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Erschienen in: Neuroradiology 1/2017

26.11.2016 | Functional Neuroradiology

Exercise training effects on memory and hippocampal viscoelasticity in multiple sclerosis: a novel application of magnetic resonance elastography

verfasst von: Brian M. Sandroff, Curtis L. Johnson, Robert W. Motl

Erschienen in: Neuroradiology | Ausgabe 1/2017

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Abstract

Introduction

Cognitive impairment is common and debilitating among persons with multiple sclerosis (MS) and might be managed with exercise training. However, the effects of exercise training on viscoelastic brain properties in this population are unknown. The present pilot study adopted a single-blind randomized controlled trial (RCT) design and is the first to examine the effect of an aerobic exercise training intervention on learning and memory and hippocampal viscoelasticity using magnetic resonance elastography (MRE) in persons with MS.

Methods

Eight fully ambulatory females with MS were randomly assigned into exercise training intervention or waitlist control conditions. The intervention condition involved 12 weeks of supervised, progressive treadmill walking exercise training. All participants underwent measures of learning and memory (i.e., California Verbal Learning Test-II; CVLT-II) and further underwent MRE scans for measurement of shear stiffness (μ) and damping ratio (ξ) of the hippocampus before and after the 12-week period.

Results

Overall, there were small-to-moderate intervention effects on CVLT-II performance (d = 0.34) and large intervention effects on hippocampal μ (d = 0.94) and hippocampal ξ (d = −1.20). Change in CVLT-II scores was strongly associated with change in μ (r = 0.93, p < 0.01) and ξ (r = −.96, p < 0.01) of the hippocampus.

Conclusion

This small pilot RCT provides exciting proof-of-concept data supporting progressive treadmill walking exercise training for potentially improving learning and memory and underlying hippocampal viscoelastic properties in persons with MS. This is important given the high prevalence and burden of MS-related memory impairment.
Literatur
1.
Zurück zum Zitat Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139–1151CrossRefPubMed Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139–1151CrossRefPubMed
2.
Zurück zum Zitat Chiaravalloti ND, Wylie G, Leavitt V, DeLuca J (2012) Increased cerebral activation after behavioral treatment for memory deficits in MS. J Neurol 259:1337–1346CrossRefPubMed Chiaravalloti ND, Wylie G, Leavitt V, DeLuca J (2012) Increased cerebral activation after behavioral treatment for memory deficits in MS. J Neurol 259:1337–1346CrossRefPubMed
3.
Zurück zum Zitat Chiaravalloti ND, Moore NB, Nikelshpur OM, DeLuca J (2013) An RCT to treat learning impairment in multiple sclerosis: the MEMREHAB trial. Neurology 81:2066–2072CrossRefPubMedPubMedCentral Chiaravalloti ND, Moore NB, Nikelshpur OM, DeLuca J (2013) An RCT to treat learning impairment in multiple sclerosis: the MEMREHAB trial. Neurology 81:2066–2072CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Motl RW, Sandroff BM, Benedict RHB (2011) Cognitive dysfunction and multiple sclerosis: developing a rationale for considering the efficacy of exercise training. Mult Scler 17(9):1034–1040CrossRefPubMed Motl RW, Sandroff BM, Benedict RHB (2011) Cognitive dysfunction and multiple sclerosis: developing a rationale for considering the efficacy of exercise training. Mult Scler 17(9):1034–1040CrossRefPubMed
5.
Zurück zum Zitat Sandroff BM (2015) Exercise and cognition in multiple sclerosis: the importance of acute exercise for developing better interventions. Neurosci Biobehav Rev 59:173–183CrossRefPubMed Sandroff BM (2015) Exercise and cognition in multiple sclerosis: the importance of acute exercise for developing better interventions. Neurosci Biobehav Rev 59:173–183CrossRefPubMed
6.
7.
Zurück zum Zitat Leavitt VM, Cirnigliaro C, Cohen A, Farag A, Brooks M, Wecht J et al (2014) Aerobic exercise increases hippocampal volume and improves memory in multiple sclerosis: preliminary findings. Neurocase 20(6):695–697CrossRefPubMed Leavitt VM, Cirnigliaro C, Cohen A, Farag A, Brooks M, Wecht J et al (2014) Aerobic exercise increases hippocampal volume and improves memory in multiple sclerosis: preliminary findings. Neurocase 20(6):695–697CrossRefPubMed
8.
Zurück zum Zitat Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, Ehman RL (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 269:1854–1857CrossRefPubMed Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, Ehman RL (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 269:1854–1857CrossRefPubMed
9.
Zurück zum Zitat Manduca A, Oliphant TE, Dresner MA, Mahowald JL, Kruse SA, Amromin E et al (2001) Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal 5:237–254CrossRefPubMed Manduca A, Oliphant TE, Dresner MA, Mahowald JL, Kruse SA, Amromin E et al (2001) Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal 5:237–254CrossRefPubMed
10.
Zurück zum Zitat Sack I, Jöhrens K, Wuerfel J, Braun J (2013) Structure-sensitive elastography: on the viscoelastic powerlaw behavior of in vivo human tissue in health and disease. Soft Matter 9:5672–5680CrossRef Sack I, Jöhrens K, Wuerfel J, Braun J (2013) Structure-sensitive elastography: on the viscoelastic powerlaw behavior of in vivo human tissue in health and disease. Soft Matter 9:5672–5680CrossRef
11.
Zurück zum Zitat Hiscox LV, Johnson CL, Barnhill E, McGarry MDJ, Huston J, van Beek EJR, et al. (in press) Magnetic resonance elastography (MRE) of the human brain: technique, findings and clinical applications. Phys Med Biol Hiscox LV, Johnson CL, Barnhill E, McGarry MDJ, Huston J, van Beek EJR, et al. (in press) Magnetic resonance elastography (MRE) of the human brain: technique, findings and clinical applications. Phys Med Biol
12.
Zurück zum Zitat Murphy MC, Huston J, Jack CR, Glaser KJ, Manduca A, Felmlee JP, Ehman RL (2011) Decreased brain stiffness in Alzheimer’s disease determined by magnetic resonance elastography. J Magn Reson Imaging 34:494–498CrossRefPubMedPubMedCentral Murphy MC, Huston J, Jack CR, Glaser KJ, Manduca A, Felmlee JP, Ehman RL (2011) Decreased brain stiffness in Alzheimer’s disease determined by magnetic resonance elastography. J Magn Reson Imaging 34:494–498CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Romano AJ, Guo J, Prokscha T, Meyer T, Hirsch S, Braun J et al (2014) In vivo waveguide elastography: effects of neurodegeneration in patients with amyotrophic lateral sclerosis. Magn Reson Med 72:1755–1761CrossRefPubMed Romano AJ, Guo J, Prokscha T, Meyer T, Hirsch S, Braun J et al (2014) In vivo waveguide elastography: effects of neurodegeneration in patients with amyotrophic lateral sclerosis. Magn Reson Med 72:1755–1761CrossRefPubMed
14.
Zurück zum Zitat Streitberger K-J, Sack I, Krefting D, Pfüller C, Braun J, Paul F, Wuerfel J (2012) Brain viscoelasticity alteration in chronic-progressive multiple sclerosis. PLoS One 7:e29888CrossRefPubMedPubMedCentral Streitberger K-J, Sack I, Krefting D, Pfüller C, Braun J, Paul F, Wuerfel J (2012) Brain viscoelasticity alteration in chronic-progressive multiple sclerosis. PLoS One 7:e29888CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Wuerfel J, Paul F, Beierbach B, Hamhaber U, Klatt D, Papazoglou S et al (2010) MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuro Image 49:2520–2525PubMed Wuerfel J, Paul F, Beierbach B, Hamhaber U, Klatt D, Papazoglou S et al (2010) MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuro Image 49:2520–2525PubMed
16.
Zurück zum Zitat Fehlner A, Behrens JR, Streitberger K-J, Papazoglou S, Braun J, Bellmann-Strobl J et al (2015) Higher-resolution MR elastography reveals early mechanical signatures of neuroinflammation in patients with clinically isolated syndrome. J Magn Reson Imaging. doi:10.1002/jmri.25129 PubMed Fehlner A, Behrens JR, Streitberger K-J, Papazoglou S, Braun J, Bellmann-Strobl J et al (2015) Higher-resolution MR elastography reveals early mechanical signatures of neuroinflammation in patients with clinically isolated syndrome. J Magn Reson Imaging. doi:10.​1002/​jmri.​25129 PubMed
17.
Zurück zum Zitat Enzinger C, Barkhof F, Ciccarelli O, Filippi M, Kappos L, Rocca MA et al (2015) Nonconventional MRI and microstructural cerebral changes in multiple sclerosis. Nat Rev Neurol 11(12):676–686CrossRefPubMed Enzinger C, Barkhof F, Ciccarelli O, Filippi M, Kappos L, Rocca MA et al (2015) Nonconventional MRI and microstructural cerebral changes in multiple sclerosis. Nat Rev Neurol 11(12):676–686CrossRefPubMed
18.
Zurück zum Zitat Johnson CL, McGarry MDJ, Van Houten EEW, Weaver JB, Paulsen KD, Sutton BP, Georgiadis JG (2013) Magnetic resonance elastography of the brain using multishot spiral readouts with self-navigated motion correction. Magn Reson Med 70:404–412CrossRefPubMed Johnson CL, McGarry MDJ, Van Houten EEW, Weaver JB, Paulsen KD, Sutton BP, Georgiadis JG (2013) Magnetic resonance elastography of the brain using multishot spiral readouts with self-navigated motion correction. Magn Reson Med 70:404–412CrossRefPubMed
19.
Zurück zum Zitat Johnson CL, Holtrop JL, McGarry MDJ, Weaver JB, Paulsen KD, Georgiadis JG, Sutton BP (2014) 3D multislab, multishot acquisition for fast, whole-brain MR elastography with high signal-to-noise efficiency. Magn Reson Med 71:477–485CrossRefPubMedPubMedCentral Johnson CL, Holtrop JL, McGarry MDJ, Weaver JB, Paulsen KD, Georgiadis JG, Sutton BP (2014) 3D multislab, multishot acquisition for fast, whole-brain MR elastography with high signal-to-noise efficiency. Magn Reson Med 71:477–485CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Johnson CL, McGarry MDJ, Gharibans AA, Weaver JB, Paulsen KD, Wang H et al (2013) Local mechanical properties of white matter structures in the human brain. Neuro Image 79:145–152PubMedPubMedCentral Johnson CL, McGarry MDJ, Gharibans AA, Weaver JB, Paulsen KD, Wang H et al (2013) Local mechanical properties of white matter structures in the human brain. Neuro Image 79:145–152PubMedPubMedCentral
21.
Zurück zum Zitat Johnson CL, Schwarb H, McGarry MDJ, Anderson AT, Huesmann GR, Sutton BP, Cohen NJ (2016) Viscoelasticity of subcortical gray matter structures. Hum Brain Mapp. doi:10.1002/hbm.23314 Johnson CL, Schwarb H, McGarry MDJ, Anderson AT, Huesmann GR, Sutton BP, Cohen NJ (2016) Viscoelasticity of subcortical gray matter structures. Hum Brain Mapp. doi:10.​1002/​hbm.​23314
22.
Zurück zum Zitat Schwarb H, Johnson CL, McGarry MDJ, Cohen NJ (2016) Medial temporal lobe viscoelasticity and relational memory performance. Neuro Image 132:534–541PubMed Schwarb H, Johnson CL, McGarry MDJ, Cohen NJ (2016) Medial temporal lobe viscoelasticity and relational memory performance. Neuro Image 132:534–541PubMed
23.
Zurück zum Zitat Sandroff BM, Balto JM, Klaren RE, Sommer SK, DeLuca J, Motl RW (in press) Systematically-developed pilot randomized controlled trial of exercise and cognition in persons with multiple sclerosis. Neurocase Sandroff BM, Balto JM, Klaren RE, Sommer SK, DeLuca J, Motl RW (in press) Systematically-developed pilot randomized controlled trial of exercise and cognition in persons with multiple sclerosis. Neurocase
24.
Zurück zum Zitat Thomas S, Reading J, Shephard RJ (1992) Revision of the physical activity readiness questionnaire. Can J Sport Sci 17:338–345PubMed Thomas S, Reading J, Shephard RJ (1992) Revision of the physical activity readiness questionnaire. Can J Sport Sci 17:338–345PubMed
25.
Zurück zum Zitat Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California Verbal Learning Test, Second edition (CVLT-II). Psychological Corporation, San Antonio, TX Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California Verbal Learning Test, Second edition (CVLT-II). Psychological Corporation, San Antonio, TX
26.
Zurück zum Zitat McGarry MDJ, Van Houten EEW, Johnson CL, Georgiadis JG, Sutton BP, Weaver JB, Paulsen KD (2012) Multiresolution MR elastography using nonlinear inversion. Med Phys 39:6388–6396CrossRefPubMedPubMedCentral McGarry MDJ, Van Houten EEW, Johnson CL, Georgiadis JG, Sutton BP, Weaver JB, Paulsen KD (2012) Multiresolution MR elastography using nonlinear inversion. Med Phys 39:6388–6396CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat McGarry MDJ, Johnson CL, Sutton BP, Van Houten EEW, Georgiadis JG, Weaver JB, Paulsen KD (2013) Including spatial information in nonlinear inversion MR elastography using soft prior regularization. IEEE Trans Med Imaging 32:1901–1909CrossRefPubMedPubMedCentral McGarry MDJ, Johnson CL, Sutton BP, Van Houten EEW, Georgiadis JG, Weaver JB, Paulsen KD (2013) Including spatial information in nonlinear inversion MR elastography using soft prior regularization. IEEE Trans Med Imaging 32:1901–1909CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuro Image 56:907–922PubMedPubMedCentral Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuro Image 56:907–922PubMedPubMedCentral
29.
Zurück zum Zitat Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuro Image 62:782–790PubMed Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuro Image 62:782–790PubMed
30.
Zurück zum Zitat McGarry MDJ, Van Houten EEW (2008) Use of a Rayleigh damping model in elastography. Med Biol Eng Comput 46:759–766CrossRefPubMed McGarry MDJ, Van Houten EEW (2008) Use of a Rayleigh damping model in elastography. Med Biol Eng Comput 46:759–766CrossRefPubMed
31.
Zurück zum Zitat Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452CrossRefPubMed Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452CrossRefPubMed
32.
Zurück zum Zitat American College of Sports Medicine (2013) ACSM’s resource manual for guidelines for exercise testing and prescription, 7th edn. Lippincott Williams & Wilkins, Philadelphia (PA) American College of Sports Medicine (2013) ACSM’s resource manual for guidelines for exercise testing and prescription, 7th edn. Lippincott Williams & Wilkins, Philadelphia (PA)
33.
Zurück zum Zitat Sandroff BM, Hillman CH, Benedict RHB, Motl RW (2015) Acute effects of walking, cycling, and yoga exercise on cognition in persons with relapsing-remitting multiple sclerosis without impaired cognitive processing speed. J Clin Exp Neuropsychol 37(2):209–219CrossRefPubMed Sandroff BM, Hillman CH, Benedict RHB, Motl RW (2015) Acute effects of walking, cycling, and yoga exercise on cognition in persons with relapsing-remitting multiple sclerosis without impaired cognitive processing speed. J Clin Exp Neuropsychol 37(2):209–219CrossRefPubMed
34.
Zurück zum Zitat Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale (NJ) Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale (NJ)
35.
Zurück zum Zitat Rutledge T, Loh C (2004) Effect sizes and statistical testing in the determination of clinical significances in behavioral medicine research. Ann Behav Med 27:138–145CrossRefPubMed Rutledge T, Loh C (2004) Effect sizes and statistical testing in the determination of clinical significances in behavioral medicine research. Ann Behav Med 27:138–145CrossRefPubMed
36.
Zurück zum Zitat Parmenter BA, Testa SM, Schretlen DJ, Weinstock-Guttman B, Benedict RHB (2009) The utility of regression-based norms in interpreting the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 6:6–16 Parmenter BA, Testa SM, Schretlen DJ, Weinstock-Guttman B, Benedict RHB (2009) The utility of regression-based norms in interpreting the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 6:6–16
37.
Zurück zum Zitat Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L et al (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108(7):3017–3022CrossRefPubMedPubMedCentral Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L et al (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108(7):3017–3022CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Mohr DC, Spring B, Freedland KE, Beckner V, Arean P, Hollon SD et al (2009) The selection and design of control conditions for randomized controlled trials of psychological interventions. Psychother Psychosom 78:275–284CrossRefPubMed Mohr DC, Spring B, Freedland KE, Beckner V, Arean P, Hollon SD et al (2009) The selection and design of control conditions for randomized controlled trials of psychological interventions. Psychother Psychosom 78:275–284CrossRefPubMed
39.
Zurück zum Zitat Ehlers DK, Fanning J, Awick EA, Kramer AF, McAuley E (2016) Contamination by an active control condition in a randomized exercise trial. PLoS One 11(10):e016426 Ehlers DK, Fanning J, Awick EA, Kramer AF, McAuley E (2016) Contamination by an active control condition in a randomized exercise trial. PLoS One 11(10):e016426
40.
Zurück zum Zitat De Giglio L, Tona F, De Luca F, Petsas N, Prosperini L, Bianchi V et al (2016) Multiple sclerosis: changes in thalamic resting-state functional connectivity induced by a home-based cognitive rehabilitation program. Radiology 280(1):202–211CrossRefPubMed De Giglio L, Tona F, De Luca F, Petsas N, Prosperini L, Bianchi V et al (2016) Multiple sclerosis: changes in thalamic resting-state functional connectivity induced by a home-based cognitive rehabilitation program. Radiology 280(1):202–211CrossRefPubMed
41.
Zurück zum Zitat Sandroff BM, Pilutti LA, Benedict RHB, Motl RW (2015) Association between physical fitness and cognitive function in multiple sclerosis: does disability status matter? Neurorehabil Neural Repair 29(3):214–223CrossRefPubMed Sandroff BM, Pilutti LA, Benedict RHB, Motl RW (2015) Association between physical fitness and cognitive function in multiple sclerosis: does disability status matter? Neurorehabil Neural Repair 29(3):214–223CrossRefPubMed
Metadaten
Titel
Exercise training effects on memory and hippocampal viscoelasticity in multiple sclerosis: a novel application of magnetic resonance elastography
verfasst von
Brian M. Sandroff
Curtis L. Johnson
Robert W. Motl
Publikationsdatum
26.11.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Neuroradiology / Ausgabe 1/2017
Print ISSN: 0028-3940
Elektronische ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-016-1767-x

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