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Progressive hemorrhagic injury in patients with traumatic intracerebral hemorrhage: characteristics, risk factors and impact on management

  • Original Article - Brain Injury
  • Published:
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Abstract

Background

Progressive hemorrhagic injury (PHI) is a common occurrence in clinical practice; however, how PHI affects clinical management remains unclear. We attempt to evaluate the characteristics and risk factors of PHI and also investigate how PHI influences clinical management in traumatic intracerebral hemorrhage (TICH) patients.

Methods

This retrospective study included a cohort of 181 patients with TICH who initially underwent conservative treatment and they were dichotomized into a PHI group and a non-PHI group. Clinical data were reviewed for comparison. Multivariate logistic regression analysis was applied to identify predictors of PHI and delayed operation.

Results

Overall, 68 patients (37.6%) experienced PHI and 27 (14.9%) patients required delayed surgery. In the PHI group, 17 patients needed late operation; in the non-PHI group, 10 patients received decompressive craniectomy. Compared to patients with non-PHI, the PHI group was more likely to require late operation (P = 0.005, 25.0 vs 8.8%), which took place within 48 h (P = 0.01, 70.6 vs 30%). Multivariate logistic regression identified past medical history of hypertension (odds ratio [OR] = 4.56; 95% confidence interval [CI] = 2.04–10.45), elevated international normalized ratio (INR) (OR = 20.93; 95% CI 7.72–71.73) and linear bone fracture (OR = 2.11; 95% CI = 1.15–3.91) as independent risk factors for PHI. Hematoma volume of initial CT scan >5 mL (OR = 3.80; 95% CI = 1.79–8.44), linear bone fracture (OR = 3.21; 95% CI = 1.47–7.53) and PHI (OR = 3.49; 95% CI = 1.63–7.77) were found to be independently associated with delayed operation.

Conclusions

Past medical history of hypertension, elevated INR and linear bone fracture were predictors for PHI. Additionally, the latter was strongly predictive of delayed operation in the studied cohort.

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References

  1. Alahmadi H, Vachhrajani S, Cusimano MD (2010) The natural history of brain contusion: an analysis of radiological and clinical progression. J Neurosurg 112:1139–1145

    Article  PubMed  Google Scholar 

  2. Allard CB, Scarpelini S, Rhind SG, Baker AJ, Shek PN, Tien H, Fernando M, Tremblay L, Morrison LJ, Pinto R, Rizoli SB (2009) Abnormal coagulation tests are associated with progression of traumatic intracranial hemorrhage. J Trauma 67:959–967

    Article  PubMed  Google Scholar 

  3. Bullock MR, Chesnut R, Ghajar J, Gordon D, Hartl R, Newell DW, Servadei F, Walters BC, Wilberger JE (2006) Guidelines for the surgical management of traumatic brain injury. Neurosurgery 58(3 Suppl):S1-S60, discussion Si-iv

  4. Cepeda S, Gomez PA, Castano-Leon AM, Martinez-Perez R, Munarriz PM, Lagares A (2015) Traumatic intracerebral hemorrhage: risk factors associated with progression. J Neurotrauma 32:1246–1253

    Article  PubMed  Google Scholar 

  5. Chang EF, Meeker M, Holland MC (2006) Acute traumatic intraparenchymal hemorrhage: risk factors for progression in the early post-injury period. Neurosurgery 58:647–656, discussion 647–656

    Article  PubMed  Google Scholar 

  6. da Luz LT, Nascimento B, Rizoli S (2013) Thrombelastography (TEG(R)): practical considerations on its clinical use in trauma resuscitation. Scand J Trauma Resusc Emerg Med 21:29

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dzik WH (2007) The James Blundell Award Lecture 2006: transfusion and the treatment of haemorrhage: past, present and future. Transfus Med 17:367–374

    Article  CAS  PubMed  Google Scholar 

  8. Engstrom M, Romner B, Schalen W, Reinstrup P (2005) Thrombocytopenia predicts progressive hemorrhage after head trauma. J Neurotrauma 22:291–296

    Article  PubMed  Google Scholar 

  9. Folkerson LE, Sloan D, Cotton BA, Holcomb JB, Tomasek JS, Wade CE (2015) Predicting progressive hemorrhagic injury from isolated traumatic brain injury and coagulation. Surgery 158:655–661

    Article  PubMed  Google Scholar 

  10. Halpern CH, Reilly PM, Turtz AR, Stein SC (2008) Traumatic coagulopathy: the effect of brain injury. J Neurotrauma 25:997–1001

    Article  PubMed  Google Scholar 

  11. Harhangi BS, Kompanje EJ, Leebeek FW, Maas AI (2008) Coagulation disorders after traumatic brain injury. Acta Neurochir (Wien) 150:165–175, discussion 175

    Article  CAS  Google Scholar 

  12. Hunt H, Stanworth S, Curry N, Woolley T, Cooper C, Ukoumunne O, Zhelev Z, Hyde C (2015) Thromboelastography (TEG) and rotational thromboelastometry (ROTEM) for trauma induced coagulopathy in adult trauma patients with bleeding. Cochrane Database Syst Rev:CD010438

  13. Juratli TA, Zang B, Litz RJ, Sitoci KH, Aschenbrenner U, Gottschlich B, Daubner D, Schackert G, Sobottka SB (2014) Early hemorrhagic progression of traumatic brain contusions: frequency, correlation with coagulation disorders, and patient outcome: a prospective study. J Neurotrauma 31:1521–1527

    Article  PubMed  Google Scholar 

  14. Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J (1996) The ABCs of measuring intracerebral hemorrhage volumes. Stroke 27:1304–1305

    Article  CAS  PubMed  Google Scholar 

  15. Kurland D, Hong C, Aarabi B, Gerzanich V, Simard JM (2012) Hemorrhagic progression of a contusion after traumatic brain injury: a review. J Neurotrauma 29:19–31

    Article  PubMed  PubMed Central  Google Scholar 

  16. Laroche M, Kutcher ME, Huang MC, Cohen MJ, Manley GT (2012) Coagulopathy after traumatic brain injury. Neurosurgery 70:1334–1345

    Article  PubMed  Google Scholar 

  17. Manolio TA, Olson J, Longstreth WT (2003) Hypertension and cognitive function: pathophysiologic effects of hypertension on the brain. Curr Hypertens Rep 5:255–261

    Article  PubMed  Google Scholar 

  18. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T, Recombinant Activated Factor VII Intracerebral Hemorrhage Trial Investigators (2005) Recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 352:777–785

    Article  CAS  PubMed  Google Scholar 

  19. Narayan RK, Maas AI, Servadei F, Skolnick BE, Tillinger MN, Marshall LF, Traumatic Intracerebral Hemorrhage Study Group (2008) Progression of traumatic intracerebral hemorrhage: a prospective observational study. J Neurotrauma 25:629–639

    Article  PubMed  Google Scholar 

  20. Oertel M, Kelly DF, McArthur D, Boscardin WJ, Glenn TC, Lee JH, Gravori T, Obukhov D, McBride DQ, Martin NA (2002) Progressive hemorrhage after head trauma: predictors and consequences of the evolving injury. J Neurosurg 96:109–116

    Article  PubMed  Google Scholar 

  21. Pires PW, Dams Ramos CM, Matin N, Dorrance AM (2013) The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol 304:H1598–1614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. R Core Team(2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Accessed 06 Mar 2014

  23. Smith JS, Chang EF, Rosenthal G, Meeker M, von Koch C, Manley GT, Holland MC (2007) The role of early follow-up computed tomography imaging in the management of traumatic brain injury patients with intracranial hemorrhage. J Trauma 63:75–82

    Article  PubMed  Google Scholar 

  24. Stein SC, Spettell C, Young G, Ross SE (1993) Delayed and progressive brain injury in closed-head trauma: radiological demonstration. Neurosurgery 32:25–30, discussion 30–21

    Article  CAS  PubMed  Google Scholar 

  25. Stein SC, Young GS, Talucci RC, Greenbaum BH, Ross SE (1992) Delayed brain injury after head trauma: significance of coagulopathy. Neurosurgery 30:160–165

    Article  CAS  PubMed  Google Scholar 

  26. Tian Y, Salsbery B, Wang M, Yuan H, Yang J, Zhao Z, Wu X, Zhang Y, Konkle BA, Thiagarajan P, Li M, Zhang J, Dong JF (2015) Brain-derived microparticles induce systemic coagulation in a murine model of traumatic brain injury. Blood 125:2151–2159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tong WS, Zheng P, Xu JF, Guo YJ, Zeng JS, Yang WJ, Li GY, He B, Yu H (2011) Early CT signs of progressive hemorrhagic injury following acute traumatic brain injury. Neuroradiology 53:305–309

    Article  PubMed  Google Scholar 

  28. Wan X, Liu S, Wang S, Zhang S, Yang H, Ou Y, Zhao M, James L, Shu K, Chen J, Lei T (2016) Elderly patients with severe traumatic brain injury could benefit from surgical treatment. World Neurosurg 89:147–152

    Article  PubMed  Google Scholar 

  29. White CL, Griffith S, Caron JL (2009) Early progression of traumatic cerebral contusions: characterization and risk factors. J Trauma 67:508–514, discussion 514–505

    Article  PubMed  Google Scholar 

  30. Wu X, Du Z, Yu J, Sun Y, Pei B, Lu X, Tang Z, Yin M, Zhou L, Hu J (2014) Activity of factor VII in patients with isolated blunt traumatic brain injury: association with coagulopathy and progressive hemorrhagic injury. J Trauma Acute Care Surg 76:114–120

    Article  CAS  PubMed  Google Scholar 

  31. Yuan F, Ding J, Chen H, Guo Y, Wang G, Gao WW, Chen SW, Tian HL (2012) Predicting progressive hemorrhagic injury after traumatic brain injury: derivation and validation of a risk score based on admission characteristics. J Neurotrauma 29:2137–2142

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 430030, Wuhan, China

    Xueyan Wan, Ting Fan, Sheng Wang, Suojun Zhang, Shengwen Liu, Hongkuan Yang, Kai Shu & Ting Lei

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  1. Xueyan Wan
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  2. Ting Fan
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  3. Sheng Wang
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  6. Hongkuan Yang
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Corresponding author

Correspondence to Sheng Wang.

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Funding

The Science and Technology Department of Hubei Province provided financial support in the form of Natural Science Foundation of Hubei, China (No. 2014CFB151) funding, and the National Health and Family Planning Commission of the People’s Republic of China provided financial support in the form of the National Clinical Key Specialty Construction Project. The sponsor had no role in the design or conduct of this research.

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Comments

I read with interest the manuscript by Wan et al. entitled “Progressive hemorrhagic injury in patients with traumatic intracerebral hemorrhage: characteristics, risk factors and impact on management”. The authors present a cohort of 181 traumatic brain injury (TBI) patients suffering from cerebral contusions. They study associations between hematoma progression and delayed surgical intervention with admission parameters and find that history of hypertension, elevated INR and linear bone fracture were predictors for progressive hemorrhage, and the latter a strong predictor of a delayed surgery.

While several previous studies analysed a similar cohorts and reach similar conclusion as to what constitutes risk factors for progressing hemorrhages, such as Chang et al. (2006) and Oertel et al. (2002), which are both mentioned by the authors, the current manuscript presents a cohort with a relatively homogeneous injury (isolated cerebral contusions) and present a more extensive laboratory testing including fibrinogen. It is important to replicate previous findings, further stressing the need to better monitor and care for patients with progressing intracranial hemorrhage. However, this study also tries to determine what parameters are related to a secondary surgical intervention. While it is tempting, I do find it difficult to assess this type of intervention in a retrospective cohort where the decision by the individual surgeon is based on a multitude of factors which are difficult to retrospectively assess, introducing several types of biases. Instead, a prospective trial with a protocol is necessary to address the question of what the strongest predictors of delayed surgical intervention are. Moreover, in many western countries, we adhere to guidelines set forth by the Brain Trauma Foundation, stating that intracranial monitoring should be used as a tool for clinical decision making. While the authors mention that they measure intracranial pressure, it would be of interest to see how the parameters monitored in real time differed between the groups that did, and did not, need delayed surgery as this could perhaps in the future provide even swifter intervention to those who really need it.

Eric Thelin

Stockholm, Sweden

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Wan, X., Fan, T., Wang, S. et al. Progressive hemorrhagic injury in patients with traumatic intracerebral hemorrhage: characteristics, risk factors and impact on management. Acta Neurochir 159, 227–235 (2017). https://doi.org/10.1007/s00701-016-3043-6

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  • DOI: https://doi.org/10.1007/s00701-016-3043-6

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