The morphological characteristics and risk of rupture of ruptured and unruptured internal carotid siphon aneurysms: a preliminary study

doi:10.21203/rs.3.rs-4954805/v1

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The morphological characteristics and risk of rupture of ruptured and unruptured internal carotid siphon aneurysms: a preliminary study

https://doi.org/10.21203/rs.3.rs-4954805/v1

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Objective

To compare the morphologic features of unruptured and ruptured aneurysms of the siphon of the internal carotid artery to find a more valuable reference to assess the rupture risk of aneurysms.

Methods

156 patients with internal carotid siphon aneurysms were retrospectively enrolled in the study, all of whom were examined by volume computed tomographic digital subtraction angiography (VCTDSA). 49 patients (51 aneurysms) in the ruptured group and 107 patients (120 aneurysms) in the unruptured group, respectively. A total of 21 indices, such as aneurysm inclination angle and width, were compared between the unruptured and ruptured groups., The univariate analysis, receiver operating characteristic (ROC) curves judging the specificity and sensitivity of the indices to determine the maximum critical value, and multifactorial logistic regression were used to analyze the results.

Results

The univariate analysis method revealed statistically significant differences in size, morphology, width, height, site, neck, inflow angle, inclination angle, parent-daughter angle, SR (Size ratio), AR (Aspect ratio), S1/S2 (area ratio), aneurysm width/neck width, maximum diameter, multiplicity, and age between the ruptured and unruptured groups of siphonotic aneurysms. The multifactorial study approach suggested that the angle of inclination (OR = 4.062, 95% CI = 1.570 ~ 10.513, P = 0.004), aneurysm size (OR = 12.607, 95% CI = 4.4 ~ 36.124, P < 0.001), and the presence of a multifocal aneurysm (OR = 4.274, 95% CI = 1.620 ~ 11.272 P = 0.003) were independent risk factors for the rupture of internal carotid siphon aneurysms.

Conclusions

The angle of inclination of the internal carotid siphon aneurysm, whether it is multiple or not, and its size are more risk factors for the morphological prediction of aneurysm rupture and valuable in assessing the risk of aneurysm rupture.

internal carotid siphon aneurysm

rupture risk

risk factors

VCTDSA

The intracranial aneurysms is relatively low incidence, but high the mortality and disability rates following rupture and hemorrhage [1]. The vast majority of spontaneous subarachnoid hemorrhages originate from ruptured intracranial aneurysms, thus early assessment of the risk of unruptured aneurysms is essential[2]. The siphon of the internal carotid artery is one of the most common sites for intracranial aneurysms, and its anatomy is special and complex because of the dural ring, connective tissues, venous plexus, sympathetic nerves, and important arterial branches, such as the ophthalmic artery. An aneurysm ruptures and bleeds in the ophthalmic artery will cause dysfunctions of the eye and the neighboring tissues. At present, the risk of rupture of aneurysms in the siphon were rarely explored in previous studies. In this study, we compared the morphological characteristics of unruptured and ruptured aneurysms in the siphon of the internal carotid artery, explored the risk factors for rupture, and provided valuable references for clinical interventions and the selection of the timing of treatment.

Clinical data

We retrospectively analyzed 156 patients with aneurysms of the siphon of the internal carotid artery (171 aneurysms in total) diagnosed by volume computed tomographic digital subtraction angiography (VCTDSA) from June 2017 to December 2022, including 107 patients (120 aneurysms) in the unruptured group and 49 patients (51 aneurysms) in the ruptured group. There were 45 males and 111 females, aged 33–85 years, with a mean age of 57.84 ± 10.48 years. The inclusion criteria were as follows: ① ruptured aneurysm group: patients with subarachnoid hemorrhage clearly diagnosed by cranial CT(Computed tomography)and intracranial aneurysm by VCTDSA; ② unruptured aneurysm group༚patients with intracranial aneurysm clearly diagnosed by VCTDSA and not ruptured. The exclusion criteria were as follows: ① poor image rendering due to artifacts such as metal or motion; ② unable to clearly diagnose rupture; ③ combined with other vascular diseases; ④ traumatic and infected aneurysms. The ethics approval was shown in the declaration.

Examination method

The patients with the supine position, were first tested by the small-dose mass injection method and then scanned in the order of head and neck VCTDSA by a GE Discovery HD750 CT. The scanning parameters were as follows: tube current 250–450 mA, scanning tube voltage 100 kV, enhancement voltage 120 kV, layer spacing and layer thickness 5 mm, field of view from 20 cm×20 cm to 24 cm×24 cm, and pitch 0.969. The reconstructed layer thickness of the raw data is 0.625mm. Iopromide contrast agent (370 mgI/mL) was injected into the elbow vein, followed by saline, both at a flow rate of 4.0 mL/s. The contrast agent dosages for CT angiography (CTA) examination and the small-dose regiment test were 45.0–55.0 mL and 4.0 mL, and the saline dosages were 40.0 mL and 15.0 mL, respectively ^[3].

Image post-processing and analysis

The VCTDSA images were first received by a GE AW4.6 workstation, and the subtraction images were post-processed by the same operator using Add/Sub software. Post-processing techniques such as volumetric reproduction (VR) and multiplanar reconstruction (MPR) were utilized to display the aneurysm and siphon in multiple directions and angles and to determine and measure the morphological indices of the aneurysm and siphon.

The results were analyzed by 2 experienced imaging physicians using the double-blind method, and the results were discussed and agreed upon. In case of a disagreement, a third physician with higher seniority was asked to make the final judgment. Morphological indices of siphon aneurysms and internal carotid siphon were observed and measured, including the location of siphon aneurysms (cavernous sinus, clinoid, and ophthalmic segments) in the unruptured and ruptured groups, as shown in Fig. 1; the shape of the aneurysms (saccular, vertebral/hemispherical, irregular, and pike shaped), as shown in Fig. 2; the morphology of the siphon of the internal carotid artery (C-, S-, U-, and V-shape), as shown in Fig. 3; and the parent-daughter angle (angle of the median line between proximal and distal arteries), the inflow angle (the angle between the midline of the proximal artery and the maximum diameter of the aneurysm past the midpoint of the neck), and the inclination angle (Angle between the horizontal line of the aneurysm neck and the maximum aneurysm length through the center of the aneurysm neckline), see Fig. 4; size (aneurysm length and diameter), width (W), height (H), aneurysm neck, maximal diameter (maximal length of the intra-aneurysm connecting line at any two points), AR (Aspect ratio), SR (Size ratio), aneurysm height/width (H/W), Aneurysm width/neck width, Mean diameter of aneurysm-carrying artery (mean of the sum of proximal and distal aneurysm-carrying arteries), and S1/S2 (aneurysm width×aneurysm length/neck width×average value of the carrier artery).

Statistical analysis

The data were analyzed statistically by SPSS2.0. The counting and measuring data were expressed as percentages and xˉ±s, respectively. The counting data were analyzed by the chi-square test; The measuring data conforming to normal distribution were analyzed by the t-test, otherwise by the Mann⁃Whitney U-test, and measuring data with P < 0.05 were included in the analysis of ROC curves, and the maximum critical values corresponding to the sensitivity and specificity of each indicator were calculated. Multi-factorial logistic regression was used to analyze the independent risk factors for the rupture of internal carotid siphon aneurysms.

Comparison of basic clinical data between patients with aneurysms in the unruptured and ruptured groups

The patients in the ruptured group was younger than the unruptured group, and had higher-incidence of multiple aneurysms than the unruptured group, both with statistically significant differences between the groups (P < 0.05). There was no statistically significant difference in the gender ratio and the incidence of single aneurysms between the two groups (P > 0.05). Table 1 displayed the details.

Table 1

Comparison of Basic Clinical Data between Patients with Aneurysms in the Unruptured and Ruptured Groups
Clinical variables	Ruptured(n = 49)	Unruptured(n = 107)	χ²/t/Z Value	P Value
Age (years)	55.64 ± 9.22	59.78 ± 12.36	-2.51	0.012*
Number of aneurysms, n (%)
Single aneurysm	35(71.4)	90(84.1)	0.848	0.447
Multi aneurysms	14(28.6)	17(15.9)	4.484	0.034*
Genders, n(%)			0.432	0.511
Male	12(24.5)	33(30.8)
Female	37(75.5)	74(69.2)
: P<0.05*

Comparison of morphological indices of aneurysms in the unruptured and ruptured groups

The incidence of vertebral or hemispheric aneurysms and aneurysm clinoid segment in the unruptured group was significantly higher than that in the ruptured group, and the aneurysm parent-daughter angle in the unruptured group was larger than that in the ruptured group, with the differences being statistically significant (P < 0.05). In the ruptured group, the incidence of irregular aneurysms and ophthalmic segment aneurysms was higher in the ruptured group than in the unruptured group. The incidence of aneurysm size, width, height, aneurysm neck, AR, SR, S1/S2, aneurysm width/neck width, maximal diameter, inclination angle, and inflow angle were greater in the ruptured group than in the unruptured group, and the differences were statistically significant (P < 0.05). The four morphologies of siphon section, saccular and pike-shaped aneurysms, aneurysm cavernous sinus segment, side of the aneurysm, average diameter of the aneurysm-carrying artery, aneurysm height/width ratio and other indicators between the two groups were not statistically significant (P > 0.05). Table 2 is shown the details.

Table 2

Comparison of Morphological Indices of Aneurysms in the Unruptured and Ruptured Groups
Clinical variables	Ruptured (51)	Unruptured (120)	χ²/t/Z Value	P Value
Tortuous shape of siphon, n(%)
U	33(64.7)	77(64.2)	0.002	0.966
V	11(21.6)	22(18.3)	0.138	0.711
C	2(3.9)	3(2.5)	—	0.632
S	5(9.8)	18(15.0)	0.562	0.453
Shape of aneurysms, n(%)
Saccular	17(33.3)	31(25.8)	0.848	0.357
Pike shaped	2(3.9)	3(2.5)	---	0.632
Vertebral/Hemispherical	16(31.4)	79(65.8)	16.268	<0.001
Irregular	16(31.4)	7(5.8)	20.297	<0.001
Side, n(%)
Left	28(54.9)	70(58.3)	0.128	0.72
Right	23(45.1)	50(41.7)	0.124	0.7
Location, n(%)
Cavernous sinus	0	9(7.5)	3.985	0.059
Clinoid	3(5.9)	21(17.5)	4.62	0.039
Ophthalmic	48(94.1)	90(75)	9.191	0.002
Size, mm	7.88 ± 6.77	2.84 ± 1.50	-5.17	<0.001
Width, mm	6.88 ± 6.28	3.14 ± 1.63	-3.58	<0.001
Height, mm	7.52 ± 6.38	2.76 ± 1.49	-5.32	<0.001
Aneurysm neck, mm	4.92 ± 2.53	3.57 ± 1.19	-3.14	0.002
Mean diameter of aneurysm-carrying artery, mm	3.56 ± 0.67	3.81 ± 0.57	1.61	0.207
Maximal diameter, mm	9.42 ± 7.41	3.99 ± 1.69	-4.75	<0.001
Aspect ratio (AR)	1.52 ± 1.04	0.81 ± 0.33	-3	0.003
Size ratio (SR)	2.28 ± 1.94	0.80 ± 0.49	-4.19	<0.001
S1/S2(area ratio)	4.20 ± 6.90	0.75 ± 0.73	-5.02	<0.001
Aneurysm width/neck width	1.31 ± 0.83	0.86 ± 0.22	-3.13	0.002
Aneurysm height/width	1.26 ± 1.04	0.93 ± 0.29	-0.29	0.77
Parent-daughter angle,°	131.39 ± 17.50	139.99 ± 20.59	-3.19	0.001
Inclination angle, °	92.40 ± 19.68	80.37 ± 19.20	-4.66	<0.001
Inflow angle,°	106.82 ± 19.79	89.72 ± 14.56	7.54	0.007
—: Fisher's exact test, no test value

ROC curves of numerical variables for internal carotid siphon aneurysms

The ROC curve analysis (Fig. 5) showed that the areas under the ROC curves (AUC) for AR, SR, area ratio (S1/S2), maximum diameter, size, width, height, parent-daughter angle, inflow angle, and angle of inclination were 0.648, 0.707, 0.748, 0.734, 0.755, 0.677, 0.762, 0.343, 0.763, and 0.730, respectively. The critical values for maximum sensitivity and specificity were 1.541, 1.578, 2.142, 6.850, 5.517, 5.35, 4, 136.817°, 95.817°, and 92.433°, respectively.

Multi-factorial Logistic Regression Analysis of Independent Risk Factors for Rupture of Internal Carotid Siphon Aneurysm

The variables with statistically significant differences in the univariate analysis were included in the multifactorial logistic regression analysis. The results (Table 3) showed that size (OR = 12.607, 95% CI = 4.400-36.124, P < 0.001), angle of inclination (OR = 4.062, 95% CI = 1.570-10.513, P = 0.004), and multiple aneurysms (OR = 4.274, 95% CI = 1.620-11.272, P = 0.003) were independent risk factors for the rupture of internal carotid siphon aneurysms.

Table 3

Multifactorial Logistic Regression Analysis of Internal Carotid Siphon Aneurysms
Clinical variables	OR	95%CI	P Value
Size	12.607	4.400 ~ 36.124	<0.001
Inclination angle	4.062	1.570 ~ 10.513	0.004
Multi aneurysms	4.274	1.620 ~ 11.272	0.003

Some researchers combined the direction of blood flow in the internal carotid artery and proposed a more accurate classification of the internal carotid artery, dividing the internal carotid artery into segments from C1 to C7, and defining the cavernous sinus segment (C4), the clinoid segment (C5), and the ophthalmic segment (C6) collectively as the siphon ^[4]. Anatomically, the C4 segment begins at the upper edge of the ligamentum teres and ends at the proximal dural ring, which is an extradural structure, and the clinoid segment (C5 segment) begins at the proximal dural ring and ends at the distal dural ring, which is still an intradural structure ^[5]. The risk of rupture of the siphon varies depending on the relationship of each segment to the dural ring. In the univariate analysis of this study, the difference between the clinoid and ophthalmic segment aneurysms was statistically significant in the middle of the unruptured and ruptured groups, whereas the difference between the cavernous sinus segment aneurysms was not statistically significant. The analysis of more than 20 morphologic indicators finally concluded that aneurysm inclination angle, size, and multiple aneurysms were independent risk factors for rupture.

Angle of inclination

The aneurysm inclination angle is the angle between the horizontal line of the aneurysm neck and the maximum aneurysm length through the center of the aneurysm neck line. Tan et al[6] concluded that the inclination angle of ruptured aneurysms was greater than that of unruptured aneurysms, Simultaneously, they found that the greater the angle of inclination, the lesser the distance of the main branch from the daughter vessels in a straight line, and the steeper the turn of the main vessel to the daughter vessels, which may result in deviation from the impingement position of the blood flow on the vessel wall. This deviation leads to changes in wall shear stress (WSS) and spatial wall shear stress gradient (WSSG). Miyata et al[7] showed a significant linear positive correlation between the aneurysm inflow rate coefficient (AIRC) and aneurysm inclination angle (γ) and suggested that a greater inclination angle affects the hemodynamic milieu and leads to aneurysm growth. The inclination angle may be the most important predisposing factor for aneurysm rupture, and it is very different in unruptured and ruptured aneurysms[8]. In the present study, the AUC for inclination angle was 0.730, and its specificity and sensitivity corresponded to a critical value of 92.433°at maximum. The multifactorial logistic regression analysis also suggested that inclination angle was an independent risk factor for rupture of aneurysms in the siphon. The authors consider that the difference in the critical value of the inclination angle between the results of this study and those of foreign studies may be due to the large individual differences in the siphon, with different the inclination angles measured for different siphon morphologies. In addition, foreign studies focused more on aneurysms in all intracranial sites, whereas the present study targeted siphon aneurysms.

Multiple aneurysms

Some scholars believe that the patients with multiple aneurysms tend to have more risk factors contributing to the occurrence and development of aneurysms, and the rupture of aneurysms. Therefore, with the increase in the number of aneurysms, the total risk of rupture will naturally continue to increase [9]. Korja et al. [10] followed 1993 consecutive patients and found that 30% of patients with subarachnoid hemorrhage had multiple aneurysms, and there were significantly more females than males. Sonobe et al. [11] studied unruptured small aneurysms < 5 mm in diameter and showed that multiple aneurysms were an important predictor of rupture of small aneurysms, and the risk of rupture of multiple aneurysms was three times higher than that of a single aneurysm, probably due to the fact that the multiple aneurysms have a different biological shape and growth pattern than single aneurysm. IF a patient has a history of hypertension, is younger than 50 years of age, and has multiple aneurysms ≥ 4 mm in diameter, treatment should be considered to prevent rupture of the aneurysm. Some investigators have suggested that ruptured aneurysms among intracranial multiple aneurysms exhibit the lowest mean wall shear stress and the highest oscillatory shear stress and that unstable blood flow can be detected based on an increase in oscillation velocity [12]. The results of the multifactorial regression analysis in this study also suggested that multiple aneurysms were an independent risk factor for rupture, with one rupture located in the clinoid segment of the internal carotid artery and the rest in the ophthalmic segment, and the risk of rupture of multiple aneurysms was 4.274 times higher than that of single aneurysms.

Size of the aneurysm

Aneurysm size is defined by measuring the length and diameter of the aneurysm. There are many studies on aneurysm size at home and abroad. Many studies indicated that the risk of rupture increases with the size of the aneurysm, and that aneurysms with a diameter exceeding 7 mm have a significantly higher risk of rupture. [13–14]. UCAS et al. [13] used aneurysms with a diameter of 3–4 mm as a control, and aneurysms with diameters of 5–6 mm, 7–9 mm, 10–24 mm, and ≥ 25 mm had risk ratios of 1.13, 3.35, 9.09, and 76.26, respectively. Juvela et al. [14] found that aneurysm size was an important determinant of aneurysm rupture in a multifactorial analysis of 142 aneurysm patients followed up over a long period of time. Inagawa et al. [15] concluded that the larger the aneurysm, the worse the World Federation of Neurological Surgery Societies (WFNS) score was, and the risk of rebleeding was higher in patients with larger aneurysms (≥ 10 mm) than in those with smaller ones (< 10 mm). A recent study used the Predictive Model for Aneurysm Rupture Risk Score (PHASES score), a composite of seven factors: aneurysm size, history of subarachnoid hemorrhage, hypertension, age, location and geographic region of the aneurysm, and aneurysm morphology, with aneurysm size accounting for a larger portion of the score. The aneurysm with higher the total composite score have higher the risk of rupture. They also found that aneurysm size was the only PHASES score variable independently related to growth and growing aneurysms were more than 30 times more likely to rupture than stable aneurysms [16]. The mean size of ruptured aneurysms in most studies was approximately 7 mm [17], similar to the mean size of ruptured aneurysms in the siphon of 7.88 mm in the present study.

In summary, this study suggests that the risk of aneurysm rupture should be emphasized in patients with multiple aneurysms in ophthalmic or clinoid segments, sizes greater than 5.517 mm, and inclination angles greater than 92.433°. Meanwhile, when comparing the unruptured group with the ruptured group, this study covered most of the validated morphological indices at home and abroad, added the morphology of the siphon, and subdivided the siphon segments (cavernous sinus segment, bed-surge segment, and ophthalmologic segment) for the sake of precision. The final results showed that the aneurysm size, angle of inclination, and multiple aneurysms were independent risk factors for rupture. However, the small sample size of this study may explain the lower rupture rate of aneurysms in the siphon compared with other sites, which needs to be further confirmed in a large, multicenter, and prospective study. In addition, further innovations are needed in the study of morphological indicators of aneurysm rupture, and new indicators should be explored to predict the risk of rupture more accurately.

Consent for publication
No applicable.

Competing interests
All of authors have no competing interests

Ethics approval

This study that involved patient records, images or biological samples was approved by the ethics committee of the Hospital of Traditional Chinese Medicine in Qijiang District, Chongqing municipality (No.28) and was conducted by the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Funding

This work was supported by the medical research Key Program of the conbination of Qijiang District Health Commission and Qijiang District Science and Technology Bureau,China (No.2023106)

Author Contribution

ZH contribute to the protocol design. RL conducted data analysis and prepared the tables. ZW and GX helped to draft manuscript. All authors reviewed the manuscript.

Acknowledgments

During my postgraduate studies, some of the data in this article were obtained from the First Hospital of Chongqing Medical University, for which I would like to express my gratitude once again.

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You are reading this latest preprint version

The morphological characteristics and risk of rupture of ruptured and unruptured internal carotid siphon aneurysms: a preliminary study

Status:

Version 1

Abstract

Objective

Methods

Results

Conclusions

Figures

Background

Methods

Clinical data

Examination method

Image post-processing and analysis

Statistical analysis

Results

Comparison of basic clinical data between patients with aneurysms in the unruptured and ruptured groups

Comparison of morphological indices of aneurysms in the unruptured and ruptured groups

ROC curves of numerical variables for internal carotid siphon aneurysms

Multi-factorial Logistic Regression Analysis of Independent Risk Factors for Rupture of Internal Carotid Siphon Aneurysm

Discussion

Angle of inclination

Multiple aneurysms

Size of the aneurysm

Conclusions

Declarations

Consent for publication
No applicable.

Competing interests
All of authors have no competing interests

Ethics approval

Funding

Author Contribution

Acknowledgments

References

Additional Declarations

Status:

Version 1

The morphological characteristics and risk of rupture of ruptured and unruptured internal carotid siphon aneurysms: a preliminary study

Status:

Version 1

Abstract

Objective

Methods

Results

Conclusions

Figures

Background

Methods

Clinical data

Examination method

Image post-processing and analysis

Statistical analysis

Results

Comparison of basic clinical data between patients with aneurysms in the unruptured and ruptured groups

Comparison of morphological indices of aneurysms in the unruptured and ruptured groups

ROC curves of numerical variables for internal carotid siphon aneurysms

Multi-factorial Logistic Regression Analysis of Independent Risk Factors for Rupture of Internal Carotid Siphon Aneurysm

Discussion

Angle of inclination

Multiple aneurysms

Size of the aneurysm

Conclusions

Declarations

Consent for publication No applicable.

Competing interests All of authors have no competing interests

Ethics approval

Funding

Author Contribution

Acknowledgments

References

Additional Declarations

Status:

Version 1

Consent for publication
No applicable.

Competing interests
All of authors have no competing interests