Introduction 

   Temporary clipping is a very useful and essential technique for dissection of an aneurysm and clipping the neck and for controlling bleeding due to a premature rupture during cerebral aneurysm surgery.^{1)2)7)9)12)14)} Mostly, temporary clipping is intentionally performed by neurosurgeon to dissect an aneurysm easily. However, it is sometimes performed inevitably to prevent massive bleeding because of the premature rupture for a long time. Because temporary clipping blocks off the blood flow to both the aneurysm and the normal brain tissue, it can cause cerebral ischemia or cerebral infarction.⁹⁾ For that reason, the time and frequency of the temporary clippings are important factors. Unfortunately, other studies have not established the optimal time and frequency for the temporary clipping. 
   The aim of this study was to analyze the relationship between temporary clipping during surgery and a cerebral infarction, and to determine the optimal time and frequency of temporary clipping through the middle cerebral artery (MCA), which has the lack of any major collateral circulation, the sensitivity to ischemia, and the easily definable neurological sequelae both clinically and radiologically. 

Materials and Methods 

   One thousand, three hundreds and fifty six patients with a cerebral aneurysm were treated surgically from January 1997 through to June 2004. Of these patients, there were 317 patients with a middle cerebral aneurysm. Eighty eight of 317 patients were excluded from the analysis for the following reasons: preoperative intracerebral hematoma, a preoperative cerebral infarction or a poor clinical state (Hunt and Hess grade V) on admission. There were 154 females and 75 males in this study, and the mean age was 53.2 (range 30~78 years). There were 39 patients with an unruptured aneurysm, and 190 patients with a ruptured aneurysm. Among the 190 patients, there were 181 patients with Hunt and Hess grade I, II, III, and 9 patients with Hunt and Hess grade IV upon admission (Table 1). 
   130 of the 190 patients with a ruptured aneurysm underwent early surgery (within 3 days after the attack). A craniotomy was performed on all patients through the pterional approach under general anesthesia with Propofol... After dural opening, the carotid cistern and sylvian fissure were dissected under a surgical microscope. After the proximal M1 and distal M2 of the internal carotid artery and aneurysm were provided for temporary clipping, the aneurysm was dissected carefully. The temporary clipping of M1 was performed intentionally because there was a high risk of a premature rupture when the adhesion of the aneurysm with the surrounding blood vessels or brain tissue was severe. Mannitol (150~200 cc) was then infused intravenously. The temporary clipping was performed for no more than 5 minutes. If the time for the temporary clipping was more than 5 minutes, the temporary clipping was removed and the procedure was repeated a minimum of 5 minutes later. The first assistant monitored the duration of the temporary clipping closely. However, the duration of the temporary clipping was over 5 minutes, when a premature rupture occurred. Direct neck clipping was performed and the blood flow of the distal M2 were inspected before and after the aneurismal neck clipping by intraoperative microvascular doppler. The brain computed tomography scan (CT scan) was performed on 1, 3, and 7 days after surgery to detect any postoperative cerebral infarction or hematoma. Postoperative patients were treated closely under the care of the intensive care unit. Brain CT scans were immediately performed if new neurological deficit was detected. 

Results 

   Low attenuated lesions on the brain CT scan within 3 days after surgery were regarded as a cerebral infarction as a result of the temporary clipping (Fig. 1). However, low attenuated lesions on the brain CT scan after 3 days after surgery were regarded as a cerebral infarction as a result of a delayed vasospasm, which occurred generally 4 days after surgery (Fig. 2). Sometimes the brain was retracted through a brain retractor in order to more easily dissect the sylvian cistern and aneurysm, and provide a good operative field. As a result of severe retraction the hemorrhagic infarction on the retraction site occurring immediately after surgery in 2 cases were regarded as a cerebral infarction resulting from the brain retraction (Fig. 3). 
   A new acute cerebral infarction developed after surgery in 20 patients (8.7%). The cause of the infarctions were as follows: 13 patients related to the temporary clipping which occurred within 3 days after surgery, 5 patients due to the vasospasm, and 2 patients due to brain retraction injury. 
   While 16 out of 20 patients (80%) with a cerebral infarction had a favorable outcome, 188 out of 209 patients (96.2%) without a cerebral infarction had a favorable outcome. This suggests that acute cerebral infarction is one of the important factors for a patient's prognosis (Table 2). 
   The incidence of an acute cerebral infarction according to the number of temporary clippings was 5.5% (3 of 55 patients) of those who underwent a single temporary clipping, 6.7% (4 of 60 patients) of those who underwent a two or three times of temporary clippings, and 20.7% (6 of 29 patients) of those who underwent more than 4 times. The incidence of an acute cerebral infarction was significantly higher when the temporary clip had been applied more than 4 times (P<0.021, Table 3). 
   The mean time for the temporary clipping without an acute cerebral infarction within postoperative 3 days (131 patients) was approximately 8 minutes and 24 seconds (504 seconds). The mean temporary clipping time of the patients with an acute cerebral infarction (13 patients) was approximately 16 minutes and 50 seconds (1010 seconds). However, there was no statistically significance (P=0.062). 

Discussion 

   The causes of a cerebral infarction after an aneurismal surgery are variable. Among these cerebral infarctions, some infarctions are inevitable occurred as a result of the clinical state of the patients and radiological findings before surgery, but others are preventable if the neurosurgeon must be careful during the operation. If the predictable causes of a cerebral infarction after surgery such as a preoperative intracerebral hematoma, a preoperative cerebral infarction or a poor clinical state (Hunt and Hess grade V) are excluded, the causes of the cerebral infarction after surgery are related to the procedures during surgery or a delayed vasospasm. In addition, most of these surgical procedures are related to the frequency or time of the temporary clipping which is a useful and essential techniques for the aneurysmal dissection or bleeding control of a premature rupture.⁴⁾ 
   Temporary clipping during cerebral aneurysm surgery is one of the essential techniques for an aneurysmal dissection or to control bleeding of a premature rupture, which blocks blood flow to the aneurysm.^{1)2)7)9)12)14)} However, the frequency or time of the temporary clipping is major factors of cerebral infarction after surgery because temporary clipping blocks off the blood flow to not only to the aneurysm but also to the normal brain tissue. In recent literature, it was reported that the incidence of a cerebral infarction after surgery was reduced when the temporary clipping were performed many times during a short period, as opposed to one time during long period, and the safety time of the temporary clipping is approximately 14 minutes.^{3)6)11)15)16)} However, it was not reported how many temporary clippings were applied. In particular, the cerebral arteries are connected around the Willis’s circle, which means that it is unreasonable for 14 minutes be used in all arteries. For example, although temporary clipping is applied to the ipsilateral internal carotid artery during surgery for an internal carotid artery aneurysm, the contralateral blood flow is supplied through the anterior communicating artery. In addition, although temporary clipping is applied to the proximal portion of the ipsilateral anterior cerebral artery during surgery for an anterior communicating artery aneurysm, the contralateral blood flow is supplied through the anterior communicating artery. Therefore, a postoperative cerebral infarction may not occur even if temporary clipping is applied for a long time. This suggests that the safety time of temporary clipping is not the same for all cerebral aneurysms. However, in a middle cerebral artery aneurysm, invariable time has been comparatively required because the contralateral blood flow, as an internal carotid artery and anterior communicating artery, has not been supplied when temporary clipping is applied to the proximal portion of the middle cerebral artery (M1). Consequently, a middle cerebral artery aneurysm is believed to be the optimal site for investigation in relation to temporary clipping during surgery and a cerebral infarction after surgery if there are no causes that trigger the cerebral infarction clinically and radiologically prior to surgery. In this study patients with middle cerebral artery aneurysm were selected and those patients with preoperative intracerebral hematoma, a cerebral infarction before surgery or a poor clinical state (Hunt and Hess grade V) upon admission were excluded. All the patients selected in this study had a favorable preoperative clinical status without other brain lesions except for a subarachnoid hemorrhage on a brain CT scan. This suggests that a postoperative cerebral infarction is related to the surgical procedures directly or a delayed vasospasm, and is not related to the preoperative state of the patients clinically and radiologically. In particular, it is believed that the cause of the cerebral infarction within postoperative 3 days is related to temporary clipping. According to this study, no cerebral infarctions occurred within 3 days in 85 patients who did not undergo temporary clipping. 
   It has been reported that the incidence of cerebral infarction after surgery is reduced when temporary clipping is performed many times during short period, as opposed to when it is performed once for a long period.^6)15)16) However, it is believed that an investigation into the optimal frequency of the temporary clipping will be necessary. According to the results of this study, the incidence of a postoperative cerebral infarction was significantly higher in patients in whom a temporary clip had been applied more than 4 times. It was considered that the time of the temporary clipping accumulated, in proportion to the increase in frequency. The temporary clipping at the site of the proximal portion of the aneurysm was performed intentionally for a dissection of an aneurysm. The clip was removed approximately 5 minutes after placing the temporary clipping and then the blood flow was perfused again. If the frequency of the temporary clipping was increased gradually, it is necessary to minimize the chance for a cerebral infarction after surgery by extending the reperfusion time intentionally. 
   The safety time for temporary clipping has not been known yet. In this study, the mean temporary clipping time of the patients without an acute cerebral infarction within 3 days after surgery was approximately 8 minutes. However, this cannot be applied to all patients. Although the mean temporary clipping time of the patients with an acute cerebral infarction within 3 days after surgery was approximately 17 minutes, some cases showed that a cerebral infarction could occur within 8 minutes. In addition, even though it was not referred to in this study, the brain perfusion of the middle cerebral artery territory was measured in some patients with a middle cerebral artery aneurysm using a brain perfusion monitor instrument (Q flow 200 perfusion monitoring system, Table 4). The results showed that the perfusion already decreased considerably in the fourth patient within 8 minutes after temporary clipping, and the temporary clipping was removed immediately. Accordingly, 8 minutes is not an absolute value. 
   Temporary clipping is one of the essential techniques for cerebral aneurysm surgery. Accordingly, it is important to know the safety time and frequency during temporary clipping. Therefore, it is believed that the cerebral blood flow has to be monitored, and a brain perfusion monitor during the temporary clipping is more useful method for preventing postoperative cerebral infarction.^{5)8)10)13)17)} 

Conclusion 

   This study examined 229 patients with a middle cerebral artery aneurysm. In 20 of these 229 patients, a new acute cerebral infarction developed after surgery (8.7%). The cause of the infarction is as follows: 13 patients related to temporary clipping (infarction occurring within 3 days after surgery), 5 patients due to delayed vasospasm, and 2 patients due to the brain retraction injury. The incidence of an acute cerebral infarction was significantly higher when the temporary clip had been applied more than 4 times. The mean temporary clipping time of the patients associated with an acute cerebral infarction didn't show statistically significance. 
   Temporary clipping affects the development of a cerebral infarction after aneurismal surgery. However, further clinical studies on the optimal time and frequency of temporary clipping using more cases and brain perfusion monitors will be needed. 

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