Navigating a grey zone: Neuromonitoring in the management of temporary internal carotid artery occlusion techniques - A case series and literature review

INTRODUCTION

The evaluation of tolerance to permanent vessel occlusion typically involves a temporary balloon occlusion test (BOT) within the angiography suite. Manual compression or occlusion techniques in the operation theater (OT) are alternatives. This ensures collateral blood flow adequacy in the circle of Willis arteries, which prevents the risk of acute ischemic events. The need for such testing arises in various clinical scenarios, including wide-neck giant aneurysms, trauma, and cranial or cervical tumors involving the internal carotid artery (ICA).^[1] However, the conventional test based only on clinical testing carries a stroke risk of 5–40%^[2] and is influenced by anatomical variations and hemodynamic factors. Thus, it is often supplemented with radiographic techniques such as venous phase delay assessment, which are based on the assumption that patients who exhibit symmetry within the venous phase during a BOT have adequate intracranial collateral circulation and will withstand the loss of the parent vessel.^[3] This can be further supplemented with monitoring of cerebral oxygenation, electrophysiological monitors, and bedside cerebral blood flow (CBF) monitoring. As a result, the anesthesiologist’s role in the BOT procedure specifically and other temporary occlusion test procedures more broadly has become increasingly important.

We present a retrospective case series that describes the outcomes of temporary occlusion test procedures and the viability of incorporating different bedside adjuncts to supplement angiographic assessment and/or clinical testing, while also highlighting the lack of standardized cutoffs in literature for interpreting the adequacy of collateral circulation with these monitors.

MATERIALS AND METHODS

A retrospective analysis of the medical records of patients, who underwent temporary vessel occlusion procedures and received additional neurological monitoring between February 2021 and February 2023 was conducted. We found data from nine patients whose findings were fully documented and who received some form of bedside monitoring such as transcranial Doppler (TCD) assessment, regional cerebral oxygen saturation (rSO₂) monitoring with near-infrared spectroscopy (NIRS) or NIRS in combination with processed electroencephalography (EEG). Table 1 displays details of the nine patients with respect to the indication of BOT, adjuncts employed during monitoring, the results of angiographic and clinical testing, and the outcome for each patient. Cases 1 and 2 [Table 1] were performed in the OT using temporary ligation techniques. An exemption from the Institute Ethics Committee was obtained based on the retrospective nature of the data collection.

DISCUSSION

In the first case, temporary clamping along with somatosensory evoked potentials (SSEP) and motor evoked potentials (MEP) monitoring was performed, which remained intact under normotensive conditions. When hypotension was induced, the SSEP signal disappeared [Figure 1], but the MEP signal remained intact. Once blood pressure (BP) normalized, the SSEP signal reappeared. Overall, the patient tolerated the vessel ligation procedure well, and no focal deficits were observed. This case highlights the utility of confirming the integrity of sensory and motor pathways during temporary vessel occlusion testing. There is evidence supporting MEP monitoring, as it exhibits greater sensitivity compared to SSEP in detecting cerebral ischemia.^[4] On the other hand, despite the absence of significant SSEP changes, patients may still experience motor impairments after surgery. Takamura et al. studied 32 patients, with 12.5% BOT-positive results, undergoing surgery with MEP monitoring.^[5] The cutoff value for MEP amplitude indicating BOT positivity was determined to be a reduction of >80% from the baseline (100% sensitivity and 100% specificity), which was significantly higher compared to EEG monitoring (100% sensitivity and 72.0% specificity).^[5] Another study investigating temporary occlusion during aneurysm surgery found that out of 97 patients, in 42 cases (30 with middle cerebral artery [MCA] aneurysms and 12 with ICA aneurysms) SSEP disappeared during the occlusion period. Thirty-nine eventually recovered their baseline SSEP levels after recirculation, and no postoperative complications were observed in them. However, for the remaining three patients, SSEP did not recover even after recirculation, and all three patients experienced post-operative complications.^[6] In our patient, MEP did not disappear, and SSEP returned to baseline after correction of hypotension, thus the decision to go ahead with parent vessel ligation was taken. It is important to remember that the induction of hypotension during BOT can have an impact on cerebral arteriolar tone, either through pharmacological effects or by triggering autoregulatory mechanisms leading to false negative rates of up to 5–15%, highlighting the need for additional confirmatory testing.

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Figure 1:

Findings of case 1 with MEP and SSEP monitoring: Left panel: MEP findings (a) Pre clamp (b) Post clamp (c) After induction of hypotension (d) After normotension. Right Panel: SSEP findings (a) Pre clamp (b) Post clamp (c) After induction of hypotension (d) After normotension. MEP: Motor evoked potentials, SSEP: Somatosensory evoked potential.

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In case 2, after placing the temporary clamp on the common carotid artery, NIRS measurements dropped from 84 to 75 on the side of occlusion. Simultaneously, TCD mean flow velocities decreased from 54 to 48 (12% drop) in the M1 MCA but eventually returned to baseline. The maximum interhemispheric rSO₂ difference reached 8% after 10 min of occlusion. Over 10 min, this hemispheric difference reduced probably signifying compensation from collaterals. Clinically, the patient appeared stable, thus the surgeon proceeded with vessel sacrifice. However, post-procedure, the patient developed contralateral weakness, with a power of 3/5 in both upper and lower limbs at discharge. A computed tomography scan revealed patchy watershed infarcts in the MCA territory on the affected side [Figure 2], likely due to embolic stroke resulting from clamp placement. Thus, techniques focusing on the assessment of global cerebral function rather than a single territory of the ICA may be more useful for the identification of such complications. Sorteberg et al. examined 136 patients using TCD-guided BOT.^[7] They found that a significant drop in MCA velocity during balloon occlusion can serve as an indicator of the patient’s tolerance to ICA sacrifice. Patients with a drop to 65% or more of baseline values are likely to tolerate the procedure, while those with a drop to 54% or less are at higher risk of developing infarction.^[7] However, assessment with TCD-based monitoring may fail to identify ischemia in the watershed zones.

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Figure 2:

Findings of Case 2: (a-c) Day 1 post-clipping non-contrast computed tomography (NCCT) shows right pterional craniotomy with pneumocephalus. Subtle hypodensities (blue arrows) are seen in the right frontal lobe and anterior temporal lobe. (d-f) Day 4 patient developed left upper limb and lower limb weakness and repeat NCCT shows well-developed infarcts (blue arrows) in the right internal watershed zone, posterior limb internal capsule and anterior temporal lobe. (g-i) Concomitant computed tomography perfusion was performed, which revealed markedly decreased cerebral blood flow, increased time to drain, and mean transit time indicative of infarcted tissue (blue arrows).

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Limited studies have investigated cerebral oxygenation monitors in BOT. A study in nasopharyngeal carcinoma patients found that all 11 BOT-positive patients demonstrated a significant drop in rSO₂ on the tested side. Through receiver operating characteristic curve analysis, they determined that a change in rSO₂ (∆rSO₂) of 5% was the most suitable cut-off value for detecting the BOT-positive group.^[8] However, NIRS rSO₂ monitoring was unable to detect false-negative results. One limitation we have observed is that pain may induce elevations in BP and subsequently increase in rSO₂ values, which can confound clinical testing. In another study, simultaneous monitoring of rSO₂ and technetium 99m-hexamethylpropyleneamine oxime single-photon emission computed tomography study was assessed during BOT, which revealed a significant correlation between ∆rSO₂ and stump pressure.^[9]

The hypothesis behind using oxygenation monitors is that in patients with inadequate collateral circulation, rSO₂ is expected to be lower on the ipsilateral side after balloon occlusion, and the presence of hypoxia in patients who fail BOT should be reflected in the interhemispheric difference between rSO₂ values. A concern regarding the use of these monitors is their potential to disrupt image acquisition. However, based on our experience, as demonstrated in Figure 3, the use of NIRS does not interfere with image acquisition.

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Figure 3:

Venous phase assessment of case 9: (a) Angiogram AP view, injected by right ICA shows arterial phase. (b and c) Early and late venous phases, respectively, demonstrate perfect synchronous venous filling of the left hemisphere through Acom. (d) The arterial phase of the injection through right ICA during hypotensive challenge demonstrates excellent cross-filling through Acom. (e and f), Early and late venous phases, respectively, show symmetry of venous filling of left ACA and MCA territories. ICA: Internal carotid artery, Acom: Anterior communicating artery, ACA: Anterior cerebral artery, MCA: Middle cerebral artery.

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In our series, eight patients (cases 2–9) undergoing temporary vessel occlusion exhibited varied degrees of reduction (3–10%) in ipsilateral rSO₂ values under normotensive conditions. In cases 7 and 8, a drop of up to 12–15% was observed post hypotension. However, none of these changes in rSO₂ values were associated with a false positive or a false-negative BOT result. Therefore, it is crucial to establish a cut-off value for ∆rSO₂ in patients undergoing BOT and correlate these values with angiographic evidence of positive or negative BOT.

The EEG changes have been shown to correspond to CBF changes in carotid endarterectomy (CEA). During CEA, a reduction in bispectral index (BIS) has been observed when cerebral ischemia occurs due to ICA cross-clamping. Thus, the use of bilateral BIS can aid in detecting a difference between hemispheres with BOT. Harclerode et al. reported a reduction in ipsilateral BIS with each balloon inflation during balloon-assisted cerebral aneurysm coiling in a case report.^[10] To date, no large studies have evaluated the utility of processed EEG monitors during BOT.

The complications that can occur during temporary vessel occlusion testing also need to be considered. Excessive manipulation during the procedure can lead to intraoperative thrombus generation or vessel dissection. Thus, it is important to prevent hypotension to maintain optimal systemic circulation during occlusion. However, hypotensive challenge is an integral aspect of clinical testing during BOT. Neuromonitoring can serve a dual role: Assessing collateral integrity and identifying complications early to facilitate prompt treatment.

While our case series provides insights into the utility of neuromonitoring during temporary vessel occlusion testing, limitations should be considered. The retrospective nature of the data collection introduces inherent biases and limitations, such as the completeness and correctness of data. Each modality has its own limitations and strengths, and a multimodal approach may yield more comprehensive information.

CONCLUSION

Our series has emphasized the varied findings in BOT studies, merging them with our experiences. As technology advances and clinical practices evolve, integrating neuromonitoring into routine procedures can enhance patient safety, but without well-defined cutoff values for interpretation, the use of individual neuromonitoring devices in BOT can potentially generate confusion among clinicians. This highlights the need for continued research and standardization of neuromonitoring protocols to enhance the accuracy of these techniques during temporary vessel occlusion testing.