The Role of Computed Tomographic Angiographyin Predicting the Development of Vasospasm Following Ruptured Intracranial Aneurysm Microsurgery

orkun 1, Kas, 2023

Genel

Review began 08/28/2023 Review ended 09/11/2023 Published 09/16/2023

Open Access Original

Article DOI: 10.7759/cureus.45386

The Role of Computed Tomographic Angiography in Predicting the Development of Vasospasm Following Ruptured Intracranial Aneurysm Microsurgery

© Copyright 2023

Varol. This is an open access article distributed under the terms of the Creative

Eyüp Varol

Commons Attribution License CC-BY 4.0., which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

1. Neurological Surgery, Umraniye Training and Research Hospital, Istanbul, TUR

Corresponding author: Eyüp Varol, dreyupvarol@gmail.com

Abstract

Introduction

Following subarachnoid hemorrhage, cerebral vasospasm is the primary cause of morbidity and death. The aim of this study is to predict the development of vasospasm by detecting changes in vessel diameter after surgery using computed tomography angiography.

Methods

We retrospectively evaluated the patients who underwent aneurysm clipping due to a bleeding aneurysm between 2019-2022. Age, gender, location, subarachnoid hemorrhage grades, development of perioperative rupture, and temporary clip use were examined. Preoperative and postoperative diameters of the internal carotid artery, A1-A2, and M1-M2 were measured. Radiological and clinical vasospasm development in the postoperative period was also documented.

Results

The aneurysm localizations of the 100 patients (mean age: 50.38±13.04 years) were anterior cerebral artery in 50 patients, internal carotid artery in 37 patients, and middle cerebral artery in 30 patients. In the postoperative follow-up, radiological vasospasm was apparent in 41 patients. The changes in arterial diameter reveal a statistically significant decrease in the internal carotid artery, M1-M2, and A1-A2 artery diameters on the operated side compared to the contralateral side (p<0.001). Based on the receiver operating characteristic (ROC) analysis, the most likely change in arterial diameter on the operated side to indicate the presence of vasospasm was calculated from the available data, where the decrease in total arterial diameter was 13.7%.

Conclusion

Vasospasm remains one of the significant causes of morbidity and mortality post subarachnoid hemorrhage. While there have been advances in imaging modalities, predicting which patients will develop vasospasm has remained elusive. Our research attempts to provide a quantifiable metric (13.7% decrease in vessel diameter) that can be an early predictor of this complication.

Categories: Neurosurgery

Keywords: computed tomographic angiography, vasospasm, hemorrhage, subarachnoid, aneurysm

Introduction

Aneurysmal subarachnoid hemorrhage (aSAH) is a life-threatening disease that affects three to 25 people per 100,000 worldwide every year [1]. Vasospasm is evident in around 40% of aSAH patients, and 20-30% of aSAH patients suffer from vasospasm-related neurological impairments [2-5]. Following subarachnoid hemorrhage (SAH), cerebral vasospasm (CVS) is one of the common causes of morbidity and death [6]. Vasospasm affects 50-70% of SAH patients, with 50% of these patients experiencing neurological symptoms (i.e., symptomatic CVS) [7]. A new focal neurological deficit that is not explained by rebleeding or hydrocephalus and an altered level of consciousness are common indications of vasospasm. CVS is well known to cause neurological impairments through delayed cerebral ischemia [3,8,9].

Cerebral infarction affects half of all symptomatic CVS patients and is deadly in 30% of cases [10]. It is critical to research CVS to support the development of effective therapies and reduce the morbidity rate of people with this ailment. Despite efforts to develop novel medicines to prevent and cure CVS, it continues to be a major cause of death and mortality in patients who survive initial aSAH therapy [11,12]. One of the objectives of critical care monitoring in these patients is early diagnosis of CVS. Cerebral digital subtraction angiography (DSA) is currently the gold standard for diagnosing CVS [13,14]. Nevertheless, it is not apparent

How to cite this article

Varol E (September 16, 2023) The Role of Computed Tomographic Angiography in Predicting the Development of Vasospasm Following Ruptured Intracranial Aneurysm Microsurgery. Cureus 15(9): e45386. DOI 10.7759/cureus.45386

if these data might be comparable to the DSA resolution images, which are the gold standard imaging

technique [15]. Magnification, the distance from the source of the image to the detector, and the viewing

angle are some of the variables that influence vessel diameter measurements on DSA. Furthermore,

measurements are frequently provided only in relative units when assessing pictures with simple imaging

viewers [16].

Transcranial Doppler (TCD) ultrasonography is one example of the non-invasive methods that can be used

to detect vasospasm in patients with aSAH. However, its low specificity and high operator dependence

render it an inadequate detection tool for vasospasm [17]. Another non-invasive imaging technique,

computed tomographic angiography (CTA), shows greater promise as a more accurate tool for evaluating

vasospasm. This established routine screening tool provides non-invasive information about cerebral artery

diameters [18]. Multidetector CTA, which enables rapid image acquisition and lower radiation exposure, has

gained popularity over the last decade. Our aim in this study is to use CTA to evaluate changes in vessel

diameter after surgery and assess the effects of those changes on vasospasm in order to predict the

development of vasospasm.

Materials And Methods

Patient data and outcome assessment

For this research, we retrospectively evaluated the collected data of patients in our clinic who underwent

aneurysm clipping due to a bleeding aneurysm between 2019 and 2022.

Inclusion criteria

The inclusion criteria included patients who underwent aneurysm clipping due to a bleeding aneurysm

between 2019 and 2022; patient age greater than 18 years and less than 85 years; availability of both

preoperative and immediate postoperative CTA and diffusion-weighted images (DWI) data; patients with

complete clinical documentation, including recorded data about age, gender, aneurysm location, Fisher

classification, Hunt-Hess (HH) classification, and World Federation of Neurosurgical Societies (WFNS)

grade; and patients who provided written informed consent.

Exclusion criteria

The exclusion criteria included patients with incomplete clinical documentation or missing preoperative or

postoperative imaging data; patients with other cerebral pathologies such as tumors, arteriovenous

malformations, or previous strokes which could interfere with accurate measurement of arterial diameters;

patients who did not provide informed consent or those unable to provide consent due to incapacitation;

patients with other surgical interventions or endovascular procedures on the cerebral arteries within the

previous year; patients with contraindications to CTA or DWI such as severe allergy to contrast agents or

metallic implants; pregnant women or those nursing; and patients with chronic kidney disease or renal

dysfunction, which contraindicates the use of contrast agents.

The recorded data concerns the patient’s age and gender, the location of the aneurysm causing subarachnoid

bleeding, Fisher classification, Hunt-Hess (HH) classification, WFNS grade, single or multiple aneurysm,

development of perioperative rupture, and temporary clip use and duration. The recorded blood volumes in

the aspirator were used to determine the amount of bleeding during the operation. Preoperative and

postoperative vessel diameters of the internal carotid artery (ICA), A1-A2, and M1-M2 were measured on

the operated and non-operated sides and noted. All measurements were made by two experienced

neurosurgeons, and their mean values were taken. The development of radiological and clinical vasospasm

in the postoperative period was also documented. If a newly developed restriction was observed on DWI, it

was evaluated as a radiological vasospasm. It was accepted as a clinical vasospasm if a newly onset

neurological deficit was observed. Patient data are reported according to common descriptive statistics.

Written informed consent was obtained from all patients, and the study was performed in accordance with

the ethical standards of the Declaration of Helsinki and under the approval of our institutional review

committee. Ethical approval for the study was obtained from the Umraniye Training and Research Hospital

Ethics Committee.

Radiological technique

The same tomography device was employed for all patients in the study. Preoperative and postoperative

vessel diameters were measured in all patients by two senior neurosurgeons, and the assessment used the

average of the measurements taken by the two neurosurgeons. Preoperative and immediate (<24 hours)

postoperative CTA and DWI were conducted according to a standard predefined imaging protocol. The

vascular diameters were assessed in preoperative and postoperative CTA images on operated and non

operated parts. Measurements were performed at 1 cm distal to the anterior cerebral artery (ACA) origin, 1

cm distal to the M1 and M2 origins, and 1 cm proximal to the formation of the ACA and middle cerebral

artery (MCA) composition for the ICA (Figure 1).

2023 Varol et al. Cureus 15(9): e45386. DOI 10.7759/cureus.45386 2 of 9

FIGURE 1: Measurements of arterial diameters in a 3D image viewer

software

a) internal carotid artery, b) M1 segment of middle cerebral artery, c) A1 segment of anterior cerebral artery, d) A2

segment of anterior cerebral artery

Preoperative and postoperative DWI were performed in all patients for radiological evaluation of vasospasm.

Statistical analysis

The Statistical Package for the Social Sciences (SPSS) version 25.0 (IBM Inc., Armonk, New York) program

was used for statistical analysis to evaluate the results of this study. Descriptive, graphical, and statistical

methods were applied to determine whether the scores obtained from each continuous variable were

normally distributed. The Kolmogorov-Smirnov test was used to test the normality of the scores obtained

from a continuous variable with the statistical method. Descriptive statistical methods (number, percentage,

mean, median, standard deviation, etc.) were used while evaluating the research data. Comparisons between

two groups in quantitative data were made with the independent samples t-test (in data with normal

distribution) and Mann-Whitney U test (in data with no normal distribution), and comparisons of more than

two groups were made with the Kruskal-Wallis test. The Bonferroni test was used to determine from which

groups the difference originated, while Chi-squared tests (Pearson’s chi-squared test, continuity correction

test, and Fisher’s exact test) were applied for qualitative comparisons between groups. Repeated

measurements were made with the paired samples t-test. Receiver operating characteristic (ROC) analysis

was used to determine the most appropriate rate of change in arterial diameter in the presence of

vasospasm. A p-value of less than 0.05 was considered statistically significant with a 95% confidence

interval.

Results

Within the scope of the study, the findings of 100 patients were analyzed. The mean age of the patients was

50.38 ± 13.04 years, and 50% of them were in the age group of 50 years and above. Of the 100 patients, 51%

were female, and 49% were male. According to radiological imaging results, the aneurysm localization was

ACA in 50 patients, ICA in 37 patients, and MCA in 30 patients. Aneurysm was observed as multiple in 16

patients and single in 84 patients. Temporary clips were applied to 47% of the patients. The presence of

perioperative rupture was reported in 34% of the patients, and the mean amount of perioperative bleeding

was 306.20 ± 191.92 mL. In the postoperative follow-up, radiological vasospasm was apparent in 41 patients.

During the treatment period, morbidity was observed in 15 (15%) patients, and mortality was observed in 13

(13%) patients (Table 1).

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n=% Mean(SD) Min.-Max. Age Total 100 50.38 (13.04) 24-79 <50 50 Age group ≥50 50 Male 49 Gender Female 51 Right 55 Surgery side Left 45 ACA 50 Aneurysm location ICA 37 MCA 30 Single 84 Aneurysm single/ multiple Multiple 16 Yes 47 Temporary clip No 53 Yes 34 Perioperative rupture No 66 Yes 41 Vasospasm No 59 Perioperative bleeding (cc) Total 100 306.20 (191.92) 50-1000 Discharged with healing 72 Discharge situation Need care 15 Dead 13

TABLE 1: Patient demographics (N=100)

ACA – anterior cerebral artery, ICA – internal carotid artery, MCA – middle cerebral artery, Min – minimum, Max – maximum, SD – standard deviation

We examined the WFNS, Fisher, and HH scale results of the patients and found that the mean scores were

2.02 ± 1.30, 2.59 ± 1.19, and 2.12 ± 1.17, respectively.

There was no statistically significant difference between the measurements made by the two neurosurgeons.

The changes in arterial diameter reveal a statistically significant decrease in the ICA, M1-M2, and A1-A2

artery diameters on the operated side compared to the contralateral side (p<0.001). The evaluation of all

arteries together found a 13.2% decrease in mean arterial diameter on the operated side and a 3% decrease

on the opposite side (p<0.001). In the preoperative period, the total arterial diameter was higher on the

operated side (2.40 ± 0.27) than on the contralateral side (2.29 ± 0.23) to a statistically significant extent

(p=0.004). In the postoperative period, a decrease in arterial diameter was detected on the operated side

(2.08 ± 0.30) compared to the contralateral side (2.22 ± 0.20), also with statistical significance (p<0.001;

Table 2).

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Preoperative Postoperative Difference %↓ Artery diameter (mm) Side Mean±SD Mean±SD p-value Mean±SD ^{Operated 3.34±0.49 2.92±0.53}<0.001^a_*12.5±8.9 ICA ^{Non-operated 3.14±0.42 3.08±0.40}<0.001^a_*1.7±4.2 ^p-value0.002^c* 0.018^c* <0.001^b* ^{Operated 2.07±0.28 1.80±0.31}<0.001^a_*12.7±9.8 ^{Non-operated 2.03±0.24 2.01±0.22}0.009^a_*1.0±4.2 M1-2 ^p-value0.332^c<0.001^c* <0.001^b* ^{Operated 1.78±0.22 1.51±0.23}<0.001^a_*14.7±12.0 A1-2 ^{Non-operated 1.68±0.21 1.54±0.20}<0.001^a_*7.7±10.0 ^p-value<0.001^c* 0.397^c<0.001^b* ^{Operated 2.40±0.27 2.08±0.30}<0.001^a_*13.2±8.3 Total ^{Non-operated 2.29±0.23 2.22±0.20}<0.001^a_*3.0±4.3 ^p-value0.004^c* <0.001^c* <0.001^b*

TABLE 2: Change in artery diameters before and after surgery (N=100)

* p<0.05, a – paired samples t-test, A1-2 – A1-2 segments of anterior cerebral artery, b – Mann-Whitney U test, c – independent samples t-test, ICA – internal carotid artery, M1-2 – M1-2 segments of middle cerebral artery, SD – standard deviation

While not statistically significant (p=0.364), the rate of vasospasm was higher in patients with perioperative

temporary clips than in those without (47% vs. 36%). The rate of vasospasm was also higher in patients with

perioperative rupture than in those without (56% vs. 33%), which was at the limit of statistical significance

(p=0.050). The rate of vasospasm was 32% in discharged patients, 80% in patients who needed care, and 46%

in patients who died (p=0.002).

The rate of vasospasm was found to be higher among those with a Fisher grade of III or above than among

those with a grade of II or below (51.7% vs. 25%, p=0.014). The rate was also higher in patients with a WFNS

score and HH classification of II or above compared to those with a score below II (WFNS: ≥II, 59.6% vs. <II,

20.8%, p<0.001; H&H: ≥II, 50% vs. <II, 21.9%, p=0.014). The Fisher grade, WFNS, and HH classification

scores of patients with vasospasm were higher than those of patients without vasospasm. This difference

was statistically significant (p<0.05). Among patients presenting with vasospasm, there was no statistically

significant difference in terms of age or amount of perioperative bleeding (p>0.05; see Table 3).

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Vasospasm p-value Yes (n=41), mean±SD No (n=59), mean±SD Age 50.71±13.69 50.15±12.68 0.763 Bleeding (cc) 332.20±214.65 288.14±174.02 0.325 ^{Fisher grade 3.00±1.00 2.31±1.24}0.005^c* ^{WFNS grade 2.32±1.21 1.81±1.33}0.002^c* ^{Hunt-Hess grade 2.34±1.11 1.97±1.20}0.020^c*

TABLE 3: Averages of some continuous variables according to the presence of vasospasm (N=100)

* p<0.05 with Mann-Whitney U test, SD – standard deviation, WFNS – World Federation of Neurosurgical Societies

Compared to patients without vasospasm, patients with vasospasm showed a greater, statistically significant

decrease in arterial diameter on both the operated and contralateral sides, ICA, M1-M2, A1-A2, and total

arterial diameters (p<0.05). In patients with perioperative rupture, there was a greater decrease in arterial

diameter on both the operated and contralateral sides, ICA, A1-A2, and total arterial diameters compared to

patients without perioperative rupture. This difference was statistically significant (p<0.05).

The area under the curve was found to be 0.967 (95% CI: 0.931-1); accordingly, the change in arterial

diameter (% decrease rate) was found to be statistically significant (p<0.001) for determining the presence of

vasospasm. Based on the ROC analysis, the most likely change in arterial diameter on the operated side to

indicate the presence of vasospasm was calculated from the available data, where the decrease in total

arterial diameter was 13.7%. For the cutoff value of 13.7%, the sensitivity was 100%, the specificity was

91.5%, the positive predictive value was 89.1%, the negative predictive value was 100%, and the overall

accuracy was 95% (Table 4).

Radiological vasospasm occurrence Cutoff value 13.7% AUC (%95 CI) 0.967 (0.931-1) p-value <0.001 Sensitivity 100% (41/41) Specificity 91.5% (54/59) PPV 89.1% (41/46) NPV 100% (54/54) Accuracy 95% (95/100)

TABLE 4: Optimal positive cutoff limit for the rate of decrease in total artery diameter of the operated side in determining the presence of vasospasm (ROC analysis results)

AUC – the area under the ROC curve, CI – confidence interval, NPV – negative predictive value, PPV – positive predictive value

Discussion

Our study aimed to bridge a critical gap in the field of neurosurgery by investigating the utility of CTA in

predicting the development of vasospasm in patients with aSAH after surgery. The primary outcomes of our

study reveal a statistically significant decrease in arterial diameters, particularly in the ICA, M1-M2, and A1-

A2 arteries on the operated side compared to the contralateral side. These findings suggest that CTA can be a

valuable tool for monitoring postoperative changes in vessel diameter, potentially identifying patients at a

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higher risk of developing vasospasm. This information can enable clinicians to take proactive measures,

such as closer neurological monitoring and targeted interventions, to prevent or mitigate the impact of

vasospasm.

Moreover, the ability to predict vasospasm early in the postoperative period can significantly improve

patient outcomes. It can lead to timely interventions that reduce the risk of cerebral infarction and its

associated morbidity and mortality. Our study lays the foundation for further research in this area. It may

contribute to developing standardized protocols for using CTA in the postoperative monitoring of aSAH

patients. The ability to predict vasospasm early and take proactive measures based on CTA measurements

can improve patient care and reduce the devastating consequences of vasospasm following aSAH.

The main cause of focal cerebral ischemia after SAH is CVS [19]. While rebleeding is the most frightening

complication that can develop after aSAH, it has gradually decreased in prominence due to the widespread

practice of early surgery. Meanwhile, vasospasm has become the most risky complication of SAH in terms of

mortality and morbidity [3,8,9]. Therefore, early recognition of vasospasm is vital. Aneurysmal SAH patients

with a history of vasospasm should take measures to prevent vasospasm, especially during the riskiest

periods. To reduce morbidity and mortality, healthcare providers must watch patients closely to intervene

quickly to treat vasospasm.

Although the literature reports a lower risk of developing vasospasm among elderly patients, the

relationship between age and vasospasm was not statistically significant in the present study (p=0.763). In

addition, while some studies evidence that arterial diameters can vary according to age and gender, our

study excludes this risk, as it evaluated not only the diameter but also the change [20]. However, we found

that the risk of developing cerebral vasospasm was statistically significant in patients with high Fisher

(p=0.005), WFNS (p=0.002), and HH (p=0.02) scores. Existing literature has reported similar findings. In

addition, some publications have associated intraprocedural bleeding during embolization with vasospasm,

which is consistent with our study [21].

Methods such as DSA, TCD, magnetic resonance imaging, CTA, computed tomography perfusion, and

magnetic resonance perfusion are used for the imaging of vasospasm. Previous studies have shown that CTA

is effective for diagnosing vasospasm, particularly through the evaluation of vasoconstriction and

volumetric vessel analysis [22,23]. While CTA has the advantages of being rapid, affordable, widely available,

and non-invasive, it also poses limitations, such as ionizing radiation, contrast injection, clip- or coil

induced artifacts, the requirement of transportation to the CT scan, and a fair level of inter-rater

reliability [24].

Imaging parameters to predict vasospasm and delayed cerebral ischemia (DCI) can be used alone or in

combination with clinical markers to increase specificity and sensitivity. To evaluate the risk of DCI, the

modified Fisher scale and the WFNS scale have been combined in the VASOGRADE scale, which uses a

straightforward, three-category grading system [25]. Another scale that enables risk assessment for in

hospital mortality is based on HH score, age, intraventricular hemorrhage, and rebleed (HAIR) [26]. The

VASOGRADE scale and HAIR score did not outperform clinical evaluation in predicting cerebral infarction

and a bad prognosis, although they were superior to radiological measurements alone [27,28]. A recent study

has developed a four-variable early score for DCI prediction that includes the WFNS scale, the modified

Fisher scale, Subarachnoid Hemorrhage Early Brain Edema Score, and intraventricular hemorrhage [29].

However, these studies have reported that these scores are effective for diagnosing vasospasm at the time of

diagnosis.

Our study stands out due to its pioneering approach, as it introduces a novel standardization method for the

early diagnosis of patients prone to developing vasospasm or vasoconstriction following postoperative

subarachnoid hemorrhage (SAH). Notably, this study is the first to propose such an approach in the existing

literature. In our study, the sensitivity was 100% for the cut-off value of 13.7% in early postoperative CTA.

The specificity was 91.5%, the positive predictive value was 89.1%, the negative predictive value was 100%,

and the overall accuracy was 95%.

Previous research on the use of CTA for the diagnosis of vasospasm has reported that imaging performed

after vasospasm develops can effectively support diagnosis [22,23]. Computed tomographic angiography has

a sensitivity of about 98% in detecting cerebral aneurysms, and the combination of CT and CTA has a

sensitivity of more than 99% in diagnosing aSAH [30]. Other studies of volumetric measurement have aimed

to predict the development of cerebral ischemia and its use in the application of treatment modalities. The

distinguishing finding of our study is that CTA performed in an early period (<24 hours) before the

development of clinical vasospasm can provide insight into the risk of vasospasm development after SAH in

patients and may help with early diagnosis, thus providing standardization of diagnosis and treatment.

Considering that CTA is a routine test performed in the preoperative and postoperative control periods, our

study claims that vasospasm can be predicted without additional imaging modalities. This study is the first

to make this suggestion in literature to our knowledge.

This research has some limitations. The most significant is its retrospective character, as all study data were

retrieved from accessible patient files, and no patient interviews or questionnaires were administered. The

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retrospective screening of CTA is another limiting factor; however, we attempted to mitigate this limitation

by having two specialist physicians perform the measurements.

Conclusions

Vasospasm is one of the most important causes of mortality and morbidity after aSAH, and there is no

definitive method to predict the development of vasospasm. By measuring the arterial diameters via CTA,

which is an easily accessible method, and comparing them with the cut-off values we have revealed in the

study, vasospasm can be predicted, and precautions can be taken accordingly.

Additional Information

Disclosures

Human subjects: Consent was obtained or waived by all participants in this study. Umraniye Training and

Research Hospital Ethics Committee issued approval B.10.1.TKH.4.34.H.GP.0.01/229. Animal subjects: All

authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In

compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services

info: All authors have declared that no financial support was received from any organization for the

submitted work. Financial relationships: All authors have declared that they have no financial

relationships at present or within the previous three years with any organizations that might have an

interest in the submitted work. Other relationships: All authors have declared that there are no other

relationships or activities that could appear to have influenced the submitted work.

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