Keywords aneurysm - cerebral infarction - intraoperative hemorrhage
Introduction
Temporary vessel occlusion enables a surgeon dissect aneurysm and clip with a lower
risk of intraoperative hemorrhage with the associated risk of ischemia. There are
studies on permissible time of occlusion of parent artery using temporary clip; however,
the actual incidence of silent ischemic events in patients with aneurysms treated
with microsurgical clipping is not well documented. The ischemia may manifest or may
be silent. Since silent ischemia does not manifest clinically, it can be picked by
various means such as positron emission tomography scans, single photon emission computed
tomography scan, or various sequences of magnetic resonance imaging (MRI). This study
is done to analyze the risk of symptomatic and silent ischemia in association with
temporary clipping used during the microsurgical clipping of intracranial aneurysms
using diffusion-weighted magnetic resonance imaging (DWMRI) and to evaluate the permissible
time which can cause even silent ischemia. It was used in our study due to the availability,
feasibility, and cost effectiveness of DWMRI.
Materials and Methods
This study evaluates patients in World Federation of Neurological Surgeons (WFNS)
grades I to III, operated for anterior circulation cerebral aneurysms over 3 years
by craniotomy and clipping of aneurysm by a single surgeon. Anesthesia given to them
was as per the standard protocol for aneurysm clipping. During surgery, the number
of temporary clips applied and the time period for which they were applied were recorded.
Other causes for possible ischemic events had been ruled out. DWMRI brain was done
prior to surgery and within 24 hours of surgery in all study patients and ischemia
signs noted by an experienced neuroradiologist and correlated with patient’s post
clipping neurological status and categorized as asymptomatic and or symptomatic ischemia.
Statistical Analysis
Baseline demographics of the study population were analyzed using descriptive statistical
parameters. For comparisons of categorical variables, Fischer’s exact or chi-square
tests are used. For comparisons of continuous variables, the rank-sum or equivalent
Mann–Whitney U test is used. For all analyses, p < 0.05 was considered statistically significant. All computations were performed
using the commercially available software programs and statistician’s aid.
Results
Out of 21 patients, 18 were in the WFNS grade I, one was in grade II, and two were
in grade III. Most common age group was 31 to 40 years consisting of eight patients
in grade I, followed by 41 to 50 years consisting of five patients in grade I, one
in grade II, and one in grade III. The mean age of presentation was 39.8 years. Out
of a total of 21 patients, 12 (57.1%) were males and 9 (42.8%) were females with male
to female ratio of 4:3. Headache was the commonest presenting symptom in all patients
followed by vomiting and loss of consciousness. Hemiparesis was reported in only two
patients.
Anterior communicating artery aneurysms constituted 11 (52.3%) patients, 7 (33.3%)
patients had middle cerebral artery (MCA) aneurysms, 2 (9.5%) patients had supraclinoid
internal carotid artery (ICA) aneurysms, and only one (4.7%) patient was harboring
aneurysms at the junction of ICA–posterior communicating artery.
Out of 21 patients, ischemic changes were noted in five (23.8%) patients on immediate
postoperative DWMRI study. Subgroup analysis as per the size of the aneurysm revealed
only one (33.3%) case of asymptomatic ischemia and no case developed symptomatic ischemia
clinically in small (<7 mm) size aneurysm group. Out of 14 cases of medium (7–14 mm)
size group, one (7.1%) patient developed symptomatic infarct and two (14.2%) patients
developed asymptomatic infarcts. One patient (33.3%) out of three cases of large-size
aneurysms (15–24 mm) size developed symptomatic infarct ([Table 1 ]).
Table 1
Aneurysm size vs. postoperative ischemia
Size of aneurysm
Symptomatic ischemic cases
Asymptomatic ischemic cases
Nonischemic cases
Total
Note: The table shows occurrence of ischemia in different groups according to the
size of aneurysms.
Small
(<7 mm)
0
1 (33.3%)
2 (66.6%)
3
Medium
(7–14 mm)
1 (7.1%)
2 (14.2%)
11 (78.5%)
14
Large
(15–24 mm)
1 (33.3%)
0
2 (66.6%)
3
Giant
(≥25 mm)
0
0
1
1
Total
2
3
16
21
In 17 (81%) cases, temporary clip was applied, out of which two (11.7%) and three
(17.6%) patients developed symptomatic and asymptomatic ischemia, respectively ([Figs. 1 ]
[2 ]). No ischemic changes were noted in four patients in whom temporary clip was not
used.
Fig. 1 Radiological images of the patient with asymptomatic infarction. (A ) NCCT head on admission showed subarachnoid hemorrhage; (B ) Preoperative angiography revealed anterior communicating artery aneurysm; (C ) Preoperative DWMRI showed no infarct; (D ) Immediate postoperative DWMRI showed a small asymptomatic infarct in the left basal
ganglion region. DWMRI, diffusion-weighted magnetic resonance imaging; NCCT, noncontrast
computed tomography.
Fig. 2 Radiological images of the patient with symptomatic infarction. (A ) NCCT head on admission showed subarachnoid hemorrhage; (B,C ) CT angiography brain suggested left MCA bifurcation aneurysm; (D ) The patient was operated for the same and developed symptomatic left side MCA territory
infarct as shown in immediate postoperative DWMRI. CT, computed tomography; DWMRI,
diffusion-weighted magnetic resonance imaging; MCA, middle cerebral artery; NCCT,
noncontrast computed tomography.
The average total mean time of temporary clip application, leading to symptomatic
as well as DWMR-proved ischemic cases, was 300 seconds. In asymptomatic but DWMR-proved
ischemic cases, the average total mean time was 123.33 seconds, however, it was 127.75
seconds in patients without any ischemic changes on DW study ([Fig. 3 ]).
Fig. 3 Number, total mean time, and maximum mean time vs. postoperative ischemia.
Single maximum mean time of the temporary clip used was 145 seconds in both symptomatic
and asymptomatic post clipping ischemic cases. In patients without any post clipping
ischemic changes, the maximum mean single time use of temporary clip was only 81.93
seconds.
Based on the average number of temporary clips applied, i.e., number of vessels in
which temporary clips were applied, was 3.5 in cases of postoperative symptomatic
ischemia, whereas average 2.33 and 1.62 clips were applied in asymptomatic ischemic
cases and in patient without any post clipping ischemia on DWMRI respectively ([Fig. 1 ]).
Glasgow outcome scale at 1 month from discharge was score 4 in post clipping symptomatic
infarct cases. It was 5 in both asymptomatic infarct cases and in patients without
ischemia. Finally, in this study, out of 21 patients, 9.52% patients developed symptomatic
ischemic changes, 14.2% patients developed asymptomatic ischemic changes on DWMRI.
Discussion
Patients in whom cerebral infarction develops after aneurysmal subarachnoid hemorrhage
(SAH) are less likely to make a good recovery and more likely to die or survive with
deficit than those without infarction.[1 ] In the present study also Glasgow outcome scale at the time of discharge was statistically
significant in post clipping ischemic group compared with the nonischemic group.
Juvela et al[2 ] have reported incidence of ischemia to be 65% on postoperative CT scan. Krayenbühl
et al[3 ] reported the incidence of symptomatic and asymptomatic ischemia to be 2 and 9.5%,
respectively. Ferch et al[4 ] also found 17% of symptomatic and 26% of radiologically evident ischemic changes
after the use of temporary clip. In this study, symptomatic and asymptomatic ischemic
changes happened in 9.52 and 14.20% patients, respectively as evidenced by DWMRI sequence.
Overall, 23.72% of our study population developed ischemic changes where temporary
clipping was used during surgeries, which is consistent with the study. Cronqvist
et al[5 ] reported over all silent and symptomatic ischemia rate of 23% using diffusion and
perfusion MRI in patients with ruptured and unruptured intracranial aneurysms treated
by endovascular coiling which is comparable to our study result of 23.8% in post clipping
group in spite of taking advantage of full anticoagulation in endovascular treatment.
Median age of patients in post clipping ischemic group was 50 and 40 years in nonischemic
group, but univariate analysis suggested no significant statistical relation of age
with post clipping ischemic changes. There is no statistically significant difference
between sex, size, and location of aneurysm between post clipping ischemic group and
no ischemic group as is previously reported.[3 ]
It has previously been suggested that the use of temporary clipping during microsurgery
of aneurysms leads to ischemic events.[4 ]
[5 ] The duration of temporary clipping was found to correlate with the increased occurrence
of ischemic events.[3 ]
[6 ] Selvapandian et al[7 ] found no statistically significant correlation between occurrence of complications
and total duration of temporary clipping or number of temporary clippings. Whereas
this study shows the multiple use of temporary clip does not cause postoperative ischemia
but single application of the clip for a longer period (single maximum time of temporary
clip application, p -value = 0.01248) may influence the occurrence of both silent and symptomatic ischemia
([Table 2 ]). According to our study, the acceptable duration of one-time temporary clip may
be less than 145 seconds that can avoid symptomatic ischemic complication to happen,
however, the duration should be kept minimum possible to less than 90 seconds to avoid
any early DWMRI ischemic changes as it might result in symptomatic ischemia in particular
case. The total time of temporary clip application was much less in our study as of
585.4 ± 858.4 seconds in contrast to other studies reported.[1 ] Although Ogilvy et al[8 ] suggested temporary clip application up to 20 minutes, in this study the critical
time period of temporary clip application is 5 minutes, that is, 300 seconds. However,
to prove, this would require further intraoperative study such as Doppler and intraoperative
video angiographies to assess changes in blood flow happening at the time of temporary
clipping ([Table 2 ]).
Table 2
Univariate analysis showing association of ischemia with various factors
Factors
Ischemic group (n = 5)
Nonischemic group (n = 16)
p -Value
Abbreviations: ACOM, anterior communicating; GOS, Glasgow outcome scale; ICA, internal
carotid artery; MCA, middle cerebral artery; PCOM, posterior communicating artery;
WFNS, World Federation of Neurological Surgeons.
Note: For categorical variables—Fischer’s exact or chi-square tests were used and
for continuous variables, the rank-sum or equivalent Mann–Whitney U test was used. Significant p -value < 0.05 is mentioned in bold letters.
Age
50 ± 18
40 ± 9
0.4949
Male/Female (%)
1(20%)/4(80%)
11(68.7%)/5(31.3%)
0.1194
Location of aneurysm
0.1474
ACOM artery
1
10
MCA
2
5
ICA bifurcation
1
1
ICA-PCOM
1
0
Size
0.6539
Small
1
2
Medium
3
11
Large
1
2
Giant
0
1
Temporary clip used
0.5322
Yes
5
12
No
0
4
Number of times temporary clip used
3 0 ± 0.84
2 ± 1.41
0.0752
Single maximum time of temporary clip application (sec)
145
81.93
0.01248 (<0.05)
Total time of temporary clip application (sec)
254
127.75
0.00815 (<0.05)
Mean GOS at 1 month
4.6
5
0.2079
WFNS grade
0.1074
I
3
15
II
1
0
III
1
1
Conclusion
The most significant factors associated with the occurrence of post clipping cerebral
ischemic changes are maximum time of single clip application and total time of temporary
clips application. The incidence of ischemic changes occurring following temporary
clip placement is more or less same as reported in endovascular treatment despite
the fact that latter procedure is taking the advantage of anticoagulation at the time
of intervention.
