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27.12.2016 | Original Communication

Cognitive impairment and structural brain changes in patients with clinically isolated syndrome at high risk for multiple sclerosis

verfasst von: Eva Hynčicová, Martin Vyhnálek, Adam Kalina, Lukáš Martinkovič, Tomáš Nikolai, Jiří Lisý, Jakub Hort, Eva Meluzínová, Jan Laczó

Erschienen in: Journal of Neurology | Ausgabe 3/2017

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Abstract

Patients with clinically isolated syndrome (CIS), unlike those with multiple sclerosis (MS), have a selective cognitive impairment which is not consistently related to structural brain changes. Our objective was to characterize a profile of cognitive impairment and its association with structural brain changes in patients with CIS who are at high risk of developing MS. Patients with CIS at high risk for MS on interferon-beta (n = 51) and age-, gender-, and education-matched controls (n = 44) underwent comprehensive neuropsychological testing and MRI brain scan with voxel-based morphometry. The CIS group had lower cognitive performance in verbal and nonverbal memory, information processing speed/attention/working memory, and executive and visuo-spatial functions compared to controls (p ≤ 0.040). Lower cognitive performance was present in 18–37 and 14–26% of patients with CIS at high risk for MS depending on the criteria used. Brain volume was reduced predominantly in fronto-temporal regions and the thalamus in the CIS group (p ≤ 0.019). Cognitive performance was not associated with structural brain changes except for the association between worse visuo-spatial performance and lower white matter volume in the CIS group (β = 0.29; p = 0.042). Our results indicated that patients with CIS at high risk for MS may have a pattern of lower cognitive performance and regional brain atrophy similar to that found in patients with MS. Lower cognitive performance may be present in up to one-third of patients with CIS at high risk for MS, but, unlike patients with MS, variability in their cognitive performance may lead to a lack of consistent associations with structural brain changes.

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Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7(12):1139–1151. doi:10.1016/S1474-4422(08)70259-X CrossRefPubMed

Potagas C, Giogkaraki E, Koutsis G, Mandellos D, Tsirempolou E, Sfagos C, Vassilopoulos D (2008) Cognitive impairment in different MS subtypes and clinically isolated syndromes. J Neurol Sci 267(1–2):100–106. doi:10.1016/j.jns.2007.10.002 CrossRefPubMed

Hildebrandt H, Hahn HK, Kraus JA, Schulte-Herbruggen A, Schwarze B, Schwendemann G (2006) Memory performance in multiple sclerosis patients correlates with central brain atrophy. Mult Scler 12(4):428–436CrossRefPubMed

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. doi:10.1001/archneur.63.9.1301 CrossRefPubMed

Calabrese M, Rinaldi F, Mattisi I, Grossi P, Favaretto A, Atzori M, Bernardi V, Barachino L, Romualdi C, Rinaldi L, Perini P, Gallo P (2010) Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 74(4):321–328. doi:10.1212/WNL.0b013e3181cbcd03 CrossRefPubMed

Khalil M, Enzinger C, Langkammer C, Petrovic K, Loitfelder M, Tscherner M, Jehna M, Bachmaier G, Wallner-Blazek M, Ropele S, Schmidt R, Fuchs S, Fazekas F (2011) Cognitive impairment in relation to MRI metrics in patients with clinically isolated syndrome. Mult Scler 17(2):173–180. doi:10.1177/1352458510384009 CrossRefPubMed

Benedict RH, Ramasamy D, Munschauer F, Weinstock-Guttman B, Zivadinov R (2009) Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry 80(2):201–206. doi:10.1136/jnnp.2008.148403 CrossRefPubMed

Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH (2012) Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol 259(1):139–146. doi:10.1007/s00415-011-6147-1 CrossRefPubMed

Glanz BI, Holland CM, Gauthier SA, Amunwa EL, Liptak Z, Houtchens MK, Sperling RA, Khoury SJ, Guttmann CR, Weiner HL (2007) Cognitive dysfunction in patients with clinically isolated syndromes or newly diagnosed multiple sclerosis. Mult Scler 13(8):1004–1010. doi:10.1177/1352458507077943 CrossRefPubMed

10.

Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML, Stromillo ML, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2007) Association of neocortical volume changes with cognitive deterioration in relapsing-remitting multiple sclerosis. Arch Neurol 64(8):1157–1161. doi:10.1001/archneur.64.8.1157 CrossRefPubMed

11.

Nocentini U, Bozzali M, Spano B, Cercignani M, Serra L, Basile B, Mannu R, Caltagirone C, De Luca J (2014) Exploration of the relationships between regional grey matter atrophy and cognition in multiple sclerosis. Brain Imaging Behav 8(3):378–386. doi:10.1007/s11682-012-9170-7 CrossRefPubMed

12.

Benedict RH, Zivadinov R, Carone DA, Weinstock-Guttman B, Gaines J, Maggiore C, Sharma J, Tomassi MA, Bakshi R (2005) Regional lobar atrophy predicts memory impairment in multiple sclerosis. AJNR Am J Neuroradiol 26(7):1824–1831PubMed

13.

Tekok-Kilic A, Benedict RH, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, Yella V, Abdelrahman N, Munschauer F, Bakshi R, Zivadinov R (2007) Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage 36(4):1294–1300. doi:10.1016/j.neuroimage.2007.04.017 CrossRefPubMed

14.

Sanchez MP, Nieto A, Barroso J, Martin V, Hernandez MA (2008) Brain atrophy as a marker of cognitive impairment in mildly disabling relapsing-remitting multiple sclerosis. Eur J Neurol 15(10):1091–1099. doi:10.1111/j.1468-1331.2008.02259.x CrossRefPubMed

15.

Zivadinov R, De Masi R, Nasuelli D, Bragadin LM, Ukmar M, Pozzi-Mucelli RS, Grop A, Cazzato G, Zorzon M (2001) MRI techniques and cognitive impairment in the early phase of relapsing-remitting multiple sclerosis. Neuroradiology 43(4):272–278CrossRefPubMed

16.

Lazeron RH, Boringa JB, Schouten M, Uitdehaag BM, Bergers E, Lindeboom J, Eikelenboom MI, Scheltens PH, Barkhof F, Polman CH (2005) Brain atrophy and lesion load as explaining parameters for cognitive impairment in multiple sclerosis. Mult Scler 11(5):524–531CrossRefPubMed

17.

Fulton JC, Grossman RI, Udupa J, Mannon LJ, Grossman M, Wei L, Polansky M, Kolson DL (1999) MR lesion load and cognitive function in patients with relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol 20(10):1951–1955PubMed

18.

Calabrese M, Agosta F, Rinaldi F, Mattisi I, Grossi P, Favaretto A, Atzori M, Bernardi V, Barachino L, Rinaldi L, Perini P, Gallo P, Filippi M (2009) Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 66(9):1144–1150. doi:10.1001/archneurol.2009.174 CrossRefPubMed

19.

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

20.

Fisniku LK, Brex PA, Altmann DR, Miszkiel KA, Benton CE, Lanyon R, Thompson AJ, Miller DH (2008) Disability and T2 MRI lesions: a 20-year follow-up of patients with relapse onset of multiple sclerosis. Brain 131(Pt 3):808–817. doi:10.1093/brain/awm329 CrossRefPubMed

21.

Tintore M, Rovira A, Rio J, Otero-Romero S, Arrambide G, Tur C, Comabella M, Nos C, Arevalo MJ, Negrotto L, Galan I, Vidal-Jordana A, Castillo J, Palavra F, Simon E, Mitjana R, Auger C, Sastre-Garriga J, Montalban X (2015) Defining high, medium and low impact prognostic factors for developing multiple sclerosis. Brain 138(Pt 7):1863–1874. doi:10.1093/brain/awv105 CrossRefPubMed

22.

Summers M, Swanton J, Fernando K, Dalton C, Miller DH, Cipolotti L, Ron MA (2008) Cognitive impairment in multiple sclerosis can be predicted by imaging early in the disease. J Neurol Neurosurg Psychiatry 79(8):955–958. doi:10.1136/jnnp.2007.138685 CrossRefPubMed

23.

Audoin B, Zaaraoui W, Reuter F, Rico A, Malikova I, Confort-Gouny S, Cozzone PJ, Pelletier J, Ranjeva JP (2010) Atrophy mainly affects the limbic system and the deep grey matter at the first stage of multiple sclerosis. J Neurol Neurosurg Psychiatry 81(6):690–695. doi:10.1136/jnnp.2009.188748 CrossRefPubMed

24.

Feuillet L, Reuter F, Audoin B, Malikova I, Barrau K, Cherif AA, Pelletier J (2007) Early cognitive impairment in patients with clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 13(1):124–127CrossRefPubMed

25.

Viterbo RG, Iaffaldano P, Trojano M (2013) Verbal fluency deficits in clinically isolated syndrome suggestive of multiple sclerosis. J Neurol Sci 330(1–2):56–60. doi:10.1016/j.jns.2013.04.004 CrossRefPubMed

26.

Panou T, Mastorodemos V, Papadaki E, Simos PG, Plaitakis A (2012) Early signs of memory impairment among multiple sclerosis patients with clinically isolated syndrome. Behav Neurol 25(4):311–326. doi:10.3233/BEN-2012-110201 CrossRefPubMed

27.

Uher T, Blahova-Dusankova J, Horakova D, Bergsland N, Tyblova M, Benedict RH, Kalincik T, Ramasamy DP, Seidl Z, Hagermeier J, Vaneckova M, Krasensky J, Havrdova E, Zivadinov R (2014) Longitudinal MRI and neuropsychological assessment of patients with clinically isolated syndrome. J Neurol 261(9):1735–1744. doi:10.1007/s00415-014-7413-9 CrossRefPubMed

28.

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

29.

Steckova T, Hlustik P, Sladkova V, Odstrcil F, Mares J, Kanovsky P (2014) Thalamic atrophy and cognitive impairment in clinically isolated syndrome and multiple sclerosis. J Neurol Sci 342(1–2):62–68. doi:10.1016/j.jns.2014.04.026 CrossRefPubMed

30.

Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69(2):292–302. doi:10.1002/ana.22366 CrossRefPubMedPubMedCentral

31.

Dufek M (2014) Léčba roztroušené sklerózy v České republice—možnosti a realita. Neurol praxi 15(1):31–35

32.

Tintore M, Rovira A, Brieva L, Grive E, Jardi R, Borras C, Montalban X (2001) Isolated demyelinating syndromes: comparison of CSF oligoclonal bands and different MR imaging criteria to predict conversion to CDMS. Mult Scler 7(6):359–363CrossRefPubMed

33.

Bezdicek O, Stepankova H, Motak L, Axelrod BN, Woodard JL, Preiss M, Nikolai T, Ruzicka E, Poreh A (2014) Czech version of Rey Auditory Verbal Learning Test: normative data. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 21(6):693–721. doi:10.1080/13825585.2013.865699 CrossRefPubMed

34.

Schmidt M (1996) Rey auditory verbal learning test: a handbook. Western Psychological Services, Los Angeles

35.

Benedict R (1997) Brief Visuospatial Memory Test-revised professional manual. Psychological Assessment Resources Inc., Odessa

36.

Smith A (1982) Symbol digit modalities test: Manual. Western Psychological Service, Los Angeles

37.

Gronwall D (1977) Paced auditory serial-addition task: a measure of recovery from concussion. Percept Mot Skills 44(2):367–373CrossRefPubMed

38.

Wechsler D (1997) WAIS-III: administration and scoring manual: Wechsler Adult Intelligence Scale. Psychological Corporation, San Antonio

39.

Bezdicek O, Motak L, Axelrod BN, Preiss M, Nikolai T, Vyhnalek M, Poreh A, Ruzicka E (2012) Czech version of the Trail Making Test: normative data and clinical utility. Arch Clin Neuropsychol 27(8):906–914. doi:10.1093/arclin/acs084 CrossRefPubMed

40.

Reitan RM (1958) Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills 8:271–276CrossRef

41.

Nikolai T, Stepankova H, Michalec J, Bezdicek O, Horakova K, Markova H, Ruzicka E, Kopecek M (2015) Testy verbální fluence, česká normativní studie pro osoby vyššího věku. Cesk Slov Neurol 78/111(3):292–299CrossRef

42.

Benton AL, Hamsher K, Varney NR, Spreen O (1983) Contributions to neuropsychological assessment: a clinical manual. Oxford, New York

43.

Loring DW, Lowenstein DH, Barbaro NM, Fureman BE, Odenkirchen J, Jacobs MP, Austin JK, Dlugos DJ, French JA, Gaillard WD, Hermann BP, Hesdorffer DC, Roper SN, Van Cott AC, Grinnon S, Stout A (2011) Common data elements in epilepsy research: development and implementation of the NINDS epilepsy CDE project. Epilepsia 52(6):1186–1191. doi:10.1111/j.1528-1167.2011.03018 CrossRefPubMedPubMedCentral

44.

Weintraub S, Salmon D, Mercaldo N, Ferris S, Graff-Radford NR, Chui H, Cummings J, DeCarli C, Foster NL, Galasko D, Peskind E, Dietrich W, Beekly DL, Kukull WA, Morris JC (2009) The Alzheimer’s Disease Centers’ Uniform Data Set (UDS): the neuropsychologic test battery. Alzheimer Dis Assoc Disord 23(2):91–101. doi:10.1097/WAD.0b013e318191c7dd CrossRefPubMedPubMedCentral

45.

Beck AT, Beamesderfer A (1974) Assessment of depression: the depression inventory. Modern Probl Pharmacopsychiatry 7:151–169CrossRef

46.

Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 56(6):893–897CrossRefPubMed

47.

Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256(3):183–194. doi:10.1111/j.1365-2796.2004.01388.x CrossRefPubMed

48.

Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, De Stefano N (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17(1):479–489CrossRefPubMed

49.

Battaglini M, Jenkinson M, De Stefano N (2012) Evaluating and reducing the impact of white matter lesions on brain volume measurements. Hum Brain Mapp 33(9):2062–2071. doi:10.1002/hbm.21344 CrossRefPubMed

50.

Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397. doi:10.1016/j.neuroimage.2014.01.060 CrossRefPubMedPubMedCentral

51.

Filippi M, Horsfield MA, Morrissey SP, MacManus DG, Rudge P, McDonald WI, Miller DH (1994) Quantitative brain MRI lesion load predicts the course of clinically isolated syndromes suggestive of multiple sclerosis. Neurology 44(4):635–641CrossRefPubMed

52.

Henry RG, Shieh M, Okuda DT, Evangelista A, Gorno-Tempini ML, Pelletier D (2008) Regional grey matter atrophy in clinically isolated syndromes at presentation. J Neurol Neurosurg Psychiatry 79(11):1236–1244. doi:10.1136/jnnp.2007.134825 CrossRefPubMedPubMedCentral

53.

Bergsland N, Horakova D, Dwyer MG, Dolezal O, Seidl ZK, Vaneckova M, Krasensky J, Havrdova E, Zivadinov R (2012) Subcortical and cortical gray matter atrophy in a large sample of patients with clinically isolated syndrome and early relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol 33(8):1573–1578. doi:10.3174/ajnr.A3086 CrossRefPubMed

54.

Shiee N, Bazin PL, Zackowski KM, Farrell SK, Harrison DM, Newsome SD, Ratchford JN, Caffo BS, Calabresi PA, Pham DL, Reich DS (2012) Revisiting brain atrophy and its relationship to disability in multiple sclerosis. PLoS One 7(5):e37049. doi:10.1371/journal.pone.0037049 CrossRefPubMedPubMedCentral

55.

Sumowski JF, Leavitt VM (2013) Cognitive reserve in multiple sclerosis. Mult Scler 19(9):1122–1127. doi:10.1177/1352458513498834 CrossRefPubMed

56.

Penner IK, Stemper B, Calabrese P, Freedman MS, Polman CH, Edan G, Hartung HP, Miller DH, Montalban X, Barkhof F, Pleimes D, Lanius V, Pohl C, Kappos L, Sandbrink R (2012) Effects of interferon beta-1b on cognitive performance in patients with a first event suggestive of multiple sclerosis. Mult Scler 18(10):1466–1471. doi:10.1177/1352458512442438 CrossRefPubMedPubMedCentral

57.

Vaneckova M, Kalincik T, Krasensky J, Horakova D, Havrdova E, Hrebikova T, Seidl Z (2012) Corpus callosum atrophy–a simple predictor of multiple sclerosis progression: a longitudinal 9-year study. Eur Neurol 68(1):23–27. doi:10.1159/000337683 CrossRefPubMed

58.

Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM (2000) Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain 123(Pt 9):1845–1849CrossRefPubMed

59.

Granberg T, Martola J, Bergendal G, Shams S, Damangir S, Aspelin P, Fredrikson S, Kristoffersen-Wiberg M (2015) Corpus callosum atrophy is strongly associated with cognitive impairment in multiple sclerosis: results of a 17-year longitudinal study. Mult Scler 21(9):1151–1158. doi:10.1177/1352458514560928 CrossRefPubMed

60.

Kearney H, Rocca MA, Valsasina P, Balk L, Sastre-Garriga J, Reinhardt J, Ruggieri S, Rovira A, Stippich C, Kappos L, Sprenger T, Tortorella P, Rovaris M, Gasperini C, Montalban X, Geurts JJ, Polman CH, Barkhof F, Filippi M, Altmann DR, Ciccarelli O, Miller DH, Chard DT (2014) Magnetic resonance imaging correlates of physical disability in relapse onset multiple sclerosis of long disease duration. Mult Scler 20(1):72–80. doi:10.1177/1352458513492245 CrossRefPubMedPubMedCentral

61.

Krámská L (2014) Hodnocení premorbidního intelektu v neuropsychologii: český test čtení slov. Czech reading test (CRT). Propsyco

Titel: Cognitive impairment and structural brain changes in patients with clinically isolated syndrome at high risk for multiple sclerosis
verfasst von: Eva Hynčicová
Martin Vyhnálek
Adam Kalina
Lukáš Martinkovič
Tomáš Nikolai
Jiří Lisý
Jakub Hort
Eva Meluzínová
Jan Laczó
Publikationsdatum: 27.12.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Journal of Neurology / Ausgabe 3/2017
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-016-8368-9

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