Advertisement

Acta Neurochirurgica

, Volume 160, Issue 8, pp 1663–1670 | Cite as

Imaging-based outcome prediction in patients with intracerebral hemorrhage

  • Peter B. Sporns
  • André Kemmling
  • Jens Minnerup
  • Uta Hanning
  • Walter Heindel
Review Article - Neurosurgery general
  • 44 Downloads
Part of the following topical collections:
  1. Neurosurgery general

Abstract

Besides the established spot sign in computed tomography angiography (CTA), recently investigated imaging predictors of hematoma growth in noncontrast computed tomography (NCCT) suggest great potential for outcome prediction in patients with intracerebral hemorrhage (ICH). Secondary hematoma growth is an appealing target for therapeutic interventions because in contrast to other determined factors, it is potentially modifiable. Even more initial therapy studies failed to demonstrate clear therapeutic benefits, there is a need for an effective patient selection using imaging markers to identify patients at risk for poor outcome and thereby tailor individual treatments for every patient. Hence, this review gives an overview about the current literature on NCCT imaging markers for neurological outcome prediction and aims to clarify the association with the established spot sign. Moreover, it demonstrates the clinical impact of these parameters and gives a roadmap for future imaging research in patients with intracerebral hemorrhage.

Keywords

Cerebral hemorrhage Intracranial hemorrhages Neuroimaging 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. 1.
    Al-Nakshabandi NA (2001) The swirl sign. Radiology.  https://doi.org/10.1148/radiology.218.2.r01fe09433
  2. 2.
    Anderson CS, Heeley E, Huang Y, Wang J, Stapf C, Delcourt C, Lindley R, Robinson T, Lavados P, Neal B, Hata J, Arima H, Parsons M, Li Y, Wang J, Heritier S, Li Q, Woodward M, Simes RJ, Davis SM, Chalmers J, INTERACT2 Investigators (2013) Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med.  https://doi.org/10.1056/NEJMoa1214609
  3. 3.
    Auer LM, Deinsberger W, Niederkorn K, Gell G, Kleinert R, Schneider G, Holzer P, Bone G, Mokry M, Korner E (1989) Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: a randomized study. J Neurosurg.  https://doi.org/10.3171/jns.1989.70.4.0530
  4. 4.
    Barras CD, Tress BM, Christensen S, MacGregor L, Collins M, Desmond PM, Skolnick BE, Mayer SA, Broderick JP, Diringer MN, Steiner T, Davis SM, Recombinant Activated Factor VII Intracerebral Hemorrhage Trial Investigators (2009) Density and shape as CT predictors of intracerebral hemorrhage growth. Stroke.  https://doi.org/10.1161/STROKEAHA.108.536888
  5. 5.
    Blacquiere D, Demchuk AM, Al-Hazzaa M, Deshpande A, Petrcich W, Aviv RI, Rodriguez-Luna D, Molina CA, Silva Blas Y, Dzialowski I, Czlonkowska A, Boulanger JM, Lum C, Gubitz G, Padma V, Roy J, Kase CS, Bhatia R, Hill MD, Dowlatshahi D, PREDICT/Sunnybrook ICH CTA Study Group (2015) Intracerebral hematoma morphologic appearance on noncontrast computed tomography predicts significant hematoma expansion. Stroke.  https://doi.org/10.1161/STROKEAHA.115.010566
  6. 6.
    Boulouis G, Morotti A, Brouwers HB, Charidimou A, Jessel MJ, Auriel E, Pontes-Neto O, Ayres A, Vashkevich A, Schwab KM, Rosand J, Viswanathan A, Gurol ME, Greenberg SM, Goldstein JN (2016) Association between hypodensities detected by computed tomography and hematoma expansion in patients with intracerebral hemorrhage. JAMA Neurol.  https://doi.org/10.1001/jamaneurol.2016.1218
  7. 7.
    Boulouis G, Morotti A, Brouwers HB, Charidimou A, Jessel MJ, Auriel E, Pontes-Neto O, Ayres A, Vashkevich A, Schwab KM, Rosand J, Viswanathan A, Gurol ME, Greenberg SM, Goldstein JN (2016) Noncontrast computed tomography hypodensities predict poor outcome in intracerebral hemorrhage patients. Stroke.  https://doi.org/10.1161/STROKEAHA.116.014425
  8. 8.
    Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G (1993) Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. StrokeGoogle Scholar
  9. 9.
    Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Sauerbeck L, Spilker J, Duldner J, Khoury J (1997) Early hemorrhage growth in patients with intracerebral hemorrhage. StrokeGoogle Scholar
  10. 10.
    Cao D, Li Q, Fu P, Zhang J, Yang J (2017) Early hematoma enlargement in primary intracerebral hemorrhage. Curr Drug Targets.  https://doi.org/10.2174/1389450118666170427151011
  11. 11.
    Chan S, Conell C, Veerina KT, Rao VA, Flint AC (2015) Prediction of intracerebral haemorrhage expansion with clinical, laboratory, pharmacologic, and noncontrast radiographic variables. Int J Stroke.  https://doi.org/10.1111/ijs.12507
  12. 12.
    Davis SM, Broderick J, Hennerici M, Brun NC, Diringer MN, Mayer SA, Begtrup K, Steiner T, Recombinant Activated Factor VII Intracerebral Hemorrhage Trial Investigators (2006) Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology 66(8):1175–1181CrossRefPubMedGoogle Scholar
  13. 13.
    Delcourt C, Huang Y, Arima H, Chalmers J, Davis SM, Heeley EL, Wang J, Parsons MW, Liu G, Anderson CS, INTERACT1 Investigators (2012) Hematoma growth and outcomes in intracerebral hemorrhage: the INTERACT1 study. Neurology 79(4):314–319CrossRefPubMedGoogle Scholar
  14. 14.
    Delcourt C, Zhang S, Arima H, Sato S, Al-Shahi Salman R, Wang X, Davies L, Stapf C, Robinson T, Lavados PM, Chalmers J, Heeley E, Liu M, Lindley RI, Anderson CS, INTERACT2 investigators (2016) Significance of hematoma shape and density in intracerebral hemorrhage: the intensive blood pressure reduction in acute intracerebral hemorrhage trial study. Stroke.  https://doi.org/10.1161/STROKEAHA.116.012921
  15. 15.
    Dowlatshahi D, Brouwers HB, Demchuk AM, Hill MD, Aviv RI, Ufholz LA, Reaume M, Wintermark M, Hemphill JC 3rd, Murai Y, Wang Y, Zhao X, Wang Y, Li N, Sorimachi T, Matsumae M, Steiner T, Rizos T, Greenberg SM, Romero JM, Rosand J, Goldstein JN, Sharma M (2016) Predicting intracerebral hemorrhage growth with the spot sign: the effect of onset-to-scan time. Stroke.  https://doi.org/10.1161/STROKEAHA.115.012012
  16. 16.
    Du FZ, Jiang R, Gu M, He C, Guan J (2014) The accuracy of spot sign in predicting hematoma expansion after intracerebral hemorrhage: a systematic review and meta-analysis. PLoS One.  https://doi.org/10.1371/journal.pone.0115777
  17. 17.
    Fiorella D, Arthur AS, Mocco JD (2016) 305 The INVEST Trial: a randomized, controlled trial to investigate the safety and efficacy of image-guided minimally invasive endoscopic surgery with Apollo vs best medical management for supratentorial intracerebral hemorrhage. Neurosurgery.  https://doi.org/10.1227/01.neu.0000489793.60158.20
  18. 18.
    Fisher CM (1971) Pathological observations in hypertensive cerebral hemorrhage. J Neuropathol Exp NeurolGoogle Scholar
  19. 19.
    Fujii Y, Tanaka R, Takeuchi S, Koike T, Minakawa T, Sasaki O (1994) Hematoma enlargement in spontaneous intracerebral hemorrhage. J Neurosurg.  https://doi.org/10.3171/jns.1994.80.1.0051
  20. 20.
    Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Tanaka R (1998) Multivariate analysis of predictors of hematoma enlargement in spontaneous intracerebral hemorrhage. Stroke 29(6):1160–1166CrossRefPubMedGoogle Scholar
  21. 21.
    Hemphill JC 3rd, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, Fung GL, Goldstein JN, Macdonald RL, Mitchell PH, Scott PA, Selim MH, Woo D, American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology (2015) Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke.  https://doi.org/10.1161/STR.0000000000000069
  22. 22.
    Huynh TJ, Flaherty ML, Gladstone DJ, Broderick JP, Demchuk AM, Dowlatshahi D, Meretoja A, Davis SM, Mitchell PJ, Tomlinson GA, Chenkin J, Chia TL, Symons SP, Aviv RI (2014) Multicenter accuracy and interobserver agreement of spot sign identification in acute intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.113.002502
  23. 23.
    Kendall BE, Radue EW (1978) Computed tomography in spontaneous intracerebral haematomas. Br J Radiol.  https://doi.org/10.1259/0007-1285-51-608-563
  24. 24.
    Kim J, Smith A, Hemphill JC 3rd, Smith WS, Lu Y, Dillon WP, Wintermark M (2008) Contrast extravasation on CT predicts mortality in primary intracerebral hemorrhage. AJNR Am J Neuroradiol 29(3):520–525CrossRefPubMedGoogle Scholar
  25. 25.
    Li Q, Zhang G, Huang YJ, Dong MX, Lv FJ, Wei X, Chen JJ, Zhang LJ, Qin XY, Xie P (2015) Blend sign on computed tomography: novel and reliable predictor for early hematoma growth in patients with intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.115.009185
  26. 26.
    Li Q, Zhang G, Xiong X, Wang XC, Yang WS, Li KW, Wei X, Xie P (2016) Black hole sign: novel imaging marker that predicts hematoma growth in patients with intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.116.013186
  27. 27.
    Li Q, Liu QJ, Yang WS, Wang XC, Zhao LB, Xiong X, Li R, Cao D, Zhu D, Wei X, Xie P (2017) Island sign: an imaging predictor for early hematoma expansion and poor outcome in patients with intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.117.017985
  28. 28.
    Li Q, Yang WS, Wang XC, Cao D, Zhu D, Lv FJ, Liu Y, Yuan L, Zhang G, Xiong X, Li R, Hu YX, Qin XY, Xie P (2017) Blend sign predicts poor outcome in patients with intracerebral hemorrhage. PLoS One.  https://doi.org/10.1371/journal.pone.0183082
  29. 29.
    Liu L, Wang Y, Meng X, Li N, Tan Y, Nie X, Liu D, Zhao X, investigators TRAIGE (2017) Tranexamic acid for acute intracerebral hemorrhage growth predicted by spot sign trial: rationale and design. Int J Stroke.  https://doi.org/10.1177/1747493017694394
  30. 30.
    Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T, Trial Investigators FAST (2008) Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med.  https://doi.org/10.1056/NEJMoa0707534
  31. 31.
    Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, Karimi A, Shaw MD, Barer DH, investigators STICH (2005) Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet 365(9457):387–397CrossRefPubMedGoogle Scholar
  32. 32.
    Meretoja A, Churilov L, Campbell BC, Aviv RI, Yassi N, Barras C, Mitchell P, Yan B, Nandurkar H, Bladin C, Wijeratne T, Spratt NJ, Jannes J, Sturm J, Rupasinghe J, Zavala J, Lee A, Kleinig T, Markus R, Delcourt C, Mahant N, Parsons MW, Levi C, Anderson CS, Donnan GA, Davis SM (2014) The spot sign and tranexamic acid on preventing ICH growth–AUStralasia Trial (STOP-AUST): protocol of a phase II randomized, placebo-controlled, double-blind, multicenter trial. Int J Stroke.  https://doi.org/10.1111/ijs.12132
  33. 33.
    Morgenstern LB, Demchuk AM, Kim DH, Frankowski RF, Grotta JC (2001) Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage. NeurologyGoogle Scholar
  34. 34.
    Morotti A, Goldstein JN (2016) New oral anticoagulants and their reversal agents. Curr Treat Options Neurol.  https://doi.org/10.1007/s11940-016-0430-5
  35. 35.
    New PF, Aronow S (1976) Attenuation measurements of whole blood and blood fractions in computed tomography. Radiology.  https://doi.org/10.1148/121.3.635
  36. 36.
    Ovesen C, Havsteen I, Rosenbaum S, Christensen H (2014) Prediction and observation of post-admission hematoma expansion in patients with intracerebral hemorrhage. Front Neurol.  https://doi.org/10.3389/fneur.2014.00186
  37. 37.
    Qureshi AI, Palesch YY, Barsan WG, Hanley DF, Hsu CY, Martin RL, Moy CS, Silbergleit R, Steiner T, Suarez JI, Toyoda K, Wang Y, Yamamoto H, Yoon BW, ATACH-2 Trial Investigators and the Neurological Emergency Treatment Trials Network (2016) Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med.  https://doi.org/10.1056/NEJMoa1603460
  38. 38.
    Schlunk F, Greenberg SM (2015) The pathophysiology of intracerebral hemorrhage formation and expansion. Transl Stroke Res.  https://doi.org/10.1007/s12975-015-0410-1
  39. 39.
    Selariu E, Zia E, Brizzi M, Abul-Kasim K (2012) Swirl sign in intracerebral haemorrhage: definition, prevalence, reliability and prognostic value. BMC Neurol.  https://doi.org/10.1186/1471-2377-12-109
  40. 40.
    Shimoda Y, Ohtomo S, Arai H, Okada K, Tominaga T (2017) Satellite sign: a poor outcome predictor in intracerebral hemorrhage. Cerebrovasc Dis.  https://doi.org/10.1159/000477179
  41. 41.
    Spiotta AM, Fiorella D, Vargas J, Khalessi A, Hoit D, Arthur A, Lena J, Turk AS, Chaudry MI, Gutman F, Davis R, Chesler DA, Turner RD (2015) Initial multicenter technical experience with the Apollo device for minimally invasive intracerebral hematoma evacuation. Neurosurgery.  https://doi.org/10.1227/NEU.0000000000000698
  42. 42.
    Sporns PB, Schwake M, Kemmling A, Minnerup J, Schwindt W, Niederstadt T, Schmidt R, Hanning U (2017) Comparison of spot sign, blend sign and black hole sign for outcome prediction in patients with intracerebral hemorrhage. J Stroke.  https://doi.org/10.5853/jos.2016.02061
  43. 43.
    Sporns PB, Schwake M, Schmidt R, Kemmling A, Minnerup J, Schwindt W, Cnyrim C, Zoubi T, Heindel W, Niederstadt T, Hanning U (2017) Computed tomographic blend sign is associated with computed tomographic angiography spot sign and predicts secondary neurological deterioration after intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.116.014068
  44. 44.
    Steiner T, Bosel J (2010) Options to restrict hematoma expansion after spontaneous intracerebral hemorrhage. Stroke.  https://doi.org/10.1161/STROKEAHA.109.552919
  45. 45.
    Takeda R, Ogura T, Ooigawa H, Fushihara G, Yoshikawa S, Okada D, Araki R, Kurita H (2013) A practical prediction model for early hematoma expansion in spontaneous deep ganglionic intracerebral hemorrhage. Clin Neurol Neurosurg.  https://doi.org/10.1016/j.clineuro.2012.10.016
  46. 46.
    Tan LA, Lopes DK, Munoz LF, Shah Y, Bhabad S, Jhaveri M, Moftakhar R (2016) Minimally invasive evacuation of intraventricular hemorrhage with the Apollo vibration/suction device. J Clin Neurosci.  https://doi.org/10.1016/j.jocn.2015.08.037
  47. 47.
    Tsivgoulis G, Katsanos AH (2015) Intensive blood pressure reduction in acute intracerebral hemorrhage: a meta-analysis. Neurology.  https://doi.org/10.1212/WNL.0000000000001696
  48. 48.
    Wang CW, Liu YJ, Lee YH, Hueng DY, Fan HC, Yang FC, Hsueh CJ, Kao HW, Juan CJ, Hsu HH (2014) Hematoma shape, hematoma size, Glasgow coma scale score and ICH score: which predicts the 30-day mortality better for intracerebral hematoma? PLoS One.  https://doi.org/10.1371/journal.pone.0102326
  49. 49.
    Yu Z, Zheng J, Ali H, Guo R, Li M, Wang X, Ma L, Li H, You C (2017) Significance of satellite sign and spot sign in predicting hematoma expansion in spontaneous intracerebral hemorrhage. Clin Neurol Neurosurg 162:67–71CrossRefPubMedGoogle Scholar
  50. 50.
    Yu Z, Zheng J, Guo R, Ma L, Li M, Wang X, Lin S, Li H, You C (2017) Performance of blend sign in predicting hematoma expansion in intracerebral hemorrhage: a meta-analysis. Clin Neurol Neurosurg 163:84–89CrossRefPubMedGoogle Scholar
  51. 51.
    Zheng J, Yu Z, Xu Z, Li M, Wang X, Lin S, Li H, You C (2017) The accuracy of the spot sign and the blend sign for predicting hematoma expansion in patients with spontaneous intracerebral hemorrhage. Med Sci Monit 23:2250–2257CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Zuccarello M, Brott T, Derex L, Kothari R, Sauerbeck L, Tew J, Van Loveren H, Yeh HS, Tomsick T, Pancioli A, Khoury J, Broderick J (1999) Early surgical treatment for supratentorial intracerebral hemorrhage: a randomized feasibility study. Stroke. 30(9):1833–1839Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Clinical RadiologyUniversity Hospital of MuensterMuensterGermany
  2. 2.Institute of NeuroradiologyUniversity Hospital of LuebeckLuebeckGermany
  3. 3.Department of NeurologyUniversity Hospital of MuensterMuensterGermany
  4. 4.Department of Diagnostic and Interventional NeuroradiologyUniversity Medical Center Hamburg-EppendorfHamburgGermany

Personalised recommendations