A Comparative Analysis between Intraoperative Fluorescein Sodium Videoangiography and Postoperative Imaging for Evaluating Clipped Intracranial Aneurysms

Abstract

Introduction

The evaluation of clipped intracranial aneurysms postoperatively is crucial for successful surgical treatment and minimizing risks such as residual aneurysms and complications. Fluorescein sodium videoangiography (FL-VA) has been introduced to aid in this assessment, but comparative studies with postoperative imaging remain limited.

Materials and Methods

A prospective observational study was conducted on 57 patients with 64 intracranial aneurysms who underwent surgery between December 2021 and September 2022. FL-VA was performed, followed by postoperative computed tomography angiography (CTA). Discordance between FL-VA and CTA findings was analyzed statistically.

Results

FL-VA showed complete occlusion in 57 out of 61 aneurysms (93.4%), with 10 cases of discordance identified in postoperative CTA. One patient showed a neck remnant in FL-VA, but CTA revealed a residual aneurysm. Another patient displayed neck remnant and stenosis in branching vessels on CTA, not identified by FL-VA. Additionally, five aneurysms had neck remnants, and three had stenosis in branching vessels, detected in CTA but missed in FL-VA. Statistical analysis did not reveal significant associations between discordance and studied factors.

Conclusion

FL-VA shows potential as an effective intraoperative assessment tool for clipped intracranial aneurysms, although further research is needed to establish its definitive efficacy and reliability compared with other modalities.

Keywords

sodium fluorescein - intracranial aneurysms - microsurgery

Introduction

Since the significant findings by McKissock et al highlighting the benefits of surgical intervention for ruptured intracranial aneurysms, substantial efforts have been directed toward maximizing the safety and efficacy of surgical aneurysm obliteration.[1] These efforts have shown that complete aneurysm obliteration of the aneurysm while maintaining blood flow through parent and branch vessels is the hallmark of successful surgical therapy.

According to the available literature, the frequency of aneurysm remnants and adjacent vessel compromise in postoperative angiography ranges between 1.8 and 3.6% and 1.6 and 21%, respectively.[2] Importantly, inadequate aneurysm occlusion as well as inadvertent arterial sacrifice increases the risk of (re)bleeding and cerebral ischemia. The current rates of the latter vary from 4 to 18% and 3 to 14%, respectively.[3] [4] Therefore, intraoperative assessment of clipped intracranial aneurysms is of utmost importance in neurovascular surgery.

To minimize the risk of these unintended consequences, many advocate for employing various intraoperative techniques to visualize blood flow in the vessels and confirm aneurysm occlusion. These include Doppler ultrasonography, intraoperative cerebral angiography (DSA [digital subtraction angiography]), and fluorescence technologies.[5]

The integration of fluorescence technologies in neurovascular surgery began following the initial description of indocyanine green (ICG) video angiography in 2003.[6] It quickly became an established practice as data regarding the use of ICG substantially grew, and ICG video angiography (ICG-VA) proved to be highly effective in preventing postoperative complications.[7] [8] So far, however, only the literature regarding the use of ICG is available leaving the application of much more cost-effective fluorescein to be evaluated.

Comparing the findings of intraoperative fluorescein sodium videoangiography (FL-VA) and postoperative computed tomography angiography (CTA), this study aims to assess whether FL-VA is a suitable modality for intraoperative evaluation of aneurysmal obliteration adequacy and the patency of parent and adjacent vessels.

Materials and Methods

This observational prospective study analyzed consecutive patients who underwent surgery for either ruptured or unruptured aneurysms at the Department of Neurosurgery, Santa Casa BH, Belo Horizonte, Minas Gerais, from December 2021 to September 2022. It was reported following the Preferred Reporting of Case Series in Surgery (PROCESS) guidelines.

Approval for this study was obtained from the Institutional Medical Ethics Committee (CAE 4540520503854). Patients' informed consents were obtained for participation in this study.

Population

Between December 2021 and September 2022, a total of 57 patients (64 aneurysms) underwent craniotomy procedures for intracranial aneurysm clipping ([Tables 1] and [2]). Fifty-four patients underwent FL-VA and postoperative CTA. Three patients did not undergo postoperative CTA due to poor clinical conditions.

Table 1 Demographic and clinical data of the 57 patients

Data	n (%)
Age (years)
≤60	34 (23.4%)
> 60	23 (35.9%)
Sex
Male	12 (29.7%)
Female	45 (70.3%)
Ruptured aneurysm
No	24 (42.1%)
Yes	33 (57.9%)
Multiple aneurysm
No	42 (65.6%)
Yes	15 (34.4%)
Hunt–Hess grade (ruptured aneurysm)
Hunt–Hess > 2	12
Hunt–Hess ≤ 2	21

Table 2 Characteristics of the 64 aneurysms (57 patients)

Data	n (%)
Intraoperative rupture
No	48 (75%)
Yes	16 (25%)
Neck size (mm)
< 4 mm	38 (59.4%)
≥4 mm	26 (40.6%)
Aneurysm size (mm)
≤12	60 (93.7%)
> 12	04. (6.3%)
Dome-to-neck ratio
< 2	34 (53.1%)
≥2	30 (46.9%)
Aneurysm calcification
No	56 (87.5%)
Yes	08 (12.5%)
Thrombosed aneurysm
No	59 (92.2%)
Yes	05 (7.8%)
Location
Posterior circulation	02 (3.1%)
Vertebral artery	01 (1.55%)
Basilar artery	01 (1.55%)
Anterior circulation	62 (96,9%)
Anterior communicating artery (ACoA)	17 (26.6%)
Pericallosal	02 (3.1%)
Middle cerebral artery (MCA)	24 (37.5%)
Internal carotid artery (ICA)	19 (29.7%)

The following descriptive data were collected: patient age and sex; number of clipped aneurysms; aneurysm location, size, neck size, dome-to-neck ratio, rupture status; Hunt–Hess grade (if ruptured); intraoperative rupture; aneurysm calcification and thrombosed aneurysm.

Intraoperative Fluorescence Module

This study used an OPMI PENTERO 800 neurosurgical operating microscope with a YELLOW 560 integrated fluorescence filter module for imaging fluorescein fluorescence (Carl Zeiss Meditec AG). The YELLOW 560 module utilizes intravascular sodium fluorescein to delineate the fluorescence signal and visualize nonfluorescent tissue against a relatively subdued background (depending on the depth of the operative field). This setting often allows for safe and feasible manipulation of vessels. This module is set up for excitation in the range of 460 to 500 nm and an emission range between 540 and 690 nm, which matches those of sodium fluorescein. For generating a white light impression of nonfluorescent tissue, an optical mixing of light using specifically defined amounts of blue and red light are created. This technology allows improved observation of tissue details and often optimizes intraoperative vascular manipulation under the fluorescence mode using the operator's microscope oculars.

Sodium Fluorescein

Sodium fluorescein is a yellow-red, synthetic salt dye that is most commonly used to evaluate flow patterns of sub-terranean waters, as a cosmetic and pharmacologic color, and as a labeling agent in protein research. It has a molecular weight of 376.7 kDa.

Sodium Fluorescein Videoangiography

After aneurysm clipping, we administered a 0.5 mg/kg bolus intravenous dose of sodium fluorescein (Citopharma, Belo Horizonte, Minas Gerais, Brazil) through a peripheral intravenous line, and the intracranial area of interest was inspected through the microscope-integrated YELLOW 560 module. Approximately 30 seconds later, cerebral arterial, capillary, and venous phases were observed fluorescing through the oculars in yellow-green colors. Based on our experience, this dosage represents the minimum amount necessary to sustain a sufficient fluorescence signal detectable within the arteries when utilizing the YELLOW 560 module.

The following FL-VA data were collected: whether a presence of residual aneurysm, visibility of any neck remnants, the presence of occlusion or stenosis in parent or branching vessels, and the complete occlusion of the aneurysm.

Postoperative Computed Tomography Angiography

Postoperative CTA was performed in 54 of the 57 patients with 61 aneurysms. All CTA studies were performed on a 128-channel multidetector row CT system (SOMATOM go.Top, Siemens Healthineers, United States), with patients' heads fixed in a neutral position during the examination to prevent motion artifacts. For imaging, we utilized the following parameters: 100 kVp, 320 mAs, 64 × 0.625 mm detector collimation, 0.6 second gantry rotation time, a pitch of 0.984, section thickness of 0.625 mm, 220 mm field of view, and 512 × 512 matrix. The CTA protocol was performed before and after a bolus of 70 mL of nonionic contrast medium (Iohexol: 350 mg iodine/mL; Citopharma, Belo Horizonte, Minas Gerais, Brazil) was injected into the antecubital vein with an automated power injector at a flow rate of 4 mL/s, followed by 40 mL of saline chaser. A bolus tracking method was used routinely to achieve optimal synchronization of contrast medium flow and scanning.

A three-dimensional (3D) workstation (RadiAnt DICOM Viewer 2021.2, Medixant, Poland) was used to reconstruct 3D datasets. The neuroradiologist analyzing the postoperative CTA was unaware of findings on the intraoperative FL-VA.

CTA was employed for postoperative evaluation as part of the routine practice in our service, primarily due to the unavailability of DSA in the public health care system where this study was conducted. Although DSA is considered the gold standard, CTA was used for its noninvasive nature and its high sensitivity and specificity for detecting residual aneurysms and parent vessel occlusions, as demonstrated by Bharatha et al.[9]

Following image acquisition, the attending neuroradiologist interpreted the findings. The following CTA data were collected: whether a presence of residual aneurysm, visibility of any neck remnants, the presence of occlusion or stenosis in parent or branching vessels, and the complete occlusion of the aneurysm. These findings were compared with the surgeon's findings after the FL-VA.

Comparison of FL-VA with Postoperative Computed Tomography Angiography

Statistical Analysis

The acquired data were entered into a computer database. A univariate model was created using the statistical software package SPSS (version 9.1, SAS Institute, Inc.) to determine which factors predict an FL-VA–postoperative CTA discordance.

The dependent variable for this model was FL-VA–CTA discordance, which was defined by the surgeon's intraoperative findings differing from the radiologist's postoperative CTA findings.

Independent variables were patient age and sex; location of the aneurysm, size, and rupture status, neck size, dome-to-neck ratio, aneurysm size, intraoperative rupture, aneurysm calcification, and thrombosed aneurysm. Statistical significance was defined as p <0.05.

Results

Clinical Outcome

The characteristics of the patients and aneurysms studied are listed in [Tables 1] and [2]. Of the 57 patients submitted to microsurgery, 40 (70.2%) showed good outcomes, modified Rankin Scale ≤ 2 (mRS ≤ 2). Four patients died (mortality rate: 7.0%). In the 3-month follow-up, 52 patients were evaluated, of whom 40 (76.9%) showed good outcomes (mRS ≤ 2).

Twenty-four patients had unruptured aneurysms. Among them, there were three ischemic complications, with one patient who died (mortality rate: 4.1%), one patient who recovered from motor deficits within 3 months of follow-up, and one patient who did not show recovery. Therefore, after 3 months of follow-up, 91.6% of the patients showed good outcomes (mRS ≤ 2).

Thirty-three patients had ruptured aneurysms, of these 12 patients were admitted with a Hunt–Hess grade >2. Twenty-two patients (66.6%) showed good outcomes. Three patients died (mortality rate: 9%).

Comparison of Intraoperative FL-VA with Postoperative CTA

FL-VA revealed complete occlusion in 93.4% of the studied aneurysms (57 out of 61), with four aneurysms showing neck remnants. No instances of vessel stenosis or residual aneurysm components were observed in any of the cases.

Postoperative CTA was conducted in 54 patients (61 aneurysms). The results of the CTA revealed complete occlusion in 51 out of the 61 aneurysms, accounting for 83.6% of the cases.

Ten cases of discordance between FL-VA and CTA were identified: one patient was indicated as a neck remnant in FL-VA, but CTA revealed a residual aneurysm. One patient's CTA showed neck remnant and stenosis in branching vessels, that it was not identified by FL-VA. Five aneurysms had neck remnants (Case 2), and three cases had stenosis in branching vessels (Case 1), which were not observed in FL-VA but were detected in CTA. Consequently, unexpected findings were discovered in 16.4% of the aneurysms in postoperative CTA.

In the three cases where CTA revealed stenosis in branching vessels, blood flow was adequate, and no ischemic complications were identified in these patients. Patients with neck remnants were managed conservatively with imaging follow-up. In the patient with an aneurysm remnant, it was a nonruptured calcified aneurysm, and the remnant measured 6 mm. The decision was also made to follow up with imaging. The data presented in the flow diagram are illustrated in [Fig. 1].

Fig. 1 Flow diagram of FL-VA and CTA findings in aneurysm study. CTA, computed tomography angiography; FL-VA, fluorescein sodium videoangiography.

Discordance versus Nondiscordance Group

Characteristics of the FL-VA–postoperative CTA discordance group compared with the nondiscordance group are presented in [Table 3]. In the univariate analysis, none of the predetermined variables listed in [Table 3] showed statistical significance.

Table 3 Comparison of FL-VA–CT angiography discordance to nondiscordance[a]

	Data analysis
	Nondiscordance		Discordance		p-Value[a]
	n	%	n	%
Sex
Female	34	82.9	7	17.1	1.00
Male	13	81.3	3	18.8
Age (y)
≤60	34	87.2	5	12.8	0.47
> 60	17	77.3	5	22.7
Ruptured aneurysm
No	21	80.8	5	19.2	0.73
Yes	30	85.7	5	14.3
Intraoperative rupture
No	39	83.0	8	17.0	1.00
Yes	12	85.7	2	14.3
Location
ICA	15	83.3	3	16.7	–
MCA	18	78.3	5	21.7
ACoA	16	94.1	1	5.9
Pericallosal	1	100.0	0	0.0
Posterior circulation	1	50.0	1	50.0
Neck size (mm)
< 4	20	80.0	5	20.0	0.73
≥4	31	86.1	5	19.3
Aneurysm size (mm)
> 12	3	75.0	1	25.0	0.52
≤12	48	84.2	9	15.8
Dome-to-neck ratio
< 2	27	81.8	6	18.2	0.74
≥2	24	85.7	4	14.3
Aneurysm calcification
No	43	81.1	10	18.9	0.33
Yes	8	100	0	0.0
Thrombosed aneurysm
No	49	84.5	9	15.5	0.42
Yes	2	66.7	1	33.3

Abbreviations: ACoA, anterior communicating artery; ICA, internal carotid artery; MCA, middle cerebral artery.

^a Fisher's exact test.

Illustrative Cases

Case 1

A 59-year-old patient with a ruptured aneurysm. CTA revealed the presence of basilar tip aneurysm. FL-VA revealed complete occlusion of the aneurysm, and flow in the larger and millimetric branches adjacent to the aneurysm. Postoperative CTA showed stenosis of the contralateral posterior cerebral artery ([Fig. 2]).

Fig. 2 Visualization with white light. (A) Exposure of the basilar tip aneurysm (white arrow). (B) Clipping of the aneurysm with 01 clip (white arrow). Visualization with yellow 560. (C) FL-VA showing complete aneurysm occlusion with flow in both the posterior cerebral artery (white arrow) and perforating arteries (yellow arrow). (D) Postoperative CT angiography revealed stenosis of the contralateral posterior cerebral artery (white arrow) with preserved blood flow. CT, computed tomography; FL-VA, fluorescein sodium videoangiography.

Case 2

A 66-year-old patient with an unruptured aneurysm. CTA revealed an aneurysm in the left middle cerebral artery (ACM). After the placement of the clip, the videoangiography suggested complete occlusion of the aneurysm. Postoperative CTA showed small neck remnant ([Fig. 3]).

Fig. 3 Visualization with white light. (A) Clipping of the aneurysm with 01 clip. Visualization with yellow 560. (B) FL-VA showing complete aneurysm occlusion (white arrow). (C) Postoperative CT angiography showed small neck remnant (white arrow). CT, computed tomography; FL-VA, fluorescein sodium videoangiography.

Discussion

The aim of aneurysm surgery is to achieve complete exclusion of the aneurysm from the circulation while preserving parent and branching vessels. Multiple intraoperative monitoring methods, including intraoperative DSA, microvascular Doppler ultrasonography, electrophysiological monitoring, and fluorescence technologies, have been introduced.[10] [11] [12] [13]

Intraoperative DSA is considered the gold standard technique for intraoperative monitoring and is advocated by some groups for most cases of intracranial aneurysms. However, the practical difficulties associated with the routine use of this modality for all aneurysm clippings have limited its utility to selected patients.[8] [14] Moreover, the invasive nature of this procedure, its higher cost, and a complication rate of 0.4 to 3.5% restrict its use to selected cases in most centers.[2] [3]

Fluorescence Technologies in Aneurysm Surgery

Fluorescence modules have been effectively integrated with operating microscopes and have gained widespread use. In many institutions worldwide, ICG has been routinely incorporated in surgery for both unruptured and ruptured cerebral aneurysms.[3] [4] [15] [16] ICG has similar rates of clip repositioning and parent vessel stenosis when compared with intraoperative DSA.[3] [7] [15]

Intraoperative fluorescein videoangiography (FL-VA) has proven to be a valuable alternative to ICG for cerebral aneurysm microsurgery. However, there are a limited number of studies that compare postoperative imaging with intraoperative findings of FL-VA.[4] [5] [17] [18] [19] [20] [21]

Previous Studies and Findings

Küçükyürük et al conducted a study with 50 consecutive patients. After aneurysm clipping, they infused 100 mg of fluorescein intravenously. FL-VA allowed for real-time assessment of the surgical field in a 3D view through binoculars, providing good image quality. In 79.68% of the aneurysms, FL-VA confirmed that the clip application was appropriate. However, postoperative angiographies indicated remnants at the aneurysm neck in five patients and parent artery stenosis in three patients, which went undetected intraoperatively. This resulted to an unexpected finding rate of 12.5%.[17]

In the present study, utilizing an FL dose of 0.5 mg/kg per administration, unexpected findings were identified in 16.3% of the aneurysms in postoperative CTA. One aneurysm indicated as a neck remnant in FL-VA, but CTA revealed a residual aneurysm. Five aneurysms had neck remnants, and three had stenosis in branching vessels, which were not observed in FL-VA but were detected in CTA. These findings are similar to studies that have compared the results of ICG-VA with postoperative DSA or CTA, which found that the concordance between ICG-VA and postoperative imaging typically remains around 90%.[8] [11] [16] [22] [23]

Factors Affecting Concordance

The observed discordance between FL-VA and CTA did not reveal any significant association with the studied factors. Distinct findings emerged from investigations on ICG-VA. Studies such as that by Dashti et al[16] highlighted variations in videoangiography using fluorescence, especially in cases of deep-seated aneurysms. They examined 239 ICG-VAs done in 190 patients with intracranial aneurysms and noted a notably high occurrence of neck remnants in deep-seated aneurysms (64%), compared with the overall rate of neck remnants, which was 6% among the cases.[16] Gruber et al[22] supported these observations, attributing the diminished image quality in ICG-VA to the challenges posed by deep surgical fields. In the present study, the presence of a deep-seated (anterior communicating artery and posterior circulation) aneurysm was not found to be a factor associated with discordance between FL-VA and postoperative imaging, a common observation in most FL-VA studies. This is attributed to the ability to acquire good quality imaging with FL-VA even in deep surgical fields.[20] [24]

Comparison between FL-VA and ICG-VA

FL-VA offers significant advantages during surgery, as it allows the continuation of microsurgical procedures while imaging is performed. Furthermore, several authors have demonstrated that FL-VA provides superior visualization compared with ICG-VA in deep-seated aneurysms. One of the primary factors contributing to this superiority is the absence of “chromatic aberration” in FL-VA. Unlike ICG-VA, which operates in the near-infrared spectrum (∼800 nm) and often results in image distortions due to suboptimal optical performance, FL-VA emits fluorescence within the visible spectrum (∼500–600 nm), where surgical optical systems achieve higher precision.[25] [26]

In addition to improved image clarity, FL-VA demonstrated higher fluorescence intensity values, particularly in deep perforators, further underscoring its imaging advantages.[25] [26] A prospective comparative analysis conducted by Lane et al found that FL-VA provided greater imaging detail in 32% of patients compared with ICG-VA, highlighting its superior capacity for visualizing complex vascular structures and enhancing intraoperative decision-making.[21] [27]

Disadvantages of FL-VA

The main disadvantage of FL-VA is the loss of quality when using sodium fluorescein repeatedly due to its staining effect on the vessel wall. To address this, a lower dose of 0.5 mg/kg was used in this study. This approach reduces drug uptake by the vessel wall, thereby maintaining better image quality even with repeated applications, compared with the use of higher doses. Another limitation of FL-VA is its inability to visualize anatomy beyond what is directly visible within the surgical field.[20] [21] [25] [28]

Limitations

First, despite this being a prospective case series regarding FL-VA use in cerebral aneurysm surgeries, it was conducted at a single center. Second, despite numerous studies demonstrating the high sensitivity and specificity of postoperative CTA in detecting residual aneurysms and adjacent vessel stenosis, DSA is still considered the gold standard. This preference highlights DSA's superior spatial resolution and its ability to detect subtle residual aneurysms or vessel stenosis that CTA might miss. Excluding DSA may introduce biases, such as underestimating small residuals due to CTA limitations. Finally, prospective and randomized studies are necessary to compare the results of FL-VA with other techniques such as ICG-VA and intraoperative DSA.

Conclusion

This study's findings indicate that FL-VA and CTA are largely concordant, although some discrepancies remain. Further prospective, randomized studies are needed to compare FL-VA with other techniques like ICG-VA to establish its definitive efficacy and reliability. Despite its limitations, FL-VA presents a promising alternative for intraoperative assessment in aneurysm microsurgeries.

Conflict of Interest

None declared.

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Publication History

Article published online:
26 May 2025