Indocyanine green fluorescence video angiography – An indispensable tool for avoiding vascular complications during microsurgical clipping of ruptured intracranial aneurysms and improving surgical outcome

A preliminary study

Abstract

Background: 

The surgical complications in aneurysmal microsurgical clipping are attributable primarily to vascular compromise and retraction injury. The vascular complications almost 50% of these. ICG-VA gives us intraoperative real-time high definition functional imaging of the cerebrovascular tree, thereby allowing immediate quality assessment and control of aneurysm obliteration and parent vessel optimisation. Here we report our preliminary data of an ongoing series of patient study.

Objective: 

This study aims at evaluating the role of ICG VA in avoiding vascular complications during microsurgical clipping of ruptured intracranial aneurysms and ascertaining normative data for ICG dye administration.

Materials and Methods: 

The study aimed at determining the utility of microscope incorporated (Leica M530 OHX microscope) ICG VA in ruptured aneurysm surgery. We used ICG-VA in 17 patients of ruptured aneurysm with WFNS grade 1 and 2 as an adjunct to surgery. We studied multiple patient characteristics, intraoperative ICG peak flow and washout time of dye, and changes made in the operative decisions, and outcome of the surgeries.

Results: 

ICG-VA helped in intraoperative decision making for 5 out of 17 patients. In one patient, inadequate clipping with residual neck was confirmed with ICG-VA and the clip was adjusted. In three patient's perforator/additional vessel compromise was found hence needed clip readjustment, whereas in two patients ICG-VA demonstrated residual filling of large neck sac and 2nd clip was applied in tandem.

Conclusion: 

ICG VA is a conclusively simple adjunctive tool for the early detection and prevention of vascular compromise of multiple vessels and perforators during ruptured aneurysm surgery.

INTRODUCTION

The microsurgical intracranial aneurysmal clipping aims at total isolation of the aneurysmal sac from the vascular channel along with the patency of the parent vessel in addition to that of perforating and branching vessels arising from it. Any degree of compromise of patency of these vessels can produce ischaemic infarcts along with resultant deficits adding to morbidity. Any complications following the microsurgical clipping of unruptured aneurysms are very easily identified as a new post-operative deficit that develops in the immediate post-operative period is assumed to be a surgical complication.[^1,2,3] Ischaemia has been complicating microsurgical clipping in almost 21% of cases.[^1,2] Assessing deficits induced due to micro-neurosurgical complications is much harder in microsurgical clipping of ruptured aneurysms due to associated post-subarachnoid haemorrhage (SAH) cerebral oedema, higher chances of aneurysm rupture intraoperatively and vasospasm, which adds to the difficulty of the procedure, thereby increasing the risk of surgical complications. Optimal clip application and preservation of parent vessel flow are of utmost importance in microsurgical clipping.[²] A previous study reports that,[^2,3] approximately 9.5% of patients with World Federation of Neurosurgical Societies (WFNS) Grade 1 or 2 SAH, underwent surgery and faced a surgical complication attributable to vascular insufficiency.[³] There have been radical changes in aneurysm surgery, especially with the use of intraoperative tools aimed at determining the assessment of flow and the effectiveness of clip application. The use of indocyanine green video angiography (ICG-VA) intraoperatively provides us with real-time high-definition functional imaging of the cerebral vascular tree, intraoperative evaluation of clip placement and assessment of parent vessel flow and allowing clip readjustment if needed.

The ease of application, functional high-definition instantaneous imaging, relatively better safety profile and low cost are the strong proponents for the use of ICG-VA to evaluate the clipping adequacy.[^3,4] ICG-VA has been used for quite long now, but there are still only a few studies examining whether it reduces the risk of vascular compromise while microsurgical clipping. We aim to evaluate if the surgical complications related to vascular compromise while clipping of ruptured aneurysms can be reduced by the use of ICG-VA. Here, we report our preliminary data in 17 cases of ruptured aneurysms with WFNS Grade 1 and 2.

SUBJECTS AND METHODS

We, at our centre, have been using ICG-VA since 2019, integrated to the Leica M530 OHX surgical microscope (Leica Microsystems, Wetzlar, Germany). Only patients with WFNS Grade 1 and 2 who presented within 20 days of rupture were included in this study. Patients with WFNS Grades of 3–5, time since bleed of over 20 days and use of other methods (e.g., EC-IC bypass) were not included. A thorough neurological examination followed by a computed tomography (CT) scan confirmed the diagnosis of SAH. The diagnosis of aneurysm and delineation of aneurysm architecture were done using CT angiography of brain and/or digital subtraction angiography brain. All patients underwent microsurgical clipping by the same senior neurosurgeon (S. S. G.). For administration of ICG, 0.5 mg/kg ICG dye was diluted in 10 ml of distilled water with a saline flush pre- and post-clipping. This study also aims at collective normative data for ICG dye after intravenous administration. The following parameters were studied: age, gender, WFNS score on presentation, post-ictal time, the position of aneurysm, size of aneurysm, timing of surgery, peak flow and washout times of ICG intraoperatively, pre- and post-operative Glasgow Coma Score (Glasgow Coma Scale [GCS] was recorded on post-operative day 2 and at the time of discharge) and post-operative imaging findings to correlate with deficits if any. Vascular complication was defines as the onset of a new focal neurological deficit within 24 h postoperatively or if a new infarct appeared on post operative magnetic resonance imaging which corresponds to the surgical territory, not accounting to direct brain trauma, retraction injury, haematoma, vasospasm and hydrocephalus. In the case of inconclusive radiology, a vascular injury would comprise new-onset neurological deficit with no other likely pathology. Intraoperative ICG use has some limitations like its usefulness is limited in atherosclerotic or calcified aneurysm walls.[^5,6,7] In thrombosed, atherosclerotic or calcified aneurysms, the fluorescent effect of ICG can be easily missed by bare eyes of surgeons as ICG-VA is a subjective investigation. Proper time must be allowed for ICG to wash out before reinjecting to avoid false-positive results.[⁵]

RESULTS

We performed ICG-VA before clipping of aneurysm in all 17 patients. The minimum time gap between two consecutive dye administrations was 5 min. No side effects related to the use of ICG dye in any of the patients. ICG-VA was done pre-clipping, and then clipping was performed. After clipping, again, ICG-VA was repeated. Pre- and post-clipping ICG-VA were analysed, and the observations are as follows. The mean age of our study group was 55.05 ± 5.23 years. The mean time of presentation to the hospital since ictus was 14.2 ± 1.65 h, with the majority of the patient being in WFNS Grade 1 followed by Grade 2. The calculated mean size of the aneurysm was seen to be 5.05 ± 1.67 mm with a mean pre-operative GCS of 14.5 ± 0.4 and post-operative GCS of 14.7 ± 0.5 [Table 1]. The patient data and changes made in the operative plan are shown in [Table 2]. ICG-VA was helpful in 29.4% of patients to change the intraoperative decision based on VA images. T-test was conducted on mean peak and wash out times for the different locations of aneurysms, and the results are shown in [Table 3]. The mean peak time was 13 ± 6.89 s for anterior communicating (ACOM), 11.4 ± 1.14 s for middle cerebral artery (MCA) and 13.6 ± 4.35 for internal cerebral artery (ICA) aneurysms, and the mean washout times were 33.6 ± 11.23, 34.4 ± 6.06 and 32.6 ± 8.14 for ACOM, MCA and ICA aneurysms, respectively. T-test was done and values of peak and washout times had aP< 0.05. In one patient, inadequate clipping with the residual neck was confirmed with ICG-VA and the clip was readjusted. In three patients' perforator/additional vessel, the compromise was found and hence needed clip readjustment, whereas in two patients, ICG-VA demonstrated residual filling of large neck sac and 2^nd clip was applied in tandem.

Table 1: Mean values of the patient parameters recorded

Table 2: Patient demographics and observations on indocyanine green video angiography

Table 3: Mean of peak and washout times (s)

DISCUSSION

Of 17 cases, the intraoperative decision was changed in 5 cases [Figure 1 and Figure 2] after ICG-VA analysis. No side effects of ICG use were noted. It was observed that most of the patients had ACOM artery aneurysms, followed by MCA aneurysms and very few with ICA aneurysms [Table 2]. This study points out the effectiveness of intraoperative use of ICG-VA while clipping of ruptured intracranial aneurysms in reducing the risk of vascular injury related to suboptimal clip placement. In our study, only patients with WFNS Grade 1 and 2 aneurysmal SAH were included as it is the category, in which good technique can bring out excellent results in terms of outcome.[^8,9] In ruptured aneurysm surgery, chances of complication are more as compared to unruptured aneurysms as the brain retraction injury is more likely in the presence of post-SAH cerebral oedema, and vascular injury due to ischaemia. Since WFNS Grades 1 and 2 patients exhibit no focal neurological deficits, this enables us to attribute any post-surgical ischaemic complications directly to intraoperative complications. As per a recent Cochrane review for aneurysmal SAH,[^10,11] any deterioration during post-operative day 1 was classified as a surgical complication. The appearance of delayed ischaemic neurological deficit (DIND) is multifactorial. However, sometimes, DIND may develop as a result of compromised flow from a suboptimal placed aneurysmal clip,[^2,5,7,8] thereby emphasising the role of avoiding vascular compromise to improve patient outcomes. This study infers that the institution of routine ICG use was substantial in minimising vascular complications. The use of ICG-VA is nowadays a routine practise in many centres, thus providing an additional tool that acts as a measure of surgical surety regarding the post-operative result.

Figure 1: (a) Intraoperative picture of the right ICA aneurysm before clipping (b) depicting the ICG-VA images of Pcom artery reduced flow (red arrow), (c) posy clip adjustment established flow as visible on ICG-VA image (blue arrow). ICG-VA: Indocyanine green video angiography

Figure 2: Pre (a) and post (b) clipping intraoperative images of anterior circulation aneurysm (c) shows pre-adjustment ICG-VA image showing residual filling of sac, (d) shows complete obliteration of flow to sac post-adjustment of clip). ICG-VA: Indocyanine green video angiography

This study is also aimed at collective normative data for normal peak and washout times of intravenously administered ICG for the Indian population, however, further data are being collected in this ongoing study as the sample size increases.

To summarise, the use of ICG-VA is a relatively simple and cheaper surgical tool for aneurysmal clipping which empowers the surgeon by reducing avoidable technical errors. However, more studies with a larger sample size are needed to prove the statistical significance and consistency of the same. This decline in surgical complications has led to decreased morbidity and mortality in patients undergoing microsurgical clipping and hence should be used where ever possible to improve surgical outcomes.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.