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.
Similar content being viewed by others
References
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):905–915
Hermier M, Nighoghossian N (2004) Contribution of susceptibility-weighted imaging to acute stroke assessment. Stroke 35(8):1989–1994
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):1831–1835
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):338–343
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):991–994
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):272–277
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):372–377
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):98–104
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):11–20
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):1377–1382
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):831–836
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):1539–1545
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–e426
Consultation WE (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363(9403):157–163
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):637–642
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):2211-2219
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):719–729
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):2526–2530
Tsushima Y, Tanizaki Y, Aoki J, Endo K (2002) MR detection of microhemorrhages in neurologically healthy adults. Neuroradiology 44(1):31–36
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):409–415
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):2845–2849
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):904–910
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):198–211
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):2136–2145
Yano K, Reed DM, MacLean CJ (1989) Serum cholesterol and hemorrhagic stroke in the Honolulu Heart Program. Stroke 20(11):1460–1465
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):59–66
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yamada, S., Satow, T., Fukuda, A. et al. Severe underweight and cerebral microbleeds. J Neurol 259, 2707–2713 (2012). https://doi.org/10.1007/s00415-012-6574-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-012-6574-7