Journal of Clinical Neuroscience 18 (2011) 905–909

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Journal of Clinical Neuroscience

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Clinical Study

Indications for the use of temporary arterial occlusion during aneurysm repair:an institutional experience

Behzad Eftekhar �, Michael Kerin Morgan ⇑Australian School of Advanced Medicine, Macquarie University, Balaclava Road, North Ryde, Sydney, New South Wales 2109, Australia

a r t i c l e i n f o a b s t r a c t

Article history:Received 10 December 2010Accepted 19 December 2010

Keywords:Intracranial aneurysmTemporary clippingSurgery

0967-5868/$ - see front matter � 2011 Elsevier Ltd. Adoi:10.1016/j.jocn.2010.12.009

⇑ Corresponding author. Tel.: +61 2 9812 3500; faxE-mail address: michael.morgan@mq.edu.au (M.K.

� Dr Eftekhar is supported by a scholarship fundMedical, Pty Limited.

This study was undertaken to determine variables that could predict, in the preoperative period, the like-lihood for the need for intraoperative temporary arterial occlusion using clips (temporary clipping) whensurgically repairing intracranial aneurysms. Data collected prospectively between October 1989 andMarch 2010 of 1129 unruptured intracranial aneurysms in 934 patients who were managed surgicallywas examined retrospectively. Temporary clipping was used in 400 patients (35.4%). Regression analysisof putative predictive variables revealed that aneurysms of a larger size, irregular fundus shape or mid-line location were more likely to be treated with temporary clipping.

Basilar caput aneurysms larger than 10 mm were always managed with temporary clipping. There wasno combination of factors studied that consistently predicted that temporary clipping would not beneeded. Therefore, the potential need for temporary clipping must be considered for every patient withan aneurysm.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Although reversible arterial occlusion by temporary arterialocclusion using clips (temporary clipping) is an established toolin the armamentarium of the vascular neurosurgeon,1–10 it remainsselectively employed. Predicting aneurysms that are likely to needtemporary clipping can assist in operative preparation (for exam-ple with the anticipated need for cerebral protection againstischemia).

The option to use temporary clipping is an individual choicemade by the neurosurgeon based upon many factors, includingpreoperative vascular imaging, intraoperative findings and pastexperience with this technique. When the option to temporarilyclip is exercised, a considerable re-adjustment to the physiologicalparameters of the patient needs to be made by the anaesthetist. Anawareness that temporary clipping will be used, or is very unlikelyto be used, may assist the anaesthetist in their decision making andthus minimise intraoperative delays. Specific preoperative factorsthat can assist in the prediction for the need of temporary clippinghave not been addressed in the literature.

In this study, based on a single surgeon’s experience inmicrosurgical management of unruptured intracranial aneurysms,

ll rights reserved.

: +61 2 9812 3600.Morgan).ed by Johnson and Johnson

we investigated preoperative variables that might help predict theneed for temporary clipping.

2. Materials and methods

A retrospective study examined a prospectively collected data-base of a single surgeon (MKM) of unruptured intracranial aneu-rysms operated between October 1989 and March 2010. Thedatabase included demographic, clinical, anatomical and outcomedata.

Patients were included if they had at least one surgically treatedunruptured intracranial aneurysm as shown on digital subtractionangiography (DSA) or axial CT angiography (CTA). Patients wereexcluded if they had traumatic or mycotic aneurysms.

Size, shape, presence of irregularities (secondary ‘‘bubbles’’ or‘‘blebs’’), presence of thrombi or calcifications in the aneurysmon CT scan, and coexisting aneurysms in other locations wererecorded.

An orbito-pterional craniotomy was used for most anterior cir-culation aneurysms. Posterior inferior cerebellar (PICA) and verte-bral artery aneurysms were repaired using a far lateral suboccipitalcraniotomy. An orbito-pterional craniotomy with extensive Sylvianfissure opening and zygomaticotemporal approach with or withoutmedial petrosectomy (for low or large basilar aneurysms) wereused for repair of most basilar artery aneurysms. Multiple aneu-rysms (ipsilateral or contralateral) were generally repaired duringthe same operation from a one-sided craniotomy where feasible.

Table 1General characteristics of 1129 aneurysms in 934 patients who underwent intraop-erative temporary arterial occlusion using clips, the aneurysms and operations.

Characteristics

Mean age (range in years,13/934 missing)1

52.2 (9–82)

Age by decade (13/934 missing) (%) <40 143 (15.53)40–49 249 (27.04)50–59 240 (26.06)60–69 205 (22.26)>69 84 (9.12)

No. aneurysms (female/male) (%)1 815/314 (72.2/27.8)

No. aneurysms in patients whosmoke1

110 (9.75%)

Aneurysm size (mm) (%)(17/1129 missing)

<7 611 (54.95)7–12 242 (21.76)13–24 134 (12.05)>24 125 (11.24)

Aneurysm location (no./1129) (%) Posteriorcirculation

136 (12.05)

Basilar tipBasilar

83 (7.35)

Trunk 14 (1.24)PICA 14 (1.24)VA 25 (2.21)

ICA 430 (38.09)ACoA 131 (11.60)MCA 363 (32.15)Other 67 (5.9)

Aneurysm side (no./1129) (%) (3missing)

Right 472 (41.8)Left 464 (41)Bilateral/midline 190 (16.83)

Bubbles or blebs on CT scan(no./1129 aneurysms)

267 (23.65)

Calcium on CT scan 75 (6.64)Thrombus on CT scan 15 (1.33)Associated AVM 86 (7.62)Previous GDC 21 (1.86)Procedures (no./1129) (%) Clipping 1047 (92.7)

Clip and suture 1Trap 7 (0.6)Trap and bypass 73 (6.4)Wrapreinforcement

1

AVM = arteriovenous malformation, GDC = Guglielmi detachable coil, ICA = internalcarotid artery, MCA = middle cerebral artery, PICA = Posterior inferior cerebellarartery, VA = vertebral artery,

1 Age, sex and smoking status were based on patients’ general characteristics.

906 B. Eftekhar, M.K. Morgan / Journal of Clinical Neuroscience 18 (2011) 905–909

During temporary clipping, a systolic blood pressure of160 mm Hg was aimed for by the anaesthetists. If temporary clip-ping was anticipated to be longer than 15 minutes, thiopentonewas administered prior to temporary clip application.

2.1. Definitions

The employment of temporary clipping per aneurysm (ratherthan per patient or per surgical procedure) was considered thedependent variable. The predictive value of the following preoper-ative variables was investigated: age, sex, smoking status, preoper-ative modified Rankin Scale (mRS), family history of aneurysm, sizeof the aneurysm, previous coiling, associated arteriovenous malfor-mation, calcium in the wall of the aneurysm on CT scan, thrombuswithin the aneurysm on CT scan, bubbles (or blebs) on CTA or DSA,midline location and specific sites (internal carotid artery [ICA],middle cerebral artery [MCA], anterior communicating artery[ACoA]; posterior circulation including basilar trunk, basilar caput,posterior inferior cerebellar artery [PICA] and vertebral artery).

2.2. Statistical analysis

Univariate logistic regression analysis was used to determinewhich of the many factors should be entered into the multivariateanalysis. Multivariate logistic regression analysis was performed toidentify independent predictors for surgical outcome. A p value ofless than 0.05 was considered statistically significant.

We used a receiver operating characteristic (ROC) curve to iden-tify the optimal cut-off aneurysm size discriminating betweenthose aneurysms treated with temporary clipping and those thatwere not. A ROC curve is widely accepted as a method for selectingan optimal cut-off point for a test and for comparing the accuracyof diagnostic tests. The curve is generated by plotting sensitivity ofall possible cut-off points for the test on the y axis as a function ofspecificity on the x axis.11,12 Then the cut-off point optimising thesensitivity and specificity of the test (usually the point nearest tothe left upper corner [Fig. 1] is identified based on the ROC curve).

3. Results

A total of 1129 unruptured intracranial aneurysms in 934 pa-tients were managed surgically by MKM in 946 operations duringthe study, of which 400 (35.4%) were treated with temporary clip-

Fig. 1. A receiver operating characteristic curve analysis showing that a cut-offaneurysm size of 7 mm has 70% specificity and 71% sensitivity to separate theaneurysms that were managed with temporary clipping from those that were not.

ping. Table 1 shows the general characteristics of the study popu-lation. The mean patient age was 52.2 years (range: 9–82 years),with a female (F) preponderance (F:M ratio of 2.6:1).

3.1. Aneurysmal characteristics

Size distribution of the aneurysms is shown in Table 1. The 1–2-mm-diameter aneurysms were operated coincidentally with otherlarger intracranial aneurysms. A total of 267 (23.65%) aneurysmswere irregularly shaped, 75 (6.64%) were calcified and 15 (1.33%)had thrombi encroaching upon the aneurysm neck identified onCT imaging. There were 136 (12.05%) aneurysms in the posteriorcirculation. Of all aneurysms, 92.7% were surgically clipped. Thosethat were not treated by surgical clipping underwent trapping andbypass or Teflon wrapping and clip reinforcement of the wrapping.

3.2. Predictors of the use for temporary clipping

Table 2 shows the results of regression analyses of various pre-operative predictors. The use of temporary clipping was the depen-dent variable. Positive family history in univariate analysis wasstatistically significant (in bold type) as a negative predictor, but

Table 2Logistic regression analyses of prognostic factors for intraoperative temporary arterialocclusion using clips.

Factor Oddsratio

pvalue

95% Confidenceinterval

Age 1.002 0.617 0.992–1.012Sex 1.095 0.509 0.835–1.435Smoking 1.188 0.403 0.793–1.779Positive family history 0.555 0.001 0.389–0.792Preoperative MRS 1.119 0.069 0.991–1.264Calcium on CT 2.079 0.002 1.299–3.329Thrombus on CT 2.773 0.055 0.980–7.849Bubbles or blebs on CT 1.696 0.000 1.282–2.245Midline location 1.923 0.000 1.402–2.636Basilar caput 2.074 0.001 1.324–3.250Posterior circulation 1.569 0.015 1.091–2.254Basilar trunk 0.493 0.280 0.1368–1.778PICA 0.493 0.280 0.1368–1.778Vertebral artery 1.703 0.189 0.769–3.769Internal carotid artery 0.700 0.006 0.542–0.904Middle cerebral artery 0.989 0.935 0.761–1.284Anterior communicating

artery1.817 0.001 1.258–2.622

Size of the aneurysm 1.139 0.000 1.116–1.163Size of the aneurysm > 7 mm 5.583 0.000 4.271–7.298Size of the aneurysm adjusted

for1.137 0.000 1.114–1.161

positive family history 0.829 0.333 0.567–1.211Size of the aneurysm adjusted

for1.138 0.000 1.115–1.161

calcium on CT 1.278 0.353 0.761–2.147Size of the aneurysm adjusted

for1.143 0.000 1.120–1.167

bubbles or blebs on CT scan 1.963 0.000 1.442–2.673Size of the aneurysm adjusted

for1.146 0.000 1.122–1.170

midline location 2.517 0.000 1.784–3.552Size of the aneurysm adjusted

for1.142 0.000 1.119–1.16

basilar caput 2.636 0.000 1.630–4.261Size of the aneurysm adjusted

for1.160 0.000 1.134–1.186

ICA 0.387 0.000 0.282–0.530Size of the aneurysm adjusted

for1.147 0.000 1.123–1.171

ACoA 2.674 0.000 1.802–3.969Size of the aneurysm adjusted

for1.139 0.000 1.116–1.162

posterior circulation 1.523 0.040 1.020–2.274

The analysis is based on 1,129 aneurysms.Bold type represents significant prognostic factors (p < 0.05).ACoA = anterior communicating artery, ICA = internal carotid artery.

Table 3Frequency of temporary clipping in different aneurysm locations.

Location No. aneurysms needing temporaryclipping (% of total per location)

ICA 131 (30.47)MCA 128 (35.26)ACoA 63 (48.09)Posterior circulation 61 (44.85)

Basilar tip 43 (51.81)Basilar trunk 3 (21.43)PICA 3 (21.43)Vertebral 12 (48.00)

Other 17 (24.64)

ACoA = anterior communicating artery, ICA = internal carotid artery,MCA = middle cerebral artery, PICA = posterior inferior cerebellar artery.

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when adjusted with the size of the aneurysm, family history didnot maintain its significance. We interpreted this to mean thatthose with a positive family history were discovered to have asmaller aneurysm.

3.2.1. SizeAneurysm size was a significant factor. Temporary clipping was

more likely with larger aneurysms. Size maintained its statisticalsignificance when adjusted for: bubbles (or blebs) on CT scan, mid-line location, specific artery of origin (ICA, ACoA), basilar caput, andposterior circulation.

Fig. 1 illustrates the results of the ROC curve analysis. ROCshows that an aneurysm size cut-off of 7 mm has 70% specificityand 71% sensitivity to separate the aneurysms that were managedwith temporary clipping from those that were not. Aneurysms lar-ger than 7 mm were more likely to undergo temporary clipping(odds ratio [OR] 5.58, 95% confidence interval [CI] 4.27–7.29).The percentage of temporary clipping increases from 18.5% inaneurysms sized less than or equal to 7 mm to 63.1% in aneurysms

greater than 15 mm. For aneurysms greater than 7 mm, 55.9%needed temporary clipping.

3.2.2. Aneurysm featuresIn univariate analysis, calcification of the aneurysm (as seen on

the CT scan) and presence of irregularity were each statistically sig-nificant prognostic factors. However, when adjusted for the size ofthe aneurysm, only the presence of the irregularity maintained sig-nificance as an independent factor.

3.2.3. Location of the aneurysmMidline location was a significant variable. Among specific sites,

the ACoA and posterior circulation aneurysms (particularly basilarcaput location) were more likely to have been repaired with theuse of temporary clipping. ICA were less likely to be repaired withtemporary clipping. These variables maintained their statisticalsignificance when adjusted for the size of the aneurysm or pres-ence of irregularity on the CTA.

Table 3 shows the frequency of temporary clipping in differentaneurysm locations. Basilar caput, ACoA and vertebral arteries hadthe highest percentage of temporary clipping.

As was mentioned above, based on our statistical analysis, sizewas the main predictive factor, followed by location and irregular-ity, for the use of temporary clipping. However, none of these fac-tors could reliably predict the need for temporary clipping. Amongdifferent combinations, only basilar caput aneurysms larger than10 mm always were repaired using temporary clipping.

4. Discussion

We analysed a single surgeon’s treatment of 1129 intracranialunruptured aneurysms over more than 20 years. In 35.4% of casesreversible arterial occlusion by temporary clipping was used. Ourresults showed that aneurysms that were more likely to be re-paired with the assistance of temporary clipping were larger, hadirregular shapes, were midline, or were in specific sites (includingACoA and the basilar caput).

Since the development of the temporary clipping technique inaneurysm surgery by Pool13,14 in the 1960s, it has become animportant adjunct in the surgical management of cerebral aneu-rysms. Temporary arterial occlusion is particularly useful in aneu-rysms that are densely adherent to surrounding vasculature andalso large and giant aneurysms with calcification and thrombosisthat require evacuation before clipping.15

The use of temporary clipping by neurosurgeons varies, and isestimated to range from 0% to 80%.16 For any single neurosurgeon,this also varies with aneurysm location and configuration. The use

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of temporary clipping for any aneurysm almost certainly reflectsthe surgical complexity of repairing that aneurysm. Because com-plex aneurysms are more likely to have adverse outcomes, therehave been reports suggesting that temporary clipping may contrib-ute these adverse outcomes.17,18 However, this association is al-most certainly coincidental. Nonetheless, because of thisassociation, there is no consensus regarding the role of temporaryclipping.6,10 It has been the senior author’s (MKM) practice to usemannitol for all aneurysm surgery. Thiopentone (aiming for tem-porary burst suppression) is also used when temporary clippingis anticipated to be longer than 15 minutes. The surgeon’s decisionto use temporary clipping relates both to safety and efficacy ofaneurysm repair. The basis for this decision includes determinationthat:

� an intra-operative aneurysm rupture would be difficult to con-trol with small calibre suction without temporary clipping (aswould occur in basilar and posteriorly directed ACoA aneurysmsand large aneurysms)� manipulation of the fundus or neck may predispose to embolic

infarction without temporary clipping (those with a calcifiedneck or containing thrombus)� reduction in aneurysm tension with temporary clipping would

facilitate more effective aneurysm neck occlusion (aneurysmsthat would be at risk of the clip blades migrating onto the par-ent artery due to tension of the fundus and those aneurysmsthat are likely to be manipulated with vascular forceps to easeinto the clip blades)� the aneurysm fundus will be opened during its repair (aneu-

rysms where suturing of the neck is more appropriate to repairthan clipping and those in which thrombus needs removal priorto repair)� temporary clipping in older patients with an atheromatous par-

ent artery may increase the risk of embolic infarction or perma-nent occlusion.

Among different combinations of predictive factors, only basilarcaput aneurysms larger than 10 mm were always repaired withtemporary clipping. That none of the other combinations couldreliably predict the use of temporary clipping underlines theimportance of the surgeon’s intraoperative judgement.

Our study shows that the size of the aneurysm is a statisticallysignificant predictor for the use of temporary clipping during aneu-rysm repair. The reason for this is related to the ease of control ofbleeding if intraoperative rupture were to occur and the complex-ity of repair. Practically, the 7-mm diameter size cut-off separatedthose aneurysms that required temporary clipping from those thatdid not with 71% sensitivity and 70% specificity. This is generally inagreement with the related literature for larger aneurysms,19–23

irregularly shaped aneurysms24–28 and where temporary arterialarrest can be useful to decrease the risk of rupture duringdissection.29

The finding that posterior circulation aneurysms (particularlybasilar tip aneurysms) were more likely to be repaired with tempo-rary clipping is in agreement with the literature.21,23,30–33 Theopposite is true for ICA aneurysms. They were less likely to needtemporary clipping. Many anterior circulation aneurysms, particu-larly those more distally located, can be accessed with less diffi-culty in comparison with the other locations, rather than patientgeneral characteristics. In case of rupture, proximal control canbe achieved more easily for these aneurysms. There is also morelikely to be atheroma in the MCA and ICA that might count againsta decision to use temporary clipping for aneurysms in theselocations.

As was not unexpected, all the statistically significant variablesfor predicting the use for temporary clipping were related to aneu-

rysms features and their locations, rather than patient generalcharacteristics. No other variables were of prognostic value forthe use for temporary clipping.

Planning operative strategy is crucial for success of complexneurosurgical procedures. Based on a large series of surgically re-paired unruptured aneurysms, we have shown that larger aneu-rysms, irregular aneurysm shape, midline aneurysms and thosein specific sites (including ACoA and the posterior circulation, par-ticularly tip of the basilar) were more likely to be repaired with theuse of temporary clipping. Of importance, no combination of vari-ables examined predicted with certainty absence of the use of tem-porary clipping. Therefore, both surgical and anaesthetic teamsmust always be prepared for the employment of temporary clip-ping when managing cerebral aneurysms.

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