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The effect of age and microstructural white matter integrity on lap time variation and fast-paced walking speed

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Abstract

Macrostructural white matter damage (WMD) is associated with less uniform and slower walking in older adults. The effect of age and subclinical microstructural WM degeneration (a potentially earlier phase of WM ischemic damage) on walking patterns and speed is less clear. This study examines the effect of age on the associations of regional microstructural WM integrity with walking variability and speed, independent of macrostructural WMD. This study involved 493 participants (n = 51 young; n = 209 young-old; n = 233 old-old) from the Baltimore Longitudinal Study of Aging. All completed a 400-meter walk test and underwent a concurrent brain MRI with diffusion tensor imaging. Microstructural WM integrity was measured as fractional anisotropy (FA). Walking variability was measured as trend-adjusted variation in time over ten 40-meter laps (lap time variation, LTV). Fast-paced walking speed was assessed as mean lap time (MLT). Multiple linear regression models of FA predicting LTV and MLT were adjusted for age, sex, height, weight, and WM hyperintensities. Independent of WM hyperintensities, lower FA in the body of the corpus callosum was associated with higher LTV and longer MLT only in the young-old. Lower FA in superior longitudinal, inferior fronto-occipital, and uncinate fasciculi, the anterior limb of the internal capsule, and the anterior corona radiate was associated with longer MLT only in the young-old. While macrostructural WMD is known to predict more variable and slower walking in older adults, microstructural WM disruption is independently associated with more variable and slower fast-paced walking only in the young-old. Disrupted regional WM integrity may be a subclinical contributor to abnormal walking at an earlier phase of aging.

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References

  • Alexander, D. C., Pierpaoli, C., Basser, P. J., & Gee, J. C. (2001). Spatial transformations of diffusion tensor magnetic resonance images. IEEE Transactions on Medical Imaging, 20, 1131–1139.

    Article  CAS  PubMed  Google Scholar 

  • Beauchet, O., Annweiler, C., Lecordroch, Y., Allali, G., Dubost, V., Herrmann, F. R., & Kressig, R. W. (2009). Walking speed-related changes in stride time variability: effects of decreased speed. Journal of Neuroengineering and Rehabilitation, 6, 32.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhadelia, R. A., Price, L. L., Tedesco, K. L., Scott, T., Qiu, W. Q., Patz, S., Folstein, M., Rosenberg, I., Caplan, L. R., & Bergethon, P. (2009). Diffusion tensor imaging, white matter lesions, the corpus callosum, and gait in the elderly. Stroke; a Journal of Cerebral Circulation, 40, 3816–3820.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bielak, A. A., Hultsch, D. F., Strauss, E., Macdonald, S. W., & Hunter, M. A. (2010). Intraindividual variability in reaction time predicts cognitive outcomes 5 years later. Neuropsychology, 24, 731–741.

    Article  PubMed  Google Scholar 

  • Bolandzadeh, N., Liu-Ambrose, T., Aizenstein, H., Harris, T., Launer, L., Yaffe, K., Kritchevsky, S. B., Newman, A., & Rosano, C. (2014). Pathways linking regional hyperintensities in the brain and slower gait. NeuroImage, 99, 7–13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brach, J. S., Studenski, S. A., Perera, S., VanSwearingen, J. M., & Newman, A. B. (2007). Gait variability and the risk of incident mobility disability in community-dwelling older adults. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 62, 983–988.

    Article  Google Scholar 

  • Bruijn, S. M., Van Impe, A., Duysens, J., & Swinnen, S. P. (2014). White matter microstructural organization and gait stability in older adults. Frontiers in Aging Neuroscience, 6, 104.

    Article  PubMed  PubMed Central  Google Scholar 

  • Charlton, R. A., Barrick, T. R., McIntyre, D. J., Shen, Y., O'Sullivan, M., Howe, F. A., Clark, C. A., Morris, R. G., & Markus, H. S. (2006). White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology, 66, 217–222.

    Article  CAS  PubMed  Google Scholar 

  • Davatzikos, C., Genc, A., Xu, D., & Resnick, S. M. (2001). Voxel-based morphometry using the RAVENS maps: methods and validation using simulated longitudinal atrophy. NeuroImage, 14, 1361–1369.

    Article  CAS  PubMed  Google Scholar 

  • de Laat, K. F., Tuladhar, A. M., van Norden, A. G., Norris, D. G., Zwiers, M. P., & de Leeuw, F. E. (2011a). Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain: a Journal of Neurology, 134, 73–83.

    Article  Google Scholar 

  • de Laat, K. F., van Norden, A. G., Gons, R. A., van Oudheusden, L. J., van Uden, I. W., Norris, D. G., Zwiers, M. P., & de Leeuw, F. E. (2011b). Diffusion tensor imaging and gait in elderly persons with cerebral small vessel disease. Stroke; a Journal of Cerebral Circulation, 42, 373–379.

    Article  PubMed  Google Scholar 

  • Della Nave, R., Foresti, S., Pratesi, A., Ginestroni, A., Inzitari, M., Salvadori, E., Giannelli, M., Diciotti, S., Inzitari, D., & Mascalchi, M. (2007). Whole-brain histogram and voxel-based analyses of diffusion tensor imaging in patients with leukoaraiosis: correlation with motor and cognitive impairment. AJNR. American Journal of Neuroradiology, 28, 1313–1319.

    Article  CAS  PubMed  Google Scholar 

  • Dunsky, A., Dickstein, R., Ariav, C., Deutsch, J., & Marcovitz, E. (2006). Motor imagery practice in gait rehabilitation of chronic post-stroke hemiparesis: four case studies. International Journal of Rehabilitation Research Internationale Zeitschrift fur Rehabilitationsforschung Revue Internationale de Recherches de Readaptation, 29, 351–356.

    Article  PubMed  Google Scholar 

  • Gallo, A., Rovaris, M., Riva, R., Ghezzi, A., Benedetti, B., Martinelli, V., Falini, A., Comi, G., & Filippi, M. (2005). Diffusion-tensor magnetic resonance imaging detects normal-appearing white matter damage unrelated to short-term disease activity in patients at the earliest clinical stage of multiple sclerosis. Archives of Neurology, 62, 803–808.

    Article  PubMed  Google Scholar 

  • Hendelman, W., (2006). Atlas of Functional Neuroanatomy: CRC Press.

  • Juurlink, B. H. (1997). Response of glial cells to ischemia: roles of reactive oxygen species and glutathione. Neuroscience and Biobehavioral Reviews, 21, 151–166.

    Article  CAS  PubMed  Google Scholar 

  • Kang, H. G., & Dingwell, J. B. (2008). Separating the effects of age and walking speed on gait variability. Gait & Posture, 27, 572–577.

    Article  Google Scholar 

  • Klein, A., Dal, Canton T., Ghosh, S.S., Landman, B., Lee, J., Worth, A., (2010). Open labels: online feedback for a public resource of manually labeled brain images. In: 16th Annual Meeting for the Organization of Human Brain Mapping.

  • Kochunov, P., Lancaster, J., Hardies, J., Thompson, P. M., Woods, R. P., Cody, J. D., Hale, D. E., Laird, A., & Fox, P. T. (2005). Mapping structural differences of the corpus callosum in individuals with 18q deletions using targetless regional spatial normalization. Human Brain Mapping, 24, 325–331.

    Article  PubMed  Google Scholar 

  • Kochunov, P., Thompson, P. M., Lancaster, J. L., Bartzokis, G., Smith, S., Coyle, T., Royall, D. R., Laird, A., & Fox, P. T. (2007). Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. NeuroImage, 35, 478–487.

    Article  CAS  PubMed  Google Scholar 

  • Koo, B. B., Bergethon, P., Qiu, W. Q., Scott, T., Hussain, M., Rosenberg, I., Caplan, L. R., & Bhadelia, R. A. (2012). Clinical prediction of fall risk and white matter abnormalities: a diffusion tensor imaging study. Archives of Neurology, 69, 733–738.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamantia, A. S., & Rakic, P. (1990). Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. Journal of Comparative Neurology, 291, 520–537.

    Article  CAS  PubMed  Google Scholar 

  • Lao, Z., Shen, D., Liu, D., Jawad, A. F., Melhem, E. R., Launer, L. J., Bryan, R. N., & Davatzikos, C. (2008). Computer-assisted segmentation of white matter lesions in 3D MR images using support vector machine. Academic Radiology, 15, 300–313.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lauzon, C. B., Asman, A. J., Esparza, M. L., Burns, S. S., Fan, Q., Gao, Y., Anderson, A. W., Davis, N., Cutting, L. E., & Landman, B. A. (2013). Simultaneous analysis and quality assurance for diffusion tensor imaging. PLoS One, 8, e61737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, S., Aggen, S. H., Nesselroade, J. R., & Baltes, P. B. (2001). Short-term fluctuations in elderly people’s sensorimotor functioning predict text and spatial memory performance: the Macarthur successful aging studies. Gerontology, 47, 100–116.

    Article  CAS  PubMed  Google Scholar 

  • Lim, I. A., Faria, A. V., Li, X., Hsu, J. T., Airan, R. D., Mori, S., & van Zijl, P. C. (2013). Human brain atlas for automated region of interest selection in quantitative susceptibility mapping: application to determine iron content in deep gray matter structures. NeuroImage, 82, 449–469.

    Article  PubMed  PubMed Central  Google Scholar 

  • MacDonald, S. W., Hultsch, D. F., & Dixon, R. A. (2003). Performance variability is related to change in cognition: evidence from the Victoria longitudinal study. Psychology and Aging, 18, 510–523.

    Article  PubMed  Google Scholar 

  • Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., Jr., & Pandya, D. N. (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cerebral Cortex, 15, 854–869.

    Article  PubMed  Google Scholar 

  • McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939–944.

  • McTigue, D. M., & Tripathi, R. B. (2008). The life, death, and replacement of oligodendrocytes in the adult CNS. Journal of Neurochemistry, 107, 1–19.

    Article  CAS  PubMed  Google Scholar 

  • Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.

    Article  CAS  PubMed  Google Scholar 

  • Penke, L., Munoz Maniega, S., Murray, C., Gow, A. J., Hernandez, M. C., Clayden, J. D., Starr, J. M., Wardlaw, J. M., Bastin, M. E., & Deary, I. J. (2010). A general factor of brain white matter integrity predicts information processing speed in healthy older people. Journal of Neuroscience, 30, 7569–7574.

    Article  CAS  PubMed  Google Scholar 

  • Raybaud, C. (2010). The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation. Neuroradiology, 52, 447–477.

    Article  PubMed  Google Scholar 

  • Rosano, C., Brach, J., Studenski, S., Longstreth, W. T., Jr., & Newman, A. B. (2007). Gait variability is associated with subclinical brain vascular abnormalities in high-functioning older adults. Neuroepidemiology, 29, 193–200.

    Article  PubMed  PubMed Central  Google Scholar 

  • Scherder, E., Eggermont, L., Visscher, C., Scheltens, P., & Swaab, D. (2011). Understanding higher level gait disturbances in mild dementia in order to improve rehabilitation: ‘last in-first out. Neuroscience and Biobehavioral Reviews, 35, 699–714.

    Article  PubMed  Google Scholar 

  • Sen, P. N., & Basser, P. J. (2005). A model for diffusion in white matter in the brain. Biophysical Journal, 89, 2927–2938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sexton, C. E., Walhovd, K. B., Storsve, A. B., Tamnes, C. K., Westlye, L. T., Johansen-Berg, H., & Fjell, A. M. (2014). Accelerated changes in white matter microstructure during aging: a longitudinal diffusion tensor imaging study. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34, 15425–15436.

    Article  CAS  Google Scholar 

  • Shock, N., Greulich, R., Andres, R., Arenberg, D., Costa, P., Lakatta, E., Tobin, J., (1984). Normal human aging: The Baltimore longitudinal study of aging. NIH Publ No. 84–245.

  • Simonsick, E. M., Montgomery, P. S., Newman, A. B., Bauer, D. C., & Harris, T. (2001). Measuring fitness in healthy older adults: the health ABC long distance corridor walk. Journal of the American Geriatrics Society, 49, 1544–1548.

    Article  CAS  PubMed  Google Scholar 

  • Simonsick, E. M., Newman, A. B., Ferrucci, L., Satterfield, S., Harris, T. B., Rodondi, N., Bauer, D. C., & Health, A. B. C. S. (2009). Subclinical hypothyroidism and functional mobility in older adults. Archives of Internal Medicine, 169, 2011–2017.

    Article  PubMed  PubMed Central  Google Scholar 

  • Simonsick, E. M., Schrack, J. A., Glynn, N. W., & Ferrucci, L. (2014). Assessing fatigability in mobility-intact older adults. Journal of the American Geriatrics Society, 62, 347–351.

    Article  PubMed  PubMed Central  Google Scholar 

  • Starr, J. M., Leaper, S. A., Murray, A. D., Lemmon, H. A., Staff, R. T., Deary, I. J., & Whalley, L. J. (2003). Brain white matter lesions detected by magnetic resonance [correction of resosnance] imaging are associated with balance and gait speed. Journal of Neurology, Neurosurgery and Psychiatry, 74, 94–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, H. L., Jacobs, D. R., Jr., Schucker, B., Knudsen, J., Leon, A. S., & Debacker, G. (1978). A questionnaire for the assessment of leisure time physical activities. Journal of Chronic Diseases, 31, 741–755.

    Article  CAS  PubMed  Google Scholar 

  • Thorburne, S. K., & Juurlink, B. H. (1996). Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. Journal of Neurochemistry, 67, 1014–1022.

    Article  CAS  PubMed  Google Scholar 

  • Tian, Q., Simonsick, S.M., Resnick, S.M., Shardell, M.D., Ferrucci, L., Studenski, S.A., (2015). Lap Time Variation and Executive Function in Older Adults: The Baltimore Longitudinal Study of Aging. Age and Ageing.

  • Van Impe, A., Coxon, J. P., Goble, D. J., Doumas, M., & Swinnen, S. P. (2012). White matter fractional anisotropy predicts balance performance in older adults. Neurobiology of Aging, 33, 1900–1912.

    Article  PubMed  Google Scholar 

  • Vercruysse, S., Leunissen, I., Vervoort, G., Vandenberghe, W., Swinnen, S., & Nieuwboer, A. (2015). Microstructural changes in white matter associated with freezing of gait in Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 30, 567–576.

    Article  Google Scholar 

  • Vermeulen, J., Neyens, J. C., van Rossum, E., Spreeuwenberg, M. D., & de Witte, L. P. (2011). Predicting ADL disability in community-dwelling elderly people using physical frailty indicators: a systematic review. BMC Geriatrics, 11, 33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vestergaard, S., Patel, K. V., Bandinelli, S., Ferrucci, L., & Guralnik, J. M. (2009). Characteristics of 400-meter walk test performance and subsequent mortality in older adults. Rejuvenation Research, 12, 177–184.

    Article  PubMed  PubMed Central  Google Scholar 

  • Werring, D. J., Clark, C. A., Barker, G. J., Thompson, A. J., & Miller, D. H. (1999). Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology, 52, 1626–1632.

    Article  CAS  PubMed  Google Scholar 

  • Westlye, L. T., Walhovd, K. B., Dale, A. M., Bjornerud, A., Due-Tonnessen, P., Engvig, A., Grydeland, H., Tamnes, C. K., Ostby, Y., & Fjell, A. M. (2010). Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cerebral Cortex, 20, 2055–2068.

    Article  PubMed  Google Scholar 

  • Zacharaki, E.I., Kanterakis, S., Bryan, R.N., Davatzikos, C., (2008). Measuring brain lesion progression with a supervised tissue classification system. Medical image computing and computer-assisted intervention: MICCAI International Conference on Medical Image Computing and Computer-Assisted Intervention 11:620–627.

  • Zheng, J. J., Delbaere, K., Close, J. C., Sachdev, P., Wen, W., Brodaty, H., & Lord, S. R. (2012). White matter hyperintensities are an independent predictor of physical decline in community-dwelling older people. Gerontology, 58, 398–406.

    Article  PubMed  Google Scholar 

  • Zonderman, A. B., Giambra, L. M., Arenberg, D., Resnick, S. M., Costa, P. T., Jr., & Kawas, C. H. (1995). Changes in immediate visual memory predict cognitive impairment. Archives of Clinical Neuropsychology, 10, 111–123.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Intramural Research Program of the National Institute on Aging. Authors would like to thank the National Institutes of Health Editorial Fellows Editorial Board.

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The authors declare no conflict of interest.

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Authors and Affiliations

  1. Longitudinal Studies Section, Translational Gerontology Branch, National Institute on Aging, 251 Bayview Blvd., Suite 100, Rm 04B316, Baltimore, 21224, USA

    Qu Tian, Luigi Ferrucci, Eleanor M. Simonsick, Michelle D. Shardell & Stephanie A. Studenski

  2. Laboratory of Behavioral Neuroscience, National Institute on Aging, Baltimore, 21224, USA

    Susan M. Resnick, Vijay K. Venkatraman & Christopher E. Gonzalez

  3. School of Engineering, Vanderbilt University, Nashville, 37212, USA

    Bennett A. Landman

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  1. Qu Tian
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  2. Luigi Ferrucci
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  4. Eleanor M. Simonsick
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  9. Stephanie A. Studenski
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Correspondence to Qu Tian.

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Tian, Q., Ferrucci, L., Resnick, S.M. et al. The effect of age and microstructural white matter integrity on lap time variation and fast-paced walking speed. Brain Imaging and Behavior 10, 697–706 (2016). https://doi.org/10.1007/s11682-015-9449-6

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