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Neurocritical Care

, Volume 30, Issue 2, pp 405–413 | Cite as

Spontaneous Hyperventilation in Severe Traumatic Brain Injury: Incidence and Association with Poor Neurological Outcome

  • Pierre EsnaultEmail author
  • Johanna Roubin
  • Mickael Cardinale
  • Erwan D’Aranda
  • Ambroise Montcriol
  • Pierre-Julien Cungi
  • Philippe Goutorbe
  • Christophe Joubert
  • Arnaud Dagain
  • Eric Meaudre
Original Article
  • 180 Downloads

Abstract

Background

Hypocapnia induces cerebral vasoconstriction leading to a decrease in cerebral blood flow, which might precipitate cerebral ischemia. Hypocapnia can be intentional to treat intracranial hypertension or unintentional due to a spontaneous hyperventilation (SHV). SHV is frequent after subarachnoid hemorrhage. However, it is understudied in patients with severe traumatic brain injury (TBI). The objective of this study was to describe the incidence and consequences on outcome of SHV after severe TBI.

Methods

We conducted a retrospective, observational study including all intubated TBI patients admitted in the trauma center and still comatose 24 h after the withdrawal of sedation. SHV was defined by the presence of at least one arterial blood gas (ABG) with both PaCO2 < 35 mmHg and pH > 7.45. Patient characteristics and outcome were extracted from a prospective registry of all intubated TBI admitted in the intensive care unit. ABG results were retrieved from patient files. A multivariable logistic regression model was developed to determine factors independently associated with unfavorable outcome (defined as a Glasgow Outcome Scale between 1 and 3) at 6-month follow-up.

Results

During 7 years, 110 patients fully respecting inclusion criteria were included. The overall incidence of SHV was 69.1% (95% CI [59.9–77]). Patients with SHV were more severely injured (median head AIS score (5 [4–5] vs. 4 [4–5]; p = 0.016)) and exhibited an elevated morbidity during their stay. The proportion of patients with an unfavorable functional neurologic outcome was significantly higher in patients with SHV: 40 (52.6%) versus 6 (17.6%), p = 0.0006. After adjusting for confounders, SHV remains an independent factor associated with unfavorable outcome at the 6-month follow-up (OR 4.1; 95% CI [1.2–14.4]).

Conclusions

SHV is common in patients with a persistent coma after a severe TBI (overall rate: 69%) and was independently associated with unfavorable outcome at 6-month follow-up.

Keywords

Severe traumatic brain injury Spontaneous hyperventilation Hypocapnia Respiratory alkalosis Glasgow Outcome Scale 

Abbreviations

TBI

Traumatic brain injury

GCS

Glasgow Coma Scale

CPP

Cerebral perfusion pressure

PbtO2

Brain tissue oxygen tension

ICU

Intensive care unit

ICP

Intracranial pressure

FiO2

Oxygen inspired fraction

GOS

Glasgow Outcome Scale

ROC

Receiver operating characteristic

95% CI

95% confidence intervals

Notes

Authors’ contributions

PE, JR, and CJ contributed to the study concept and design. PE, JR, MC, ED, AM, PJC, and AS contributed to the acquisition of data. PE, PG, AD, and BP contributed to the analysis and interpretation of data. PE, PG, JB, and EM contributed to the drafting of manuscript and critical revision of the manuscript for important intellectual content. All authors read and approved the final manuscript.

Source of support

None.

Compliance with Ethical Standards

Conflict of interest

The authors have no conflicts of interest to report.

Ethical Approval and Consent to Participate

Institutional Review Board of the Sainte Anne Military Hospital, Toulon (France), approved the study and waived the requirement for informed consent from the patients or patient’s kin given the observational nature of the study.

Supplementary material

12028_2018_639_MOESM1_ESM.docx (13 kb)
Additional Table. Comparison between Arterial Blood Gas with Spontaneous Hyperventilation criteria and those without. (DOCX 12 kb)

References

  1. 1.
    Madden JA. The effect of carbon dioxide on cerebral arteries. Pharmacol Ther. 1993;59(2):229–50.CrossRefGoogle Scholar
  2. 2.
    Ito H, Ibaraki M, Kanno I, Fukuda H, Miura S. Changes in the arterial fraction of human cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J Cereb Blood Flow Metab. 2005;25(7):852–7.CrossRefGoogle Scholar
  3. 3.
    Raichle ME, Plum F. Hyperventilation and cerebral blood flow. Stroke. 1972;3(5):566–75.CrossRefGoogle Scholar
  4. 4.
    Curley G, Kavanagh BP, Laffey JG. Hypocapnia and the injured brain: more harm than benefit. Crit Care Med. 2010;38(5):1348–59.CrossRefGoogle Scholar
  5. 5.
    Ghajar J, Hariri RJ, Narayan RK, Iacono LA, Firlik K, Patterson RH. Survey of critical care management of comatose, head-injured patients in the United States. Crit Care Med. 1995;23(3):560–7.CrossRefGoogle Scholar
  6. 6.
    Neumann JO, Chambers IR, Citerio G, Enblad P, Gregson BA, Howells T, et al. The use of hyperventilation therapy after traumatic brain injury in Europe: an analysis of the BrainIT database. Intensive Care Med. 2008;34(9):1676–82.CrossRefGoogle Scholar
  7. 7.
    Muizelaar JP, Marmarou A, Ward JD, Kontos HA, Choi SC, Becker DP, et al. Adverse effects of prolonged hyperventilation in patients with severe head injury: a randomized clinical trial. J Neurosurg. 1991;75(5):731–9.CrossRefGoogle Scholar
  8. 8.
    Dumont TM, Visioni AJ, Rughani AI, Tranmer BI, Crookes B. Inappropriate prehospital ventilation in severe traumatic brain injury increases in-hospital mortality. J Neurotrauma. 2010;27(7):1233–41.CrossRefGoogle Scholar
  9. 9.
    Godoy DA, Seifi A, Garza D, Lubillo-Montenegro S, Murillo-Cabezas F. Hyperventilation therapy for control of posttraumatic intracranial hypertension. Front Neurol. 2017;8:250.CrossRefGoogle Scholar
  10. 10.
    Roberts BW, Karagiannis P, Coletta M, Kilgannon JH, Chansky ME, Trzeciak S. Effects of PaCO2 derangements on clinical outcomes after cerebral injury: a systematic review. Resuscitation. 2015;27:1–48.Google Scholar
  11. 11.
    Stringer WA, Hasso AN, Thompson JR, Hinshaw DB, Jordan KG. Hyperventilation-induced cerebral ischemia in patients with acute brain lesions: demonstration by xenon-enhanced CT. AJNR Am J Neuroradiol. 1993;14(2):475–84.Google Scholar
  12. 12.
    Coles JP, Minhas PS, Fryer TD, Smielewski P, Aigbirihio F, Donovan T, et al. Effect of hyperventilation on cerebral blood flow in traumatic head injury: clinical relevance and monitoring correlates. Crit Care Med. 2002;30(9):1950–9.CrossRefGoogle Scholar
  13. 13.
    Coles JP, Fryer TD, Coleman MR, Smielewski P, Gupta AK, Minhas PS, et al. Hyperventilation following head injury: effect on ischemic burden and cerebral oxidative metabolism. Crit Care Med. 2007;35(2):568–78.CrossRefGoogle Scholar
  14. 14.
    Carney N, Totten AM, O’Reilly C, Ullman JS, Hawryluk GWJ, Bell MJ, et al. Guidelines for the management of severe traumatic brain injury, fourth edition. Neurosurgery. 2017;80:6–15.Google Scholar
  15. 15.
    Geeraerts T, Velly L, Abdennour L, Asehnoune K, Audibert G, Bouzat P, et al. Management of severe traumatic brain injury (first 24 hours). Anaesth Crit Care Pain Med. 2018;37(2):171–86.CrossRefGoogle Scholar
  16. 16.
    Marehbian J, Muehlschlegel S, Edlow BL, Hinson HE, Hwang DY. Medical management of the severe traumatic brain injury patient. Neurocrit Care. 2017;30:1–17.Google Scholar
  17. 17.
    Brain Trauma Foundation, American Association of Neurological Surgeons, Congress of Neurological Surgeons. Guidelines for the management of severe traumatic brain injury. J Neurotrauma. 2007;24:S1–106.CrossRefGoogle Scholar
  18. 18.
    Gaviani P, Gonzalez RG, Zhu J-J, Batchelor TT, Henson JW. Central neurogenic hyperventilation and lactate production in brainstem glioma. Neurology. 2005;64(1):166–7.CrossRefGoogle Scholar
  19. 19.
    Møller K, Høgh P, Larsen FS, Strauss GI, Skinhøj P, Sperling BK, et al. Regional cerebral blood flow during hyperventilation in patients with acute bacterial meningitis. Clin Physiol. 2000;20(5):399–410.CrossRefGoogle Scholar
  20. 20.
    Solaiman O, Singh JM. Hypocapnia in aneurysmal subarachnoid hemorrhage: incidence and association with poor clinical outcomes. J Neurosurg Anesthesiol. 2013;25(3):254–61.CrossRefGoogle Scholar
  21. 21.
    Williamson CA, Sheehan KM, Tipirneni R, Roark CD, Pandey AS, Thompson BG, et al. The association between spontaneous hyperventilation, delayed cerebral ischemia, and poor neurological outcome in patients with subarachnoid hemorrhage. Neurocrit Care. 2015;23(3):330–8.CrossRefGoogle Scholar
  22. 22.
    Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;1(7905):480–4.CrossRefGoogle Scholar
  23. 23.
    Fayol P, Carrière H, Habonimana D, Preux P-M, Dumond J-J. French version of structured interviews for the Glasgow Outcome Scale: guidelines and first studies of validation. Ann Readapt Med Phys. 2004;47(4):142–56.CrossRefGoogle Scholar
  24. 24.
    Leitch AG, McLennan JE, Balkenhol S, Loudon RG, McLaurin RL. Mechanisms of hyperventilation in head injury: case report and review. Neurosurgery. 1979;5(6):701–7.CrossRefGoogle Scholar
  25. 25.
    Meyfroidt G, Baguley IJ, Menon DK. Paroxysmal sympathetic hyperactivity: the storm after acute brain injury. Lancet Neurol. 2017;16(9):721–9.CrossRefGoogle Scholar
  26. 26.
    Kontos HA, Raper AJ, Patterson JL. Analysis of vasoactivity of local pH, PCO2 and bicarbonate on pial vessels. Stroke. 1977;8(3):358–60.CrossRefGoogle Scholar
  27. 27.
    Alberti E, Hoyer S, Hamer J, Stoeckel H, Packschiess P, Weinhardt F. The effect of carbon dioxide on cerebral blood flow and cerebral metabolism in dogs. Br J Anaesth. 1975;47(9):941–7.CrossRefGoogle Scholar
  28. 28.
    Muizelaar JP, van der Poel HG, Li ZC, Kontos HA, Levasseur JE. Pial arteriolar vessel diameter and CO2 reactivity during prolonged hyperventilation in the rabbit. J Neurosurg. 1988;69(6):923–7.CrossRefGoogle Scholar
  29. 29.
    Huttunen J, Tolvanen H, Heinonen E, Voipio J, Wikström H, Ilmoniemi RJ, et al. Effects of voluntary hyperventilation on cortical sensory responses. Electroencephalographic and magnetoencephalographic studies. Exp Brain Res. 1999;125(3):248–54.CrossRefGoogle Scholar
  30. 30.
    Graham EM, Apostolou M, Mishra OP, Delivoria-Papadopoulos M. Modification of the N-methyl-d-aspartate (NMDA) receptor in the brain of newborn piglets following hyperventilation induced ischemia. Neurosci Lett. 1996;218(1):29–32.Google Scholar
  31. 31.
    Mykita S, Golly F, Dreyfus H, Freysz L, Massarelli R. Effect of CDP-choline on hypocapnic neurons in culture. J Neurochem. 1986;47(1):223–31.CrossRefGoogle Scholar
  32. 32.
    Carrera E, Schmidt JM, Fernandez L, Kurtz P, Merkow M, Stuart M, et al. Spontaneous hyperventilation and brain tissue hypoxia in patients with severe brain injury. J Neurol Neurosurg Psychiatry. 2010;81(7):793–7.CrossRefGoogle Scholar
  33. 33.
    Valadka AB, Gopinath SP, Contant CF, Uzura M, Robertson CS. Relationship of brain tissue PO2 to outcome after severe head injury. Crit Care Med. 1998;26(9):1576–81.CrossRefGoogle Scholar
  34. 34.
    van Santbrink H, Maas AI, Avezaat CJ. Continuous monitoring of partial pressure of brain tissue oxygen in patients with severe head injury. Neurosurgery. 1996;38(1):21–31.CrossRefGoogle Scholar
  35. 35.
    Haberthür C, Fabry B, Stocker R, Ritz R, Guttmann J. Additional inspiratory work of breathing imposed by tracheostomy tubes and non-ideal ventilator properties in critically ill patients. Intensive Care Med. 1999;25(5):514–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society 2018

Authors and Affiliations

  • Pierre Esnault
    • 1
    Email author
  • Johanna Roubin
    • 1
  • Mickael Cardinale
    • 1
  • Erwan D’Aranda
    • 1
  • Ambroise Montcriol
    • 1
  • Pierre-Julien Cungi
    • 1
  • Philippe Goutorbe
    • 1
  • Christophe Joubert
    • 2
  • Arnaud Dagain
    • 2
    • 3
  • Eric Meaudre
    • 1
    • 3
  1. 1.Intensive Care UnitSainte Anne Military HospitalToulonFrance
  2. 2.Department of NeurosurgerySainte Anne Military HospitalToulonFrance
  3. 3.French Military Health Service Academy UnitParisFrance

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