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

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

https://doi.org/10.21203/rs.3.rs-3764469/v1

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Comparing the findings of intraoperative fluorescein sodium videoangiography (FL-VA) and post operative Computed Tomography Angiography (CTA), this study aims to assess whether FL-VA is a suitable modality for intraoperative evaluation of aneurysmal obliteration and the patency of parent and adjacent vessels. This study is an observational prospective analysis focused on patients who underwent surgery for aneurysms at the Department of Neurosurgery, Santa Casa BH, Belo Horizonte, Minas Gerais, from December 2021 to September 2022. 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. FL-VA revealed complete occlusion in 93.4% of the studied aneurysms (57 out of 61). Ten cases of discordance between FL-VA and CTA were identified: One patient was indicated as a neck remnant in FL-VA, but CT angiography revealed a residual aneurysm; one patient CT angiography showed neck remnant and stenosis in branching vessels, that it was not identified by FL-VA; five aneurysms had neck remnants, and three cases had stenosis in branching vessels, which were not observed in FL-VA but were detected in CTA. No studied factor showed significant association with the discordance observed between FL-VA and CT angiography. The results of this study contribute to the increasing evidence that supports FL-VA as a highly valuable modality for the intraoperative assessment of aneurysmal obliteration and the patency of parent and adjacent vessels

Microsurgery

Neurosurgery

Fluorescein

Intracranial Aneurysms

Clipped

Since McKissock et al. [15] first demonstrated the benefits of surgical intervention for ruptured intracranial aneurysms, significant efforts have been devoted toward optimizing the safety and efficacy of surgical aneurysm obliteration. From these efforts we have learned that total obliteration of the aneurysm while maintaining blood flow through parent and branch vessels is the hallmark of successful surgical therapy.

Based on the literature, the rate of aneurysm remnant and neighboring vessel compromise in the post-operative angiography varies from 1.8 to 3.6% and 1.6–21%, respectively [23]. Importantly, incomplete aneurysm occlusion as well as inadvertent arterial sacrifice increases the risk of (re)bleeding and cerebral ischemia. The actual rates of the latter vary from 4 to 18% and 3–14%, respectively [ 26, 27]. Therefore, intraoperative assessment of clipped intracranial aneurysms is of utmost importance in neurovascular surgery.

To minimize the risk of these unintended consequences, many have advocated for the use of different intraoperative techniques are employed to view the blood flow in the vessels that surround the aneurysm, that including doppler ultrasonography, intraoperative cerebral angiography (DSA) and fluorescent technologies [7].

The use of fluorescent technologies in neurovascular surgery emerged after indocyanine green (ICG) video angiography was first described in 2003 [19]. It shortly became a standard of care as data regarding the use of ICG have grown substantially and ICG video angiography (ICG-VA) proved to be very efficient in preventing postoperative complications [16, 18]. 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.

This study is an observational prospective analysis focused on 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.

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

Population

Between December 2021 and September 2022, a total of 57 patients underwent craniotomy procedures for intracranial aneurysm clipping. Fifty-four patients underwent FL-VA and postoperative CT angiography. Three patients did not have the clinical conditions to undergo the post-operative CT angiography.

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

Intraoperative Fluorescence module

In this study was 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 delineates the fluorescent signal using intravascular sodium fluorescein and visualizes nonfluorescent tissue in a relatively dim background (based on the depth of the operative field), where manipulation of vessels is often safe and possible. This module is optimized for excitation in the range of 460–500 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 Videoangiography

After aneurysm clipping, we administered a 0.5mg/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. In our experience, this is the lowest dose that maintains adequate fluorescent signal detectable within the arteries using 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 patients of the 57 patients with 61 aneurysms. All CTA studies were performed on a 128-channel multidetector row CT system (Somaton go.Top, Siemens Healthineers, USA), with patients’ heads fixed in a neutral position during the examination in order to prevent motion artifacts. For acquisition we used the following parameters: 100 kVp, 320 mAs, 64 × 0.625 mm detector collimation, 0.6 s gantry rotation time, a pitch of 0.984, section thickness of 0.625 mm, 220 mm FOV 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 fow 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 fow and scanning. The scan started manually once the contrast reached the aortic arch.

A 3D workstation (RadiAnt DICOM® Viewer 2021.2, Medixant, Poland) was used to reconstruct 3D data sets. The neuroradiologist analyzing the postoperative CT angiography was unaware of findings on the intraoperative FL-VA. CT Angiography was used instead of digital subtraction angiography (DSA) due to its non-invasive character, and high sensitivity and specificity for residual aneurysm detection and parent vessel occlusion which was demonstrated by Bharatha et al.[1]

Following image acquisition, the attending neuroradiologist interpreted the findings. The following CTA data was 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 post operative Computed Tomography Angiography

Statistical Analysis

Collected data were entered into a computer data-base. 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 post-operative CTA findings.

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

Clinical Outcome

Of the 57 patients submitted to microsurgery, 40 (70.2%) showed good outcomes, modified Rankin Scale ≤ 2 (mRS ≤ 2). Four patients died, for a mortality rate of 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 and Hess grade > 2. Twenty-two patients (66.6%) showed good outcomes. Three patients died, for a mortality rate of 9%.

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%)
Mutiple aneurysm
No	42 (65,6%)
Yes	15 (34,4%)
Location
Posterior circulation	2 (3,1%)
Anterior circulation	55 (96,9%)
Hunt Hess grade (ruptures aneurysm)
Hunt Hess > 2	12
Hunt Hess ≤ 2	21

Comparison of intraoperative FL-VA with postoperative CT- Angiography

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 CT angiography revealed a residual aneurysm. One patient CT angiography 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 3 cases where CTA revealed stenosis in branching vessels, blood flow was adequate, and no ischemic complications were identified in these patients. In cases of neck remnants, a decision was made to follow up with imaging. In the patient with an aneurysm remnant, it was a non-ruptured calcified aneurysm, and the remnant measured 6mm. The decision was also made to follow up with imaging.

Discordance vs Nondiscordance group

Characteristics of the FL-VA – postoperative CTA discordance group compared with the nondiscordance group are outlined in Table 2. In univariate analysis, none of the pre-determined variables listed in Table 2 were statistically significant.

Table 2

– Comparison of FL-VA–CT Angiography discordance to nondiscordance*
	Data Analysis
	Nondiscordance		Discordance		p-value*
	n	%	n	%	p-value*
Sex
Female	34	82.9	7	17,1	1.00
Male	13	81.3	3	18.8
Age (years)
≤ 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-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

*Fisher’s exact test

Illustrative Cases

Case 1

A 59-year-old patient with a ruptured aneurysm. CT Angiography 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 CT angiography showed stenosis of the contralateral posterior cerebral artery (Fig. 1).

Case 2

A 66-year-old patient with a unruptured aneurysm. CT Angiography revealed of an aneurysm in the left middle cerebral artery (ACM). After the placement of the clip, the videoangiography suggested complete occlusion of the aneurysm. Postoperative CT angiography showed small neck remnant (Fig. 2).

The goal of aneurysm surgery is to achieve complete exclusion of the aneurysm from the circulation while preserving parent and perforating/branching vessels. A variety of intraoperative monitoring techniques such as intraoperative DSA, micro vascular Doppler ultrasonography, electrophysiological monitoring, and fluorescents techniques have been introduced. [3, 8, 17, 25]

Intraoperative DSA is the gold standard technique for intraoperative monitoring and is advocated by some groups for most cases of intracranial aneurysms, the practical difficulties associated with the routine use of this modality for all aneurysm clippings have limited its utility to selected patients.[9, 18] Moreover, the invasive nature of this procedure, higher cost and the complication rate of 0.4–3.5% restricted its use to selected higher risk cases in most centers.[23, 27]

Fluorescence modules have been successfully integrated with the operating microscope and became widely used. In many institutions worldwide, ICG has been routinely incorporated in surgery for elective and ruptured cerebral aneurysms[2, 20, 26, 27]. It has similar rates of clip reposition and parent vessel stenosis when compared head-to-head with either intraoperative or postoperative DSA [16, 20, 27].

Intraoperative FL-VA has proven to be a valuable alternative to ICG for cerebral aneurysm microsurgery. Nevertheless, there is a limited number of studies that compare postoperative imaging with intraoperative findings of FL-VA.[5, 7, 10, 12, 14, 26, 28]

Küçükyürük et al. in a study with 50 consecutive patients. After clip ligation of the aneurysm, they administered 100 mg of fluorescein intravenously. FL-VA allowed for the real-time assessment of the surgical field in a three-dimensional view through binoculars, providing good image quality. In 79.68% of the aneurysms, FL-VA confirmed that the clip application was satisfactory. However, postoperative angiographies revealed remnants at the aneurysm neck in 5 patients and parent artery stenosis in 3 patients, which were not recognized intraoperatively, resulting in an unexpected finding rate of 12.5%.[10]

In the present study, utilizing an FL dose of 0.5 mg/kg per administration, unexpected findings were identified in 16.3% (10 aneurysms) of the postoperative CTA. One aneurysm indicated as a neck remnant in FL-VA, but CT angiography 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 CT angiography. These findings are similar with studies that have compared the results of ICG-VA with postoperative DSA or CTA. These studies have consistently found that the concordance between ICG-VA and postoperative imaging typically remains at around 90%.[2–4, 6, 18]

Dashti et al (2009) studied 239 ICG-VA done in 190 patients with intracranial aneurysms and found an unexpectedly high rate of neck residuals in deep-sited aneurysms (64%) as compared to the overall rate of neck residues in 6% of the cases. In addition, the branch vessel occlusion was observed in 6% of the cases with no incidence of parent artery occlusion.[2]

While no studied factor showed significant association with the discordance observed between FL-VA and CT angiography, distinct findings emerged from investigations on ICG-VA. Studies, such as those by Dashti et al.[2], demonstrated discrepancies in videoangiography using fluorescence, particularly in cases of deep-seated aneurysms. Gruber et al.[4] echoed these observations, attributing the diminished image quality in ICG videoangiography to the challenges posed by deep surgical fields. In this study, the presence of a deep-seated (ACoA and posterior circulation) aneurysm was not found to be a factor associated with discordance between FL-VA and post-operative 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-seated field [14, 24].

According to certain authors, a comparison between intraoperative ICG-VA and FL-VA reveals several advantages associated with FL-VA. It allows for the continuation of microsurgery while FL-VA is being performed. In addition, it delivers high-quality images suitable for evaluation of even small perforating arteries due to lack of ‘chromatic aberration’ that ICG-VA is prone to. Moreover, the ease of interpretation of these images obtained intraoperatively is similar to ICG-VA[21, 22]. In a prospective comparative analysis reported by Lane et al.[12, 13], FL-VA provided even superior detail in 32% of patients when compared with ICG-VA.

Concerning the disadvantages of FL-VA, the main one is the loss of quality when using sodium fluorescein repeatedly due to its stain on the vessel wall. Another limitation of FL-VA is its inability to visualize anatomy beyond what is directly visible within the surgical field. [11, 12, 14, 21]

Limitations:

Firstly, despite it being a prospective case series regarding FL-VA use in cerebral aneurysm surgeries, it was conducted at a single center. Secondly, despite numerous studies demonstrating the high sensitivity and specificity of postoperative CT angiography in detecting residual aneurysms and adjacent vessel stenosis, digital arteriography is still considered the gold standard. Finally, prospective and randomized studies are still necessary to compare the results of FL-VA with other techniques such as ICG-VA and IA.

The results of this study contribute to the increasing evidence that supports FL-VA as a highly valuable modality for the intraoperative assessment of aneurysmal obliteration and the patency of parent and adjacent vessels

Conflict of Interest

The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical Approval

Approval for this study was obtained from the Institutional Medical Ethics Committee of Santa Casa de Misericórdia de Belo Horizonte (CAAE 31703420.0.0000.5138). Informed consents from patients were obtained for participation in this study. Attached is the consolidated opinion of the Institutional Medical Ethics Committee. It is available in the native language (Portuguese).

Funding

Not applicable.

Avaliability of data and materials

All data is organized in a Microsoft Excel spreadsheet. If necessary, we can send the editors this data. In addition, the patients' consent forms are printed. If necessary, authors can scan them and forward them to the editorial team.

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No competing interests reported.

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

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Abstract

Figures

Introduction

Methods

Population

Intraoperative Fluorescence module

Sodium Fluorescein Videoangiography

Postoperative Computed Tomography Angiography

Comparison of FL-VA with post operative Computed Tomography Angiography

Statistical Analysis

Results

Clinical Outcome

Comparison of intraoperative FL-VA with postoperative CT- Angiography

Discordance vs Nondiscordance group

Discussion

Conclusion

Declarations

References

Additional Declarations

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