Education protects against cognitive changes associated with multiple sclerosis

Restorative Neurology and Neuroscience

Volumn 31, Issue 5, 2013, Pages 619-631

  Scarpazza, C ^a,b   Braghittoni, D ^a,b   Casale, B ^a,b   Malagu S ^c   Mattioli, F ^d   Di Pellegrino, G ^a,b   Ladavas, E ^a,b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c BUFALINI HOSPITAL   (Italy)

^d Neuropsychology Unit   (Italy)

Author keywords

cognitive reserve; education; Multiple sclerosis

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; COGNITIVE RESERVE; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPANDED DISABILITY STATUS SCALE; FATIGUE; FEMALE; HEALTH EDUCATION; HUMAN; INFORMATION PROCESSING; MALE; MULTIPLE SCLEROSIS; OCCUPATION; PRIORITY JOURNAL;

ADULT; COGNITION DISORDERS; COGNITIVE RESERVE; EDUCATIONAL STATUS; FEMALE; HUMANS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE;

EID: 84883852931     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-120261     Document Type: Article

References (70)

1. Andel, R., Vigen, C., Mack, W.J., Clark, L.J. & Gatz, M.(2006 The effect of education and occupational complexity on rate of cognitive decline in Alzheimer's patients. J Int Neuropsychol Soc, 12(1), 147-52
2. Amato, M.P., Ponziani, G., Rossi, F., Liedl, C.L., Stefanile, C., & Rossi, L. (2001). Quality of life in multiple sclerosis: The impact of depression, fatigue and disability. Mult Scler, 7, 340-344
3. Amato, M.P., Zipoli, V., & Portaccio, E. (2006). Multiple sclerosis related cognitive changes: A review of cross-sectional and longitudinal studies. J Neurol Sci, 245, 41-46
4. Amato, M.P., Portaccio, E., Goretti, B., Zipoli, V., Battaglini, M., Bartolozzi, M.L., Stromilla, M.L., 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
5. Bakshi, R. (2003). Fatigue associated with multiple sclerosis: Diagnosis, impact and management. Mult Scler, 9, 219-227
6. Bakshi, R., Shaikh, Z.A., Miletich, R.S., Czarnecki, D., Dmochowski, J., Henschel, K., Janardhan, V., Dubey, N., & Kinkel, P.R. (2000). Fatigue in multiple sclerosis and its relationship to depression and neurologic disability. Mult Scler, 6, 181-185
7. Beck, A.T., Ward, C., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Arch Gen Psychiatry, 4, 561-571
8. Benedict, R.H., Wahlig, E., & Bakshi, R. (2005). Predicting quality of life in multiple sclerosis: Accounting for physical disability, fatigue, cognition, mood disorder, personality, and behavior change. J Neurol Sci, 231, 29-34
9. Benedict, R.H.B., Bruce, J.M., Dwyer, M.G., Abdelrahman, M., Hussein, S.,Weinstock-Guttman, B., Garg, N., Munschauer, F., &Zivadinov, R. (2006). Neocortical Atrophy, ThirdVentricular Width, and Cognitive Dysfunction in Multiple Sclerosis. Arch Neurol, 63, 1301-1306
10. Benedict, R., Morrow, S., Weinstock-Guttman, B., Cookfair, D., & Schretlen, D.J. (2010). Cognitive reserve moderates decline in information processing speed in multiple sclerosis patients. J Int Neuropsychol Soc, 16, 829-835
11. Bergendal, G., Fredrikson, S., & Almkvist, O. (2007). Selective decline in information processing in subgroups of multiple sclerosis: An 8 year old longitudinal study. Eur Neurol, 57, 193-292
12. Bol, Y., Duits, A.A., Hupperts, R.M., Verlinden, I., & Verhey, F.R.J. (2010). The impact of fatigue on cognitive functioning in patients with multiple sclerosis. Clin Rehabil, 24, 854-862
13. Bonnet, M.C., Deloire, M.S.A., Salort, E., Dousset, V., Petry, K.G., Brochet, B.&AQUISEP study group. (2006). Evidence of cognitive compensation associated with educational level in early relapsing-remitting multiple sclerosis. J Neurol Sci, 251, 23-28
14. Boringa, J.B., Lazeron, R.H., Reuling, I.E.,Adér, H.J., Pfennings, L., Lindeboom, J., de Sonneville, L.M., Kalkers, N.F., & Polman, C.H. (2001). The brief repeatable battery of neuropsychological tests: Normative values allow application in multiple sclerosis clinical practice. Mult Scler, 7(4), 263-267
15. Brickman, A.M., Siedlecki, K.L., Muraskin, J., Manly, J.J., Luchsinger, J.A., Yeung, L.K., Brown, T.R., DeCarli, C., & Stern, Y. (2011). White matter hyperintesities and cognition: Testing the reserve hypothesis. Neurobioly (Aging), 32, 1588-1598
16. Calabrese, P. (2006). Neuropsychology of multiple sclerosis. An overview. J Neur, 253, S10-S15
17. Calabrese, M., Filippi, M., & Gallo, P. (2010). Cortial lesions in multiple sclerosis. Nat Rev Neurosci, 6, 438-444
18. Chiaravalloti, N.D., & DeLuca, J. (2008). Cognitive impairment in multiple sclerosis. Lancet Neurol, 7, 1139-1151
19. Ciaramelli, E., Serino, A., Benassi, M.G., & Bolzani, R. (2006 Standardizzazione di tre test di memoria di lavoro. Giornale italiano di psicologia. a. XXXIII, n. 2, 451-468
20. Christodoulou, C., Krupp, L.B., Liang, Z., Huang, W., Melville, P., Roque, C., Scherl, W.F., Morgen, T., MacAllister, W.S., Li, L., Tudorica, L.A., Li, X., Roche, P., & Peyster, R. (2003 Cognitive performance and MR markers of cerebral injury in cognitively impaired MS patients. Neurology, 60(11), 1793-1798
21. DeLuca, J., Johnson, S.K., & Natelson, B.H. (1993). Information processing efficiency in chronic fatigue syndrome and multiple sclerosis. Arch Neurol, 50, 301-304
22. DeLuca, J., Chelune, G.J., Tulsky, D.S., Lengerfelder, J. & Chairavalloti, N.D. (2004). Is speed processing deficit or working memory the primary information processing deficit in multiple sclerosis? J Clin ExpNeuropsyc, 26(4), 550-562
23. DeLuca, J. (2005). Fatigue, cognition and mental effort, De Luca J, In, pp. Ed. Fatigue as a window to the brain. Cambridge, MA, USA:MIT Press, 37-57
24. Demaree, H.A., DeLuca, J., Gaudino, E.A., & Diamond, J. (1999 Speed of information processing as a key deficit in multiple sclerosis: Implication for rehabilitation. J Neurol Neurosur Psyy, 67, 661-663
25. Duque, B., Sepulcre, J., Bejarano, B., Samarach, L., Pastor, P., & Villoslada, P. (2008). Memory decline evolves independently of disease activity in MS. Mult Sclers, 14, 947-953
26. Elkins, J.S., Longstreth, W.T., Manolio, T.A., Newman, A.B., Bhadelia, R.A., & Johnson, S.C. (2006). Education and the cognitive decline associated with MRI defined brain infarct. Neurology, 67, 435-440
27. Farmer, J.E., Kanne, S.M., Haunt, J.S., Williams, J., Johnstone, B., & Kirk, K. (2002). Memory functioning following traumatic brain injury in children with premorbid learning problems. Dev Neuropsychol, 22, 455-469
28. Flachenecker, P.,Kumpfel, T., Kallman, B., Gottschalk, M., Grauner, O., & Rieckam, P. (2002). Fatigue in multiple sclerosis: A comparison of different rating scales and correlation to clinical parameter. Mult Sclers, 8, 523-526
29. Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psy Res, 12(3), 189-198
30. Forn, C., Belenguer, A., Parcet-Ibars, M.A., & Avila, C. (2008 Information-processing speed is the primary deficit underlying the poor performance of multiple sclerosis in the Paced Auditory Serial Addition Test (PASAT). J Clin ExpNeuropsyc, 30(7), 789-796
31. Freitas, C., Perez, J., Knobel, M., Tormos, J.M., Oberman, L., Eldaief, M., Bashir, S.,Vernet, M., Peña-Ǵomez, C.,&Pascual-Leone, A. (2011). Changes in cortical plasticity across the lifespan. Front Aging Neurosci, 3, 1-8
32. Garibotto, V., Borroni, B., Kalbe, E., Herholz, K., Salmon, E., Holtoff, V., Sorbi, S., Cappa, S.F., Padovani, A., Fazio, F., & Perani, D. (2008). Education and occupation as proxies for reserve in aMCI converters and AD: FDG-PET evidence. Neurology, 71(17), 1342-1349
33. Grima, D.T., Torrance, G.W., Francis, G., Rice, G., Rosner, A.J., & Lafortune, L. (2000). Cost and health quality of life consequences of multiple sclerosis. Mult Sclers, 6, 91-98
34. Gronwall, D.M. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. PercePTMotor Skill, 44(2), 367-373
35. Jefferson, A.L., Gibbons, L.E., Rentz, D.M., Carvalho, J.O., Manly, J., Bennett, D.A., & Jones, R.N. (2011). A life course model of cognitive activities, socioeconomic status, education, reading ability, and cognition. J Amn Ger Soc, 59(8), 1403-1411
36. Katzman, R., Terry, R., DeTeresa, R., Brown, T., Davies, P., Fuld, P., Renbing, X.,&Peck, A. (1988). Clinical, pathological and neurochemical changes in dementia: A subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol, 23(2), 138-144
37. Krupp, L.B.&Elkins, L.E. (2009). Fatigue and declines in cognitive functioning in multiple sclerosis. Neurology, 55, 934-939
38. Kurtzke, J.F. (1983). Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology, 33(11), 1444-14452
39. Landro, N.I., Gulowsen-Celius, E., & Sletvold, H. (2004). Depressive symptoms account for deficit information processing speed but not for impaired working memory in early phase multiple sclerosis. J Neurol Sci, 217, 211-216
40. Lazeron, R.H.C., Rombouts, A.S.R.B., Scheltens, P., Polman, C.H., & Barkhof, F. (2004). A fMRI study of planning related brain activity in patients with moderately advanced multiple sclerosis. Mult Scler, 10, 549-555
41. McCarthy, M., Beaumont, J.G., Thompson, R., & Peacock, S. (2005). Modality-specific aspects of sustained and divided attentional performance in multiple sclerosis. Arch clinneuropsychol, 20, 705-718
42. McDonald, W.I., Compston, A., Edan, G., Goodkin, D., Hartung, H.P., Lublin, F.D., McFarland, H.F., Paty, D.W., Polman, C.H., Reingold, S.C., Sandberg-Wollheim, M., Sibley, W., Thompson, A., Van Den Noort, S.,Weinshenker, B.Y.,&Wolinsky, J.S. (2001). Recommended diagnostic criteria for multiple sclerosis: Guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol, 50(1), 121-127
43. Morrow, S.A., Weinstock-Guttman, B., Munschauer, F.E., Hojnacki, D., & Benedict, R.H.B. (2009). Subjective fatigue is not associated with cognitive impairment in multiple sclerosis: Cross-sectional and longitudinal analysis. Mult Scler, 15, 998-1005
44. Mullaoglu, M., & Ostun, E(2008). Fatigue in multiple sclerosis. Review. J Clin Nurs, 18, 1231-1238
45. Parmenter, B.A., Denney, D.R. & Lynch, S.G. (2003). The cognitive performance of patients with multiple sclerosis during periods of high and low fatigue. Mult Scler, 9, 111-118
46. Nucci, M.,Mapelli, D.,&Mondini, S. (2011). The cognitive reserve questionnaire (CRIq):Anewinstrument for measuring the cognitive reserve. Aging Clin Exp Res, 24(3), 218-26
47. Parmenter, B.A., Shucard, J.L., Benedict, H.B., & Shucard, D.W. (2006). Working memory deficits in multiple sclerosis: Comparison between the n-back task and the Paced Auditory Serial Addition Test. J Int Neuropsychol Soc, 12, 667-687
48. Parmenter, B.A.,Weinstock-Guttman, B., Garg, N., Munschauer, F., &Benedict, R.H.B. (2007). Screening for cognitive impairment in multiple sclerosis using the Symbol Digit Modalities Test. Mult Scler, 13, 52-57
49. Polman, C.H., Reingold, S.C., Banwell, B., Clanet, M., Cohen, J.A., Filippi, M., Fujihara, K., Havrdova, E., Hutchinson, M., Kappos, L., Lublin, F.D., Montalban, X., O'Connor, P., Sandberg-Wollheim, M., Thompson, A.J., Waubant, E., Weinshenker, B., & Wolinsky, J.S. (2011). Diagnostic Criteria for Multiple Sclerosis: 2010 revisions to the McDonald Criteria. Ann Neurol, 69, 292-302
50. Portaccio, E., Amato, M.P., Bartolozzi, M.L., Zipoli,V.,Mortilla, M., Guidi, L., Siracusa, G., sorbi, S., Federico, A., & De Stefano, N. Neocortical volume decrease in relapsing-remitting multiple sclerosis with mild cognitive impairment. J Neurol Sci, 245, 195-199
51. Prakash, R.S., Snook, E.M., Lewis, J.M., Molt,R.W.,&Kramer, A.F. (2008). Cognitive impairments in relapsing remitting multiple sclerosis: A meta-analysis. Mult Scler, 14, 1250-1261
52. Rao, S.M. (1986). Neuropsychology of multiple sclerosis: A critical review. J Clin Exper Neuropsychol, 8, 503-542
53. Rao, S.M., Leo, G.J., Bernardin, L., & Unverzagt, F. (1991). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns and predictors. Neurology, 41(5), 685-691
54. Santiago, O., Guardia, J., Casado, O., Carmona, O., & Atbizu, T. (2007). Specifictity of frontal dysfunctions in relapsing remitting multiple sclerosis. Arch Clini Neuropsychol, 22, 623-629
55. Scarmeas, N., & Stern, Y. (2003). Cognitive reserve and lifestyle. J Clin Exp Neuropsyc, 25(5), 625-633
56. Schapiro, R. (2002). The pathophysiology of MS-related fatigue: What is the role of wake promotion? Int J MS care, 37-57
57. Sepulcre, J., Vanotti, S., Hernandez, R., Sandoval, G., Caceres, F., Garcea, O. & Villoslada, P. (2006). Cognitive imparment in patients with multiple sclerosis using the Brief Repeatable Battery Neuropsychology test. Mult Scler, 12, 187-195
58. Serino, A., Ciaramelli, E., Disantantonio, A., Malaǵu, S., Servadei, F.,&Ladavas, E. (2007). A pilot study for rehabilitation of central executive deficits after traumatic brain injury. Brain Injury, 21(1), 11-19
59. Staffen, W., Mair, A., Zauner, H., Unterrainer, J., Neiderthofer, H., Kutzelnigg, A., Ritter, S., Golaszewski, S., Iglseder, B., & Ladurner, G. (2002). Cognitive function and fMRI in patients with multiple sclerosis: Evidence for compensatory cortical activation during an attention task. Brain, 125, 1275-1282
60. Stern, Y., Gurland, B., Tatemichi, T.K., Tang, M.X., Wilder, D., & Mayeux, R. (1994). Influence of education and occupation on the incidence of Alzheimer's disease. JAMA, 271, 1004-1010
61. Stern, Y., Albert, S., Tang, M.X. & Tsai, W.Y. (1999). Rate of memory decline in AD is related to education and occupation: Cognitive reserve? Neurology, 53(9), 1942-197
62. Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc, 8(3), 448-460
63. Stern,Y. (2006). Cognitive reserve and Alzheimer's disease. Review. Alz Dis Assoc Dis, 20, 112-117
64. Stern, Y. (2009). Cognitive reserve. Reviews and prospective. Neuropsychologia, 47, 2015-2028
65. Sumowski, J.F., Chiaravalloti, N., & De Luca, J. (2009a). Cognitive reserve protects against cognitive dysfunction in multiple sclerosis. J Clin Exp Neuropsyc, 31(8), 913-926
66. Sumowski, J.F., Chiaravalloti, N.,Wylie, G. & De Luca, J. (2009b Cognitive reserve moderated the negative effect of brain atrophy on cognitive efficiency in multiple sclerosis. J IntNeuropsyc Soc, 15, 606-612
67. Sumowski, J.F., Wylie, G., Chiaravalloti, N., & DeLuca, J. (2010 Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: Functional magnetic resonance imaging evidence for cognitive reserve. Brain, 133, 362-374
68. Tellez, N., Rio, J., Tintoré, M., Nos, C., Galan, I., & Montalban, X. (2006). Fatigue in multiple sclerosis persists over time. A longitudinal study. J Neur, 253, 1466-1470
69. Tombaugh, T.N. (2006).Acomprehensive reviewof the Paced Auditory Serial Addition Test (PASAT). Arch Clin Neuropsychy, 21, 53-76
70. Zoccolotti, P., Pizzamiglio, L., Pittau, P.A., & Galati, G. (1994 Batteria di test per l'esame dell'attenzione. Roma PSYTEST; 1994