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Published in: BMC Neurology 1/2016

Open Access 01-12-2016 | Research article

Reserve-related activities and MRI metrics in multiple sclerosis patients and healthy controls: an observational study

Authors: Carolyn E. Schwartz, Michael G. Dwyer, Ralph Benedict, Bianca Weinstock-Guttman, Niels P. Bergsland, Jei Li, Murali Ramanathan, Robert Zivadinov

Published in: BMC Neurology | Issue 1/2016

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Abstract

Background

To examine whether past and current reserve-related activities make the brain less susceptible to MS pathology (i.e., lesions or disease-related atrophy).

Methods

This secondary analysis of a cohort study included 276 healthy controls (HC), and 65 clinically isolated syndrome (CIS), 352 relapsing-remitting MS (RR) and 109 secondary- progressive MS (SPMS) patients. Past reserve-related activities comprised educational and occupational attainment. Current reserve-related activities comprised strenuous and non-strenuous activities. MRI was performed on 3 T scanner. Regression and non-parametric analysis examined relationships between MRI metrics and reserve-related activities.

Results

Multivariate models (HC as referent) revealed significant interactions in predicting strenuous reserve-related activities with chronic lesion burden (for CIS), brain- (for RR & SPMS), subcortical- (for CIS, RR, & SPMS) and amygdala- (for RR) volumes. Maximal Lifetime Brain Growth was higher for RR patients who engaged in running before and after diagnosis, rather than only before or never. Residual Brain Volume was higher in RR patients who did weights-exercise before and after diagnosis, as compared to only before.

Conclusions

Reserve-related activities are related to brain health cross-sectionally in all MS subgroups, and longitudinally in RR patients. Consistent with reserve theory, RR patients who maintained strenuous activities had higher Maximal Lifetime Brain Growth and Residual Brain Volume. The study’s limitations are discussed, including the potential for recall bias and design limitations that preclude causal inference.
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Literature
1.
go back to reference Stern Y. Cognitive reserve: Theory and applications. New York: Taylor & Francis; 2007. Stern Y. Cognitive reserve: Theory and applications. New York: Taylor & Francis; 2007.
2.
go back to reference Barulli D, Stern Y. Efficiency capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17(10):502–09.CrossRefPubMed Barulli D, Stern Y. Efficiency capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17(10):502–09.CrossRefPubMed
3.
go back to reference Schwartz CE, Rapkin BD, Healy BC. Reserve and Reserve-Building Activities Research: Key challenges and future directions. Under review. 2015 Schwartz CE, Rapkin BD, Healy BC. Reserve and Reserve-Building Activities Research: Key challenges and future directions. Under review. 2015
4.
go back to reference Schwartz CE, Quaranto BR, Healy BC, Benedict RH, Vollmer TL. Cognitive reserve and symptom experience in multiple sclerosis: a buffer to disability progression over time? Arch Phys Med Rehabil. 2013;94(10):1971–81.CrossRefPubMed Schwartz CE, Quaranto BR, Healy BC, Benedict RH, Vollmer TL. Cognitive reserve and symptom experience in multiple sclerosis: a buffer to disability progression over time? Arch Phys Med Rehabil. 2013;94(10):1971–81.CrossRefPubMed
5.
go back to reference Schwartz CE, Ayandeh A, Ramanathan M, Benedict RH, Dwyer MG, Weinstock-Guttman B, et al. Reserve-building activities in multiple sclerosis patients and healthy controls: A descriptive study. BMC Neurol. 2015;15:135.CrossRefPubMedPubMedCentral Schwartz CE, Ayandeh A, Ramanathan M, Benedict RH, Dwyer MG, Weinstock-Guttman B, et al. Reserve-building activities in multiple sclerosis patients and healthy controls: A descriptive study. BMC Neurol. 2015;15:135.CrossRefPubMedPubMedCentral
6.
go back to reference Sumowski JF, Wylie GR, DeLuca J, Chiaravalloti N. Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain. 2010;133:362–74.CrossRefPubMed Sumowski JF, Wylie GR, DeLuca J, Chiaravalloti N. Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain. 2010;133:362–74.CrossRefPubMed
7.
go back to reference Sumowski JF, Wylie GR, Chiaravalloti N, DeLuca J. Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology. 2010;74(24):1942–5.CrossRefPubMedPubMedCentral Sumowski JF, Wylie GR, Chiaravalloti N, DeLuca J. Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology. 2010;74(24):1942–5.CrossRefPubMedPubMedCentral
8.
go back to reference Schwartz CE, Snook EM, Quaranto BR, Benedict RH, Vollmer T. Cognitive reserve and patient-reported outcomes. MS J. 2013;19(1):87–105. Schwartz CE, Snook EM, Quaranto BR, Benedict RH, Vollmer T. Cognitive reserve and patient-reported outcomes. MS J. 2013;19(1):87–105.
9.
go back to reference Schwartz CE, Quaranto BR, Healy BC, Benedict RH, Vollmer T. Altruism and health outcomes in multiple sclerosis: The effect of cognitive reserve. J Positive Psychology. 2013;8(2):144–52.CrossRef Schwartz CE, Quaranto BR, Healy BC, Benedict RH, Vollmer T. Altruism and health outcomes in multiple sclerosis: The effect of cognitive reserve. J Positive Psychology. 2013;8(2):144–52.CrossRef
10.
go back to reference Schwartz CE, Ayandeh A, Rodgers J, Duberstein P, Weinstock-Guttman B, Benedict RH. A new perspective on proxy report: Investigating implicit processes of understanding through patient-proxy congruence. Quality of Life Research. 2015;24(11):2637–49. Schwartz CE, Ayandeh A, Rodgers J, Duberstein P, Weinstock-Guttman B, Benedict RH. A new perspective on proxy report: Investigating implicit processes of understanding through patient-proxy congruence. Quality of Life Research. 2015;24(11):2637–49.
11.
go back to reference Schwartz CE, Snook E, Quaranto B, Benedict RH, Rapkin BD, Vollmer T. Cognitive reserve and appraisal in multiple sclerosis. Multiple Sclerosis Related Disorders. 2013;2(1):36–44.CrossRefPubMed Schwartz CE, Snook E, Quaranto B, Benedict RH, Rapkin BD, Vollmer T. Cognitive reserve and appraisal in multiple sclerosis. Multiple Sclerosis Related Disorders. 2013;2(1):36–44.CrossRefPubMed
12.
go back to reference ECTRIMS. Time matters in multiple sclerosis—international consensus recommendations on diagnosis, management and access to treatment. Barcelona: ECTRIMS; 2015. ECTRIMS. Time matters in multiple sclerosis—international consensus recommendations on diagnosis, management and access to treatment. Barcelona: ECTRIMS; 2015.
13.
go back to reference Sumowski JF, Chiaravalloti N, Wylie G, Deluca J. Cognitive reserve moderates the negative effect of brain atrophy on cognitive efficiency in multiple sclerosis. J Int Neuropsychol Soc. 2009;15(4):606–12.CrossRefPubMed Sumowski JF, Chiaravalloti N, Wylie G, Deluca J. Cognitive reserve moderates the negative effect of brain atrophy on cognitive efficiency in multiple sclerosis. J Int Neuropsychol Soc. 2009;15(4):606–12.CrossRefPubMed
14.
go back to reference Sumowski JF, Rocca MA, Leavitt VM, Riccitelli G, Comi G, Deluca J, et al. Brain reserve and cognitive reserve in multiple sclerosis: What you’ve got and how you use it. Neurology. 2013;80(24):2186–93.CrossRefPubMedPubMedCentral Sumowski JF, Rocca MA, Leavitt VM, Riccitelli G, Comi G, Deluca J, et al. Brain reserve and cognitive reserve in multiple sclerosis: What you’ve got and how you use it. Neurology. 2013;80(24):2186–93.CrossRefPubMedPubMedCentral
15.
go back to reference Booth AJ, Rodgers JD, Schwartz CE, Quaranto BR, Weinstock-Guttman B, Zivadinov R, et al. Active cognitive reserve influences the regional atrophy to cognition link in multiple sclerosis. J Int Neuropsychol Soc. 2013;19(10):1128–33.CrossRefPubMed Booth AJ, Rodgers JD, Schwartz CE, Quaranto BR, Weinstock-Guttman B, Zivadinov R, et al. Active cognitive reserve influences the regional atrophy to cognition link in multiple sclerosis. J Int Neuropsychol Soc. 2013;19(10):1128–33.CrossRefPubMed
16.
go back to reference IRTFIT. Software for the computation of the statistics involved in item response theory likelihood-ratio tests for differential item functioning [program]. UNC at Chapel Hill; 2001 IRTFIT. Software for the computation of the statistics involved in item response theory likelihood-ratio tests for differential item functioning [program]. UNC at Chapel Hill; 2001
17.
go back to reference Cappellani R, Bergsland N, Weinstock-Guttman B, Kennedy C, Carl E, Ramasamy D, et al. Subcortical deep gray matter pathology in patients with multiple sclerosis is associated with white matter lesion burden and atrophy but not with cortical atrophy: a diffusion tensor MRI study. AJNR Am J Neuroradiol. 2014;35(5):912–19.CrossRefPubMed Cappellani R, Bergsland N, Weinstock-Guttman B, Kennedy C, Carl E, Ramasamy D, et al. Subcortical deep gray matter pathology in patients with multiple sclerosis is associated with white matter lesion burden and atrophy but not with cortical atrophy: a diffusion tensor MRI study. AJNR Am J Neuroradiol. 2014;35(5):912–19.CrossRefPubMed
18.
go back to reference Gabelic T, Ramasamy DP, Weinstock-Guttman B, Hagemeier J, Kennedy C, Melia R, et al. Prevalence of radiologically isolated syndrome and white matter signal abnormalities in healthy relatives of patients with multiple sclerosis. AJNR Am J Neuroradiol. 2014;35(1):106–12.CrossRefPubMed Gabelic T, Ramasamy DP, Weinstock-Guttman B, Hagemeier J, Kennedy C, Melia R, et al. Prevalence of radiologically isolated syndrome and white matter signal abnormalities in healthy relatives of patients with multiple sclerosis. AJNR Am J Neuroradiol. 2014;35(1):106–12.CrossRefPubMed
19.
go back to reference O’Connor K, Weinstock-Guttman B, Carl E, Kilanowski C, Zivadinov R, Ramanathan M. Patterns of dietary and herbal supplement use by multiple sclerosis patients. J Neurol. 2012;259(4):637–44.CrossRefPubMed O’Connor K, Weinstock-Guttman B, Carl E, Kilanowski C, Zivadinov R, Ramanathan M. Patterns of dietary and herbal supplement use by multiple sclerosis patients. J Neurol. 2012;259(4):637–44.CrossRefPubMed
20.
go back to reference Zivadinov R, Marr K, Cutter G, Ramanathan M, Benedict RH, Kennedy C, et al. Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011;77(2):138-144. Zivadinov R, Marr K, Cutter G, Ramanathan M, Benedict RH, Kennedy C, et al. Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011;77(2):138-144.
21.
go back to reference Perneczky R, Drzezga A, Boecker H, Ceballos-Baumann AO, Granert O, Förstl H, et al. Activities of daily living, cerebral glucose metabolism, and cognitive reserve in Lewy body and Parkinson’s disease. Dement Geriatr Cogn Disord. 2008;26(5):475–81.CrossRefPubMed Perneczky R, Drzezga A, Boecker H, Ceballos-Baumann AO, Granert O, Förstl H, et al. Activities of daily living, cerebral glucose metabolism, and cognitive reserve in Lewy body and Parkinson’s disease. Dement Geriatr Cogn Disord. 2008;26(5):475–81.CrossRefPubMed
22.
go back to reference Zivadinov R, Heininen-Brown M, Schirda CV, Poloni GU, Magnano CR, Durfee J, et al. Abnormal subcortical deep-gray matter susceptibility-weighted imaging filtered phase measurements in patients with multiple sclerosis A case–control study. Neuroimage. 2012;59:331–39.CrossRefPubMed Zivadinov R, Heininen-Brown M, Schirda CV, Poloni GU, Magnano CR, Durfee J, et al. Abnormal subcortical deep-gray matter susceptibility-weighted imaging filtered phase measurements in patients with multiple sclerosis A case–control study. Neuroimage. 2012;59:331–39.CrossRefPubMed
23.
go back to reference Gelineau-Morel R, Tomassini V, Jenkinson M, Johansen-Berg H, Matthews PM, Palace J. The effect of hypointense white matter lesions on automated gray matter segmentation in multiple sclerosis. Hum Brain Mapp. 2012;33:2802–14.CrossRefPubMed Gelineau-Morel R, Tomassini V, Jenkinson M, Johansen-Berg H, Matthews PM, Palace J. The effect of hypointense white matter lesions on automated gray matter segmentation in multiple sclerosis. Hum Brain Mapp. 2012;33:2802–14.CrossRefPubMed
24.
go back to reference Patenaude B, Smith S, Kennedy D, Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage. 2011;56:907–22.CrossRefPubMedPubMedCentral Patenaude B, Smith S, Kennedy D, Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage. 2011;56:907–22.CrossRefPubMedPubMedCentral
25.
go back to reference Modica CM, Bergsland N, Dwyer MG, Ramasamy DP, Carl E, Zivadinov R, et al. Cognitive reserve moderates the impact of subcortical gray matter atrophy on neuropsychological status in multiple sclerosis. Multiple sclerosis. 2015;28:1352458515579443. Modica CM, Bergsland N, Dwyer MG, Ramasamy DP, Carl E, Zivadinov R, et al. Cognitive reserve moderates the impact of subcortical gray matter atrophy on neuropsychological status in multiple sclerosis. Multiple sclerosis. 2015;28:1352458515579443.
26.
go back to reference Sormani MP, Kappos L, Cohen J, Barkhof F, Sprenger T, Meier DP, et al. Normalized brain volume predicts cognitive performance in MS: an analysis of a large cohort from fingolimod phase III studies (P7. 284). Neurology. 2015;84(14 (Supplement):P7–284. Sormani MP, Kappos L, Cohen J, Barkhof F, Sprenger T, Meier DP, et al. Normalized brain volume predicts cognitive performance in MS: an analysis of a large cohort from fingolimod phase III studies (P7. 284). Neurology. 2015;84(14 (Supplement):P7–284.
27.
go back to reference Zar JH. Biostatistical Analysis. 2nd ed. Prentice Hall: Englewood Cliffs; 1984. Zar JH. Biostatistical Analysis. 2nd ed. Prentice Hall: Englewood Cliffs; 1984.
28.
go back to reference Stata 13 [program]. College Station. TX: StataCorp LP; 2013. Stata 13 [program]. College Station. TX: StataCorp LP; 2013.
29.
go back to reference RStudio [program]. 0.98.1103 version. Boston: R Studio Inc; 2009–2014 RStudio [program]. 0.98.1103 version. Boston: R Studio Inc; 2009–2014
30.
go back to reference van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A. 1999;96(23):13427–31.CrossRefPubMedPubMedCentral van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A. 1999;96(23):13427–31.CrossRefPubMedPubMedCentral
31.
go back to reference Aguiar Jr AS, Castro AA, Moreira EL, Glaser V, Santos AR, Tasca CI, et al. Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev. 2011;132(11–12):560–7.CrossRefPubMed Aguiar Jr AS, Castro AA, Moreira EL, Glaser V, Santos AR, Tasca CI, et al. Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev. 2011;132(11–12):560–7.CrossRefPubMed
32.
go back to reference Lovden M, Wenger E, Martensson J, Lindenberger U, Backman L. Structural brain plasticity in adult learning and development. Neurosci Biobehav Rev. 2013;37(9, Part B):2296–310.CrossRefPubMed Lovden M, Wenger E, Martensson J, Lindenberger U, Backman L. Structural brain plasticity in adult learning and development. Neurosci Biobehav Rev. 2013;37(9, Part B):2296–310.CrossRefPubMed
33.
go back to reference Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25(6):295–301.CrossRefPubMed Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25(6):295–301.CrossRefPubMed
Metadata
Title
Reserve-related activities and MRI metrics in multiple sclerosis patients and healthy controls: an observational study
Authors
Carolyn E. Schwartz
Michael G. Dwyer
Ralph Benedict
Bianca Weinstock-Guttman
Niels P. Bergsland
Jei Li
Murali Ramanathan
Robert Zivadinov
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2016
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-016-0624-1

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