Abstract
The aim of this consensus paper was to define the state of the art on cognitive assessment of persons with multiple sclerosis (PwMS), with the purpose of providing recommendations for the Italian centers involved in MS management. While there are no formal guidelines published regarding the assessment of cognitive function in MS, on the basis of an expert opinion meeting, held in Milan (Italy) on July 4, 2016, we report the recommendations of a panel of Italian experts including MS neurologists and neuropsychologists for the assessment and follow-up of cognitive function in adult MS subjects.
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21 March 2019
In the original article, Maria Pia Amato���s second affiliation was not included. The second affiliation is IRCCS Fondazione Don Carlo Gnocchi, Florence, Italy. The correct affiliation is presented here.
21 March 2019
In the original article, Maria Pia Amato���s second affiliation was not included. The second affiliation is IRCCS Fondazione Don Carlo Gnocchi, Florence, Italy. The correct affiliation is presented here.
Notes
The Rao battery is not comparable with the BICAMS. If at baseline only the Rao battery was performed, then SDMT has to be used during the follow-up.
References
Cheng EM, Crandall CJ, Bever CT Jr, Giesser B, Haselkorn JK, Hays RD, Shekelle P, Vickrey BG (2010) Quality indicators for multiple sclerosis. Mult Scler 16(8):970–980. https://doi.org/10.1177/1352458510372394
Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7(12):1139–1151. https://doi.org/10.1016/S1474-4422(08)70259-X
Rocca MA, Amato MP, De Stefano N, Enzinger C, Geurts JJ, Penner IK, Rovira A, Sumowski JF, Valsasina P, Filippi M, MAGNIMS Study Group (2015) Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol 14(3):302–317. https://doi.org/10.1016/S1474-4422(14)70250-9
Patti F, Nicoletti A, Messina S, Bruno E, Fermo SL, Quattrocchi G, Chisari CG, Maimone D, Cilia S, Zappia M (2015) Prevalence and incidence of cognitive impairment in multiple sclerosis: a population-based survey in Catania, Sicily. J Neurol 262(4):923–930. https://doi.org/10.1007/s00415-015-7661-3
Rao SM, Leo GJ, Ellington L, Nauertz T, Bernardin L, Unverzagt F (1991) Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology 41(5):692–696
Langdon DW (2011) Cognition in multiple sclerosis. Curr Opin Neurol 24(3):244–249. https://doi.org/10.1097/WCO.0b013e328346a43b
Fischer M, Kunkel A, Bublak P, Faiss JH, Hoffmann F, Sailer M, Schwab M, Zettl UK, Köhler W (2014) How reliable is the classification of cognitive impairment across different criteria in early and late stages of multiple sclerosis? J Neurol Sci 343(1–2):91–99. https://doi.org/10.1016/j.jns.2014.05.042
Amato MP, Hakiki B, Goretti B, Rossi F, Stromillo ML, Giorgio A, Roscio M, Ghezzi A, Guidi L, Bartolozzi ML, Portaccio E, De Stefano N, Italian RIS/MS Study Group (2012) Association of MRI metrics and cognitive impairment in radiologically isolated syndromes. Neurology 78(5):309–314. https://doi.org/10.1212/WNL.0b013e31824528c9
Amato MP, Zipoli V, Goretti B, Portaccio E, De Caro MF, Ricchiuti L, Siracusa G, Masini M, Sorbi S, Trojano M (2006) Benign multiple sclerosis: cognitive, psychological and social aspects in a clinical cohort. J Neurol 253(8):1054–1059
Amato MP, Portaccio E, Stromillo ML, Goretti B, Zipoli V, Siracusa G, Battaglini M, Giorgio A, Bartolozzi ML, 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.0000324621.58447.00
Amato MP, Krupp LB, Charvet LE, Penner I, Till C (2016) Pediatric multiple sclerosis: cognition and mood. Neurology 87(9 Suppl 2):S82–S87. https://doi.org/10.1212/WNL.0000000000002883
Amato MP, Goretti B, Ghezzi A, Lori S, Zipoli V, Moiola L, Falautano M, De Caro MF, Viterbo R, Patti F, Vecchio R, Pozzilli C, Bianchi V, Roscio M, Martinelli V, Comi G, Portaccio E, Trojano M, Multiple Sclerosis Study Group of the Italian Neurological Society (2010) Cognitive and psychosocial features in childhood and juvenile MS: two-year follow-up. Neurology 75(13):1134–1140. https://doi.org/10.1212/WNL.0b013e3181f4d821
Amato MP, Goretti B, Ghezzi A, Hakiki B, Niccolai C, Lori S, Moiola L, Falautano M, Viterbo RG, Patti F, Cilia S, Pozzilli C, Bianchi V, Roscio M, Martinelli V, Comi G, Portaccio E, Trojano M, MS Study Group of the Italian Neurological Society (2014) Neuropsychological features in childhood and juvenile multiple sclerosis: five-year follow-up. Neurology 83(16):1432–1438. https://doi.org/10.1212/WNL.0000000000000885
Amato MP, Ponziani G, Pracucci G, Bracco L, Siracusa G, Amaducci L (1995) Cognitive impairment in early-onset multiple sclerosis. Pattern, predictors, and impact on everyday life in a 4-year follow-up. Arch Neurol 52(2):168–172
Amato MP, Ponziani G, Siracusa G, Sorbi S (2001) Cognitive dysfunction in early-onset multiple sclerosis: a reappraisal after 10 years. Arch Neurol 58(10):1602–1606
Amato MP, Zipoli V, Portaccio E (2006) Multiple sclerosis-related cognitive changes: a review of cross-sectional and longitudinal studies. J Neurol Sci 245(1–2):41–46
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 RG, Amato MP (2017) Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Mult Scler 23(9):1258–126
Rao SM, Cognitive Function Study Group of the National Multiple Sclerosis (1990) A manual for the brief repeatable battery of neuropsychological tests in multiple sclerosis. Medical College of Wisconsin, Milwaukee
Barbarotto R, Laiacona M, Frosio R, Vecchio M, Farinato A, Capitani E (1998) A normative study on visual reaction times and two Stroop colour-word tests. Ital J Neurol Sci 19:161–170
Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46(10):1121–1123
Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389
Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33(11):1444–1452
Amato MP, Portaccio E, Goretti B, Zipoli V, Ricchiuti L, De Caro MF, Patti F, Vecchio R, Sorbi S, Trojano M (2006) The Rao’s brief repeatable battery and Stroop test: normative values with age, education and gender corrections in an Italian population. Mult Scler 12(6):787–793
Zipoli V, Goretti B, Hakiki B, Siracusa G, Sorbi S, Portaccio E, Amato MP (2010) Cognitive impairment predicts conversion to multiple sclerosis in clinically isolated syndromes. Mult Scler 16(1):62–67. https://doi.org/10.1177/1352458509350311
Deloire M, Ruet A, Hamel D, Bonnet M, Brochet B (2010) Early cognitive impairment in multiple sclerosis predicts disability outcome several years later. Mult Scler 16(5):581–587. https://doi.org/10.1177/1352458510362819
Moccia M, Lanzillo R, Palladino R, Chang KC, Costabile T, Russo C, De Rosa A, Carotenuto A, Saccà F, Maniscalco GT, Brescia Morra V (2016) Cognitive impairment at diagnosis predicts 10-year multiple sclerosis progression. Mult Scler 22(5):659–667. https://doi.org/10.1177/1352458515599075
Rosti E, Hamalainen P, Koivisto K, Hokkanen L (2007) PASAT in detecting cognitive impairment in relapsing-remitting MS. Appl Neuropsychol 14(2):101–112
Fischer JS, Rudick RA, Cutter GR, Reingold SC (1999) The multiple sclerosis functional composite measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society clinical outcomes assessment task force. Mult Scler 5(4):244–250
Nagels G, D’hooghe MB, Kos D, Engelborghs S, De Deyn PP (2008) Within-session practice effect on paced auditory serial addition test in multiple sclerosis. Mult Scler 14(1):106–111
Sandry J, Paxton J, Sumowski JF (2016) General mathematical ability predicts PASAT performance in patients: implications for clinical interpretation and cognitive reserve. J Int Neuropsychol Soc 22(3):375–378. https://doi.org/10.1017/S1355617715001307
Goretti B, Viterbo RG, Portaccio E, Niccolai C, Hakiki B, Piscolla E, Iaffaldano P, Trojano M, Amato MP (2014) Anxiety state affects information processing speed in patients with multiple sclerosis. Neurol Sci 35(4):559–563. https://doi.org/10.1007/s10072-013-1544-0
Smith A (1982) Symbol digit modalities test (SDMT) manual (revised). Western Psychological Services, Los Angeles
Langdon DW, Amato MP, Boringa J, Brochet B, Foley F, Fredrikson S, Hämäläinen P, Hartung HP, Krupp L, Penner IK, Reder AT, Benedict RH (2012) Recommendations for a brief international cognitive assessment for multiple sclerosis (BICAMS). Mult Scler 18(6):891–898. https://doi.org/10.1177/1352458511431076
Parmenter BA, Weinstock-Guttman B, Garg N, Munschauer F, Benedict RH (2007) Screening for cognitive impairment in multiple sclerosis using the symbol digit modalities test. Mult Scler 13(1):52–57
Drake AS, Weinstock-Guttman B, Morrow SA, Hojnacki D, Munschauer FE, Benedict RH (2010) Psychometrics and normative data for the multiple sclerosis functional composite: replacing the PASAT with the symbol digit modalities test. Mult Scler 16(2):228–237. https://doi.org/10.1177/1352458509354552
Benedict RH, Duquin JA, Jurgensen S, Rudick RA, Feitcher J, Munschauer FE, Panzara MA, Weinstock-Guttman B (2008) Repeated assessment of neuropsychological deficits in multiple sclerosis using the symbol digit modalities test and the MS neuropsychological screening questionnaire. Mult Scler 14(7):940–946. https://doi.org/10.1177/1352458508090923
Lopez-Gongora M, Querol L, Escartin A (2015) 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 15:40. https://doi.org/10.1186/s12883-015-0296-2
Rudick RA, Miller D, Bethoux F, Rao SM, Lee JC, Stough D, Reece C, Schindler D, Mamone B, Alberts J (2014) The multiple sclerosis performance test (MSPT): an iPad-based disability assessment tool. J Vis Exp 88:e51318. https://doi.org/10.3791/51318
Pardini M, Uccelli A, Grafman J, Yaldizli Ö, Mancardi G, Roccatagliata L (2014) Isolated cognitive relapses in multiple sclerosis. J Neurol Neurosurg Psychiatry 85(9):1035–1037. https://doi.org/10.1136/jnnp-2013-307275
Dagenais E, Rouleau I, Demers M, Jobin C, Roger E, Chamelian L, Duquette P (2013) Value of the MoCA test as a screening instrument in multiple sclerosis. Can J Neurol Sci 40(3):410–415
Benedict RH, Munschauer F, Linn R, Miller C, Murphy E, Foley F, Jacobs L (2003) Screening for multiple sclerosis cognitive impairment using a self-administered 15-item questionnaire. Mult Scler 9(1):95–101
Benedict RH, Cox D, Thompson LL, Foley F, Weinstock-Guttman B, Munschauer F (2004) Reliable screening for neuropsychological impairment in multiple sclerosis. Mult Scler 10(6):675–678
Goretti B, Patti F, Cilia S, Mattioli F, Stampatori C, Scarpazza C, Amato MP, Portaccio E (2014) The Rao’s brief repeatable battery version B: normative values with age, education and gender corrections in an Italian population. Neurol Sci 35(1):79–82. https://doi.org/10.1007/s10072-013-1558-7
Delis DC, Kaplan E, Kramer JH (2001) Delis–Kaplan executive function system. The Psychological Corporation, San Antonio
Mattioli F, Stampatori C, Bellomi F, Scarpazza C, Galli P, Guarneri C, Corso B, Montomoli C, Niccolai C, Goretti B, Amato MP, Riboni E, Tomasina CD, Falautano M, Capra R (2014) Assessing executive functi with the D-KEFS sorting test: normative data for a sample of the Italian adult population. Neurol Sci 35(12):1895–1902. https://doi.org/10.1007/s10072-014-1857-7
Benedict RH, Fischer JS, Archibald CJ, Arnett PA, Beatty WW, Bobholz J, Chelune GJ, Fisk JD, Langdon DW, Caruso L, Foley F, LaRocca NG, Vowels L, Weinstein A, DeLuca J, Rao SM, Munschauer F (2002) Minimal neuropsychological assessment of MS patients: a consensus approach. Clin Neuropsychol 16(3):381–397
Migliore S, Ghazaryan A, Simonelli I, Pasqualetti P, Landi D, Palmieri MG, Moffa F, Rinaldi P, Vernieri F, Filippi MM (2016) Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) in the Italian population. Neurol Sci 37(8):1261–1270. https://doi.org/10.1007/s10072-016-2578-x
Erlanger DM, Kaushik T, Caruso LS, Benedict RH, Foley FW, Wilken J, Cadavid D, Deluca J (2014) Reliability of a cognitive endpoint for use in a multiple sclerosis pharmaceutical trial. J Neurol Sci 340(1–2):123–129. https://doi.org/10.1016/j.jns.2014.03.009
Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California verbal learning test, second edition (CVLT-II). Psychological Corporation, San Antonio
Benedict RHB (1997) The brief visuospatial memory test revised (BVMT-R). Psychosocial Assessment Resources Inc, Lutz
Benedict RH, Amato MP, Boringa J, Brochet B, Foley F, Fredrikson S, Hamalainen P, Hartung H, Krupp L, Penner I, Reder AT, Langdon D (2012) Brief international cognitive assessment for MS (BICAMS): international standards for validation. BMC Neurol 12:55. https://doi.org/10.1186/1471-2377-12-55
Goretti B, Niccolai C, Hakiki B, Sturchio A, Falautano M, Minacapelli E, Martinelli V, Incerti C, Nocentini U, Murgia M, Fenu G, Cocco E, Marrosu MG, Garofalo E, Ambra FI, Maddestra M, Consalvo M, Viterbo RG, Trojano M, Losignore NA, Zimatore GB, Pietrolongo E, Lugaresi A, Langdon D, Portaccio E, Amato MP (2014) The brief international cognitive assessment for multiple sclerosis (BICAMS): normative values with gender, age and education corrections in the Italian population. BMC Neurol 14:171. https://doi.org/10.1186/s12883-014-0171-6
Saccà F, Costabile T, Carotenuto A, Lanzillo R, Moccia M, Pane C, Russo CV, Barbarulo AM, Casertano S, Rossi F, Signoriello E, Lus G, Brescia Morra V (2017) The EDSS integration with the Brief International Cognitive Assessment for Multiple Sclerosis and orientation tests. Mult Scler 23(9):1289–1296
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 MG, Garofalo E, Ambra FI, Maddestra M, Consalvo M, Viterbo RG, Trojano M, Losignore NA, Zimatore GB, Pietrolongo E, Lugaresi A, Pippolo L, Roscio M, Ghezzi A, Castellano D, Stecchi S, Amato MP (2015) A comparison of the brief international cognitive assessment for multiple sclerosis and the brief repeatable battery in multiple sclerosis patients. BMC Neurol 15:204. https://doi.org/10.1186/s12883-015-0460-8
Stern Y (2009) Cognitive reserve. Neuropsychologia 47(10):2015–2028. https://doi.org/10.1016/j.neuropsychologia.2009.03.004
Sumowski JF, Chiaravalloti N, DeLuca J (2009) Cognitive reserve protects against cognitive dysfunction in multiple sclerosis. J Clin Exp Neuropsychol 31(8):913–926. https://doi.org/10.1080/13803390902740643
Amato MP, Razzolini L, Goretti B, Stromillo ML, Rossi F, Giorgio A, Hakiki B, Giannini M, Pastò L, Portaccio E, De Stefano N (2013) Cognitive reserve and cortical atrophy in multiple sclerosis: a longitudinal study. Neurology 80(19):1728–1733. https://doi.org/10.1212/WNL.0b013e3182918c6f
Nucci M, Mapelli D, Mondini S (2012) Cognitive reserve questionnaire (CRIq): a new instrument for measuring the cognitive reserve. Aging Clin Exp Res 24(3):218–226. https://doi.org/10.3275/7800
Colombo L, Sartori G, Brivio C (2002) Stima del quoziente intellettivo tramite l’applicazione del TIB (Test Breve di Intelligenza). Giornale Italiano di Psicologia XXIX(3 settembre):613–637
Bright P, Hale E, Gooch VJ, Myhill T, van der Linde I (2016) The National Adult Reading Test: restandardisation against the Wechsler adult intelligence scale-fourth edition. Neuropsychol Rehabil 14:1–9. https://doi.org/10.1080/09602011.2016.1231121
International Federation of Multiple Sclerosis Societies. Minimal Record of Disability—1983 (1984) Acta Neurol Scand Suppl 101:169–190
Ontaneda D, Cohen JA, Amato MP (2017) Clinical outcome measures for progressive MS trials. Mult Scler 23(12):1627–1635
Morrow SA, Drake A, Zivadinov R, Munschauer F, Weinstock-Guttman B, Benedict RH (2010) Predicting loss of employment over three years in multiple sclerosis: clinically meaningful cognitive decline. Clin Neuropsychol 24(7):1131–1145. https://doi.org/10.1080/13854046.2010.511272
Amato MP, Langdon D, Montalban X, Benedict RH, DeLuca J, Krupp LB, Thompson AJ, Comi G (2013) Treatment of cognitive impairment in multiple sclerosis: position paper. J Neurol 260(6):1452–1468. https://doi.org/10.1007/s00415-012-6678-0
Rao SM, Leo GJ, Bernardin L, Unverzagt F (1991) Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology 41(5):685–691
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This work was supported by Biogen Italia S.r.l.
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Amato, M.P., Morra, V.B., Falautano, M. et al. Cognitive assessment in multiple sclerosis—an Italian consensus. Neurol Sci 39, 1317–1324 (2018). https://doi.org/10.1007/s10072-018-3427-x
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DOI: https://doi.org/10.1007/s10072-018-3427-x