Skip to main content

Correlation between degree of white matter hyperintensities and global gray matter volume decline rate

Neuroradiology volume 53, pages 397–403 (2011)Cite this article

Abstract

Introduction

Whether the degree of white matter hyperintensities (WMHs) shows a significant correlation with the rate of global gray matter volume decline over a period following initial baseline measurement remains unclear. The purpose of the present study was to reveal the relationship between the degree of WMHs at baseline and the rate of global gray matter volume decline by applying a longitudinal design.

Methods

Using a 6-year longitudinal design and magnetic resonance images of the brains of 160 healthy individuals aged over 50 years and living in the community, we analyzed the correlation between degree of WMHs using Fazekas scaling at baseline and rate of global gray matter volume decline 6 years later. To obtain the rate of global gray matter volume decline, we calculated global gray matter volume and intracranial volume at baseline and at follow-up using a fully automated method.

Results

The annual percentage change in the gray matter ratio (GMR, APCGMR), in which GMR represents the percentage of gray matter volume in the intracranial volume, showed a significant positive correlation with the degree of deep WMHs and periventricular WMHs at baseline, after adjusting for age, gender, present history of hypertension, and diabetes mellitus.

Conclusion

Our results suggest that degree of WMHs at baseline predicts the rate of gray matter volume decline 6 years later and that simple visual scaling of WMHs could contribute to predicting the rate of global gray matter volume decline.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  1. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36

    PubMed  Article  CAS  Google Scholar 

  2. Taki Y, Goto R, Evans A, Zijdenbos A, Neelin P, Lerch J, Sato K, Ono S, Kinomura S, Nakagawa M, Sugiura M, Watanabe J, Kawashima R, Fukuda H (2004) Voxel-based morphometry of human brain with age and cerebrovascular risk factors. Neurobiol Aging 25:455–463

    PubMed  Article  Google Scholar 

  3. Fotenos AF, Snyder AZ, Girton LE, Morris JC, Buckner RL (2005) Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD. Neurology 64:1032–1039

    PubMed  CAS  Google Scholar 

  4. Kramer JH, Mungas D, Reed BR, Wetzel ME, Burnett MM, Miller BL, Weiner MW, Chui HC (2007) Longitudinal MRI and cognitive change in healthy elderly. Neuropsychology 21:412–418

    PubMed  Article  Google Scholar 

  5. Zimmerman ME, Brickman AM, Paul RH, Grieve SM, Tate DF, Gunstad J, Cohen RA, Aloia MS, Williams LM, Clark CR, Whitford TJ, Gordon E (2006) The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. Am J Geriatr Psychiatry 14:823–833

    PubMed  Article  Google Scholar 

  6. Longstreth WT Jr, Manolio TA, Arnold A, Burke GL, Bryan N, Jungreis CA, Enright PL, O'Leary D, Fried L (1996) Clinical correlates of white matter findings on cranial magnetic resonance imaging of 3301 elderly people. The Cardiovascular Health Study. Stroke 27:1274–1282

    PubMed  Google Scholar 

  7. Oosterman JM, Van Harten B, Weinstein HC, Scheltens P, Sergeant JA, Scherder EJ (2008) White matter hyperintensities and working memory: an explorative study. Aging Neuropsychology & Cognition 15:384–399

    Article  Google Scholar 

  8. Oosterman JM, Vogels RL, van Harten B, Gouw AA, Scheltens P, Poggesi A, Weinstein HC, Scherder EJ (2008) The role of white matter hyperintensities and medial temporal lobe atrophy in age-related executive dysfunctioning. Brain Cogn 68:128–133

    PubMed  Article  Google Scholar 

  9. Nebes RD, Meltzer CC, Whyte EM, Scanlon JM, Halligan EM, Saxton JA, Houck PR, Boada FE, Dekosky ST (2006) The relation of white matter hyperintensities to cognitive performance in the normal old: education matters. Aging Neuropsychology & Cognition 13:326–340

    Article  Google Scholar 

  10. Basile AM, Pantoni L, Pracucci G, Asplund K, Chabriat H, Erkinjuntti T, Fazekas F, Ferro JM, Hennerici M, O'Brien J, Scheltens P, Visser MC, Wahlund LO, Waldemar G, Wallin A, Inzitari D, LADIS Study G (2006) Age, hypertension, and lacunar stroke are the major determinants of the severity of age-related white matter changes. The LADIS (Leukoaraiosis and Disability in the Elderly) Study. Cerebrovasc Dis 21:315–322

    PubMed  Article  Google Scholar 

  11. Park MK, Jo I, Park MH, Kim TK, Jo SA, Shin C (2005) Cerebral white matter lesions and hypertension status in the elderly Korean: the Ansan Study. Arch Gerontol Geriatr 40:265–273

    PubMed  Article  Google Scholar 

  12. Taki Y, Kinomura S, Sato K, Goto R, Inoue K, Okada K, Ono S, Kawashima R, Fukuda H (2006) Both global gray matter volume and regional gray matter volume negatively correlate with lifetime alcohol intake in non-alcohol-dependent Japanese men: a volumetric analysis and a voxel-based morphometry. Alcohol Clin Exp Res 30:1045–1050

    PubMed  Article  Google Scholar 

  13. Taki Y, Kinomura S, Sato K, Inoue K, Goto R, Okada K, Uchida S, Kawashima R, Fukuda H (2008) Relationship between body mass index and gray matter volume in 1, 428 healthy individuals. Obesity 16:119–124

    PubMed  Article  Google Scholar 

  14. Wen W, Sachdev PS, Chen X, Anstey K (2006) Gray matter reduction is correlated with white matter hyperintensity volume: a voxel-based morphometric study in a large epidemiological sample. Neuroimage 29:1031–1039

    PubMed  Article  Google Scholar 

  15. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol American Journal 149:351–356

    CAS  Google Scholar 

  16. Sato K, Taki Y, Fukuda H, Kawashima R (2003) Neuroanatomical database of normal Japanese brains. Neural Netw 16:1301–1310

    PubMed  Article  Google Scholar 

  17. Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    PubMed  Article  CAS  Google Scholar 

  18. Friston KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210

    Article  Google Scholar 

  19. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Georg Thieme, Stuttgart

    Google Scholar 

  20. Ashburner J, Neelin P, Collins DL, Evans A, Friston K (1997) Incorporating prior knowledge into image registration. Neuroimage 6:344–352

    PubMed  Article  CAS  Google Scholar 

  21. Rossi R, Boccardi M, Sabattoli F, Galluzzi S, Alaimo G, Testa C, Frisoni GB (2006) Topographic correspondence between white matter hyperintensities and brain atrophy. J Neurol 253:919–927

    PubMed  Article  CAS  Google Scholar 

  22. Firbank MJ, Wiseman RM, Burton EJ, Saxby BK, O'Brien JT, Ford GA (2007) Brain atrophy and white matter hyperintensity change in older adults and relationship to blood pressure. Brain atrophy, WMH change and blood pressure. J Neurol 254:713–721

    PubMed  Article  Google Scholar 

  23. Brickman AM, Zahra A, Muraskin J, Steffener J, Holland CM, Habeck C, Borogovac A, Ramos MA, Brown TR, Asllani I, Stern Y (2009) Reduction in cerebral blood flow in areas appearing as white matter hyperintensities on magnetic resonance imaging. Psychiatry Res 172:117–120

    PubMed  Article  Google Scholar 

  24. Bastos-Leite AJ, Kuijer JP, Rombouts SA, Sanz-Arigita E, van Straaten EC, Gouw AA, van der Flier WM, Scheltens P, Barkhof F (2008) Cerebral blood flow by using pulsed arterial spin-labeling in elderly subjects with white matter hyperintensities. AJNR Am J Neuroradiol 29:1296–1301

    PubMed  Article  CAS  Google Scholar 

  25. Meyer JS, Rauch GM, Crawford K, Rauch RA, Konno S, Akiyama H, Terayama Y, Haque A (1999) Risk factors accelerating cerebral degenerative changes, cognitive decline and dementia. Int J Geriatr Psychiatry 14:1050–1061

    PubMed  Article  CAS  Google Scholar 

  26. Appelman AP, van der Graaf Y, Vincken KL, Tiehuis AM, Witkamp TD, Mali WP, Geerlings MI, SMART Study G (2008) Total cerebral blood flow, white matter lesions and brain atrophy: the SMART-MR study. J Cereb Blood Flow Metab 28:633–639

    Article  Google Scholar 

  27. Symon L, Pasztor E, Dorsch NW, Branston NM (1973) Physiological responses of local areas of the cerebral circulation in experimental primates determined by the method of hydrogen clearance. Stroke 4:632–642

    PubMed  CAS  Google Scholar 

  28. Young RS, Hernandez MJ, Yagel SK (1982) Selective reduction of blood flow to white matter during hypotension in newborn dogs: a possible mechanism of periventricular leukomalacia. Ann Neurol 12:445–448

    PubMed  Article  CAS  Google Scholar 

  29. Pantoni L, Garcia JH (1997) Pathogenesis of leukoaraiosis: a review. Stroke 28:652–659

    PubMed  CAS  Google Scholar 

  30. Le Bihan D (2003) Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4:469–480

    PubMed  Article  Google Scholar 

  31. van Buchem MA, Udupa JK, McGowan JC, Miki Y, Heyning FH, Boncoeur-Martel MP, Kolson DL, Polansky M, Grossman RI (1997) Global volumetric estimation of disease burden in multiple sclerosis based on magnetization transfer imaging. AJNR Am J Neuroradiol 18:1287–1290

    PubMed  Google Scholar 

  32. Ropele S, Seewann A, Gouw AA, van der Flier WM, Schmidt R, Pantoni L, Inzitari D, Erkinjuntti T, Scheltens P, Wahlund LO, Waldemar G, Chabriat H, Ferro J, Hennerici M, O'Brien J, Wallin A, Langhorne P, Visser MC, Barkhof F, Fazekas F, LADIS study group (2009) Quantitation of brain tissue changes associated with white matter hyperintensities by diffusion-weighted and magnetization transfer imaging: the LADIS (Leukoaraiosis and Disability in the Elderly) study. J Magn Reson Imaging 29:268–274

    PubMed  Article  Google Scholar 

  33. Abe O, Yamasue H, Aoki S, Suga M, Yamada H, Kasai K, Masutani Y, Kato N, Kato N, Ohtomo K (2008) Aging in the CNS: comparison of gray/white matter volume and diffusion tensor data. Neurobiol Aging 29:102–116

    PubMed  Article  Google Scholar 

  34. Ibrahim I, Horacek J, Bartos A, Hajek M, Ripova D, Brunovsky M, Tintera J (2009) Combination of voxel based morphometry and diffusion tensor imaging in patients with Alzheimer's disease. Neuroendocrinology Letters 30:39–45

    PubMed  Google Scholar 

  35. Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43:1683–1689

    PubMed  CAS  Google Scholar 

  36. Scheltens PM, Barkhof FM, Leys DM, Wolters ECM, Ravid RP, Kamphorst WM (1995) Histopathologic correlates of white matter changes on MRI in Alzheimer's disease and normal aging. Neurology 45:883–888

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Inoue and K. Okada for insightful comments, and K. Inaba, K. Saito, N. Ishibashi, and H. Masuyama for technical help in collecting data.

This study was funded by the National Institute of Mental Health, the National Institute of Neurological Disorders and Stroke, the National Institute on Drug Abuse and the U.S. National Cancer Institute. Part of this research was supported by a grant from the Telecommunications Advancement Organization of Japan. This study was also supported in part by the 21st Century Center of Excellence (COE) Program (Ministry of Education, Culture, Sports, Science and Technology; MEXT), entitled "Future Medical Engineering-based Bio-nanotechnology" at Tohoku University, and a grant from the JSPS-CIHR Joint Health Research Program. This work was also supported by the MEXT Grant-in-Aid for Young Scientists (B), 18790864.

Conflict of interest statement

We declare that we have no conflict of interest.

Author information

Affiliations

  1. Division of Developmental Cognitive Neuroscience, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryocho, Aobaku, 980-8575, Sendai, Japan

    Yasuyuki Taki & Ryuta Kawashima

  2. Department of Nuclear Medicine and Radiology, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan

    Shigeo Kinomura, Kazunori Sato, Ryoi Goto, Kai Wu & Hiroshi Fukuda

  3. Department of Functional Brain Imaging, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan

    Ryuta Kawashima

  4. Smart Ageing International Research Center, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan

    Ryuta Kawashima

Authors
  1. Yasuyuki Taki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shigeo Kinomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazunori Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ryoi Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kai Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ryuta Kawashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroshi Fukuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasuyuki Taki.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Taki, Y., Kinomura, S., Sato, K. et al. Correlation between degree of white matter hyperintensities and global gray matter volume decline rate. Neuroradiology 53, 397–403 (2011). https://doi.org/10.1007/s00234-010-0746-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-010-0746-x

Keywords

  • Aging
  • White matter hyperintensities
  • Gray matter
  • Volumetry
  • Longitudinal