Skip to main content
Log in

Dynamic Autoregulatory Response After Aneurysmal Subarachnoid Hemorrhage and Its Relation to Angiographic Vasospasm and Clinical Outcome

  • Original Article
  • Published:
Neurocritical Care Aims and scope Submit manuscript

Abstract

Background

Impaired cerebral autoregulation (CA) is increasingly recognized to contribute to sequelae after aneurysmal subarachnoid hemorrhage (SAH). The current study characterizes the course of the dynamic autoregulation index (ARI) during the first 8 days after SAH and its coherence with angiographic vasospasm (VS) and clinical outcome.

Methods

Fifty-one patients with SAH were prospectively included within 48 h after the ictus. The ARI was determined daily for each hemisphere with the thigh cuff test. The degree of cerebral VS was evaluated based on a baseline digital subtraction angiography (DSA) after the ictus and a follow-up DSA on day 8. The clinical outcome was determined by the Modified Rankin Scale (mRS), the Glasgow Outcome Scale Extended (GOSE), and the National Institute of Health Stroke Scale (NIHSS) at discharge from the intensive care unit.

Results

Impaired CA significantly correlated with unfavorable clinical outcome scores (mRS, p = 0.0021; GOSE, p = 0.0027; NIHSS, p = 0.0091). ARI-values of patients with a favorable clinical outcome (mRS 0–3) showed a significant improvement during the first 8 days (+0.1964/day; p = 0.0148) compared to a significant decrease of ARI-values in patients with an unfavorable clinical outcome (–0.2976/day; p = 0.0182). The degree of CA impairment significantly correlated with the severity of VS in the middle cerebral artery (p = 0.0184).

Conclusions

Early deterioration of CA significantly correlates with unfavorable clinical outcome and severity of angiographic vasospasm. Dynamic CA measurements might represent an important tool in stratifying therapy guidelines in patients after SAH.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. 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;43:3230–7.

    Article  PubMed  Google Scholar 

  2. Diedler J, Sykora M, Rupp A, et al. Impaired cerebral vasomotor activity in spontaneous intracerebral hemorrhage. Stroke. 2009;40:815–9.

    Article  PubMed  Google Scholar 

  3. Saeed NP, Panerai RB, Horsfield MA, Robinson TG. Does stroke subtype and measurement technique influence estimation of cerebral autoregulation in acute ischaemic stroke? Cerebrovasc Dis. 2013;35:257–61.

    Article  CAS  PubMed  Google Scholar 

  4. Buczek J, Karliński M, Kobayashi A, Białek P, Członkowska A. Hyperperfusion syndrome after carotid endarterectomy and carotid stenting. Cerebrovasc Dis. 2013;35:531–7.

    Article  PubMed  Google Scholar 

  5. Atkins ER, Brodie FG, Rafelt SE, Panerai RB, Robinson TG. Dynamic cerebral autoregulation is compromised acutely following mild ischaemic stroke but not transient ischaemic attack. Cerebrovasc Dis. 2010;29:228–35.

    Article  PubMed  Google Scholar 

  6. Abstracts of the 18th Meeting of the European Society of Neurosonology and Cerebral Hemodynamics (ESNCH) and the 3rd Meeting of the Cerebral Autoregulation Network (CARNet).Cerebrovasc Dis. 2013;35 Suppl 2:1–77. May 24–27, 2013 Porto, Portugal.

  7. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke. 1989;20:45–52.

    Article  CAS  PubMed  Google Scholar 

  8. Barth M, Woitzik J, Weiss C, et al. Correlation of clinical outcome with pressure-, oxygen-, and flow-related indices of cerebrovascular reactivity in patients following aneurysmal SAH. Neurocrit Care. 2010;12:234–43.

    Article  PubMed  Google Scholar 

  9. Budohoski KP, Czosnyka M, Smielewski P, et al. Cerebral autoregulation after subarachnoid hemorrhage: comparison of three methods. J Cereb Blood Flow Metab. 2013;33:449–56.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Christ M, Noack F, Schroeder T, et al. Continuous cerebral autoregulation monitoring by improved cross-correlation analysis: comparison with the cuff deflation test. Intensive Care Med. 2007;33:246–54 Epub 2006 Dec 2.

    Article  PubMed  Google Scholar 

  11. Tzeng YC, Ainslie PN, Cooke WH, et al. Assessment of cerebral autoregulation: the quandary of quantification. Am J Physiol Heart Circ Physiol. 2012;303:H658–71.

    Article  CAS  PubMed  Google Scholar 

  12. 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;38:981–6.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  14. Soehle M, Czosnyka M, Pickard JD, Kirkpatrick PJ. Continuous assessment of cerebral autoregulation in subarachnoid hemorrhage. Anesth Analg 2004;98:1133–9, table of contents.

  15. Raabe A, Beck J, Berkefeld J, et al. Recommendations for the management of patients with aneurysmal subarachnoid hemorrhage. Zentralbl Neurochir. 2005;66:79–91.

    Article  CAS  PubMed  Google Scholar 

  16. Macdonald RL, Kassell NF, Mayer S, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke. 2008;39:3015–21.

    Article  CAS  PubMed  Google Scholar 

  17. Hlatky R, Furuya Y, Valadka AB, et al. Dynamic autoregulatory response after severe head injury. J Neurosurg. 2002;97:1054–61.

    Article  PubMed  Google Scholar 

  18. Mahony PJ, Panerai RB, Deverson ST, Hayes PD, Evans DH. Assessment of the thigh cuff technique for measurement of dynamic cerebral autoregulation. Stroke. 2000;31:476–80.

    Article  CAS  PubMed  Google Scholar 

  19. Park CW, Sturzenegger M, Douville CM, Aaslid R, Newell DW. Autoregulatory response and CO2 reactivity of the basilar artery. Stroke. 2003;34:34–9.

    Article  PubMed  Google Scholar 

  20. Vavilala MS, Newell DW, Junger E, et al. Dynamic cerebral autoregulation in healthy adolescents. Acta Anaesthesiol Scand. 2002;46:393–7.

    Article  CAS  PubMed  Google Scholar 

  21. Jünger EC, Newell DW, Grant GA, et al. Cerebral autoregulation following minor head injury. J Neurosurg. 1997;86:425–32.

    Article  PubMed  Google Scholar 

  22. Engelhard K, Werner C, Mollenberg O, Kochs E. Effects of remifentanil/propofol in comparison with isoflurane on dynamic cerebrovascular autoregulation in humans. Acta Anesthesiol Scand. 2001;45:971–6.

    Article  CAS  Google Scholar 

  23. Barth M, Moratin B, Dostal M, Kalenka A, Scharf J, Schmieder K. Correlation of clinical outcome and angiographic vasospasm with the dynamic autoregulatory response after aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl. 2012;114:157–60.

    Article  PubMed  Google Scholar 

  24. Jaeger M, Schuhmann MU, Soehle M, Meixensberger J. Continuous assessment of cerebrovascular autoregulation after traumatic brain injury using brain tissue oxygen pressure reactivity. Crit Care Med. 2006;34:1783–8.

    Article  PubMed  Google Scholar 

  25. Czosnyka M, Smielewski P, Kirkpatrick P, Laing RJ, Menon D, Pickard JD. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 1997;41:11–7; discussion 7–9.

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

    Article  CAS  PubMed  Google Scholar 

  27. Dohmen C, Bosche B, Graf R, et al. Identification and clinical impact of impaired cerebrovascular autoregulation in patients with malignant middle cerebral artery infarction. Stroke. 2007;38:56–61.

    Article  PubMed  Google Scholar 

  28. Reinhard M, Gerds TA, Grabiak D, et al. Cerebral dysautoregulation and the risk of ischemic events in occlusive carotid artery disease. J Neurol. 2008;255:1182–9.

    Article  PubMed  Google Scholar 

  29. Schmieder K, Moller F, Engelhardt M, et al. Dynamic cerebral autoregulation in patients with ruptured and unruptured aneurysms after induction of general anesthesia. Zentralbl Neurochir. 2006;67:81–7.

    Article  CAS  PubMed  Google Scholar 

  30. Frontera JA, Rundek T, Schmidt JM, et al. Cerebrovascular reactivity and vasospasm after subarachnoid hemorrhage: a pilot study. Neurology. 2006;66:727–9.

    Article  CAS  PubMed  Google Scholar 

  31. 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;47:819–25.

    Article  CAS  PubMed  Google Scholar 

  32. 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;29:158–63.

    Article  CAS  PubMed  Google Scholar 

  33. 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;95:393–401.

    Article  CAS  PubMed  Google Scholar 

  34. Voldby B, Enevoldsen EM, Jensen FT. Cerebrovascular reactivity in patients with ruptured intracranial aneurysms. J Neurosurg. 1985;62:59–67.

    Article  CAS  PubMed  Google Scholar 

  35. Otite F, Mink S, Tan CO, et al. Impaired cerebral autoregulation is associated with vasospasm and delayed cerebral ischemia in subarachnoid hemorrhage. Stroke. 2014;45:677–82.

    Article  PubMed Central  PubMed  Google Scholar 

  36. Tiecks FP, Lam AM, Aaslid R, Newell DW. Comparison of static and dynamic cerebral autoregulation measurements. Stroke. 1995;26:1014–9.

    Article  CAS  PubMed  Google Scholar 

  37. Strebel S, Lam AM, Matta B, Mayberg TS, Aaslid R, Newell DW. Dynamic and static cerebral autoregulation during isoflurane, desflurane, and propofol anesthesia. Anesthesiology. 1995;83:66–76.

    Article  CAS  PubMed  Google Scholar 

  38. van Lieshout JJ, Secher NH. Point:counterpoint: sympathetic activity does/does not influence cerebral blood flow. Point: sympathetic activity does influence cerebral blood flow. J Appl Physiol. 2008;105:1364–6.

    Article  PubMed  Google Scholar 

  39. Diehl RR, Linden D, Lucke D, Berlit P. Phase relationship between cerebral blood flow velocity and blood pressure. Clinical test of autoregulation. Stroke. 1995;26:1801–4.

    Article  CAS  PubMed  Google Scholar 

  40. Steinmeier R, Bauhuf C, Hubner U, et al. Slow rhythmic oscillations of blood pressure, intracranial pressure, microcirculation, and cerebral oxygenation. Dynamic interrelation and time course in humans. Stroke. 1996;27:2236–43.

    Article  CAS  PubMed  Google Scholar 

  41. Steinmeier R, Hofmann RP, Bauhuf C, Hubner U, Fahlbusch R. Continuous cerebral autoregulation monitoring by cross-correlation analysis. J Neurotrauma. 2002;19:1127–38.

    Article  PubMed  Google Scholar 

  42. Périard D, Rey MA, Casagrande D, Vesin JM, Carrera E, Hayoz D. The effect of valsartan versus non-RAAS treatment on autoregulation of cerebral blood flow. Cerebrovasc Dis. 2012;34:78–85.

    Article  PubMed  Google Scholar 

  43. Brodie FG, Atkins ER, Robinson TG, Panerai RB. Reliability of dynamic cerebral autoregulation measurement using spontaneous fluctuations in blood pressure. Clin sci (Lond). 2009;116:513–20.

    Article  Google Scholar 

  44. Ramos EG, Simpson DM, Panerai RB, Nadal J, Lopes JM, Evans DH. Objective selection of signals for assessment of cerebral blood flow autoregulation in neonates. Physiol Meas. 2006;27:35–49.

    Article  CAS  PubMed  Google Scholar 

  45. Katsogridakis E, Bush G, Fan L, et al. Detection of impaired cerebral autoregulation improves by increasing arterial blood pressure variability. J Cereb Blood Flow Metab. 2013;33:519–23.

    Article  PubMed Central  PubMed  Google Scholar 

  46. Czosnyka M, Smielewski P, Lavinio A, Pickard JD, Panerai RB. An assessment of dynamic autoregulation from spontaneous fluctuations of cerebral blood flow velocity: a comparison of two models, index of autoregulation and mean flow index. Anaesth Analg. 2008;106:234–9.

    Article  Google Scholar 

  47. Piechnik SK, Yang X, Czosnyka M, et al. The continuous assessment of cerebrovascular reactivity: a validation of the method in healthy volunteers. Anesth Analg. 1999;89:944–9.

    CAS  PubMed  Google Scholar 

  48. 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;41:2391–5.

    Article  PubMed  Google Scholar 

  49. Banks JL, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke. 2007;38:1091–6.

    Article  PubMed  Google Scholar 

  50. Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2011;31:1443–51.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Barth.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fontana, J., Moratin, J., Ehrlich, G. et al. Dynamic Autoregulatory Response After Aneurysmal Subarachnoid Hemorrhage and Its Relation to Angiographic Vasospasm and Clinical Outcome. Neurocrit Care 23, 355–363 (2015). https://doi.org/10.1007/s12028-014-0104-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-014-0104-7

Keywords

Navigation