Cognitive Impairment in Early Stages of Multiple Sclerosis

Czech version

Authors: E. Hynčicová ¹; E. Meluzínová ¹; M. Vyhnálek ^1,3; J. Libertínová ¹; I. Kovářová ²; T. Nikolai ^1,2; J. Hort ^1,3; J. Laczó ^1,3
Authors‘ workplace: Neurologická klinika 2. LF UK a FN v Motole, Praha ¹; Neurologická klinika 1. LF UK a VFN v Praze ²; ICRC, FN u sv. Anny v Brně ³
Published in: Cesk Slov Neurol N 2013; 76/109(6): 690-694
Category: Review Article

Overview

Multiple sclerosis (MS) is a chronic disease affecting brain and spinal cord and leading primarily to motor disability. Cognitive deficit in patients with MS are often neglected in routine clinical practise despite its significant impact on patients’ quality of life. Recent studies have suggested that cognitive impairment is present in almost 65% of patients with MS even at the earliest stages of the disease – in patients with clinically isolated syndrome (CIS). The goal of this review was to summarize results of previous studies focused on cognitive deficit in patients with MS. We put particular emphasis on early stages of the disease including patients after the first clinical manifestation of the disease (CIS), who are likely to develop clinically definite multiple sclerosis (CDMS). We further describe the relationship between cognitive functions and structural changes on magnetic resonance imaging (MRI). We also mention the most commonly used neuropsychological batteries and pharmacological and non-pharmacological treatments of cognitive deficits in patients with MS. The final part of the review focuses on fatigue, depression and quality of life.

Key words:
multiple sclerosis – clinically isolated syndrome – cognitive deficit – neuropsychological tests – magnetic resonance imaging

The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.

The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.

Sources

1. Schulz D, Kopp B, Kunkel A, Faiss JH. Cognition in the early stage of multiple sclerosis. J Neurol 2006; 253(8): 1002– 1010.

2. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol 2008; 7(12): 1139– 1151.

3.Vleugels L, Lafosse C, van Nunen A, Nachtergaele S, Ketelaer P, Charlier M et al. Visuoperceptual impairment in multiple sclerosis patients diagnosed with neuropsychological tasks. Mult Scler 2000; 6(4): 241– 254.

4. Laatu S, Hämäläinen P, Revonsuo A, Portin R, Ruutiainen J. Semantic memory deficit in multiple sclerosis; impaired understanding of conceptual meanings. J Neurol Sci 1999; 162(2): 152– 161.

5. Štecková T, Hluštík P, Sládková V, Doláková J, Zapletalová J, Kaňovský P. Kognitivní dysfunkce u pacientů s klinickým izolovaným syndromem a roztroušenou sklerózou. Cesk Slov Neurol N 2011; 74/ 107(5): 551– 555.

6. Rao SM, Leo GJ, Bernardin L, Unverzagt F. Cognitive dysfunction in multiple sclerosis: I. Frequency, patterns, and prediction. Neurology 1991; 41(5): 685– 691.

7.Audoin B, Au Duong MV, Ranjeva JP, Ibarrola D, Malikova I, Confort‑ Gouny S et al. Magnetic resonance study of the influence of tissue damage and cortical reorganization on PASAT performance at the earliest stage of multiple sclerosis. Hum Brain Mapp 2005; 24(3): 216– 228.

8. Huijbregts SC, Kalkers NF, de Sonneville LM, de Groot V, Reuling IE, Polman CH. Differences in cognitive impairment of relapsing remitting, secondary, and primary progressive MS. Neurology 2004; 63(2): 335– 339.

9. Denney DR, Gallagher KS, Lynch SG. Deficits in processing speed in patients with multiple sclerosis: evidence from explicit and covert measures. Arch Clin Neuropsychol 2011; 26(2): 110– 119.

10. 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(1– 2): 129– 136.

11. DeLuca J, Chelune GJ, Tulsky DS, Lengenfelder J, Chiaravalloti ND. Is speed of processing or working memory the primary information processing deficit in multiple sclerosis? J Clin Exp Neuropsychol 2004; 26(4): 550– 562.

12. Janculjak D, Mubrin A, Brinar V, Spilich G. Changes of attention and memory in a group of patients with multiple sclerosis. Clin Neurol Neurosurg 2002; 104(3): 221– 227.

13. Bergendal G, Fredrikson S, Almkvist O. Selective decline in information processing in subgroups of multiple sclerosis: an 8 year old longitudinal study. Eur Neurol 2007; 57(4): 193– 202.

14. Winkelmann A, Engel C, Apel. Cognitive impairment in multiple sclerosis. J Neurol 2008; 255 (Suppl 2): 309– 310.

15. Potagas C, Giogkaraki E, Koutsis G, Mandellos D,Tsirempolou E, Sfagos C et al. Cognitive impairment in different MS subtypes and clinically isolated syndromes. J Neurol Sci 2008; 267(1– 2): 100– 106.

16. Drew M, Tippett LJ, Starkey NJ, Isler RB. Executive dysfunction and cognitive impairment in a large community‑based sample with multiple sclerosis form New Zealand: a descriptive study. Arch Clin Neuropsychol 2008; 23(1): 1– 19.

17. Bagert B, Camplair P, Bourdette D. Cognitive dysfunction in multiple sclerosis: natural history, pathophysiology and management. CNS Drugs 2002; 16(7): 445– 455.

18. Simioni S, Ruffieux C, Bruggimann L, Annoni JM, Schluep M. Cognition, mood and fatigue in patients in the early stage of multiple sclerosis. Swiss Med Wkly 2007; 137(35– 36): 496– 501.

19. Parmenter BA, Zivadinov R, Kerenyi L, Gavett R, Weinstock‑ Guttman B, Dwyer MG et al. Validity of the Wisconsin Card Sorting and Delis‑ Kaplan Executive Function System (DKEFS) Sorting Tests in multiple sclerosis. J Clin Exp Neuropsychol 2007; 29(2): 215– 223.

20. Arnett PA, Higginson CI, Randolph JJ. Depression in multiple sclerosis: relationship to planning ability. J Int Neuropsychol Soc 2001; 7(6): 665– 674.

21. Denney DR, Lynch SG, Parmenter BA, Horne N. Cognitive impairment in relapsing and primary progressive multiple sclerosis: mostly a matter of speed. J Int Neuropsychol Soc 2004; 10(7): 948– 956.

22. Grant I, McDonald WI, Trimble MR, Smith E, Reed R.Deficient learning and memory in early and middle phases of multiple sclerosis. J Neurol Neurosurg Psychiatry 1984; 47(3): 250– 255.

23. Grafman J, Rao S, Bernardin L, Leo GJ. Automatic memory processes in patients with multiple sclerosis. Arch Neurol 1991; 48(10): 1072– 1075.

24. Jønsson A, Andresen J, Storr L, Tscherning T, Soelberg Sørensen P, Ravnborg M. Cognitive impairment in newly diagnosed multiple sclerosis patients: a 4‑year follow‑up study. J Neurol Sci 2006; 245(1– 2): 77– 85.

25. Rao SM. Neuropsychology of multiple sclerosis: a critical review. J Clin Exp Neuropsychol 1986; 8(5): 503– 542.

26. Thornton AE, Raz N. Memory impairment in multiple sclerosis: a quantitative review. Neuropsychology 1997; 11(3): 357– 366.

27. Haase C, Tinnefeld M, Lienemann M, Ganz RE, Faustmann PM. Depression and cognitive impairment in disability‑free early multiple sclerosis. Behav Neurol 2003; 14(1– 2): 39– 45.

28. Camp SJ, Stevenson VL, Thompson AJ, Miller DH, Borras C, Auriacombe S et al. Cognitive function in primary progressive and transitional progressive multiple sclerosis: a controlled study with MRI correlates. Brain 1999; 122(7): 1341– 1348.

29. De Sonneville LM, Boringa JB, Reuling IE, Lazeron RH, Adèr HJ, Polman CH. Information processing characteristics in subtypes of multiple sclerosis. Neuropsychologia 2002; 40(11): 1751– 1755.

30. Bruce JM, Bruce AS, Arnett PA. Mild visual acuity disturbances are associated with performance on tests of complex visual attention in MS. J Int Neuropsychol Soc 2007; 13(3): 544– 548.

31. Achiron A, Barak Y. Cognitive impairment in probable multiple sclerosis. J Neurol Neurosurg Psychiatry 2003; 74(4): 443– 446.

32. Henry JD, Beatty WW. Verbal fluency deficits in multiple sclerosis. Neuropsychologia 2006; 44(7): 1166– 1174.

33. Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML et al. Association of neocortical volume changes with cognitive deterioration in relapsing‑ remitting multiple sclerosis. Arch Neurol 2007; 64(8): 1157– 1161.

34. 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– 1200 .

35. Folstein MF, Folstein SE, McHugh PR. “Mini‑mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12(3): 189– 198.

36. Mathuranath PS, Cherian JP, Mathew R, George A,Alexander A, Sarma SP. Mini mental state examination and the Addenbrooke‘s cognitive examination: effect of education and norms for a multicultural population. Neurol India 2007; 55(2): 106– 110.

37. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005; 53(4): 695– 699.

38. Hummelová‑ Fanfrdlová Z, Rektorová I, Sheardová K,Bartoš A, Línek V, Ressner P et al. Česká adaptace Addenbrookského kognitivního testu (Addenbrooke’s Cognitive Examination). Československá psychologie 2009; 53(4): 376– 388.

39. Sánchez MP, Nieto A, Barroso J, Martín V, Hernández MA. Brain atrophy as a marker of cognitive impairment in mildly disabling relapsing‑ remitting multiple sclerosis. Eur J Neurol 2008; 15(10): 1091– 1099.

40. Tekok‑ Kilic A, Benedict RH, Weinstock‑ Guttman B,Dwyer MG, Carone D, Srinivasaraghavan B et al. Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage 2007; 36(4): 1294– 1300.

41. Reuter F, Zaaraoui W, Crespy L, Faivre A, Rico A, Malikova I et al. Cognitive impairment at the onset of multiple sclerosis: relationship to lesion location. Mult Scler 2011; 17(6): 755– 758.

42. Calabrese M, Rocca MA, Atzori M, Mattisi I, Favaretto A, Perini P et al. A 3‑year magnetic resonance imaging study of cortical lesions in relapse‑ onset multiple sclerosis. Ann Neurol 2010; 67(3): 376– 383.

43. Calabrese M, Agosta F, Rinaldi F, Mattisi I, Grossi P,Favaretto A et al. Cortical lesions and atrophy associated with cognitive impairment in relapsing‑ remitting multiple sclerosis. Arch Neurol 2009; 66(9): 1144– 1150.

44. Obhlídalová I, Keřkovský M, Štourač P, Bednařík P,Vlčková E. Diagnostické možnosti zobrazovacích metod v hodnocení morfologického korelátu kognitivních změn u pacientů s roztroušenou sklerózou. Cesk Slov Neurol N 2012; 75/ 108(2): 170– 178.

45. Amato MP, Bartolozzi ML, Zipoli V, Portaccio E, Mortilla M, Guidi L et al. Neocortical volume decrease in relapsing‑ remitting MS patients with mild cognitive impairment. Neurology 2004; 63(1): 89– 93.

46. Benedict RH, Zivadinov R, Carone DA, Weinstock‑ Guttman B, Gaines J, Maggiore C et al. Regional lobar atrophy predicts memory impairment in multiple sclerosis. AJNR Am J Neuroradiol. 2005; 26(7): 1824– 1831.

47. Houtchens MK, Benedict RH, Killiany R, Sharma J,Jaisani Z, Singh B et al. Thalamic atrophy and cognition in multiple sclerosis. Neurology 2007; 69(12): 1213– 1223.

48. Lin F, Yu C, Liu Y, Li K, Lei H. Diffusion tensor group tractography of the corpus callosum in clinically isolated syndrome. AJNR Am J Neuroradiol 2011; 32(1): 92– 98.

49. Rimkus Cde M, Junqueira Tde F, Lyra KP, Jackowski MP, Machado MA, Miotto EC et al. Corpus callosum microstructural changes correlate with cognitive dysfunction in early stages of relapsing‑ remitting multiple sclerosis: axial and radial diffusivities approach. Mult Scler Int 2011; 2011: 304875.

50. Kalincik T, Vaneckova M, Tyblova M, Krasensky J, Seidl Z, Havrdova E et al. Volumetric MRI markers and predictors of disease activity in early multiple sclerosis: a longitudinal cohort study. PLoS One 2012; 7(11): e50101.

51. Vaneckova M, Kalincik T, Krasensky J, Horakova D, Havrdova E, Hrebikova T et al. Corpus callosum atrophy – a simple predictor of multiple sclerosis progression: a longitudinal 9‑year study. Eur Neurol 2012; 68(1): 23– 27.

52. Feinstein A. Mood disorders in multiple sclerosis and the effects on cognition. J Neurol Sci 2006; 245(1– 2): 63– 66.

53. Haase CG, Tinnefeld M, Lienemann M, Ganz RE, Faustmann PM. Depression and cognitive impairment in disability‑free early multiple sclerosis. Behav Neurol 2003; 14(1– 2): 39– 45.

54. Anhoque CF, Domingues SC, Carvalho T, Teixeira AL, Domingues RB. Anxiety and depressive symptoms in clinically isolated syndrome and multiple sclerosis. Arq Neuropsiquiatr 2011; 69(6): 882– 886.

55. Zajicek JP, Ingram WM, Vickery J, Creanor S, Wright DE, Hobart JC. Patient‑ orientated longitudinal study of multiple sclerosis in south west England (The South West Impact of Multiple Sclerosis Project, SWIMS). 1: Protocol and baseline characteristics of cohort. BMC Neurol 2010; 10: 88.

56. Honarmand K, Akbar N, Kou N, Feinstein A. Predicting employment status in multiple sclerosis patients: the utility of the MS functional composite. J Neurol 2011; 258 (2): 244– 249.

57. Schultheis MT, Weisser V, Ang J, Elovic E, Nead R,Sestito N. Examining the relationship between cognition and driving performance in multiple sclerosis. Arch Phys Med Rehabil 2010; 91(3): 465– 473.

58. Leo GJ, Rao SM. Effects of intravenous physostigmine and lecithin on memory loss in multiple sclerosis: Report of a pilot study. J Neurol Rehabil 1988; 2: 123– 129.

59. Johnson SK, Diamond BJ, Rausch S, Kaufman M, Shiflett SC, Graves L. The effect of Gingko biloba on functional measures in multiple sclerosis: a pilot randomized controlled trial. Explore 2006; 2(1): 19– 24.

60. Zakzanis KK. Distinct neurocognitive profiles in multiple sclerosis subtypes. Arch Clin Neuropsychol 2000; 15(2): 115–136.