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Early Transcranial Doppler Evaluation of Cerebral Autoregulation Independently Predicts Functional Outcome After Aneurysmal Subarachnoid Hemorrhage

  • Carla B. RynkowskiEmail author
  • Airton Leonardo de Oliveira Manoel
  • Marcelo Martins dos Reis
  • Corina Puppo
  • Paulo Valdeci Worm
  • Diego Zambonin
  • Marino Muxfeldt Bianchin
Original Work
  • 11 Downloads

Abstract

Background

Cerebral autoregulation (CA) impairment after aneurysmal subarachnoid hemorrhage (SAH) has been associated with delayed cerebral ischemia and an unfavorable outcome. We investigated whether the early transient hyperemic response test (THRT), a transcranial Doppler (TCD)-based CA evaluation method, can predict functional outcome 6 months after aneurysmal SAH.

Methods

This is a prospective observational study of all aneurysmal SAH patients consecutively admitted to a single center between January 2016 and February 2017. CA was evaluated within 72 h of hemorrhage by THRT, which describes the changes in cerebral blood flow velocity after a brief compression of the ipsilateral common carotid artery. CA was considered to be preserved when an increase ≥ 9% of baseline systolic velocity was present. According to the modified Rankin Scale (mRS: 4–6), the primary outcome was unfavorable 6 months after hemorrhage. Secondary outcomes included cerebral infarction, vasospasm on TCD, and an unfavorable outcome at hospital discharge.

Results

Forty patients were included (mean age = 54 ± 12 years, 70% females). CA was impaired in 19 patients (47.5%) and preserved in 21 (52.5%). Impaired CA patients were older (59 ± 13 vs. 50 ± 9, p = 0.012), showed worse neurological conditions (Hunt&Hess 4 or 5–47.4% vs. 9.5%, p = 0.012), and clinical initial condition (APACHE II physiological score—12 [5.57–13] vs. 3.5 [3, 4, 5], p = 0.001). Fourteen patients in the impaired CA group and one patient in the preserved CA group progressed to an unfavorable outcome (73.7% vs. 4.7%, p = 0.0001). The impaired CA group more frequently developed cerebral infarction than the preserved CA group (36.8% vs. 0%, p = 0.003, respectively). After multivariate analysis, impaired CA (OR 5.15 95% CI 1.43–51.99, p = 0.033) and the APACHE II physiological score (OR 1.67, 95% CI 1.01–2.76, p = 0.046) were independently associated with an unfavorable outcome.

Conclusions

Early CA impairment detected by TCD and admission APACHE II physiological score independently predicted an unfavorable outcome after SAH.

Keywords

Subarachnoid hemorrhage Cerebral circulation Transcranial Doppler Cerebral autoregulation Transient hyperemic response test 

Notes

Acknowledgements

We thank Vânia Naomi Hirakata for assistance with statistical analyzes, the laboratory team of Hospital Cristo Redentor for assistance with blood collection and Neurosurgery residents of Hospital Cristo Redentor for helping with the acquisition of some data. MMB is supported by Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq) (Grants #485423/2012-0, #307084/2014-0, #438548/2018-3 #312683/2018-9).

Authors’ Contributions

CBR contributed to the conception and design, acquisition, analysis and interpretation of data, drafting the article. ALOM contributed to statistical analysis, critically revising and drafting the article. MMR contributed to the design, acquisition, and analysis of data. CP contributed to conception and design, analysis and interpretation of data, critically revising the article. PVW contributed to acquisition, analysis, and interpretation of data. DZ contributed to acquisition and analysis of data. MMB contributed to conception and design, analysis, and interpretation of data, critically revising the article and supervising the study.

Source of Support

None.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from each participant in the study.

References

  1. 1.
    Johnston SC, Selvin S, Gress DR. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology. 1998;50:1413–8.CrossRefGoogle Scholar
  2. 2.
    Lovelock CE, Rinkel G, Rochwell PM. Time trends in outcome of subarachnoid hemorrhage: population-based study and systematic review. Neurology. 2010;74:1494–501.CrossRefGoogle Scholar
  3. 3.
    Diringer MN, Zazulia AR. Aneurysmal subarachnoid hemorrhage: strategies for preventing vasospasm in the intensive care unit. Semin Respir Crit Care Med. 2017;38(6):760–7.CrossRefGoogle Scholar
  4. 4.
    Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010;41(8):e519–36.CrossRefGoogle Scholar
  5. 5.
    Fauvage B, Canet C, Coppo F, Jacquot C, Payen JF. Long-term outcome of patients after aneurysmal SAH. Ann Fr Anesth Reanim. 2007;26(11):959–64.CrossRefGoogle Scholar
  6. 6.
    de Oliveira Manoel AL, Mansur A, Silva GS, Germans MR, Jaja BN, Kouzmina E, et al. Functional outcome after poor-grade subarachnoid hemorrhage: a single-center study and systematic literature review. Neurocrit Care. 2016;25(3):338–50.CrossRefGoogle Scholar
  7. 7.
    Galea JP, Dulhanty L, Patel HC, UK, Ireland Subarachnoid Hemorrhage Database C. Predictors of outcome in aneurysmal subarachnoid hemorrhage patients: observations from a multicenter data set. Stroke. 2017;48(11):2958–63.CrossRefGoogle Scholar
  8. 8.
    Weir B, Grace M, Hansen J, Rothberg C. Time course of vasospasm in man. J Neurosurg. 1978;48(2):173–8.CrossRefGoogle Scholar
  9. 9.
    Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJ, Rinkel GJ. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology. 2009;51(12):813–9.CrossRefGoogle Scholar
  10. 10.
    Shen J, Pan JW, Fan ZX, Xiong XX, Zhan RY. Dissociation of vasospasm-related morbidity and outcomes in patients with aneurysmal subarachnoid hemorrhage treated with clazosentan: a meta-analysis of randomized controlled trials. J Neurosurg. 2013;119(1):180–9.CrossRefGoogle Scholar
  11. 11.
    Brathwaite S, Macdonald RL. Current management of delayed cerebral ischemia: update from results of recent clinical trials. Transl Stroke Res. 2014;5(2):207–26.CrossRefGoogle Scholar
  12. 12.
    Otite F, Mink S, Tan CO, Puri A, Zamani AA, Mehregan A, et al. Impaired cerebral autoregulation is associated with vasospasm and delayed cerebral ischemia in subarachnoid hemorrhage. Stroke. 2014;45(3):677–82.CrossRefGoogle Scholar
  13. 13.
    de Oliveira Manoel AL, Macdonald RL. Neuroinflammation as a target for intervention in subarachnoid hemorrhage. Front Neurol. 2018;9:292.CrossRefGoogle Scholar
  14. 14.
    Lassen NA. Cerebral blood flow and oxygen consumption in man. Physiol Rev. 1959;39:183–238.CrossRefGoogle Scholar
  15. 15.
    Panerai RB. Assessment of cerebral pressure autoregulation in humans—a review of measurement methods. Physiol Meas. 1998;19:305–38.CrossRefGoogle Scholar
  16. 16.
    Budohoski KP, Czosnyka M, Smielewski P, Kasprowicz M, Helmy A, Bulters D, et al. Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke. 2012;43(12):3230–7.CrossRefGoogle Scholar
  17. 17.
    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.CrossRefGoogle Scholar
  18. 18.
    Fontana J, Moratin J, Ehrlich G, Scharf J, Weiss C, Schmieder K, et al. Dynamic autoregulatory response after aneurysmal subarachnoid hemorrhage and its relation to angiographic vasospasm and clinical outcome. Neurocrit Care. 2015;23(3):355–63.CrossRefGoogle Scholar
  19. 19.
    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.CrossRefGoogle Scholar
  20. 20.
    Budohoski KP, Czosnyka M, Kirkpatrick PJ, Reinhard M, Varsos GV, Kasprowicz M, et al. Bilateral failure of cerebral autoregulation is related to unfavorable outcome after subarachnoid hemorrhage. Neurocrit Care. 2015;22(1):65–73.CrossRefGoogle Scholar
  21. 21.
    Donnelly J, Budohoski KP, Smielewski P, Czosnyka M. Regulation of the cerebral circulation: bedside assessment and clinical implications. Crit Care. 2016;20(1):129.CrossRefGoogle Scholar
  22. 22.
    Rivera-Lara L, Zorrilla-Vaca A, Geocadin R, Ziai W, Healy R, Thompson R, et al. Predictors of outcome with cerebral autoregulation monitoring: a systematic review and meta-analysis. Crit Care Med. 2017;45(4):695–704.CrossRefGoogle Scholar
  23. 23.
    Giller CA. A bedside test for cerebral autoregulation using transcranial Doppler ultrasound. Acta Neurochir (Wien). 1991;108:7–14.CrossRefGoogle Scholar
  24. 24.
    Soehle M, Chatfield DA, Czosnyka M, Kirkpatrick PJ. Predictive value of initial clinical status, intracranial pressure and transcranial Doppler pulsatility after subarachnoid haemorrhage. Acta Neurochir (Wien). 2007;149(6):575–83.CrossRefGoogle Scholar
  25. 25.
    Diringer MN, Bleck TP, Claude Hemphill J 3rd, Menon D, Shutter L, Vespa P, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit Care. 2011;15(2):211–40.CrossRefGoogle Scholar
  26. 26.
    Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, 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.CrossRefGoogle Scholar
  27. 27.
    de Oliveira Manoel AL, Goffi A, Marotta TR, Schweizer TA, Abrahamson S, Macdonald RL. The critical care management of poor-grade subarachnoid haemorrhage. Crit Care. 2016;20(1):21.CrossRefGoogle Scholar
  28. 28.
    Sloan MA, et al. Transcranial Doppler detection of vertebrobasilar vasospasm following subarachnoid hemorrhage. Stroke. 1994;25:2187–97.CrossRefGoogle Scholar
  29. 29.
    Vergouwen MDI, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies. Stroke. 2010;41:2391–5.CrossRefGoogle Scholar
  30. 30.
    Smielewski P, Czosnyka M, Kirkpatrick P, McEroy H, Rutkowska H, Pickard JD. Assessment of cerebral autoregulation using carotid artery compression. Stroke. 1996;27(12):2197–203.CrossRefGoogle Scholar
  31. 31.
    Smielewski P, Czosnyka M, Kirkpatrick P, Pickard JD. Evaluation of the transient hyperemic response test in head-injured patients. J Neurosurg. 1997;86:773–8.CrossRefGoogle Scholar
  32. 32.
    Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38(8):2315–21.CrossRefGoogle Scholar
  33. 33.
    Lo BW, Fukuda H, Nishimura Y, Farrokhyar F, Thabane L, Levine MA. Systematic review of clinical prediction tools and prognostic factors in aneurysmal subarachnoid hemorrhage. Surg Neurol Int. 2015;6:135.CrossRefGoogle Scholar
  34. 34.
    Lang EW, Diehl RR, Mehdorn M. 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.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    Rasulo FA, et al. Are optimal cerebral perfusion pressure and cerebrovascular autoregulation related to long-term outcome in patients with aneurysmal subarachnoid hemorrhage? J Neurosurg Anesthesiol. 2012;24:3–8.CrossRefGoogle Scholar
  37. 37.
    Gaasch M, Schiefecker AJ, Kofler M, Beer R, Rass V, Pfausler B, et al. Cerebral autoregulation in the prediction of delayed cerebral ischemia and clinical outcome in poor-grade aneurysmal subarachnoid hemorrhage patients. Crit Care Med. 2018;46(5):774–80.CrossRefGoogle Scholar
  38. 38.
    Tam AKH, Ilodigwe D, Mocco J, Mayer S, Kassell N, Ruefenacht D, et al. Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocrit Care. 2010;13(2):182–9.CrossRefGoogle Scholar
  39. 39.
    Lam JMK, Smielewski P, Czosnyka M, Pickard JD, Kirkpatrick P. Prediction delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery. 2000;47:819–26.CrossRefGoogle Scholar
  40. 40.
    Carrera E, Schmidt JM, Oddo M, Fernandez L, Claassen J, Seder D, et al. Transcranial Doppler for predicting delayed cerebral ischemia after subarachnoid hemorrhage. Neurosurgery. 2009;65(2):316–23 (discussion 23-4).CrossRefGoogle Scholar
  41. 41.
    Smielewski P, Czosnyka M, Iyer V, Piechnik S, Whitehouse H, Pickard J. Computerised transient hyperaemic response test—a method for the assessment of cerebral autoregulation. Ultrasound Med Biol. 1995;21(5):599–611.CrossRefGoogle Scholar
  42. 42.
    Ferguson S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67 (discussion 67).CrossRefGoogle Scholar
  43. 43.
    Schmidt JM, Rincon F, Fernandez A, Resor C, Kowalski RG, Claassen J, et al. Cerebral infarction associated with acute subarachnoid hemorrhage. Neurocrit Care. 2007;7(1):10–7.CrossRefGoogle Scholar
  44. 44.
    Jabbarli R, Reinhard M, Niesen WD, Roelz R, Shah M, Kaier K, et al. Predictors and impact of early cerebral infarction after aneurysmal subarachnoid hemorrhage. Eur J Neurol. 2015;22(6):941–7.CrossRefGoogle Scholar
  45. 45.
    Stienen MN, Germans M, Burkhardt JK, Neidert MC, Fung C, Bervini D, et al. Predictors of in-hospital death after aneurysmal subarachnoid hemorrhage: analysis of a nationwide database (Swiss SOS [Swiss Study on Aneurysmal Subarachnoid Hemorrhage]). Stroke. 2018;49(2):333–40.CrossRefGoogle Scholar
  46. 46.
    Claassen J, Vu A, Kreiter KT, Kowalski RG, Du EY, Ostapkovich N, et al. Effect of acute physiologic derangements on outcome after subarachnoid hemorrhage. Crit Care Med. 2004;32(3):832–8.CrossRefGoogle Scholar
  47. 47.
    Lantigua H, Ortega-Gutierrez S, Schmidt JM, Lee K, Badjatia N, Agarwal S, et al. Subarachnoid hemorrhage: who dies, and why? Crit Care. 2015;19:309.CrossRefGoogle Scholar
  48. 48.
    Tseng MY, Al-Rawi PG, Czosnyka M, Hutchinson PJ, Richards H, Pickard JD, et al. Enhancement of cerebral blood flow using systemic hypertonic saline therapy improves outcome in patients with poor-grade spontaneous subarachnoid hemorrhage. J Neurosurg. 2007;107(2):274–82.CrossRefGoogle Scholar
  49. 49.
    Yundt KD, Grubb RL Jr, Diringer MN, Powers WJ. Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. J Cereb Blood Flow Metab. 1998;18(4):419–24.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society 2019

Authors and Affiliations

  • Carla B. Rynkowski
    • 1
    • 2
    Email author
  • Airton Leonardo de Oliveira Manoel
    • 3
    • 4
  • Marcelo Martins dos Reis
    • 5
  • Corina Puppo
    • 6
  • Paulo Valdeci Worm
    • 5
  • Diego Zambonin
    • 5
  • Marino Muxfeldt Bianchin
    • 1
    • 7
  1. 1.Graduate Program in Medical ScienceUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Adult Critical Care UnitHospital Cristo RedentorPorto AlegreBrazil
  3. 3.Critical Care UnitHospital Paulistano, UnitedHealth Group BrazilSão PauloBrazil
  4. 4.Keenan Research Centre for Biomedical Science, St. Michael’s HospitalUniversity of TorontoTorontoCanada
  5. 5.Department of NeurosurgeryHospital Cristo RedentorPorto AlegreBrazil
  6. 6.Hospital de Clínicas Dr. Manuel QuintelaUniversidad de la RepublicaMontevideoUruguay
  7. 7.Division of NeurologyHospital de Clínicas de Porto Alegre – B.R.A.I.NPorto AlegreBrazil

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