Advertisement

Diagnostic accuracy of somatosensory evoked potentials during intracranial aneurysm clipping for perioperative stroke

  • Ahmed I. Kashkoush
  • Christopher Nguyen
  • Jeffrey Balzer
  • Miguel Habeych
  • Donald J. Crammond
  • Parthasarathy D. ThirumalaEmail author
Original Research
  • 77 Downloads

Abstract

Somatosensory evoked potentials (SSEPs) are utilized during aneurysm clipping to detect intraoperative ischemia. We assess the diagnostic accuracy of SSEPs in predicting perioperative stroke during aneurysm clipping. A retrospective review was conducted of 429 consecutive patients who underwent surgical clipping for ruptured and unruptured cerebral aneurysms with intraoperative SSEP monitoring from 2006 to 2013. The relationship between perioperative stroke and SSEP changes was analyzed by calculating the sensitivity, specificity, and area under a Receiving Operating Characteristic curve. Sensitivity and specificity were 42% and 90%, respectively. Area under the curve was 0.66 (95% confidence interval, 0.53–0.79). Reclassification of reversible temporary clip changes to correct for paradoxical classification of SSEP false positives raised the sensitivity from 42 to 65% (p = 0.041, Chi squared test). EEG (electroencephalography) changes increased the specificity (98% vs. 90%, p < 0.001, McNemar’s test), but not sensitivity (48% vs. 42%, p = 0.621, McNemar’s test) of SSEPs for perioperative stroke. A stepwise logistic regression model selected SSEP amplitude loss (p = 0.006, OR = 3.7 [95% CI 1.5–9.2]) and the SSEP change duration (p = 0.034, OR = 1.8 [95% CI 1.1–3.1]) as independent predictors of perioperative stroke. SSEP changes induced by temporary clipping were highly reversible compared to other SSEP changes (94% vs. 60%, p = 0.003, Fisher exact test), and typically responded to clip removal or readjustment. SSEP changes have high specificity and modest sensitivity for perioperative stroke. Stroke risk is a function of both the magnitude of SSEP amplitude loss and the duration of its loss. Given the modest sensitivity, patients may benefit from multimodal monitoring including motor-evoked potentials during cerebral aneurysm surgery.

Keywords

Diagnostic accuracy Intracranial aneurysm Intraoperative neuromonitoring Somatosensory evoked potentials 

Notes

Funding

None.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Krayenbuhl N, et al. Symptomatic and silent ischemia associated with microsurgical clipping of intracranial aneurysms: evaluation with diffusion-weighted MRI. Stroke. 2009;40(1):129–33.CrossRefPubMedGoogle Scholar
  2. 2.
    Jun T, et al. Preliminary study on safe thresholds for temporary internal carotid artery occlusion in aneurysm surgery based on motor-evoked potential monitoring. Surg Neurol Int. 2014;5:47.CrossRefGoogle Scholar
  3. 3.
    Wicks RT, et al. Impact of changes in intraoperative somatosensory evoked potentials on stroke rates after clipping of intracranial aneurysms. Neurosurgery. 2012;70(5):1114–24.  https://doi.org/10.1227/NEU.0b013e31823f5cf7.CrossRefPubMedGoogle Scholar
  4. 4.
    Friedman W, et al. Evoked potential monitoring during aneurysm operation: observation after fifty cases. Neurosurgery. 1987;20(5):678–87.CrossRefPubMedGoogle Scholar
  5. 5.
    Quiñones-Hinojosa A, et al. Transcranial motor evoked potentials during basilar artery aneurysm surgery: technique application for 30 consecutive patients. Neurosurgery. 2004;54(4):916–24.CrossRefPubMedGoogle Scholar
  6. 6.
    Penchet G, et al. Use of intraoperative monitoring of somatosensory evoked potentials to prevent ischaemic stroke after surgical exclusion of middle cerebral artery aneurysms. Acta Neurochir. 2007;149(4):357–64.CrossRefPubMedGoogle Scholar
  7. 7.
    Lopéz JR, Chang SD, Steinberg GK. The use of electrophysiological monitoring in the intraoperative management of intracranial aneurysms. J Neurol Neurosurg Psychiatry. 1999;66(2):189–96.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Little J, Lesser R, Luders H. Electrophysiological monitoring during basilar aneurysm operation. Neurosurgery. 1987;20(3):421–7.CrossRefPubMedGoogle Scholar
  9. 9.
    Schramm J, et al. Surgical and electrophysiological observations during clipping of 134 aneurysms with evoked potential monitoring. Neurosurgery. 1990;26(1):61–70.CrossRefPubMedGoogle Scholar
  10. 10.
    Buchthal A, Belopavlovic M, Mooij J. Evoked potential monitoring and temporary clipping in cerebral aneurysm surgery. Acta Neurochir. 1988;99(1–2):28–36.CrossRefGoogle Scholar
  11. 11.
    Kashkoush AI, et al. Somatosensory evoked potentials during temporary arterial occlusion for intracranial aneurysm surgery: predictive value for perioperative stroke. World Neurosurg. 2017;104:442–51.CrossRefPubMedGoogle Scholar
  12. 12.
    Kashkoush AI, et al. Perioperative stroke after cerebral aneurysm clipping: risk factors and postoperative impact. J Clin Neurosci. 2017;44:188–95.CrossRefPubMedGoogle Scholar
  13. 13.
    Branston N, et al. Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp Neurol. 1974;45(2):195–208.CrossRefPubMedGoogle Scholar
  14. 14.
    Morawetz RB, et al. Cerebral blood flow determined by hydrogen clearance during middle cerebral artery occlusion in unanesthetized monkeys. Stroke. 1978;9(2):143–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Nwachuku EL, Balzer J, Yabes JG, Habeych ME, Crammond DJ, Thirumala PD. Diagnostic value of somatosensory evoked potential changes during carotid endarterectomy: a systematic review and meta-analysis. JAMA Neurol. 2015;72(1):73–80.CrossRefPubMedGoogle Scholar
  16. 16.
    Balzer JR, et al. Simultaneous somatosensory evoked potential and electromyographic recordings during lumbosacral decompression and instrumentation. Neurosurgery. 1998;42(6):1318–24 discussion 1324-5.CrossRefPubMedGoogle Scholar
  17. 17.
    Chen ZY, Wong HK, Chan YH. Variability of somatosensory evoked potential monitoring during scoliosis surgery. J Spinal Disord Tech. 2004;17(6):470–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Guo L, Gelb AW. The use of motor evoked potential monitoring during cerebral aneurysm surgery to predict pure motor deficits due to subcortical ischemia. Clin Neurophysiol. 2011;122(4):648–55.CrossRefPubMedGoogle Scholar
  19. 19.
    Skirboll S, Newell D. Noninvasic physiologic evaluation of the aneurysm patient. Neurosurg Clin N Am. 1998;9(3):463–83.CrossRefPubMedGoogle Scholar
  20. 20.
    Holland N. Subcortical strokes from intracranial aneurysm surgery: implications for intraoperative neuromonitoring. J Clin Neurophysiol. 1998;15(5):439–46.CrossRefPubMedGoogle Scholar
  21. 21.
    Thirumala PD, et al. Somatosensory-evoked potential monitoring during instrumented scoliosis corrective procedures: validity revisited. Spine J. 2014;14(8):1572–80.CrossRefPubMedGoogle Scholar
  22. 22.
    York DH, Chabot RJ, Gaines RW. Response variability of somatosensory evoked potentials during scoliosis surgery. Spine (Phila Pa 1976). 1987;12(9):864–76.CrossRefGoogle Scholar
  23. 23.
    Brigadier G. Aids to the examination of the peripheral nervous system. London: Crown Copyright. 70; 1943.Google Scholar
  24. 24.
    Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974;2(7872):81–4.CrossRefPubMedGoogle Scholar
  25. 25.
    Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143(1):29–36.CrossRefPubMedGoogle Scholar
  26. 26.
    Zhu F, et al. Intraoperative evoked potential monitoring for detecting cerebral injury during adult aneurysm clipping surgery: a systematic review and meta-analysis of diagnostic test accuracy. BMJ Open. 2019;9(2):e022810.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Mizoi K, Yoshimoto T. Permissible temporary occlusion time in aneurysm surgery as evaluated by evoked potential monitoring. Neurosurgery. 1993;33(3):434–40 discussion 440.PubMedGoogle Scholar
  28. 28.
    Wang M, et al. A prediction of postoperative neurological deficits following intracranial aneurysm surgery using somatosensory evoked potential deterioration duration. Neurosurg Rev. 2019.  https://doi.org/10.1007/s10143-019-01077-5.CrossRefPubMedGoogle Scholar
  29. 29.
    Felbaum D, et al. Real-time evaluation of anterior choroidal artery patency during aneurysm clipping. Cureus. 2016;8(2):e495.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Raabe A, et al. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52(1):132–9 discussion 139.PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Ahmed I. Kashkoush
    • 1
  • Christopher Nguyen
    • 2
  • Jeffrey Balzer
    • 3
    • 4
  • Miguel Habeych
    • 3
  • Donald J. Crammond
    • 3
  • Parthasarathy D. Thirumala
    • 3
    • 5
    Email author
  1. 1.Department of Neurological SurgeryCleveland Clinic FoundationClevelandUSA
  2. 2.Penn Dental MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  3. 3.Department of Neurological SurgeryUniversity of Pittsburgh Medical Center, UPMCPittsburghUSA
  4. 4.Department of NeuroscienceUniversity of PittsburghPittsburghUSA
  5. 5.Department of NeurologyUniversity of Pittsburgh Medical CenterPittsburghUSA

Personalised recommendations