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ORIGINAL ARTICLE
Year : 2022 | Volume
: 55
| Issue : 6 | Page : 207-214
Intraoperative blood flow monitor for aneurysm clipping: A comparison between Flowmetry and Indocyanine Green videoangiography
Li Chun David Chen1, Shiu-Jau Chen2
1 Department of Neurosurgery, MacKay Memorial Hospital, Taipei, Taiwan
2 Department of Neurosurgery, MacKay Memorial Hospital, Taipei; Department of Medicine, MacKay Medical College, New Taipei, Taiwan
Correspondence Address:
Shiu-Jau Chen
Department of Medicine, MacKay Medicine College, New Taipei, Taiwan; Department of Neurosurgery, MacKay Memorial Hospital, Taipei
Taiwan
Source of Support: None, Conflict of Interest: None
DOI: 10.4103/fjs.fjs_237_21
Background: Both indocyanine green videoangiography (ICG-VA) and flowmetry were considered beneficial in preventing parent artery compromise during aneurysm surgery. However, the appropriate strategy that should be used remains controversial. The objective of the study is to assess the outcomes of aneurysm clipping through flowmetry or ICG-VA monitoring.
Materials and Methods: This retrospective cohort study included 75 patients who underwent aneurysm clipping with vascular patency monitoring. In total, 42 patients underwent flowmetry monitoring and 33 ICG-VA monitoring. Preoperative disease severity and functional outcomes were assessed using the World Federation of Neurosurgical Societies (WFNS) grading system and the modified Rankin scale, respectively.
Results: As compared with ICG-VA, flowmetry group had nonsignificant higher incidence of clip modification (31.7% vs. 18.2%, P = 0.29) and residual neck (22% vs. 10%, P = 0.218). Besides Fisher grade, flowmetry monitoring (Crude odds ratio [OR] = 0124, P = 0.015), young age, and anterior communicating artery location were the independent risk factors for vasospasm based on multivariate analysis. The incidence of parent artery compromise did not differ between both groups. Old age, poor preoperative WFNS grade, low Glasgow coma scale (GCS) score, left-side location, and long hospital stay were associated with poor functional outcomes in the univariate analysis. However, only the GCS score was considered a prognostic factor in the multivariate analysis (Adjusted OR = 0.03, P = 0.034).
Conclusion: Both monitoring methods have similar functional outcomes. Although not influencing outcome, the flowmetry group has a higher incidence of angiographic vasospasm than the ICG-VA group. The vessel preparation for flowmetry monitoring is more complicated than that for ICG-VA; thus, we recommend ICG-VA for routine monitoring. Flowmetry may be applicable in distal aneurysms when hemodynamic insufficiency in a parent artery is suspected.
Keywords: Cerebral aneurysm, angiography, clipping, flowmetry, indocyanine green videoangiography, residual aneurysm, subarachnoid hemorrhage, vasospasm, World Federation of Neurosurgical Societies grade, fluorescence image
Subarachnoid hemorrhage due to aneurysm rupture accounts for about 10% of all stroke cases in Taiwan.[1] Although patients received proper treatment, the mortality rate still ranges from 20% to 30% during a 1-year follow-up.[2] Approximately 20% of survivors may present with moderate or severe disability for 10 years.[3] Nowadays, both endovascular treatment and surgical clipping are used for the treatment of the intracerebral aneurysm. However, there is still a debate regarding which treatment modality is better.[4] Although the probability of disability-free survival was significantly higher in the endovascular group than in the neurosurgical group from 1 to 10 years, surgery is still beneficial in some cases, including lower retreatment rates.[5] Endovascular treatment is associated with a low mortality rate, short hospital stay, and low treatment costs.[2],[3],[6] However, the procedure still has considerable complications. Recanalization, intraoperative rupture, infarction due to coil migration, and parent artery stenosis might occur and worsen patient outcomes.[7] Therefore, conventional craniotomy with clipping is still a good treatment option, particularly for young patients and aneurysms with wide-based neck, distal location, and mass effect.
The complications of surgical clipping included premature rupture of aneurysm, re-bleeding of aneurysm with residual neck, and ischemia due to parent artery occlusion. Intraoperative flowmetry and indocyanine green videoangiography (ICG-VA) monitoring techniques were found to be beneficial in preventing parent artery compromise.[8],[9],[10] Thus, the present study aimed to present the use of these blood flow monitoring techniques in aneurysm clipping. Moreover, the surgical outcomes of flowmetry and ICG-VA were assessed.
MethodsPatient selection
This retrospective cohort study included patients with intracranial aneurysms who underwent craniotomy and aneurysm clipping with flow monitoring from January 2009 to January 2019. Patients with fusiform, blister, distal terminal artery aneurysms, and aneurysms associated with arteriovenous malformation were excluded from the study. Thus, a total of 75 patients who underwent surgery were enrolled. The study protocol was reviewed and approved by the institutional review board (IRB approval number: 19MMHIS185e). Forty-three patients underwent surgery from January 2009 to May 2013 when TransonicR flowmetry was the only flow monitoring method available. From May 2013 to 2019, ICG-VA was available in our hospital and became the primary monitoring modality. Thirty-two patients underwent surgery during this period, and four of them a combined flowmetry monitoring. Medical chart review was conducted, and data about the number of times clip replacement was performed were recorded. In three patients, the aneurysm did not rupture. In cases of multiple aneurysms, the ruptured ones were taken into image assessment. Of the 75 patients, 71 underwent postoperative cerebral angiography approximately 1 week after clipping and at least one cerebral computer tomography[11] scan after surgery.
Operation technique
During the operation, the aneurysm sac and the parent artery were detected. The target arteries were identified and dissected more distally through flowmetry monitoring compared with ICG-VA monitoring to appropriately cover the vessel with the probe [[Figure 1]a, [Figure 1]b, [Figure 1]c [Figure 1]d and Video 1]
Figure 1: (a-d) A-com aneurysm clipping using flowmetry monitoring. The ICA, A1, and A2 flow was assessed with a probe before and after clipping. (e-h) P-com and ICA double aneurysm clipping using ICG-VA monitoring. Dye retention was not observed in the aneurysm sac after clipping. ICA: Internal carotid artery, ICG-VA: Indocyanine green videoangiographyOutcome assessment
Complications identified on radiographic images included parent artery stenosis, residual aneurysm, vasospasm, encephalomalacia, and hydrocephalus. The presence of complications was based on the radiologists' reports of cerebral angiography or computed tomography (CT) scan findings. Kotowski et al. classified residual aneurysm into a four-category scale,[12] which was as follows: grade 0, complete aneurysm occlusion; Grade 1, residual neck (<2 mm, <50%); Grade 2, residual remnant (>2 mm, <50%); and Grade 3, residual aneurysm (>50%). Grade 2 and 3 residual aneurysms were considered statistically significant, and Grade 3 residual aneurysm requires further treatment. Vasospasm was defined as the presence of vessel stenosis on follow-up cerebral angiography. For postoperative images, seven patients received internal carotid artery angiography on both sides. Twelve patients had examinations only on the aneurysm side. Hydrocephalus was managed using ventriculoperitoneal shunt under the patient's consent.
In relation to patient outcome, the patient's condition was assessed before operation using the World Federation of Neurosurgical Societies (WFNS) grading system. Preoperative WFNS grades of 1–2 were classified as good and the other grades as poor.[13] The patients' functional outcome at 6 months was evaluated using the modified Rankin scale.[14],[15] Scaling grades of 0–2 were considered favorable outcomes and grades of 3–6 as unfavorable outcomes.
Statistical analysis
The clinical characteristics of the patients who underwent the two monitoring modalities were assessed using Student's t-test for continuous variables and Fisher's exact or Chi-square test for categorical variables. To investigate the possible predictive factors of functional outcome, we introduced significant variables in the previous univariate analyzes into the multivariable logistic regression model with a stepwise selection. A value of P < 0.05 was considered statistically significant. Data analyses were conducted using the Statistical Package for the Social Sciences software version 22 (IBM SPSS, IBM Corp., Armonk, NY, USA).
ResultsDemography
The mean age of the participants is 56.8 years, with a peak at 51–60 years. The demographic characteristics of the two groups are shown in [Table 1]. Clip readjustment is performed in 19 (25.3%) cases.
Table 1: Baseline characteristics of the patients monitored via flowmetry or indocyanine green videoangiographyComplications
The complications in the two groups are depicted in [Table 2]. Five patients presented with parent artery compromise, two with P-com aneurysm, two with A-com aneurysm, and one with middle cerebral artery (MCA) aneurysm. The radiologists' reports included 24 residual aneurysms. Twelve aneurysms were classified as Grade 1, and the other 12 were considered as residual aneurysms [Grade 2 in eight, [Figure 2]]. Four patients with Grade 3 residual aneurysms underwent further transarterial coil embolization. Angiographic vasospasm was noted in 19 cases, and five patients had clinical symptoms that required triple-H therapy. Eight of them had diffuse vasospasm involving all major vessels. The others occurred mostly around the parent artery of the aneurysm. Thirty-four patients had hydrocephalus, and 56 patients had any degree of encephalomalacia on follow-up CT scan. The outcomes of the two groups did not differ significantly, except for the presence of angiographic vasospasm.
Figure 2: Postoperative cerebral angiography showing residual neck (Grade 1, neck <2 mm, a-d), remnant (Grade 2, neck more than 2 mm but <50% sac remained, e-h)Functional outcome
Old age, poor preoperative WFNS grade, low Glasgow coma scale (GCS) score, left-side location, and long hospital stay were associated with poor functional outcomes in the univariate analysis [Table 3]. However, only the GCS score was considered a prognostic factor in the multivariate analysis [Table 4]. Both flow monitoring methods did not influence the incidence of the residual aneurysm [Supplement Table 1]. Young age, A-com location, and flowmetry monitoring were independent risk factors for vasospasm based on the multivariate analysis [Table 5] and [Table 6]. We also found a positive correlation between the Fisher grading scale and the incidence of vasospasm (3.16 in vasospasm group vs. 2.52 in no vasospasm group with a P = 0.02 from t-test).
Table 3: Predictive factors for functional outcomes in the univariate logistic binary regression analysis
Table 4: Predictive factors for functional outcomes in the multivariate logistic binary regression analysis
Table 6: Independent risk factors for vasospasm in the multivariate analysis
Flow monitor and parent artery compromise
The common complications during aneurysm clipping include premature rupture of aneurysm, parent artery compromise, incomplete clipping, and residual neck. ICG-VA is a method that can easily confirm complete clipping if dye is not retained in the aneurysm sac.[16],[17],[18] In the same way, parent artery obstruction can be ruled out. However, the sufficiency of blood flow cannot be validated. In addition, ICG-VA can only be used with certain advanced operative microscopes. On contrary, intraoperative flowmetry can directly measure blood flow in the parent artery, thereby confirming adequate perfusion. In this study, radiologists have reported five patients to have compromised parent arteries. Four of them were under flowmetry monitoring. Two were P-com artery which was not our measurement target. Reasons for unexpected parent artery stenosis may be: first, angiographic vessel diameter narrowing does not always consistently correlate with physiological flow decrease. Second, vasospasm may interfere with the diagnosis of vessel compromise if it occurs near the aneurysm.
Clip modification under flow monitoring
In a recent systemic review, the mis-clipping rate that eluded microscopic visual observation and identified at ICG-VA is 6.1%, whereas mis-clippings that eluded ICG-VA and identified at DSA is 4.5%.[19] Other than ICG-VA, the use of other intraoperative methods, such as electrophysiological monitoring and flowmetry, are recommended to ensure the safety of aneurysm clipping. During flowmetry monitoring, blood flow in the index artery is sometimes difficult to identify before clipping, the recommended reference data for each artery can be used to confirm whether blood flow is adequate. If the flow is <25% of the preclipping (or reference) data, repositioning of the clip is recommended.[9] In our series, 19 (26%) patients underwent clip readjustment due to suspected hemodynamic insufficiency in the parent artery or incomplete clipping. Of the 19 patients, seven presented with MCA aneurysms, 10 with A-com aneurysms, and 2 with P-com aneurysms. Patients with aneurysms in the A-com artery and MCA were at higher risk of parent vessel compromise requiring clip readjustment than other patients in our series (odds ratio [OR]: 9.12, P < 0.01). The flowmetry group had a higher incidence of clip readjustment rate than the ICG-VA group (13/42 [31.7%] vs. 6/33 [18.2%], P = 0.29). However, the result was not significantly different between the two groups. In previous studies, Amin-Hanjani et al. reported a clip replacement rate of 25.5% in flowmetry monitoring, and Roessler et al. revealed a clip modification rate of 15% with the use of ICG-VA.[9],[20] A study that used multimodal intraoperative monitors has reported a clip reposition rate of 40.6%, which is attributed to motor evoked potential decrease in 9.3%, flowmetry in 22.91%, and ICG-VA in 8.3% of patients.[21] The result was similar to ours showing that flow alterations occurred more frequently in distal than in proximal aneurysms.
Incidence of residual neck
Hallout reported that residual aneurysms (Raymond–Roy Grade 3) occurred in 4.5% of patients with MCA aneurysm who underwent clipping without ICG-VA assistance.[22] In our study, the incidence rate of Grade 3 residual aneurysm was 5.6% (4/71). In a previous study, the residual neck remnant missed rate in ICG-VA monitoring was 10%, which was similar to our ICG-VA group.[20] Sindou et al. classified incomplete clipping into five grades. In their study, the incidence rate of incomplete clipping was 6.9%. Among their patients, 4% presented with the residual neck (Grades 1, 2) and 1.9% (Grades 3–5) with true incomplete clipping with residual sac.[23] In our series, we had a higher incidence of residuals than in literature reports. The radiologists reported that 12 (16%) patients had a significant residual neck. Eight patients presented with residual remnants (Grade 2) and four with residual aneurysms (Grade 3) that require further coil embolization. However, most Grade 2 residual remnants were discovered and expected during the operation. For distally located aneurysms, including the MCA territory, relatively fewer collaterals were observed, and parent artery compromise might cause catastrophic infarction. If such a phenomenon occurred, the adequate flow must be achieved first if the wall of the aneurysm remnant looked healthy. This phenomenon can explain the high incidence of the postoperative residual neck in our study compared with the other studies.[24] The higher incidence of the residual neck was partially attributed to the usage of 3D reconstruction angiography, which has a higher sensitivity than 2D conventional angiography. Goertz reported that 3D angiography facilitated the precise detection of aneurysms and vasculature and reduced the rate of periprocedural ischemia.[25] In our series, the residual neck was not a predictive factor of poor outcome [Table 4]. The blood flow monitoring method did not influence the incidence of residual aneurysm [Supplement Table 1]. No clinical evidence of re-bleeding was observed from the residual neck during the follow-up period in our series.
Prognostic factors for functional outcome and vasospasm
The poor prognostic factors of ruptured cerebral aneurysms include old age, WFNS grade V, high modified Fisher grade, wider neck aneurysm, postoperative pneumonia, low initial Hunt and Hess grade, hypertension, acute infarction on CT scan, and hydrocephalus.[26],[27] In this study, old age, poor preoperative WFNS grade, low GCS score, left-side location, and long hospital stay were associated with poor functional outcomes in the univariate analysis [Table 3]. However, only the GCS score was a prognostic factor in the multivariate analysis [Table 4]. In the study of Aggarwal and Sodhi et al., the patient's initial SAH grade (both Hunt and Hess and WFNS grades) was correlated to outcomes.[13],[26] Young age, A-com location, and flowmetry monitoring were independent risk factors for vasospasm in our series based on the multivariate analysis [Table 5] and [Table 6]. Kale et al. reported that patients aged <50 years were at a 5-fold increased risk of vasospasm compared with older patients.[28] The proposed mechanism was that the capacious subarachnoid space in older patients facilitated an easier washout of accumulated blood clots with cerebrospinal fluid than in younger patients.[29] However, the influence of age on vasospasm was still controversial based on a systemic review.[29] The possibility of vessel manipulation as an explanation for the higher incidence of angiographic vasospasm in the flowmetry group than in the ICG-VA group was still under debate. Operative time and use of temporary occlusion during surgery and coiling did not influence the incidence of vasospasm in other reports.[29]
Intraoperative cerebral angiography as an alternative
Intraoperative cerebral angiography is a good method for detecting incomplete clipping, residual neck, and parent artery stenosis. Ares et al. conducted a critical analysis of the usage of intraoperative cerebral angiography during aneurysm clipping. They have reported that intraoperative cerebral angiography has influenced the management of about one-fifth of the cases. The method is particularly beneficial in detecting residuals for A-com aneurysms rather than MCA aneurysms.[30] Moreover, it exhibits all the advantages of intraoperative sonography (flowmetry) and intraoperative ICG retention test and is considered a gold standard.[31] However, it can only be performed in a hybrid operating room. The team members must standby during the operation to perform postoperative cerebral angiography. In terms of the cost of the personnel and hybrid operation room, it is more expensive than ICG-VA and flowmetry. The selective or routine usage of the procedure during aneurysm clipping remains controversial.[32]
Limitations
Retrospective design and small sample size were the limitations of our study. The angiography results such as vasospasm, residual neck, and vasospasm were based on different radiologists' opinions without consensus. We did not have long-term angiography follow-up data to show the destination of the residual neck or sac.
ConclusionSimilar to previous reports, our study showed that patients with a high preoperative GCS score who underwent aneurysm clipping had better long-term outcomes. With the advancement in flowmetry and ICG-VA, we could prevent parent artery compromise. No significant difference was observed in terms of functional outcomes between the two monitoring methods. Flowmetry monitoring required more parent artery dissection, exposure, and manipulation to properly place the probe, which may increase the risk of premature rupture. Thus, we recommend ICG-VA for routine monitoring. However, flowmetry can be used in selective distal aneurysms when parental artery compromise cannot be prevented with ICG-VA.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
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