Acta Neurochirurgica

, Volume 155, Issue 11, pp 2085–2096 | Cite as

Stratification of intraoperative ischemic impact by somatosensory evoked potential monitoring, diffusion-weighted imaging and magnetic resonance angiography in carotid endarterectomy with routine shunt use

  • Tomohiro InoueEmail author
  • Kazuo Tsutsumi
  • Kazuhiro Ohwaki
  • Akira Tamura
  • Hideaki Ono
  • Isamu Saito
  • Nobuhito Saito
Clinical Article - Vascular



Routine shunting to minimize ischemia during carotid endarterectomy (CEA) is controversial. The aim of this study was to stratify the ischemic parameters associated with CEA and evaluate the effect of routine shunting in attempting to mitigate those ischemia.


Data from 248 CEAs with routine shunting were retrospectively evaluated. Our assessment included somatosensory evoked potential (SSEP) amplitude reduction more than 50 % and longer than 5 min (SSEP<50%, >5 min), new postoperative diffusion-weighted imaging lesions (new DWI lesions), and severe stenosis as indicated by reduced ipsilateral middle cerebral artery (MCA) signal on preoperative magnetic resonance angiography (MRA asymmetry), as surrogates of hypoperfusion, microembli, and hemodynamic impairment, respectively.


SSEP<50%, >5 min occurred in 15 % of CEAs during cross-clamping, and shunting reversed the SSEP changes. New DWI lesions were observed in 4.1 %. Pre-clamping the common and external carotid artery during dissection (pre-clamp method) decreased the rate of new DWI lesions compared to without pre-clamping (3.5 % vs. 7.5 %, P = 0.22). Occlusion time was significantly longer in the pre-clamp method than without pre-clamping (P < 0.0001). However, the incidence of SSEP<50%, >5 min was not increased with the pre-clamp method (p = 1.0) when using information regarding SSEP and collaterals to modify the speed of shunt manipulation. MRA asymmetry was identified in 39 CEAs (15.8 %) with correction of asymmetry postoperatively. MRA asymmetry correlated with symptomatic hyperperfusion (P = 0.0034). Only three CEAs had symptomatic hyperperfusion (1.2 %) with minimal symptoms. Ten CEAs sustained transient ischemia, symptomatic hyperperfusion, or 30-day-stroke (composite postoperative ischemic symptoms). Logistic regression analysis confirmed that SSEP<50%, >5 min (p = 0.009), new DWI lesions (p = 0.004) and MRA asymmetry (p = 0.042) were independent predictors of composite postoperative ischemic symptoms.


SSEP<50%, >5 min, new DWI lesions, and MRA asymmetry were able to stratify the ischemic impacts in CEA. Meticulous routine shunting could mitigate those appropriately.


Carotid endarterectomy Cerebral ischemia Diffusion-weighted imaging Magnetic resonance angiography Shunt Somatosensory evoked potentials 



Carotid angiography


Common carotid artery


Carotid endarterectomy


Computed tomography


Computed tomographic angiography


Digital subtraction angiography


Diffusion-weighted imaging


External carotid artery


Internal carotid artery


Middle cerebral artery


Magnetic resonance angiography


Magnetic resonance imaging


Single photon emission computed tomography


Somatosensory evoked potentials


Superficial temporal artery


Transient ischemic attack


T2-weighted imaging



Conflicts of interest


Supplementary material

Video 1

Video clip showing CEA with the pre-clamp method. (MPG 30988 kb)


  1. 1.
    AbuRahma AF, Mousa AY, Stone PA (2011) Shunting during carotid endarterectomy. J Vasc Surg 54:1502–1510PubMedGoogle Scholar
  2. 2.
    Altinbas A, van Zandvoort MJE, van den Berg E, Jongen LM, Algra A, Moll FL, Nederkoorn PJ, Mali WPTM, Bonati LH, Brown MM, Kappelle LJ, van der Worp HB (2011) Cognition after carotid endarterectomy or stenting. A randomized comparison. Neurology 77:1084–1090PubMedCrossRefGoogle Scholar
  3. 3.
    Beese U, Langer H, Lang W, Dinkel M (1998) Comparison of near-infrared spectroscopy and somatosensory evoked potentials for the detection of cerebral ischemia during carotid endarterectomy. Stroke 29:2032–2037PubMedCrossRefGoogle Scholar
  4. 4.
    Bellosta R, Luzzani L, Carugati C, Talarico M, Sarcina A (2006) Routine shunting is a safe and reliable method of cerebral protection during carotid endarterectomy. Ann Vasc Surg 20:482–487PubMedCrossRefGoogle Scholar
  5. 5.
    Bond R, Rerkasem K, Rothwell PM (2003) Routine or selective carotid artery shunting for carotid endarterectomy (and different methods of monitoring in selective shunting). Stroke 34:824–825PubMedCrossRefGoogle Scholar
  6. 6.
    Branston NM, Ladds A, Symon L, Wang AD (1984) Comparison of the effect of ischemia on early components of the soamtosensory evoked potential in brainstem, thalamus, and cerebral cortex. J Cereb Blood Flow Metab 4:68–81PubMedCrossRefGoogle Scholar
  7. 7.
    Brinkman SD, Braun P, Ganji S, Morrell RM, Jacobs LA (1984) Neuropsychological performance one week after carotid endarterectomy reflects intra-operative ischemia. Stroke 15(3):497–503PubMedCrossRefGoogle Scholar
  8. 8.
    Cho H, Nemoto EM, Yonas H, Balzer J, Sclabassi RJ (1998) Cerebral monitoring by means of oximetry and somatosensory evoked potentials during carotid endarterectomy. J Neurosurg 89:533–538PubMedCrossRefGoogle Scholar
  9. 9.
    De Rango P, Caso V, Leys D, Paciaroni M, Lenti M, Cao P (2008) The role of carotid artery stenting and carotid endarterectomy in cognitive performance. A systematic review. Stroke 39:3116–3127PubMedCrossRefGoogle Scholar
  10. 10.
    De Vleeschauer P, Horsch S, Matamorous R (1988) Monitoring of somatosensory evoked potential in carotid surgery: results, usefulness and limitations of the method. Ann Vasc Surg 2(1):63–68CrossRefGoogle Scholar
  11. 11.
    Feliziani FT, Polidori MC, Rango PD, Mangialasche F, Monastero R, Ercolani S, Raichi T, Cornacchiola V, Nelles G, Cao P, Mecocci P (2010) Cognitive performance in elderly patients undergoing carotid endarterectomy or carotid artery stenting: a twelve-month follow-up study. Cerebrovasc Dis 30:244–251PubMedCrossRefGoogle Scholar
  12. 12.
    Furui T, Hasuo M (1984) Indwelling double-balloon shunt for carotid endarterectomy. Technical note. J Neurosurg 60:861–863PubMedCrossRefGoogle Scholar
  13. 13.
    Gaunt ME, Martin PJ, Smith JL, Rimmer T, Cherryman G, Ratliff DA, Bell PRF, Naylor AR (1994) Clinical relevance of intraoperative embolization detected by transcranial Doppler ultrasonography during carotid endarterectomy: a prospective study of 100 patients. Br J Surg 81:1435–1439PubMedCrossRefGoogle Scholar
  14. 14.
    Ghogawala Z, Westerveld M, Amin-Hanjani S (2008) Cognitive outcome after carotid revascularization: the role of cerebral emboli and hypoperfusion. Neurosurgery 62:385–395PubMedCrossRefGoogle Scholar
  15. 15.
    Halsey JH (1992) Risk and benefit of shunting in carotid endarterectomy. Stroke 23:1589–1587CrossRefGoogle Scholar
  16. 16.
    Hamdan AD, Pomposelli FB, Gibbons GW, Campbell DR, LoGerfo FW (1999) Perioperative stroke after 1001 consecutive carotid endarterectomy procedures without an electroencephalogram. Arch Surg 134:412–415PubMedCrossRefGoogle Scholar
  17. 17.
    Heyer EJ, Adams DC, Solomon RA, Todd GJ, Quest DO, McMahon DJ, Steneck SD, Choudhri TF, Connolly ES (1998) Neuropsychometric changes in patients after carotid endarterectomy. Stroke 29:1110–1115PubMedCrossRefGoogle Scholar
  18. 18.
    Heyer EJ, DeLaPaz R, Halazum HJ, Rampersad A, Sciacca R, Zurica J, Benvenisty AI, Quest DO, Todd GJ, Lavine S, Solomon RA, Connolly ES (2006) Neuropsychological dysfunction in the absence of structural evidence for cerebral ischemia after uncomplicated carotid endarterectomy. Neurosurgery 58:474–480PubMedCrossRefGoogle Scholar
  19. 19.
    Heyer EJ, Sharma R, Rampersad A, Winfree CJ, Mack WJ, Solomon RA, Todd GJ, McCormick PC, McMurtry JG, Quest DO, Stern Y, Lazar RM, Connolly ES (2002) A controlled prospective study of neuropsychological dysfunction following carotid endarterectomy. Arch Neurol 59:217–222PubMedCrossRefGoogle Scholar
  20. 20.
    Hirooka R, Ogasawara K, Inoue T, Fujiwara S, Sasaki M, Chida K, Ishigaki D, Kobayashi M, Nishimoto H, Otawara Y, Tsushima E, Ogawa A (2009) Simple assessment of cerebral hemodynamics using single-slab three dimensional time-of-flight magnetic resonance angiography in patients with quantitative perfusion single-photon emission computed tomography. AJNR Am J Neuroradiol 30:559–563PubMedCrossRefGoogle Scholar
  21. 21.
    Inoue T, Ohwaki K, Tamura A, Tsutsumi K, Saito I, Saito N (2013) Subclinical ischemia verified by somatosensory evoked potential amplitude reduction during carotid endarterectomy: negative effects on cognitive performance. J Neurosurg. doi: 10.3171/2013.1JNS121668 Google Scholar
  22. 22.
    Inoue T, Tsutsumi K, Maeda K, Adachi S, Tanaka S, Yako K, Saito K, Kunii N (2006) Incidence of ischemic lesions by diffusion-weighted imaging after carotid endarterectomy with routine shunt usage. Neurol Med Chir (Tokyo) 46:529–534CrossRefGoogle Scholar
  23. 23.
    Kawamata T, Okada Y, Kawashima A, Yoneyama T, Yamaguchi K, Ono Y, Hori T (2009) Postcarotid endarterectomy cerebral hyperperfusion can be prevented by minimizing intraoperative cerebral ischemia and strict postoperative blood pressure control under continuous sedation. Neurosurgery 64:447–454PubMedCrossRefGoogle Scholar
  24. 24.
    Kuroda H, Ogasawara K, Hirooka R, Kobayashi M, Fujiwara S, Chida K, Ishigaki D, Otawara Y, Ogawa A (2009) Prediction of cerebral hyperperfusion after carotid endarterectomy using middle cerebral artery signal intensity in preoperative single-slab 3-dimensional time-of-flight magnetic resonance angiography. Neurosurgery 64:1065–1072PubMedCrossRefGoogle Scholar
  25. 25.
    Lal BK, Younes M, Cruz G, Kapadia I, Jamil Z, Pappas PJ (2011) Cognitive changes after surgery vs stenting for carotid artery stenosis. J Vasc Surg 54:691–698PubMedCrossRefGoogle Scholar
  26. 26.
    Manninen PH, Tan TK, Sarjeant RM (2001) Somatosensory evoked potential monitoring during carotid endarterectomy in patients with a stroke. Anesth Analg 93:39–44PubMedCrossRefGoogle Scholar
  27. 27.
    Mazul-Sunko B, Hromatko I, Tadinac M, Sekulić A, Ivanec Ž, Gvozudenović A, Tomašević B, Gavranović Z, Maladić-Batinica I, Čima A, Vrkić N, Lovričević I (2010) Subclinical neurocognitive dysfunction after carotid endarterectomy—the impact of shunting. J Neurosurg Anesthesiol 22:195–201PubMedCrossRefGoogle Scholar
  28. 28.
    Mocco J, Wilson DA, Komotar RJ, Zurica J, Mack WJ, Halazun HJ, Hatami R, Sciacca RR, Connolly ES, Heyer EJ (2006) Predictors of neurocognitive decline after carotid endarterectomy. Neurosurgery 58:844–850PubMedCrossRefGoogle Scholar
  29. 29.
    North American Symptomatic Carotid Endarterectomy Trial Collaborators (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445–453CrossRefGoogle Scholar
  30. 30.
    Ogasawara K, Yamadate K, Kobayashi M, Endo H, Fukuda T, Yoshida K, Terasaki K, Inoue T, Ogawa A (2005) Postoperative cerebral hyperperfusion associated with impaired cognitive function in patients undergoing carotid endarterectomy. J Neurosurg 102:38–44PubMedCrossRefGoogle Scholar
  31. 31.
    Ropper AH (1986) Evoked potentials in cerebral ischemia. Stroke 17:3–5PubMedCrossRefGoogle Scholar
  32. 32.
    Rowed DW, Houlden DA, Burkholder LM, Taylor AB (2004) Comparison of monitoring technique for intraoperative cerebral ischemia. Can J Neurol Sci 31:347–356PubMedGoogle Scholar
  33. 33.
    Schnaudigel S, Gröschel K, Pilgram SM, Kastrup A (2008) New brain lesions after carotid stenting versus carotid endarterectomy. A systematic review of the literature. Stroke 39:1911–1919PubMedCrossRefGoogle Scholar
  34. 34.
    Skejelland M, Krohg-SØrensen K, TennØe B, Bakke SJ, Brucher R, Russell D (2009) Cerebral microemboli and brain injury during carotid artery endarterectomy and stenting. Stroke 40:230–234CrossRefGoogle Scholar
  35. 35.
    Smith JL, Evans DH, Fan L, Gaunt ME, London NJM, Bell PRF, Naylor AR (1995) Interpretation of embolic phenomena during carotid endarterectomy. Stroke 26:2281–2284PubMedCrossRefGoogle Scholar
  36. 36.
    Sundt TM Jr, Sharbrough FW, Piepgras DG, Kearns TP, Messick J Jr, O’Fallon WM (1981) Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy: with results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc 56:533–543PubMedGoogle Scholar
  37. 37.
    Sztriha LK, Nemeth D, Sefcsik T, Vecsei L (2009) Carotid stenosis and the cognitive function. J Neurol Sci 283:36–40PubMedCrossRefGoogle Scholar
  38. 38.
    Wasser K, Pilgram-Pastor SM, Schnaudigel S, Stojanovic T, Schmidt H, Knauf J, Gröschel K, Knauth M, Hildebrandt H, Kastrup A (2011) New brain lesions after carotid revascularization are not associated with cognitive performance. J Vasc Surg 53:61–70PubMedCrossRefGoogle Scholar
  39. 39.
    Weigand MA, Laipple A, Plaschke K, Eckstein HH, Martin E, Bardenheuer HJ (1999) Concentration changes of malondialdehyde across the cerebral vascular bed and shedding of l-selectin during carotid endarterectomy. Stroke 30:306–311PubMedCrossRefGoogle Scholar
  40. 40.
    Wolf O, Heider P, Heinz M, Poppert H, Sander D, Greil O, Weiss W, Hanke M, Eckstein H (2004) Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusion-weighted imaging. Stroke:e373–e375Google Scholar
  41. 41.
    Woodworth GF, McGirt MJ, Than KD, Huang J, Perler BA, Tamargo RJ (2007) Selective versus routine intraoperative shunting during carotid endarterectomy: a multivariate outcome analysis. Neurosurgery 61:1170–1177PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Tomohiro Inoue
    • 1
    Email author
  • Kazuo Tsutsumi
    • 2
  • Kazuhiro Ohwaki
    • 3
  • Akira Tamura
    • 1
  • Hideaki Ono
    • 4
  • Isamu Saito
    • 1
  • Nobuhito Saito
    • 4
  1. 1.Department of NeurosurgeryFuji Brain Institute and HospitalFujinomiya-shiJapan
  2. 2.Department of NeurosurgeryShowa General HospitalTokyoJapan
  3. 3.Department of Hygiene and Public HealthTeikyo University School of MedicineTokyoJapan
  4. 4.Department of NeurosurgeryUniversity of TokyoTokyoJapan

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