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Validation and Comparison of Noncontrast CT Scores to Predict Intracerebral Hemorrhage Expansion

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Abstract

Background and purpose

The BAT, BRAIN, and HEP scores have been proposed to predict hematoma expansion (HE) with noncontrast computed tomography (NCCT). We sought to validate these tools and compare their diagnostic performance.

Methods

We retrospectively analyzed two cohorts of patients with primary intracerebral hemorrhage. HE expansion was defined as volume growth > 33% or > 6 mL. Two raters analyzed NCCT scans and calculated the scores, blinded to clinical and imaging data. The inter-rater reliability was assessed with the interclass correlation statistic. Discrimination and calibration were calculated with area under the curve (AUC) and Hosmer–Lemeshow χ2 statistic, respectively. AUC comparison between different scores was explored with DeLong test. We also calculated the sensitivity, specificity, positive, and negative predictive values of the dichotomized scores with cutoffs identified with the Youden’s index.

Results

A total of 230 subjects were included, of whom 86 (37.4%) experienced HE. The observed AUC for HE were 0.696 for BAT, 0.700 for BRAIN, and 0.648 for HEP. None of the scores had a significantly superior AUC compared with the others (all p > 0.4). All the scores had good calibration (all p > 0.3) and good-to-excellent inter-rater reliability (interclass correlation > 0.8). BAT ≥ 3 showed the highest specificity (0.81), whereas BRAIN ≥ 6 had the highest sensitivity (0.76).

Conclusions

The BAT, BRAIN, and HEP scores can predict HE with acceptable discrimination and require just a baseline NCCT scan. These tools may be used to stratify the risk of HE in clinical practice or randomized controlled trials.

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References

  1. Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet. 2009;373(9675):1632–44.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Morotti A, Goldstein JN. Diagnosis and management of acute intracerebral hemorrhage. Emerg Med Clin North Am. 2016;34(4):883–99.

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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(14):1238–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Steiner T, Bösel J. Options to restrict hematoma expansion after spontaneous intracerebral hemorrhage. Stroke. 2010;41(2):402–9.

    Article  PubMed  Google Scholar 

  5. 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(4):307–14.

    Article  PubMed  Google Scholar 

  6. Romero JM, Bart Brouwers H, Lu J, Almandoz JED, Kelly H, Heit J, et al. Prospective validation of the computed tomographic angiography spot sign score for Intracerebral hemorrhage. Stroke. 2013;44(11):3097–102.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Brouwers HB, Chang Y, Falcone GJ, Cai X, Ayres AM, Battey TWK, et al. Predicting hematoma expansion after primary intracerebral hemorrhage. JAMA Neurol. 2014;71(2):158.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Morotti A, Brouwers HB, Romero JM, Jessel MJ, Vashkevich A, Schwab K, et al. Intensive blood pressure reduction and spot sign in intracerebral hemorrhage. JAMA Neurol. 2017;74(8):950.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Boulouis G, Morotti A, Charidimou A, Dowlatshahi D, Goldstein JN. Noncontrast computed tomography markers of intracerebral hemorrhage expansion. Stroke. 2017;48(4):1120–5.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wang X, Arima H, Al-Shahi Salman R, Woodward M, Heeley E, Stapf C, et al. Clinical prediction algorithm (BRAIN) to determine risk of hematoma growth in acute intracerebral hemorrhage. Stroke. 2015;46(2):376–81.

    Article  CAS  PubMed  Google Scholar 

  11. Yao X, Xu Y, Siwila-Sackman E, Wu B, Selim M. The HEP score: a nomogram-derived hematoma expansion prediction scale. Neurocrit Care. 2015;23(2):179–87.

    Article  PubMed  Google Scholar 

  12. Morotti A, Dowlatshahi D, Boulouis G, Al-Ajlan F, Demchuk AM, Aviv RI, et al. Predicting intracerebral hemorrhage expansion with noncontrast computed tomography: the BAT score. Stroke. 2018;49(5):1163–9.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Pezzini A, Grassi M, Paciaroni M, Zini A, Silvestrelli G, Iacoviello L, et al. Obesity and the risk of intracerebral hemorrhage: the multicenter study on cerebral hemorrhage in Italy. Stroke. 2013;44(6):1584–9.

    Article  CAS  PubMed  Google Scholar 

  14. Pezzini A, Grassi M, Iacoviello L, Zedde M, Marcheselli S, Silvestrelli G, et al. Serum cholesterol levels, HMG-CoA reductase inhibitors and the risk of intracerebral haemorrhage. The Multicenter Study on Cerebral Haemorrhage in Italy (MUCH-Italy). J Neurol Neurosurg Psychiatry. 2016;87(9):924–9.

    Article  PubMed  Google Scholar 

  15. Hemphill JC, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2015;46(7):2032–60.

    Article  PubMed  Google Scholar 

  16. Li Q, Zhang G, Huang Y-J, Dong M-X, Lv F-J, Wei X, et al. Blend sign on computed tomography: novel and reliable predictor for early hematoma growth in patients with intracerebral hemorrhage. Stroke. 2018;49(5):1163–9.

    Article  Google Scholar 

  17. 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(8):961.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hallgren KA. Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol. 2012;8(1):23–34.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Steyerberg EW, Vickers AJ, Cook NR, Gerds T, Gonen M, Obuchowski N, et al. Assessing the performance of prediction models: a framework for traditional and novel measures. Epidemiology. 2010;21(1):128–38.

    Article  PubMed  PubMed Central  Google Scholar 

  20. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44(3):837–45.

    Article  CAS  PubMed  Google Scholar 

  21. Lord AS, Gilmore E, Choi HA, Mayer SA. Time course and predictors of neurological deterioration after intracerebral hemorrhage. Stroke. 2015;46(3):647–52.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Sprigg N, Flaherty K, Appleton JP, Salman RA-S, Bereczki D, Beridze M, et al. Tranexamic acid for hyperacute primary IntraCerebral Haemorrhage (TICH-2): an international randomised, placebo-controlled, phase 3 superiority trial. Lancet. 2018;391(10135):2107–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 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(11):1033–43.

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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(25):2355–65.

    Article  CAS  PubMed  Google Scholar 

  25. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med. 2008;358(20):2127–37.

    Article  CAS  PubMed  Google Scholar 

  26. Inoue Y, Miyashita F, Koga M, Minematsu K, Toyoda K. Unclear-onset intracerebral hemorrhage: clinical characteristics, hematoma features, and outcomes. Int J Stroke. 2017;12(9):961–8.

    Article  PubMed  Google Scholar 

  27. Fassbender K, Grotta JC, Walter S, Grunwald IQ, Ragoschke-Schumm A, Saver JL. Mobile stroke units for prehospital thrombolysis, triage, and beyond: benefits and challenges. Lancet Neurol. 2017;16(3):227–37.

    Article  PubMed  Google Scholar 

  28. 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(6):548–54.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Boulouis G, Charidimou A, Morotti A. Consensus needed for noncontrast CT markers in intracerebral hemorrhage. Am J Neuroradiol. 2018;39(6):E78–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Huttner HB, Steiner T, Hartmann M, Köhrmann M, Juettler E, Mueller S, et al. Comparison of ABC/2 estimation technique to computer-assisted planimetric analysis in warfarin-related intracerebral parenchymal hemorrhage. Stroke. 2006;37(2):404–8.

    Article  PubMed  Google Scholar 

  31. Morotti A, Boulouis G, Charidimou A, Schwab K, Kourkoulis C, Anderson CD, et al. Integration of computed tomographic angiography spot sign and noncontrast computed tomographic hypodensities to predict hematoma expansion. Stroke. 2018;49(9):2067–73.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Yu Z, Zheng J, Xia F, Guo R, Ma L, You C, et al. BAT score versus spot sign in predicting intracerebral hemorrhage expansion. World Neurosurg. 2019;126:e694–8. https://doi.org/10.1016/j.wneu.2019.02.125.

    Article  PubMed  Google Scholar 

  33. Yogendrakumar V, Ramsay T, Fergusson DA, Demchuk AM, Aviv RI, Rodriguez-Luna D, et al. Independent validation of the hematoma expansion prediction score: a non-contrast score equivalent in accuracy to the spot sign. Neurocrit Care. 2019. https://doi.org/10.1007/s12028-019-00740-5.

    Article  PubMed  Google Scholar 

  34. Al-Shahi Salman R, Frantzias J, Lee RJ, Lyden PD, Battey TWK, Ayres AM, et al. Absolute risk and predictors of the growth of acute spontaneous intracerebral haemorrhage: a systematic review and meta-analysis of individual patient data. Lancet Neurol. 2018;17(10):885–94.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Huynh TJ, Aviv RI, Dowlatshahi D, Gladstone DJ, Laupacis A, Kiss A, et al. Validation of the 9-point and 24-point hematoma expansion prediction scores and derivation of the PREDICT A/B scores. Stroke. 2015;46(11):3105–10.

    Article  CAS  PubMed  Google Scholar 

  36. Lim JX, Han JX, See AAQ, Lew VH, Chock WT, Ban VF, et al. External validation of hematoma expansion scores in spontaneous intracerebral hemorrhage in an Asian patient cohort. Neurocrit Care. 2018;30:394–404.

    Article  Google Scholar 

  37. Hilkens NA, van Asch CJJ, Werring DJ, Wilson D, Rinkel GJE, Algra A, et al. Predicting the presence of macrovascular causes in non-traumatic intracerebral haemorrhage: the DIAGRAM prediction score. J Neurol Neurosurg Psychiatry. 2018;89(7):674–9.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Scienze Cliniche e Sperimentali, Clinica Neurologica, Università degli Studi di Brescia, Brescia, Italy

    Loris Poli, Valeria De Giuli, Filomena Caria, Alessandro Padovani & Alessandro Pezzini

  2. Stroke Unit, IRCCS Fondazione Istituto Neurologico Nazionale C. Mondino, Pavia, Italy

    Eleonora Leuci, Elisa Candeloro, Alessandra Persico, Anna Cavallini & Andrea Morotti

  3. U.O. di Neurologia, Istituto Clinico Fondazione Poliambulanza, Brescia, Italy

    Paolo Costa

  4. Stroke Unit, Neurologia Vascolare, Azienda Socio-Sanitaria Territoriale (ASST) Spedali Civili, Brescia, Italy

    Massimo Gamba & Mauro Magoni

  5. Dipartimento di Neurologia d’Urgenza, IRCCS Fondazione Istituto Neurologico Nazionale C. Mondino, Pavia, Italy

    Giuseppe Micieli

Authors
  1. Loris Poli
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  2. Eleonora Leuci
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  3. Paolo Costa
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  4. Valeria De Giuli
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  5. Filomena Caria
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  8. Massimo Gamba
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  12. Alessandro Padovani
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  13. Alessandro Pezzini
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  14. Andrea Morotti
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Contributions

LP contributed to project development, data analysis, manuscript writing, and editing; EL contributed to project development, data collection, and manuscript editing; PC contributed to data collection and manuscript editing; VDeG contributed to data collection and manuscript editing; FC contributed to data collection and manuscript editing; EC contributed to data collection and manuscript editing; AP contributed to data collection and manuscript editing; MG contributed to data collection and manuscript editing; MM contributed to data collection and manuscript editing; GM contributed to data collection and manuscript editing; AC contributed to data collection and manuscript editing; AP contributed to project development, data analysis, and manuscript editing; AP contributed to project development, data analysis, and manuscript editing; AM contributed to project development, data analysis, manuscript writing, and editing.

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Correspondence to Loris Poli.

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All authors declare that they have no conflicts of interest.

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All the procedures for this study received approval from the local institutional review board at each site. Written informed consent was either obtained by patients, family members, or waived by the institutional review board.

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Poli, L., Leuci, E., Costa, P. et al. Validation and Comparison of Noncontrast CT Scores to Predict Intracerebral Hemorrhage Expansion. Neurocrit Care 32, 804–811 (2020). https://doi.org/10.1007/s12028-019-00797-2

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