Recommendations for cognitive screening and management in multiple sclerosis care

Rosalind Kalb, Meghan Beier, Ralph Hb Benedict, Leigh Charvet, Kathleen Costello, Anthony Feinstein, Jeffrey Gingold, Yael Goverover, June Halper, Colleen Harris, Lori Kostich, Lauren Krupp, Ellen Lathi, Nicholas LaRocca, Ben Thrower, John DeLuca, Rosalind Kalb, Meghan Beier, Ralph Hb Benedict, Leigh Charvet, Kathleen Costello, Anthony Feinstein, Jeffrey Gingold, Yael Goverover, June Halper, Colleen Harris, Lori Kostich, Lauren Krupp, Ellen Lathi, Nicholas LaRocca, Ben Thrower, John DeLuca

Abstract

Purpose: To promote understanding of cognitive impairment in multiple sclerosis (MS), recommend optimal screening, monitoring, and treatment strategies, and address barriers to optimal management.

Methods: The National MS Society ("Society") convened experts in cognitive dysfunction (clinicians, researchers, and lay people with MS) to review the published literature, reach consensus on optimal strategies for screening, monitoring, and treating cognitive changes, and propose strategies to address barriers to optimal care.

Recommendations: Based on current evidence, the Society makes the following recommendations, endorsed by the Consortium of Multiple Sclerosis Centers and the International Multiple Sclerosis Cognition Society: Increased professional and patient awareness/education about the prevalence, impact, and appropriate management of cognitive symptoms. For adults and children (8+ years of age) with clinical or magnetic resonance imaging (MRI) evidence of neurologic damage consistent with MS: As a minimum, early baseline screening with the Symbol Digit Modalities Test (SDMT) or similarly validated test, when the patient is clinically stable; Annual re-assessment with the same instrument, or more often as needed to (1) detect acute disease activity; (2) assess for treatment effects (e.g. starting/changing a disease-modifying therapy) or for relapse recovery; (3) evaluate progression of cognitive impairment; and/or (4) screen for new-onset cognitive problems. For adults (18+ years): more comprehensive assessment for anyone who tests positive on initial cognitive screening or demonstrates significant cognitive decline, especially if there are concerns about comorbidities or the individual is applying for disability due to cognitive impairment. For children (<18 years): neuropsychological evaluation for any unexplained change in school functioning (academic or behavioral). Remedial interventions/accommodations for adults and children to improve functioning at home, work, or school.

Keywords: Multiple sclerosis; cognition; cognitive dysfunction; rehabilitation; remediation; screening; treatment.

Conflict of interest statement

Declaration of Conflicting Interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

    1. Foley FW, Benedict RHB, Gromisch ES, et al. The Need for screening, assessment, and treatment for cognitive dysfunction in multiple sclerosis: Results of a multidisciplinary CMSC consensus conference, September 24, 2010. Int J MS Care 2012; 14: 58–64.
    1. Benedict RH, DeLuca J, Phillips G, et al. Validity of the Symbol Digit Modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult Scler 2017; 23: 721–733.
    1. Benedict R, Fishman I, McClellan M, et al. Validity of the Beck Depression Inventory–Fast Screen in multiple sclerosis. Mult Scler 2003; 9: 393–396.
    1. Honarmand K, Feinstein A. Validation of the Hospital Anxiety and Depression Scale for use with multiple sclerosis patients. Mult Scler 2009; 15: 1518–1524.
    1. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol 2008; 7: 1139–1151.
    1. Zhang X, Zhang F, Huang D, et al. Contribution of gray and white matter abnormalities to cognitive impairment in multiple sclerosis. Int J Mol Sci 2017; 18: 46.
    1. Trapp BD, Ransohoff R, Rudick R. Axonal pathology in multiple sclerosis: Relationship to neurologic disability. Curr Opin Neurol 1999; 12: 295–302.
    1. Achiron A, Chapman J, Magalashvili D, et al. Modeling of cognitive impairment by disease duration in multiple sclerosis: A cross-sectional study. PLoS ONE 2013; 8: e71058.
    1. Olazarán J, Cruz I, Benito-León J, et al. Cognitive dysfunction in multiple sclerosis: Methods and prevalence from the GEDMA study. Eur Neurol 2009; 61: 87–93.
    1. Rao SM, Leo GJ, Bernardin L, et al. Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology 1991; 41: 685–691.
    1. Amato MP, Krupp LB, Charvet LE, et al. Pediatric multiple sclerosis: Cognition and mood. Neurology 2016; 87: S82–S87.
    1. Julian L, Serafin D, Charvet L, et al. Cognitive impairment occurs in children and adolescents with multiple sclerosis: Results from a United States network. J Child Neurol 2013; 28: 102–107.
    1. Johnen A, Landmeyer NC, Bürkner P-C, et al. Distinct cognitive impairments in different disease courses of multiple sclerosis—A systematic review and meta-analysis. Neurosci Biobehav Rev 2017; 83: 568–578.
    1. Gouveia A, Dias SP, Santos T, et al. Cognitive impairment and magnetic resonance imaging correlates in primary progressive multiple sclerosis. Acta Neurol Scand 2017; 136: 109–115.
    1. Ruano L, Portaccio E, Goretti B, et al. Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Mult Scler 2017; 23: 1258–1267.
    1. Hynčicová E, Vyhnálek M, Kalina A, et al. Cognitive impairment and structural brain changes in patients with clinically isolated syndrome at high risk for multiple sclerosis. J Neurol 2017; 264: 482–493.
    1. Diker S, Has AC, Kurne A, et al. The association of cognitive impairment with gray matter atrophy and cortical lesion load in clinically isolated syndrome. Mult Scler Relat Disord 2016; 10: 14–21.
    1. Labiano-Fontcuberta A, Martínez-Ginés ML, Aladro Y, et al. A comparison study of cognitive deficits in radiologically and clinically isolated syndromes. Mult Scler 2016; 22: 250–253.
    1. Glanz BI, Holland CM, Gauthier SA, et al. Cognitive dysfunction in patients with clinically isolated syndromes or newly diagnosed multiple sclerosis. Mult Scler 2007; 13: 1004–1010.
    1. Cortese M, Riise T, Bjørnevik K, et al. Preclinical disease activity in multiple sclerosis: A prospective study of cognitive performance prior to first symptom. Ann Neurol 2016; 80: 616–624.
    1. Amato MP, Razzolini L, Goretti B, et al. Cognitive reserve and cortical atrophy in multiple sclerosis: A longitudinal study. Neurology 2013; 80: 1728–1733.
    1. Amato MP, Ponziani G, Siracusa G, et al. Cognitive dysfunction in early-onset multiple sclerosis: A reappraisal after 10 years. Arch Neurol 2001; 58: 1602–1606.
    1. Lacy M, Hauser M, Pliskin N, et al. The effects of long-term interferon-beta-1b treatment on cognitive functioning in multiple sclerosis: A 16-year longitudinal study. Mult Scler 2013; 19: 1765–1772.
    1. Bergendal G, Fredrikson S, Almkvist O. Selective decline in information processing in subgroups of multiple sclerosis: An 8-year longitudinal study. Eur Neurol 2007; 57: 193–202.
    1. Amato MP, Portaccio E, Goretti B, et al. Relevance of cognitive deterioration in early relapsing-remitting MS: A 3-year follow-up study. Mult Scler 2010; 16: 1474–1482.
    1. Amato MP, Goretti B, Ghezzi A, et al. Neuropsychological features in childhood and juvenile multiple sclerosis: Five-year follow-up. Neurology 2014; 83: 1432–1438.
    1. Deloire MSA, Ruet A, Hamel D, et al. MRI predictors of cognitive outcome in early multiple sclerosis. Neurology 2011; 76: 1161–1167.
    1. Benedict RHB, Fischer JS, Archibald CJ, et al. Minimal neuropsychological assessment of MS patients: A consensus approach. Clin Neuropsychol 2002; 16: 381–397.
    1. Carotenuto A. Look beyond the door, not through the keyhole: Evidence from a cognitive assessment including social cognition evaluation in multiple sclerosis. Eur J Neurol 2018; 25: 205–206.
    1. Cotter J, Firth J, Enzinger C, et al. Social cognition in multiple sclerosis: A systematic review and meta-analysis. Neurology 2016; 87: 1727–1736.
    1. Denney DR, Lynch SG, Parmenter BA. A 3-year longitudinal study of cognitive impairment in patients with primary progressive multiple sclerosis: Speed matters. J Neurol Sci 2008; 267: 129–136.
    1. Van Schependom J, D’hooghe MB, Cleynhens K, et al. Reduced information processing speed as primum movens for cognitive decline in MS. Mult Scler 2015; 21: 83–91.
    1. Chiaravalloti ND, Moore NB, Nikelshpur OM, et al. An RCT to treat learning impairment in multiple sclerosis: The MEMREHAB trial. Neurology 2013; 81: 2066–2072.
    1. Genova HM, DeLuca J, Chiaravalloti N, et al. The relationship between executive functioning, processing speed, and white matter integrity in multiple sclerosis. J Clin Exp Neuropsychol 2013; 35: 631–641.
    1. Goverover Y, Strober L, Chiaravalloti N, et al. Factors that moderate activity limitation and participation restriction in people with multiple sclerosis. Am J Occup Ther 2015; 69: 6902260020.
    1. Cattaneo D, Lamers I, Bertoni R, et al. Participation restriction in people with multiple sclerosis: Prevalence and correlations with cognitive, walking, balance, and upper limb impairments. Arch Phys Med Rehabil 2017; 98: 1308–1315.
    1. Kavaliunas A, Danylaite Karrenbauer V, Gyllensten H, et al. Cognitive function is a major determinant of income among multiple sclerosis patients in Sweden acting independently from physical disability. Mult Scler. Epub ahead of print 1 November 2017. DOI: 10.1177/1352458517740212.
    1. Morrow SA, Classen S, Monahan M, et al. On-road assessment of fitness-to-drive in persons with MS with cognitive impairment: A prospective study. Mult Scler 2018; 24: 1499–1506.
    1. Rao SM, Leo GJ, Ellington L, et al. Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology 1991; 41: 692–696.
    1. Ruet A, Deloire M, Hamel D, et al. Cognitive impairment, health-related quality of life and vocational status at early stages of multiple sclerosis: A 7-year longitudinal study. J Neurol 2013; 260: 776–784.
    1. Papathanasiou A, Messinis L, Zampakis P, et al. Corpus callosum atrophy as a marker of clinically meaningful cognitive decline in secondary progressive multiple sclerosis. Impact on employment status. J Clin Neurosci 2017; 43: 170–175.
    1. Campbell J, Rashid W, Cercignani M, et al. Cognitive impairment among patients with multiple sclerosis: Associations with employment and quality of life. Postgrad Med J 2017; 93: 143–147.
    1. Kordovski VM, Frndak SE, Fisher CS, et al. Identifying employed multiple sclerosis patients at-risk for job loss: When do negative work events pose a threat? Mult Scler Relat Disord 2015; 4: 409–413.
    1. Benedict RHB, Rodgers JD, Emmert N, et al. Negative work events and accommodations in employed multiple sclerosis patients. Mult Scler 2014; 20: 116–119.
    1. Goverover Y, Chiaravalloti N, DeLuca J. Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) and performance of everyday life tasks: Actual reality. Mult Scler 2016; 22: 544–550.
    1. Till C, Racine N, Araujo D, et al. Changes in cognitive performance over a 1-year period in children and adolescents with multiple sclerosis. Neuropsychology 2013; 27: 210–219.
    1. Charvet LE, O’Donnell EH, Belman AL, et al. Longitudinal evaluation of cognitive functioning in pediatric multiple sclerosis: Report from the US pediatric multiple sclerosis network. Mult Scler 2014; 20: 1502–1510.
    1. Mikaeloff Y, Caridade G, Billard C, et al. School performance in a cohort of children with CNS inflammatory demyelination. Eur J Paediatr Neurol 2010; 14: 418–424.
    1. Dehning M, Kim J, Nguyen CM, et al. Neuropsychological performance, brain imaging, and driving violations in multiple sclerosis. Arch Phys Med Rehabil 2014; 95: 1818–1823.
    1. Lamargue-Hamel D, Deloire M, Saubusse A, et al. Cognitive evaluation by tasks in a virtual reality environment in multiple sclerosis. J Neurol Sci 2015; 359: 94–99.
    1. Schultheis MT, Garay E, Millis SR, et al. Motor vehicle crashes and violations among drivers with multiple sclerosis. Arch Phys Med Rehabil 2002; 83: 1175–1178.
    1. Gerstenecker A, Lowry K, Myers T, et al. Medical decision-making capacity and its cognitive predictors in progressive MS: Preliminary evidence. J Neurol Sci 2017; 380: 38–43.
    1. Bruce JM, Hancock LM, Arnett P, et al. Treatment adherence in multiple sclerosis: Association with emotional status, personality, and cognition. J Behav Med 2010; 33: 219–227.
    1. Goverover Y, Haas S, DeLuca J. Money management activities in persons with multiple sclerosis. Arch Phys Med Rehabil 2016; 97: 1901–1907.
    1. Tracy VL, Basso MR, Marson DC, et al. Capacity for financial decision making in multiple sclerosis. J Clin Exp Neuropsychol 2017; 39: 46–57.
    1. Figved N, Myhr K-M, Larsen J-P, et al. Caregiver burden in multiple sclerosis: The impact of neuropsychiatric symptoms. J Neurol Neurosurg Psychiatry 2007; 78: 1097–1102.
    1. Labiano-Fontcuberta A, Mitchell AJ, Moreno-García S, et al. Anxiety and depressive symptoms in caregivers of multiple sclerosis patients: The role of information processing speed impairment. J Neurol Sci 2015; 349: 220–225.
    1. Thorpe LU, Knox K, Jalbert R, et al. Predictors of institutionalization for people with multiple sclerosis. Disabil Health J 2015; 8: 271–277.
    1. Romero K, Shammi P, Feinstein A. Neurologists’ accuracy in predicting cognitive impairment in multiple sclerosis. Mult Scler Relat Disord 2015; 4: 291–295.
    1. Beatty WW, Goodkin DE. Screening for cognitive impairment in multiple sclerosis. An evaluation of the Mini-Mental State Examination. Arch Neurol 1990; 47: 297–301.
    1. Peyser JM, Edwards KR, Poser CM, et al. Cognitive function in patients with multiple sclerosis. Arch Neurol 1980; 37: 577–579.
    1. Benedict RHB, Cookfair D, Gavett R, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 2006; 12: 549–558.
    1. Langdon DW, Amato MP, Boringa J, et al. Recommendations for a Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS). Mult Scler 2012; 18: 891–898.
    1. Roy S, Rodgers J, Drake AS, et al. Stable neuropsychiatric status in multiple sclerosis: A 3-year study. Mult Scler 2016; 22: 569–574.
    1. Conradsson D, Ytterberg C, von Koch L, et al. Changes in disability in people with multiple sclerosis: A 10-year prospective study. J Neurol 2018; 265: 119–126.
    1. López-Góngora M, Querol L, Escartín A. A one-year follow-up study of the Symbol Digit Modalities Test (SDMT) and the Paced Auditory Serial Addition Test (PASAT) in relapsing-remitting multiple sclerosis: An appraisal of comparative longitudinal sensitivity. BMC Neurol 2015; 15: 40.
    1. Niccolai C, Portaccio E, Goretti B, et al. A comparison of the brief international cognitive assessment for multiple sclerosis and the brief repeatable battery in multiple sclerosis patients. BMC Neurol 2015; 15: 204.
    1. Van Schependom J, D’hooghe MB, Cleynhens K, et al. The Symbol Digit Modalities Test as sentinel test for cognitive impairment in multiple sclerosis. Eur J Neurol 2014; 21: 1219–1225; e71–e72.
    1. Sonder JM, Burggraaff J, Knol DL, et al. Comparing long-term results of PASAT and SDMT scores in relation to neuropsychological testing in multiple sclerosis. Mult Scler 2014; 20: 481–488.
    1. Morrow SA, O’Connor PW, Polman CH, et al. Evaluation of the Symbol Digit Modalities Test (SDMT) and MS Neuropsychological Screening Questionnaire (MSNQ) in natalizumab-treated MS patients over 48 weeks. Mult Scler 2010; 16: 1385–1392.
    1. Parmenter BA, Weinstock-Guttman B, Garg N, et al. Screening for cognitive impairment in multiple sclerosis using the Symbol Digit Modalities Test. Mult Scler 2007; 13: 52–57.
    1. Bigi S, Marrie RA, Till C, et al. The computer-based Symbol Digit Modalities Test: Establishing age-expected performance in healthy controls and evaluation of pediatric MS patients. Neurol Sci 2017; 38: 635–642.
    1. Charvet LE, Beekman R, Amadiume N, et al. The Symbol Digit Modalities Test is an effective cognitive screen in pediatric onset multiple sclerosis (MS). J Neurol Sci 2014; 341: 79–84.
    1. Strober LB, Rao SM, Lee J-C, et al. Cognitive impairment in multiple sclerosis: An 18 year follow-up study. Mult Scler Relat Disord 2014; 3: 473–481.
    1. Morrow SA, Drake A, Zivadinov R, et al. Predicting loss of employment over three years in multiple sclerosis: Clinically meaningful cognitive decline. Clin Neuropsychol 2010; 24: 1131–1145.
    1. Pardini M, Uccelli A, Grafman J, et al. Isolated cognitive relapses in multiple sclerosis. J Neurol Neurosurg Psychiatry 2014; 85: 1035–1037.
    1. Morrow SA, Jurgensen S, Forrestal F, et al. Effects of acute relapses on neuropsychological status in multiple sclerosis patients. J Neurol 2011; 258: 1603–1608.
    1. Rao SM, Losinski G, Mourany L, et al. Processing speed test: Validation of a self-administered, iPad®-based tool for screening cognitive dysfunction in a clinic setting. Mult Scler 2017; 23: 1929–1937.
    1. Ruet A, Deloire MSA, Charré-Morin J, et al. A new computerised cognitive test for the detection of information processing speed impairment in multiple sclerosis. Mult Scler 2013; 19: 1665–1672.
    1. Benedict RHB, Cox D, Thompson LL, et al. Reliable screening for neuropsychological impairment in multiple sclerosis. Mult Scler 2004; 10: 675–678.
    1. Akbar N, Honarmand K, Feinstein A. Self-assessment of cognition in multiple sclerosis: The role of personality and anxiety. Cogn Behav Neurol 2011; 24: 115–121.
    1. O’Brien A, Gaudino-Goering E, Shawaryn M, et al. Relationship of the Multiple Sclerosis Neuropsychological Questionnaire (MSNQ) to functional, emotional, and neuropsychological outcomes. Arch Clin Neuropsychol 2007; 22: 933–948.
    1. Charvet LE, Shaw M, Frontario A, et al. Cognitive impairment in pediatric-onset multiple sclerosis is detected by the Brief International Cognitive Assessment for Multiple Sclerosis and computerized cognitive testing. Mult Scler 2017; 24: 512–519.
    1. Benedict RH, Morrow S, Rodgers J, et al. Characterizing cognitive function during relapse in multiple sclerosis. Mult Scler 2014; 20: 1745–1752.
    1. Wybrecht D, Reuter F, Pariollaud F, et al. New brain lesions with no impact on physical disability can impact cognition in early multiple sclerosis: A ten-year longitudinal study. PLoS ONE 2017; 12: e0184650.
    1. Deloire M, Ruet A, Hamel D, et al. Early cognitive impairment in multiple sclerosis predicts disability outcome several years later. Mult Scler 2010; 16: 581–587.
    1. Pitteri M, Romualdi C, Magliozzi R, et al. Cognitive impairment predicts disability progression and cortical thinning in MS: An 8-year study. Mult Scler 2017; 23: 848–854.
    1. Moccia M, Lanzillo R, Palladino R, et al. Cognitive impairment at diagnosis predicts 10-year multiple sclerosis progression. Mult Scler 2016; 22: 659–667.
    1. Patti F. Optimizing the benefit of multiple sclerosis therapy: The importance of treatment adherence. Patient Prefer Adherence 2010; 4: 1–9.
    1. Marin SE, Banwell BB, Till C. Cognitive trajectories in 4 patients with pediatric-onset multiple sclerosis: Serial evaluation over a decade. J Child Neurol 2013; 28: 1577–1586.
    1. Ruano L, Branco M, Portaccio E, et al. Patients with paediatric-onset multiple sclerosis are at higher risk of cognitive impairment in adulthood: An Italian collaborative study. Mult Scler 2018; 24: 1234–1242.
    1. Amato MP, Portaccio E, Stromillo ML, et al. Cognitive assessment and quantitative magnetic resonance metrics can help to identify benign multiple sclerosis. Neurology 2008; 71: 632–638.
    1. Amato MP, Zipoli V, Goretti B, et al. Benign multiple sclerosis: Cognitive, psychological and social aspects in a clinical cohort. J Neurol 2006; 253: 1054–1059.
    1. Gajofatto A, Turatti M, Bianchi MR, et al. Benign multiple sclerosis: Physical and cognitive impairment follow distinct evolutions. Acta Neurol Scand 2016; 133: 183–191.
    1. Damasceno A, Damasceno BP, Cendes F. No evidence of disease activity in multiple sclerosis: Implications on cognition and brain atrophy. Mult Scler 2016; 22: 64–72.
    1. Portaccio E, Stromillo ML, Goretti B, et al. Neuropsychological and MRI measures predict short-term evolution in benign multiple sclerosis. Neurology 2009; 73: 498–503.
    1. Correale J, Peirano I, Romano L. Benign multiple sclerosis: A new definition of this entity is needed. Mult Scler 2012; 18: 210–218.
    1. Modica CM, Bergsland N, Dwyer MG, et al. Cognitive reserve moderates the impact of subcortical gray matter atrophy on neuropsychological status in multiple sclerosis. Mult Scler 2016; 22: 36–42.
    1. Sandroff BM, Schwartz CE, DeLuca J. Measurement and maintenance of reserve in multiple sclerosis. J Neurol 2016; 263: 2158–2169.
    1. Feinstein A, Lapshin H, O’Connor P, et al. Sub-threshold cognitive impairment in multiple sclerosis: The association with cognitive reserve. J Neurol 2013; 260: 2256–2261.
    1. Benedict RHB, Morrow SA, Weinstock Guttman B, et al. Cognitive reserve moderates decline in information processing speed in multiple sclerosis patients. J Int Neuropsychol Soc 2010; 16: 829–835.
    1. Chiaravalloti ND, DeLuca J. The influence of cognitive dysfunction on benefit from learning and memory rehabilitation in MS: A sub-analysis of the MEMREHAB trial. Mult Scler 2015; 21: 1575–1582.
    1. Goverover Y, Chiaravalloti N, DeLuca J. The influence of executive functions and memory on self-generation benefit in persons with multiple sclerosis. J Clin Exp Neuropsychol 2013; 35: 775–783.
    1. Mohr DC, Hart SL, Julian L, et al. Screening for depression among patients with multiple sclerosis: Two questions may be enough. Mult Scler 2007; 13: 215–219.
    1. Arnett PA, Higginson CI, Randolph JJ. Depression in multiple sclerosis: Relationship to planning ability. J Int Neuropsychol Soc 2001; 7: 665–674.
    1. Arnett PA, Higginson CI, Voss WD, et al. Depression in multiple sclerosis: Relationship to working memory capacity. Neuropsychology 1999; 13: 546–556.
    1. Arnett PA, Higginson CI, Voss WD, et al. Depressed mood in multiple sclerosis: Relationship to capacity-demanding memory and attentional functioning. Neuropsychology 1999; 13: 434–446.
    1. Leavitt VM, Wylie G, Krch D, et al. Does slowed processing speed account for executive deficits in multiple sclerosis? Evidence from neuropsychological performance and structural neuroimaging. Rehabil Psychol 2014; 59: 422–428.
    1. National Multiple Sclerosis Society. Applying for social security disability benefits: A guidebook for people with MS and their healthcare providers, (2017, accessed 10 April 2018).
    1. Goverover Y, Chiaravalloti N, Genova H, et al. A randomized controlled trial to treat impaired learning and memory in multiple sclerosis: The self-GEN trial. Mult Scler 2018; 24: 1096–1104.
    1. Goverover Y, Chiaravalloti N, DeLuca J. Self-generation to improve learning and memory of functional activities in persons with multiple sclerosis: Meal preparation and managing finances. Arch Phys Med Rehabil 2008; 89: 1514–1521.
    1. Chiaravalloti ND, Deluca J. Self-generation as a means of maximizing learning in multiple sclerosis: An application of the generation effect. Arch Phys Med Rehabil 2002; 83: 1070–1079.
    1. Goverover Y, Chiaravalloti ND, Deluca J. Task meaningfulness and degree of cognitive impairment: Do they affect self-generated learning in persons with multiple sclerosis? Neuropsychol Rehabil 2014; 24: 155–171.
    1. Goverover Y, Basso M, Wood H, et al. Examining the benefits of combining two learning strategies on recall of functional information in persons with multiple sclerosis. Mult Scler 2011; 17: 1488–1497.
    1. Chiaravalloti ND, Wylie G, Leavitt V, et al. Increased cerebral activation after behavioral treatment for memory deficits in MS. J Neurol 2012; 259: 1337–1346.
    1. Sumowski JF, Chiaravalloti N, Deluca J. Retrieval practice improves memory in multiple sclerosis: Clinical application of the testing effect. Neuropsychology 2010; 24: 267–272.
    1. Bonavita S, Sacco R, Della Corte M, et al. Computer-aided cognitive rehabilitation improves cognitive performances and induces brain functional connectivity changes in relapsing remitting multiple sclerosis patients: An exploratory study. J Neurol 2015; 262: 91–100.
    1. Charvet LE, Yang J, Shaw MT, et al. Cognitive function in multiple sclerosis improves with telerehabilitation: Results from a randomized controlled trial. PLoS ONE 2017; 12: e0177177.
    1. Pusswald G, Mildner C, Zebenholzer K, et al. A neuropsychological rehabilitation program for patients with multiple sclerosis based on the model of the ICF. NeuroRehabilitation 2014; 35: 519–527.
    1. Parisi L, Rocca MA, Mattioli F, et al. Changes of brain resting state functional connectivity predict the persistence of cognitive rehabilitation effects in patients with multiple sclerosis. Mult Scler 2014; 20: 686–694.
    1. Sandroff BM, Motl RW, Deluca J. The influence of cognitive impairment on the fitness-cognition relationship in multiple sclerosis. Med Sci Sports Exerc 2017; 49: 1184–1189.
    1. Motl RW, Hubbard EA, Sreekumar N, et al. Pallidal and caudate volumes correlate with walking function in multiple sclerosis. J Neurol Sci 2015; 354: 33–36.
    1. Klaren RE, Hubbard EA, Motl RW, et al. Objectively measured physical activity is associated with brain volumetric measurements in multiple sclerosis. Behav Neurol 2015; 2015: 482536.
    1. Leavitt VM, Cirnigliaro C, Cohen A, et al. Aerobic exercise increases hippocampal volume and improves memory in multiple sclerosis: Preliminary findings. Neurocase 2014; 20: 695–697.
    1. Motl RW, Sandroff BM, DeLuca J. Exercise training and cognitive rehabilitation: A symbiotic approach for rehabilitating walking and cognitive functions in multiple sclerosis? Neurorehabil Neural Repair 2016; 30: 499–511.
    1. Geisler MW, Sliwinski M, Coyle PK, et al. The effects of amantadine and pemoline on cognitive functioning in multiple sclerosis. Arch Neurol 1996; 53: 185–188.
    1. Morrow SA, Rosehart H, Johnson AM. The effect of Fampridine-SR on cognitive fatigue in a randomized double-blind crossover trial in patients with MS. Mult Scler Relat Disord 2017; 11: 4–9.
    1. Sumowski JF, Chiaravalloti N, Erlanger D, et al. L-amphetamine improves memory in MS patients with objective memory impairment. Mult Scler 2011; 17: 1141–1145.
    1. Morrow SA, Kaushik T, Zarevics P, et al. The effects of L-amphetamine sulfate on cognition in MS patients: Results of a randomized controlled trial. J Neurol 2009; 256: 1095–1102.
    1. Morrow SA, Smerbeck A, Patrick K, et al. Lisdexamfetamine dimesylate improves processing speed and memory in cognitively impaired MS patients: A phase II study. J Neurol 2013; 260: 489–497.
    1. Peyro SaintPaul L, Creveuil C, Heinzlef O, et al. Efficacy and safety profile of memantine in patients with cognitive impairment in multiple sclerosis: A randomized, placebo-controlled study. J Neurol Sci 2016; 363: 69–76.
    1. Huolman S, Hämäläinen P, Vorobyev V, et al. The effects of rivastigmine on processing speed and brain activation in patients with multiple sclerosis and subjective cognitive fatigue. Mult Scler 2011; 17: 1351–1361.
    1. Shaygannejad V, Janghorbani M, Ashtari F, et al. Effects of rivastigmine on memory and cognition in multiple sclerosis. Can J Neurol Sci 2008; 35: 476–481.
    1. Krupp LB, Christodoulou C, Melville P, et al. Donepezil improved memory in multiple sclerosis in a randomized clinical trial. Neurology 2004; 63: 1579–1585.
    1. Krupp LB, Christodoulou C, Melville P, et al. Multicenter randomized clinical trial of donepezil for memory impairment in multiple sclerosis. Neurology 2011; 76: 1500–1507.
    1. Lovera JF, Kim E, Heriza E, et al. Ginkgo biloba does not improve cognitive function in MS: A randomized placebo-controlled trial. Neurology 2012; 79: 1278–1284.
    1. Goverover Y, Chiaravalloti ND, O’Brien AR, et al. 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: 390–407.
    1. Morrow SA, Rosehart H, Pantazopoulos K. Anxiety and depressive symptoms are associated with worse performance on objective cognitive tests in MS. J Neuropsychiatry Clin Neurosci 2016; 28: 118–123.
    1. Portaccio E. Differential diagnosis, discerning depression from cognition. Acta Neurol Scand 2016; 134(Suppl. 200): 14–18.
    1. Hughes AJ, Parmenter BA, Haselkorn JK, et al. Sleep and its associations with perceived and objective cognitive impairment in individuals with multiple sclerosis. J Sleep Res 2017; 26: 428–435.
    1. Patel VP, Walker LAS, Feinstein A. Processing speed and distractibility in multiple sclerosis: The role of sleep. Mult Scler Relat Disord 2017; 11: 40–42.
    1. Braley TJ, Kratz AL, Kaplish N, et al. Sleep and cognitive function in multiple sclerosis. Sleep 2016; 39: 1525–1533.
    1. Cruce R, Vosoughi R, Freedman MS. Cognitive impact of anticholinergic medication in MS: Adding insult to injury? Mult Scler Relat Disord 2012; 1: 156–161.
    1. Thelen JM, Lynch SG, Bruce AS, et al. Polypharmacy in multiple sclerosis: Relationship with fatigue, perceived cognition, and objective cognitive performance. J Psychosom Res 2014; 76: 400–404.
    1. Feinstein A, Banwell E, Pavisian B. What to make of cannabis and cognition in MS: In search of clarity amidst the haze. Mult Scler 2015; 21: 1755–1760.
    1. Pavisian B, Staines WR, Feinstein A. Cannabis-induced alterations in brain activation during a test of information processing speed in patients with MS. Mult Scler J Exp Transl Clin 2015; 1: 2055217315588223.
    1. Pavisian B, MacIntosh BJ, Szilagyi G, et al. Effects of cannabis on cognition in patients with MS: A psychometric and MRI study. Neurology 2014; 82: 1879–1887.
    1. Romero K, Pavisian B, Staines WR, et al. Multiple sclerosis, cannabis, and cognition: A structural MRI study. Neuroimage Clin 2015; 8: 140–147.
    1. Patel VP, Feinstein A. Cannabis and cognitive functioning in multiple sclerosis: The role of gender. Mult Scler J Exp Transl Clin 2017; 3: 205521731771302.

Source: PubMed

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