Skip to main content

Effect of Shivering on Brain Tissue Oxygenation During Induced Normothermia in Patients With Severe Brain Injury

Abstract

Background

We analyzed the impact of shivering on brain tissue oxygenation (PbtO2) during induced normothermia in patients with severe brain injury.

Methods

We studied patients with severe brain injury who developed shivering during induced normothermia. Induced normothermia was applied to treat refractory fever (body temperature [BT] ≥38.3°C, refractory to conventional treatment) using a surface cooling device with computerized adjustment of patient BT target to 37 ± 0.5°C. PbtO2, intracranial pressure, mean arterial pressure, cerebral perfusion pressure, and BT were monitored continuously. Circulating water temperature of the device system was measured to assess the intensity of cooling.

Results

Fifteen patients (10 with severe traumatic brain injury, 5 with aneurysmal subarachnoid hemorrhage) were treated with induced normothermia for an average of 5 ± 2 days. Shivering caused a significant decrease in PbtO2 levels both in SAH and TBI patients. Compared to baseline, shivering was associated with an overall reduction of PbtO2 from 34.1 ± 7.3 to 24.4 ± 5.5 mmHg (P < 0.001). A significant correlation was found between the magnitude of shivering-associated decrease of PbtO2 (ΔPbtO2) and circulating water temperature (R = 0.82, P < 0.001).

Conclusion

In patients with severe brain injury treated with induced normothermia, shivering was associated with a significant decrease of PbtO2, which correlated with the intensity of cooling. Monitoring of therapeutic cooling with computerized thermoregulatory systems may help prevent shivering and optimize the management of induced normothermia. The clinical significance of shivering-induced decrease in brain tissue oxygenation remains to be determined.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Dietrich WD, Bramlett HM. Hyperthermia and central nervous system injury. Prog Brain Res. 2007;162:201–17.

    Article  CAS  PubMed  Google Scholar 

  2. 2.

    Diringer MN, Reaven NL, Funk SE, Uman GC. Elevated body temperature independently contributes to increased length of stay in neurologic intensive care unit patients. Crit Care Med. 2004;32:1489–95.

    Article  PubMed  Google Scholar 

  3. 3.

    Busto R, Dietrich WD, Globus MY, Valdes I, Scheinberg P, Ginsberg MD. Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab. 1987;7:729–38.

    CAS  PubMed  Google Scholar 

  4. 4.

    Ginsberg MD, Busto R. Combating hyperthermia in acute stroke: a significant clinical concern. Stroke. 1998;29:529–34.

    CAS  PubMed  Google Scholar 

  5. 5.

    Oddo M, Frangos S, Milby A, et al. Induced normothermia attenuates cerebral metabolic distress in patients with aneurysmal subarachnoid hemorrhage and refractory fever. Stroke. 2009;40:1913–6.

    Article  PubMed  Google Scholar 

  6. 6.

    Marion DW. Controlled normothermia in neurologic intensive care. Crit Care Med. 2004;32:S43–5.

    Article  PubMed  Google Scholar 

  7. 7.

    Doufas AG, Sessler DI. Physiology and clinical relevance of induced hypothermia. Neurocrit Care. 2004;1:489–98.

    Article  PubMed  Google Scholar 

  8. 8.

    Sessler DI. Complications and treatment of mild hypothermia. Anesthesiology. 2001;95:531–43.

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Hata JS, Shelsky CR, Hindman BJ, Smith TC, Simmons JS, Todd MM. A prospective, observational clinical trial of fever reduction to reduce systemic oxygen consumption in the setting of acute brain injury. Neurocrit Care. 2008;9:37–44.

    Article  PubMed  Google Scholar 

  10. 10.

    Thoresen M, Satas S, Loberg EM, et al. Twenty-four hours of mild hypothermia in unsedated newborn pigs starting after a severe global hypoxic-ischemic insult is not neuroprotective. Pediatr Res. 2001;50:405–11.

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Thoresen M, Simmonds M, Satas S, Tooley J, Silver IA. Effective selective head cooling during posthypoxic hypothermia in newborn piglets. Pediatr Res. 2001;49:594–9.

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Bhatia A, Gupta AK. Neuromonitoring in the intensive care unit. II. Cerebral oxygenation monitoring and microdialysis. Intensive Care Med. 2007;33:1322–8.

    Article  PubMed  Google Scholar 

  13. 13.

    Nortje J, Gupta AK. The role of tissue oxygen monitoring in patients with acute brain injury. Br J Anaesth. 2006;97:95–106.

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Dings J, Meixensberger J, Amschler J, Hamelbeck B, Roosen K. Brain tissue pO2 in relation to cerebral perfusion pressure, TCD findings and TCD-CO2-reactivity after severe head injury. Acta Neurochir (Wien). 1996;138:425–34.

    Article  CAS  Google Scholar 

  15. 15.

    Doppenberg EM, Zauner A, Bullock R, Ward JD, Fatouros PP, Young HF. Correlations between brain tissue oxygen tension, carbon dioxide tension, pH, and cerebral blood flow—a better way of monitoring the severely injured brain? Surg Neurol. 1998;49:650–4.

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Mazzeo AT, Bullock R. Monitoring brain tissue oxymetry: will it change management of critically ill neurologic patients? J Neurol Sci. 2007;261:1–9.

    Article  PubMed  Google Scholar 

  17. 17.

    Kett-White R, Hutchinson PJ, Al-Rawi PG, Gupta AK, Pickard JD, Kirkpatrick PJ. Adverse cerebral events detected after subarachnoid hemorrhage using brain oxygen and microdialysis probes. Neurosurgery. 2002;50:1213–21. discussion 21–2.

    Article  PubMed  Google Scholar 

  18. 18.

    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;26:1576–81.

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    van den Brink WA, van Santbrink H, Steyerberg EW, et al. Brain oxygen tension in severe head injury. Neurosurgery. 2000;46:868–76. discussion 76–8.

    Article  PubMed  Google Scholar 

  20. 20.

    Mayer SA, Kowalski RG, Presciutti M, et al. Clinical trial of a novel surface cooling system for fever control in neurocritical care patients. Crit Care Med. 2004;32:2508–15.

    Article  PubMed  Google Scholar 

  21. 21.

    Geocadin RG, Carhuapoma JR. Medivance Arctic sun temperature management system. Neurocrit Care. 2005;3:63–7.

    Article  PubMed  Google Scholar 

  22. 22.

    Haugk M, Sterz F, Grassberger M, et al. Feasibility and efficacy of a new non-invasive surface cooling device in post-resuscitation intensive care medicine. Resuscitation. 2007;75:76–81.

    Article  PubMed  Google Scholar 

  23. 23.

    Kimberger O, Ali SZ, Markstaller M, et al. Meperidine and skin surface warming additively reduce the shivering threshold: a volunteer study. Crit Care. 2007;11:R29.

    Article  PubMed  Google Scholar 

  24. 24.

    Eberhart LH, Doderlein F, Eisenhardt G, et al. Independent risk factors for postoperative shivering. Anesth Analg. 2005;101:1849–57.

    Article  PubMed  Google Scholar 

  25. 25.

    Sagir O, Gulhas N, Toprak H, Yucel A, Begec Z, Ersoy O. Control of shivering during regional anaesthesia: prophylactic ketamine and granisetron. Acta Anaesthesiol Scand. 2007;51:44–9.

    Article  CAS  PubMed  Google Scholar 

  26. 26.

    Kurz A, Ikeda T, Sessler DI, et al. Meperidine decreases the shivering threshold twice as much as the vasoconstriction threshold. Anesthesiology. 1997;86:1046–54.

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    Doufas AG, Lin CM, Suleman MI, et al. Dexmedetomidine and meperidine additively reduce the shivering threshold in humans. Stroke. 2003;34:1218–23.

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Oddo M, Levine JM, Frangos S, et al. Effect of mannitol and hypertonic saline on cerebral oxygenation in patients with severe traumatic brain injury and refractory intracranial hypertension. J Neurol Neurosurg Psychiatry. 2009;80:916–20.

    Article  CAS  PubMed  Google Scholar 

  29. 29.

    Oddo M, Milby A, Chen I, et al. Hemoglobin concentration and cerebral metabolism in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2009;40:1275–81.

    Article  CAS  PubMed  Google Scholar 

  30. 30.

    Holtzclaw BJ. Shivering in acutely ill vulnerable populations. AACN Clin Issues. 2004;15:267–79.

    PubMed  Article  Google Scholar 

  31. 31.

    Imrie MM, Hall GM. Body temperature and anaesthesia. Br J Anaesth. 1990;64:346–54.

    Article  CAS  PubMed  Google Scholar 

  32. 32.

    Bilotta F, Pietropaoli P, La Rosa I, Spinelli F, Rosa G. Effects of shivering prevention on haemodynamic and metabolic demands in hypothermic postoperative neurosurgical patients. Anaesthesia. 2001;56:514–9.

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Badjatia N, Kowalski RG, Schmidt JM, et al. Predictors and clinical implications of shivering during therapeutic normothermia. Neurocrit Care. 2007;6:186–91.

    Article  PubMed  Google Scholar 

  34. 34.

    Crossley AW, Mahajan RP. The intensity of postoperative shivering is unrelated to axillary temperature. Anaesthesia. 1994;49:205–7.

    CAS  PubMed  Google Scholar 

  35. 35.

    Tsai YC, Chu KS. A comparison of tramadol, amitriptyline, and meperidine for postepidural anesthetic shivering in parturients. Anesth Analg. 2001;93:1288–92.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Professor Patrick D. Lyden, MD, Chairman, Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA, for the careful and helpful review of the manuscript and Prof. Scott E. Kasner, MD, Director, Comprehensive Stroke Center, Department of Neurology, University of Pennsylvania Medical Center, Philadelphia, PA, for statistical assistance. This work was supported by Research Grants from the SICPA Foundation, Switzerland (MO), the Integra Foundation (PDLR), and the Mary Elisabeth Groff Surgical and Medical Research Trust (PDLR).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Joshua M. Levine.

Additional information

This work was performed in the Neurointensive Care Unit, Hospital of the University of Pennsylvania, Philadelphia, PA.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Oddo, M., Frangos, S., Maloney-Wilensky, E. et al. Effect of Shivering on Brain Tissue Oxygenation During Induced Normothermia in Patients With Severe Brain Injury. Neurocrit Care 12, 10–16 (2010). https://doi.org/10.1007/s12028-009-9280-2

Download citation

Keywords

  • Induced normothermia
  • Fever control
  • Temperature management
  • Surface cooling
  • Shivering
  • Brain tissue oxygenation
  • Brain injury
  • SAH
  • TBI
  • Neurointensive care
  • Neurocritical care