Accepted Manuscript

Morphological Risk Factors for Rupture of Small (<7 mm) Posterior Communicating
Artery Aneurysms
Nan Lv, Zhengzhe Feng, Chi Wang, Wei Cao, Yibin Fang, Christof Karmonik, Jianmin
Liu, Qinghai Huang
PII:

S1878-8750(15)01759-3

DOI:

10.1016/j.wneu.2015.12.055

Reference:

WNEU 3552

To appear in:

World Neurosurgery

Received Date: 1 September 2015

Revised Date:

14 December 2015

Accepted Date: 16 December 2015

Please cite this article as: Lv N, Feng Z, Wang C, Cao W, Fang Y, Karmonik C, Liu J, Huang Q,
Morphological Risk Factors for Rupture of Small (<7 mm) Posterior Communicating Artery Aneurysms,
World Neurosurgery (2016), doi: 10.1016/j.wneu.2015.12.055.
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Morphological Risk Factors for Rupture of Small (<7 mm) Posterior

Communicating Artery Aneurysms
Nan Lv1*, Zhengzhe Feng1*, Chi Wang1, Wei Cao1, Yibin Fang1, Christof

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Karmonik2, Jianmin Liu1, Qinghai Huang1

Affiliation: 1. Department of Neurosurgery, Changhai Hospital, Second Military
Medical University, Shanghai, China; 2. Cerebrovascular Center, Department of

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Neurosurgery, Houston Methodist, Houston, Texas

*Nan Lv and Zhengzhe Feng contributed equally to this work and should be regarded

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as co-first authors

Nan Lv, M.D. (lvnan2008@163.com); Zhengzhe Feng, M.D. (shchfzz@163.com);

Chi Wang, M.D. (watch_2008@163.com); Wei Cao, M.D. (1023122590@qq.com);
Yibin

Fang,

M.D.

(fangyibin@ip.163.com);

Christof

Karmonik,

PhD

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(CKarmonik@houstonmethodist.org); Jianmin Liu, M.D. (chstroke@163.com);

Qinghai Huang, M.D. (ocinhqh@163.com)
Corresponding authorQinghai Huang

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Mailing address: Department of Neurosurgery, Changhai Hospital, Changhai Road

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168, Shanghai, 200433, China

Email: ocinhqh@163.com
Phone: +86 21-31161784
Fax: +86 21-31161784

Funding: National Natural Science Foundation of China (No. 81571118 and No.
81301004) and Shanghai Education Commission Innovation Fund (No. 14ZZ081).
Keywords: intracranial aneurysm; posterior communicating artery; morphology;
rupture

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Abstract
Background: The management of small unruptured intracranial aneurysms is still
controversial. Given the distinctive natural history of aneurysm at different locations,

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location-specific analysis might be a reasonable approach. This study aimed to

investigate morphological discriminators for rupture status by focusing on only
posterior communicating artery (PcomA) aneurysms smaller than 7 mm.

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Methods: In 108 small PcomA aneurysms (68 ruptured, 40 unruptured), clinical and
morphological characteristics were compared between the ruptured and unruptured

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groups. Multivariate logistic regression analysis was performed to determine the

independent predictors for the rupture status of small PcomA aneurysms.
Results: None of the clinical characteristics were significantly different between the
ruptured and unruptured group (P>0.05). The ruptured group revealed a significantly

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larger size (P=0.009), aspect ratio (P=0.009), size ratio (P=0.002), dome-to-neck ratio
(P=0.002), inflow angle (P<0.001) and proportion of bleb formation (P=0.039).
Bottleneck factor (P=0.154), diameter of PcomA (P=0.302) and fetal-type PcomA

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(P=0.832) showed no significance. With multivariate analyses, size ratio (P=0.012)

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and inflow angle (P=0.001) were shown to be independently associated with the
rupture status of small PcomA aneurysms.
Conclusions: Morphological characteristics were closely related with the rupture
status of small PcomA aneurysms. Size ratio and inflow angle were independent risk
factors for rupture and might be useful in clinical risk stratification of small PcomA
aneurysms.

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Introduction
Unruptured intracranial aneurysms (IAs) are increasingly detected, and the
majority of them are small16,22. Although the International Study of Unruptured

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Intracranial Aneurysms (ISUIA) trial reported that the rupture rate of unruptured IAs
smaller than 7 mm is very low23, a recent prospective Finnish cohort study showed
that 25% of the patients with small (<7 mm) unruptured IAs had an aneurysmal

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subarachnoid hemorrhage (SAH) during a lifelong follow-up13. Thus, the

effectiveness of aneurysm size as a predictor for rupture remains controversial.

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Moreover, the correlation between IA rupture with their location has been revealed by
various studies6,8. Compared with other locations, the posterior communicating artery
(PcomA) and the anterior communicating artery had a higher incidence of ruptured
aneurysms6. Meanwhile, the percentage of small aneurysms in PcomA aneurysms was
particularly high7. Considering the potential risks of therapy, clinical decision-making

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for unruptured PcomA aneurysms, especially for those smaller than 7 mm, is difficult.
Therefore, in this study, we reviewed the clinical and morphological characteristics of

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small PcomA aneurysms (<7 mm) in a single institution to screen for the possible

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predictors of their rupture.

Materials and Methods

Ethics Statement

The Institution Review Board of the Second Military Medical University

affiliated to Changhai Hospital approved this retrospective study, and the requirement
for informed consent was waived. The patients information was anonymized and

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de-identified prior to analysis.
Patients and Clinical Characteristics
We retrospectively reviewed a total of 135 consecutive patients diagnosed with

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PcomA aneurysms between January 2014 and June 2015 at Changhai Hospital. All the
PcomA aneurysms were determined and measured using three-dimensional rotational
angiography (3DRA). After exclusion of patients with multiple aneurysms and

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PcomA aneurysms larger than 7 mm, 108 PcomA aneurysms were included in the
study. Of these PcomA aneurysms, 68 were ruptured with a history of SAH and 40

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were unruptured. For the 40 patients in the unruptured group, 14 presented with mild
headache or dizziness, 7 suffered from ischemic events, 8 presented with symptoms of
oculomotor nerve palsy, and the other 11 aneurysms were detected incidentally
without symptoms of cerebrovascular diseases. The clinical characteristics were

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collected as the following: age, gender, hypertension, diabetes mellitus, current

smoking status, history of familial SAH, and presence of homolateral oculomotor
nerve palsy. Hypertension was defined as taking antihypertensive agents, a systolic

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blood pressure of 140 mmHg, or a diastolic blood pressure of 90 mmHg. Diabetes

mellitus was defined as taking antidiabetic agents, treatment with insulin injections, a

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fasting plasma glucose level of 126 mg/dl, a random plasma glucose level of > 200
mg/dl, or a hemoglobin A1c level of 6.5%. Current smoker was defined as those
who had smoked at least 100 cigarettes during their lifetime and reported smoking
every day or some days before being admitted.
Radiological Findings and Morphological Calculations
The 3DRA was performed using the Artis zee Biplane angiographic system
(Siemens, VC14, Germany). All of the acquired 3DRA data were transferred to the

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syngo X Workplace (Siemens, VB15, Germany) for reconstruction of the 3D internal
carotid artery vessel tree and exported in a stereolithography (STL) format to
GEOMAGIC STUDIO 9.0 software (Geomagic, Morrisville, North Carolina). Firstly,
we defined the neck plane as the location where the aneurysmal sac pouched outward

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from the parent vessel. After that, the models were divided into the aneurysm dome
and the inlet and outlet planes of the parent artery, and then exported in STL formats.
These formats were imported into Matlab 7.0 (The MathWorks, Inc., Natick, MA,

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USA), which was used to calculate and visualize the morphological parameters.

Through the above process, we could obtain the morphological parameters of the

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PcomA aneurysms as defined in previous studies4,25 (Figure 1). Size of aneurysm

dome was defined as the maximum diameter of the aneurysm dome. Dome height was
the longest dimension from the neck to the dome tip and dome width were measured
perpendicular to the dome height. Aspect ratio (AR) was computed by dividing dome

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height by neck width. Size ratio (SR) was calculated by dividing size by the average
diameter of parent arteries and dome-to-neck ratio (DN) by dividing size by neck

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width. Bottleneck factor (BN) was defined as the ratio of dome width to neck width.
Inflow angle was the angle between inflow and the aneurysms main axis from the

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center of the neck to the tip of the dome. In addition, we evaluated the presence of
bleb formation on the aneurysms and whether the PcomA was fetal type. A fetal-type
PcomA was defined as a PcomA that has the same or larger caliber as the P2 segment
of the posterior cerebral artery, and is associated with an atrophic P1 segment.
Statistical Analysis
Statistical analyses were performed using Microsoft Excel 2003 and SAS
9.1(SAS Institute Inc., Cary, NC, USA). Variables were expressed as median

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(interquartile range), or number of patients (%) as appropriate. Mann-Whitney U-test
was used for measurement data and the chi-square test was performed for
cross-tabulation. The parameters found to be significant (P<0.05) in univariate
analysis were further analyzed using multivariate logistic regression (backward

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elimination) to identify those that retained significance when accounting for all

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relevant parameters. P<0.05 (two sided) was the criterion for statistical significance.

Results

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Univariate Analysis

The baseline and morphological characteristics of the 108 small PcomA

aneurysms are shown in Table 1. The patients ages ranged from 42 to 82, with a

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median age of 60 years. Twenty-four were males and 84 were females. No baseline
variables included in this study showed significant difference (P>0.05), which
indicated that the morphological characteristics of the 2 groups were comparable.

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The size of PcomA aneurysms ranged from 1.23 to 6.84 mm, with a median size
of 4.36 mm. The ruptured PcomA aneurysms were proved to have a significantly

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larger size (P=0.009), AR (P=0.009), SR (P=0.002), DN (P=0.002), and inflow angle

(P<0.001). Bleb formation was observed in a significantly higher proportion of the
ruptured PcomA aneurysms (P=0.039). Other morphological characteristics, including
diameter of PcomA (P=0.302), BN (P=0.154) and fetal-type PcomA (P=0.832) were
revealed to have no significance between the ruptured and unruptured groups.
Multivariate Analysis
Multivariate logistic regression was performed to identify the independent risk

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factors of small PcomA aneurysms rupture using a backward elimination process. All
the significant parameters that were significant in univariate analysis were included.
The result showed that SR (Odds ratio [OR]: 1.67; 95% confidence interval [CI]:
1.12-2.50; P=0.012) and inflow angle (OR: 2.01; 95%CI: 1.32-3.05; P=0.001) were

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independently associated with the rupture status of small PcomA aneurysms (Table

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2).

Discussion

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With the wider availability of modern imaging techniques, patients with

unruptured IAs are increasingly detected, even with small asymptomatic ones16.
Previous studies revealed that the size of IA was significantly correlated to their
rupture status, and the risk of unruptured IAs smaller than 7 mm was relatively low8,23.

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For small IAs in the anterior circulation, the predicted risk of rupture may be even
lower than the risk of treatment complications9. However, according to studies
depending on the locations, rupture of small anterior circulation aneurysms was the

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main cause of aneurysmal SAH, which carries a high rate of mortality and

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morbidity2,3,11,17. As a result, clinical decision-making for small unruptured IAs is still

difficult for physicians, and reliable predictors for rupture risk are much needed.
Various attempts have been made to stratify the rupture risk of intracranial

aneurysms5,15. Currently, several clinical, hemodynamic and morphological variables,

including familial SAH history, aneurysm size, and low wall shear stress (WSS), have
been consistently associated with an increased risk of aneurysm rupture8,22,24.
However, these findings were obtained by analysis of a limited number of parameters
with a relatively small sample size. Furthermore, most of these studies were not

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location-specific. In fact, the proportion of small aneurysms and their risk of rupture
varies in different locations6,10. The anatomic geometry, vessel wall thickness, and
blood flow pattern of IAs in different locations are distinctive. This might be the

be more likely to achieve accurate results.

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reason why some findings are conflicting. As a result, location-specific studies may

Without considering location, IA size loses relevance to rupture risk6,11. In this

study, although the aneurysm size of the ruptured group was significantly larger than

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that of the unruptured group, it was not retained as an independent risk factor that

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discriminated the rupture status of PcomA aneurysms. The variability of the rupture
risk might be related to the caliber of the originating or parent vessel. SR, a parameter
firstly proposed by Dhar et al4, which incorporates the IA parent vessel geometry into
a morphological index, had been shown to be related with aneurysm rupture in some
previous studies12,14. Kashiwazaki et al12 demonstrated that SR could accurately

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predict the rupture risk of UIAs, especially small aneurysms (<5 mm). In another
prospectively designed study, Rahman et al18 also confirmed the correlation between

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SR and aneurysm rupture status. In the current study, our results indicated SR as an
independent risk factor for rupture of small PcomA aneurysms.

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Hemodynamics is believed to play an important role in the growth and rupture of

IAs5,24. Former hemodynamic studies indicated that the flow pattern inside the
aneurysm dome was determined by the relationships between the aneurysm dome and
its parent vessels to some extent1,20. In aneurysms with higher SR, more complex flow,
multiple vortices, and lower aneurysmal wall shear were observed. This
hemodynamic pattern was thought to be associated with rupture of IAs20. Besides SR,
which represents the size relationship between the aneurysm dome and its parent
artery, the inflow angle might reflect the spatial relationship between them. Several

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studies have confirmed the significant role of inflow angle in predicting aneurysm
rupture1,21. In our study, increasing inflow angle was highly correlated with rupture
status of PcomA aneurysms. From the point of view of hemodynamics, increasing
inflow angle might result in higher inflow velocity and greater wall shear stress

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magnitude and spatial gradients in the inflow zone and dome, as well as a greater
transmission of kinetic energy into the distal portion of the dome1. These
hemodynamic features might be important factors that increase the risk of rupture.

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Most morphological studies of rupture risk, including the current one, are based

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on the comparison between post-ruptured and unruptured aneurysms. We know that

the analysis of aneurysms in pre-rupture status might be more accurate due to the
possible change of morphology after rupture. Several studies have reported some rare
cases with radiographic records not long before rupture5,19. However, it is difficult to
capture the specific status clinically to gain a considerable sample size for accurate

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statistical analysis. Therefore, currently, comparisons between post-ruptured and

unruptured IAs are used as an available alternative method, which could still provide

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Limitations

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meaningful findings for clinicians to discriminate rupture status of IAs.

In the current study, we identified SR and inflow angle as independent risk

factors for rupture of small PcomA aneurysms, which are convenient and quick
measurements for the clinical prediction of aneurysm rupture. The study does have
several limitations. Firstly, as a retrospect study, there was an inherent bias selection
of the PcomA aneurysms, especially as it did not include aneurysms larger than 7 mm.
In addition, the relatively small and unbalanced sample size of both groups might

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affect the analysis. Due to the limited sample size, we only used several most widely
studied parameters to ensure the reliability of the multivariate analysis. Finally,
morphology of the PcomA aneurysms might change after aneurysm rupture, which

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could affect the accuracy of calculations.

Conclusions

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This study showed that not only the aneurysm size, but also SR, AR, DN, inflow
angle and bleb formation were significantly different between ruptured and

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unruptured small PcomA aneurysms. Most importantly, this is the first demonstration
that SR and inflow angle are independent factors for predicting the rupture risk of

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small PcomA aneurysms.

Competing Interests

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None.

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Acknowledgement

We gratefully acknowledge the Shanghai Supercomputer Center for its helpful

provision of calculation software. This study received funding from National Natural
Science Foundation of China (No. 81571118 and No. 81301004) and Shanghai
Education Commission (No. 14ZZ081).

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Figure Legend
Figure 1. Definitions of Morphological Parameters. Size = Dmax; aspect ratio =
Height/Neck; size ratio = 6Dmax/(D1+D2+D3+D4+D5+D6); diameter of PcomA =

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(D5+D6)/2; dome-to-neck ratio = Dmax/Neck; bottleneck factor=Width/Neck; inflow

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angle=.

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Table 1 Clinical and Morphological Characteristics of Small PcomA Aneurysms

PcomA aneurysms
Variables

Total (n=108)

Ruptured (n=68)

Unruptured (n=40)

P Value

Age

60 (52, 66)

58 (51, 63)

Male

24 (22.2)

13 (19.1)

Hypertension

53 (49.1)

31 (45.6)

Diabetes Mellitus

11 (10.2)

4 (5.9)

Current Smoking

17 (15.7)

9 (13.2)

8 (20.0)

0.351

9 (8.3)

5 (7.4)

4 (10.0)

0.904

Oculomotor Nerve Palsy

62 (56, 67)

0.056

11 (27.5)

0.312

22 (55.0)

0.345

7 (17.5)

0.054

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Familial SAH

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Clinical Characteristics

18 (16.7)

10 (14.7)

8 (20.0)

0.476

Size, mm

4.36 (3.23, 5.47)

4.50 (3.60, 5.696)

3.92 (2.46, 4.72)

0.009

Diameter of PcomA

1.84 (1.27, 2.25)

1.80 (1.11, 2.18)

1.99 (1.53, 2.50)

0.302

Aspect Ratio (AR)

0.97 (0.75, 1.37)

1.08 (0.84, 1.37)

0.83 (0.66, 1.24)

0.009

1.61 (1.20, 1.94)

1.72 (1.30, 2.09)

1.42 (0.90, 1.77)

0.002

1.08 (0.91, 1.41)

1.16 (0.96, 1.59)

0.97 (0.86, 1.22)

0.002

1.13 (0.94, 1.35)

1.18 (1.01, 1.38)

1.09 (0.90, 1.32)

0.154

113 (98, 128)

119 (105, 132)

99 (89, 118)

<0.001

49 (45.4)

36 (52.9)

13 (32.5)

0.039

31 (28.7)

20 (29.4)

11 (27.5)

0.832

Size Ratio (SR)

Dome-to-Neck Ratio (DN)

Inflow Angle,
Bleb Formation

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Bottleneck Factor (BN)

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Morphological Characteristics

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Fetal Type PcomA

Variables are expressed as median (interquartile range), or number of patients (%)

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Table 2 Independent Risk Factors for Rupture of Small PcomA Aneurysms
P Value

Odds Ratio

95% Confidence Interval

Size Ratio (SR)

0.012

1.67

1.12-2.50

Inflow Angle

0.001

2.01

1.32-3.05

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Variables

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Morphological Risk Factors for Rupture of Small (<7 mm) Posterior

Communicating Artery Aneurysms

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Highlights:
We reviewed clinical and morphological characteristics of 108 small
PcomA aneurysms.

Morphology was proved to be closely related with rupture status of

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Size, AR, SR, DN, inflow angle and bleb formation were significant
parameters.

Size ratio and inflow angle were independent risk factors for

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aneurysm rupture

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PcomA aneurysms.

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Abbreviations list:
AR = aspect ratio
BN = bottleneck factor

DN = dome-to-neck ratio
IA = intracranial aneurysm
OR = odds ratio

SC

PcomA = posterior communicating artery

STL = stereolithography
WSS = wall shear stress

M
AN
U

SAH = subarachnoid hemorrhage

SR = size ratio

EP

TE
D

3DRA = three-dimensional rotational angiography

AC
C

RI
PT

CI = confidence interval

ACCEPTED MANUSCRIPT

Disclosure- Conflict of Interest

We declare that the manuscript is original, has not been published before and is not
currently being considered for publication elsewhere. We wish to confirm that there

RI
PT

are no known conflicts of interest associated with this publication and there has been
no significant financial support for this work that could have influenced its outcome.

AC
C

EP

TE
D

M
AN
U

SC

This manuscript has been read and approved by all named authors.