RESEARCH PAPER Neurologia i Neurochirurgia Polska

Polish Journal of Neurology and Neurosurgery

2020, Volume 54, no. 1, pages: 47–53
DOI: 10.5603/PJNNS.a2020.0007
Copyright © 2020 Polish Neurological Society
ISSN 0028–3843

Diagnostic value of non-enhanced computed tomography

in identifying location of ruptured cerebral aneurysm
in patients with aneurysmal subarachnoid haemorrhage
Marcin Sawicki1, Krzysztof Kościukiewicz1, Dariusz Jeżewski2, Kornel Chełstowski3, Piotr Gołofit1,
Michał M. Skoczylas1, Michał Gębka1, Kornelia Grabizna4, Katarzyna Kołaczyk1,
Łukasz Zwarzany1, Leszek Sagan2, Wojciech Poncyljusz1
1
Department of Diagnostic Imaging and Interventional Radiology, Pomeranian Medical University, Szczecin, Poland
2
Department of Neurosurgery, Pomeranian Medical University, Szczecin, Poland
3
Department of Laboratory Diagnostics, Pomeranian Medical University, Szczecin, Poland
4
Inter Medical Clinic, Kolobrzeg, Poland

ABSTRACT
Background. In patients with SAH and multiple aneurysms, the ruptured lesion must be identified to prevent recurrent
bleeding.
Aim of the study. To assess the diagnostic value of non-enhanced computed tomography (NECT) in identifying the rupture site
in patients with subarachnoid haemorrhage (SAH) and multiple aneurysms.
Material and methods. We included patients with SAH revealed by NECT and multiple aneurysms detected on computed to-
mography angiography (CTA) in whom a ruptured aneurysm was identified during neurosurgery. Two radiologists predicted the
location of the ruptured aneurysm based on the distribution of the SAH and location of intracerebral haematoma (ICH) by NECT.
Results. Eighty-three patients with a mean age of 55.7 ± 14.4 years were included. Ruptured aneurysms were significantly larger
(mean size 7.7 ± 4.7 mm) than unruptured aneurysms (mean size 5.9 ± 4.5 mm; p = 0.014). Interobserver agreement was 0.86
(p < 0.001). Overall sensitivity and specificity of radiological prediction were 78.3% (95% CI, 68.6%-87.1%) and 96.4% (95% CI, 94.3%-
97.8%) respectively. Overall PPV and NPV were 78.3% (95% CI, 67.6%-86.3%) and 96.8% (95% CI, 94.8%-98.1%) respectively. The
sensitivity and PPV for aneurysms in the anterior communicating, anterior, and middle cerebral arteries appeared to be significantly
higher than in other locations (p = 0.015 and 0.019 respectively). Analysis of independent predictive factors of correct radiological
location revealed that ICH predisposes to a correct radiological diagnosis with an odds ratio of 8.57 (95% CI, 1.07-68.99; p = 0.03).
Conclusions. NECT has a high diagnostic value in identifying the source of bleeding in patients with multiple aneurysms for
anterior circulation aneurysms, especially with coexisting ICH. For other locations, NECT is not reliable enough to base treatment
decisions upon.
Key words: intracranial aneurysm, multidetector computed tomography, observer variation, subarachnoid haemorrhage
(Neurol Neurochir Pol 2020; 54 (1): 47–53)

Introduction (up to 45% of all patients with intracranial aneurysms [1, 2])
is challenging. The correct identification of the ruptured aneu-
Endovascular or neurosurgical treatment of patients after rysm in cases of multiple aneurysms is of crucial importance,
subarachnoid haemorrhage (SAH) with multiple aneurysms not only in endovascular but also in surgically treated patients.

Address for correspondence: Marcin Sawicki, Department of Diagnostic Imaging and Interventional Radiology, Pomeranian Medical University, Szczecin,
Poland, e-mail: msaw@pum.edu.pl

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Neurologia i Neurochirurgia Polska 2020, vol. 54, no. 1

During open cranial surgery it is usually easy to identify the of Neurosurgery of our university hospital from March
ruptured aneurysm which should be clipped first, before the 2012 to November 2017. We included patients fulfilling the
remaining unruptured lesions. following criteria: NECT revealing SAH performed within
But in cases where multiple aneurysms cannot be rea- 24 hours of the onset of symptoms; multiple aneurysms
ched with one approach, correct localisation of the bleeding detected on CTA carried out immediately after the NECT;
aneurysm is needed. Endovascular therapeutic options are and ruptured aneurysms identified during neurosurgical
being used increasingly because the results of randomised treatment.
controlled trials indicate that endovascular coiling is associated The exclusion criterion was poor quality NECT or CTA
with a better outcome [3, 4]. However, endovascular therapy images not sufficient for reliable assessment.
may be associated with greater uncertainty as to whether
the bleeding aneurysm has been treated. In the presence of Non-enhanced CT protocol
multiple aneurysms, errors about the location of the ruptured NECT was carried out using Somatom Sensation 64 and
aneurysm can result in postoperative rebleeding. Therefore, Somatom Definition AS+ scanners (Siemens, Erlangen,
correctly identifying every ruptured lesion is crucial for tre- Germany). The scanning parameters were as follows: 120 kV,
atment planning. 380 mAs, range C1-C2 level to the vertex, FOV 220 mm and
Clinical signs can be helpful to locate the rupture site, matrix 512 × 512, collimation of 64×0.6 mm with a pitch of
but these are usually uncharacteristic and sometimes actually 1.2, slice thickness 5 mm, and slice increment 5 mm with
misleading. In the study by Nehls et al., clinical signs were Kernel H31s.
indicative in only 7% of patients [5].
The accuracy of digital subtraction angiography (DSA) or Image interpretation
magnetic resonance imaging (MRI) has also been assessed in NECT scans were assessed by a board-certified radiologist
several studies [6–9]. However, they showed poor reliability with 12 years of experience in neuroradiology (‘Radiologist 1’)
for DSA [6]. The accuracy of MRI has indicated that this and an uncertified radiology resident in the 4th year of training
technique is promising [7–9]. However, the application of (‘Radiologist 2’). They were blinded to each other’s findings,
MRI is limited due to insufficient availability, logistical chal- clinical data, the initial NECT report, the CTA results, and
lenges (including difficulty in scanning acutely ill patients), the findings of neurosurgery. The final decision concerning
predisposition to motion artifacts, patient compliance, long the predicted location of the ruptured aneurysm was reached
study time, contraindications, and cost. by consensus.
Routine diagnostic work-up of suspected SAH is usually As the aim of the study was limited to assessing solely the
based on non-enhanced computed tomography (NECT) and diagnostic value of NECT findings as predictors of aneurysmal
computed tomography angiography (CTA). rupture, NECT was analysed without knowledge of the distri-
The sensitivity of CTA in detecting cerebral aneurysms is bution of multiple aneurysms in CTA. Information regarding
high, and known to exceed 95%. However, in cases with multi- the locations of particular aneurysms already detected by CTA
ple aneurysms CTA reveals all lesions with high sensitivity, but would have biased our results.
usually leaves the key question unanswered i.e. which of them Location and extent of SAH was classified according
has ruptured? Therefore, to increase the diagnostic value of to the Hijdra scale that divides the subarachnoid space
CT in identifying the bleeding lesion, additional information into 10 compartments [12]. Each compartment was given
is required. We hypothesised that NECT could provide just 0-3 points according to the amount of blood: 0 = no blood;
such additional information. 1 = small amount of blood; 2 = partially filled with blood; and
Several previous studies analysing different features in 3 = completely filled with blood. This gave a minimum score
NECT as predictors of the rupture site have been equivocal of 1 and a maximum score of 30.
and provided divergent results [2, 5, 10, 11]. Both radiologists predicted the site of the ruptured an-
Therefore, the aim of the present study was to assess the eurysm based on the distribution of SAH and the location
diagnostic value of NECT in identifying the location of a rup- of the intracerebral haematoma (ICH) which was observed
tured cerebral aneurysm in patients with SAH and multiple in some cases.
aneurysms.
Reference method
Materials and methods Radiological prediction was verified by surgery as the
reference standard. The site of craniectomy and the surgical
Study participants approach was chosen after analysis of NECT and CTA findings
For this retrospective cohort study, the approval of by the neuroradiologist and neurosurgeon. CTA features
the local Bioethical Commission was obtained. Informed which were regarded as associated with rupture included
consent was waived. We reviewed the records of 256 pa- size, irregular shape, the presence of a nipple, focal spasm, or
tients with aneurysmal SAH treated in the Department focal mass effect.

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 Marcin Sawicki et al., Value of NECT in detecting ruptured aneurysm

During surgical treatment, the following findings were p = 0.014). ICH was detected in 25 (30%) cases. The mean
regarded as indications of an aneurysmal rupture: a healed Hijdra score was 17 ± 9 (range 1–30).
thrombotic cap over the top of the aneurysm, a localised clot Interobserver agreement between the two radiologists was
near the aneurysm, and very easy collapse (rupture) before very high; Kendall’s tau-b value was 0.86 (p < 0.001).
or after clipping. The presence of at least one of these features CTA revealed two aneurysms in 66 (80%) patients, three
was recognised as proof of aneurysmal rupture. in 16 (19%) patients, and four in one (1%) patient.
During the same surgical procedure, after clipping the Based on NECT, the radiologists predicted the location
ruptured aneurysm, all other accessible aneurysms were of the ruptured aneurysm correctly (i.e. in line with surgical
reached, confirmed as unruptured, and clipped if indicated. findings) in 65 of the 83 cases; hence, the sensitivity was 78.3%
(95% CI, 68.6% to 87.1%) (Fig. 1 and 2). Detailed results of
Data collection sensitivity, specificity, PPV and NPV are presented in Table 2.
Demographic data including age and gender was noted. Notably, the sensitivity for aneurysms located in the
The predicted location of the ruptured aneurysm and Hijdra anterior circulation (anterior cerebral artery [ACA], anterior
scale score were recorded by both radiologists. The location communicating artery [ACom], and middle cerebral artery
of the ruptured aneurysm identified during surgery was re- [MCA]) appeared to be significantly higher than in other
corded. The size of the ruptured aneurysm was measured on locations, including posterior circulation aneurysms: 92.3%
CTA retrospectively analysed after surgical treatment. The size (95% CI, 80.6% to 97.5%) vs. 56.7% (95% CI, 37.7% to 74.0%)
of an aneurysm was defined as its largest diameter. Both the with p = 0.015 (Chi-square).
two radiologists made three measurements of the aneurysm, We found overall specificity of radiological prediction of
and a mean value from these six measurements was used for 96.4% (95% CI, 94.3%-97.8%).
further analyses. Overall PPV and NPV were 78.3% (95% CI, 67.6%-
Additionally, location and size of unruptured aneurysms 86.3%) and 96.8% (95% CI, 94.8%-98.1%) respectively.
based on CTA, presence of ICH, and time from onset of As with the sensitivity, PPV for aneurysms in the ante-
symptoms to performing NECT, were noted. rior circulation (ACA, ACom and MCA) appeared to be
significantly higher than in other locations: 85.7% (95%
Statistical analysis CI, 73.2%-93.2%) vs. 62.9% (95% CI, 42.5%-79.9%) with
Chi-square test was used to compare sensitivities, specifici- p = 0.019 (Chi-square).
ties, positive predictive values (PPVs) and negative predictive We did not find significant differences in age, gender, Hij-
values (NPVs) of radiological diagnoses for different locations dra scale or size of the ruptured aneurysm between the groups
of aneurysms. U Mann-Whitney’s test was applied to compare with correct and incorrect radiological diagnoses. However,
sizes of ruptured and unruptured aneurysms. Interobserver the prevalence of ICH was significantly higher in the group
agreement was assessed with Kendall’s tau-b value. A multiva- with a correct radiological diagnosis than in the group with
riate logistic regression model was used to find independent an incorrect diagnosis (Tab. 3).
demographic and clinical predictors of false radiological
diagnoses. P < 0.05 was considered statistically significant.
For statistical analysis, STATISTICA 13.3 software (TIBCO Table 1. Distribution of ruptured aneurysms
Software Inc., Palo Alto, CA, USA) was used. A medical sta-
n = 83 Percentage
tistician evaluated the results of the analyses.
ACA right 1 1
ACA left 1 1
Results
ACom 26 32
Of the 256 patients whose records were reviewed, multiple MCA right 13 16
aneurysms were detected in 83 (32%) CTA examinations. None MCA left 11 13
of the patients was excluded due to poor image quality. These ICA right 8 10
83 patients were included in the study. This group included ICA left 14 16
60 (72%) females and 23 (28%) males. The mean age of these BA 4 5
patients was 55.7 ± 14.4 years (range 21–90). NECT was per-
PCA right 1 1
formed after a mean interval of 9.1 ± 3.3 hours following the
PCA left - 0
onset of symptoms.
The distribution of ruptured aneurysms is presented in PICA right 1 1

Table 1. The mean size of the ruptured aneurysm (7.7 ± 4.7 mm, PICA left 3 4
range 2–27) was significantly larger compared to the mean ACA — anterior cerebral artery; ACom — anterior communicating artery; MCA — middle cerebral
artery; ICA — internal carotid artery; BA — basilar artery; PCA —posterior cerebral artery; PICA —
size of an unruptured aneurysm (5.9 ± 4.5 mm, range 2–13; posterior inferior cerebellar artery

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A B

Figure 1. Patient with SAH and multiple cerebral aneurysms in whom localisation of ruptured aneurysm was correctly predicted by radiolo-
gists in NECT (A) on basis of clear lateralisation of SAH (arrows). CTA (B) reveals left MCA aneurysm (arrow)

A B

Figure 2. Patient with SAH and multiple cerebral aneurysms in whom localisation of ruptured aneurysm was incorrectly predicted by radio-
logists in NECT (A) showing bilateral, diffuse bleeding (arrows). Radiologists chose anterior communicating artery as localisation of ruptured
aneurysm, while surgical verification revealed left internal carotid/posterior communicating artery aneurysm to be bleeding source. CTA (B)
presents ruptured aneurysm (arrow)

Among 18 falsely predicted ruptured aneurysm locations, In seeking independent predictors of the correct location
we found only one patient (with aneurysms located in the right of the ruptured aneurysm by the radiologists, we analysed
MCA and the right internal carotid artery - ICA) in whom an gender, age, Hijdra scale, size of the ruptured aneurysm, the
unruptured aneurysm was revealed with CTA in a location presence of an ICH, and the time from onset of symptoms to
wrongly considered by the radiologist to the location of a rup- performing NECT. The presence of an ICH appeared to be
tured aneurysm. The radiologist selected an MCA aneurysm as an independent predictor of a correct radiological diagnosis,
the ruptured one, but surgical verification confirmed an ICA with an odds ratio of 8.57 (95% CI, 1.07-68.99; p = 0.03).
aneurysm as the source of bleeding. In the remaining 17 cases, Gender, age, Hijdra scale, size of the ruptured aneurysm, and
although CTA detected multiple aneurysms, none of them was the time from onset of symptoms to performing NECT were
positioned in the location falsely predicted by the radiologists. not independent predictors of correct results.

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 Marcin Sawicki et al., Value of NECT in detecting ruptured aneurysm

Table 2. Results of radiological diagnosis for particular locations of ruptured aneurysms

Location Sensitivity Specificity PPV NPV
ACA 50.0 (2.6–97.3) 100 (94.4–100) 100 (5.5–100) 98.8 (92.5–99.9)
ACom 92.3 (73.4–98.7) 92.9 (82.2–97.7) 85.7 (66.4–95.3) 96.4 (86.4–99.4)
MCA 95.8 (76.9–99.8) 93.2 (82.7–97.8) 85.2 (65.4–95.2) 98.3 (89.4–99.9)
ICA 59.1 (36.7–78.5) 93.4 (83.3–97.9) 76.5 (49.8–92.2) 90.1 (80.1–95.6)
BA 75.0 (21.9–98.7) 93.7 (85.2–97.7) 37.5 (10.2–74.1) 98.7 (91.8–99.9)
PCA 0.0 (0–94.5) 100 (94.4–100) NA 98.8 (92.6–99.9)
PICA 25.0 (1.3–78.1) 98.7 (92.2–99.9) 50.0 (2.7–97.3) 96.3 (88.8–99.0)
Overall 78.3 (67.6–86.3) 96.4 (94.3–97.8) 78.3 (67.6–86.3) 96.8 (94.8–98.1)
Results are presented as percentages and 95% confidence interval.
PPV — positive predictive value; NPV — negative predictive value; ACA — anterior cerebral artery; ACom — anterior communicating artery; MCA — middle cerebral artery; ICA — internal carotid artery; BA —
basilar artery; PCA — posterior cerebral artery; PICA — posterior inferior cerebellar artery; NA — not applicable

Table 3. Comparison of demographic and clinical data between groups with correct and incorrect radiological diagnoses. Prevalence of intracerebral haema-
toma (ICH) significantly higher in group with correct radiological diagnosis
Parameter Correct radiological diagnosis (n = 65) Incorrect radiological diagnosis (n = 18) P value
Age (years) 54.8 ± 15.2 59.1 ± 10.3 0.2
Gender (f/m) 44/21 16/2 0.2
Hijdra score (points) 17.2 ± 9.5 18.1 ± 9.1 0.8
Ruptured aneurysm size (mm) 8.0 ± 4.9 6.2 ± 3.3 0.17
ICH 24 (36.9%) 1 (5.6%) 0.03

Discussion space in this region. This may enable the blood jet to spread
in many different directions. Takeuchi et al. described a case
Our results indicate an overall sensitivity of 78.3% and of a ruptured internal carotid/posterior communicating artery
specificity of 96.4% of NECT in correctly locating the ruptured aneurysm in which blood clots were found in the cisterna
aneurysm, with very high interobserver agreement. magna, the fourth ventricle and the lateral ventricles [13].
Several previous studies assessing the amount and distri- Such blood distribution was misleading because it suggested
bution of subarachnoid blood in NECT have shown divergent that the ruptured aneurysm was located in the posterior fossa.
results. In their study of 168 patients, van der Jagt et al. found Possible explanations considered by the authors included the
that only the location of a parenchymal haematoma predicted formation of adhesions in the subarachnoid cisterns due to an
the site of rupture, but it was present in only 15% of cases [2]. earlier minor leakage, the orientation of the aneurysm (po-
They found that the distribution of blood was significant only steroinferior direction), and early wash out of the blood clot.
for ACA and ACom aneurysms. Nehls et al. were able to locate Lee et al. presented two cases of bilateral ICA aneurysms that
the rupture site in 45% of 35 patients using NECT findings [5]. produced a contralateral distribution of clots on NECT [14].
The sensitivity of NECT in identifying the ruptured lesion was They explained these misleading findings as due to adhesion
about 70% in the study by Karttunen et al. of 180 aneurysms and obliteration of the subarachnoid cisterns from a previous
[10]. Latchaw et al. found that NECT could define the location haemorrhage, with deviation of the direction of haemorrhage.
of the ruptured aneurysm in approximately 80% of cases [11]. In contrast, the distribution of SAH from ACA, ACom
We found significantly higher sensitivity and PPV of the and MCA aneurysms is far more characteristic. In these cases,
radiological diagnosis for ruptured aneurysms in the ACA, blood is typically present in the suprasellar cistern, along the
ACom and MCA compared to other locations, including the cerebral falx and in the Sylvian fissures. However, in ACA
posterior circulation. A similar difference in sensitivity was and ACom aneurysms both Sylvian fissures are filled equally,
also reported by van der Jagt et al. and Karttunen et al. [2, 10]. whereas in MCA aneurysms usually clear lateralisation is
We agree with these authors; this method seems unreliable for observed, with larger amounts of blood observed in the he-
locating posterior circulation aneurysms. misphere ipsilateral to the ruptured aneurysm.
We suggest that an uncharacteristic distribution of SAH It is worth underlining that our study provides novel infor-
from ruptured posterior circulation aneurysms could be cau- mation because, unlike others, we performed detailed analysis
sed by the complex anatomical structure of the subarachnoid of each particular false result. We compared the locations of

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unruptured aneurysms revealed by CTA with the sites falsely Conclusions

diagnosed by radiologists. It appeared that there was only
one case of the 18 patients whose NECT led the radiologist In patients with SAH and multiple cerebral aneurysms,
to choose a location in which an unruptured aneurysm was NECT can identify the source of bleeding with high accuracy
detected with CTA. Therefore, the remaining 17 results should for ACA, ACom and MCA aneurysms, especially with the
be regarded as inconclusive. presence of ICH. For other locations, the method seems to
In other words, radiologists chose the wrong aneurysm as be not accurate enough to be relied upon to make treatment
a source of SAH in only one case. decisions. However, in combination with CTA, the ruptured
Directly proportional dependence between the aneurysmal aneurysm can be identified in almost every patient.
size and the risk of rupture confirmed by our study has alre-
ady been widely discussed in the literature, including RCTs. Declarations of interest: The authors declare no conflict of
However, this issue is beyond the scope of the present study. interest.
Our analysis of the relationship of demographic and clini- Funding: No funding source to declare.
cal features to the sensitivity of radiological diagnosis found
that the presence of ICH independently predisposes to the References
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