Keywords
aneurysm surgery - temporary occlusion - elective - intermittent - time limit
Introduction
Temporary occlusion of the proximal vessel is being increasingly used as an adjunct
during aneurysm surgery. It helps to reduce the pressure within the dome, reduces
its size, facilitates safer dissection, and consequently reduces the incidence of
intraoperative rupture. Further, in select cases, it aids in evacuating thrombus or
atherosclerotic plaque before clipping. Temporary clipping could be either “on demand”
as during an intraoperative rupture or used electively. It could be placed continuously
or intermittently. Despite its increasing use, there are no clear guidelines regarding
its practice. One of the most important parameters is the safe time limit for temporary
occlusion. Various studies have attempted to address this concern with no reliable
conclusions. Perioperative monitoring techniques, the logical choice to guide the
duration of temporary clipping, suffer from a lack of “global monitoring” system.
We have been impressed with its usage and practice when used electively in an intermittent
fashion. We reviewed our protocol for the last 5 years and analyzed it to provide
a practical, safe time period (range) of intermittent occlusion, which is irrespective
of the vascular territory in the anterior circulation.
Methods and Patients
Patients in whom elective, intermittent, temporary clipping protocol was used during
1999 to 2004 were prospectively analyzed. Selection criteria included patients with
aneurysms in the anterior circulation. Those patients with multiple aneurysms who
underwent temporary occlusion of a single proximal vessel were also included. Exclusion
criteria included those with posterior circulation aneurysms and those in whom temporary
occlusions of arteries in different vascular territories were done during the course
of the same surgery. During the initial years, the proximal vessel occlusion lasted
up to an average of 10 minutes per episode, while during the latter period, we reduced
the occlusion period to between 5 and 7 minutes. The period of reperfusion was 5 minutes
in both protocols. We compared the results of these two groups with respect to the
territory involved, number of intermittent clippings, the total duration of occlusion,
and the immediate postoperative status of the patient.
Surgical Procedure
The standard anesthetic protocol was followed as for any aneurysm surgery such as
avoiding acute hypertension and achieving adequate brain relaxation. Patients remained
normothermic and euvolemic. Prior to temporary occlusion propofol as an infusion and
mannitol were started, measures were taken to avoid the anticipated hypotension during
propofol infusion. EtCO2 (end tidal carbon dioxide) was kept in the range of 30 to 35 mm Hg. In general, the
temporary clip was applied on the proximal vessel well away from the site of dissection
to provide adequate working space, taking care to avoid the perforators. The clip
was applied for a fixed period (approximately 5 or 10 minutes) with a 5-minute reperfusion
break between clip applications. Patientʼs early postoperative clinical status was
taken for assessment, as immediate deficit would be reflective of the temporary occlusion.
A delayed deficit could be due to other factors such as vasospasm or other postoperative
complications. Computed tomography (CT) brain assessment was not a part of the study
design. It is included in the results when available and relevant. As a rule, early
surgery was preferred; however, some underwent delayed surgery, due to late referral,
old age, or a complex aneurysm.
The patients were divided into two groups, Group I, the shorter duration group with
a temporary clipping time of less than 7 minutes, and Group II, the longer duration
group with a temporary clipping time of about 10 minutes and more. Categorical variables
were analyzed using the chi-square test and the continuous variables were analyzed
using the Mann–Whitney test and the univariate binary logistic regression. The statistical
analysis was performed using SPSS 11.0 (IBM Corporation, Armonk, New York, United
States) for windows.
Results
The total number of patients who satisfied the criteria was 68. There were 34 patients
in each of these groups. In Group I among the 34 patients, there were 21 males and
13 females. Age ranged from 28 to 84 years (mean, 57 years). Five patients had multiple
aneurysms. There were two intraoperative ruptures, one of them developing a deficit.
In Group II, among the 34 patients, there were 16 males and 18 females. Age ranged
from 40 to 70 years (mean, 54 years). Here, again five patients had multiple aneurysms.
There were eight intraoperative ruptures; one of them developed a deficit.
The details of the artery clipped, number of intermittent clippings, and the total
period of clipping with the average are given in [Tables 1] and [2].
Table 1
Details of the artery clipped, number of intermittent clippings, and the total period
of clipping in Group I (total no. of patients 34)
|
Artery clipped
(no. of patients)
|
No. of intermittent clippings
|
Total period of clipping (min)
(average)
|
|
Internal carotid artery (11)
|
1–9 times
|
5–44 (12.64)
|
|
Anterior cerebral artery (17)
|
1–9 times
|
6–43 (19.35)
|
|
Middle cerebral artery (6)
|
1–7 times
|
5–36 (21.83)
|
Table 2
Details of the artery clipped, number of intermittent clippings, and the total period
of clipping in Group II (total no. of patients 34)
|
Artery clipped (no. of patients)
|
No. of intermittent clippings
|
Total period of clipping (min) (average)
|
|
Internal carotid artery (11)
|
1–6 times
|
10–57 (24.18)
|
|
Anterior cerebral artery (16)
|
2–6 times
|
18–59 (31.44)
|
|
Middle cerebral artery (7)
|
2–6 times
|
12–40 (27.71)
|
Details of complications in both the groups are given in [Tables 3] and [4]. Analysis of complications among the patients in Group I revealed none in the middle
cerebral artery (MCA) region. The two patients who developed deficits among the anterior
cerebral artery (ACA) group were elderly and were World Federation of Neurosurgical
Societies Grade 3 preoperatively. In one of them the deficit resolved and the CT did
not reveal any infarcts. Other associated factors could have played a major role in
the complications. Only two patients, one in the internal cerebral artery (ICA) and
one in the ACA group, had deficits and proven infarcts postoperatively.
Table 3
Details of Group I complications
|
Age (y) and sex
|
WFNS grade
|
Aneurysm location
|
Timing of surgery
|
Vessel occluded
|
No. of intermittent occlusions
|
Total duration of occlusion
|
Immediate postoperative deficits
|
CT findings
|
Remarks
|
|
ICA (1 complication)
|
|
|
38/F
|
Grade 1
|
Left ICA bifurcation
|
2nd postictal day
|
Left ICA
|
5, 5, 7 min
|
17 min
|
Right hemiparesis
|
Infarct-L thalamus and adjoining internal capsule
|
−
|
|
ACA (2 complications)
|
|
|
84/M
|
Grade 3
|
AComA
|
24th postictal day
|
Left A1 segment
|
4, 3, 3 min
|
10 min
|
Minimal right hemiparesis
|
No obvious infarcts
|
Weakness resolved over the next few days
|
|
75/M
|
Grade 3
|
AComA
|
14th postictal day
|
Left A1 segment
|
6, 5, 7 min
|
18 min
Intraoperative rupture
|
Mild right hemiparesis
|
Infarct in the anterior limb of the internal capsule
|
−
|
|
MCA (0 complication)
|
Abbreviations: ACA, anterior cerebral artery; AComA, anterior communicating artery;
CT, computed tomography; GCS, Glasgow Coma Scale; ICA, internal carotid artery; MCA,
middle cerebral artery; WFNS, World Federation of Neurosurgical Societies.
Table 4
Details of Group II complications
|
Age (y) and sex
|
WFNS grade
|
Aneurysm location
|
Timing of surgery
|
Vessel occluded
|
No. of intermittent occlusions
|
Total duration of occlusion
|
Postoperative deficits
|
CT findings
|
Remarks
|
|
ICA (2 complications)
|
|
|
51/M
|
Grade 1
|
Left AComA
|
5th postictal day
|
Left ICA
|
10, 9, 11 min
|
30 min
|
Right lower limb 4/5
|
Small infarct-L thalamus and adjoining internal capsule close to the genu
|
Resolved by the time of discharge
|
|
52/M
|
Grade 1
|
Right PComA
|
12th postictal day
|
Right ICA
|
12 min
|
12 min
|
Left hemiparesis
|
−
|
−
|
|
ACA (4 complications)
|
|
|
65/F
|
Grade 1
|
AComA
|
3rd postictal day
|
Left A1 segment
|
8, 9, 5 min
|
21 min
|
Right lower limb paresis
|
No obvious infarcts
|
Weakness resolved over the next few days
|
|
46/M
|
Grade 1
|
Right PComA and AComA
|
5th postictal day
|
Right A1 segment
Right ICA not occluded
|
8, 10 min
|
18 min
|
Left hemiplegia
|
Large infarct on the right side, posterior temporal, and adjacent parietal region
|
Weakness resolved over the next few days
|
|
70/F
|
Grade 2
|
AComA
|
3rd postictal day
|
Right A1 segment
+ Both A2s segments twice
|
5, 8, 7, 6, 6, 3 min
|
35 min
|
Rebleed in the immediate postoperative period
|
Massive rebleed with hydrocephalus
|
Died soon after
|
|
55/F
|
Grade 3
Preoperative right hemiplegia
|
AComA
|
14th postictal day
|
Right A1 segment
|
5, 10, 5 min
|
20 min
|
Left lower limb weak
|
No obvious infarcts
|
−
|
|
MCA (2 complications)
|
|
60/M
|
Grade 2
|
Left MCA bifurcation
|
5th postictal day
|
Left M1 segment
|
8, 4 min
|
12 min
|
Aphasic and hemiplegic
|
−
|
−
|
|
51/M
|
Grade 3
Preoperative left hemiparesis
|
Right MCA bifurcation
|
1st postictal day
|
Right M1 segment and hematoma evacuation
|
5, 5, 8, 10 min
|
28 min
Intraoperative rupture
|
Left hemiplegia
|
Right MCA territory infarct
|
−
|
Abbreviations: ACA, anterior cerebral artery; AComA, anterior communicating artery;
ICA, internal carotid artery; MCA, middle cerebral artery; PComA, posterior communicating
artery; WFNS, World Federation of Neurosurgical Societies.
In Group II, among the MCA group one patient had a low Glasgow Coma Scale score preoperatively
and had undergone hematoma evacuation and clipping of the aneurysm emergently in the
same sitting with intraoperative rupture. Among the ICA group, one patient had only
a lower limb weakness, which resolved by the time of discharge, and the CT did reveal
an infarct. The ACA group registered the maximum number of complications. One of the
complications was that of a rebleed in the immediate postoperative period and hence
it does not reflect the temporary clipping problem. Another patient had an infarct
in the posterior temporal and adjacent parietal region suggestive of MCA territory
infarct and hence may not reflect the A1-segment clipping.
Statistical Methods
Statistical analyses were done using SPSS 11.0 for windows and a p value of less than 0.05 was considered significant. Although the incidence of complications
was more in Group II (23.5 vs. 8.8%), this difference was not statistically significant.
It was also found that the numbers of intermittent clippings were not significantly
different among patients with complications as compared with those without (p = 0.693), which was also supported by univariate binary logistic regression (odds
ratio = 0.84; 95% confidence interval 0.56–1.25). Mann–Whitney test was done to assess
the total duration of clipping between the two groups. It revealed that the total
duration was significantly longer in Group II (p value = 0.000). The total duration of clipping, however, was not significantly different
between those who developed complications and those who did not (p = 0.86). The incidence of complications was not associated with the location of the
aneurysm (p = 0.9).
Discussion
Temporary Clipping
The role of temporary clipping in aneurysm microsurgery has been well accepted.[1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11] Intraoperative rupture is considered the most important and serious complication
associated with a grave prognosis with relation to aneurysm surgery.[1]
[3]
[4]
[6]
[8]
[9]
[12]
[13]
[14]
[15]
[16]
[17] Use of temporary occlusion in reducing its incidence apparently played a major role
in improved outcome after aneurysm surgery.[1]
[6]
[18] Studies evaluating the efficacy of temporary clipping have looked into various aspects
such as preoperative clinical status,[2]
[10] patient profile,[2]
[10] relation to timing of surgery,[2]
[7] the safe time limit,[4]
[7]
[8]
[10]
[16]
[19] vascular territory,[2]
[4]
[7]
[10]
[19] cerebral protection measures,[9]
[10]
[15]
[19]
[20] anesthetic technique, intraoperative monitoring,[10]
[12]
[14]
[16]
[21] employing various techniques such as electrophysiological monitoring,[8]
[10]
[12]
[16]
[22] cortical blood flow,[14]
[21] neurochemical monitoring,[5]
[23] postoperative clinical assessment,[2]
[4]
[9]
[10] and postoperative radiological assessment.[2]
[9]
[10]
[19] Each of these factors has their own limitations.
Postoperative Evaluation
Two major methods of patient evaluation are clinical and radiological. Clinical evaluation
is influenced by various factors such as preoperative clinical status, timing of surgery,
retractor injuries, perforator injury, exacerbating vasospasm, venous, or parenchymal
injuries, which could cause postoperative deficits. With regard to radiological assessment,
all postoperative hypodensities need not be infarcts. They could be postoperative
changes or secondary to venous occlusion.[10]
[19]
Duration of Occlusion
Studies have reported a wide range of safe occlusion times.[2]
[4]
[7]
[8]
[9]
[10]
[11]
[14]
[16]
[17]
[21] Specific arterial territories have been analyzed with regard to the duration.[2]
[7]
[10]
[14]
[16]
[19] In the anterior circulation, MCA territory is thought to be particularly vulnerable
to long occlusion periods. It has been shown that the safe period of occlusion could
vary even within an individual vascular territory, depending on collateral supply,
as within the MCA territory there is large individual variation.[7]
[8]
[14]
[19] Review of these studies reveals that the safe occlusion period is variable for individuals
and vascular territories, as the factors influencing it are manifold.[2]
[3]
[4]
[5]
[7]
[10]
[17] The only consensus is that increasing periods of occlusion lead to increasing chances
of infarction.[2]
[10]
Intermittent versus Continuous
Temporary clipping could be on demand following intraoperative aneurysm rupture or
elective and further it could be continuous or intermittent. There have been conflicting
reports regarding its implications. Some studies have found that continuous occlusion
is better than intermittent, and that intermittent occlusion may in fact predispose
to ischemia.[9]
[10]
[14]
[17]
[24] On the other hand, studies have also shown that intermittent occlusion with periods
of reperfusion appears to be safer than a single episode of continuous occlusion.[2]
[5]
[17]
[19] Experimental studies also support such a view.[17]
[25]
[26]
[27]
[28]
[29]
Our Protocol
The major complication of temporary clipping is its potential ischemic sequelae. Risk
of ischemia during temporary clipping would depend on the following: (1) patient profile,
(2) the vessel clipped, (3) characteristics of collateral supply, and (4) duration
of clipping. Among these, duration of temporary clipping is the only factor we have
control over. Any study trying to focus on one parameter would need to keep all other
factors uniform which in the present context would invariably be complicated by a
multitude of factors influencing the outcome; hence, we decided to concentrate on
evolving a protocol for the safe duration of temporary clipping.[10]
Unlike some studies, ours was a prospective analysis. Based on the available information,
one could conclude that shorter the occlusion period, safer would be the procedure.
By incorporating intermittent occlusions, one could lengthen the total period of occlusion.
Regarding the duration of occlusion, a period of 5 to 7 minutes was considered to
be long enough to provide adequate time for dissection and yet short enough to be
within the safe range. A range was decided rather than a specific figure, as in practice
the actual occlusion period would fall within a range. We planned on a practical protocol
in using temporary clipping without considering patient profile, clinical grade, vascular
territory, as it would be in a clinical setting, to assess the technique's safety.
No monitoring technique was used as it was not available. Anesthetic technique too
was standard normotensive, normothermic with administration of propofol and mannitol
during temporary occlusion. As mentioned earlier, we relied on the immediate postoperative
status of the patient to assess the impact of the temporary clipping, as any delayed
neurological deficits could have other causes.
Analysis of Results and Complications
Analysis of Results and Complications
Between the groups, the total number of patients and their distribution among vascular
territories happened to be similar. The overall incidence of complications was less
in Group I, validating our hypothesis, though it was not reflected in the statistical
analyses, probably due to the small sample size. The total duration of clipping period
was longer in Group II and was statistically significant. It must be stated that these
patients were also treated during the initial period of the study. Hence, the shorter
duration of total period of clipping and increasing experience of the surgeons could
have influenced the decreased complications in Group I. Interestingly, the incidences
of complications were the lowest in the MCA territory among both groups, despite the
fact that MCA territory is supposedly the most vulnerable to ischemia. The incidence
of intraoperative ruptures was more in Group II; however, the complications were not
influenced by these events in both the groups. The important observation was that
occurrences of complications in both the groups did not correlate with either the
total duration of occlusion or the number of intermittent clippings. Other associated
factors probably influenced these complications.
In our experience, use of temporary clipping makes the aneurysm dome, soft, compressible,
and hence aids in dissection which decreases the chance of a rupture. With a similar
protocol, one could go on till the procedure could be completed safely without a finite
endpoint. Another interesting observation is that in the immediate postoperative period,
there is often a mild paucity of movements on the involved side, which resolves as
the patient recovers from anesthesia. We believe from our experience that with short
periods of intermittent clipping, one has the dual advantage of more safety and long
periods of total occlusion time.[1]
[2]
[10]
In conclusion, elective temporary occlusion of proximal artery appears to be a safe
method to employ during aneurysm surgery. When used in an intermittent fashion with
periods of reperfusion, the total duration of occlusion can be prolonged to complete
the surgical clipping effectively. The reduction in duration of the individual clipping
episode resulted in a reduced complications rate, which however did not result in
statistical significance. A larger sample size could clarify the issue.