Skip to main content
Top
Published in:

Open Access 01-12-2024 | Systematic Review

Comparing cognitive impairment using MACFIMS in patients with multiple sclerosis and healthy controls: a systematic review and meta-analysis

Authors: Amirreza Nasirzadeh, Mohammad Mohammadi, Melika Arab Bafrani, Aynaz Mohammadi, Hossein Bakhtiari-Dovvombaygi

Published in: BMC Neurology | Issue 1/2024

Login to get access

Abstract

Background

Multiple sclerosis (MS) is a chronic autoimmune disorder affecting the central nervous system, leading to a range of symptoms that impact physical, psychiatric, and cognitive functions. Cognitive dysfunction is prevalent among patients with MS (pwMS), affecting at least 65% of patients, and includes deficits in processing speed, attention, learning, memory, and executive function. Despite the significant impact on daily life, cognitive impairment in MS patients is often underrecognized in clinical settings.

Methods

This systematic review and meta-analysis aimed to evaluate cognitive function using the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS) battery among pwMS patients and healthy controls (HCs). A comprehensive search of the Web of Science, PubMed, Scopus, and Cochrane Library databases was conducted on January 2024 following the PRISMA guidelines. Eligible studies included peer-reviewed research assessing the validity of the MACFIMS in adult MS patients. Data extraction and quality assessment were performed using standardized tools, and statistical analyses were conducted using R4.2.3.

Results

Eight studies met the inclusion criteria, including a total of 1,481 pwMS and 1,072 HCs. The meta-analysis revealed significant cognitive deficits in pwMS patients compared to HCs across all the MACFIMS subtests, including language, spatial processing, new learning and memory, processing speed, and executive function. Processing speed and working memory were the most affected domains, with 36% of pwMS showing impairment on the Symbol Digit Modalities Test (SDMT). Subgroup analyses indicated that the Expanded Disability Status Scale (EDSS) score significantly influenced cognitive impairment, while disease duration had a limited impact.

Conclusions

The MACFIMS effectively discriminates between pwMS patients and HCs, demonstrating its validity as a comprehensive cognitive assessment tool for MS. Routine cognitive screening, particularly for processing speed and working memory, is crucial for early detection and intervention. Future research should focus on the sensitivity and specificity of the MACFIMS across diverse MS subtypes and cultural contexts to enhance its global applicability in clinical practice.
Appendix
Available only for authorised users
Literature
2.
go back to reference Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sørensen PS, Thompson AJ, et al. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology. 2014;83(3):278–86.PubMedPubMedCentralCrossRef Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sørensen PS, Thompson AJ, et al. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology. 2014;83(3):278–86.PubMedPubMedCentralCrossRef
3.
go back to reference Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018;17(2):162–73.PubMedCrossRef Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018;17(2):162–73.PubMedCrossRef
4.
go back to reference Filippi M, Bar-Or A, Piehl F, Preziosa P, Solari A, Vukusic S, et al. Author correction: multiple sclerosis. Nat Reviews Disease Primers. 2018;4(1):49.CrossRef Filippi M, Bar-Or A, Piehl F, Preziosa P, Solari A, Vukusic S, et al. Author correction: multiple sclerosis. Nat Reviews Disease Primers. 2018;4(1):49.CrossRef
5.
go back to reference Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, et al. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS. Multiple Scler J. 2020;26(14):1816–21.CrossRef Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, et al. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS. Multiple Scler J. 2020;26(14):1816–21.CrossRef
6.
go back to reference Habbestad A, Willumsen JS, Aarseth JH, Grytten N, Midgard R, Wergeland S, et al. Increasing age of multiple sclerosis onset from 1920 to 2022: a population-based study. J Neurol. 2024;271(4):1610–7.PubMedCrossRef Habbestad A, Willumsen JS, Aarseth JH, Grytten N, Midgard R, Wergeland S, et al. Increasing age of multiple sclerosis onset from 1920 to 2022: a population-based study. J Neurol. 2024;271(4):1610–7.PubMedCrossRef
7.
go back to reference Jellinger KA. Cognitive impairment in multiple sclerosis: from phenomenology to neurobiological mechanisms. J Neural Transm. 2024;131(8):871–99.PubMedCrossRef Jellinger KA. Cognitive impairment in multiple sclerosis: from phenomenology to neurobiological mechanisms. J Neural Transm. 2024;131(8):871–99.PubMedCrossRef
8.
go back to reference Oreja-Guevara C, Ayuso Blanco T, Brieva Ruiz L, Hernández Pérez MÁ, Meca-Lallana V, Ramió-Torrentà L. Cognitive dysfunctions and assessments in multiple sclerosis. Front Neurol. 2019;10:581.PubMedPubMedCentralCrossRef Oreja-Guevara C, Ayuso Blanco T, Brieva Ruiz L, Hernández Pérez MÁ, Meca-Lallana V, Ramió-Torrentà L. Cognitive dysfunctions and assessments in multiple sclerosis. Front Neurol. 2019;10:581.PubMedPubMedCentralCrossRef
9.
go back to reference Sumowski JF, Benedict R, Enzinger C, Filippi M, Geurts JJ, Hamalainen P, et al. Cognition in multiple sclerosis: state of the field and priorities for the future. Neurology. 2018;90(6):278–88.PubMedPubMedCentralCrossRef Sumowski JF, Benedict R, Enzinger C, Filippi M, Geurts JJ, Hamalainen P, et al. Cognition in multiple sclerosis: state of the field and priorities for the future. Neurology. 2018;90(6):278–88.PubMedPubMedCentralCrossRef
10.
go back to reference DeLuca J, Chiaravalloti ND, Sandroff BM. Treatment and management of cognitive dysfunction in patients with multiple sclerosis. Nat Reviews Neurol. 2020;16(6):319–32.CrossRef DeLuca J, Chiaravalloti ND, Sandroff BM. Treatment and management of cognitive dysfunction in patients with multiple sclerosis. Nat Reviews Neurol. 2020;16(6):319–32.CrossRef
11.
go back to reference Sehanovic A, Smajlovic D, Tupkovic E, Ibrahimagic OC, Kunic S, Dostovic Z, et al. Cognitive disorders in patients with multiple sclerosis. Materia socio-medica. 2020;32(3):191.PubMedPubMedCentralCrossRef Sehanovic A, Smajlovic D, Tupkovic E, Ibrahimagic OC, Kunic S, Dostovic Z, et al. Cognitive disorders in patients with multiple sclerosis. Materia socio-medica. 2020;32(3):191.PubMedPubMedCentralCrossRef
12.
go back to reference Longley WA, Honan C. Cognitive impairment in multiple sclerosis: the role of the general practitioner in cognitive screening and care coordination. Australian J Gen Pract. 2022;51(4):225–31.CrossRef Longley WA, Honan C. Cognitive impairment in multiple sclerosis: the role of the general practitioner in cognitive screening and care coordination. Australian J Gen Pract. 2022;51(4):225–31.CrossRef
15.
go back to reference Romero K, Shammi P, Feinstein A. Neurologists׳ accuracy in predicting cognitive impairment in multiple sclerosis. Multiple Scler Relat Disorders. 2015;4(4):291–5.CrossRef Romero K, Shammi P, Feinstein A. Neurologists׳ accuracy in predicting cognitive impairment in multiple sclerosis. Multiple Scler Relat Disorders. 2015;4(4):291–5.CrossRef
16.
go back to reference Elwick H, Smith L, Mhizha-Murira JR, Topcu G, Leighton P, Drummond A, et al. Cognitive assessment in multiple sclerosis clinical care: a qualitative evaluation of stakeholder perceptions and preferences. Neuropsychological Rehabilitation. 2022;32(7):1456–74.PubMedCrossRef Elwick H, Smith L, Mhizha-Murira JR, Topcu G, Leighton P, Drummond A, et al. Cognitive assessment in multiple sclerosis clinical care: a qualitative evaluation of stakeholder perceptions and preferences. Neuropsychological Rehabilitation. 2022;32(7):1456–74.PubMedCrossRef
17.
go back to reference Kalb R, Beier M, Benedict RH, Charvet L, Costello K, Feinstein A, et al. Recommendations for cognitive screening and management in multiple sclerosis care. Multiple Scler J. 2018;24(13):1665–80.CrossRef Kalb R, Beier M, Benedict RH, Charvet L, Costello K, Feinstein A, et al. Recommendations for cognitive screening and management in multiple sclerosis care. Multiple Scler J. 2018;24(13):1665–80.CrossRef
18.
go back to reference Klein OA, Das Nair R, Ablewhite J, Drummond A. Assessment and management of cognitive problems in people with multiple sclerosis: a National Survey of Clinical Practice. Int J Clin Pract. 2019;73(3):e13300.CrossRef Klein OA, Das Nair R, Ablewhite J, Drummond A. Assessment and management of cognitive problems in people with multiple sclerosis: a National Survey of Clinical Practice. Int J Clin Pract. 2019;73(3):e13300.CrossRef
19.
go back to reference Potticary H, Langdon D. A systematic review and meta-analysis of the brief cognitive assessment for multiple sclerosis (BICAMS) international validations. J Clin Med. 2023;12(2):703.PubMedPubMedCentralCrossRef Potticary H, Langdon D. A systematic review and meta-analysis of the brief cognitive assessment for multiple sclerosis (BICAMS) international validations. J Clin Med. 2023;12(2):703.PubMedPubMedCentralCrossRef
20.
go back to reference Meca-Lallana V, Gascón-Giménez F, Ginestal-López RC, Higueras Y, Téllez-Lara N, Carreres-Polo J et al. Cognitive impairment in multiple sclerosis: diagnosis and monitoring. Neurol Sci. 2021:1–11. Meca-Lallana V, Gascón-Giménez F, Ginestal-López RC, Higueras Y, Téllez-Lara N, Carreres-Polo J et al. Cognitive impairment in multiple sclerosis: diagnosis and monitoring. Neurol Sci. 2021:1–11.
21.
go back to reference Thrue C, Riemenschneider M, Hvid L, Stenager E, Dalgas U. Time matters: early-phase multiple sclerosis is accompanied by considerable impairments across multiple domains. Multiple Scler J. 2021;27(10):1477–85.CrossRef Thrue C, Riemenschneider M, Hvid L, Stenager E, Dalgas U. Time matters: early-phase multiple sclerosis is accompanied by considerable impairments across multiple domains. Multiple Scler J. 2021;27(10):1477–85.CrossRef
22.
go back to reference Langdon D. Fast facts: cognition in multiple sclerosis. 2023. Langdon D. Fast facts: cognition in multiple sclerosis. 2023.
23.
go back to reference Langdon D, Amato M, Boringa J, Brochet B, Foley F, Fredrikson S, et al. Recommendations for a brief international cognitive assessment for multiple sclerosis (BICAMS). Multiple Scler J. 2012;18(6):891–8.CrossRef Langdon D, Amato M, Boringa J, Brochet B, Foley F, Fredrikson S, et al. Recommendations for a brief international cognitive assessment for multiple sclerosis (BICAMS). Multiple Scler J. 2012;18(6):891–8.CrossRef
24.
go back to reference Benedict RH, Cookfair D, Gavett R, Gunther M, Munschauer F, Garg N, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2006;12(4):549–58.PubMedCrossRef Benedict RH, Cookfair D, Gavett R, Gunther M, Munschauer F, Garg N, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2006;12(4):549–58.PubMedCrossRef
25.
go back to reference Smith A. Symbol digit modalities test. The clinical neuropsychologist. 1973. Smith A. Symbol digit modalities test. The clinical neuropsychologist. 1973.
26.
go back to reference Benedict RHB, Zivadinov R. Reliability and validity of neuropsychological screening and assessment strategies in MS. J Neurol. 2007;254(2):II22–5.PubMed Benedict RHB, Zivadinov R. Reliability and validity of neuropsychological screening and assessment strategies in MS. J Neurol. 2007;254(2):II22–5.PubMed
27.
go back to reference Elwood RW. The California Verbal Learning Test: psychometric characteristics and clinical application. Neuropsychol Rev. 1995;5:173–201.PubMedCrossRef Elwood RW. The California Verbal Learning Test: psychometric characteristics and clinical application. Neuropsychol Rev. 1995;5:173–201.PubMedCrossRef
28.
go back to reference Barr W, Morrison C, Zaroff C, Devinsky O. Use of the brief Visuospatial Memory Test—revised (BVMT-R) in neuropsychological evaluation of epilepsy surgery candidates. Epilepsy Behav. 2004;5(2):175–9.PubMedCrossRef Barr W, Morrison C, Zaroff C, Devinsky O. Use of the brief Visuospatial Memory Test—revised (BVMT-R) in neuropsychological evaluation of epilepsy surgery candidates. Epilepsy Behav. 2004;5(2):175–9.PubMedCrossRef
29.
go back to reference Benedict RH, Schretlen D, Groninger L, Dobraski M, Shpritz B. Revision of the brief Visuospatial Memory Test: studies of normal performance, reliability, and validity. Psychol Assess. 1996;8(2):145.CrossRef Benedict RH, Schretlen D, Groninger L, Dobraski M, Shpritz B. Revision of the brief Visuospatial Memory Test: studies of normal performance, reliability, and validity. Psychol Assess. 1996;8(2):145.CrossRef
30.
go back to reference Delis DC, Kaplan E, Kramer JH. Delis-Kaplan executive function system. Assessment. 2001. Delis DC, Kaplan E, Kramer JH. Delis-Kaplan executive function system. Assessment. 2001.
31.
go back to reference Ruff R, Light R, Parker S, Levin H. Benton controlled oral word association test: reliability and updated norms. Arch Clin Neuropsychol. 1996;11(4):329–38.PubMedCrossRef Ruff R, Light R, Parker S, Levin H. Benton controlled oral word association test: reliability and updated norms. Arch Clin Neuropsychol. 1996;11(4):329–38.PubMedCrossRef
32.
go back to reference Benton AL, Varney N. Hamsher Kd. Judgment of line orientation. 1983. Benton AL, Varney N. Hamsher Kd. Judgment of line orientation. 1983.
33.
go back to reference Tranel D, Vianna E, Manzel K, Damasio H, Grabowski T. Neuroanatomical correlates of the Benton facial recognition test and judgment of line orientation test. J Clin Exp Neuropsychol. 2009;31(2):219–33.PubMedPubMedCentralCrossRef Tranel D, Vianna E, Manzel K, Damasio H, Grabowski T. Neuroanatomical correlates of the Benton facial recognition test and judgment of line orientation test. J Clin Exp Neuropsychol. 2009;31(2):219–33.PubMedPubMedCentralCrossRef
34.
go back to reference Benedict R, Amato M, Boringa J, Brochet B, Foley F, Fredrikson S, et al. Brief International Cognitive Assessment for MS (BICAMS): international standards for validation. MULTIPLE Scler J. 2011;17:S397–8. Benedict R, Amato M, Boringa J, Brochet B, Foley F, Fredrikson S, et al. Brief International Cognitive Assessment for MS (BICAMS): international standards for validation. MULTIPLE Scler J. 2011;17:S397–8.
35.
go back to reference Feinstein A, Lapshin H, O’Connor P. Looking anew at cognitive dysfunction in multiple sclerosis: the gorilla in the room. Neurology. 2012;79(11):1124–9.PubMedPubMedCentralCrossRef Feinstein A, Lapshin H, O’Connor P. Looking anew at cognitive dysfunction in multiple sclerosis: the gorilla in the room. Neurology. 2012;79(11):1124–9.PubMedPubMedCentralCrossRef
36.
go back to reference Maubeuge N, Deloire MS, Brochet B, Ehrlé N, Charré-Morin J, Saubusse A, et al. Validation of the French version of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Multiple Scler Relat Disorders. 2021;48:102692.CrossRef Maubeuge N, Deloire MS, Brochet B, Ehrlé N, Charré-Morin J, Saubusse A, et al. Validation of the French version of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Multiple Scler Relat Disorders. 2021;48:102692.CrossRef
37.
go back to reference Dusankova JB, Kalincik T, Havrdova E, Benedict RH. Cross cultural validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). Clin Neuropsychol. 2012;26(7):1186–200.PubMedCrossRef Dusankova JB, Kalincik T, Havrdova E, Benedict RH. Cross cultural validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). Clin Neuropsychol. 2012;26(7):1186–200.PubMedCrossRef
38.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group* t. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.PubMedCrossRef Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group* t. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.PubMedCrossRef
39.
go back to reference Hong QN, Fàbregues S, Bartlett G, Boardman F, Cargo M, Dagenais P, et al. The mixed methods Appraisal Tool (MMAT) version 2018 for information professionals and researchers. Educ Inform. 2018;34(4):285–91.CrossRef Hong QN, Fàbregues S, Bartlett G, Boardman F, Cargo M, Dagenais P, et al. The mixed methods Appraisal Tool (MMAT) version 2018 for information professionals and researchers. Educ Inform. 2018;34(4):285–91.CrossRef
40.
go back to reference Argento O, Incerti CC, Quartuccio ME, Magistrale G, Francia A, Caltagirone C, et al. The Italian validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the application of the cognitive impairment index scoring procedure in MS patients. Neurol Sci. 2018;39(7):1237–44.PubMedCrossRef Argento O, Incerti CC, Quartuccio ME, Magistrale G, Francia A, Caltagirone C, et al. The Italian validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the application of the cognitive impairment index scoring procedure in MS patients. Neurol Sci. 2018;39(7):1237–44.PubMedCrossRef
41.
go back to reference Berard JA, Walker LAS. Validity and sensitivity of Canadian normative data for the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) battery. Mult Scler Relat Disord. 2022;63:103865.PubMedCrossRef Berard JA, Walker LAS. Validity and sensitivity of Canadian normative data for the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) battery. Mult Scler Relat Disord. 2022;63:103865.PubMedCrossRef
42.
go back to reference Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR, et al. Validity and reliability of a persian translation of the Minimal Assessment of cognitive function in multiple sclerosis (MACFIMS). Clin Neuropsychol. 2012;26(6):975–84.PubMedCrossRef Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR, et al. Validity and reliability of a persian translation of the Minimal Assessment of cognitive function in multiple sclerosis (MACFIMS). Clin Neuropsychol. 2012;26(6):975–84.PubMedCrossRef
43.
go back to reference Maubeuge N, Deloire MSA, Brochet B, Ehrlé N, Charré-Morin J, Saubusse A, et al. Validation of the French version of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Mult Scler Relat Disord. 2021;48:102692.PubMedCrossRef Maubeuge N, Deloire MSA, Brochet B, Ehrlé N, Charré-Morin J, Saubusse A, et al. Validation of the French version of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Mult Scler Relat Disord. 2021;48:102692.PubMedCrossRef
44.
go back to reference Migliore S, Ghazaryan A, Simonelli I, Pasqualetti P, Landi D, Palmieri MG, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) in the Italian population. Neurol Sci. 2016;37(8):1261–70.PubMedCrossRef Migliore S, Ghazaryan A, Simonelli I, Pasqualetti P, Landi D, Palmieri MG, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) in the Italian population. Neurol Sci. 2016;37(8):1261–70.PubMedCrossRef
45.
go back to reference Migliore S, Ghazaryan A, Simonelli I, Pasqualetti P, Squitieri F, Curcio G, et al. Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behav Neurol. 2017;2017:7404289.PubMedPubMedCentralCrossRef Migliore S, Ghazaryan A, Simonelli I, Pasqualetti P, Squitieri F, Curcio G, et al. Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behav Neurol. 2017;2017:7404289.PubMedPubMedCentralCrossRef
46.
go back to reference McGinley MP, Goldschmidt CH, Rae-Grant AD. Diagnosis and treatment of multiple sclerosis: a review. JAMA. 2021;325(8):765–79.PubMedCrossRef McGinley MP, Goldschmidt CH, Rae-Grant AD. Diagnosis and treatment of multiple sclerosis: a review. JAMA. 2021;325(8):765–79.PubMedCrossRef
47.
go back to reference Johnen A, Landmeyer NC, Bürkner P-C, Wiendl H, Meuth SG, Holling H. Distinct cognitive impairments in different disease courses of multiple sclerosis—A systematic review and meta-analysis. Neurosci Biobehavioral Reviews. 2017;83:568–78.CrossRef Johnen A, Landmeyer NC, Bürkner P-C, Wiendl H, Meuth SG, Holling H. Distinct cognitive impairments in different disease courses of multiple sclerosis—A systematic review and meta-analysis. Neurosci Biobehavioral Reviews. 2017;83:568–78.CrossRef
48.
go back to reference Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R, et al. Validity of the Symbol Digit modalities Test as a cognition performance outcome measure for multiple sclerosis. Multiple Scler J. 2017;23(5):721–33.CrossRef Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R, et al. Validity of the Symbol Digit modalities Test as a cognition performance outcome measure for multiple sclerosis. Multiple Scler J. 2017;23(5):721–33.CrossRef
49.
go back to reference Grothe M, Jochem K, Strauss S, Langner S, Kirsch M, Hoffeld K, et al. Performance in information processing speed is associated with parietal white matter tract integrity in multiple sclerosis. Front Neurol. 2022;13:982964.PubMedPubMedCentralCrossRef Grothe M, Jochem K, Strauss S, Langner S, Kirsch M, Hoffeld K, et al. Performance in information processing speed is associated with parietal white matter tract integrity in multiple sclerosis. Front Neurol. 2022;13:982964.PubMedPubMedCentralCrossRef
50.
go back to reference Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict R. 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 Scler J. 2009;15(9):1077–84.CrossRef Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict R. 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 Scler J. 2009;15(9):1077–84.CrossRef
51.
go back to reference Rocca MA, Amato MP, De Stefano N, Enzinger C, Geurts JJ, Penner I-K, et al. Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol. 2015;14(3):302–17.PubMedCrossRef Rocca MA, Amato MP, De Stefano N, Enzinger C, Geurts JJ, Penner I-K, et al. Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol. 2015;14(3):302–17.PubMedCrossRef
52.
go back to reference Goverover Y, Chiaravalloti ND, O’Brien AR, DeLuca J. Evidenced-based cognitive rehabilitation for persons with multiple sclerosis: an updated review of the literature from 2007 to 2016. Arch Phys Med Rehabil. 2018;99(2):390–407.PubMedCrossRef Goverover Y, Chiaravalloti ND, O’Brien AR, DeLuca J. Evidenced-based cognitive rehabilitation for persons with multiple sclerosis: an updated review of the literature from 2007 to 2016. Arch Phys Med Rehabil. 2018;99(2):390–407.PubMedCrossRef
53.
go back to reference Chiaravalloti ND, Moore NB, Weber E, DeLuca J. The application of strategy-based Training to enhance memory (STEM) in multiple sclerosis: a pilot RCT. Neuropsychological Rehabilitation. 2021;31(2):231–54.PubMedCrossRef Chiaravalloti ND, Moore NB, Weber E, DeLuca J. The application of strategy-based Training to enhance memory (STEM) in multiple sclerosis: a pilot RCT. Neuropsychological Rehabilitation. 2021;31(2):231–54.PubMedCrossRef
54.
go back to reference Mousavi S, Zare H, Etemadifar M. Evaluating the effectiveness of cognitive rehabilitation on everyday memory in multiple sclerosis patients. Neuropsychological Rehabilitation. 2018. Mousavi S, Zare H, Etemadifar M. Evaluating the effectiveness of cognitive rehabilitation on everyday memory in multiple sclerosis patients. Neuropsychological Rehabilitation. 2018.
55.
go back to reference Ruet A, Brochet B. Cognitive assessment in patients with multiple sclerosis: from neuropsychological batteries to ecological tools. Annals Phys Rehabilitation Med. 2020;63(2):154–8.CrossRef Ruet A, Brochet B. Cognitive assessment in patients with multiple sclerosis: from neuropsychological batteries to ecological tools. Annals Phys Rehabilitation Med. 2020;63(2):154–8.CrossRef
56.
go back to reference Glukhovsky L, Brandstadter R, Leavitt VM, Krieger S, Buyukturkoglu K, Fabian M, et al. Hippocampal volume is more related to patient-reported memory than objective memory performance in early multiple sclerosis. Multiple Scler J. 2021;27(4):568–78.CrossRef Glukhovsky L, Brandstadter R, Leavitt VM, Krieger S, Buyukturkoglu K, Fabian M, et al. Hippocampal volume is more related to patient-reported memory than objective memory performance in early multiple sclerosis. Multiple Scler J. 2021;27(4):568–78.CrossRef
57.
go back to reference van Dam M, Krijnen EA, Nauta IM, Fuchs TA, de Jong BA, Klein M et al. Identifying and understanding cognitive profiles in multiple sclerosis: a role for visuospatial memory functioning. J Neurol. 2024:1–12. van Dam M, Krijnen EA, Nauta IM, Fuchs TA, de Jong BA, Klein M et al. Identifying and understanding cognitive profiles in multiple sclerosis: a role for visuospatial memory functioning. J Neurol. 2024:1–12.
58.
go back to reference Sumowski JF, Rocca MA, Leavitt VM, Riccitelli G, Comi G, DeLuca J, et al. Brain reserve and cognitive reserve in multiple sclerosis: what you’ve got and how you use it. Neurology. 2013;80(24):2186–93.PubMedPubMedCentralCrossRef Sumowski JF, Rocca MA, Leavitt VM, Riccitelli G, Comi G, DeLuca J, et al. Brain reserve and cognitive reserve in multiple sclerosis: what you’ve got and how you use it. Neurology. 2013;80(24):2186–93.PubMedPubMedCentralCrossRef
59.
go back to reference Chen MH, Chiaravalloti ND, DeLuca J. Neurological update: cognitive rehabilitation in multiple sclerosis. J Neurol. 2021;268(12):4908–14.PubMedCrossRef Chen MH, Chiaravalloti ND, DeLuca J. Neurological update: cognitive rehabilitation in multiple sclerosis. J Neurol. 2021;268(12):4908–14.PubMedCrossRef
60.
go back to reference Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R. Validity of the Symbol Digit modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult Scler. 2017;23(5):721–33.PubMedPubMedCentralCrossRef Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R. Validity of the Symbol Digit modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult Scler. 2017;23(5):721–33.PubMedPubMedCentralCrossRef
61.
go back to reference Calocer F, Ng HS, Zhu F, Zhao Y, Dejardin O, Leray E, et al. Low socioeconomic status was associated with a higher mortality risk in multiple sclerosis. Multiple Scler J. 2023;29(3):466–70.CrossRef Calocer F, Ng HS, Zhu F, Zhao Y, Dejardin O, Leray E, et al. Low socioeconomic status was associated with a higher mortality risk in multiple sclerosis. Multiple Scler J. 2023;29(3):466–70.CrossRef
62.
go back to reference Towfighi A, Berger RP, Corley AM, Glymour MM, Manly JJ, Skolarus LE. Recommendations on social determinants of health in neurologic disease. Neurology. 2023;101(7Supplement1):S17–26.PubMed Towfighi A, Berger RP, Corley AM, Glymour MM, Manly JJ, Skolarus LE. Recommendations on social determinants of health in neurologic disease. Neurology. 2023;101(7Supplement1):S17–26.PubMed
Metadata
Title
Comparing cognitive impairment using MACFIMS in patients with multiple sclerosis and healthy controls: a systematic review and meta-analysis
Authors
Amirreza Nasirzadeh
Mohammad Mohammadi
Melika Arab Bafrani
Aynaz Mohammadi
Hossein Bakhtiari-Dovvombaygi
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2024
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-024-03943-2