Characterizing cognitive deficits and potential predictors in multiple sclerosis: A large nationwide study applying Brief International Cognitive Assessment for Multiple Sclerosis in standard clinical care.


Journal

Journal of neuropsychology
ISSN: 1748-6653
Titre abrégé: J Neuropsychol
Pays: England
ID NLM: 101468753

Informations de publication

Date de publication:
09 2020
Historique:
received: 15 04 2019
revised: 10 01 2020
pubmed: 15 2 2020
medline: 6 10 2021
entrez: 15 2 2020
Statut: ppublish

Résumé

With the proposal of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) battery, the need to screen for cognitive deficits within standard clinical care of patients with multiple sclerosis (MS) has been acknowledged. Data regarding how patient characteristics might predict low cognitive performance and therefore require particularly close monitoring is, however, limited so far. We investigated a large, nationwide patient cohort from ambulatory settings, representing the typical distribution of different subtypes, levels of physical disability, and disease durations. Besides cognitive testing with BICAMS, additional sampling of multiple demographics and clinical variables allowed us to characterize general and domain-specific prevalence patterns of cognitive impairment (CI) as well as to delineate which factors are associated with cognitive performance. In a total of 1,094 patients, CI was present in 28% (using a conservative cut-off of the 5th percentile below normative values), with information-processing speed being most frequently affected. Impairment was overall higher in patients with primary progressive (PPMS) and secondary progressive MS than in patients with relapsing-remitting (RR)MS. Regression modelling revealed that disease subtype (i.e., PPMS), long disease duration, high physical disability, unemployment, low educational level, high age, male sex, and the absence of current disease-modifying treatment were important predictors for worse BICAMS' test performance. These results emphasize the importance of continuous cognitive assessment during regular neurological follow-up visits, with a particular focus on patients being identified as high-risk subjects for CI according to the reported factors.

Identifiants

pubmed: 32056386
doi: 10.1111/jnp.12202
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

347-369

Informations de copyright

© 2020 The British Psychological Society.

Références

Achiron, A., Chapman, J., Magalashvili, D., Dolev, M., Lavie, M., Bercovich, E., … Barak, Y. (2013). Modeling of cognitive impairment by disease duration in multiple sclerosis: A cross-sectional study. PLoS ONE, 8, e71058. https://doi.org/10.1371/journal.pone.0071058
Amato, M. P., Ponziani, G., Siracusa, G., & Sorbi, S. (2001). Cognitive dysfunction in early-onset multiple sclerosis: A reappraisal after 10 years. Archives of Neurology, 58, 1602-1606. https://doi.org/10.1001/archneur.58.10.1602
Amato, M. P., Portaccio, E., Goretti, B., Zipoli, V., Iudice, A., Della Pina, D., … De Stefano, N. (2010). Relevance of cognitive deterioration in early relapsing-remitting MS: A 3-year follow-up study. Multiple Sclerosis Journal, 16, 1474-1482. https://doi.org/10.1177/1352458510380089
Amato, M. P., Zipoli, V., & Portaccio, E. (2006). Multiple sclerosis-related cognitive changes: A review of cross-sectional and longitudinal studies. Journal of the Neurological Sciences, 245, 41-46. https://doi.org/10.1016/j.jns.2005.08.019
Beatty, W. W., Blanco, C. R., Wilbanks, S. L., Paul, R. H., & Hames, K. A. (1995). Demographic, clinical, and cognitive characteristics of multiple sclerosis patients who continue to work. Journal of Neurorehabilitation and Neural Repair, 9, 167-173. https://doi.org/10.1177/154596839500900306
Benedict, R. H. B. (1997). Brief visuospatial memory test-revised: Professional manual. Odessa, FL: Psychological Assessment Resources.
Benedict, R. H., DeLuca, J., Phillips, G., LaRocca, N., Hudson, L. D., & Rudick, R., Multiple Sclerosis Outcome Assessments Consortium. (2017). Validity of the symbol digit modalities test as a cognition performance outcome measure for multiple sclerosis. Multiple Sclerosis Journal, 23, 721-733. https://doi.org/10.1177/1352458517690821
Benedict, R. H. B., & Zivadinov, R. (2011). Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nature Reviews Neurology, 7, 332-342. https://doi.org/10.1038/nrneurol.2011.61
Bergendal, G., Fredrikson, S., & Almkvist, O. (2007). Selective decline in information processing in subgroups of multiple sclerosis: An 8-year longitudinal study. European Neurology, 57, 193-202. https://doi.org/10.1159/000099158
Blum, D., Yonelinas, A. P., Luks, T., Newitt, D., Oh, J., Lu, Y., … Pelletier, D. (2002). Dissociating perceptual and conceptual implicit memory in multiple sclerosis patients. Brain and Cognition, 50(1), 51-61. https://doi.org/10.1016/S0278-2626(02)00009-X
Bobholz, J. A., & Rao, S. M. (2003). Cognitive dysfunction in multiple sclerosis: a review of recent developments. Current Opinion in Neurology, 16, 283-288. https://doi.org/10.1097/01.wco.0000073928.19076.84
Borghi, M., Cavallo, M., Carletto, S., Ostacoli, L., Zuffranieri, M., Picci, R. L., … Malucchi, S. (2013). Presence and significant determinants of cognitive impairment in a large sample of patients with multiple sclerosis. PLoS ONE, 8, e69820. https://doi.org/10.1371/journal.pone.0069820
Brochet, B., & Ruet, A. (2019). Cognitive impairment in multiple sclerosis with regards to disease duration and clinical phenotypes. Frontiers in Neurology, 10, 261. https://doi.org/10.3389/fneur.2019.00261
Chiaravalloti, N. D., & Deluca, J. (2008). Cognitive impairment in multiple sclerosis. The Lancet Neurology, 7, 1139-1151. https://doi.org/10.1016/S1474-4422(08)70259-X
Corfield, F., & Langdon, D. (2018). A systematic review and meta-analysis of the brief cognitive assessment for multiple sclerosis (BICAMS). Neurology and Therapy, 72, 287-306. https://doi.org/10.1007/s40120-018-0102-3
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California Verbal Learning Test (CVLT-II) adult version: Manual (2nd ed.). San Antonio, TX: Psychological Corporation.
Denney, D. R., Lynch, S. G., & Parmenter, B. A. (2008). A 3-year longitudinal study of cognitive impairment in patients with primary progressive multiple sclerosis: Speed matters. Journal of the Neurological Sciences, 267, 129-136. https://doi.org/10.1016/j.jns.2007.10.007
Denney, D. R., Lynch, S. G., Parmenter, B. A., & Horne, N. (2004). Cognitive impairment in relapsing and primary progressive multiple sclerosis: Mostly a matter of speed. Journal of the International Neuropsychological Society, 10, 948-956. https://doi.org/10.1017/S1355617704107030
Denney, D. R., Sworowski, L. A., & Lynch, S. G. (2005). Cognitive impairment in three subtypes of multiple sclerosis. Archives of Clinical Neuropsychology, 20, 967-981. https://doi.org/10.1016/j.acn.2005.04.012
Dusankova, J. B., Kalincik, T., Havrdova, E., & Benedict, R. H. B. (2012). Cross cultural validation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). Clinical Neuropsychologist, 26, 1186-1200. https://doi.org/10.1080/13854046.2012.725101
Filser, M., Schreiber, H., Pöttgen, J., Ullrich, S., Lang, M., & Penner, I.-K. (2018). The Brief International Cognitive Assessment in Multiple Sclerosis (BICAMS): Results from the German validation study. Journal of Neurology, 265(1), 2587-2593. https://doi.org/10.1007/s00415-018-9034-1.
Fischer, M., Bublak, P., Faiss, J. H., Hoffmann, F., Sailer, M., Schwab, M., … Köhler, W. (2014). How reliable is the classification of cognitive impairment across different criteria in early and late stages of multiple sclerosis? Journal of the Neurological Sciences, 343, 91-99. https://doi.org/10.1016/j.jns.2014.05.042
Flachenecker, P., Kobelt, G., Berg, J., Capsa, D., Gannedahl, M., & The European Multiple Sclerosis Platform. (2017). New insights into the burden and costs of multiple sclerosis in Europe: Results for Germany. Multiple Sclerosis Journal, 23(2_Suppl), 78-90. https://doi.org/10.1177/1352458517708141
Gaudino, E. A., Chiaravalloti, N. D., DeLuca, J., & Diamond, B. J. (2001). A comparison of memory performance in relapsing-remitting primary progressive and secondary progressive, multiple sclerosis. Neuropsychiatry, Neuropsychology and Behavioral Neurology, 14(1), 32-44.
Ghaffar, O., Fiati, M., & Feinstein, A. (2012). Occupational attainment as a marker of cognitive reserve in multiple sclerosis. PLoS ONE, 7, e47206. https://doi.org/10.1371/journal.pone.0047206
Goretti, B., Niccolai, C., Hakiki, B., Sturchio, A., Falautano, M., Minacapelli, E., … Amato, M. P. (2014). The brief international cognitive assessment for multiple sclerosis (BICAMS): Normative values with gender, age and education corrections in the Italian population. BMC Neurology, 14(1), 171. https://doi.org/10.1186/s12883-014-0171-6
Helmstaedter, C., Lendt, M., & Lux, S. (2001). VLMT - Verbaler Lern-und Merkfähigkeitstest. Manual (1st ed.). Göttingen, Germany: Hogrefe Verlag.
Honarmand, K., Akbar, N., Kou, N., & Feinstein, A. (2011). Predicting employment status in multiple sclerosis patients: The utility of the MS functional composite. Journal of Neurology, 258, 244-249. https://doi.org/10.1007/s00415-010-5736-8
Huijbregts, S. C. J., Kalkers, N. F., de Sonneville, L. M. J., de Groot, V., & Polman, C. H. (2006). Cognitive impairment and decline in different MS subtypes. Journal of the Neurological Sciences, 245, 187-194. https://doi.org/10.1016/j.jns.2005.07.018
Huijbregts, S. C. J., Kalkers, N. F., de Sonneville, L. M. J., de Groot, V., Reuling, I. E. W., & Polman, C. H. (2004). Differences in cognitive impairment of relapsing remitting, secondary, and primary progressive MS. Neurology, 63, 335-339. https://doi.org/10.1212/01.WNL.0000129828.03714.90
Johnen, A., Bürkner, P. C., Landmeyer, N. C., Ambrosius, B., Calabrese, P., Motte, J., … Ziemann, U. (2019). Can we predict cognitive decline after initial diagnosis of multiple sclerosis? Results from the German National early MS cohort (KKNMS). Journal of Neurology, 266, 386-397. https://doi.org/10.1007/s00415-018-9142-y
Johnen, A., Landmeyer, N. C., Bürkner, P. C., Wiendl, H., Meuth, S. G., & Holling, H. (2017). Distinct cognitive impairments in different disease courses of multiple sclerosis - A systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews, 83, 568-578. https://doi.org/10.1016/j.neubiorev.2017.09.005
Kobelt, G., Thompson, A., Berg, J., Gannedahl, M., Eriksson, J., Group, M. S., & Plattform, E. M. S. (2017). New insights into the burden and costs of multiple sclerosis in Europe. Multiple Sclerosis Journal, 23, 1123-1136. https://doi.org/10.1177/1352458517708125
Köhler, W., Fischer, M., Bublak, P., Faiss, J. H., Hoffmann, F., Kunkel, A., … Penner, I. K. (2017). Information processing deficits as a driving force for memory impairment in MS: A cross-sectional study of memory functions and MRI in early and late stage MS. Multiple Sclerosis and Related Disorders, 18, 119-127. https://doi.org/10.1016/j.msard.2017.09.026
Langdon, D. W. (2011). Cognition in multiple sclerosis. Current Opinion in Neurology, 24, 244-249. https://doi.org/10.1097/WCO.0b013e328346a43b
Langdon, D., Amato, M., Boringa, J., Brochet, B., Foley, F., Fredrikson, S., … Benedict, R. (2012). Recommendations for a Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS). Multiple Sclerosis Journal, 18, 891-898. https://doi.org/10.1177/1352458511431076
Leclercq, E., Cabaret, M., Guilbert, A., Jougleux, C., Vermersch, P., & Moroni, C. (2014). The influence of age and illness duration on cognitive impairment in aging patients with relapsing-remitting multiple sclerosis (RR-MS). Geriatrie et Psychologie Neuropsychiatrie Du Vieillissement, 12, 331-338. https://doi.org/10.1684/pnv.2014.0482
Matias-Guiu, J. A., Cortés-Martínez, A., Valles-Salgado, M., Oreja-Guevara, C., Pytel, V., Montero, P., … Matias-Guiu, J. (2017). Functional components of cognitive impairment in multiple sclerosis: A cross-sectional investigation. Frontiers in Neurology, 8, 643. https://doi.org/10.3389/fneur.2017.00643
Morrow, S. A., Kaushik, T., Zarevics, P., Erlanger, D., Bear, M. F., Munschauer, F. E., & Benedict, R. H. B. (2009). The effects of l-amphetamine sulfate on cognition in MS patients: results of a randomized controlled trial. Journal of Neurology, 256, 1095-1102. https://doi.org/10.1007/s00415-009-5074-x
Morrow, S. A., Rosehart, H., & Pantazopoulos, K. (2015). Anxiety and depressive symptoms are associated with worse performance on objective cognitive tests in MS. The Journal of Neuropsychiatry and Clinical Neurosciences, 28, 118-123. https://doi.org/10.1176/appi.neuropsych.15070167
Ozakbas, S., Turkoglu, R., Tamam, Y., Terzi, M., Taskapilioglu, O., Yucesan, C., … Turkes, N. (2018). Prevalence of and risk factors for cognitive impairment in patients with relapsing-remitting multiple sclerosis: Multi-center, controlled trial. Multiple Sclerosis and Related Disorders, 22, 70-76. https://doi.org/10.1016/j.msard.2018.03.009
Patti, F. (2009). Cognitive impairment in multiple sclerosis. Multiple Sclerosis Journal, 15(1), 2-8. https://doi.org/10.1177/1352458508096684
Patti, F., Amato, M. P., Trojano, M., Bastianello, S., Tola, M. R., Goretti, B., … Luccichenti, G. (2009). Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis (COGIMUS) study. Multiple Sclerosis, 15, 779-788. https://doi.org/10.1177/1352458509105544
Pinter, D., Sumowski, J., DeLuca, J., Fazekas, F., Pichler, A., Khalil, M., … Enzinger, C. (2014). Higher education moderates the effect of T2 lesion load and third ventricle width on cognition in multiple sclerosis. PLoS ONE, 9(1), e87567. https://doi.org/10.1371/journal.pone.0087567
Planche, V., Gibelin, M., Cregut, D., Pereira, B., & Clavelou, P. (2016). Cognitive impairment in a population-based study of patients with multiple sclerosis: differences between late relapsing-remitting, secondary progressive and primary progressive multiple sclerosis. European Journal of Neurology, 23, 282-289. https://doi.org/10.1111/ene.12715
Polman, C. H., Reingold, S. C., Banwell, B., Clanet, M., Cohen, J. A., Filippi, M., … Wolinsky, J. S. (2011). Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Annals of Neurology, 69, 292-302. https://doi.org/10.1002/ana.22366
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. Journal of the Neurological Sciences, 267, 100-106. https://doi.org/10.1016/j.jns.2007.10.002
Prakash, R. S., Snook, E. M., Lewis, J. M., Motl, R. W., & Kramer, A. F. (2008). Cognitive impairments in relapsing-remitting multiple sclerosis: A meta-analysis. Multiple Sclerosis, 14, 1250-1261. https://doi.org/10.1177/1352458508095004
Reynolds, R., Roncaroli, F., Nicholas, R., Radotra, B., Gveric, D., & Howell, O. (2011). The neuropathological basis of clinical progression in multiple sclerosis. Acta Neuropathologica, 122, 155-170. https://doi.org/10.1007/s00401-011-0840-0
Rimkus, C. M., Avolio, I. M. B., Miotto, E. C., Pereira, S. A., Mendes, M. F., Callegaro, D., & Leite, C. D. C. (2018). The protective effects of high-education levels on cognition in different stages of multiple sclerosis. Multiple Sclerosis and Related Disorders, 22, 41-48. https://doi.org/10.1016/j.msard.2018.03.001
Roy, S., Benedict, R. H. B., Drake, A. S., & Weinstock-Guttman, B. (2016). Impact of pharmacotherapy on cognitive dysfunction in patients with multiple sclerosis. CNS Drugs, 30, 209-225. https://doi.org/10.1007/s40263-016-0319-6
Ruano, L., Portaccio, E., Goretti, B., Niccolai, C., Severo, M., Patti, F., … Amato, M. P. (2017). Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Multiple Sclerosis Journal, 23, 1258-1267. https://doi.org/10.1177/1352458516674367
Ruet, A., & Brochet, B. (2018). Cognitive assessment in patients with multiple sclerosis: From neuropsychological batteries to ecological tools. Annals of Physical and Rehabilitation Medicine, in press. https://doi.org/10.1016/j.rehab.2018.01.006
Ruet, A., Deloire, M., Charre-Morin, J., Hamel, D., & Brochet, B. (2013). Cognitive impairment differs between primary progressive and relapsing-remitting MS. Neurology, 80, 1501-1508. https://doi.org/10.1212/WNL.0b013e31828cf82f
Salter, A., Thomas, N., Tyry, T., Cutter, G., & Marrie, R. A. (2017). Employment and absenteeism in working-age persons with multiple sclerosis. Journal of Medical Economics, 20, 493-502. https://doi.org/10.1080/13696998.2016.1277229
Scherer, P., Baum, K., Bauer, H., Göhler, H., & Miltenburger, C. (2004). Normierung der Brief Repeatable Battery of Neuropsychological tests (BRB-N) für den deutschsprachigen Raum. Anwendung bei schubförmig remittierenden und sekundär progredienten Multiple-Sklerose-Patienten. Nervenarzt, 75, 984-990. https://doi.org/10.1007/s00115-004-1729-0
Schmidt, M. (1996). Rey auditory verbal learning test: A handbook. Los Angeles, CA: Western Psychological Services.
Schoonheim, M. M., Meijer, K. A., & Geurts, J. J. G. (2015). Network collapse and cognitive impairment in multiple sclerosis. Frontiers in Neurology, 6, 82. https://doi.org/10.3389/fneur.2015.00082
Schoonheim, M. M., Vigeveno, R. M., Lopes, F. C. R., Pouwels, P. J. W., Polman, C. H., Barkhof, F., & Geurts, J. J. G. (2014). Sex-specific extent and severity of white matter damage in multiple sclerosis: Implications for cognitive decline. Human Brain Mapping, 35, 2348-2358. https://doi.org/10.1002/hbm.22332
Smestad, C., Sandvik, L., Landrø, N. I., & Celius, E. G. (2010). Cognitive impairment after three decades of multiple sclerosis. European Journal of Neurology, 17, 499-505. https://doi.org/10.1111/j.1468-1331.2009.02889.x
Smith, A. (1982). Symbol digit modalities test (SDMT) manual (revised). Los Angeles, CA: Western Psychological Services.
Strober, L., Englert, J., Munschauer, F., Weinstock-Guttman, B., Rao, S., & Benedict, R. H. B. (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. Multiple Sclerosis, 15, 1077-1084. https://doi.org/10.1177/1352458509106615
Strober, L. B., Rao, S. M., Lee, J. C., Fischer, E., & Rudick, R. (2014). Cognitive impairment in multiple sclerosis: An 18 year follow-up study. Multiple Sclerosis and Related Disorders, 3, 473-481. https://doi.org/10.1016/j.msard.2014.03.004
Sumowski, J. F., Benedict, R., Enzinger, C., Filippi, M., Geurts, J. J., Hamalainen, P., … Rao, S. (2018). Cognition in multiple sclerosis: State of the field and priorities for the future. Neurology, 90, 278-288. https://doi.org/10.1212/WNL.0000000000004977
Torkildsen, O., Myhr, K. M., & Bø, L. (2016). Disease-modifying treatments for multiple sclerosis - a review of approved medications. European Journal of Neurology, 23, 18-27. https://doi.org/10.1111/ene.12883
van Hooren, S. A. H., Valentijn, A. M., Bosma, H., Ponds, R. W. H. M., van Boxtel, M. P. J., & Jolles, J. (2007). Cognitive functioning in healthy older adults aged 64-81: A cohort study into the effects of age, sex, and education. Aging, Neuropsychology, and Cognition, 14(1), 40-54. https://doi.org/10.1080/138255890969483

Auteurs

Alina Renner (A)

Cogito Center for Applied Neurocognition and Neuropsychological Research, Düsseldorf, Germany.

Sharon J Baetge (SJ)

Cogito Center for Applied Neurocognition and Neuropsychological Research, Düsseldorf, Germany.

Melanie Filser (M)

Cogito Center for Applied Neurocognition and Neuropsychological Research, Düsseldorf, Germany.

Sebastian Ullrich (S)

.05 Statistikberatung, Düsseldorf, Germany.

Christoph Lassek (C)

Neurological Group Practice, Kassel, Vellmar, Germany.

Iris-Katharina Penner (IK)

Cogito Center for Applied Neurocognition and Neuropsychological Research, Düsseldorf, Germany.
Department of Neurology, Medical Faculty, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany.

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