Treatment of cognitive impairment in multiple sclerosis: Position paper

Journal of Neurology

Volumn 260, Issue 6, 2013, Pages 1452-1468

  Amato, Maria Pia ^a   Langdon, Dawn ^b   Montalban, Xavier ^c   Benedict, Ralph H B ^d   Deluca, John ^e   Krupp, Lauren B ^f   Thompson, Alan J ^g   Comi, Giancarlo ^h  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d UNIVERSITY AT BUFFALO   (United States)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^f STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Cognition; Cognitive rehabilitation; Disease modifying drugs; Multiple sclerosis; Symptomatic treatment; Treatment

Indexed keywords

3,4 DIAMINOPYRIDINE; 4 AMINOPYRIDINE; AMANTADINE; AMPHETAMINE; BETA1A INTERFERON; DONEPEZIL; FINGOLIMOD; INTERFERON BETA SERINE; MODAFINIL; PEMOLINE; RIVASTIGMINE;

BEHAVIOR THERAPY; COGNITIVE DEFECT; DRUG MEGADOSE; EXECUTIVE FUNCTION; HEALTH PROGRAM; HUMAN; LEARNING; MEMORY; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGY; PRIORITY JOURNAL; REVIEW; SELF CARE;

COGNITION DISORDERS; HUMANS; MULTIPLE SCLEROSIS;

EID: 84878827647     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-012-6678-0     Document Type: Review

References (102)

1. Peyser JM, Rao SM, LaRocca NG, Kaplan E (1990) Guidelines for neuropsychological research in multiple sclerosis. Arch Neurol 47:94-97 (Pubitemid 20024163)
2. Rao S, Leo G, Bernardin L, Unverzagt F (1991) Cognitive dysfunction in multiple sclerosis: frequency, patterns, and predictions. Neurology 41:685-691
3. Rao SM (1997) Neuropsychological aspects of multiple sclerosis. In: Raine CS, McFarland HF, Tourtellotte WW (eds) Multiple sclerosis: clinical and pathogenetic basis. Chapman & Hall, London, pp 357-362
4. Benedict RH, Cookfair D, Gavett R et al (2006) Validity of the minimal assessment of cognitive function in multiple sclerosis. J Int Neuropsychol Soc 12:549-558 (Pubitemid 44070305)
5. Benedict R, Bobholz J (2007) Multiple sclerosis. Semin Neurol 27(1):78-85 (Pubitemid 46239042)
6. Amato MP, Portaccio E, Goretti B et al (2010) Cognitive impairment in early stages of multiple sclerosis. Neurol Sci 31(Suppl 2):S211-S214
7. Amato MP, Zipoli V, Portaccio E (2008) Cognitive changes in multiple sclerosis. Expert Rev Neurother 8:1585-1596
8. Benedict RH, Bruce JM, Dwyer MG, Abdelrahman N, Hussein S, Weinstock-Guttman B, Garg N, Munschauer F, Zivadinov R (2006) Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 63(9):1301-1306 (Pubitemid 44379833)
9. Amato MP, Portaccio E, Goretti B et al (2010) Relevance of cognitive deterioration in early relapsing-remitting MS: a 3-year follow-up study. Mult Scler 16:1474-1482
10. Zipoli V, Goretti B, Hakiki B et al (2010) Cognitive impairment predicts conversion to multiple sclerosis in clinically isolated syndromes. Mult Scler 16:62-67
11. Reuter F, Zaaraoui W, Crespy L, Faivre A, Rico A, Malikova I et al (2011) Frequency of cognitive impairment dramatically increases during the first 5 years of multiple sclerosis. J Neurol Neurosurg Psychiatry 82(10):1157-1159
12. Lebrun C, Blanc F, Brassat D, Zephir H, de Seze J, CFSEP (2010) Cognitive function in radiologically isolated syndrome. Mult Scler 16(8):919-925
13. Amato MP, Hakiki B, Goretti B, et al (2012) Association of T1 lesion volume and neocortical atrophy with cognitive impairment in radiologically isolated syndromes. Neurology (in press)
14. Amato MP, Zipoli V, Goretti B et al (2006) Benign multiple sclerosis: cognitive, psychological and social aspects in a clinical cohort. J Neurol 253:1054-1059 (Pubitemid 44441131)
15. Benedict RH, Zivadinov R (2011) Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat Rev Neurol 7(6):332-342
16. Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139-1151
17. Comi G (2010) Effects of disease modifying treatments on cognitive dysfunction in multiple sclerosis. Neurol Sci 31(Suppl 2):S261-S264
18. Sumowski JF, Wylie GR, Chiaravalloti ND, DeLuca J (2010) Intellectual enrichment lessens the effect of brain atrophy on learning and memory in MS. Neurology 74:1942-1945
19. 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 (Pubitemid 39585247)
20. Sonder J, Bosma L, van der Linden F, Knol D, Polman C, Uitdehaag B (2012) Proxy measurements in multiple sclerosis: agreement on different patient-reported outcome scales. Mult Scler 18(2):196-201
21. Rudick R, Antel J, Confavreux C et al (1997) Recommendations from the National Multiple Sclerosis Society Clinical Outcomes Assessment Task Force. Ann Neurol 42:379-382 (Pubitemid 127744543)
22. Rao SM (1990) A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. Milwaukee, Wisconsin
23. Benedict RH, Fischer JS, Archibald CJ et al (2002) Minimal neuropsychological assessment of MS patients: a consensus approach. Clin Neuropsychol 16:381-397 (Pubitemid 36390381)
24. Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict RH (2009) Sensitivity of conventional memory tests in multiple sclerosis: comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Mult Scler 15:1077-1084
25. Jønsson A, Korfitzen EM, Heltberg A, Ravnborg MH, Byskov-Ottosen E (1993) Effects of neuropsychological treatment in patients with multiple sclerosis. Acta Neurol Scand 88:394-400 (Pubitemid 23347527)
26. Solari A (2010) Methodological aspects of randomized controlled trials on cognitive interventions. Neurol Sci 31(2):279-282
27. O'Brien AR, Chiaravalloti N, Goverover Y, Deluca J (2008) Evidenced-based cognitive rehabilitation for persons with multiple sclerosis: a review of the literature. Arch Phys Med Rehabil 89:761-769 (Pubitemid 351406321)
28. das Nair R, Ferguson H, Stark DL, Lincoln NB (2012) Memory Rehabilitation for people with multiple sclerosis. Cochrane Database Syst Rev 14(3):CD008754
29. DeLuca J, Barbieri-Berger S, Johnson SK (1994) The nature of memory impairments in multiple sclerosis: acquisition versus retrieval. J Clin Exp Neuropsychol 16(2):183-189 (Pubitemid 24119769)
30. DeLuca J, Gaudino EA, Diamond BJ, Christodoulou C, Engel RA (1998) Acquisition and storage deficits in multiple sclerosis. J Clin Exp Neuropsychol 20:376-390 (Pubitemid 28539557)
31. Gaudino EA, Chiaravalloti ND, DeLuca J, Diamond BJ (2001) A comparison of memory performance in relapsing-remitting, primary progressive and secondary progressive, multiple sclerosis. Neuropsychiatry Neuropsychol Behav Neurol 14(1):32-44 (Pubitemid 32179135)
32. Goverover Y, Chiaravalloti N, DeLuca J (2008) Self-generation to improve learning and memory of functional activities in persons with multiple sclerosis: meal preparation and managing finances. Arch Phys Med Rehabil 89:1514-1521
33. Basso MR, Lowery N, Ghormley C, Combs D, Johnson J (2006) Self-generated learning in people with multiple sclerosis. J Int Neuropsychol Soc 12:640-648 (Pubitemid 44462862)
34. Basso MR, Ghormley C, Lowery N, Combs D, Bornstein RA (2002) Self-generated learning in people with multiple sclerosis: an extension of Chiaravalloti and DeLuca (2002). J Clin Exp Neuropsychol 30:63-69
35. Goverover Y, Hillary FG, Chiaravalloti N, Arango-Lasprilla JC, DeLuca J (2009) A functional application of the spacing effect to improve learning and memory in persons with multiple sclerosis. J Clin Exp Neuropsychol 31:513-522
36. Goverover Y, Basso MR, Wood H, Chiaravalloti N, DeLuca J (2011) Examining the benefits of combining two learning strategies on recall of functional information in persons with multiple sclerosis. Mult Scler 17(12):1488-1497
37. Chiaravalloti ND, DeLuca J, Moore NB, Ricker JH (2005) Treating learning impairments improves memory performance in multiple sclerosis: a randomized clinical trial. Mult Scler 11:58-68 (Pubitemid 40259976)
38. Chiaravalloti ND, Wylie G, Leavitt V, DeLuca J (2012) Increased cerebral activation after behavioral treatment for memory deficits in MS. J Neurol 259(7):1337-1346
39. Brenk A, Laun K, Haase CG (2008) Short-term cognitive training improves mental efficacy and mood in patients with multiple sclerosis. Eur Neurol 60:304-309
40. Tesar N, Bandion K, Baumhackl U (2005) Efficacy of a neuropsychological training programme for patients with multiple sclerosis - a randomised controlled trial. Wien Klin Wochenschr 117:747-754 (Pubitemid 41818518)
41. Hildebrandt H, Lanz M, Hahn HK et al (2007) Cognitive training in MS: effects and relation to brain atrophy. Res Neurol Neurosci 25:33-43 (Pubitemid 46631012)
42. Mendozzi L, Pugnetti L, Motta A, Barbieri E, Gambini A, Cazzullo CL (1998) Computer-assisted memory retraining of patients with multiple sclerosis. Ital J Neurol Sci 19:S431-S438
43. DeLuca J, Chelune GJ, Tulsky DS, Lengenfelder J, Chiaravalloti ND (2004) Is speed of processing or working memory the primary information processing deficit in multiple sclerosis? J Clin Exp Neuropsychol 26:550-562 (Pubitemid 39318348)
44. Acevedo A, Loewenstein DA (2007) Nonpharmacological cognitive interventions in aging and dementia. J Geriatr Psychiatry Neurol 20(4):239-249 (Pubitemid 350077304)
45. Ball K, Edwards JD, Ross LA (2007) The impact of speed of processing training on cognitive and everyday functions. J Gerontol Ser B Psychol Sci Soc Sci 1:19-31
46. Plohmann AM, Kappos L, Ammann W et al (1998) Computer assisted retraining of attentional impairments in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 64:455-462 (Pubitemid 28195945)
47. Solari A, Motta A, Mendozzi L et al (2004) Computer-aided retraining of memory and attention in people with multiple sclerosis: a randomized, double-blind controlled trial. J Neurol Sci 222:99-104 (Pubitemid 38881513)
48. Mattioli F, Stampatori C, Zanotti D, Parrinello G, Capra R (2010) Efficacy and specificity of intensive rehabilitation of attention and executive functions in multiple sclerosis. J Neurol Sci 288:101-105
49. O'Brien A, Chiaravalloti N, Arango-Lasprilla JC, Lengenfelder J, DeLuca J (2007) An investigation of the differential effect of self-generation to improve learning and memory in multiple sclerosis and traumatic brain injury. Neuropsychol Rehabil 17:273-292 (Pubitemid 46684026)
50. Sastre-Garriga J, Alonso J, Renom M et al (2011) A functional magnetic resonance proof of concept pilot trial of cognitive rehabilitation in multiple sclerosis. Mult Scler 17:457-476
51. Birnboim S, Miller A (2004) Cognitive strategies application of multiple sclerosis patients. Mult Scler 10:67-73 (Pubitemid 38100529)
52. Fink F, Rischkau E, Butt M, Klein J, Eling P, Hildebrandt H (2010) Efficacy of an executive function intervention programme in MS: a placebo-controlled and pseudo-randomized trial. Mult Scler 16:1148-1151
53. Allen DN, Goldstein G, Heyman RA, Rondinelli T (1998) Teaching memory strategies to persons with multiple sclerosis. J Rehabil Res Dev 35:405-410 (Pubitemid 29180034)
54. Brissart H, Leroy M, Debouverie M (2010) Cognitive rehabilitation in multiple sclerosis: preliminary results and presentation of a new program, PROCOG-SEP]. Rev Neurol (Paris) 166:406-411
55. Chiaravalloti ND, DeLuca J (2002) Self-generation as a means of maximizing learning in multiple sclerosis: an application of the generation effect. Arch Phys Med Rehabil 83:1070-1079 (Pubitemid 34832933)
56. Shatil E, Metzer A, Horvitz O, Miller A (2010) Home-based personalized cognitive training in MS patients: a study of adherence and cognitive performance. Neuro Rehabil 26:143-153
57. Sumowski JF, Chiaravalloti N, DeLuca J (2010) Retrieval practice improves memory in multiple sclerosis: clinical application of the testing effect. Neuropsychology 24:267-272
58. Vogt A, Kappos L, Calabrese P et al (2009) Working memory training in patients with multiple sclerosis. Restor Neurol Neurosci 27:225-235
59. Archibald CJ, Fisk JD (2000) Information processing efficiency in patients with multiple sclerosis. J Clin Exp Neuropsychol 22:686-701
60. Rao SM (1989) On the nature of memory disturbance in multiple sclerosis. J Clin Exp Neuropsychol 11:699-712 (Pubitemid 19271848)
61. Geisler MW, Sliwinski M, Coyle PK, Masur DM, Doscher C, Krupp LB (1996) The effects of amantadine and pemoline on cognitive functioning in multiple sclerosis. Arch Neurol 53:185-188 (Pubitemid 26055267)
62. Smith A (1982) Symbol digit modalities test: manual. Western Psychological Services, Los Angeles
63. Benedict RH (2005) Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis. J Int Neuropsychol Soc 11:727-736 (Pubitemid 41631486)
64. Harel Y, Appleboim N, Lavie M, Achiron A (2009) Single dose of methylphenidate improves cognitive performance in multiple sclerosis patients with impaired attention process. J Neurol Sci 276:38-40
65. Benedict RH, Munschauer F, Zarevics P et al (2008) Effects of l-amphetamine sulfate on cognitive function in multiple sclerosis patients. J Neurol 255:848-852
66. Morrow SA, Kaushik T, Zarevics P et al (2009) The effects of l-amphetamine sulfate on cognition in MS patients: results of a randomized controlled trial. J Neurol 256:1095-1102
67. Sumowski JF, Chiaravalloti N, Erlanger D, Kaushik T, Benedict RH, Deluca J (2011) l-amphetamine improves memory in MS patients with objective memory impairment. Mult Scler 17(9):1141-1145
68. Möller F, Poettgen J, Broemel F, Neuhaus A, Daumer M, Heesen C (2011) HAGIL (Hamburg Vigil Study): a randomized placebo-controlled double-blind study with modafinil for treatment of fatigue in patients with multiple sclerosis. Mult Scler 17(8):1002-1009
69. Lange R, Volkmer M, Heesen C, Liepert J (2009) Modafinil effects in multiple sclerosis patients with fatigue. J Neurol 256:645-650
70. Brickenkamp R (2002) Test d2. Aufmerksamkeits-Belastungs-Test, 9th edn. The d2 test. Test of attention under pressure, 9th edn. Hogrefe, Göttingen
71. Stankoff B, Waubant E, Confavreux C et al (2005) Modafinil for fatigue in MS: a randomized placebo-controlled double-blind study. Neurology 64:1139-1143
72. Wilken JA, Sullivan C, Wallin M et al (2008) Treatment of multiple sclerosis-related cognitive problems with adjunctive modafinil: rationale and preliminary supportive data. Int J MS Care 10:1-10
73. Waxman SG (1982) Membranes, myelin, and the pathophysiology of multiple sclerosis. N Engl J Med 306:1529-1533 (Pubitemid 12123934)
74. Bever CT Jr, Anderson PA, Leslie J et al (1996) Treatment with oral 3,4 diaminopyridine improves leg strength in multiple sclerosis patients: results of a randomized, double- blind, placebo-controlled, crossover trial. Neurology 47:1457-1462 (Pubitemid 26422536)
75. Bever CT Jr, Young D, Anderson PA et al (1994) The effects of 4-aminopyridine in multiple sclerosis patients: results of a randomized, placebo-controlled, double-blind, concentration-controlled, crossover trial. Neurology 44:1054-1059 (Pubitemid 24188176)
76. Rossini PM, Pasqualetti P, Pozzilli C et al (2001) Fatigue in progressive multiple sclerosis: results of a randomized, double-blind, placebo-controlled, crossover trial of oral 4-aminopyridine. Mult Scler 7:354-358 (Pubitemid 33138344)
77. Krupp LB, Christodoulou C, Melville P, Scherl WF, MacAllister WS, Elkins LE (2004) Donepezil improved memory in multiple sclerosis in a randomized clinical trial. Neurology 63:1579-1585 (Pubitemid 39507572)
78. Krupp LB, Christodoulou C, Melville P et al (2011) Multicenter randomized clinical trial of donepezil for memory impairment in multiple sclerosis. Neurology 76:1500-1507
79. Shaygannejad V, Janghorbani M, Ashtari F, Zanjani HA, Zakizade N (2008) Effects of rivastigmine on memory and cognition in multiple sclerosis. Can J Neurol Sci 35:476-481
80. Smits RC, Emmen HH, Bertelsmann FW, Kulig BM, van Loenen AC, Polman CH (1994) The effects of 4-aminopyridine on cognitive function in patients with multiple sclerosis: a pilot study. Neurology 44:1701-1705 (Pubitemid 24286651)
81. Lovera JF, Frohman E, Brown TR et al (2010) Memantine for cognitive impairment in multiple sclerosis: a randomized placebo-controlled trial. Mult Scler 16(6):715-723
82. Gold R, Wolinsky JS, Amato MP, Comi G (2010) Evolving expectations around early management of multiple sclerosis. Ther Adv Neurol Disord 3(6):351-367
83. Pliskin NH, Hamer DP, Goldstein DS, Towle VL, Reder AT, Noronha A (1996) Improved delayed visual reproduction test performance in multiple sclerosis patients receiving interferon beta-1b. Neurology 47:1463-1468 (Pubitemid 26422537)
84. Barak Y, Achiron A (2002) Effect of interferon-beta-1b on cognitive functions in multiple sclerosis. Eur Neurol 47:11-14
85. Fischer JS, Priore RL, Jacobs LD et al (2000) Neuropsychological effects of interferon beta-1a in relapsing multiple sclerosis. Multiple Sclerosis Collaborative Research Group. Ann Neurol 48:885-892
86. Patti F, Amato MP, Bastianello S et al (2010) Effects of immunomodulatory treatment with subcutaneous interferon beta-1a on cognitive decline in mildly disabled patients with relapsing-remitting multiple sclerosis. Mult Scler 16:68-77
87. Weinstein A, Scwid SI, Schiffer RB, McDermott MP, Giang DW, Goodman AD (1999) Neuropsychologic status in multiple sclerosis after treatment with glatiramer. Arch Neurol 56:319-324 (Pubitemid 29120229)
88. Schwid SR, Goodman AD, Weinstein A, McDermott MP, Johnson KP (2007) Cognitive function in relapsing multiple sclerosis: minimal changes in a 10-year clinical trial. J Neurol Sci 255:57-63 (Pubitemid 46414020)
89. Polman CH, O'Connor PW, Havrdova E, Hutchinson M, Kappos L, Miller DH, Phillips JT, Lublin FD, Giovannoni G, Wajgt A, Toal M, Lynn F, Panzara MA, Sandrock AW, AFFIRM Investigators (2006) A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 354(9):899-910
90. Rudick RA, Stuart WH, Calabresi PA, SENTINEL Investigators et al (2006) Natalizumab plus interferon beta-1a for relapsing multiple sclerosis. N Engl J Med 354(9):911-923
91. Mattioli F, Stampatori C, Capra R (2011) The effect of natalizumab on cognitive function in patients with relapsing-remitting multiple sclerosis: preliminary results of a 1-year follow-up study. Neurol Sci 32:83-88
92. Cohen JA, Barkhof F, Comi G et al (2010) Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med 362(5):402-415
93. Kappos L, Polman C, Pozzilli C, Thompson A, Beckmann K, Dahlke F, European Study Group in Final analysis of the European multicenter trial on IFNbeta-1b in secondary-progressive MS (2001) Interferon beta-1b in Secondary-Progressive MS. Neurology 57(11):1969-1975
94. Panitch H, Miller A, Paty D, Weinshenker B, North American Study Group on Interferon beta-1b in Secondary Progressive MS (2004) Interferon beta-1b in secondary progressive MS: results from a 3-year controlled study. Neurology 63(10):1788-1795 (Pubitemid 39532370)
95. Cohen JA, Cutter GR, Fischer JS et al (2002) Benefit of interferon beta-1a on MSFC progression in secondary progressive MS. Neurology 59:679-687
96. Leary SM, Miller DH, Stevenson VL, Brex PA, Chard DT, Thompson AJ (2003) Interferon beta-1a in primary progressive MS: an exploratory, randomized, controlled trial. Neurology 60(1):44-51 (Pubitemid 36070642)
97. Montalban X, Sastre-Garriga J, Tintoré M et al (2009) A single-center, randomized, double-blind, placebo-controlled study of interferon beta-1b on primary progressive and transitional multiple sclerosis. Mult Scler 15:1195-1205
98. Wolinsky JS, Narayana PA, O'Connor P et al (2007) Glatiramer acetate in primary progressive multiple sclerosis: results of a multinational, multicenter, double-blind, placebo-controlled trial. Ann Neurol 61(1):14-24 (Pubitemid 46214240)
99. Kappos L, Polman CH, Freedman MS et al (2006) Treatment with interferon beta-1b delays conversion to clinically definite and McDonald MS in patients with clinically isolated syndromes. Neurology 67(7):1242-1249 (Pubitemid 44563835)
100. Kappos L, Freedman MS, Polman CH, BENEFIT Study Group et al (2007) Effect of early versus delayed interferon beta-1b treatment on disability after a first clinical event suggestive of multiple sclerosis: a 3-year follow-up analysis of the BENEFIT study. Lancet 370(9585):389-397 (Pubitemid 47189673)
101. Kappos L, Freedman MS, Polman CH et al (2009) Long-term effect of early treatment with interferon beta-1b after a first clinical event suggestive of multiple sclerosis: 5-year active treatment extension of the phase 3 BENEFIT trial. Lancet Neurol 8(11):987-997
102. 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