impairment in multiple sclerosis: The contribution of a multiparametric structural and functional mri approach. Multiple Sclerosis Journal, 26, 513. https://doi.org/10.1111/ene.15023CrossRef

Cree, B. A., Gourraud, P. A., Oksenberg, J. R., Bevan, C., Crabtree-Hartman, E., Gelfand, J. M., Goodin, D. S., Graves, J., Green, A. J., Mowry, E., Okuda, D. T., Pelletier, D., von Büdingen, H. C., Zamvil, S. S., Agrawal, A., Caillier, S., Ciocca, C., Gomez, R., Kanner, R., … & Hauser, S. L. (2016). Long-term evolution of multiple sclerosis disability in the treatment era. Annals of Neurology, 80(4), 499–510. https://doi.org/10.1002/ana.24747CrossRefPubMedPubMedCentral

Damasceno, A., Pimentel-Silva, L. R., Damasceno, B. P., & Cendes, F. (2020). Cognitive trajectories in relapsing-remitting multiple sclerosis: A longitudinal 6-year study. Multiple Sclerosis Journal, 26(13), 1740–1751. https://doi.org/10.1177/1352458519878685CrossRefPubMed

d’Ambrosio, A., Valsasina, P., Gallo, A., De Stefano, N., Pareto, D., Barkhof, F., Ciccarelli, O., Enzinger, C., Tedeschi, G., Stromillo, M. L., Arévalo, M. J., Hulst, H. E., Muhlert, N., Koini, M., Filippi, M., & Rocca, M. A. (2020). Reduced dynamics of functional connectivity and cognitive impairment in multiple sclerosis. Multiple Sclerosis Journal, 26(4), 476–488. https://doi.org/10.1177/1352458519837707CrossRefPubMed

Day, G. S., Rae-Grant, A., Armstrong, M. J., Pringsheim, T., Cofield, S. S., & Marrie, R. A. (2018). Identifying priority outcomes that influence selection of disease-modifying therapies in MS. Neurology Clinical Practice, 8(3), 179–185. https://doi.org/10.1212/cpj.0000000000000449CrossRefPubMedPubMedCentral

Deeks, J. J., Higgins, J. P. T., & Altman, D. G. (2019). Analysing data and undertaking meta-analyses (Vol. 2nd Edition). John Wiley & Sons.

Deloire, M. S., Salort, E., Bonnet, M., Arimone, Y., Boudineau, M., Amieva, H., Barroso, B., Ouallet, J. C., Pachai, C., Galliaud, E., Petry, K. G., Dousset, V., Fabrigoule, C., & Brochet, B. (2005). Cognitive impairment as marker of diffuse brain abnormalities in early relapsing remitting multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry, 76(4), 519–526. https://doi.org/10.1136/jnnp.2004.045872CrossRef

Douglas, K. M., Gallagher, P., Robinson, L. J., Carter, J. D., McIntosh, V. V., Frampton, C. M., Watson, S., Young, A. H., Ferrier, I. N., & Porter, R. J. (2018). Prevalence of cognitive impairment in major depression and bipolar disorder. Bipolar Disorders, 20(3), 260–274. https://doi.org/10.1111/bdi.12602CrossRefPubMed

Drake, A. S., Weinstock-Guttman, B., Morrow, S. A., Hojnacki, D., Munschauer, F. E., & Benedict, R. H. (2010). Psychometrics and normative data for the Multiple Sclerosis Functional Composite: Replacing the PASAT with the Symbol Digit Modalities Test. Multiple Sclerosis, 16(2), 228–237. https://doi.org/10.1177/1352458509354552CrossRefPubMed

Dusankova, J. B., Kalincik, T., Havrdova, E., & Benedict, R. H. B. (2012). Cross cultural validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). Clinical Neuropsychologist, 26(7), 1186–1200. https://doi.org/10.1080/13854046.2012.725101CrossRefPubMed

Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56(2), 455–463. http://www.jstor.org/stable/2676988

Eshaghi, A., Riyahi-Alam, S., Roostaei, T., Haeri, G., Aghsaei, A., Aidi, M. R., Pouretemad, H. R., Zarei, M., Farhang, S., Saeedi, R., Nazeri, A., Ganjgahi, H., Etesam, F., Azimi, A. R., Benedict, R. H. B., & Sahraian, M. A. (2012). Validity and reliability of a Persian translation of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Clinical Neuropsychologist, 26(6), 975–984. https://doi.org/10.1080/13854046.2012.694912CrossRefPubMed

Farias, S. T., Mungas, D., Reed, B. R., Harvey, D., & DeCarli, C. (2009). Progression of mild cognitive impairment to dementia in clinic- vs community-based cohorts. Archives of Neurology, 66(9), 1151–1157. https://doi.org/10.1001/archneurol.2009.106CrossRefPubMedPubMedCentral

Gajofatto, A., Turatti, M., Bianchi, M., Forlivesi, S., Gobbin, F., Azzara, A., Monaco, S., & Benedetti, M. (2016). Benign multiple sclerosis: Physical and cognitive impairment follow distinct evolutions. Acta Neurologica Scandinavica, 133(3), 183–191. https://doi.org/10.1111/ane.12442CrossRefPubMed

Gois, L. C. P., Pimentel-Silva, L. R., Damasceno, B. P., & Damasceno, A. (2021). Associations between cognitive and clinical disability across MS subtypes: The role of the underlying brain damage. Multiple Sclerosis and Related Disorders, 48, 102701. https://doi.org/10.1016/j.msard.2020.102701CrossRefPubMed

Goretti, B., Viterbo, R., Portaccio, E., Niccolai, C., Hakiki, B., Piscolla, E., Iaffaldano, P., Trojano, M., & Amato, M. (2014). Anxiety state affects information processing speed in patients with multiple sclerosis. Neurological Sciences, 35(4), 559–563. https://doi.org/10.1007/s10072-013-1544-0CrossRefPubMed

Goverover, Y., Chiaravalloti, N., & DeLuca, J. (2019). Money management in multiple sclerosis: The role of cognitive, motor, and affective factors [Original Research]. Frontiers in Neurology, 10(1128). https://doi.org/10.3389/fneur.2019.01128

Hancock, L. M., Hermann, B., Schoonheim, M. M., Hetzel, S. J., Brochet, B., & DeLuca, J. (2022). Comparing diagnostic criteria for the diagnosis of neurocognitive disorders in multiple sclerosis. Multiple Sclerosis and Related Disorders, 58, 103479. https://doi.org/10.1016/j.msard.2021.103479CrossRefPubMed

Harding, K. E., Liang, K., Cossburn, M. D., Ingram, G., Hirst, C. L., Pickersgill, T. P., Te Water Naude, J., Wardle, M., Ben-Shlomo, Y., & Robertson, N. P. (2013). Long-term outcome of paediatric-onset multiple sclerosis: A population-based study. Journal of Neurology, Neurosurgery & Psychiatry, 84(2), 141. https://doi.org/10.1136/jnnp-2012-303996CrossRef

Heesen, C., Böhm, J., Reich, C., Kasper, J., Goebel, M., & Gold, S. M. (2008). Patient perception of bodily functions in multiple sclerosis: Gait and visual function are the most valuable. Multiple Sclerosis Journal, 14(7), 988–991. https://doi.org/10.1177/1352458508088916CrossRefPubMed

Hughes, A. J., Bhattarai, J., Paul, S., & Beier, M. (2019). 2019/05/01/). Depressive symptoms and fatigue as predictors of objective-subjective discrepancies in cognitive function in multiple sclerosis. Multiple Sclerosis and Related Disorders, 30, 192–197. https://doi.org/10.1016/j.msard.2019.01.055CrossRefPubMedPubMedCentral

Hulst, H. E., Schoonheim, M. M., Roosendaal, S. D., Popescu, V., Schweren, L. J., van der Werf, Y. D., Visser, L. H., Polman, C. H., Barkhof, F., & Geurts, J. J. (2012). Functional adaptive changes within the hippocampal memory system of patients with multiple sclerosis. Hum Brain Mapp, 33(10), 2268–2280. https://doi.org/10.1002/hbm.21359CrossRefPubMed

Iaffaldano, P., Viterbo, R. G., Goretti, B., Portaccio, E., Amato, M. P., & Trojano, M. (2014). Emotional and neutral verbal memory impairment in multiple sclerosis. Multiple Sclerosis, 1, 408–409. https://doi.org/10.1016/j.jns.2014.03.038CrossRef

Jakimovski, D., Weinstock-Guttman, B., Roy, S., Jaworski, M., Hancock, L., Nizinski, A., Srinivasan, P., Fuchs, T. A., Szigeti, K., Zivadinov, R., & Benedict, R. H. (2019). Cognitive profiles of aging in multiple sclerosis. Frontiers in Aging Neuroscience. https://doi.org/10.3389/fnagi.2019.00105CrossRefPubMedPubMedCentral

Jandric, D., Lipp, I., Paling, D., Rog, D., Castellazzi, G., Haroon, H., Parkes, L., Parker, G., Tomassini, V., & Muhlert, N. (2021). Mechanisms of network changes in cognitive impairment in multiple sclerosis. Neurology, 97, 19. https://doi.org/10.1212/WNL.0000000000012834CrossRef

Johnen, A., Landmeyer, N. C., Bürkner, P.-C., Wiendl, H., Meuth, S. G., & Holling, H. (2017). Distinct cognitive impairments in different disease courses of multiple sclerosis—A systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews, 83, 568–578. https://doi.org/10.1016/j.neubiorev.2017.09.005CrossRef

Jonkman, L., Rosenthal, D. M., Sormani, M. P., Miles, L., Herbert, J., Grossman, R. I., & Inglese, M. (2015). Gray matter correlates of cognitive performance differ between relapsing-remitting and primary-progressive multiple sclerosis. Multiple Sclerosis, 1, 362. https://doi.org/10.1371/journal.pone.0129380CrossRef

Julian, L., Merluzzi, N. M., & Mohr, D. C. (2007). The relationship among depression, subjective cognitive impairment, and neuropsychological performance in multiple sclerosis. Multiple Sclerosis Journal, 13(1), 81–86. https://doi.org/10.1177/1352458506070255CrossRefPubMed

Kinsinger, S. W., Lattie, E., & Mohr, D. C. (2010). Relationship between depression, fatigue, subjective cognitive impairment, and objective neuropsychological functioning in patients with multiple sclerosis. Neuropsychology, 24(5), 573–580. https://doi.org/10.1037/a0019222CrossRefPubMedPubMedCentral

Kurtzke, J. F. (1983). Rating neurologic impairment in multiple sclerosis: An Expanded Disability Status Scale (EDSS). Neurology, 33(11), 1444–1452. https://doi.org/10.1212/wnl.33.11.1444CrossRefPubMed

Lanzillo, R., Prinster, A., Scarano, V., Liuzzi, R., Coppola, G., Florio, C., Salvatore, E., Schiavone, V., Brunetti, A., Muto, M., Orefice, G., Alfano, B., Bonavita, V., & Morra, V. B. (2006). Neuropsychological assessment, quantitative MRI and ApoE gene polymorphisms in a series of MS patients treated with IFN beta-1b. Journal of the Neurological Sciences, 245(1–2), 141–145. https://doi.org/10.1016/j.jns.2005.08.023CrossRefPubMed

Leboeuf-Yde, C., & Lauritsen, J. M. (1995). The prevalence of low back pain in the literature. A structured review of 26 Nordic studies from 1954 to 1993. Spine (Phila Pa 1976), 20(19), 2112–2118. https://doi.org/10.1097/00007632-199510000-00009CrossRefPubMed

Leray, E., Moreau, T., Fromont, A., & Edan, G. (2016). Epidemiology of multiple sclerosis. Revue Neurologique, 172(1), 3–13. https://doi.org/10.1016/j.neurol.2015.10.006CrossRefPubMed

Lozano-Soto, E., Cruz-López, Á., Gutiérrez, R., González, M., Sanmartino, F., Rashid-Lopez, R., Espinosa-Rosso, R., Forero, L., & González-Rosa, J. J. (2021). Predicting neuropsychological impairment in relapsing remitting multiple sclerosis: The Role of clinical measures, treatment, and neuropsychiatry symptoms. Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists, 36(4), 475–484. https://doi.org/10.1093/arclin/acaa088CrossRefPubMed

Ma, A. Y., Vitorino, R. C., Hojjat, S. P., Mulholland, A. D., Zhang, L., Lee, L., Carroll, T. J., Cantrell, C. G., Figley, C. R., & Aviv, R. I. (2017). The relationship between white matter fiber damage and gray matter perfusion in largescale functionally defined networks in multiple sclerosis. Multiple Sclerosis Journal, 23, 1884–1892. https://doi.org/10.1177/1352458517691149CrossRefPubMed

Maarouf, A., Audoin, B., Pariollaud, F., Gherib, S., Rico, A., Soulier, E., Confort-Gouny, S., Guye, M., Schad, L., Pelletier, J., Ranjeva, J.-P., & Zaaraoui, W. (2017). Increased total sodium concentration in gray matter better explains cognition than atrophy in MS. Neurology, 88(3), 289–295. https://doi.org/10.1212/WNL.0000000000003511CrossRefPubMed

Mashayekhi, F., Sadigh-Eteghad, S., Naseri, A., Asadi, M., Abbasi Garravnd, N., & Talebi, M. (2022). ApoE4-positive multiple sclerosis patients are more likely to have cognitive impairment: A cross-sectional study. Neurol Sci, 43(2), 1189–1196. https://doi.org/10.1007/s10072-021-05383-zCrossRefPubMed

Maubeuge, N., Deloire, M. S. A., Brochet, B., Ehrle, N., Charre-Morin, J., Saubusse, A., Ruet, A., BICAFMS Study Investigators. (2021). Validation of the French version of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Multiple Sclerosis and Related Disorders, 48, 102692. https://doi.org/10.1016/j.msard.2020.102692CrossRefPubMed

McIntosh-Michaelis, S. A., Roberts, M. H., Wilkinson, S. M., Diamond, I. D., McLellan, D. L., Martin, J. P., & Spackman, A. J. (1991). The prevalence of cognitive impairment in a community survey of multiple sclerosis. British Journal of Clinical Psychology, 30(4), 333–348. https://doi.org/10.1111/j.2044-8260.1991.tb00954.xCrossRefPubMed

McKay, K. A., Manouchehrinia, A., Berrigan, L., Fisk, J. D., Olsson, T., & Hillert, J. (2019). Long-term cognitive outcomes in patients with pediatric-onset vs adult-onset multiple sclerosis. JAMA Neurology, 76(9), 1028–1034. https://doi.org/10.1001/jamaneurol.2019.1546CrossRefPubMedPubMedCentral

McNicholas, N., O’connell, K., Yap, S. M., Killeen, R. P., Hutchinson, M., & McGuigan, C. (2018). Cognitive dysfunction in early multiple sclerosis: A review. QJM: An International Journal of Medicine, 111(6), 359–364. https://doi.org/10.1093/qjmed/hcx070CrossRefPubMed

Meijer, K. A., Eijlers, A. J. C., Douw, L., Uitdehaag, B. M., Barkhof, F., Geurts, J. J., & Schoonheim, M. M. (2017). Increased connectivity of hub networks and cognitive impairment in multiple sclerosis. Neurology, 88(22), 2107–2114. https://doi.org/10.1212/WNL.0000000000003982CrossRefPubMed

Migliore, S., Ghazaryan, A., Simonelli, I., Pasqualetti, P., Squitieri, F., Curcio, G., Landi, D., Palmieri, M., Moffa, F., Filippi, M., & Vernieri, F. (2017). Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behavioural Neurology, 2017, 7404289. https://doi.org/10.1155/2017/7404289CrossRefPubMedPubMedCentral

Moccia, M., Lanzillo, R., Palladino, R., Chang, K. C., Costabile, T., Russo, C., De Rosa, A., Carotenuto, A., Sacca, F., Maniscalco, G. T., & Brescia Morra, V. (2016). Cognitive impairment at diagnosis predicts 10-year multiple sclerosis progression. Multiple Sclerosis, 22(5), 659–667. https://doi.org/10.1177/1352458515599075CrossRefPubMed

Mortensen, G. L., Theódórsdóttir, Á., Sejbæk, T., & Illes, Z. (2020). Patient attitudes to routine cognitive testing in multiple sclerosis. Patient preference and adherence, 14, 693–704. https://doi.org/10.2147/PPA.S245623CrossRefPubMedPubMedCentral

Niccolai, C., Portaccio, E., Goretti, B., Hakiki, B., Giannini, M., Pastò, L., Righini, I., Falautano, M., Minacapelli, E., Martinelli, V., Incerti, C., Nocentini, U., Fenu, G., Cocco, E., Marrosu, M. G., Garofalo, E., Ambra, F. I., Maddestra, M., Consalvo, M., Viterbo, R. G., Trojano, M., Losignore, N. A., Zimatore, G. B., Pietrolongo, E., Lugaresi, A., Pippolo, L., Roscio, M., Ghezzi, A., Castellano, D., Stecchi, S., & Amato, M. P. (2015). A comparison of the brief international cognitive assessment for multiple sclerosis and the brief repeatable battery in multiple sclerosis patients. BMC Neurology, 15(1), 204. https://doi.org/10.1186/s12883-015-0460-8CrossRefPubMedPubMedCentral

Ouzzani, M., Hammady, H., Fedorowicz, Z., & Elmagarmid, A. (2016). Rayyan — A web and mobile app for systematic reviews. Systematic Reviews, 5(210). https://doi.org/10.1186/s13643-016-0384-4

Ozkul, C., Guclu-Gunduz, A., Eldemir, K., Apaydin, Y., Yazici, G., & Irkec, C. (2020). Clinical features and physical performance in multiple sclerosis patients with and without cognitive impairment: a cross-sectional study. International Journal of Rehabilitation Research, 43(4), 316–323. https://doi.org/10.1097/mrr.0000000000000428CrossRefPubMed

Parsons, O. A., Stewart, K. D., & Arenberg, D. (1957). Impairment of abstracting ability in multiple sclerosis. The Journal of Nervous And Mental Disease, 125(2), 221–225. https://doi.org/10.1097/00005053-195704000-00007CrossRefPubMed

Patti, F., Amato, M. P., Trojano, M., Bastianello, S., Tola, M. R., Goretti, B., Caniatti, L., Di Monte, E., Ferrazza, P., Brescia Morra, V., Lo Fermo, S., Picconi, O., Luccichenti, G., & COGIMUS Study Group. (2009). Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis (COGIMUS) study. Multiple Sclerosis, 15(7), 779–788. https://doi.org/10.1177/1352458509105544CrossRefPubMed

Planche, V., Gibelin, M., Cregut, D., Pereira, B., & Clavelou, P. (2016). Cognitive impairment in a population-based study of patients with multiple sclerosis: Differences between late relapsing-remitting, secondary progressive and primary progressive multiple sclerosis. European Journal of Neurology, 23(2), 282–289. https://doi.org/10.1111/ene.12715CrossRefPubMed

Portaccio, E., Goretti, B., Zipoli, V., Nacmias, B., Stromillo, M. L., Bartolozzi, M. L., Siracusa, G., Guidi, L., Federico, A., Sorbi, S., De Stefano, M., & Amato, M. P. (2009a). APOE-ε4 is not associated with cognitive impairment in relapsing-remitting multiple sclerosis. Multiple Sclerosis, 15(12), 1489–1494. https://doi.org/10.1177/1352458509348512CrossRefPubMed

Portaccio, E., Goretti, B., Zipoli, V., Siracusa, G., Sorbi, S., & Amato, M. (2009b). A short version of Rao’s Brief Repeatable Battery as a screening tool for cognitive impairment in multiple sclerosis. The Clinical Neuropsychologist, 23(2), 268–275. https://doi.org/10.1080/13854040801992815CrossRefPubMed

Prakash, R. S., Snook, E. M., Lewis, J. M., Motl, R. W., & Kramer, A. F. (2008). Cognitive impairments in relapsing-remitting multiple sclerosis: A meta-analysis. Multiple Sclerosis Journal, 14(9), 1250–1261. https://doi.org/10.1177/1352458508095004CrossRefPubMed

Preziosa, P., Rocca, M. A., Pagani, E., Stromillo, M. L., Enzinger, C., Gallo, A., Hulst, H. E., Atzori, M., Pareto, D., Riccitelli, G. C., Copetti, M., De Stefano, N., Fazekas, F., Bisecco, A., Barkhof, F., Yousry, T. A., Arevalo, M. J., Filippi, M., MS Group. (2016). Structural MRI correlates of cognitive impairment in patients with multiple sclerosis: A multicenter study. Human Brain Mapping, 37(4), 1627–1644. https://doi.org/10.1002/hbm.23125CrossRefPubMedPubMedCentral

Rao, S. M., Leo, G. J., Bernardin, L., & Unverzagt, F. (1991a). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology, 41(5), 685–691. https://doi.org/10.1212/wnl.41.5.685CrossRefPubMed

Rao, S. M., Leo, G. J., Ellington, L., Nauertz, T., Bernardin, L., & Unverzagt, F. (1991b). Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology, 41(5), 692–696. https://doi.org/10.1212/wnl.41.5.692CrossRefPubMed

Rayes, H. A., Tani, C., Kwan, A., Marzouk, S., Colosimo, K., Medina-Rosas, J., Mustafa, A., Su, J., Lambiris, P., Mosca, M., & Touma, Z. (2018). What is the prevalence of cognitive impairment in lupus and which instruments are used to measure it? A systematic review and meta-analysis. Seminars in Arthritis and Rheumatism, 48(2), 240–255. https://doi.org/10.1016/j.semarthrit.2018.02.007CrossRefPubMed

Rimkus, Cd. M., Junqueira Tde, F., Lyra, K. P., Jackowski, M. P., Machado, M. A., Miotto, E. C., Callegaro, D., Otaduy, M. C., & Leite Cda, C. (2011). Corpus callosum microstructural changes correlate with cognitive dysfunction in early stages of relapsing-remitting multiple sclerosis: Axial and radial diffusivities approach. Multiple Sclerosis International, 2011, 304875. https://doi.org/10.1155/2011/304875CrossRefPubMedPubMedCentral

Rimkus, C. M., Schoonheim, M. M., Steenwijk, M. D., Vrenken, H., Eijlers, A. J., Killestein, J., Wattjes, M. P., Leite, C. C., Barkhof, F., & Tijms, B. M. (2019). Gray matter networks and cognitive impairment in multiple sclerosis. Multiple Sclerosis, 25(3), 382–391. https://doi.org/10.1177/1352458517751650CrossRefPubMed

Rocca, M. A., Valsasina, P., Hulst, H. E., Abdel-Aziz, K., Enzinger, C., Gallo, A., Pareto, D., Riccitelli, G., Muhlert, N., Ciccarelli, O., Barkhof, F., Fazekas, F., Tedeschi, G., Arevalo, M. J., & Filippi, M. (2014). Functional correlates of cognitive dysfunction in multiple sclerosis: A multicenter fMRI study. Human Brain Mapping, 35(12), 5799–5814. https://doi.org/10.1002/hbm.22586CrossRefPubMedPubMedCentral

Ruano, L., Branco, M., Portaccio, E., Goretti, B., Niccolai, C., Patti, F., Chisari, C., Gallo, P., Grossi, P., Ghezzi, A., Roscio, M., Mattioli, F., Stampatori, C., Simone, M., Viterbo, R. G., & Amato, M. P. (2018). Patients with paediatric-onset multiple sclerosis are at higher risk of cognitive impairment in adulthood: An Italian collaborative study. Multiple Sclerosis Journal, 24(9), 1234–1242. https://doi.org/10.1177/1352458517717341CrossRefPubMed

Ruano, L., Portaccio, E., Goretti, B., Niccolai, C., Severo, M., Patti, F., Cilia, S., Gallo, P., Grossi, P., Ghezzi, A., Roscio, M., Mattioli, F., Stampatori, C., Trojano, M., Viterbo, R. G., & Amato, M. P. (2017). Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Multiple Sclerosis Journal, 23(9), 1258–1267. https://doi.org/10.1177/1352458516674367CrossRefPubMed

Sacco, R., Bisecco, A., Corbo, D., Della Corte, M., d’Ambrosio, A., Docimo, R., Gallo, A., Esposito, F., Esposito, S., Cirillo, M., Lavorgna, L., Tedeschi, G., & Bonavita, S. (2015). Cognitive impairment and memory disorders in relapsing-remitting multiple sclerosis: The role of white matter, gray matter and hippocampus. Journal of Neurology, 262(7), 1691–1697. https://doi.org/10.1007/s00415-015-7763-yCrossRefPubMed

Scherer, R. & Emslander, V. (2024). Utilizing primary study quality in meta-analyses in psychology: A step-by-step tutorial. PsyArXiv. https://doi.org/10.31234/osf.io/8emsa

Schoonhoven, D. N., Fraschini, M., Tewarie, P., Uitdehaag, B. M., Eijlers, A. J., Geurts, J. J., Hillebr, A., Schoonheim, M. M., Stam, C. J., & Strijbis, E. M. (2019). Resting-state MEG measurement of functional activation as a biomarker for cognitive decline in MS. Multiple Sclerosis, 25(14), 1896–1906. https://doi.org/10.1177/1352458518810260CrossRefPubMed

Sehanovic, A., Smajlovic, D., Tupkovic, E., Ibrahimagic, O. C., Kunic, S., Dostovic, Z., Zoletic, E., & Pasic, Z. (2020). Cognitive disorders in patients with multiple sclerosis. Materia Sociomedica, 32(3), 191. https://simsrad.net.ocs.mq.edu.au/login?url=http://ovidsp.ovid.com/ovidweb.cgi?T=JS&CSC=Y&NEWS=N&PAGE=fulltext&D=pmnm&AN=33424448https://libkey.io/libraries/590/openurl?sid=OVID:medline&id=pmid:33424448&id=doi:10.5455%2Fmsm.2020.32.191-195&issn=1512-7680&isbn=&volume=32&issue=3&spage=191&pages=191-195&date=2020&title=Materia+Sociomedica&atitle=Cognitive+Disorders+in+Patients+with+Multiple+Sclerosis.&aulast=Sehanovic

Sexton, E., McLoughlin, A., Williams, D. J., Merriman, N. A., Donnelly, N., Rohde, D., Hickey, A., Wren, M. A., & Bennett, K. (2019). Systematic review and meta-analysis of the prevalence of cognitive impairment no dementia in the first year post-stroke. European Stroke Journal, 4(2), 160–171. https://doi.org/10.1177/2396987318825484CrossRefPubMedPubMedCentral

Singer, B. A., Keith, S., Howerter, A., Doll, H., Pham, T., & Mehta, R. (2021). A study comparing patient and clinician perspectives of treatments for multiple sclerosis via group concept mapping. Patient Preference and Adherence, 15, 975–987. https://doi.org/10.2147/ppa.S297052CrossRefPubMedPubMedCentral

Skorve, E., Lundervold, A. J., Torkildsen, O., & Myhr, K. M. (2023). Assessment of cognitive function in early stages of multiple sclerosis. Validation of BICAMS in Norway. Multiple Sclerosis Journal, 24, 798. https://doi.org/10.1016/j.msard.2022.104398CrossRef

Strober, L., Englert, J., Munschauer, F., Weinstock-Guttman, B., Rao, S., & Benedict, R. H. (2009). Sensitivity of conventional memory tests in multiple sclerosis: Comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Multiple Sclerosis, 15(9), 1077–1084. https://doi.org/10.1177/1352458509106615CrossRefPubMed

Sumowski, J. F., Benedict, R., Enzinger, C., Filippi, M., Geurts, J. J., Hamalainen, P., Hulst, H., Inglese, M., Leavitt, V. M., Rocca, M. A., Rosti-Otajarvi, E. M., & Rao, S. (2018). Cognition in multiple sclerosis: State of the field and priorities for the future. Neurology, 90(6), 278–288. https://doi.org/10.1212/wnl.0000000000004977CrossRefPubMedPubMedCentral

Talebi, M., Sadigh-Eteghad, S., Talebi, M., Naseri, A., & Zafarani, F. (2022). Predominant domains and associated demographic and clinical characteristics in multiple sclerosis-related cognitive impairment in mildly disabled patients. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery, 58(1), 48. https://doi.org/10.1186/s41983-022-00485-7CrossRef

Tierney, J. F., Stewart, L. A., & Clarke, M. (2023) Chapter 26: Individual participant data. In: J. P. T. Higgins, J. Thomas, J. Chandler, M. Cumpston, T. Li, M. J. Page, V. A. Welch (Eds.) Cochrane Handbook for Systematic Reviews of Interventions version 6.4 (updated August 2023). Cochrane, 2023. Available from www.training.cochrane.org/handbook

Topcular, B., Ozcan, M., Kurt, E., Kuscu, D., Icen, N., Sutlas, P., Kirbas, D., & Bingol, A. (2012). Cognitive impairment in relapsing-remitting multiple sclerosis. Noropsikiyatri Arsivi, 49(3), 178–182. https://doi.org/10.4274/npa.y6089CrossRef

Tran, T., Milanovic, M., Holshausen, K., & Bowie, C. R. (2021). What is normal cognition in depression? Prevalence and functional correlates of normative versus idiographic cognitive impairment. Neuropsychology, 35(1), 33. https://doi.org/10.1037/neu0000717CrossRefPubMed

Walker, B. F. (2000). The prevalence of low back pain: A systematic review of the literature from 1966 to 1998. J Spinal Disord, 13(3), 205–217. https://doi.org/10.1097/00002517-200006000-00003CrossRefPubMed

Walton, C., King, R., Rechtman, L., Kaye, W., Leray, E., Marrie, R. A., Robertson, N., La Rocca, N., Uitdehaag, B., van der Mei, I., Wallin, M., Helme, A., Angood Napier, C., Rijke, N., & Baneke, P. (2020). Rising prevalence of multiple sclerosis worldwide: Insights from the Atlas of MS, third edition. Multiple Sclerosis, 26(14), 1816–1821. https://doi.org/10.1177/1352458520970841CrossRefPubMed

Whiting, P. F., Rutjes, A. W., Westwood, M. E., Mallett, S., Deeks, J. J., Reitsma, J. B., Leeflang, M. M., Sterne, J. A., & Bossuyt, P. M. (2011). QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Annals of Internal Medicine, 155(8), 529–536. https://doi.org/10.7326/0003-4819-155-8-201110180-00009CrossRefPubMed

Yazgan, Y. Z., Tarakcı, E., Gungor, F., & Kurtuncu, M. (2021). Understanding the impact of cognitive impairment and disease severity on activities of daily living in MS patients with different disability levels. Clinical Neurology and Neurosurgery, 200, 106398. https://doi.org/10.1016/j.clineuro.2020.106398CrossRefPubMed

Yohannes, A. M. P. M. F., Chen, W. P. M. P. H. M., Moga, A. M. M., Leroi, I. M., & Connolly, M. J. M. D. (2017). Cognitive impairment in chronic obstructive pulmonary disease and chronic heart failure: A systematic review and meta-analysis of observational studies. Journal of the American Medical Directors Association, 18(5), 451.e451-451.e411. https://doi.org/10.1016/j.jamda.2017.01.014CrossRef

Van Schependom, J., D’Hooghe, M. B., Cleynhens, K., D’Hooge, M., Haelewyck, M. C., De Keyser, J., & Nagels, G. (2014). The Symbol Digit Modalities Test as sentinel test for cognitive impairment in multiple sclerosis. European Journal of Neurology, 21(9), 1219–e72. https://doi.org/10.1111/ene.12463CrossRefPubMed

Winter, M., Tallantyre, E. C., Brice, T. A. W., Robertson, N. P., Jones, D. K., & Chamberland, M. (2021). Tract-specific MRI measures explain learning and recall differences in multiple sclerosis. Brain Communications, 3(2), fcab065. https://doi.org/10.1093/braincomms/fcab065CrossRefPubMedPubMedCentral

Zhang, X., Zhang, F., Huang, D., Wu, L., Ma, L., Liu, H., Zhao, Y., Yu, S., & Shi, J. (2016). Contribution of gray and white matter abnormalities to cognitive impairment in multiple sclerosis. International Journal of Molecular Sciences, 18(1), 27. https://doi.org/10.3390/ijms18010046CrossRef

Title: The Prevalence of Cognitive Impairment in Relapsing-Remitting Multiple Sclerosis: A Systematic Review and Meta-analysis
Authors: Wendy Wu
Heather Francis
Abbie Lucien
Tyler-Ann Wheeler
Milena Gandy
Publication date: 08-04-2024
Publisher: Springer US
Keyword: Multiple Sclerosis
Published in: Neuropsychology Review
Print ISSN: 1040-7308
Electronic ISSN: 1573-6660
DOI: https://doi.org/10.1007/s11065-024-09640-8

At a glance: The STEP trials

Springer Medicine

The Prevalence of Cognitive Impairment in Relapsing-Remitting Multiple Sclerosis: A Systematic Review and Meta-analysis

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content