Advertisement

Journal of Neurology

, Volume 259, Issue 12, pp 2707–2713 | Cite as

Severe underweight and cerebral microbleeds

  • Shigeki YamadaEmail author
  • Takeshi Satow
  • Atsushi Fukuda
  • Miki Ito
  • Masaaki Saiki
Original Communication

Abstract

Severely low and/or high body mass index (BMI) has been associated with intracerebral hemorrhage (ICH) risk in several large cohorts. The aim of this study is to assess the relationship between BMI and the presence of cerebral microbleeds. The presence and number of microbleeds were assessed on three-dimensional T2*-weighted gradient-recalled-echo sequence on magnetic resonance imaging (MRI). The inclusion criteria were participants aged >40 years old without aneurysmal subarachnoid hemorrhage and any type of cerebral vascular malformations. BMI was categorized into severe underweight (<17.0 kg/m2), mild underweight (17.0–18.4 kg/m2), normal range (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), and obese (≥30.0 kg/m2). Multivariate analyses were adjusted for age, sex, hypertension, smoking, alcohol, stroke subtype, severity of periventricular hyperintensities and deep white matter hyperintensities, and dementia. Additionally, we conducted stratification analyses by age, ICH, smoking habit, or history of any kind of cancer, respectively. A total of 384 participants (232 males, 152 females; mean age 67.5 years) met our inclusion criteria. Overall mean BMI was 22.8 ± 3.6 kg/m2. On multivariate analyses, severe underweight carried a significantly higher risk for cerebral microbleeds (3.48, 1.06–11.4) compared with normal range BMI, even after stratification in the subgroup aged ≥60 years (7.23, 1.57–33.2), nonsmokers (4.75, 1.10–20.5), noncancer subgroup (5.66, 1.31–24.5), and non-ICH subgroup (3.81, 1.14–12.7). We found that severe underweight was an independent significant risk factor for presence of cerebral microbleeds, even after effect of aging, smoking, or preexisting illness was eliminated.

Keywords

Cerebral microbleeds Body mass index Underweight Magnetic susceptibility Magnetic resonance imaging 

Notes

Acknowledgments

We would like to thank the patients for participating in this study. In addition we acknowledge the officers of Shiga Medical Center for Adults who managed baseline survey of clinical data. This research was supported by research funds intended to promote the hospital functions of the Japan Labor Health and Welfare Organization.

Conflicts of interest

Dr. Yamada and co-authors declare no disclosure and no conflicts of interest. He is the corresponding author for this study and the principal investigator. None of the authors received any royalties.

Ethical standard

All human studies must state that they have been approved by the appropriate ethics committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

References

  1. 1.
    Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M (1999) Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 30(4):905–915PubMedCrossRefGoogle Scholar
  2. 2.
    Hermier M, Nighoghossian N (2004) Contribution of susceptibility-weighted imaging to acute stroke assessment. Stroke 35(8):1989–1994PubMedCrossRefGoogle Scholar
  3. 3.
    Jeerakathil T, Wolf PA, Beiser A, Hald JK, Au R, Kase CS, Massaro JM, DeCarli C (2004) Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham Study. Stroke 35(8):1831–1835PubMedCrossRefGoogle Scholar
  4. 4.
    Nandigam RN, Viswanathan A, Delgado P, Skehan ME, Smith EE, Rosand J, Greenberg SM, Dickerson BC (2009) MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. AJNR Am J Neuroradiol 30(2):338–343PubMedCrossRefGoogle Scholar
  5. 5.
    Roob G, Schmidt R, Kapeller P, Lechner A, Hartung HP, Fazekas F (1999) MRI evidence of past cerebral microbleeds in a healthy elderly population. Neurology 52(5):991–994PubMedCrossRefGoogle Scholar
  6. 6.
    Vernooij MW, Ikram MA, Wielopolski PA, Krestin GP, Breteler MM, van der Lugt A (2008) Cerebral microbleeds: accelerated 3D T2*-weighted GRE MR imaging versus conventional 2D T2*-weighted GRE MR imaging for detection. Radiology 248(1):272–277PubMedCrossRefGoogle Scholar
  7. 7.
    Wycliffe ND, Choe J, Holshouser B, Oyoyo UE, Haacke EM, Kido DK (2004) Reliability in detection of hemorrhage in acute stroke by a new three-dimensional gradient recalled echo susceptibility-weighted imaging technique compared to computed tomography: a retrospective study. J Magn Reson Imaging 20(3):372–377PubMedCrossRefGoogle Scholar
  8. 8.
    Yamada S, Saiki M, Satow T, Fukuda A, Ito M, Minami S, Miyamoto S (2012) Periventricular and deep white matter leukoaraiosis have a closer association with cerebral microbleeds than age. Eur J Neurol 19(1):98–104PubMedCrossRefGoogle Scholar
  9. 9.
    Bazzano LA, Gu D, Whelton MR, Wu X, Chen CS, Duan X, Chen J, Chen JC, He J (2010) Body mass index and risk of stroke among Chinese men and women. Ann Neurol 67(1):11–20PubMedCrossRefGoogle Scholar
  10. 10.
    Cui R, Iso H, Toyoshima H, Date C, Yamamoto A, Kikuchi S, Kondo T, Watanabe Y, Koizumi A, Wada Y, Inaba Y, Tamakoshi A (2005) Body mass index and mortality from cardiovascular disease among Japanese men and women: the JACC study. Stroke 36(7):1377–1382PubMedCrossRefGoogle Scholar
  11. 11.
    Song YM, Sung J, Davey Smith G, Ebrahim S (2004) Body mass index and ischemic and hemorrhagic stroke: a prospective study in Korean men. Stroke 35(4):831–836PubMedCrossRefGoogle Scholar
  12. 12.
    Rexrode KM, Hennekens CH, Willett WC, Colditz GA, Stampfer MJ, Rich-Edwards JW, Speizer FE, Manson JE (1997) A prospective study of body mass index, weight change, and risk of stroke in women. JAMA 277(19):1539–1545PubMedCrossRefGoogle Scholar
  13. 13.
    Strazzullo P, D’Elia L, Cairella G, Garbagnati F, Cappuccio FP, Scalfi L (2010) Excess body weight and incidence of stroke: meta-analysis of prospective studies with 2 million participants. Stroke 41(5):e418–e426PubMedCrossRefGoogle Scholar
  14. 14.
    Consultation WE (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363(9403):157–163CrossRefGoogle Scholar
  15. 15.
    Fazekas F, Kleinert R, Roob G, Kleinert G, Kapeller P, Schmidt R, Hartung H-P (1999) Histopathologic Analysis of Foci of Signal Loss on Gradient-Echo T2*-Weighted MR Images in Patients with Spontaneous Intracerebral Hemorrhage: evidence of Microangiopathy-Related Microbleeds. AJNR Am J Neuroradiol 20(4):637–642PubMedGoogle Scholar
  16. 16.
    Berrington de Gonzalez A, Hartge P, Cerhan JR, Flint AJ, Hannan L, MacInnis RJ, Moore SC, Tobias GS, Anton-Culver H, Freeman LB, Beeson WL, Clipp SL, English DR, Folsom AR, Freedman DM, Giles G, Hakansson N, Henderson KD, Hoffman-Bolton J, Hoppin JA, Koenig KL, Lee IM, Linet MS, Park Y, Pocobelli G, Schatzkin A, Sesso HD, Weiderpass E, Willcox BJ, Wolk A, Zeleniuch-Jacquotte A, Willett WC, Thun MJ (2010) Body-mass index and mortality among 1.46 million white adults. N Engl J Med 363 (23):2211-2219Google Scholar
  17. 17.
    Zheng W, McLerran DF, Rolland B, Zhang X, Inoue M, Matsuo K, He J, Gupta PC, Ramadas K, Tsugane S, Irie F, Tamakoshi A, Gao YT, Wang R, Shu XO, Tsuji I, Kuriyama S, Tanaka H, Satoh H, Chen CJ, Yuan JM, Yoo KY, Ahsan H, Pan WH, Gu D, Pednekar MS, Sauvaget C, Sasazuki S, Sairenchi T, Yang G, Xiang YB, Nagai M, Suzuki T, Nishino Y, You SL, Koh WP, Park SK, Chen Y, Shen CY, Thornquist M, Feng Z, Kang D, Boffetta P, Potter JD (2011) Association between body-mass index and risk of death in more than 1 million Asians. N Engl J Med 364(8):719–729PubMedCrossRefGoogle Scholar
  18. 18.
    Biffi A, Cortellini L, Nearnberg CM, Ayres AM, Schwab K, Gilson AJ, Rost NS, Goldstein JN, Viswanathan A, Greenberg SM, Rosand J (2011) Body mass index and etiology of intracerebral hemorrhage. Stroke 42(9):2526–2530PubMedCrossRefGoogle Scholar
  19. 19.
    Tsushima Y, Tanizaki Y, Aoki J, Endo K (2002) MR detection of microhemorrhages in neurologically healthy adults. Neuroradiology 44(1):31–36PubMedCrossRefGoogle Scholar
  20. 20.
    Oki I, Nakamura Y, Okamura T, Okayama A, Hayakawa T, Kita Y, Ueshima H (2006) Body mass index and risk of stroke mortality among a random sample of Japanese adults: 19-year follow-up of NIPPON DATA80. Cerebrovasc Dis 22(5–6):409–415PubMedCrossRefGoogle Scholar
  21. 21.
    Lee SH, Bae HJ, Yoon BW, Kim H, Kim DE, Roh JK (2002) Low concentration of serum total cholesterol is associated with multifocal signal loss lesions on gradient-echo magnetic resonance imaging: analysis of risk factors for multifocal signal loss lesions. Stroke 33(12):2845–2849PubMedCrossRefGoogle Scholar
  22. 22.
    Iso H, Jacobs DR Jr, Wentworth D, Neaton JD, Cohen JD (1989) Serum cholesterol levels and six-year mortality from stroke in 350,977 men screened for the multiple risk factor intervention trial. N Engl J Med 320(14):904–910PubMedCrossRefGoogle Scholar
  23. 23.
    De Caterina R, Scarano M, Marfisi R, Lucisano G, Palma F, Tatasciore A, Marchioli R (2010) Cholesterol-lowering interventions and stroke: insights from a meta-analysis of randomized controlled trials. J Am Coll Cardiol 55(3):198–211PubMedCrossRefGoogle Scholar
  24. 24.
    Noda H, Iso H, Irie F, Sairenchi T, Ohtaka E, Doi M, Izumi Y, Ohta H (2009) Low-density lipoprotein cholesterol concentrations and death due to intraparenchymal hemorrhage: the Ibaraki Prefectural Health Study. Circulation 119(16):2136–2145PubMedCrossRefGoogle Scholar
  25. 25.
    Yano K, Reed DM, MacLean CJ (1989) Serum cholesterol and hemorrhagic stroke in the Honolulu Heart Program. Stroke 20(11):1460–1465PubMedCrossRefGoogle Scholar
  26. 26.
    Anderson KM, Wilson PW, Garrison RJ, Castelli WP (1987) Longitudinal and secular trends in lipoprotein cholesterol measurements in a general population sample. The Framingham Offspring Study. Atherosclerosis 68(1–2):59–66PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Shigeki Yamada
    • 1
    • 4
    Email author
  • Takeshi Satow
    • 1
  • Atsushi Fukuda
    • 2
    • 3
  • Miki Ito
    • 2
  • Masaaki Saiki
    • 1
  1. 1.Department of NeurosurgeryShiga Medical Center for AdultsMoriyamaJapan
  2. 2.Department of RadiologyShiga Medical Center for AdultsMoriyamaJapan
  3. 3.Department of RadiologyShiga Medical Center for ChildrenMoriyamaJapan
  4. 4.Department of NeurosurgeryHamamatsu Rosai HospitalHamamatsu-shiJapan

Personalised recommendations