Advertisement

Neurological Sciences

, Volume 39, Issue 8, pp 1317–1324 | Cite as

Cognitive assessment in multiple sclerosis—an Italian consensus

  • Maria Pia AmatoEmail author
  • Vincenzo Brescia Morra
  • Monica Falautano
  • Angelo Ghezzi
  • Benedetta Goretti
  • Francesco Patti
  • Alice Riccardi
  • Flavia Mattioli
Review Article

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.

Keywords

Multiple sclerosis Cognitive assessment 

Notes

Acknowledgments

This work was supported by Biogen Italia S.r.l.

References

  1. 1.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  2. 2.
    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 CrossRefPubMedGoogle Scholar
  3. 3.
    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 CrossRefPubMedGoogle Scholar
  4. 4.
    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 CrossRefPubMedGoogle Scholar
  5. 5.
    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):692–696CrossRefPubMedGoogle Scholar
  6. 6.
    Langdon DW (2011) Cognition in multiple sclerosis. Curr Opin Neurol 24(3):244–249.  https://doi.org/10.1097/WCO.0b013e328346a43b CrossRefPubMedGoogle Scholar
  7. 7.
    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 CrossRefPubMedGoogle Scholar
  8. 8.
    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 CrossRefPubMedGoogle Scholar
  9. 9.
    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):1054–1059CrossRefPubMedGoogle Scholar
  10. 10.
    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 CrossRefPubMedGoogle Scholar
  11. 11.
    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 CrossRefPubMedGoogle Scholar
  12. 12.
    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 CrossRefPubMedGoogle Scholar
  13. 13.
    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 CrossRefPubMedGoogle Scholar
  14. 14.
    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):168–172CrossRefPubMedGoogle Scholar
  15. 15.
    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):1602–1606CrossRefPubMedGoogle Scholar
  16. 16.
    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):41–46CrossRefPubMedGoogle Scholar
  17. 17.
    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):1258–126CrossRefPubMedGoogle Scholar
  18. 18.
    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, MilwaukeeGoogle Scholar
  19. 19.
    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 19:161–170CrossRefPubMedGoogle Scholar
  20. 20.
    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):1121–1123CrossRefPubMedGoogle Scholar
  21. 21.
    Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389CrossRefPubMedGoogle Scholar
  22. 22.
    Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33(11):1444–1452CrossRefPubMedGoogle Scholar
  23. 23.
    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):787–793CrossRefPubMedGoogle Scholar
  24. 24.
    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 CrossRefPubMedGoogle Scholar
  25. 25.
    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 CrossRefPubMedGoogle Scholar
  26. 26.
    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 CrossRefPubMedGoogle Scholar
  27. 27.
    Rosti E, Hamalainen P, Koivisto K, Hokkanen L (2007) PASAT in detecting cognitive impairment in relapsing-remitting MS. Appl Neuropsychol 14(2):101–112CrossRefPubMedGoogle Scholar
  28. 28.
    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):244–250CrossRefPubMedGoogle Scholar
  29. 29.
    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):106–111CrossRefPubMedGoogle Scholar
  30. 30.
    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 CrossRefPubMedGoogle Scholar
  31. 31.
    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 CrossRefPubMedGoogle Scholar
  32. 32.
    Smith A (1982) Symbol digit modalities test (SDMT) manual (revised). Western Psychological Services, Los AngelesGoogle Scholar
  33. 33.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    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):52–57CrossRefPubMedGoogle Scholar
  35. 35.
    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 CrossRefPubMedGoogle Scholar
  36. 36.
    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 CrossRefPubMedGoogle Scholar
  37. 37.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    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 CrossRefGoogle Scholar
  39. 39.
    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 CrossRefPubMedGoogle Scholar
  40. 40.
    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):410–415CrossRefPubMedGoogle Scholar
  41. 41.
    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):95–101CrossRefPubMedGoogle Scholar
  42. 42.
    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):675–678CrossRefPubMedGoogle Scholar
  43. 43.
    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 CrossRefPubMedGoogle Scholar
  44. 44.
    Delis DC, Kaplan E, Kramer JH (2001) Delis–Kaplan executive function system. The Psychological Corporation, San AntonioGoogle Scholar
  45. 45.
    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 CrossRefPubMedGoogle Scholar
  46. 46.
    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):381–397CrossRefPubMedGoogle Scholar
  47. 47.
    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 CrossRefPubMedGoogle Scholar
  48. 48.
    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 CrossRefPubMedGoogle Scholar
  49. 49.
    Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California verbal learning test, second edition (CVLT-II). Psychological Corporation, San AntonioGoogle Scholar
  50. 50.
    Benedict RHB (1997) The brief visuospatial memory test revised (BVMT-R). Psychosocial Assessment Resources Inc, LutzGoogle Scholar
  51. 51.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    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):1289–1296CrossRefPubMedGoogle Scholar
  54. 54.
    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 CrossRefPubMedCentralPubMedGoogle Scholar
  55. 55.
    Stern Y (2009) Cognitive reserve. Neuropsychologia 47(10):2015–2028.  https://doi.org/10.1016/j.neuropsychologia.2009.03.004 CrossRefPubMedCentralPubMedGoogle Scholar
  56. 56.
    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 CrossRefPubMedGoogle Scholar
  57. 57.
    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 CrossRefPubMedGoogle Scholar
  58. 58.
    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 CrossRefPubMedGoogle Scholar
  59. 59.
    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):613–637Google Scholar
  60. 60.
    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 CrossRefGoogle Scholar
  61. 61.
    International Federation of Multiple Sclerosis Societies. Minimal Record of Disability—1983 (1984) Acta Neurol Scand Suppl 101:169–190Google Scholar
  62. 62.
    Ontaneda D, Cohen JA, Amato MP (2017) Clinical outcome measures for progressive MS trials. Mult Scler 23(12):1627–1635CrossRefPubMedGoogle Scholar
  63. 63.
    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 CrossRefPubMedGoogle Scholar
  64. 64.
    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 CrossRefPubMedGoogle Scholar
  65. 65.
    Rao SM, Leo GJ, Bernardin L, Unverzagt F (1991) Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology 41(5):685–691CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Italia S.r.l., part of Springer Nature 2018

Authors and Affiliations

  • Maria Pia Amato
    • 1
    Email author
  • Vincenzo Brescia Morra
    • 2
  • Monica Falautano
    • 3
  • Angelo Ghezzi
    • 4
  • Benedetta Goretti
    • 1
  • Francesco Patti
    • 5
  • Alice Riccardi
    • 6
  • Flavia Mattioli
    • 7
  1. 1.Department of NEUROFARBAUniversity of FlorenceFlorenceItaly
  2. 2.Department NSROUniversity of NaplesNaplesItaly
  3. 3.Department of Neurology, INSPEVita-Salute University and IRCCS-San Raffaele HospitalMilanItaly
  4. 4.Centro Studi Sclerosi MultiplaGallarate Hospital Vita-Salute UniversityGallarateItaly
  5. 5.Department of Neurosciences G.F. IngrassiaUniversity of CataniaCataniaItaly
  6. 6.Multiple Sclerosis Centre, Department of Neurosciences-DNSPadovaItaly
  7. 7.Neuropsychology UnitSpedali Civili of BresciaBresciaItaly

Personalised recommendations