Journal of Clinical Neuroscience 22 (2015) 69–72

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Clinical Study

Surgical treatment of patients with unruptured intracranial aneurysms S.F. Chen a, Y. Kato b,⇑, R. Sinha c, A. Kumar d, T. Watabe b, S. Imizu b, J. Oda b, D. Oguri b, H. Sano b, Y. Hirose b a

Department of Neurosurgery, The First Affiliated Hospital of Xiamen University, Xiamen, China Department of Neurosurgery, Fujita Health University Hospital, 1-98, Dengakugakubo, Kutsukake, Toyoake, Aichi 470-1192, Japan c Department of Neurosurgery, St. Stephen’s Hospital, Delhi, India d Department of Neurosurgery, Nizam’s Institute of Medical Science, Hyderabad, India b

a r t i c l e

i n f o

Article history: Received 27 January 2014 Accepted 24 May 2014

Keywords: Clipping Treatment Unruptured intracranial aneurysm

a b s t r a c t We present our experience with elective microsurgical clipping of unruptured intracranial aneurysms (UIA) and analyze this management. A total of 150 patients with UIA were reviewed and data were collected with regard to age, sex, presence of symptoms, location and size of the aneurysms, surgical complications and postoperative 1 year outcomes. Aneurysm size was assessed either by three-dimensional CT angiography or digital subtraction angiogram. Glasgow Outcome Scale was used to assess clinical outcomes. One hundred and fifty patients with 165 aneurysms were treated in this series. The mean size of the UIA was 5.6 mm. Eighty aneurysms (48.5%) were less than 5 mm in size, and 73 (44.2%) were from 5 to 10 mm. Ten (6.1%) of the aneurysms were large and two (1.2%) were giant. One hundred and fortythree were asymptomatic and seven were symptomatic before surgery. The outcome was good in 147 patients (98%), and only three patients (2%) had a treatment-related unfavorable outcome. Five patients experienced transient neurological deficits and one patient experienced permanent neurological deficits. Overall 98.7% of the treated aneurysms were satisfactorily obliterated. Wound complications were seen only in three patients. In conclusion, UIA pose a significant challenge for neurosurgeons, where a delicate balance between benefits and possible risks must be weighed. If the requisite expertise is available, they can be treated surgically with low morbidity and a good outcome at specialized neurovascular centers. Ó 2014 Published by Elsevier Ltd.

1. Introduction

2. Materials and methods

The management of unruptured intracranial aneurysms (UIA) remains one of the most controversial topics in neurosurgery [1–4]. The guidelines for treating UIA differ between countries, with differences in health care systems and epidemiological factors. Recent advances in noninvasive imaging, including CT angiography (CTA), and MR angiography (MRA) have increased the clinician’s ability to diagnose UIA, and the use of new surgical techniques has lead to improved and safe treatment of UIA [5,6]. We present an overview of the results of surgical treatment of UIA at a specialized neurovascular center. We also review the literature regarding the risk of rupture and risk of surgical clipping in UIA and treatment recommendations or guidelines for the management of UIA, to further understand the optimal treatment strategies for an individual patient.

A total of 205 patients with intracranial aneurysms were treated by surgical clipping at our tertiary care centre in Japan between January 2011 and December 2011. All the surgical procedures were performed by two experienced senior neurosurgeons with assistance from four other colleagues. Of these 205 patients, 55 patients with subarachnoid hemorrhage (SAH) due to ruptured aneurysms were excluded. The data reported in this study represent only those who underwent surgical obliteration of UIA. Using the clinical records, we reviewed the 150 patients with UIA and data were collected with regard to age, sex, presence of symptoms, location and size of the aneurysm, surgical complications and postoperative 1 year outcome at follow-up. One hundred and five (70%) patients were female and 45 were male. Patient age ranged between 29 and 79 years (mean age 57.8 years). Most patients were in their sixth (65, 43.3%) or fifth (38, 25.3%) decades of life. Thirty patients (20%) were older than 70 years of age. Aneurysm size was assessed by direct interpretation of three-dimensional CT angiography (3D-CTA) or digital

⇑ Corresponding author. Tel.: +81 56 293 9253; fax: +81 56 293 3118. E-mail address: [email protected] (Y. Kato). http://dx.doi.org/10.1016/j.jocn.2014.05.048 0967-5868/Ó 2014 Published by Elsevier Ltd.

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subtraction angiography. Also, the following measurements of the cerebral aneurysms were collected from the preoperative imaging: maximum height, maximum width of the aneurysmal sac and maximum neck diameter. In this series, micro-Doppler examination was performed after clipping in all patients to assess blood flow in parent and branching vessels. Endoscopy was used to verify correct clipping. In most cases we also used microscope-integrated near-infrared indocyanine green videoangiography. Intraoperative angiography was performed in patients treated by retrograde suction decompression assisted clipping through the existing catheter to confirm obliteration of the aneurysm and patency of the parent vessels. After surgery, all patients underwent postoperative CTA or digital subtraction angiography in specific circumstances. Clinical outcome was assessed by the Glasgow Outcome Scale. 3. Results Altogether, 150 patients with 165 aneurysms were treated in this series. One hundred and six patients had a single aneurysm and 44 (29.3%) patients had multiple aneurysms. Of the 44 patients with multiple aneurysms, 12 were treated with clipping of coexisting aneurysms in the same surgery. Most aneurysms (40%) were in middle cerebral artery (MCA) territory while 24.2% involved the anterior communicating artery complex or the distal anterior cerebral artery (ACA). In the internal carotid artery (ICA), 21.8% aneurysms were in the posterior communicating segment and 10.3% were in the ophthalmic segment. Cavernous segment ICA and basilar artery aneurysms were rare. Anatomical location of all the aneurysms is summarized in Table 1. The mean size of the UIA was 5.6 mm. Eighty aneurysms (48.5%) were less than 5 mm in size, and 73 (44.2%) were from 5 to 10 mm. Ten (6.1%) of the aneurysms were large (10–25 mm) and two (1.2%) were giant (>25 mm). Before surgery 143 aneurysms were asymptomatic and seven were symptomatic. Of the seven symptomatic patients, two presented with visual disturbance and five presented with oculomotor nerve palsy. Of the 143 asymptomatic patients, 29 were found to have UIA during examination for non-specific symptoms, including headache, vertigo or numbness; three were detected during the treatment of other ruptured aneurysms and the remaining 111 patients were found to have UIA during a routine ‘‘brain checkup’’. One anterior communicating artery complex aneurysm and nine distal ACA aneurysms were treated via an interhemispheric approach. Three patients with unruptured superior hypophyseal artery aneurysms were treated via a contralateral pterional approach. Four patients with basilar artery aneurysms were treated via a fronto-temporo-zygomatic craniotomy with combined subtemporal and transylvian (half and half) approach. The remaining patients underwent fronto-temporal craniotomy with ipsilateral pterional approach. Two patients with large ophthalmic segment aneurysms were managed with intentional reconstruction of the aneurysm neck followed by endovascular coiling. Eight patients with large or giant ICA aneurysms were treated by retrograde suction decompression assisted clipping. MCA–superficial Table 1 Distribution of unruptured aneurysms

temporal artery bypass surgery was included in the treatment of one patient with a large MCA aneurysm. After treatment, wound complications were found in three patients (surgical repair for cerebrospinal fluid leak was done in two patients while one patient with wound infection required redo surgery) (Table 2). One patient developed chronic subdural hematomas which required surgical evacuation 2 months after surgery. Frontal contusions, possibly caused by brain retraction, were detected in one patient on the postoperative CT images. There were no deaths related to surgical treatment in this series. The postoperative 1 year outcome was good in 147 patients (98%), and only three patients (2%) had a treatment-related unfavorable outcome. Five patients experienced transient neurological deficits and one patient experienced permanent neurological deficit (Table 2). Overall, 98.7% of the treated aneurysms were satisfactorily obliterated as confirmed by the postoperative 3D-CTA and/or digital subtraction angiography. 4. Discussion The surgical management of patients with UIA has become an area of controversy during the past 20 years, as surgery requires an accurate assessment of risk compared with the natural history of the disease [2,7]. In Japan, UIA are frequently diagnosed by the Brain Docs system (a brain screening program), which not only detects unruptured cerebral aneurysms, but also identifies other asymptomatic brain diseases. This system has gained popularity in the context of increasing use of accurate MRI/MRA [8]. With advances in neuroimaging, UIA are being diagnosed more frequently. Furthermore, the actual risk of surgical obliteration of unruptured aneurysms has probably changed in recent times, with improvement in the surgical armamentarium as well as better postoperative care [7]. The aim of this study was to present an overview of the results of surgical treatment of UIA at a specialized neurovascular center and to analyze our current management strategies. 4.1. Risk of rupture of UIA The prevalence of UIA has been estimated to range between 1 and 6% of the population, depending on the study [3]. The annual rupture risk of all intracranial aneurysms has been reported as between 1 to 3% in retrospective studies. The first international study of unruptured intracranial aneurysms (ISUIA) was based on a retrospective analysis designed to assess the natural history of UIA [9]. They assessed the natural history of unruptured intracranial aneurysms in 1449 patients with 1937 aneurysms. In 727 patients who had no prior history of SAH, the cumulative rate of rupture for aneurysms less than 10 mm in size was less than 0.05% per year, and the rate was approximately 0.5% per year in 722 patients who had a history of SAH. The rupture rate of aneurysms that were 10 mm or more in diameter was less than 1% per year in both groups. However, it is known that the results of the ISUIA were in conflict with those of other studies. Patients of the ISUIA were collected from the time period when UIA were Table 2 Treatment-associated complications

Location

Number

%

Middle cerebral artery Posterior communicating segment Anterior communicating artery Distal anterior cerebral artery Ophthalmic segment Intracavernous sinus Basilar artery Total

66 36 31 9 17 2 4 165

40 21.8 18.9 5.5 10.3 1.2 2.4 100

CSF fistula Wound infection Chronic subdural hematoma Permanent neurological deficits Transient neurological deficits Total complications CSF = cerebrospinal fluid.

Number

%

2 1 1 1 5 10

1.3 0.7 0.7 0.7 3.3 6.7

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operated on, and the retrospective part of the follow-up study did not include all patients who were conservatively managed who also were very likely to be older than those who were excluded due to surgical treatment. In addition, patients with a prior SAH were younger than those without, and it was not analyzed statistically whether aneurysm group (prior SAH or not) was an independent risk factor for aneurysm rupture when age was taken into account [10]. The second study of ISUIA had a prospective evaluation of the natural history of 2686 UIA in 1692 patients [11]. In this analysis, 5 year cumulative rupture rates for patients who did not have a history of SAH with aneurysms located in ICA, anterior communicating artery, ACA, or MCA were 0%, 2.6%, 14.5%, and 40% for aneurysms less than 7 mm, 7–12 mm, 13–24 mm, and 25 mm or greater, respectively, compared with rates of 2.5%, 14.5%, 18.4%, and 50%, respectively, for the same size categories involving posterior circulation and posterior communicating artery aneurysms. On the basis of the rupture rates reported by ISUIA, one can generally conclude that surgical treatment of UIA less than 7 mm in size and located in the ICA, ACA or MCA territory is not advisable. However, some studies have found that even smaller UIA carry a risk of rupture. The small unruptured aneurysm verification study (SUAVe Study, Japan) reported in 2004 that the annual rupture rate of small unruptured aneurysms (under 5 mm diameter) was 0.8% and another 18 aneurysms enlarged during follow-up [12]. Important factors for aneurysmal rupture and enlargement were multiplicity of aneurysms, female sex, patient aged over 70 years, and location of the aneurysm (higher risk in ACA and basilar artery aneurysms). The growth rate may be faster in multiple aneurysms than in any single aneurysm [12]. In 2010, after patients had been followed for a mean of 41.0 months, the study demonstrated the average annual risk of rupture of single unruptured aneurysms less than 5 mm in diameter as 0.34% per year, that of multiple unruptured aneurysms was 0.95% per year, and the overall rate was 0.54% per year [13]. Furthermore, Ohashi et al. reported a series of 280 patients with ruptured aneurysms, of which 74.3% ranged between 1 and 10 mm [14]. Additionally the International Subarachnoid Aneurysm Trial (ISAT) of 2143 patients with SAH showed half of the aneurysms to be less than 5 mm and an additional 40% were between 6 and 10 mm. This discrepancy may be due to some limitations of ISUIA. For example, lower-risk aneurysms such as cavernous segment aneurysms were overrepresented [15]. During the study, 534 of the 1692 patients were switched to a therapeutic intervention and were removed from follow-up. Fifty-two who died of intracranial hemorrhage were also removed from the analysis, but it is unclear whether there was adequate evaluation to ensure that these intracranial hemorrhages were not a result of aneurysmal rupture [3]. Also, many of the investigators in ISUIA were experienced aneurysm surgeons, and the study subjects were probably carefully selected to be at a relatively low risk of rupture. Also, the patients followed by ISUIA were aware of their aneurysms and may have taken steps, such as healthy lifestyle habits, that may have reduced their risk of rupture [15]. The best way to study the natural history of unruptured aneurysms is to simply observe them without treatment incidentally diagnosed [13]. Juvela et al. provided a comprehensive observational study that lacked the bias of surgical selection, because all unruptured aneurysms were not surgically treated in their department before 1979. In 1993, the authors followed 142 patients with 181 unruptured aneurysms, of which the median diameter was 4 mm at the beginning of the follow-up period, for a median of 13.9 years. They reported an annual rupture risk of 1.4% [16]. The cumulative rate of bleeding was 10% at 10 years, 26% at 20 years, and 32% at 30 years after the diagnosis. In 2000, when the median follow-up time was 19.7 years, they reported an average annual

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rupture incidence of 1.3% and the cumulative rate of bleeding was 10.5% at 10 years, 23% at 20 years, and 30.3% at 30 years after diagnosis [17]. 4.2. Risk of surgical clipping of UIA The risk of surgical clipping of UIA cannot be ignored, especially when deciding the treatment strategy. Reported outcomes vary significantly between types of studies. In a meta-analysis which included 61 studies in 1998, Raaymakers et al. identified that mortality was 2.6% and permanent morbidity occurred in 10.9% of patients [18]. The assessment of 1917 patients in the ISUIA study in 2003 showed 1.5% mortality and 11.7% morbidity at 30 days, and 2.3% mortality and 9.8% morbidity at 1 year [11]. In 2005, Tony Lee et al. reported the cumulative clipping mortality and morbidity in 30 studies including 11,363 patients, was 17.8% (ranged from 0.0% to 25.1%) [1]. However, these findings are usually not applicable to individual surgical patients with UIA, because surgical difficulty varies according to the size and location of the aneurysm [2]. There have been no studies of surgical risk based on the location and size of an aneurysm to our knowledge. Meanwhile, it is noteworthy that classification of morbidity varied widely in different studies. There has been an excessive emphasis on the necessity for surgical treatment of large UIA because of their higher risk of rupture. However, the higher surgical risk should also be considered while treating these large UIA. Careful consideration of surgical risk and detailed informed consent are necessary for patients with large UIA. To improve the surgical results, the neurosurgeon should be careful to avoid ischemic complications, including perforator injuries or temporary occlusion of the parent artery. For preservation of the perforator or parent artery, dome clipping with or without wrapping should be performed in cases where a high risk for perforator injury and parent artery occlusion or stenosis by neck clipping is anticipated [2]. When discussing the risk of surgical clipping of UIA, an issue rarely mentioned, despite its importance, is the experience of the neurosurgeon [2]. Results are definitely much better at centers dealing with high numbers of aneurysms. Since most of the patients with UIA are asymptomatic, clipping surgery must always try to minimize the operative risks as far as possible. Furthermore, with advances in endovascular technique, conventional microneurosurgeons are now facing more complex cerebral aneurysms, which cannot be simply obliterated using the usual microsurgical techniques. Bypass techniques and skull base techniques are often required in the management of some wide neck aneurysms [3,19]. At our center, residents are not allowed to perform a clipping surgery for an unruptured aneurysm. The senior neurosurgeons perform the surgery or guide the junior neurosurgeons during the whole procedure, transferring their experience to the younger neurosurgeons and residents, which is thus, an optimal strategy to master any art. In our series, there were no deaths related to surgical treatment and the postoperative 1 year follow-up revealed that only three patients (2%) had a treatment-related unfavorable outcome. Our results show good consistency with the results available in the literature at the time of writing [2,19,20]. Use of new surgical techniques, for instance, intraoperative indocyanine green angiography, has contributed immensely in achieving optimal outcomes for UIA [6]. 4.3. Surgical strategy Decision-making during the management of UIA is a delicate process for both neurosurgeons and patients. It is well known that guidelines differ between countries, with differences in health care systems and epidemiological factors [8]. In Finland, based on their

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long-term follow-up, Juvela recommended surgical or endovascular treatment for all aneurysms

Surgical treatment of patients with unruptured intracranial aneurysms.

We present our experience with elective microsurgical clipping of unruptured intracranial aneurysms (UIA) and analyze this management. A total of 150 ...
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