Skip to main content
Log in

Expansion-Prone Hematoma: Defining a Population at High Risk of Hematoma Growth and Poor Outcome

  • Original Research
  • Published:
Neurocritical Care Aims and scope Submit manuscript

Abstract

Background

Noncontrast computed tomography (CT) markers are increasingly used for predicting hematoma expansion. The aim of our study was to investigate the predictive value of expansion-prone hematoma in predicting hematoma expansion and outcome in patients with intracerebral hemorrhage (ICH).

Methods

Between July 2011 and January 2017, ICH patients who underwent baseline CT scan within 6 h of symptoms onset and follow-up CT scan were recruited into the study. Expansion-prone hematoma was defined as the presence of one or more of the following imaging markers: blend sign, black hole sign, or island sign. The diagnostic performance of blend sign, black hole sign, island sign, and expansion-prone hematoma in predicting hematoma expansion was assessed. Predictors of hematoma growth and poor outcome were analyzed using multivariable logistical regression analysis.

Results

A total of 282 patients were included in our final analysis. Of 88 patients with early hematoma growth, 69 (78.4%) had expansion-prone hematoma. Expansion-prone hematoma had a higher sensitivity and accuracy for predicting hematoma expansion and poor outcome when compared with any single imaging marker. After adjustment for potential confounders, expansion-prone hematoma independently predicted hematoma expansion (OR 28.33; 95% CI 12.95–61.98) and poor outcome (OR 5.67; 95% CI 2.82–11.40) in multivariable logistic model.

Conclusion

Expansion-prone hematoma seems to be a better predictor than any single noncontrast CT marker for predicting hematoma expansion and poor outcome. Considering the high risk of hematoma expansion in these patients, expansion-prone hematoma may be a potential therapeutic target for anti-expansion treatment in future clinical studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet. 2009;373:1632–44.

    Article  PubMed  PubMed Central  Google Scholar 

  2. VanDerWerf J, Kurowski D, Siegler J, Ganguly T, Cucchiara B. Combination of intra-hematomal hypodensity on CT and BRAIN scoring improves prediction of hemorrhage expansion in ICH. Neurocrit Care. 2018. https://doi.org/10.1007/s12028-018-0507-y.

    Article  PubMed  Google Scholar 

  3. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9:167–76.

    Article  PubMed  Google Scholar 

  4. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al. Recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med. 2005;352:777–85.

    Article  CAS  PubMed  Google Scholar 

  5. Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. Stroke. 1993;24:987–93.

    Article  CAS  Google Scholar 

  6. Davis SM, Broderick J, Hennerici M, Brun NC, Diringer MN, Mayer SA, et al. Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology. 2006;66:1175–81.

    Article  CAS  Google Scholar 

  7. Delcourt C, Huang Y, Arima H, Chalmers J, Davis SM, Heeley EL, et al. Hematoma growth and outcomes in intracerebral hemorrhage: the INTERACT1 study. Neurology. 2012;79:314–9.

    Article  PubMed  Google Scholar 

  8. Fujii Y, Tanaka R, Takeuchi S, Koike T, Minakawa T, Sasaki O. Hematoma enlargement in spontaneous intracerebral hemorrhage. J Neurosurg. 1994;80:51–7.

    Article  CAS  PubMed  Google Scholar 

  9. Brouwers HB, Greenberg SM. Hematoma expansion following acute intracerebral hemorrhage. Cerebrovasc Dis. 2013;35:195–201.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wada R, Aviv RI, Fox AJ, Sahlas DJ, Gladstone DJ, Tomlinson G, et al. CT angiography “spot sign” predicts hematoma expansion in acute intracerebral hemorrhage. Stroke. 2007;38:1257–62.

    Article  PubMed  Google Scholar 

  11. Goldstein JN, Fazen LE, Snider R, Schwab K, Greenberg SM, Smith EE, et al. Contrast extravasation on CT angiography predicts hematoma expansion in intracerebral hemorrhage. Neurology. 2007;68:889–94.

    Article  CAS  PubMed  Google Scholar 

  12. Demchuk AM, Dowlatshahi D, Rodriguez-Luna D, Molina CA, Blas YS, Dzialowski I, et al. Prediction of haematoma growth and outcome in patients with intracerebral haemorrhage using the CT-angiography spot sign (PREDICT): a prospective observational study. Lancet Neurol. 2012;11:307–14.

    Article  PubMed  Google Scholar 

  13. Heit JJ, Iv M, Wintermark M. Imaging of intracranial hemorrhage. J Stroke. 2017;19(1):11–27.

    Article  PubMed  Google Scholar 

  14. Caplan LR. Recognizing and preventing intracerebral hematoma expansion. JAMA Neurol. 2016;73:914–5.

    Article  PubMed  Google Scholar 

  15. Morotti A, Brouwers HB, Romero JM, Jessel MJ, Vashkevich A, Schwab K, et al. Intensive blood pressure reduction and spot sign in intracerebral hemorrhage: a secondary analysis of a randomized clinical trial. JAMA Neurol. 2017;74:950–60.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Boulouis G, Morotti A, Charidimou A, Dowlatshahi D, Goldstein JN. Noncontrast computed tomography markers of intracerebral hemorrhage expansion. Stroke. 2017;48:1120–5.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Li Q, Zhang G, Huang YJ, Dong MX, Lv FJ, Wei X, et al. Blend sign on computed tomography: novel and reliable predictor for early hematoma growth in patients with intracerebral hemorrhage. Stroke. 2015;46:2119–23.

    Article  PubMed  Google Scholar 

  18. Li Q, Zhang G, Xiong X, Wang XC, Yang WS, Li KW, et al. Black hole sign: novel imaging marker that predicts hematoma growth in patients with intracerebral hemorrhage. Stroke. 2016;47:1777–81.

    Article  PubMed  Google Scholar 

  19. Li Q, Liu QJ, Yang WS, Wang XC, Zhao LB, Xiong X, et al. Island sign: an imaging predictor for early hematoma expansion and poor outcome in patients with intracerebral hemorrhage. Stroke. 2017;48:3019–25.

    Article  PubMed  Google Scholar 

  20. Dowlatshahi D, Demchuk AM, Flaherty ML, Ali M, Lyden PL, Smith EE. Defining hematoma expansion in intracerebral hemorrhage: relationship with patient outcomes. Neurology. 2011;76:1238–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Boulouis G, Morotti A, Brouwers HB, Charidimou A, Jessel MJ, Auriel E, et al. Association between hypodensities detected by computed tomography and hematoma expansion in patients with intracerebral hemorrhage. JAMA Neurol. 2016;73:961–8.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Anderson CS, Heeley E, Huang Y, Wang J, Stapf C, Delcourt C, et al. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med. 2013;368:2355–65.

    Article  CAS  PubMed  Google Scholar 

  23. Koch S, Elkind MS, Testai FD, Brown WM, Martini S, Sheth KN, et al. Racial-ethnic disparities in acute blood pressure after intracerebral hemorrhage. Neurology. 2016;87:786–91.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Roquer J, Rodríguez-Campello A, Jiménez-Conde J, Cuadrado-Godia E, Giralt-Steinhauer E, Vivanco Hidalgo RM, et al. Sex-related differences in primary intracerebral hemorrhage. Neurology. 2016;87:257–62.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Morotti A, Boulouis G, Romero JM, Brouwers HB, Jessel MJ, Vashkevich A, et al. Blood pressure reduction and noncontrast CT markers of intracerebral hemorrhage expansion. Neurology. 2017;89:548–54.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Boulouis G, Morotti A, Brouwers HB, Charidimou A, Jessel MJ, Auriel E, et al. Noncontrast computed tomography hypodensities predict poor outcome in intracerebral hemorrhage patients. Stroke. 2016;47:2511–6.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Li Q, Yang WS, Wang XC, Cao D, Zhu D, Lv FJ, et al. Blend sign predicts poor outcome in patients with intracerebral hemorrhage. PLoS ONE. 2017;12:e0183082.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wu G, Shen Z, Wang L, Sun S, Luo J, Mao Y. Post-operative re-bleeding in patients with hypertensive ICH is closely associated with the CT blend sign. BMC Neurol. 2017;17:131.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Zheng J, Yu Z, Xu Z, Li M, Wang X, Lin S, et al. The accuracy of the spot sign and the blend sign for predicting hematoma expansion in patients with spontaneous intracerebral hemorrhage. Med Sci Monit. 2017;23:2250–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sporns PB, Schwake M, Kemmling A, Minnerup J, Schwindt W, Niederstadt T, et al. Comparison of spot sign, blend sign and black hole sign for outcome prediction in patients with intracerebral hemorrhage. J Stroke. 2017;19:333–9.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Yu Z, Zheng J, Ma L, Guo R, Li M, Wang X, et al. The predictive accuracy of the black hole sign and the spot sign for hematoma expansion in patients with spontaneous intracerebral hemorrhage. Neurol Sci. 2017;38:1591–7.

    Article  PubMed  Google Scholar 

  32. Sporns PB, Schwake M, Schmidt R, Kemmling A, Minnerup J, Schwindt W, et al. Computed tomographic blend sign is associated with computed tomographic angiography spot sign and predicts secondary neurological deterioration after intracerebral hemorrhage. Stroke. 2017;48:131–5.

    Article  PubMed  Google Scholar 

  33. Sheth KN, Cushing TA, Wendell L, Lev MH, Romero JM, Schwab K, et al. Comparison of hematoma shape and volume estimates in warfarin versus non-warfarin-related intracerebral hemorrhage. Neurocrit Care. 2010;12:30–4.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Barras CD, Tress BM, Christensen S, MacGregor L, Collins M, Desmond PM, et al. Density and shape as CT predictors of intracerebral hemorrhage growth. Stroke. 2009;40:1325–31.

    Article  PubMed  Google Scholar 

  35. Delcourt C, Zhang S, Arima H, Sato S, Al-Shahi Salman R, Wang X, et al. Significance of hematoma shape and density in intracerebral hemorrhage: the intensive blood pressure reduction in acute intracerebral hemorrhage trial study. Stroke. 2016;47:1227–32.

    Article  CAS  PubMed  Google Scholar 

  36. Qureshi AI, Palesch YY, Barsan WG, Hanley DF, Hsu CY, Martin RL, et al. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med. 2016;375:1033–43.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Butcher K, Selim M. Acute blood pressure management in intracerebral hemorrhage: equipoise resists an attack. Stroke. 2016;47:3065–6.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (Grant No. 81200899, the National Health and Family Planning Commission of Chongqing (Grant No. 2017MSXM014), China Association for Science and Technology Young Talent Project (Grant No. 2017QNRC001) and National Key Research and Development Program of China (Nos. 2018YFC1312200, 2018YFC1312203).

Author information

Authors and Affiliations

Authors

Contributions

QL had full access to all of the data in the study. QL, Z-PT, PX contributed to study concept and design; QL, Y-QS, X-FX, DC, RL, LD, MW helped in acquisition, analysis, or interpretation of data; QL contributed to drafting of the manuscript; QL, Y-QS, X-FX, M-ZX, Z-PT, GW, PX helped in critical revision of the manuscript; W-SY, F-JL contributed to statistical analysis; QL helped in obtaining funding; QL, PX contributed to administrative, technical, or material support.

Corresponding authors

Correspondence to Qi Li, Guo-Feng Wu, Zhou-Ping Tang or Peng Xie.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests. No other Disclosures were reported.

Ethical Approval

The Ethics Committee of the First Affiliated Hospital of Chongqing Medical University, China, approved the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Q., Shen, YQ., Xie, XF. et al. Expansion-Prone Hematoma: Defining a Population at High Risk of Hematoma Growth and Poor Outcome. Neurocrit Care 30, 601–608 (2019). https://doi.org/10.1007/s12028-018-0644-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-018-0644-3

Keywords

Navigation