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Bilateral Failure of Cerebral Autoregulation is Related to Unfavorable Outcome After Subarachnoid Hemorrhage

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Abstract

Backround

The extent of hemodynamic disturbances following subarachnoid hemorrhage (SAH) varies. We aim to determine the prognostic implications of unilateral and bilateral autoregulatory failure on delayed cerebral ischemia (DCI) and outcome.

Methods

Ninety-eight patients with aneurysmal SAH were recruited. Autoregulation was assessed using systolic flow index—Sxa. Interhemispheric difference in autoregulation was calculated to assess the spatial distribution and symmetry of autoregulatory changes. Assessment of interhemispheric difference in autoregulation in combination with overall autoregulation was used to measure the extent of autoregulatory impairment. Patients were dichotomized by the presence of DCI and 3-month mRS.

Results

Higher flow velocity and worse autoregulation (p < 0.0000001, 95 % CI 10.7–21.3 and p = 0.00001, 95 % CI 0.03–0.07 for difference in FV and Sxa, respectively) were found ipsilateral to the ischemic hemisphere or location of aneurysm (if no ischemia detected). DCI group had a higher interhemispheric difference of autoregulation than non-DCI group (p = 0.035, 95 % CI 0.003–0.08). 16/18 patients with unfavorable outcome vs. 17/72 with favorable outcome had overall poor autoregulation with low interhemispheric differences (p = 0.0013, χ 2). Unilateral autoregulatory failure was seen on a median day 3, bilateral on day 4, and vasospasm was detected on day 6.

Conclusions

Unilateral autoregulation failure was seen in patients who developed DCI (worse ipsilateral to the ischemic hemisphere). Bilateral autoregulation failure was seen more frequently in patients with unfavorable outcome. Analysis of the temporal profile showed unilateral dysautoregulation as the primary event predisposing to DCI, which in selected cases led to bilateral failure and unfavorable outcomes.

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References

  1. Mayer SA, Kossoff SB. Withdrawal of life support in the neurological intensive care unit. Neurology. 1999;52(8):1602–9.

    Article  CAS  PubMed  Google Scholar 

  2. Molyneux AJ, Kerr RS, Birks J, et al. Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol. 2009;8(5):427–33.

    Article  PubMed Central  PubMed  Google Scholar 

  3. Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28(3):660–4.

    Article  CAS  PubMed  Google Scholar 

  4. Budohoski KP, Czosnyka M, Smielewski P, et al. Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke. 2012;43(12):3230–7.

    Article  PubMed  Google Scholar 

  5. Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke. 2007;38(3):981–6.

    Article  PubMed  Google Scholar 

  6. Jaeger M, Soehle M, Schuhmann MU, Meixensberger J. Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke. 2012;43(8):2097–101.

    Article  PubMed  Google Scholar 

  7. Lam JM, Smielewski P, Czosnyka M, Pickard JD, Kirkpatrick PJ. Predicting delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery. 2000;47(4):816–9.

    Article  Google Scholar 

  8. Lang EW, Diehl RR, Mehdorn HM. Cerebral autoregulation testing after aneurysmal subarachnoid hemorrhage: the phase relationship between arterial blood pressure and cerebral blood flow velocity. Crit Care Med. 2001;29(1):158–63.

    Article  CAS  PubMed  Google Scholar 

  9. Pickard JD, Matheson M, Patterson J, Wyper D. Prediction of late ischemic complications after cerebral aneurysm surgery by the intraoperative measurement of cerebral blood flow. J Neurosurg. 1980;53(3):305–8.

    Article  CAS  PubMed  Google Scholar 

  10. Ratsep T, Asser T. Cerebral hemodynamic impairment after aneurysmal subarachnoid hemorrhage as evaluated using transcranial Doppler ultrasonography: relationship to delayed cerebral ischemia and clinical outcome. J Neurosurg. 2001;95(3):393–401.

    Article  CAS  PubMed  Google Scholar 

  11. Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke. 2005;36(8):1627–32.

    Article  CAS  PubMed  Google Scholar 

  12. Harper AM, Deshmukh VD, Sengupta D, Rowan JO, Jennett WB. The effect of experimental spasm on the CO2 response of cerebral bloodflow in primates. Neuroradiology. 1972;3(3):134–6.

    Article  CAS  PubMed  Google Scholar 

  13. Schmidt EA, Piechnik SK, Smielewski P, Raabe A, Matta BF, Czosnyka M. Symmetry of cerebral hemodynamic indices derived from bilateral transcranial Doppler. J Neuroimag. 2003;13(3):248–54.

    Article  Google Scholar 

  14. Schmidt EA, Czosnyka M, Steiner LA, et al. Asymmetry of pressure autoregulation after traumatic brain injury. J Neurosurg. 2003;99(6):991–8.

    Article  PubMed  Google Scholar 

  15. Hu K, Lo M-T, Peng CK, et al. Nonlinear pressure-flow relationship is able to detect asymmetry of brain blood circulation associated with midline shift. J Neurotrauma. 2009;26(2):227–33.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Lang EW, Yip K, Griffith J, Lagopoulos J, Mudaliar Y, Dorsch NW. Hemispheric asymmetry and temporal profiles of cerebral pressure autoregulation in head injury. J Clin Neurosci. 2003;10(6):670–3.

    Article  PubMed  Google Scholar 

  17. Reinhard M, Roth M, Muller T, Czosnyka M, Timmer J, Hetzel A. Cerebral autoregulation in carotid artery occlusive disease assessed from spontaneous blood pressure fluctuations by the correlation coefficient index. Stroke. 2003;34(9):2138–44.

    Article  CAS  PubMed  Google Scholar 

  18. Gooskens I, Schmidt EA, Czosnyka M, et al. Pressure-autoregulation, CO2 reactivity and asymmetry of haemodynamic parameters in patients with carotid artery stenotic disease. A clinical appraisal. Acta Neurochir (Wien) 2003;145(7):527–32; discussion 532.

  19. Telman G, Kouperberg E, Nitecki S, et al. Cerebral hemodynamics in symptomatic and asymptomatic patients with severe unilateral carotid stenosis before and after carotid endarterectomy. Eur J Vasc Endovasc Surg. 2006;32(4):375–8.

    Article  CAS  PubMed  Google Scholar 

  20. Komotar RJ, Schmidt JM, Starke RM, et al. Resuscitation and critical care of poor-grade subarachnoid hemorrhage. Neurosurgery. 2009;64(3):391–7.

    Article  Google Scholar 

  21. Bederson JB, Connolly ES Jr, Batjer HH, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40(3):994–1025.

    Article  PubMed  Google Scholar 

  22. Vergouwen MD, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–5.

    Article  PubMed  Google Scholar 

  23. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012;43(6):1711–37.

    Article  PubMed  Google Scholar 

  24. Claassen J, Bernardini GL, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32(9):2012–20.

    Article  CAS  PubMed  Google Scholar 

  25. Budohoski KP, Reinhard M, Aries MJ, et al. Monitoring cerebral autoregulation after head injury. Which component of transcranial Doppler flow velocity is optimal? Neurocrit Care. 2011;17(2):211–8.

    Article  Google Scholar 

  26. Czosnyka M, Smielewski P, Kirkpatrick P, Menon DK, Pickard JD. Monitoring of cerebral autoregulation in head-injured patients. Stroke. 1996;27(10):1829–34.

    Article  CAS  PubMed  Google Scholar 

  27. Zweifel C, Castellani G, Czosnyka M, et al. Continuous assessment of autoregualtion with near infrared spectroscopy in adults after subarachnoid hemorrhage. Stroke. 2010;41(9):1963–8.

  28. Heilbrun MP, Olesen J, Lassen NA. Regional cerebral blood flow studies in subarachnoid hemorrhage. J Neurosurg. 1972;37(1):36–44.

    Article  CAS  PubMed  Google Scholar 

  29. Piechnik SK, Czosnyka M, Harris NG, Minhas PS, Pickard JD. A model of the cerebral and cerebrospinal fluid circulations to examine asymmetry in cerebrovascular reactivity. J Cereb Blood Flow Metab. 2001;21(2):182–92.

    Article  CAS  PubMed  Google Scholar 

  30. Maas AI, Hukkelhoven CW, Marshall LF, Steyerberg EW. Prediction of outcome in traumatic brain injury with computed tomographic characteristics: a comparison between the computed tomographic classification and combinations of computed tomographic predictors. Neurosurgery. 2005;57(6):1173–82.

    Article  PubMed  Google Scholar 

  31. Rinne J, Hernesniemi J, Niskanen M, Vapalahti M. Analysis of 561 patients with 690 middle cerebral artery aneurysms: anatomic and clinical features as correlated to management outcome. Neurosurgery. 1996;38(1):2–11.

    Article  CAS  PubMed  Google Scholar 

  32. Sorrentino E, Budohoski KP, Kasprowicz M, et al. Critical thresholds for transcranial Doppler indices of cerebral autoregulation in traumatic brain injury. Neurocrit Care. 2011;14(2):188–93.

    Article  PubMed  Google Scholar 

  33. Czosnyka M, Richards H, Kirkpatrick P, Pickard J. Assessment of cerebral autoregulation with ultrasound and laser Doppler wave forms: an experimental study in anesthetized rabbits. Neurosurgery. 1994;35(2):283–7.

    Google Scholar 

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Conflict of interest

Karol P Budohoski, Peter J Kirkpatrick, Matthias Reinhard, Georgios V Varsos, Magdalena Kasprowicz, Mirosław Ząbek, and John D Pickard report no conflict of interest. Peter Smielewski and Marek Czosnyka ICM + Software are licensed by Cambridge Enterprise, Cambridge, UK, http://www.neurosurg.cam.ac.uk/icmplus/. MC and PS have a financial interest in a fraction of the licensing fee.

Sponsorship and Funding

KPB received a grant from St Catherine’s College, University of Cambridge. MK was supported by Polish Ministry of Science and Higher Education. JDP is a recipient of National Institute of Health Research Senior Investigator Awards. MC is a recipient of National Institute of Health Research Senior Investigator Award - CSF dynamics.

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Authors and Affiliations

  1. Division of Neurosurgery, Department of Clinical Neurosciences, Addenbrooke’s Hospital, University of Cambridge, Hills Road, CB2 0QQ, Cambridge, UK

    Karol P. Budohoski, Marek Czosnyka, Peter J. Kirkpatrick, Georgios V. Varsos, Magdalena Kasprowicz, John D. Pickard & Peter Smielewski

  2. Department of Neurology, University of Freiburg, Freiburg, Germany

    Matthias Reinhard

  3. Institute of Biomedical Engineering and Instrumentation, Wrocław University of Technology, Wrocław, Poland

    Magdalena Kasprowicz

  4. Department of Neurosurgery, Postgraduate Medical Center, Mazovia Bródno Hospital, Warsaw, Poland

    Mirosław Ząbek

Authors
  1. Karol P. Budohoski
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  2. Marek Czosnyka
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  3. Peter J. Kirkpatrick
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  4. Matthias Reinhard
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  7. Mirosław Ząbek
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  8. John D. Pickard
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  9. Peter Smielewski
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Correspondence to Karol P. Budohoski.

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Budohoski, K.P., Czosnyka, M., Kirkpatrick, P.J. et al. Bilateral Failure of Cerebral Autoregulation is Related to Unfavorable Outcome After Subarachnoid Hemorrhage. Neurocrit Care 22, 65–73 (2015). https://doi.org/10.1007/s12028-014-0032-6

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  • DOI: https://doi.org/10.1007/s12028-014-0032-6

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