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Prediction of Delayed Cerebral Ischemia After Subarachnoid Hemorrhage Using Cerebral Blood Flow Velocities and Cerebral Autoregulation Assessment

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Abstract

Background

The risk of delayed cerebral ischemia (DCI) after subarachnoid hemorrhage (SAH) is associated with large cerebral artery vasospasm, but vasospasm is not a strong predictor for DCI. Assessment of cerebral autoregulation with transcranial Doppler (TCD) may improve the prediction of DCI. The aim of this prospective study was to assess the value of TCD-derived variables to be used alone or in combination for prediction of DCI.

Methods

We included consecutive patients with low-grade aneurysmal SAH within 4 days of aneurysm rupture. Cerebral autoregulation was evaluated using the moving correlation coefficient Mx calculated from spontaneous fluctuations of cerebral blood flow velocities and arterial blood pressure. Transcranial color-coded sonography was performed to assess large artery vasospasm.

Results

Thirty patients (19 women and 11 men; mean age ± SD 44.7 ± 12.1 years) were included. Twenty (66.7 %) patients had vasospasm. DCI occurred in six (20 %) patients after a median delay of 10 days (range 8–13 days). Cerebral autoregulation was impaired at baseline and at day 7 and then returned to normal at day 14. Neither cerebral autoregulation impairment nor large artery vasospasm alone was associated with DCI. In contrast, the combination of large artery vasospasm with worsening impairment of cerebral autoregulation from baseline to day 7 was significantly correlated to subsequent DCI (p = 0.007).

Conclusions

Early deterioration of cerebral autoregulation was strongly predictive of DCI in patients with large artery vasospasm after low-grade SAH. Our results suggest that consideration to both cerebral blood flow velocities and cerebral autoregulation may improve the prediction of DCI.

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References

  1. 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 

  2. Koffijberg H, Buskens E, Granath F, et al. Subarachnoid haemorrhage in Sweden 1987–2002: regional incidence and case fatality rates. J Neurol Neurosurg Psychiatry. 2008;79(3):294–9.

    Article  CAS  PubMed  Google Scholar 

  3. Qureshi AI, Suri MF, Nasar A, et al. Trends in hospitalization and mortality for subarachnoid hemorrhage and unruptured aneurysms in the United States. Neurosurgery. 2005;57(1):1–8 discussion 1-8.

    Article  PubMed  Google Scholar 

  4. van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369(9558):306–18.

    Article  PubMed  Google Scholar 

  5. Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm–the clinical manifestations. Neurosurgery. 1977;1(3):245–8.

    Article  CAS  PubMed  Google Scholar 

  6. Seiler RW, Grolimund P, Aaslid R, Huber P, Nornes H. Cerebral vasospasm evaluated by transcranial ultrasound correlated with clinical grade and CT-visualized subarachnoid hemorrhage. J Neurosurg. 1986;64(4):594–600.

    Article  CAS  PubMed  Google Scholar 

  7. Grosset DG, McDonald I, Cockburn M, Straiton J, Bullock RR. Prediction of delayed neurological deficit after subarachnoid haemorrhage: a CT blood load and Doppler velocity approach. Neuroradiology. 1994;36(6):418–21.

    Article  CAS  PubMed  Google Scholar 

  8. Grosset DG, Straiton J, du Trevou M, Bullock R. Prediction of symptomatic vasospasm after subarachnoid hemorrhage by rapidly increasing transcranial Doppler velocity and cerebral blood flow changes. Stroke. 1992;23(5):674–9.

    Article  CAS  PubMed  Google Scholar 

  9. de Rooij NK, Rinkel GJ, Dankbaar JW, Frijns CJ. Delayed cerebral ischemia after subarachnoid hemorrhage: a systematic review of clinical, laboratory, and radiological predictors. Stroke. 2013;44(1):43–54.

    Article  PubMed  Google Scholar 

  10. Kassell NF, Sasaki T, Colohan AR, Nazar G. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke. 1985;16(4):562–72.

    Article  CAS  PubMed  Google Scholar 

  11. Ohkuma H, Manabe H, Tanaka M, Suzuki S. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2000;31(7):1621–7.

    Article  CAS  PubMed  Google Scholar 

  12. Rabinstein AA, Friedman JA, Weigand SD, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35(8):1862–6.

    Article  PubMed  Google Scholar 

  13. 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 

  14. 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 

  15. 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):819–25 discussions 25-6.

    Article  CAS  PubMed  Google Scholar 

  16. 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 

  17. 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 

  18. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke. 1989;20(1):45–52.

    Article  CAS  PubMed  Google Scholar 

  19. Lysakowski C, Walder B, Costanza MC, Tramer MR. Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review. Stroke. 2001;32(10):2292–8.

    Article  CAS  PubMed  Google Scholar 

  20. Soehle M, Czosnyka M, Pickard JD, Kirkpatrick PJ. Continuous assessment of cerebral autoregulation in subarachnoid hemorrhage. Anesth Analg. 2004;98(4):1133–9 table of contents.

    Article  PubMed  Google Scholar 

  21. Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013;35(2):93–112.

    Article  PubMed  Google Scholar 

  22. Nasr N, Traon AP, Czosnyka M, Tiberge M, Schmidt E, Larrue V. Cerebral autoregulation in patients with obstructive sleep apnea syndrome during wakefulness. Eur J Neurol. 2009;16(3):386–91.

    Article  CAS  PubMed  Google Scholar 

  23. Lindegaard KF. The role of transcranial Doppler in the management of patients with subarachnoid haemorrhage–a review. Acta Neurochir Suppl. 1999;72:59–71.

    CAS  PubMed  Google Scholar 

  24. Krejza J, Kochanowicz J, Mariak Z, Lewko J, Melhem ER. Middle cerebral artery spasm after subarachnoid hemorrhage: detection with transcranial color-coded duplex US. Radiology. 2005;236(2):621–9.

    Article  PubMed  Google Scholar 

  25. 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 

  26. Lavinio A, Schmidt EA, Haubrich C, Smielewski P, Pickard JD, Czosnyka M. Noninvasive evaluation of dynamic cerebrovascular autoregulation using Finapres plethysmograph and transcranial Doppler. Stroke. 2007;38(2):402–4.

    Article  PubMed  Google Scholar 

  27. Smielewski P, Czosnyka M, Steiner L, Belestri M, Piechnik S, Pickard JD. ICM+: software for on-line analysis of bedside monitoring data after severe head trauma. Acta Neurochir Suppl. 2005;95:43–9.

    Article  CAS  PubMed  Google Scholar 

  28. Jaeger M, Soehle M, Schuhmann MU, Meixensberger J. Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke. 2011;43(8):2097–101.

    Article  Google Scholar 

  29. Dernbach PD, Little JR, Jones SC, Ebrahim ZY. Altered cerebral autoregulation and CO2 reactivity after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1988;22(5):822–6.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. Stein SC, Browne KD, Chen XH, Smith DH, Graham DI. Thromboembolism and delayed cerebral ischemia after subarachnoid hemorrhage: an autopsy study. Neurosurgery. 2006;59(4):781–7 discussion 7-8.

    Article  PubMed  Google Scholar 

  32. Romano JG, Forteza AM, Concha M, et al. Detection of microemboli by transcranial Doppler ultrasonography in aneurysmal subarachnoid hemorrhage. Neurosurgery. 2002;50(5):1026–30 discussion 30-1.

    PubMed  Google Scholar 

  33. Sun BL, Zheng CB, Yang MF, Yuan H, Zhang SM, Wang LX. Dynamic alterations of cerebral pial microcirculation during experimental subarachnoid hemorrhage. Cell Mol Neurobiol. 2009;29(2):235–41.

    Article  PubMed  Google Scholar 

  34. 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(3):677–82.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  36. Budohoski KP, Czosnyka M, Smielewski P, et al. Cerebral autoregulation after subarachnoid hemorrhage: comparison of three methods. J Cereb Blood Flow Metab. 2013;33(3):449–56.

    Article  PubMed Central  PubMed  Google Scholar 

  37. 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. 2012;17(2):211–8.

    Article  PubMed  Google Scholar 

  38. Proust F, Callonec F, Clavier E, et al. Usefulness of transcranial color-coded sonography in the diagnosis of cerebral vasospasm. Stroke. 1999;30(5):1091–8.

    Article  CAS  PubMed  Google Scholar 

  39. Mariak Z, Krejza J, Swiercz M, Kordecki K, Lewko J. Accuracy of transcranial color Doppler ultrasonography in the diagnosis of middle cerebral artery spasm determined by receiver operating characteristic analysis. J Neurosurg. 2002;96(2):323–30.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a grant from “la Direction de la Recherche Clinique et de l’Innovation (DRCI)” at Toulouse University Hospital, Toulouse, France. Portions of this work were presented in oral communication form at the National Neurosurgery Conference, Toulouse, France, 2012 and at the International Stroke Conference, Hawaï, Honolulu, 2013.

Conflict of interest

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

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Authors and Affiliations

  1. Department of Neurology, University Hospital of Toulouse, Toulouse, France

    Lionel Calviere, Nathalie Nasr, Alain Viguier & Vincent Larrue

  2. Department of Neurosurgery, University Hospital of Toulouse, Toulouse, France

    Bernard Tissot & Jean-Christophe Sol

  3. Department of Biostatistics and Epidemiology, University Hospital of Toulouse, Toulouse, France

    Catherine Arnaud

  4. Academic Neurosurgical Unit, Addenbrooke’s Hospital, University of Cambridge, Cambridge, UK

    Marek Czosnyka

  5. Neurovascular Unit, Department of Neurology, CHU Purpan, Hopital Pierre Paul Riquet, Place du Dr Baylac, 31059, Toulouse Cedex 9, France

    Lionel Calviere

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  1. Lionel Calviere
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Correspondence to Lionel Calviere.

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Calviere, L., Nasr, N., Arnaud, C. et al. Prediction of Delayed Cerebral Ischemia After Subarachnoid Hemorrhage Using Cerebral Blood Flow Velocities and Cerebral Autoregulation Assessment. Neurocrit Care 23, 253–258 (2015). https://doi.org/10.1007/s12028-015-0125-x

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  • DOI: https://doi.org/10.1007/s12028-015-0125-x

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