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The Impact of Invasive Brain Oxygen Pressure Guided Therapy on the Outcome of Patients with Traumatic Brain Injury: A Systematic Review and Meta-Analysis

Neurocritical Care volume 37, pages 779–789 (2022)Cite this article

Abstract

Traumatic brain injury (TBI) is a major public health burden, causing death and disability worldwide. Intracranial hypertension and brain hypoxia are the main mechanisms of secondary brain injury. As such, management strategies guided by intracranial pressure (ICP) and brain oxygen (PbtO2) monitoring could improve the prognosis of these patients. Our objective was to summarize the current evidence regarding the impact of PbtO2-guided therapy on the outcome of patients with TBI. We performed a systematic search of PubMed, Scopus, and the Cochrane library databases, following the protocol registered in PROSPERO. Only studies comparing PbtO2/ICP–guided therapy with ICP-guided therapy were selected. Primary outcome was neurological outcome at 3 and 6 months assessed by using the Glasgow Outcome Scale; secondary outcomes included hospital and long-term mortality, burden of intracranial hypertension, and brain tissue hypoxia. Out of 6254 retrieved studies, 15 studies (n = 37,245 patients, of who 2184 received PbtO2-guided therapy) were included in the final analysis. When compared with ICP-guided therapy, the use of combined PbO2/ICP–guided therapy was associated with a higher probability of favorable neurological outcome (odds ratio 2.21 [95% confidence interval 1.72–2.84]) and of hospital survival (odds ratio 1.15 [95% confidence interval 1.04–1.28]). The heterogeneity (I2) of the studies in each analysis was below 40%. However, the quality of evidence was overall low to moderate. In this meta-analysis, PbtO2-guided therapy was associated with reduced mortality and more favorable neurological outcome in patients with TBI. The low-quality evidence underlines the need for the results from ongoing phase III randomized trials.

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References

  1. Injury GBDTB, Spinal Cord Injury C. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 2019;18(1):56–87. DOI: https://doi.org/10.1016/S1474-4422(18)30415-0.

  2. Dewan MC, Rattani A, Gupta S, et al. Estimating the global incidence of traumatic brain injury. J Neurosurg. 2018. https://doi.org/10.3171/2017.10.JNS17352.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kaur P, Sharma S. Recent advances in pathophysiology of traumatic brain injury. Curr Neuropharmacol. 2018;16(8):1224–38. https://doi.org/10.2174/1570159X15666170613083606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Akerlund CA, Donnelly J, Zeiler FA, et al. Impact of duration and magnitude of raised intracranial pressure on outcome after severe traumatic brain injury: A CENTER-TBI high-resolution group study. PLoS ONE. 2020;15(12): e0243427. https://doi.org/10.1371/journal.pone.0243427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Carney N, Totten AM, O’Reilly C, et al. Guidelines for the management of severe traumatic brain injury. Fourth Edn Neurosurg. 2017;80(1):6–15. https://doi.org/10.1227/NEU.0000000000001432.

    Article  Google Scholar 

  6. Hawryluk GWJ, Aguilera S, Buki A, et al. A management algorithm for patients with intracranial pressure monitoring: the Seattle International Severe Traumatic Brain Injury Consensus Conference (SIBICC). Intensive Care Med. 2019;45(12):1783–94. https://doi.org/10.1007/s00134-019-05805-9.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chesnut RM, Temkin N, Carney N, et al. A trial of intracranial-pressure monitoring in traumatic brain injury. N Engl J Med. 2012;367(26):2471–81. https://doi.org/10.1056/NEJMoa1207363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Maloney-Wilensky E, Gracias V, Itkin A, et al. Brain tissue oxygen and outcome after severe traumatic brain injury: a systematic review. Crit Care Med. 2009;37(6):2057–63. https://doi.org/10.1097/CCM.0b013e3181a009f8.

    Article  PubMed  Google Scholar 

  9. Oddo M, Levine JM, Mackenzie L, et al. Brain hypoxia is associated with short-term outcome after severe traumatic brain injury independently of intracranial hypertension and low cerebral perfusion pressure. Neurosurgery. 2011;69(5):1037–45. https://doi.org/10.1227/NEU.0b013e3182287ca7.

    Article  PubMed  Google Scholar 

  10. Stiefel MF, Udoetuk JD, Spiotta AM, et al. Conventional neurocritical care and cerebral oxygenation after traumatic brain injury. J Neurosurg. 2006;105(4):568–75. https://doi.org/10.3171/jns.2006.105.4.568.

    Article  PubMed  Google Scholar 

  11. Bouzat P, Sala N, Payen JF, Oddo M. Beyond intracranial pressure: optimization of cerebral blood flow, oxygen, and substrate delivery after traumatic brain injury. Ann Intensive Care. 2013;3(1):23. https://doi.org/10.1186/2110-5820-3-23.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Xie Q, Wu HB, Yan YF, Liu M, Wang ES. Mortality and outcome comparison between brain tissue oxygen combined with intracranial pressure/cerebral perfusion pressure-guided therapy and intracranial pressure/cerebral perfusion pressure-guided therapy in traumatic brain injury: a meta-analysis. World Neurosurg. 2017;100:118–27. https://doi.org/10.1016/j.wneu.2016.12.097.

    Article  PubMed  Google Scholar 

  13. Nangunoori R, Maloney-Wilensky E, Stiefel M, et al. Brain tissue oxygen-based therapy and outcome after severe traumatic brain injury: a systematic literature review. Neurocrit Care. 2012;17(1):131–8. https://doi.org/10.1007/s12028-011-9621-9.

    Article  CAS  PubMed  Google Scholar 

  14. Komisarow JM, Toro C, Curley J, et al. Utilization of brain tissue oxygenation monitoring and association with mortality following severe traumatic brain injury. Neurocrit Care. 2022;36(2):350–6. https://doi.org/10.1007/s12028-021-01394-y.

    Article  CAS  PubMed  Google Scholar 

  15. Hoffman H, Abi-Aad K, Bunch KM, Beutler T, Otite FO, Chin LS. Outcomes associated with brain tissue oxygen monitoring in patients with severe traumatic brain injury undergoing intracranial pressure monitoring. J Neurosurg. 2021;135(6):1799–806. https://doi.org/10.3171/2020.11.JNS203739.

    Article  CAS  PubMed  Google Scholar 

  16. Okonkwo DO, Shutter LA, Moore C, et al. Brain oxygen optimization in severe traumatic brain injury phase-II: a phase II randomized trial. Crit Care Med. 2017;45(11):1907–14. https://doi.org/10.1097/CCM.0000000000002619.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lin CM, Lin MC, Huang SJ, et al. A prospective randomized study of brain tissue oxygen pressure-guided management in moderate and severe traumatic brain injury patients. Biomed Res Int. 2015;2015: 529580. https://doi.org/10.1155/2015/529580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Spiotta AM, Stiefel MF, Gracias VH, et al. Brain tissue oxygen-directed management and outcome in patients with severe traumatic brain injury. J Neurosurg. 2010;113(3):571–80. https://doi.org/10.3171/2010.1.JNS09506.

    Article  PubMed  Google Scholar 

  19. Narotam PK, Morrison JF, Nathoo N. Brain tissue oxygen monitoring in traumatic brain injury and major trauma: outcome analysis of a brain tissue oxygen-directed therapy. J Neurosurg. 2009;111(4):672–82. https://doi.org/10.3171/2009.4.JNS081150.

    Article  PubMed  Google Scholar 

  20. Stiefel MF, Spiotta A, Gracias VH, et al. Reduced mortality rate in patients with severe traumatic brain injury treated with brain tissue oxygen monitoring. J Neurosurg. 2005;103(5):805–11. https://doi.org/10.3171/jns.2005.103.5.0805.

    Article  PubMed  Google Scholar 

  21. Lee HC, Chuang HC, Cho DY, Cheng KF, Lin PH, Chen CC. Applying cerebral hypothermia and brain oxygen monitoring in treating severe traumatic brain injury. World Neurosurg. 2010;74(6):654–60. https://doi.org/10.1016/j.wneu.2010.06.019.

    Article  PubMed  Google Scholar 

  22. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372: n71. https://doi.org/10.1136/bmj.n71.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Barrit S, Al Barajraji M, El Hadweh S, et al. Brain tissue oxygenation-guided therapy and outcome in traumatic brain injury: a single-center matched cohort study. Brain Sci. 2022;12(7):887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343: d5928. https://doi.org/10.1136/bmj.d5928.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sterne JA, Hernan MA, Reeves BC, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355: i4919. https://doi.org/10.1136/bmj.i4919.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5. https://doi.org/10.1007/s10654-010-9491-z.

    Article  PubMed  Google Scholar 

  27. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924–6. https://doi.org/10.1136/bmj.39489.470347.AD.

    Article  PubMed  PubMed Central  Google Scholar 

  28. McMillan T, Wilson L, Ponsford J, Levin H, Teasdale G, Bond M. The glasgow outcome scale - 40 years of application and refinement. Nat Rev Neurol. 2016;12(8):477–85. https://doi.org/10.1038/nrneurol.2016.89.

    Article  PubMed  Google Scholar 

  29. Martini RP, Deem S, Yanez ND, et al. Management guided by brain tissue oxygen monitoring and outcome following severe traumatic brain injury. J Neurosurg. 2009;111(4):644–9. https://doi.org/10.3171/2009.2.JNS08998.

    Article  PubMed  Google Scholar 

  30. Adamides AA, Cooper DJ, Rosenfeldt FL, et al. Focal cerebral oxygenation and neurological outcome with or without brain tissue oxygen-guided therapy in patients with traumatic brain injury. Acta Neurochir (Wien). 2009;151(11):1399–409. https://doi.org/10.1007/s00701-009-0398-y.

    Article  CAS  Google Scholar 

  31. Green JA, Pellegrini DC, Vanderkolk WE, Figueroa BE, Eriksson EA. Goal directed brain tissue oxygen monitoring versus conventional management in traumatic brain injury: an analysis of in hospital recovery. Neurocrit Care. 2013;18(1):20–5. https://doi.org/10.1007/s12028-012-9797-7.

    Article  CAS  PubMed  Google Scholar 

  32. Wang Z, Zhang R, Han Z, et al. Application of continuous monitoring of intracranial pressure and brain oxygen partial pressure in the treatment of patients with severe craniocerebral injury. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2021;33(4):449–54. https://doi.org/10.3760/cma.j.cn121430-20201106-00700.

    Article  PubMed  Google Scholar 

  33. McCarthy MC, Moncrief H, Sands JM, et al. Neurologic outcomes with cerebral oxygen monitoring in traumatic brain injury. Surgery. 2009;146(4):585–90. https://doi.org/10.1016/j.surg.2009.06.059.

    Article  PubMed  Google Scholar 

  34. Barrit S, Al Barajraji M, El Hadwe S, et al. Brain tissue oxygenation-guided therapy and outcome in traumatic brain injury: a single-center matched cohort study. Hopital Erasme: Université Libre de Bruxelles (ULB), Brussels, Belgium; 2022.

    Google Scholar 

  35. Meixensberger J, Jaeger M, Vath A, Dings J, Kunze E, Roosen K. Brain tissue oxygen guided treatment supplementing ICP/CPP therapy after traumatic brain injury. J Neurol Neurosurg Psychiatry. 2003;74(6):760–4. https://doi.org/10.1136/jnnp.74.6.760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Citerio G, Oddo M, Taccone FS. Recommendations for the use of multimodal monitoring in the neurointensive care unit. Curr Opin Crit Care. 2015;21(2):113–9. https://doi.org/10.1097/MCC.0000000000000179.

    Article  PubMed  Google Scholar 

  37. LeRoux P, Menon DK, Citerio G, et al. Consensus summary statement of the International Multidisciplinary Consensus Conference on Multimodality Monitoring in Neurocritical Care : a statement for healthcare professionals from the Neurocritical Care Society and the European Society of Intensive Care Medicine. Intensive Care Med 2014;40(9):1189–209. https://doi.org/10.1007/s00134-014-3369-6.

  38. Kofke WA, Rajagopalan S, Ayubcha D, et al. Defining a taxonomy of intracranial hypertension: is ICP more than just a number? J Neurosurg Anesthesiol. 2020;32(2):120–31. https://doi.org/10.1097/ANA.0000000000000609.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Oddo M, Bosel J, Participants in the International Multidisciplinary Consensus Conference on Multimodality M. Monitoring of brain and systemic oxygenation in neurocritical care patients. Neurocrit Care 2014;21 Suppl 2:S103–20. https://doi.org/10.1007/s12028-014-0024-6.

  40. Rose JC, Neill TA, Hemphill JC. Continuous monitoring of the microcirculation in neurocritical care: an update on brain tissue oxygenation. Curr Opin Crit Care. 2006;12(2):97–102. https://doi.org/10.1097/01.ccx.0000216574.26686.e9.

    Article  PubMed  Google Scholar 

  41. Chang JJ, Youn TS, Benson D, et al. Physiologic and functional outcome correlates of brain tissue hypoxia in traumatic brain injury. Crit Care Med. 2009;37(1):283–90. https://doi.org/10.1097/CCM.0b013e318192fbd7.

    Article  CAS  PubMed  Google Scholar 

  42. De Georgia MA. Brain tissue oxygen monitoring in neurocritical care. J Intensive Care Med. 2015;30(8):473–83. https://doi.org/10.1177/0885066614529254.

    Article  PubMed  Google Scholar 

  43. van den Brink WA, van Santbrink H, Steyerberg EW, et al. Brain oxygen tension in severe head injury. Neurosurgery 2000;46(4):868–76; https://doi.org/10.1097/00006123-200004000-00018.

  44. Bardt TF, Unterberg AW, Hartl R, Kiening KL, Schneider GH, Lanksch WR. Monitoring of brain tissue PO2 in traumatic brain injury: effect of cerebral hypoxia on outcome. Acta Neurochir Suppl 1998;71:153–6. (https://www.ncbi.nlm.nih.gov/pubmed/9779171).

  45. Diringer MN. Hyperoxia: good or bad for the injured brain? Curr Opin Crit Care. 2008;14(2):167–71. https://doi.org/10.1097/MCC.0b013e3282f57552.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Johnston AJ, Steiner LA, Coles JP, et al. Effect of cerebral perfusion pressure augmentation on regional oxygenation and metabolism after head injury. Crit Care Med. 2005;33(1):189–95. https://doi.org/10.1097/01.ccm.0000149837.09225.bd.

    Article  PubMed  Google Scholar 

  47. Tolias CM, Reinert M, Seiler R, Gilman C, Scharf A, Bullock MR. Normobaric hyperoxia–induced improvement in cerebral metabolism and reduction in intracranial pressure in patients with severe head injury: a prospective historical cohort-matched study. J Neurosurg. 2004;101(3):435–44. https://doi.org/10.3171/jns.2004.101.3.0435.

    Article  PubMed  Google Scholar 

  48. Zygun DA, Nortje J, Hutchinson PJ, Timofeev I, Menon DK, Gupta AK. The effect of red blood cell transfusion on cerebral oxygenation and metabolism after severe traumatic brain injury. Crit Care Med. 2009;37(3):1074–8. https://doi.org/10.1097/CCM.0b013e318194ad22.

    Article  CAS  PubMed  Google Scholar 

  49. Fletcher JJ, Bergman K, Blostein PA, Kramer AH. Fluid balance, complications, and brain tissue oxygen tension monitoring following severe traumatic brain injury. Neurocrit Care. 2010;13(1):47–56. https://doi.org/10.1007/s12028-010-9345-2.

    Article  PubMed  Google Scholar 

  50. East JM, Viau-Lapointe J, McCredie VA. Transfusion practices in traumatic brain injury. Curr Opin Anaesthesiol. 2018;31(2):219–26. https://doi.org/10.1097/ACO.0000000000000566.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Contant CF, Valadka AB, Gopinath SP, Hannay HJ, Robertson CS. Adult respiratory distress syndrome: a complication of induced hypertension after severe head injury. J Neurosurg. 2001;95(4):560–8. https://doi.org/10.3171/jns.2001.95.4.0560.

    Article  CAS  PubMed  Google Scholar 

  52. Robertson CS, Valadka AB, Hannay HJ, et al. Prevention of secondary ischemic insults after severe head injury. Crit Care Med. 1999;27(10):2086–95. https://doi.org/10.1097/00003246-199910000-00002.

    Article  CAS  PubMed  Google Scholar 

  53. Martini RP, Deem S, Treggiari MM. Targeting brain tissue oxygenation in traumatic brain injury. Respir Care. 2013;58(1):162–72. https://doi.org/10.4187/respcare.01942.

    Article  PubMed  Google Scholar 

  54. Chesnut R, Aguilera S, Buki A, et al. A management algorithm for adult patients with both brain oxygen and intracranial pressure monitoring: the Seattle International Severe Traumatic Brain Injury Consensus Conference (SIBICC). Intensive Care Med. 2020;46(5):919–29. https://doi.org/10.1007/s00134-019-05900-x.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Raj R, Skrifvars M, Bendel S, et al. Predicting six-month mortality of patients with traumatic brain injury: usefulness of common intensive care severity scores. Crit Care. 2014;18(2):R60. https://doi.org/10.1186/cc13814.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Esterov D, Bellamkonda E, Mandrekar J, Ransom JE, Brown AW. Cause of death after traumatic brain injury: a population-based health record review analysis referenced for nonhead trauma. Neuroepidemiology. 2021;55(3):180–7. https://doi.org/10.1159/000514807.

    Article  PubMed  Google Scholar 

  57. Gates TM, Baguley IJ, Nott MT, Simpson GK. External causes of death after severe traumatic brain injury in a multicentre inception cohort: clinical description and risk factors. Brain Inj. 2019;33(7):821–9. https://doi.org/10.1080/02699052.2019.1600020.

    Article  PubMed  Google Scholar 

  58. Pentland B, Hutton LS, Jones PA. Late mortality after head injury. J Neurol Neurosurg Psychiatry. 2005;76(3):395–400. https://doi.org/10.1136/jnnp.2004.037861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Intensive Care, Erasme University Hospital, Université Libre de Bruxelles, Route de Lennik, 808, 1070, Brussels, Belgium

    Elisa Gouvêa Bogossian, Alberto Diosdado, Filippo Annoni & Fabio Silvio Taccone

  2. Department of Neurosurgery, Erasme University Hospital, Université Libre de Bruxelles, Brussels, Belgium

    Sami Barrit, Mejdeddine Al Barajraji & Sophie Schuind

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  1. Elisa Gouvêa Bogossian
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  2. Alberto Diosdado
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Contributions

AD, EGB, and FST conceived the study; AD, SM, and MAB performed the screening and selected the articles for the systematic review. AD, EGB, and FA extracted the data from the articles; EGB and FST conducted the statistical analysis. AD, EGB, and FST wrote the first draft of the article; FA, SS, SM, and MAB revised the text for intellectual content. All authors read and approved the final manuscript.

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Correspondence to Elisa Gouvêa Bogossian.

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Gouvêa Bogossian, E., Diosdado, A., Barrit, S. et al. The Impact of Invasive Brain Oxygen Pressure Guided Therapy on the Outcome of Patients with Traumatic Brain Injury: A Systematic Review and Meta-Analysis. Neurocrit Care 37, 779–789 (2022). https://doi.org/10.1007/s12028-022-01613-0

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Keywords

  • Head injury
  • Cerebral oxygenation
  • Mortality
  • Glasgow outcome scale
  • Multimodal neuromonitoring