Original Article
Outcome After Clipping of Unruptured Intracranial Aneurysms Depends on Caseload ¨ zkan1, Ramazan Jabbarli1, Karsten H. Wrede1, Daniela Pierscianek1, Philipp Dammann1, Nicolai El Hindy1, Neriman O 1 1 2 1 Oliver Mu¨ller , Dietmar Stolke , Michael Forsting , Ulrich Sure
OBJECTIVE: Although most neurovascular centers currently have a coil first policy, the percentage of coiled versus clipped aneurysms, as well as treatment outcomes, varies strongly between these centers. This study evaluates the impact of an increase in clipping caseload on treatment outcome in a large single-center series.
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METHODS: All consecutive patients who underwent microsurgical clipping of unruptured intracranial aneurysms between January 2003 and April 2014 in our department were analyzed retrospectively. According to the change of the chairman in the neurosurgical department (1 September 2008) with a subsequent increase in the clipping volume, the entire cohort was divided into 2 groups with equal time intervals (historic and current cohorts).
CONCLUSIONS: The improvement of the surgical outcome after increasing the clipping caseload underlines the importance of sufficient surgical volume for maintenance of competitive treatment results.
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RESULTS: There were 94 clipped unruptured intracranial aneurysms in the historic cohort and 252 in the current cohort. Unfavorable outcome at 6 months postoperatively (defined as modified Rankin Score >2) was observed in 8 cases (8.5%) in the historic cohort and 7 cases (2.8%) in the current cohort (P < 0.0001). The surgical mortality decreased from 3.2% to 0%. Cerebral infarction on postoperative computed tomography scan was observed in 25 cases (26.6%) in the historic cohort and 19 cases (7.5%) in the current cohort (P < 0.0001). Within the current cohort, there was a progressive improvement of surgical outcome over the time.
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Key words Cerebral infarct - Clipping - Complication - Morbidity - Mortality - Outcome - Unruptured intracranial aneurysm -
Abbreviations and Acronyms CT: Computed tomography DSA: Digital subtraction angiography EM: Electrophysiologic monitoring ICG VA: Indocyanine green videoangiography
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INTRODUCTION
R
ecent improvements in noninvasive imaging techniques and their greater availability have resulted in more frequent detection and treatment of unruptured intracranial aneurysms (UIAs).1,2 Because of the progressive refinement of endovascular techniques, including the introduction of balloonassisted and stent-supported coiling as well as flow diverters and Web devices, the number of aneurysms treated by means of coil embolization rather than open surgery has substantially increased.3 In particular, the percentage of UIAs treated in the United States by means of coiling increased from 20% in 2001 to 63% in 2008.4 The resulting decrease in microsurgical volume has been shown to be associated with a worse clinical outcome after neurosurgical clipping.5 This unfavorable trend carries the risk for aneurysm surgery to be even less competitive in the future. Despite the increasing popularity of endovascular coiling in the therapy of UIAs, the final treatment allocation is still a matter of interdisciplinary decision between the neurosurgeon and the neurointerventionalist. In our high-volume neurovascular center (about 170 aneurysms treated annually), endovascular coiling became an increasingly dominant treatment option for intracranial aneurysms in the late
OR: Odds ratio UIA: Unruptured intracranial aneurysm From the 1Department of Neurosurgery, University Hospital of Essen, Essen; and 2Institute for Diagnostic and Interventional Radiology, University Hospital of Essen, Essen, Germany To whom correspondence should be addressed: Ramazan Jabbarli, M.D. [E-mail: [email protected]] Supplementary digital content available online. Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2015.12.043 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
1990s to early 2000s. However, after the appointment of a new chairman in the neurosurgical department on 1 September 2008, there was a new consensus between neurosurgical and neuroradiologic departments on a more balanced treatment allocation. Subsequently, a significant rearrangement of the clip/coil ratio has been observed since then in favor of aneurysm clipping. Based on this single-center real-life experience, we aimed to identify the impact of the increase in clipping caseload on postoperative functional outcome and clipping-related complications. METHODS Patient Population and Study Design This retrospective review was based on our institutional aneurysm database containing all consecutive patients with intracranial aneurysms treated in our university hospital since 1 January 2003. All individuals with primary microsurgical clipping of saccular UIAs were eligible for this study. The following cases were excluded from the final analysis: 1) patients with wrapped aneurysms without the use of a clip; 2) clipping of a UIA during the first 3 weeks after subarachnoid hemorrhage from another ruptured aneurysm; 3) poor clinical condition (defined as modified Rankin Score6 >2) before UIA surgery. All cases included in the final analysis were divided into 2 groups: patients treated between 1 January 2003 and 31 August 2008 were allocated to the historic cohort; all patients operated on after the change of the chairmanship (1 September 2008) were included in the current cohort. For the formation of 2 identical time intervals of 68 months each, the current cohort contained all appropriate cases treated until 30 April 2014. Data were collected after the approval of the institutional ethics committee (EthikKommission, Medizinische Fakultät der Universität DuisburgEssen, registration number, 15-6331-BO) and registration in the German clinical trial register (DRKS, unique identifier, DRKS00008749). Clinical Management of UIAs The diagnostic workup of UIAs and the decision on the advisability of UIA treatment remained unchanged across the time interval investigated. Diagnostic digital subtraction angiography (DSA) was obligatory in all cases before treatment allocation. Decision making regarding the necessity for treatment of the UIA, as well as the subsequent allocation to coiling or clipping, was always discussed interdisciplinarily between the senior neurosurgeon and the senior neuroradiologist, taking into account the available literature on the topic,7,8 the personal experience of the specialists involved, and the above-mentioned consensus on balanced treatment allocation. All clipping procedures were performed in a microsurgical manner and included the obligatory use of at least 1 intraoperative blood flow monitoring tool (microvascular Doppler ultrasonography or indocyanine green videoangiography [ICG VA]). In addition, electrophysiologic monitoring (EM) was also applied in most surgeries, depending on the individual decision of the neurosurgeon. The patients were routinely admitted postoperatively to our neurosurgical intensive care unit for 1 day, unless a longer stay was required for clinical reasons. All patients underwent early
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postoperative computed tomography (CT) within 24 hours after the operation. In cases of delayed postoperative neurologic deficits, additional follow-up CT scans were also performed. Moreover, postoperative DSA was routinely performed during the first week after clipping for the documentation of aneurysm occlusion. The patients underwent routine outpatient clinical follow-up at 6 months after surgery. Data Management The following outcome measurements were defined as study end points: A) development of cerebral infarction on postoperative CT scan; B) incomplete aneurysm obliteration necessitating direct retreatment defined as grade IV or V aneurysm remnants according to the Sindou classification9; C) parent vessel stenosis on postoperative DSA defined as any narrowing of the parent vessel at the site of the clip as documented by the radiologists; D) unfavorable outcome at 6 months after surgery (defined as modified Rankin Score >2), when surgical mortality was also addressed. Demographic and clinical data of the patients on admission and during the hospital stay were retrospectively collected from the hospital chart records. The characteristics of the clipped aneurysms (location, size of neck and dome) were collected from the preoperative DSA reports. All postoperative CT scans were reviewed to identify new cerebral infarctions. Hypodensities on CT imaging resulting from the surgical approach were excluded from the analysis. Postoperative DSAs were reviewed with regard to aneurysm obliteration and parent vessel stenosis (or occlusion) by clip material. The expertise of surgeons was operationalized as the number of years since the neurosurgical board examination and the individual complication rates. None of the surgeons underwent subspecialty training in cerebrovascular surgery outside our institution. Statistical Analysis The baseline characteristics of the cohorts were univariately correlated. Continuous variables were analyzed using the Student t test for normally distributed data and the Mann-Whitney U test for nonnormally distributed data. Categorical variables were analyzed using the c2 test or Fisher exact test, as appropriate. Multivariate binary logistic analysis (using stepwise backward regression) was performed to evaluate the impact of the clipping caseload on postoperative functional outcome, with the inclusion of potential confounders (patients’ age and use of intraoperative diagnostic tools). Differences with a P value 2 before the surgery). Accordingly, 94 unruptured intracranial aneurysms (UIAs) fulfilled the inclusion criteria in the historic cohort. In the current cohort, 432 aneurysms were surgically treated. Of these, 176 were clipped during subarachnoid hemorrhage and therefore were excluded. In addition, 4 cases were disregarded because of the poor initial modified Rankin Score. As a result, 252 clipped unruptured intracranial aneurysms were included in the final analysis from the current cohort.
UIAs were included in the final analysis. Of these, 94 UIAs were clipped before 1 September 2008 and 252 thereafter (i.e., >2.6fold increase of the number of clipped UIAs). The baseline demographic and clinical characteristics of the treated patients are shown in Table 1. Treatment Outcome Cerebral infarction was documented on the postoperative CT scan(s) in 25 cases (26.6%) in the historic cohort. In the current
Table 1. Demographic and Clinical Characteristics of the Treated Patients Characteristic Age, years
Historic Cohort, Current Cohort, P Mean (SD) or n (%) Mean (SD) or n (%) Value 49.6 (10.8)
53.9 (10.3)
0.0006
Sex, female
66 (70.2)
187 (74.2)
0.4121
Aneurysm size, mm
7.4 (5.6)
6.7 (3.9)
0.9409
Aneurysm location
0.2756
MCA
65 (69.1)
187 (74.2)
ICA
14 (14.9)
24 (9.5)
ACA
12 (12.8)
38 (15.1)
3 (3.2)
3 (1.2)
PC
SD, standard deviation; MCA, middle cerebral artery; ICA, internal carotid artery; ACA, anterior cerebral artery; PC, posterior circulation.
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cohort, this complication was seen less frequently; only 19 UIA surgeries (7.5%) were associated with postoperative cerebral infarction (P < 0.0001; odds ratio [OR], 0.23; 95% confidence interval, 0.12e0.43, see Figure 2). In both cohorts, the probability of the clipping-related cerebral infarction was independent from UIA location. Parent vessel stenosis was visualized in 5 postoperative DSAs in both groups indicating the reduction of this complication from 5.3% to 2% (OR, 0.36; P ¼ 0.1428). Incomplete UIA occlusion requiring retreatment was documented in postoperative DSAs in 4 cases (4.3%) in the historic and 5 cases (2%) in the current cohort (OR, 0.46; P ¼ 0.2614). More detailed data on the rates of aneurysm remnants after clipping and their clinical consequences have already been reported elsewhere.9 In the historic cohort, an unfavorable outcome at 6 months follow-up occurred after 8 operations (8.5%). In contrast, only 7 UIAs (2.8%) were associated with an unfavorable outcome in the current cohort (OR, 0.31; 95% confidence interval, 0.11e0.87; P ¼ 0.0332). Moreover, 3 patients (3.2%) died in the historic cohort as a result of surgical complications, whereas no surgical mortality was documented in the current cohort. One patient treated in the current cohort had an uncomplicated postoperative course. However, in the further postoperative clinical course, this patient experienced a subarachnoid hemorrhage from an untreated basilar tip aneurysm scheduled for treatment. This patient died as a result of the complications of subarachnoid hemorrhage. Further subanalysis within the current cohort showed that the surgical outcome progressively improved over time. In particular, 6 of 7 cases (>85%) with surgical morbidity occurred during the first half of the period for the current cohort (Supplementary Figure 1). Surgical Aspects The surgical staff were analyzed for the entire period of the study, including individual clipping and complication rates. The individual clipping volume significantly increased over the 2 time intervals; the mean annual caseload for each neurovascular surgeon (as primary surgeon) increased from 6.5 to 17.5 aneurysms (P ¼ 0.0026). The individual complication rates ranged between 0% and 28.6% in the historic cohort and between 0% and 7.7% in the current cohort. The individual complication rates appeared to be more balanced in the current cohort (standard deviation 2.95 versus 9.63 in the historic cohort). The surgical staff gradually changed over this 11-year period; about half of UIAs were clipped by the same 4 surgeons in both groups (50 and 111 UIAs in the historic and current cohorts, respectively). In addition to the new neurosurgical chairman, the remaining neurosurgeons not presented in the historic cohort (n ¼ 6) were our former residents who trained for neurovascular surgery at our institution after the increase of the clipping caseload. Regarding surgical experience, the surgeons in the current cohort were significantly younger (mean time after the neurosurgical board examination was 6.9 years [ 4.4] versus 14.2 years [ 8.7] for the surgeons in the historic cohort; P < 0.0001). Although ICG VA and EM were more frequently used in the current cohort (P < 0.0001), these intraoperative diagnostic tools did not correlate with the functional outcome. In addition, the
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
Table 2. Multivariate Logistic Regression Analysis for the Predictors of Unfavorable Functional Outcome After Unruptured Intracranial Aneurysm Clipping Steps 1
Figure 2. The frequency and rate of cerebral infarction identified on postoperative computed tomography scans was significantly lower in the current cohort compared with the historic cohort.
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improvement in functional outcome in the patients treated after September 2008 was independent of the above-mentioned diagnostic tools in the multivariate analysis (Table 2). DISCUSSION This single-center retrospective observational study shows significantly better surgical outcome and fewer clipping-related complications as a result of the increase of surgical volume. Increasing Dominance of Endovascular Coiling A Trend without any Cons? First described by Walter Dandy in 1938,10 surgical clipping of intracranial aneurysms remained the only treatment option for this potentially fatal cerebral pathology over many decades.11 After the invention of endovascular aneurysm coiling in 1991 by Guido Guglielmi12 and publication of data from the International Subarachnoid Aneurysm Trial in 2005,7 endovascular intervention has become the first-line treatment for ruptured intracranial aneurysms and UIAs in many neurovascular centers.13 Technical progress in endovascular treatments, including the introduction of balloon- and stent-assisted coiling as well as flow diverters and Web devices, has substantially changed the ratio between endovascular treatments and open surgery in favor of the endovascular approach.3 In particular, the proportion of UIAs treated in the United States with coiling increased from 20% in 2001 to 63% in 2008.4 In a recent publication from the United Kingdom, Teo et al.14 reported a 6fold decrease in the number of surgically treated intracranial aneurysms in their center. This decreasing trend of microsurgical clipping may have a substantial effect on treatment outcome of surgically treated individuals. Zacharia et al.5 showed that the decrease of microsurgical volume has worsened clipping results. Furthermore, Le Reste et al.15 identified a significant correlation between surgical neurovascular experience and the risk for intraoperative complications during aneurysm surgery. According to recent data, surgical treatment of UIA is associated with a 1.06%e4.9% risk of permanent morbidity2,16,17 and 0%e 1.6% mortality2,18. Although these results are better compared with reports from the last decades,1 endovascular treatment shows superior results in terms of functional disability (at least, for the
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4
5
Parameter Surgery in current cohort*
Odds Ratio (95% Confidence Interval)
P Value
0.99 (0.99e1.00)
0.055
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.74 (0.58e12.85)
0.203
Aneurysm locationz
1.23 (0.66e2.32)
0.513
Use of intraoperative ICG VA
1.84 (0.52e6.47)
0.343
Use of intraoperative EM
0.58 (0.20e1.69)
0.316
Surgery in current cohort*
0.99 (0.99e1.00)
0.056
Agey
1.09 (1.03e1.16)
0.004
Sex, female
2.68 (0.57e12.53)
0.211
Use of intraoperative ICG VA
1.79 (0.51e6.27)
0.365
Use of intraoperative EM
0.59 (0.20e1.72)
0.335
Surgery in current cohort*
0.99 (0.99e1.00)
0.009
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.79 (0.60e12.97)
0.191
Use of intraoperative EM
0.64 (0.22e1.82)
0.402
Surgery in current cohort*
0.99 (0.99e1.00)
0.010
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.81 (0.61e13.03)
0.186
Surgery in current cohort*
0.99 (0.99e1.00)
0.012
Agey
1.09 (1.03e1.15)
0.005
ICG VA, indocyanine green videoangiography; EM, electrophysiologic monitoring. *Per day since 1 September 2008. yPer year in age increase. zThe location of the treated aneurysm was presented as a scale based on the rates of surgical cases: 1, MCA; 2, ACA; 3, ICA; 4, PC.
short-term outcome) and treatment-related complications in many meta-analyses.19,20 Taking into account the continuously decreasing percentage of clipped aneurysms in most neurovascular centers, there is a serious risk for further worsening of surgical results. We acknowledge the currently dominant role of endovascular coiling for treatment of patients with intracranial aneurysms. Nevertheless, microsurgical clipping remains an important component of aneurysm management. Certain intracranial aneurysms remain better candidates for open surgery than for coiling.20 Moreover, microsurgical clipping provides higher occlusion rates and therefore ensures a lower rebleeding risk than endovascular treatment.21 In addition, there is also a need for surgical retreatment for specific cases of incompletely coiled aneurysms (and vice versa).22 The recent developments toward bypass surgery may become a lifesaving alternative for some complex aneurysms.23 Therefore, the availability of a safe and competitive microsurgical treatment for intracranial aneurysms is of
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
paramount importance for the entire population of aneurysm carriers. Increase of Surgical Volume Improves the Outcome of Clipping In our series, the treatment in the current cohort (characterized by an increase in surgical volume) and younger age of patients were independently associated with a favorable outcome after aneurysm surgery. In particular, permanent postoperative morbidity was significantly reduced from 8.5% to 2.8%. Moreover, surgical mortality could be completely eliminated (from 3.2% to 0%). This improvement in functional outcome was as a result of the reduction in clipping-related complications, especially cerebral infarction. Apart from the significantly higher age of the patients in the current cohort, the remaining baseline parameters of both cohorts were similar, including the characteristics of the treated UIAs. The higher age of the patients in the current cohort meant a higher risk for unfavorable outcome and cerebral infarction. The strong association between these factors is well acknowledged24 and is also shown in our multivariate analysis (P ¼ 0.005, Table 2). Regarding the use of intraoperative diagnostic modalities, ICG VA and EM have been more frequently applied in recent years. A positive effect of these intraoperative technical advances on clipping results is widely acknowledged.25,26 However, in our univariate and multivariate analyses, ICG VA and EM were not associated with the functional outcome. The increase in the institutional caseload was associated with a significant increase in the individual caseload for each neurosurgeon. In addition, our analyses pointed to a more balanced distribution of the complication rates in the current cohort. This apparently reflects a certain level of neurovascular surgical expertise for all neurosurgeons operating at the time of higher clipping caseload. Moreover, the risk for unfavorable outcome decreased progressively (Supplementary Figure 1) within the current cohort, a sign of further gradual improvement of neurovascular surgical expertise. We believe that our data reflect the substantial role of increased surgical volume for improvement of surgical outcome and complication rates. These findings are in line with previous reports5,15 on the negative correlation between clipping results and neurovascular surgical expertise.
REFERENCES 1. Raaymakers TW, Rinkel GJ, Limburg M, Algra A. Mortality and morbidity of surgery for unruptured intracranial aneurysms: a meta-analysis. Stroke. 1998;29:1531-1538. 2. Kunz M, Bakhshai Y, Zausinger S, Fesl G, Janssen H, Brückmann H, et al. Interdisciplinary treatment of unruptured intracranial aneurysms: impact of intraprocedural rupture and ischemia in 563 aneurysms. J Neurol. 2013;260:1304-1313. 3. Nussbaum ES, Madison MT, Myers ME, Goddard J. Microsurgical treatment of unruptured intracranial aneurysms. A consecutive surgical experience consisting of 450 aneurysms treated in the endovascular era. Surg Neurol. 2007;67:457-464 [discussion: 464-456].
Sufficient neurovascular surgical expertise is paramount for providing competitive treatment results in aneurysm surgery. In the face of the worldwide decreasing ratio of clipped aneurysms, establishment of nationwide specialized neurovascular centers with higher caseloads should be considered. This can help to improve surgical outcome for individual patients, as well as ensure excellent training for future neurovascular surgeons. Study Limitations Because of the retrospective study design, the quality of the presented data depends on the accuracy of the documentation in the electronic medical reports. Moreover, the role of surgeondependent impact on surgical outcome cannot be fully ruled out, because both cohorts were not treated by the same neurosurgeons (with the same clipping rates). In addition, our analysis cannot exclude all potential confounders of unfavorable outcome (such as the complications arising from perioperative anesthesiologic and intensive care). Regarding the risk of cerebral infarction, magnetic resonance imaging would have been preferable over CT for infarct detection.27 However, magnetic resonance imaging was not available in most cases as a routine postoperative follow-up. Our analysis is based on a single-center case series, which limits the generalizability of the results. Nevertheless, our real-life experience presents a rare circumstance in the current era of endovascular dominance. Therefore, we believe that the presented data will be of value for future treatment strategies for intracranial aneurysms. CONCLUSIONS Clipping volume seems to be a key factor for improvement of clipping outcome and reduction of the risk for clipping-related complications. Substantial neurovascular surgical expertise is of paramount importance to ensure competitive treatment results of aneurysm clipping. ACKNOWLEDGMENTS We would like to give special thanks to Prof. Dr. Ilonka Kreitschmann-Andermahr (Department of Neurosurgery, University Hospital of Essen) for critically revising the manuscript before submission.
4. Brinjikji W, Rabinstein AA, Nasr DM, Lanzino G, Kallmes DF, Cloft HJ. Better outcomes with treatment by coiling relative to clipping of unruptured intracranial aneurysms in the United States, 2001-2008. AJNR Am J Neuroradiol. 2011;32: 1071-1075. 5. Zacharia BE, Ducruet AF, Hickman ZL, Grobelny BT, Badjatia N, Mayer SA, et al. Technological advances in the management of unruptured intracranial aneurysms fail to improve outcome in New York state. Stroke. 2011;42: 2844-2849. 6. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604-607.
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7. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809-817. 8. Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110. 9. Jabbarli R, Pierscianek D, Wrede K, Dammann P, Schlamann M, Forsting M, et al. Aneurysm remnant after clipping: the risks and consequences. J Neurosurg. 2016. in press.
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10. Dandy WE. Intracranial aneurysm of the internal carotid artery: cured by operation. Ann Surg. 1938; 107:654-659.
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unruptured intracranial aneurysms. J Clin Neurosci. 2015;22:69-72.
11. Kivisaari RP, Porras M, Ohman J, Siironen J, Ishii K, Hernesniemi J. Routine cerebral angiography after surgery for saccular aneurysms: is it worth it? Neurosurgery. 2004;55:1015-1024.
18. Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, et al. Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke. 2010;41: 1471-1476.
12. Guglielmi G, Vinuela F, Sepetka I, Macellari V. Electrothrombosis of saccular aneurysms via endovascular approach. Part 1: Electrochemical basis, technique, and experimental results. J Neurosurg. 1991;75:1-7.
19. Hwang JS, Hyun MK, Lee HJ, Choi JE, Kim JH, Lee NR, et al. Endovascular coiling versus neurosurgical clipping in patients with unruptured intracranial aneurysm: a systematic review. BMC Neurol. 2012;12:99.
13. Giussani C, Mejdoubi M, Tremoulet M, Roux FE. The role of surgery when endovascular treatment is considered the first choice therapy for ruptured intracranial aneurysms. J Neurosurg Sci. 2008;52: 61-69. 14. Teo M, Martin S, Ponweera A, Macey A, Suttner N, Brown J, et al. Results of surgical clipping in a neurointerventional dominant department. Br J Neurosurg. 2015:1-7. 15. Le Reste PJ, Henaux PL, Riffaud L, Haegelen C, Morandi X. Influence of cumulative surgical experience on the outcome of poor-grade patients with ruptured intracranial aneurysm. Acta Neurochir (Wien). 2015;157:1-7. 16. Brown RD Jr, Broderick JP. Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurology. 2014;13:393-404. 17. Chen SF, Kato Y, Sinha R, Kumar A, Watabe T, Imizu S, et al. Surgical treatment of patients with
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20. Lanzino G, Murad MH. d’Urso PI, Rabinstein AA. Coil embolization versus clipping for ruptured intracranial aneurysms: a meta-analysis of prospective controlled published studies. AJNR Am J Neuroradiol. 2013;34:1764-1768. 21. Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DPH, et al. Clipping versus coiling for ruptured intracranial aneurysms: a systematic review and meta-analysis. Stroke. 2013;44:29-37. 22. Waldron JS, Halbach VV, Lawton MT. Microsurgical management of incompletely coiled and recurrent aneurysms: trends, techniques, and observations on coil extrusion. Neurosurgery. 2009; 64(5 suppl 2):301-315 [discussion: 315-317]. 23. Maldaner N, Guhl S, Mielke D, Musahl C, Schmidt NO, Wostrack M, et al. Changes in volume of giant intracranial aneurysms treated by surgical strategies other than direct clipping. Acta Neurochir (Wien). 2015;157:1117-1123 [discussion: 1123].
24. Jabbarli R, Reinhard M, Roelz R, Shah M, Niesen WD, Kaier K, et al. Early identification of individuals at high risk for cerebral infarction after aneurysmal subarachnoid hemorrhage: the BEHAVIOR score. J Cereb Blood Flow Metab. 2015;35: 1587-1592. 25. Jo KI, Kim HR, Yeon JY, Hong SC, Kim JS. Treatment outcomes of surgical clipping for unruptured anterior circulation aneurysm-single institute experiences in the era of neurophysiologic monitoring and endovascular treatment. Neurosurg Rev. 2015;38:677-682. 26. Dengler J, Cabraja M, Faust K, Picht T, Kombos T, Vajkoczy P. Intraoperative neurophysiological monitoring of extracranial-intracranial bypass procedures. J Neurosurg. 2013;119:207-214. 27. Kivisaari RP, Salonen O, Servo A, Autti T, Hernesniemi J, Ohman J. MR imaging after aneurysmal subarachnoid hemorrhage and surgery: a long-term follow-up study. AJNR Am J Neuroradiol. 2001;22:1143-1148. Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 16 November 2015; accepted 10 December 2015 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2015.12.043 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
Supplementary Figure 1. Cumulative percentage of surgical complications in the current cohort. The figure shows a progressive improvement of the clipping outcome over time. In particular, >85% (6 of 7) of all cases with unfavorable outcome occurred during the first half of the observational time of the current cohort (the dashed lines). Moreover, about half of the complications happened between September 2008 and January 2010.
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Outcome After Clipping of Unruptured Intracranial Aneurysms Depends on Caseload ¨ zkan1, Ramazan Jabbarli1, Karsten H. Wrede1, Daniela Pierscianek1, Philipp Dammann1, Nicolai El Hindy1, Neriman O 1 1 2 1 Oliver Mu¨ller , Dietmar Stolke , Michael Forsting , Ulrich Sure
OBJECTIVE: Although most neurovascular centers currently have a coil first policy, the percentage of coiled versus clipped aneurysms, as well as treatment outcomes, varies strongly between these centers. This study evaluates the impact of an increase in clipping caseload on treatment outcome in a large single-center series.
-
METHODS: All consecutive patients who underwent microsurgical clipping of unruptured intracranial aneurysms between January 2003 and April 2014 in our department were analyzed retrospectively. According to the change of the chairman in the neurosurgical department (1 September 2008) with a subsequent increase in the clipping volume, the entire cohort was divided into 2 groups with equal time intervals (historic and current cohorts).
CONCLUSIONS: The improvement of the surgical outcome after increasing the clipping caseload underlines the importance of sufficient surgical volume for maintenance of competitive treatment results.
-
-
RESULTS: There were 94 clipped unruptured intracranial aneurysms in the historic cohort and 252 in the current cohort. Unfavorable outcome at 6 months postoperatively (defined as modified Rankin Score >2) was observed in 8 cases (8.5%) in the historic cohort and 7 cases (2.8%) in the current cohort (P < 0.0001). The surgical mortality decreased from 3.2% to 0%. Cerebral infarction on postoperative computed tomography scan was observed in 25 cases (26.6%) in the historic cohort and 19 cases (7.5%) in the current cohort (P < 0.0001). Within the current cohort, there was a progressive improvement of surgical outcome over the time.
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Key words Cerebral infarct - Clipping - Complication - Morbidity - Mortality - Outcome - Unruptured intracranial aneurysm -
Abbreviations and Acronyms CT: Computed tomography DSA: Digital subtraction angiography EM: Electrophysiologic monitoring ICG VA: Indocyanine green videoangiography
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INTRODUCTION
R
ecent improvements in noninvasive imaging techniques and their greater availability have resulted in more frequent detection and treatment of unruptured intracranial aneurysms (UIAs).1,2 Because of the progressive refinement of endovascular techniques, including the introduction of balloonassisted and stent-supported coiling as well as flow diverters and Web devices, the number of aneurysms treated by means of coil embolization rather than open surgery has substantially increased.3 In particular, the percentage of UIAs treated in the United States by means of coiling increased from 20% in 2001 to 63% in 2008.4 The resulting decrease in microsurgical volume has been shown to be associated with a worse clinical outcome after neurosurgical clipping.5 This unfavorable trend carries the risk for aneurysm surgery to be even less competitive in the future. Despite the increasing popularity of endovascular coiling in the therapy of UIAs, the final treatment allocation is still a matter of interdisciplinary decision between the neurosurgeon and the neurointerventionalist. In our high-volume neurovascular center (about 170 aneurysms treated annually), endovascular coiling became an increasingly dominant treatment option for intracranial aneurysms in the late
OR: Odds ratio UIA: Unruptured intracranial aneurysm From the 1Department of Neurosurgery, University Hospital of Essen, Essen; and 2Institute for Diagnostic and Interventional Radiology, University Hospital of Essen, Essen, Germany To whom correspondence should be addressed: Ramazan Jabbarli, M.D. [E-mail: [email protected]] Supplementary digital content available online. Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2015.12.043 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
1990s to early 2000s. However, after the appointment of a new chairman in the neurosurgical department on 1 September 2008, there was a new consensus between neurosurgical and neuroradiologic departments on a more balanced treatment allocation. Subsequently, a significant rearrangement of the clip/coil ratio has been observed since then in favor of aneurysm clipping. Based on this single-center real-life experience, we aimed to identify the impact of the increase in clipping caseload on postoperative functional outcome and clipping-related complications. METHODS Patient Population and Study Design This retrospective review was based on our institutional aneurysm database containing all consecutive patients with intracranial aneurysms treated in our university hospital since 1 January 2003. All individuals with primary microsurgical clipping of saccular UIAs were eligible for this study. The following cases were excluded from the final analysis: 1) patients with wrapped aneurysms without the use of a clip; 2) clipping of a UIA during the first 3 weeks after subarachnoid hemorrhage from another ruptured aneurysm; 3) poor clinical condition (defined as modified Rankin Score6 >2) before UIA surgery. All cases included in the final analysis were divided into 2 groups: patients treated between 1 January 2003 and 31 August 2008 were allocated to the historic cohort; all patients operated on after the change of the chairmanship (1 September 2008) were included in the current cohort. For the formation of 2 identical time intervals of 68 months each, the current cohort contained all appropriate cases treated until 30 April 2014. Data were collected after the approval of the institutional ethics committee (EthikKommission, Medizinische Fakultät der Universität DuisburgEssen, registration number, 15-6331-BO) and registration in the German clinical trial register (DRKS, unique identifier, DRKS00008749). Clinical Management of UIAs The diagnostic workup of UIAs and the decision on the advisability of UIA treatment remained unchanged across the time interval investigated. Diagnostic digital subtraction angiography (DSA) was obligatory in all cases before treatment allocation. Decision making regarding the necessity for treatment of the UIA, as well as the subsequent allocation to coiling or clipping, was always discussed interdisciplinarily between the senior neurosurgeon and the senior neuroradiologist, taking into account the available literature on the topic,7,8 the personal experience of the specialists involved, and the above-mentioned consensus on balanced treatment allocation. All clipping procedures were performed in a microsurgical manner and included the obligatory use of at least 1 intraoperative blood flow monitoring tool (microvascular Doppler ultrasonography or indocyanine green videoangiography [ICG VA]). In addition, electrophysiologic monitoring (EM) was also applied in most surgeries, depending on the individual decision of the neurosurgeon. The patients were routinely admitted postoperatively to our neurosurgical intensive care unit for 1 day, unless a longer stay was required for clinical reasons. All patients underwent early
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postoperative computed tomography (CT) within 24 hours after the operation. In cases of delayed postoperative neurologic deficits, additional follow-up CT scans were also performed. Moreover, postoperative DSA was routinely performed during the first week after clipping for the documentation of aneurysm occlusion. The patients underwent routine outpatient clinical follow-up at 6 months after surgery. Data Management The following outcome measurements were defined as study end points: A) development of cerebral infarction on postoperative CT scan; B) incomplete aneurysm obliteration necessitating direct retreatment defined as grade IV or V aneurysm remnants according to the Sindou classification9; C) parent vessel stenosis on postoperative DSA defined as any narrowing of the parent vessel at the site of the clip as documented by the radiologists; D) unfavorable outcome at 6 months after surgery (defined as modified Rankin Score >2), when surgical mortality was also addressed. Demographic and clinical data of the patients on admission and during the hospital stay were retrospectively collected from the hospital chart records. The characteristics of the clipped aneurysms (location, size of neck and dome) were collected from the preoperative DSA reports. All postoperative CT scans were reviewed to identify new cerebral infarctions. Hypodensities on CT imaging resulting from the surgical approach were excluded from the analysis. Postoperative DSAs were reviewed with regard to aneurysm obliteration and parent vessel stenosis (or occlusion) by clip material. The expertise of surgeons was operationalized as the number of years since the neurosurgical board examination and the individual complication rates. None of the surgeons underwent subspecialty training in cerebrovascular surgery outside our institution. Statistical Analysis The baseline characteristics of the cohorts were univariately correlated. Continuous variables were analyzed using the Student t test for normally distributed data and the Mann-Whitney U test for nonnormally distributed data. Categorical variables were analyzed using the c2 test or Fisher exact test, as appropriate. Multivariate binary logistic analysis (using stepwise backward regression) was performed to evaluate the impact of the clipping caseload on postoperative functional outcome, with the inclusion of potential confounders (patients’ age and use of intraoperative diagnostic tools). Differences with a P value 2 before the surgery). Accordingly, 94 unruptured intracranial aneurysms (UIAs) fulfilled the inclusion criteria in the historic cohort. In the current cohort, 432 aneurysms were surgically treated. Of these, 176 were clipped during subarachnoid hemorrhage and therefore were excluded. In addition, 4 cases were disregarded because of the poor initial modified Rankin Score. As a result, 252 clipped unruptured intracranial aneurysms were included in the final analysis from the current cohort.
UIAs were included in the final analysis. Of these, 94 UIAs were clipped before 1 September 2008 and 252 thereafter (i.e., >2.6fold increase of the number of clipped UIAs). The baseline demographic and clinical characteristics of the treated patients are shown in Table 1. Treatment Outcome Cerebral infarction was documented on the postoperative CT scan(s) in 25 cases (26.6%) in the historic cohort. In the current
Table 1. Demographic and Clinical Characteristics of the Treated Patients Characteristic Age, years
Historic Cohort, Current Cohort, P Mean (SD) or n (%) Mean (SD) or n (%) Value 49.6 (10.8)
53.9 (10.3)
0.0006
Sex, female
66 (70.2)
187 (74.2)
0.4121
Aneurysm size, mm
7.4 (5.6)
6.7 (3.9)
0.9409
Aneurysm location
0.2756
MCA
65 (69.1)
187 (74.2)
ICA
14 (14.9)
24 (9.5)
ACA
12 (12.8)
38 (15.1)
3 (3.2)
3 (1.2)
PC
SD, standard deviation; MCA, middle cerebral artery; ICA, internal carotid artery; ACA, anterior cerebral artery; PC, posterior circulation.
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cohort, this complication was seen less frequently; only 19 UIA surgeries (7.5%) were associated with postoperative cerebral infarction (P < 0.0001; odds ratio [OR], 0.23; 95% confidence interval, 0.12e0.43, see Figure 2). In both cohorts, the probability of the clipping-related cerebral infarction was independent from UIA location. Parent vessel stenosis was visualized in 5 postoperative DSAs in both groups indicating the reduction of this complication from 5.3% to 2% (OR, 0.36; P ¼ 0.1428). Incomplete UIA occlusion requiring retreatment was documented in postoperative DSAs in 4 cases (4.3%) in the historic and 5 cases (2%) in the current cohort (OR, 0.46; P ¼ 0.2614). More detailed data on the rates of aneurysm remnants after clipping and their clinical consequences have already been reported elsewhere.9 In the historic cohort, an unfavorable outcome at 6 months follow-up occurred after 8 operations (8.5%). In contrast, only 7 UIAs (2.8%) were associated with an unfavorable outcome in the current cohort (OR, 0.31; 95% confidence interval, 0.11e0.87; P ¼ 0.0332). Moreover, 3 patients (3.2%) died in the historic cohort as a result of surgical complications, whereas no surgical mortality was documented in the current cohort. One patient treated in the current cohort had an uncomplicated postoperative course. However, in the further postoperative clinical course, this patient experienced a subarachnoid hemorrhage from an untreated basilar tip aneurysm scheduled for treatment. This patient died as a result of the complications of subarachnoid hemorrhage. Further subanalysis within the current cohort showed that the surgical outcome progressively improved over time. In particular, 6 of 7 cases (>85%) with surgical morbidity occurred during the first half of the period for the current cohort (Supplementary Figure 1). Surgical Aspects The surgical staff were analyzed for the entire period of the study, including individual clipping and complication rates. The individual clipping volume significantly increased over the 2 time intervals; the mean annual caseload for each neurovascular surgeon (as primary surgeon) increased from 6.5 to 17.5 aneurysms (P ¼ 0.0026). The individual complication rates ranged between 0% and 28.6% in the historic cohort and between 0% and 7.7% in the current cohort. The individual complication rates appeared to be more balanced in the current cohort (standard deviation 2.95 versus 9.63 in the historic cohort). The surgical staff gradually changed over this 11-year period; about half of UIAs were clipped by the same 4 surgeons in both groups (50 and 111 UIAs in the historic and current cohorts, respectively). In addition to the new neurosurgical chairman, the remaining neurosurgeons not presented in the historic cohort (n ¼ 6) were our former residents who trained for neurovascular surgery at our institution after the increase of the clipping caseload. Regarding surgical experience, the surgeons in the current cohort were significantly younger (mean time after the neurosurgical board examination was 6.9 years [ 4.4] versus 14.2 years [ 8.7] for the surgeons in the historic cohort; P < 0.0001). Although ICG VA and EM were more frequently used in the current cohort (P < 0.0001), these intraoperative diagnostic tools did not correlate with the functional outcome. In addition, the
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OUTCOME AFTER ANEURYSM CLIPPING
Table 2. Multivariate Logistic Regression Analysis for the Predictors of Unfavorable Functional Outcome After Unruptured Intracranial Aneurysm Clipping Steps 1
Figure 2. The frequency and rate of cerebral infarction identified on postoperative computed tomography scans was significantly lower in the current cohort compared with the historic cohort.
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improvement in functional outcome in the patients treated after September 2008 was independent of the above-mentioned diagnostic tools in the multivariate analysis (Table 2). DISCUSSION This single-center retrospective observational study shows significantly better surgical outcome and fewer clipping-related complications as a result of the increase of surgical volume. Increasing Dominance of Endovascular Coiling A Trend without any Cons? First described by Walter Dandy in 1938,10 surgical clipping of intracranial aneurysms remained the only treatment option for this potentially fatal cerebral pathology over many decades.11 After the invention of endovascular aneurysm coiling in 1991 by Guido Guglielmi12 and publication of data from the International Subarachnoid Aneurysm Trial in 2005,7 endovascular intervention has become the first-line treatment for ruptured intracranial aneurysms and UIAs in many neurovascular centers.13 Technical progress in endovascular treatments, including the introduction of balloon- and stent-assisted coiling as well as flow diverters and Web devices, has substantially changed the ratio between endovascular treatments and open surgery in favor of the endovascular approach.3 In particular, the proportion of UIAs treated in the United States with coiling increased from 20% in 2001 to 63% in 2008.4 In a recent publication from the United Kingdom, Teo et al.14 reported a 6fold decrease in the number of surgically treated intracranial aneurysms in their center. This decreasing trend of microsurgical clipping may have a substantial effect on treatment outcome of surgically treated individuals. Zacharia et al.5 showed that the decrease of microsurgical volume has worsened clipping results. Furthermore, Le Reste et al.15 identified a significant correlation between surgical neurovascular experience and the risk for intraoperative complications during aneurysm surgery. According to recent data, surgical treatment of UIA is associated with a 1.06%e4.9% risk of permanent morbidity2,16,17 and 0%e 1.6% mortality2,18. Although these results are better compared with reports from the last decades,1 endovascular treatment shows superior results in terms of functional disability (at least, for the
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5
Parameter Surgery in current cohort*
Odds Ratio (95% Confidence Interval)
P Value
0.99 (0.99e1.00)
0.055
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.74 (0.58e12.85)
0.203
Aneurysm locationz
1.23 (0.66e2.32)
0.513
Use of intraoperative ICG VA
1.84 (0.52e6.47)
0.343
Use of intraoperative EM
0.58 (0.20e1.69)
0.316
Surgery in current cohort*
0.99 (0.99e1.00)
0.056
Agey
1.09 (1.03e1.16)
0.004
Sex, female
2.68 (0.57e12.53)
0.211
Use of intraoperative ICG VA
1.79 (0.51e6.27)
0.365
Use of intraoperative EM
0.59 (0.20e1.72)
0.335
Surgery in current cohort*
0.99 (0.99e1.00)
0.009
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.79 (0.60e12.97)
0.191
Use of intraoperative EM
0.64 (0.22e1.82)
0.402
Surgery in current cohort*
0.99 (0.99e1.00)
0.010
Agey
1.09 (1.03e1.15)
0.005
Sex, female
2.81 (0.61e13.03)
0.186
Surgery in current cohort*
0.99 (0.99e1.00)
0.012
Agey
1.09 (1.03e1.15)
0.005
ICG VA, indocyanine green videoangiography; EM, electrophysiologic monitoring. *Per day since 1 September 2008. yPer year in age increase. zThe location of the treated aneurysm was presented as a scale based on the rates of surgical cases: 1, MCA; 2, ACA; 3, ICA; 4, PC.
short-term outcome) and treatment-related complications in many meta-analyses.19,20 Taking into account the continuously decreasing percentage of clipped aneurysms in most neurovascular centers, there is a serious risk for further worsening of surgical results. We acknowledge the currently dominant role of endovascular coiling for treatment of patients with intracranial aneurysms. Nevertheless, microsurgical clipping remains an important component of aneurysm management. Certain intracranial aneurysms remain better candidates for open surgery than for coiling.20 Moreover, microsurgical clipping provides higher occlusion rates and therefore ensures a lower rebleeding risk than endovascular treatment.21 In addition, there is also a need for surgical retreatment for specific cases of incompletely coiled aneurysms (and vice versa).22 The recent developments toward bypass surgery may become a lifesaving alternative for some complex aneurysms.23 Therefore, the availability of a safe and competitive microsurgical treatment for intracranial aneurysms is of
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
paramount importance for the entire population of aneurysm carriers. Increase of Surgical Volume Improves the Outcome of Clipping In our series, the treatment in the current cohort (characterized by an increase in surgical volume) and younger age of patients were independently associated with a favorable outcome after aneurysm surgery. In particular, permanent postoperative morbidity was significantly reduced from 8.5% to 2.8%. Moreover, surgical mortality could be completely eliminated (from 3.2% to 0%). This improvement in functional outcome was as a result of the reduction in clipping-related complications, especially cerebral infarction. Apart from the significantly higher age of the patients in the current cohort, the remaining baseline parameters of both cohorts were similar, including the characteristics of the treated UIAs. The higher age of the patients in the current cohort meant a higher risk for unfavorable outcome and cerebral infarction. The strong association between these factors is well acknowledged24 and is also shown in our multivariate analysis (P ¼ 0.005, Table 2). Regarding the use of intraoperative diagnostic modalities, ICG VA and EM have been more frequently applied in recent years. A positive effect of these intraoperative technical advances on clipping results is widely acknowledged.25,26 However, in our univariate and multivariate analyses, ICG VA and EM were not associated with the functional outcome. The increase in the institutional caseload was associated with a significant increase in the individual caseload for each neurosurgeon. In addition, our analyses pointed to a more balanced distribution of the complication rates in the current cohort. This apparently reflects a certain level of neurovascular surgical expertise for all neurosurgeons operating at the time of higher clipping caseload. Moreover, the risk for unfavorable outcome decreased progressively (Supplementary Figure 1) within the current cohort, a sign of further gradual improvement of neurovascular surgical expertise. We believe that our data reflect the substantial role of increased surgical volume for improvement of surgical outcome and complication rates. These findings are in line with previous reports5,15 on the negative correlation between clipping results and neurovascular surgical expertise.
REFERENCES 1. Raaymakers TW, Rinkel GJ, Limburg M, Algra A. Mortality and morbidity of surgery for unruptured intracranial aneurysms: a meta-analysis. Stroke. 1998;29:1531-1538. 2. Kunz M, Bakhshai Y, Zausinger S, Fesl G, Janssen H, Brückmann H, et al. Interdisciplinary treatment of unruptured intracranial aneurysms: impact of intraprocedural rupture and ischemia in 563 aneurysms. J Neurol. 2013;260:1304-1313. 3. Nussbaum ES, Madison MT, Myers ME, Goddard J. Microsurgical treatment of unruptured intracranial aneurysms. A consecutive surgical experience consisting of 450 aneurysms treated in the endovascular era. Surg Neurol. 2007;67:457-464 [discussion: 464-456].
Sufficient neurovascular surgical expertise is paramount for providing competitive treatment results in aneurysm surgery. In the face of the worldwide decreasing ratio of clipped aneurysms, establishment of nationwide specialized neurovascular centers with higher caseloads should be considered. This can help to improve surgical outcome for individual patients, as well as ensure excellent training for future neurovascular surgeons. Study Limitations Because of the retrospective study design, the quality of the presented data depends on the accuracy of the documentation in the electronic medical reports. Moreover, the role of surgeondependent impact on surgical outcome cannot be fully ruled out, because both cohorts were not treated by the same neurosurgeons (with the same clipping rates). In addition, our analysis cannot exclude all potential confounders of unfavorable outcome (such as the complications arising from perioperative anesthesiologic and intensive care). Regarding the risk of cerebral infarction, magnetic resonance imaging would have been preferable over CT for infarct detection.27 However, magnetic resonance imaging was not available in most cases as a routine postoperative follow-up. Our analysis is based on a single-center case series, which limits the generalizability of the results. Nevertheless, our real-life experience presents a rare circumstance in the current era of endovascular dominance. Therefore, we believe that the presented data will be of value for future treatment strategies for intracranial aneurysms. CONCLUSIONS Clipping volume seems to be a key factor for improvement of clipping outcome and reduction of the risk for clipping-related complications. Substantial neurovascular surgical expertise is of paramount importance to ensure competitive treatment results of aneurysm clipping. ACKNOWLEDGMENTS We would like to give special thanks to Prof. Dr. Ilonka Kreitschmann-Andermahr (Department of Neurosurgery, University Hospital of Essen) for critically revising the manuscript before submission.
4. Brinjikji W, Rabinstein AA, Nasr DM, Lanzino G, Kallmes DF, Cloft HJ. Better outcomes with treatment by coiling relative to clipping of unruptured intracranial aneurysms in the United States, 2001-2008. AJNR Am J Neuroradiol. 2011;32: 1071-1075. 5. Zacharia BE, Ducruet AF, Hickman ZL, Grobelny BT, Badjatia N, Mayer SA, et al. Technological advances in the management of unruptured intracranial aneurysms fail to improve outcome in New York state. Stroke. 2011;42: 2844-2849. 6. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604-607.
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7. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809-817. 8. Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110. 9. Jabbarli R, Pierscianek D, Wrede K, Dammann P, Schlamann M, Forsting M, et al. Aneurysm remnant after clipping: the risks and consequences. J Neurosurg. 2016. in press.
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10. Dandy WE. Intracranial aneurysm of the internal carotid artery: cured by operation. Ann Surg. 1938; 107:654-659.
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unruptured intracranial aneurysms. J Clin Neurosci. 2015;22:69-72.
11. Kivisaari RP, Porras M, Ohman J, Siironen J, Ishii K, Hernesniemi J. Routine cerebral angiography after surgery for saccular aneurysms: is it worth it? Neurosurgery. 2004;55:1015-1024.
18. Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, et al. Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke. 2010;41: 1471-1476.
12. Guglielmi G, Vinuela F, Sepetka I, Macellari V. Electrothrombosis of saccular aneurysms via endovascular approach. Part 1: Electrochemical basis, technique, and experimental results. J Neurosurg. 1991;75:1-7.
19. Hwang JS, Hyun MK, Lee HJ, Choi JE, Kim JH, Lee NR, et al. Endovascular coiling versus neurosurgical clipping in patients with unruptured intracranial aneurysm: a systematic review. BMC Neurol. 2012;12:99.
13. Giussani C, Mejdoubi M, Tremoulet M, Roux FE. The role of surgery when endovascular treatment is considered the first choice therapy for ruptured intracranial aneurysms. J Neurosurg Sci. 2008;52: 61-69. 14. Teo M, Martin S, Ponweera A, Macey A, Suttner N, Brown J, et al. Results of surgical clipping in a neurointerventional dominant department. Br J Neurosurg. 2015:1-7. 15. Le Reste PJ, Henaux PL, Riffaud L, Haegelen C, Morandi X. Influence of cumulative surgical experience on the outcome of poor-grade patients with ruptured intracranial aneurysm. Acta Neurochir (Wien). 2015;157:1-7. 16. Brown RD Jr, Broderick JP. Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurology. 2014;13:393-404. 17. Chen SF, Kato Y, Sinha R, Kumar A, Watabe T, Imizu S, et al. Surgical treatment of patients with
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20. Lanzino G, Murad MH. d’Urso PI, Rabinstein AA. Coil embolization versus clipping for ruptured intracranial aneurysms: a meta-analysis of prospective controlled published studies. AJNR Am J Neuroradiol. 2013;34:1764-1768. 21. Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DPH, et al. Clipping versus coiling for ruptured intracranial aneurysms: a systematic review and meta-analysis. Stroke. 2013;44:29-37. 22. Waldron JS, Halbach VV, Lawton MT. Microsurgical management of incompletely coiled and recurrent aneurysms: trends, techniques, and observations on coil extrusion. Neurosurgery. 2009; 64(5 suppl 2):301-315 [discussion: 315-317]. 23. Maldaner N, Guhl S, Mielke D, Musahl C, Schmidt NO, Wostrack M, et al. Changes in volume of giant intracranial aneurysms treated by surgical strategies other than direct clipping. Acta Neurochir (Wien). 2015;157:1117-1123 [discussion: 1123].
24. Jabbarli R, Reinhard M, Roelz R, Shah M, Niesen WD, Kaier K, et al. Early identification of individuals at high risk for cerebral infarction after aneurysmal subarachnoid hemorrhage: the BEHAVIOR score. J Cereb Blood Flow Metab. 2015;35: 1587-1592. 25. Jo KI, Kim HR, Yeon JY, Hong SC, Kim JS. Treatment outcomes of surgical clipping for unruptured anterior circulation aneurysm-single institute experiences in the era of neurophysiologic monitoring and endovascular treatment. Neurosurg Rev. 2015;38:677-682. 26. Dengler J, Cabraja M, Faust K, Picht T, Kombos T, Vajkoczy P. Intraoperative neurophysiological monitoring of extracranial-intracranial bypass procedures. J Neurosurg. 2013;119:207-214. 27. Kivisaari RP, Salonen O, Servo A, Autti T, Hernesniemi J, Ohman J. MR imaging after aneurysmal subarachnoid hemorrhage and surgery: a long-term follow-up study. AJNR Am J Neuroradiol. 2001;22:1143-1148. Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 16 November 2015; accepted 10 December 2015 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2015.12.043 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE RAMAZAN JABBARLI ET AL.
OUTCOME AFTER ANEURYSM CLIPPING
Supplementary Figure 1. Cumulative percentage of surgical complications in the current cohort. The figure shows a progressive improvement of the clipping outcome over time. In particular, >85% (6 of 7) of all cases with unfavorable outcome occurred during the first half of the observational time of the current cohort (the dashed lines). Moreover, about half of the complications happened between September 2008 and January 2010.
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