Abstract
Cognitive dysfunction is highly prevalent, disabling, and poorly managed in persons with multiple sclerosis (MS). However, not all persons with MS present with cognitive impairment despite having grey and white matter pathology. To explain such an observation, much attention has been drawn to other factors, namely the concept of reserve (i.e., protection against clinical manifestations of neurological damage). There is a growing body of evidence supporting brain reserve and cognitive reserve for mitigating the deleterious effects of MS pathology on cognition in MS. Measurement and maintenance of reserve is paramount. The current review addresses measures of brain and cognitive reserve, separately, that have been adopted in MS research. These measures are largely based on genetics and premorbid behavior. We propose that reserve may not be limited to premorbid factors that are not highly amenable to change. Rather, reserve can be built and maintained over time based on ongoing participation in cognitively stimulating activities. We conclude with recommendations for future research on reserve in MS samples. This will provide keen insight into potential applications for building reserve and ultimately improving the well-being of those with MS across multiple domains.
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References
Rao SM (1986) Neuropsychology of multiple sclerosis: a critical review. J Clin Exp Neuropsychol 8:503–542
Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139–1151
Amato MP, Zipoli V, Portaccio E (2006) Multiple sclerosis-related cognitive changes: a review of cross-sectional and longitudinal studies. J Neurol Sci 45:41–46
Arnett PA, Higginson CI, Randolph JJ (2001) Depression in multiple sclerosis: relationship to planning ability. J Int Neuropsychol Soc 7:665–674
Feinstein A, DeLuca J, Baune BT et al (2013) Cognitive and neuropsychiatric disease manifestations in MS. Mult Scler Relat Disord 2:4–12
Morrow SA, Drake A, Zivadinov R et al (2010) Predicting loss of employment over three years in multiple sclerosis: clinically meaningful cognitive decline. Clin Neuropsychol 24:1131–1145
Schultheis MT, Garay E, DeLuca J (2001) The influence of cognitive impairment on driving performance in multiple sclerosis. Neurology 56(8):1089–1094
Benedict RHB, Wahlig E, Bakshi R et al (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
Amato MP, Langdon D, Montalban X et al (2013) Treatment of cognitive impairment in multiple sclerosis: position paper. J Neurol 260:1452–1468
Chiaravalloti ND, Moore NB, Nikelshpur OM et al (2013) An RCT to treat learning impairment in multiple sclerosis: the MEMREHAB trial. Neurology 81:2066–2072
Schofield PW, Logroscino G, Andrews H et al (1997) An association between head circumference and Alzheimer’s disease in a population-based study of aging. Neurology 49:30–37
Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8:448–460
Stern Y (2009) Cognitive reserve. Neuropsychologia 47:2015–2028
Stern Y (2012) Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neruol 11:1006–1012
Sumowski JF, Chiravalloti N, DeLuca J (2009) Cognitive reserve protects against cognitive dysfunction in multiple sclerosis. J Clin Exp Neuropsychol 31(8):913–926
Benedict RHB, Morrow SA, Weinstock-Guttman B et al (2010) Cognitive reserve moderates decline in information processing speed in multiple sclerosis patients. J Int Neuropsychol Soc 16:829–835
Sumowski JF, Leavitt VM (2013) Cognitive reserve in multiple sclerosis. Mult Scler 19(9):1122–1127
Sumowski JF (2015) Cognitive reserve as a useful concept for early intervention research in multiple sclerosis. Front Neurol 6(176):1–5
Satz P (1993) Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology 7:273–295
Sumowski JF, Rocca MA, Leavitt VM et al (2013) Brain reserve and cognitive reserve in multiple sclerosis: what you’ve got and how you use it. Neurology 80:2186–2193
Sumowski JF, Rocca MA, Leavitt VM et al (2014) Brain Reserve and cognitive Reserve protect against cognitive decline over 4.5 years in MS. Neurology 82:1776–1783
Modica CM, Bergsland N, Dwyer MG et al (2016) Cognitive reserve moderates the impact of subcortical gray matter atrophy on neuropsychological status in multiple sclerosis. Mult Scler 22(1):36–42
Wallin MT, Page WF, Kurtzke JF (2000) Epidemiology of multiple sclerosis in US veterans VIII. Long-term survival after onset of multiple sclerosis. Brain 123:1677–1687
Bonnet MC, Deloire MSA, Salort E et al (2006) Evidence of cognitive compensation associated with educational level in early relapsing-remitting multiple sclerosis. J Neurol Sci 251:23–28
Pinter D, Sumowski J, DeLuca J et al (2014) Higher education moderates the effect of T2 lesion load and third ventricle width on cognition in multiple sclerosis. PLoS One 9(1):e87567
Martins Da Silva A, Cavaco S, Moreira I et al (2015) Cognitive reserve in multiple sclerosis: protective effects of education. Mult Scler 21(10):1312–1321
Lezak MD (2004) Neuropsychological assessment, 4th edn. Oxford University Press, New York
Wilkinson GS (1993) The Wide Range Achievement Test administration manual. Wide Range, Wilmington, DE
Sumowski JF, Chiaravalloti N, Wylie G et al (2009) Cognitive reserve moderates the negative effect of brain atrophy on cognitive efficiency in multiple sclerosis. J Int Neuropsychol Soc 15:606–612
Sumowski JF, Wylie GR, Chiaravalloti N et al (2010) Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology 74:1942–1945
Wechsler D (1999) Wechsler abbreviated scale of intelligence. The Psychological Corporation, San Antonio
Smith A (1982) Symbol Digit Modalities Test: manual. Western Psychological Services, Los Angeles
Gronwall DMA (1977) Pace auditory serial addition task: a measure of recovery from concussion. Percept Motor Skills 44:367–373
Rao S (1991) A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. National Multiple Sclerosis Society, New York
Sumowski JF, Wylie GR, DeLuca J et al (2010) Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain 133:362–374
Chiaravalloti ND, Genova HM, DeLuca J (2015) Cognitive rehabilitation in multiple sclerosis: the role of plasticity. Front Neurol 6(67):1–10
Audoin B, Reuter F, Duong MVA et al (2008) Efficiency of cognitive control recruitment in the very early stage of multiple sclerosis: a one-year fMRI follow-up study. Mult Scler 14:786–792
Loitfelder M, Fazekas F, Koschutnig K et al (2014) Brain activity changes in cognitive networks in relapsing-remitting multiple sclerosis—insights from a longitudinal fMRI study. PLoS One 9(4):e93715
Weschler D (2008) Wechsler adult intelligence scale, 4th edn. Pearson, San Antonio
Sandry J, Sumowski JF (2014) Working memory mediates the relationship between intellectual enrichment and long-term memory in multiple sclerosis: an exploratory analysis of cognitive reserve. J Int Neuropsychol Soc 20:868–872
Scarmeas N, Levy G, Tang MX et al (2001) Influence of leisure activity on the incidence of Alzheimer’s disease. Neurology 57:2236–2242
Verghese J, Lipton RB, Katz MJ et al (2003) Leisure activities and the risk of dementia in the elderly. N Engl J Med 348:2508–2516
Sumowski JF, Wylie GR, Gonnella A et al (2010) Premorbid cognitive leisure independently contributes to cognitive reserve in multiple sclerosis. Neurology 75:1428–1431
Sumowski JF, Rocca MA, Leavitt VM et al (2015) Searching for the neural basis of reserve against memory decline: intellectual enrichment linked to larger hippocampal volume in multiple sclerosis. Eur J Neurol 0:1–6
Blair JR, Spreen O (1989) Predicting premorbid IQ: a revision of the National Adult Reading Test. Clin Neuropsychol 3:129–136
Friend KB, Grattan L (2000) Use of the North American Adult Reading Test to estimate premorbid intellectual function in patients with multiple sclerosis. J Clin Exp Neuropsychol 20:846–851
Sumowski JF, Chiaravalloti N, Leavitt VM et al (2012) Cognitive reserve in secondary progressive multiple sclerosis. Mult Scler 18(10):1454–1458
Ghaffar O, Fiati M, Feinstein A (2012) Occupational attainment as a marker of cognitive reserve in multiple sclerosis. PLoS One 7(10):e47206
United States Department of Labor (1991) Dictionary of occupational titles, 4th edn. Government Printing Office, Washington, DC
Scarpazza C, Braghittoni D, Casale B et al (2013) Education protects against cognitive changes associated with multiple sclerosis. Restor Neurol Neurosci 31:619–631
Amato MP, Razzolini L, Goretti B et al (2013) Cognitive reserve and cortical atrophy in multiple sclerosis: a longitudinal study. Neurology 80:1728–1733
Paterson DH, Warburton DE (2010) Physical activity and functional limitations in older adults: a systematic review related to Canada’s Physical Activity Guidelines. Int J Behav Nutr Phys Act 7:38
Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452
Motl RW, Dlugonski D, Pilutti L et al (2012) Premorbid physical activity predicts disability progression in relapsing-remitting multiple sclerosis. J Neurol Sci 323:123–127
Hadjimichael O, Kerns RB, Rizzo MA et al (2007) Persistent pain and uncomfortable sensations in persons with multiple sclerosis. Pain 127:35–41
Scarmeas N, Stern Y (2003) Cognitive reserve and lifestyle. J Clin Exp Neuropsychol 25(5):625–633
Schwartz CE, Ayandeh A, Ramanathan M et al (2015) Reserve-building activities in multiple sclerosis patients and healthy controls: a descriptive study. BMC Neurol 15:135–142
Schwartz CE, Snook E, Quaranto B et al (2013) Cognitive reserve and patient-reported outcomes in multiple sclerosis. Mult Scler 19(1):87–105
Schwartz CE, Quaranto BR, Healy BC et al (2013) Cognitive reserve and symptom experience in multiple sclerosis: a buffer to disability progression over time? Arch Phys Med Rehabil 94:1971–1981
Sole-Padulles C, Bartres-Faz D, Junque C et al (2009) Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 30:1114–1124
Alterman T, Grosch J, Chen X et al (2008) Examining associations between job characteristics and health: linking data from the Occupational Information Network (O*NET) to two US national health surveys. J Occup Environ Med 50:1401–1413
Godin G, Shephard RJ (1985) A simple method to assess exercise behaviour in the community. Can J Appl Sport Sci 10:141–146
Schwartz CE, Vollmer T, Lee H (1999) Reliability and validity of two self-report measures of impairment and disability for MS. North American Research Consortium on Multiple Sclerosis Outcomes Study Group. Neurology 52:63–70
Sullivan JJL, Edgley K, Dehoux E (1990) A survey of multiple sclerosis. Part 1: perceived cognitive problems and compensatory strategy use. Can J Rehabil 4:99–105
Schwartz CE, Bode RK, Quaranto BR et al (2012) The Symptom Inventory disability-specific short-forms for multiple sclerosis: construct validity, responsiveness, and interpretation. Arch Phys Med Rehabil 93:1617–1628
Schwartz CE, Bode RK, Vollmer T (2012) The Symptom Inventory disability-specific short-forms for multiple sclerosis: reliability and factor structure. Arch Phys Med Rehabil 93:1629–1636
Amato MP, Goretti B, Ghezzi A et al (2008) Cognitive and psychosocial features of childhood and juvenile MS. Neurology 70(20):1891–1897
Pasto L, Portaccio E, Goretti B et al (2016) The cognitive reserve theory in the setting of pediatric-onset multiple sclerosis. Mult Scler. doi:10.1177/1352458516629559
Motl RW, Sandroff BM, DeLuca J (2016) Exercise training and cognitive rehabilitation: a symbiotic approach for rehabilitating walking and cognitive functions in multiple sclerosis? Neurorehabil Neural Repair. doi:10.1177/1545968315606993
Benedict RHB, Holtzer R, Motl RW et al (2011) Upper and lower extremity motor function and cognitive impairment in multiple sclerosis. J Int Neuropsychol Soc 17(4):643–653
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Sandroff, B.M., Schwartz, C.E. & DeLuca, J. Measurement and maintenance of reserve in multiple sclerosis. J Neurol 263, 2158–2169 (2016). https://doi.org/10.1007/s00415-016-8104-5
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DOI: https://doi.org/10.1007/s00415-016-8104-5