Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
권호 표지
DOI QR코드

DOI QR Code

The Osteoporotic Condition as a Predictive Factor for Hemorrhagic Transformation in Acute Cardioembolic Stroke

  • Won, Yu Deok (Department of Neurosurgery, Hanyang University Guri Hospital) ;
  • Kim, Jae-Min (Department of Neurosurgery, Hanyang University Guri Hospital) ;
  • Ryu, Je-Il (Department of Neurosurgery, Hanyang University Guri Hospital) ;
  • Koh, Seong-Ho (Department of Neurology, Hanyang University Guri Hospital) ;
  • Han, Myung-Hoon (Department of Neurosurgery, Hanyang University Guri Hospital) ;
  • Cheong, Jin-Hwan (Department of Neurosurgery, Hanyang University Guri Hospital)
  • Received : 2021.06.15
  • Accepted : 2021.07.05
  • Published : 2021.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective : Hemorrhagic transformation (HT) can be occurred after acute cerebral infarction. HT can worse symptoms in severe cases and adversely affect long-term prognosis. As bone and vascular smooth muscle are composed of type 1 collagen, we aimed to identify a potential relationship between bone mineral density (BMD) and HT after acute cardioembolic stroke. Methods : As an indicator of BMD, we used mean frontal skull Hounsfield unit (HU) values on brain computed tomography (CT). Multivariative hazard ratios were calculated using Cox regression analysis to identify whether the osteoporotic condition was an independent predictor of HT after acute cardioembolic stroke. Results : This 11-year analysis enrolled 506 patients who diagnosed as acute cardioembolic infarction. The first tertile of skull HU value was an independent predictor of HT development compared to the third tertile (hazard ratio, 2.12; 95% confidence interval, 1.13-3.98; p=0.020). We observed no interactions between age and skull HU with respect to HT statistically. Conclusion : The results of this study revealed an association between osteoporotic conditions and HT development after acute cardioembolic stroke. A convenient method to measure the cancellous bone HU value of the frontal skull using brain CT images may be useful for predicting HT in patients with acute cerebral infarction.

Keywords

References

  1. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. : Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in acute stroke treatment. Stroke 24 : 35-41, 1993 https://doi.org/10.1161/01.STR.24.1.35
  2. Albayram S, Kizilkilic O, Yilmaz H, Tuysuz B, Kocer N, Islak C : Abnormalities in the cerebral arterial system in osteogenesis imperfecta. AJNR Am J Neuroradiol 24 : 748-750, 2003
  3. Alswat KA : Gender disparities in osteoporosis. J Clin Med Res 9 : 382-387, 2017 https://doi.org/10.14740/jocmr2970w
  4. Arba F, Rinaldi C, Caimano D, Vit F, Busto G, Fainardi E : Blood-brain barrier disruption and hemorrhagic transformation in acute ischemic stroke: systematic review and meta-analysis. Front Neurol 11 : 594613, 2021 https://doi.org/10.3389/fneur.2020.594613
  5. Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA : Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet 353 : 878-882, 1999 https://doi.org/10.1016/S0140-6736(98)09075-8
  6. Choi MK, Kim SM, Lim JK : Diagnostic efficacy of Hounsfield units in spine CT for the assessment of real bone mineral density of degenerative spine: correlation study between T-scores determined by DEXA scan and Hounsfield units from CT. Acta Neurochir (Wien) 158 : 1421-1427, 2016 https://doi.org/10.1007/s00701-016-2821-5
  7. Cucchiara B, Kasner SE, Tanne D, Levine SR, Demchuk A, Messe SR, et al. : Factors associated with intracerebral hemorrhage after thrombolytic therapy for ischemic stroke: pooled analysis of placebo data from the Stroke-Acute Ischemic NXY Treatment (SAINT) I and SAINT II trials. Stroke 40 : 3067-3072, 2009 https://doi.org/10.1161/STROKEAHA.109.554386
  8. Cucchiara B, Tanne D, Levine SR, Demchuk AM, Kasner S : A risk score to predict intracranial hemorrhage after recombinant tissue plasminogen activator for acute ischemic stroke. J Stroke Cerebrovasc Dis 17 : 331-333, 2008 https://doi.org/10.1016/j.jstrokecerebrovasdis.2008.03.012
  9. Fiorelli M, Bastianello S, von Kummer R, del Zoppo GJ, Larrue V, Lesaffre E, et al. : Hemorrhagic transformation within 36 hours of a cerebral infarct: relationships with early clinical deterioration and 3-month outcome in the European Cooperative Acute Stroke Study I (ECASS I) cohort. Stroke 30 : 2280-2284, 1999 https://doi.org/10.1161/01.STR.30.11.2280
  10. Frosen J, Joutel A : Smooth muscle cells of intracranial vessels: from development to disease. Cardiovasc Res 114 : 501-512, 2018 https://doi.org/10.1093/cvr/cvy002
  11. Gajko-Galicka A : Mutations in type I collagen genes resulting in osteogenesis imperfecta in humans. Acta Biochim Pol 49 : 433-441, 2002 https://doi.org/10.18388/abp.2002_3802
  12. Gooijer K, Rondeel JMM, van Dijk FS, Harsevoort AGJ, Janus GJM, Franken AAM : Bleeding and bruising in osteogenesis imperfecta: International Society on Thrombosis and Haemostasis bleeding assessment tool and haemostasis laboratory assessment in 22 individuals. Br J Haematol 187 : 509-517, 2019 https://doi.org/10.1111/bjh.16097
  13. Han MH, Won YD, Na MK, Kim CH, Kim JM, Ryu JI, et al. : Association between possible osteoporosis and shunt-dependent hydrocephalus after subarachnoid hemorrhage. Stroke 49 : 1850-1858, 2018 https://doi.org/10.1161/STROKEAHA.118.021063
  14. Kerenyi L, Kardos L, Szasz J, Szatmari S, Bereczki D, Hegedus K, et al. : Factors influencing hemorrhagic transformation in ischemic stroke: a clinicopathological comparison. Eur J Neurol 13 : 1251-1255, 2006 https://doi.org/10.1111/j.1468-1331.2006.01489.x
  15. Kidwell CS, Saver JL, Carneado J, Sayre J, Starkman S, Duckwiler G, et al. : Predictors of hemorrhagic transformation in patients receiving intraarterial thrombolysis. Stroke 33 : 717-724, 2002 https://doi.org/10.1161/hs0302.104110
  16. Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, et al. : The ABCs of measuring intracerebral hemorrhage volumes. Stroke 27 : 1304-1305, 1996 https://doi.org/10.1161/01.STR.27.8.1304
  17. Lansberg MG, Albers GW, Wijman CA : Symptomatic intracerebral hemorrhage following thrombolytic therapy for acute ischemic stroke: a review of the risk factors. Cerebrovasc Dis 24 : 1-10, 2007 https://doi.org/10.1159/000103110
  18. Larrue V, von Kummer RR, Muller A, Bluhmki E : Risk factors for severe hemorrhagic transformation in ischemic stroke patients treated with recombinant tissue plasminogen activator: a secondary analysis of the European-Australasian Acute Stroke Study (ECASS II). Stroke 32 : 438-441, 2001 https://doi.org/10.1161/01.STR.32.2.438
  19. Lodder J, Krijne-Kubat B, Broekman J : Cerebral hemorrhagic infarction at autopsy: cardiac embolic cause and the relationship to the cause of death. Stroke 17 : 626-629, 1986 https://doi.org/10.1161/01.STR.17.4.626
  20. Marini S, Morotti A, Ayres AM, Crawford K, Kourkoulis CE, Lena UK, et al. : Sex differences in intracerebral hemorrhage expansion and mortality. J Neurol Sci 379 : 112-116, 2017 https://doi.org/10.1016/j.jns.2017.05.057
  21. Mondal RK, Mann U, Sharma M : Osteogenesis imperfecta with bleeding diathesis. Indian J Pediatr 70 : 95-96, 2003 https://doi.org/10.1007/BF02722753
  22. Moulin T, Crepin-Leblond T, Chopard JL, Bogousslavsky J : Hemorrhagic infarcts. Eur Neurol 34 : 64-77, 1994 https://doi.org/10.1159/000117012
  23. Paciaroni M, Agnelli G, Corea F, Ageno W, Alberti A, Lanari A, et al. : Early hemorrhagic transformation of brain infarction: rate, predictive factors, and influence on clinical outcome: results of a prospective multi-center study. Stroke 39 : 2249-2256, 2008 https://doi.org/10.1161/STROKEAHA.107.510321
  24. Ponticos M, Partridge T, Black CM, Abraham DJ, Bou-Gharios G : Regulation of collagen type I in vascular smooth muscle cells by competition between Nkx2.5 and δEF1/ZEB1. Mol Cell Biol 24 : 6151-6161, 2004 https://doi.org/10.1128/MCB.24.14.6151-6161.2004
  25. Roof RL, Hall ED : Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats. J Neurotrauma 17 : 1155-1169, 2000 https://doi.org/10.1089/neu.2000.17.1155
  26. Schreiber JJ, Anderson PA, Rosas HG, Buchholz AL, Au AG : Hounsfield units for assessing bone mineral density and strength: a tool for osteoporosis management. J Bone Joint Surg Am 93 : 1057-1063, 2011 https://doi.org/10.2106/JBJS.J.00160
  27. Selim M, Fink JN, Kumar S, Caplan LR, Horkan C, Chen Y, et al. : Predictors of hemorrhagic transformation after intravenous recombinant tissue plasminogen activator: prognostic value of the initial apparent diffusion coefficient and diffusion-weighted lesion volume. Stroke 33 : 2047-2052, 2002 https://doi.org/10.1161/01.STR.0000023577.65990.4E
  28. Sims JR, Gharai LR, Schaefer PW, Vangel M, Rosenthal ES, Lev MH, et al. : ABC/2 for rapid clinical estimate of infarct, perfusion, and mismatch volumes. Neurology 72 : 2104-2110, 2009 https://doi.org/10.1212/WNL.0b013e3181aa5329
  29. Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, et al. : Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21 : 1619-1627, 2001 https://doi.org/10.1523/JNEUROSCI.21-05-01619.2001
  30. Won YD, Kim JM, Cheong JH, Ryu JI, Koh SH, Han MH : Effect of possible osteoporosis on parenchymal-type hemorrhagic transformation in patients with cardioembolic stroke. J Clin Med 10 : 2526, 2021 https://doi.org/10.3390/jcm10112526
  31. Won YD, Na MK, Kim CH, Kim JM, Cheong JH, Ryu JI, et al. : The frontal skull Hounsfield unit value can predict ventricular enlargement in patients with subarachnoid haemorrhage. Sci Rep 8 : 10178, 2018 https://doi.org/10.1038/s41598-018-28471-1