National trends in cerebral bypass for unruptured intracranial aneurysms: a National (Nationwide) Inpatient Sample analysis of 1998–2015

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OBJECTIVE

The development and recent widespread dissemination of flow diverters may have reduced the utilization of surgical bypass procedures to treat complex or giant unruptured intracranial aneurysms (UIAs). The aim of this retrospective cohort study was to observe trends in cerebral revascularization procedures for UIAs in the United States before and after the introduction of flow diverters by using the National (Nationwide) Inpatient Sample (NIS).

METHODS

The authors extracted data from the NIS database for the years 1998–2015 using the ICD-9/10 diagnostic and procedure codes. Patients with a primary diagnosis of UIA with a concurrent bypass procedure were included in the study. Outcomes and hospital charges were analyzed.

RESULTS

A total of 216,212 patients had a primary diagnosis of UIA during the study period. The number of patients diagnosed with a UIA increased by 128% from 1998 (n = 7718) to 2015 (n = 17,600). Only 1328 of the UIA patients (0.6%) underwent cerebral bypass. The percentage of patients who underwent bypass in the flow diverter era (2010–2015) remained stable at 0.4%. Most patients who underwent bypass were white (51%), were female (62%), had a median household income in the 3rd or 4th quartiles (57%), and had private insurance (51%). The West (33%) and Midwest/North Central regions (30%) had the highest volume of bypasses, whereas the Northeast region had the lowest (15%). Compared to the period 1998–2011, bypass procedures for UIAs in 2012–2015 shifted entirely to urban teaching hospitals (100%) and to an elective basis (77%). The median hospital stay (9 vs 3 days, p < 0.0001), median hospital charges ($186,746 vs $66,361, p < 0.0001), and rate of any complication (51% vs 17%, p < 0.0001) were approximately threefold higher for the UIA patients with bypass than for those without bypass.

CONCLUSIONS

Despite a significant increase in the diagnosis of UIAs over the 17-year study period, the proportion of bypass procedures performed as part of their treatment has remained stable. Therefore, advances in endovascular aneurysm therapy do not appear to have affected the volume of bypass procedures performed in the UIA population. The authors’ findings suggest a potentially ongoing niche for bypass procedures in the contemporary treatment of UIAs.

ABBREVIATIONS FDA = Food and Drug Administration; ICD = International Classification of Diseases; NIS = National (Nationwide) Inpatient Sample; PED = Pipeline embolization device; UIA = unruptured intracranial aneurysm; US = United States.

Abstract

OBJECTIVE

The development and recent widespread dissemination of flow diverters may have reduced the utilization of surgical bypass procedures to treat complex or giant unruptured intracranial aneurysms (UIAs). The aim of this retrospective cohort study was to observe trends in cerebral revascularization procedures for UIAs in the United States before and after the introduction of flow diverters by using the National (Nationwide) Inpatient Sample (NIS).

METHODS

The authors extracted data from the NIS database for the years 1998–2015 using the ICD-9/10 diagnostic and procedure codes. Patients with a primary diagnosis of UIA with a concurrent bypass procedure were included in the study. Outcomes and hospital charges were analyzed.

RESULTS

A total of 216,212 patients had a primary diagnosis of UIA during the study period. The number of patients diagnosed with a UIA increased by 128% from 1998 (n = 7718) to 2015 (n = 17,600). Only 1328 of the UIA patients (0.6%) underwent cerebral bypass. The percentage of patients who underwent bypass in the flow diverter era (2010–2015) remained stable at 0.4%. Most patients who underwent bypass were white (51%), were female (62%), had a median household income in the 3rd or 4th quartiles (57%), and had private insurance (51%). The West (33%) and Midwest/North Central regions (30%) had the highest volume of bypasses, whereas the Northeast region had the lowest (15%). Compared to the period 1998–2011, bypass procedures for UIAs in 2012–2015 shifted entirely to urban teaching hospitals (100%) and to an elective basis (77%). The median hospital stay (9 vs 3 days, p < 0.0001), median hospital charges ($186,746 vs $66,361, p < 0.0001), and rate of any complication (51% vs 17%, p < 0.0001) were approximately threefold higher for the UIA patients with bypass than for those without bypass.

CONCLUSIONS

Despite a significant increase in the diagnosis of UIAs over the 17-year study period, the proportion of bypass procedures performed as part of their treatment has remained stable. Therefore, advances in endovascular aneurysm therapy do not appear to have affected the volume of bypass procedures performed in the UIA population. The authors’ findings suggest a potentially ongoing niche for bypass procedures in the contemporary treatment of UIAs.

Unruptured intracranial aneurysms (UIAs) have traditionally been reported to have a prevalence of 1%–2%, and they account for up to 85% of spontaneous subarachnoid hemorrhages.8 More recently, the increased use of neuroimaging modalities has led to an escalated frequency of UIA diagnoses, with prevalences of 7% in patients between 35 and 75 years of age20 and 8.8% overall.19

The International Study of Unruptured Intracranial Aneurysms (ISUIA)46 reported 5-year cumulative hemorrhage risks, stratified by aneurysm size and location, that ranged from 0% for small anterior circulation UIAs to 50% for giant posterior circulation UIAs. A recent morphometric analysis of aneurysms in the ISUIA revealed that, in addition to the previously reported risk factors of aneurysm size and location, the perpendicular height of the aneurysm and its size ratio (i.e., ratio of maximum aneurysm diameter to parent vessel diameter) were also important predictors of UIA rupture risk.25 Given the high rupture risk associated with giant (diameter > 25 mm) UIAs, treatment of these lesions should be considered.

Since the introduction of extracranial-intracranial bypass for the treatment of cerebral ischemia by Yasargil et al.47,48 in the 1970s, the indications for revascularization have expanded to the treatment of complex and giant aneurysms, which became popularized in the 1980s.39,41,42 The International Subarachnoid Aneurysm Trial (ISAT)26,27 and Barrow Ruptured Aneurysm Trial (BRAT)24,37,38 reported better interim and long-term outcomes with endovascular therapy than with surgical clipping for ruptured aneurysms. However, no randomized trials have compared endovascular versus surgical treatment for UIAs, and most of the literature pertaining to UIAs is in the form of retrospective series and meta-analyses.3,10,14,31,34,36 Technological advances in endovascular therapy have led to an increase in endovascular procedures as the treatment of choice for cerebral aneurysms, from 20% of all aneurysms in 2001 to 63% in 2008.7 The introduction of flow-diverting stents has afforded neuroendovascular surgeons the opportunity to treat otherwise challenging aneurysms (e.g., giant, recurrent, fusiform, dissecting) by endoluminal reconstruction of the affected parent vessel, which results in progressive aneurysm occlusion over time while preserving flow through the parent artery.4,13,21,30 Since substantial overlap may exist between UIAs treated with surgical bypass and those treated with endovascular flow diversion, we hypothesized that the advent and subsequent dissemination of flow diverters, specifically the Pipeline embolization device (PED; Medtronic Neurovascular) which was approved by the United States (US) Food and Drug Administration (FDA) in April 2011, may be associated with a decline in the utilization of bypass for UIAs. Therefore, the aim of this retrospective cohort study was to evaluate temporal trends in cerebral revascularization procedures for UIAs in the US by using the National (Nationwide) Inpatient Sample (NIS), with particular consideration of the modern flow diversion era.

Methods

Data Source

We extracted data from the Healthcare Cost and Utilization Project (HCUP) NIS, which was established as a federal-state-industry partnership sponsored by the Agency for Healthcare Research and Quality (AHRQ) and is the largest all-payer inpatient care database. Data are released annually, dating back to 1988. Prior to 2012, the NIS data represented a 20% stratified sample of nonfederal community hospitals in the US. Beginning in 2012, the NIS approximates a 20% sample of all discharges from community hospitals (excluding rehabilitation and long-term acute care hospitals) in the US. Weights are provided to obtain national estimates. Unweighted, the NIS comprises approximately 7 million hospital stays per year. Weighted, the NIS represents about 35 million hospital stays per year. The discharge abstract includes both the Clinical Classification Software (CCS) and International Classification of Diseases, 9th and 10th Revisions (ICD-9/10) diagnostic and procedure codes.12 The data contain information regarding admission and discharge status, demographic data, charges, length of stay, geographic locations, complications, and mortality. The NIS has been used to analyze national trends in healthcare use and charges, in quality and outcomes, and in policy.15,16,22,23,28,32,44 For this study, we used NIS data from 1998 to 2015.

Case Selection

Cases were hospitalizations in which patients had a primary diagnosis code of “cerebral aneurysm, nonruptured” (ICD-9 code 437.3 or ICD-10 code I671) with a concurrent procedure code of “bypass” (ICD-9 code 39.28 or ICD-10 codes 031G, 031H, 031J, 031K, 031L, 031M, 031N, 031S, 031T).

Patient Characteristics

The following patient characteristics were extracted: age, sex, race/ethnicity, comorbidity score, median household income by zip code, and primary payer. The comorbidity score was measured with the Elixhauser comorbidity index,12 whose score was computed using an adaptation to ICD-9 and ICD-10 codes developed by Quan et al.29 The median household income by zip code was categorized in quartiles, from 1 (lowest) to 4 (highest).

Hospital Characteristics

The following hospital characteristics were extracted: hospital bed size (small, medium, or large), hospital region (Northeast, Midwest/North Central, South, or West), hospital location and/or teaching status (rural, urban non-teaching, or urban teaching), and admission/service type (emergent or elective).

In-Hospital Outcomes

The outcomes were length of stay, hospital charges, and complications. Hospital charges were adjusted to 2015 US$ using the Medicare care component of the consumer price index (accessible through the Bureau of Labor Statistics). In our analysis, we included diagnosis codes for the following complications: renal, cardiac, neurological, neurosurgical, deep vein thrombosis and/or pulmonary embolism, infection, wound, hydrocephalus, mechanical ventilation, pneumonia, and laceration. The ICD-9 and ICD-10 codes were used to survey complications.

Statistical Analysis

Continuous variables were summarized as the mean with standard deviation or the median with interquartile range and full range, as appropriate. Categorical variables and outcomes were summarized as the frequency count and percentage. For statistical comparisons, we used generalized linear models adjusted for the clustered and stratified nature of the data. To determine whether there was a specific year during which the trend significantly changed, we used Joinpoint Regression. The significance level was set to a p value < 0.05, and all statistical tests were two-sided. Data analyses were performed using SAS (SAS Institute) and Joinpoint Regression Software (Joinpoint Regression Program, version 4.6.0.0, April 2018, Statistical Methodology and Applications Branch, Surveillance Research Program, National Cancer Institute).

Results

The study cohort comprised 216,212 patients with a primary diagnosis of UIA during the study period. Table 1 details the number of primary diagnosis codes for UIA and the number of primary or secondary procedure codes for bypass for each year of the study period (1998–2015). The number of patients with UIA as the primary diagnosis increased by 128% from 1998 (n = 7718) to 2015 (n = 17,600). However, the yearly proportion of UIA patients undergoing cerebral bypass remained stable during the study period (Fig. 1), ranging from 0.3% (1998) to 1.8% (1999). In the more recent flow diverter era (2010–2015), the annual percentage of UIA patients undergoing bypass remained stable at approximately 0.4% (Fig. 2).

TABLE 1.

Number of cases per year, 1998–2015

Bypass as Primary or Secondary Procedure
YearNo. w/ Primary Dx of UIANo.%SE of Percentage
19987,718230.300.14
19999,2481651.780.63
20009,091850.930.22
20018,388470.560.24
20028,099660.810.4
200311,690970.830.22
200410,861370.340.15
200510,537730.690.22
200614,3181060.740.22
200711,758660.560.21
200815,128660.440.12
200913,9951431.020.33
20101,11250.450.44
201117,059640.380.16
201216,785750.450.12
201316,620500.300.09
201416,205750.460.13
201517,600850.480.11

Dx = diagnosis; SE = standard error.

FIG. 1.
FIG. 1.

Rate of primary bypasses performed for primary UIAs per year, 1998–2015.

FIG. 2.
FIG. 2.

Results from Joinpoint Regression Software. Red boxes indicate observed percentage of UIA patients undergoing bypass; blue line indicates 1998–2015 slope = -0.01. Slope is significantly different from 0 at alpha = 0.05 level. Final selected model: 0 Joinpoints.

Patient Demographics and Cerebral Bypass

A total of 1328 UIA patients (0.6% of the study cohort) underwent cerebral bypass. Table 2 summarizes the demographics of the study cohort, compares the demographics of UIA patients with versus without bypass, and compares the demographics of UIA patients who underwent bypass in 1998–2011 versus 2012–2015. The UIA patients who underwent bypass were younger (median age 56 vs 57 years, p < 0.0001), and if the UIA patient was male, they were more likely to undergo bypass (38% vs 26%, p < 0.0001). The majority of patients who underwent bypass for UIA were white (51%), had an Elixhauser comorbidity index ≥ 3 (51%), had a median household income in the 3rd or 4th quartile (57%), and were privately insured (51%). Significant differences between UIA patients who underwent bypass and those who did not were observed for race/ethnicity (p < 0.0001), comorbidity index (p = 0.0035), median household income (p < 0.0001), and insurance (p < 0.0001). We also found significant differences in race/ethnicity (p < 0.0001), comorbidity index (p = 0.0071), median household income (p < 0.0001), and insurance (p < 0.0001) between patients who underwent bypass in 1998–2011 and those who did so in 2012–2015.

TABLE 2.

Demographics of patients diagnosed with UIA

Patients w/ Primary Dx of UIAPatients w/ Bypass Surgery for UIA
VariableAllNo CBCBp Value1998–20112012–2015p Value
No. of patients216,212214,8841,3281,043285
Age in yrs
 Mean (SD)57 (30)57 (30)52 (37)52 (36)50 (42)
 Median (Q1–Q3)57 (48–66)57 (48–66)56 (42–63)<0.000156 (44–64)55 (38–63)0.5146
 Range, min–max0–1000–1000–8510–840–85
Sex, no. (%)
 Male56,204 (26%)55,699 (26%)505 (38%)410 (39%)95 (33%)
 Female159,337 (74%)158,514 (74%)823 (62%)<0.0001633 (61%)190 (67%)0.0646
 Data missing671 (0%)671 (0%)0 (0%)0 (0%)0 (0%)
Race/ethnicity, no. (%)
 White124,790 (58%)124,118 (58%)672 (51%)502 (48%)170 (60%)
 Black20,575 (10%)20,502 (10%)73 (5%)<0.000148 (5%)25 (9%)<0.0001
 Other27,171 (13%)26,986 (13%)184 (14%)124 (12%)60 (21%)
 Data missing43,677 (20%)43,278 (20%)399 (30%)369 (35%)30 (11%)
Elixhauser index, no. (%)
 0679 (0%)679 (0%)0 (0%)0 (0%)0 (0%)
 149,483 (23%)49,201 (23%)282 (21%)0.0035232 (22%)50 (18%)0.0071
 264,262 (30%)63,899 (30%)363 (27%)298 (29%)65 (23%)
 3 or more101,788 (47%)101,105 (47%)683 (51%)513 (49%)170 (60%)
Median household income for patient’s zip code, no. (%)
 Quartile 145,407 (21%)45,195 (21%)213 (16%)138 (13%)75 (26%)
 Quartile 254,204 (25%)53,912 (25%)292 (22%)207 (20%)85 (30%)
 Quartile 355,109 (25%)54,796 (26%)313 (24%)<0.0001258 (25%)55 (19%)<0.0001
 Quartile 456,360 (26%)55,922 (26%)438 (33%)393 (38%)45 (16%)
 Data missing5,133 (26%)5,059 (2%)72 (5%)47 (5%)25 (9%)
Primary payer, no. (%)
 Medicare71,478 (33%)71,110 (33%)368 (28%)298 (29%)70 (25%)
 Medicaid24,168 (11%)23,984 (11%)184 (14%)114 (11%)70 (25%)
 Private103,102 (48%)102,428 (48%)673 (51%)548 (53%)125 (44%)
 Self-pay8,009 (4%)7,976 (4%)33 (3%)<0.000128 (3%)5 (2%)<0.0001
 No charge1,180 (1%)1,180 (1%)0 (0%)0 (0%)0 (0%)
 Other7,829 (1%)7,759 (4%)70 (5%)55 (5%)15 (5%)
 Data missing447 (0%)447 (0%)0 (0%)0 (0%)0 (0%)

CB = cerebral bypass; SD = standard deviation.

Boldface type indicates statistical significance.

Hospital Characteristics and Cerebral Bypass

Table 3 summarizes the hospital characteristics of the study cohort, compares the hospital characteristics of UIA patients with versus without bypass, and compares the hospital characteristics of UIA patients who underwent bypass in 1998–2011 versus 2012–2015. When considering geographic distribution, the majority of bypass procedures were performed in the West (33%) and Midwest/North Central region hospitals (30%), with Northeast region hospitals performing the least (15%). In this 17-year patient sample, most bypass procedures for UIAs were performed at large (83%) and urban teaching (96%) hospitals and on an elective basis (67%). Compared to the time period of 1998–2011, bypass procedures for UIAs in the years 2012–2015 shifted entirely to urban teaching hospitals (100%) and were more frequently performed on an elective basis (77%).

TABLE 3.

Hospital characteristics for study cohort

Patients w/ Primary Dx of UIAPatients w/ CB for UIA
VariableAllNo CBCBp Value1998–20112012–2015p Value
No. of patients216,212214,8841,3281,043285
Hospital bed size, no. (%)
 Small12,255 (6%)12,153 (6%)102 (8%)92 (9%)10 (4%)
 Medium33,868 (16%)33,743 (16%)125 (9%)<0.0001100 (10%)25 (9%)0.0089
 Large169,314 (78%)168,213 (78%)1,101 (83%)851 (82%)250 (88%)
 Data missing775 (0%)775 (0%)0 (0%)0 (0%)0 (0%)
Hospital region, no. (%)
 Northeast41,605 (19%)41,400 (19%)205 (15%)150 (14%)55 (19%)
 Midwest/North Central53,521 (25%)53,125 (25%)396 (30%)<0.0001291 (28%)105 (37%)0.0003
 South77,206 (36%)76,923 (36%)283 (21%)228 (22%)55 (19%)
 West43,880 (20%)43,436 (20%)444 (33%)374 (36%)70 (25%)
Hospital location/teaching status, no. (%)
 Rural3,723 (2%)3,708 (2%)15 (1%)15 (1%)0 (0%)
 Urban non-teaching28,466 (13%)28,424 (13%)42 (3%)<0.000142 (4%)0 (0%)0.0003
 Urban teaching183,247 (85%)181,976 (85%)1,271 (96%)986 (95%)285 (100%)
 Data missing776 (0%)776 (0%)0 (0%)0 (0%)0 (0%)
Admission/service type, no. (%)
 Emergency27,699 (13%)27,590 (13%)109 (8%)109 (10%)0 (0%)
 Elective140,724 (65%)139,838 (65%)886 (67%)<0.0001666 (64%)220 (77%)<0.0001
 Missing47,789 (22%)47,456 (22%)333 (25%)268 (26%)65 (23%)

Boldface type indicates statistical significance.

Significant differences were observed in hospital bed size (p < 0.0001), hospital region (p < 0.0001), hospital location and teaching status (p < 0.0001), and admission/service type (p < 0.0001) between UIA patients who underwent bypass and those who did not. We also found significant differences in hospital bed size (p = 0.0089), hospital region (p = 0.0003), hospital location and teaching status (p = 0.0003), and admission/service type (p < 0.0001) between patients who underwent bypass for UIA in 1998–2011 and those who did so in 2012–2015.

Length of Stay, Hospital Costs, and Complications Following Bypass for UIA

Table 4 summarizes the length of stay, hospital costs, and postoperative complications of the study cohort, compares these factors between UIA patients with and those without bypass, and compares these factors between UIA patients who underwent bypass in 1998–2011 and those who did so in 2012–2015. The median hospital stay (9 vs 3 days, p < 0.0001) and median hospital charges ($186,746 vs $66,361, p < 0.0001) were three times greater for the UIA patients who underwent bypass than for those who did not. The rate of any complication was also three times higher in the UIA patients who underwent bypass (51% vs 17%, p < 0.0001).

TABLE 4.

Length of stay, hospital costs, and complications following bypass in patients with UIAs

Patients w/ Primary Dx of UIAPatients w/ Bypass Surgery for UIA
VariableAllNo BypassBypassp Value1998–20112012–2015p Value
No. of patients216,212214,8841,3281,043285
Length of stay
 Mean (SD)4 (14)4 (13)14 (35)15 (37)12 (25)
 Median (Q1–Q3)3 (1–5)3 (1–5)9 (6–18)<0.00019 (6–18)8 (6–14)0.1660
Hospital charges (2015 US$)
 Mean (SD)89,032 (202,390)87,991 (197,540)255,751 (467,761)249,273 (471,705)279,067 (453,071)
 Median (Q1–Q3)66,752 (39,214–109,724)66,361 (39,031–108,886)186,746 (120,549–316,274)<0.0001174,311 (113,531–294,275)232,460 (151,244–339,671)<0.0001
Complications, no. (%)
 Renal643 (0%)628 (0%)15 (1%)<0.000115 (1%)0 (0%)0.0447
 Cardiac1,905 (1%)1,842 (1%)63 (5%)<0.000153 (5%)10 (4%)0.2779
 Neurological7,664 (4%)7,595 (4%)70 (5%)0.000925 (2%)45 (16%)<0.0001
 Neurosurgical8,613 (4%)8,290 (4%)322 (24%)<0.0001272 (26%)50 (18%)0.0028
 DVT/PE2,354 (1%)2,235 (1%)119 (9%)<0.000199 (9%)20 (7%)0.1904
 Pulmonary9,359 (4%)9,095 (4%)264 (20%)<0.0001209 (20%)55 (19%)0.7774
 Infection7,941 (4%)7,809 (4%)132 (10%)<0.000187 (8%)45 (16%)0.0002
 Wound134 (0%)118 (0%)16 (1%)<0.000116 (2%)0 (0%)0.0347
 Hydrocephalus3,947 (2%)3,873 (2%)73 (5%)<0.000163 (6%)10 (4%)0.0965
 Mechanical vent7,144 (3%)6,946 (3%)199 (15%)<0.0001169 (16%)30 (11%)0.0175
 Pneumonia2,833 (1%)2,753 (1%)80 (6%)<0.000160 (6%)20 (7%)0.4292
 Laceration1,177 (1%)1,148 (1%)29 (2%)<0.000129 (3%)0 (0%)0.0045
 One of the above36,546 (17%)35,873 (17%)673 (51%)<0.0001523 (50%)150 (53%)0.4547

DVT = deep vein thrombosis; PE = pulmonary embolism.

Boldface type indicates statistical significance.

Compared to the years 1998–2011, the median length of stay following bypass for UIA remained unchanged in 2012–2015 (9 vs 8 days, respectively, p = 0.1660). However, the median cost of hospitalization for bypass in UIA patients increased from $174,311 in 1998–2011 to $232,460 in 2012–2015 (p < 0.0001). Although the rate of any postoperative complication after bypass for UIA was not significantly different in 1998–2011 compared with 2012–2015 (50% vs 53%, respectively, p = 0.4547), the rates of renal (1% vs 0%, p = 0.0447), neurosurgical (26% vs 18%, p = 0.0028), wound (2% vs 0%, p = 0.0347), mechanical ventilation (16% vs 11%, p = 0.0175), and laceration (3% vs 0%, p = 0.0045) complications decreased from 1998–2011 to 2012–2015, whereas the rates of neurological (2% vs 16%, p < 0.0001) and infectious (8% vs 16%, p = 0.0002) complications increased from 1998–2011 to 2012–2015.

Discussion

In this retrospective cohort study, whose data were derived from an analysis of the NIS for the period from 1998 to 2015, we found that cerebral bypass continues to be performed in a very small proportion of UIA patients in the US. Despite the introduction of endovascular flow diversion for the treatment of UIA,5 the annual rates of bypass procedures performed for UIAs remained stable at a low rate (mean 0.4%), even in the context of an increased frequency of UIA diagnosis by 128% during the study period.

Our findings reject the supposition that the application and dissemination of flow diverters for UIAs have reduced the utilization of bypass as a treatment method. As shown by our results, the percentage of patients undergoing cerebral bypass for UIAs has remained largely unchanged between 1998 and 2015, with no change in trends since FDA approval of the PED in 2011. Bypass is still overwhelmingly performed by large academic hospitals, which may be due to the procedure’s technical complexity and the relatively few neurosurgeons who have retained expertise in the procedure.17 Our study showed that bypass procedures for the treatment of UIAs have shifted entirely to urban teaching hospitals in the time period 2012–2015. This may reflect a consolidation of referral patterns toward high-volume academic centers of excellence.1,2,17,33,39

Our analysis has shown that the bypass is predominantly performed in individuals with an Elixhauser comorbidity index of 2 or greater (77%) and is virtually never performed in individuals with a score of 0. This suggests that certain comorbidities may play a role in the progression of aneurysms to the complex lesions requiring bypass. Unsurprisingly, bypass correlated with significantly longer hospital stays and admission costs. This could be related to a more intensive use of resources or the inherent complexity of UIAs not amenable to more conventional treatments such as endovascular therapy or surgical clipping.

A noticeable finding was the much higher complication rates in patients undergoing bypass than in those who did not (51% vs 17%, p < 0.0001). This difference could be partly explained by the previously noted difference in the prevalence of comorbidities between the two groups, making patients in the bypass group more vulnerable to complications arising from preexisting medical problems. This difference could also be attributed to an increased operative morbidity associated with bypass procedures and the technical complexities arising from the lesions themselves.17 It should also be noted that the overall complication rate in patients undergoing bypass has gradually decreased over time. This could be explained by improvements in surgical techniques, the patient concentration in high-volume academic centers, and changes in the selection criteria for bypass in light of emerging endovascular options.40

Our results challenge the notion that the emergence of flow diversion has decreased the need for cerebral bypass in the contemporary management of UIAs not amenable to endovascular coiling or surgical clipping, which implies that many of those complex lesions that warrant bypass surgery are still not amenable to flow diversion or other novel endovascular devices. Despite its high costs and need for prolonged hospitalization, cerebral bypass remains necessary for certain aneurysms with challenging anatomy or giant aneurysms, both of which are poor candidates for flow diversion.35 Bypass appears to provide a high cure rate with good vessel patency in appropriately selected patients18 and continues to represent an acceptable alternative for aneurysms that are otherwise untreatable by other means. Therefore, training future generations of vascular neurosurgeons in developing and maintaining proficiency in this surgical technique is paramount in keeping this modality available for these complicated aneurysms.

We can hypothesize, based on FDA approval of the PED for proximal internal carotid artery aneurysms from the petrous to superior hypophyseal segments, that more recent bypasses may be used more frequently for distally located aneurysms (e.g., anterior cerebral artery, middle cerebral artery, posterior inferior cerebellar artery) for which flow diversion has not yet been proven or accepted as the preferred treatment.5,50 Based on the available literature, there does not appear to be a substantial change in the rates of graft vessel patency over time (i.e., pre-45 vs post-PED43,49 eras), although recent publications from the US have suggested an increasing preference for the radial artery as the interposition graft of choice rather than the saphenous vein.6,9,11,33 However, we emphasize that these trends are inferred from the literature and cannot be informed by the NIS database used in this study.

Study Strengths and Limitations

The NIS provides a large sample size and an opportunity to look at the trends and practice patterns across the US. Researchers who query this database can answer a question in a comprehensive manner. The NIS also provides inpatient outcomes and hospitalization charges.

Limitations associated with the NIS include those associated with a retrospective cohort study (e.g., selection, treatment, and referral biases), coding errors, underestimation of mortality, and an inability to provide detailed long-term clinical outcomes. The NIS does not provide longitudinal information such as inpatient and outpatient services, medications, and overall costs related to outcome. Thus, we were unable to ascertain from the NIS any changes in treatment paradigm, graft choice, graft patency, or long-term clinical outcomes over the study period. We were also unable to determine the specific type or severity of postoperative neurological or neurosurgical complications. Additionally, the clinical indication for bypass, type and location of aneurysms, neuroimaging data, and clinical decision-making involved in the selection of UIA patients for bypass cannot be extracted from this database. Another major limitation of our study is the lack of data from the NIS with respect to the use of flow diversion because endovascular aneurysm embolization procedure codes do not currently distinguish between coiling and flow diversion. Therefore, it is possible that the complexity of UIAs undergoing intervention has increased over time, concurrently with the increased frequency of UIA diagnoses, thereby potentially expanding the indications of bypass for the treatment of aneurysms that cannot be adequately occluded with flow diverters.

Conclusions

Cerebral revascularization appears to have maintained a role in the treatment of UIAs over the past two decades, despite concurrent advances in endovascular techniques and devices in this time period. The impact of the introduction and subsequent propagation of endovascular flow diversion techniques on the rates of bypass procedures performed for the treatment of UIAs appears to be limited. Further detailed studies are warranted to evaluate the risk-benefit profiles of various revascularization approaches for the treatment of UIAs not amenable to surgical clipping or endovascular therapy. While challenging in the contemporary era of aneurysm treatment, the development and maintenance of expertise in cerebral bypass techniques at high-volume centers of excellence remain necessary for the comprehensive management of particularly difficult cases.

Disclosures

Dr. Williams has served as a consultant for Monteris.

Author Contributions

Acquisition of data: Sharma. Analysis and interpretation of data: Sharma. Drafting the article: Sharma, Fortuny. Critically revising the article: Ding, Sharma, Ugiliweneza, Khattar, Andaluz, James, Williams. Reviewed submitted version of manuscript: Ding, Sharma, Ugiliweneza, Fortuny, Khattar, Andaluz, James, Williams. Statistical analysis: Ugiliweneza. Administrative/technical/material support: Ding, Boakye. Study supervision: Ding, Boakye.

References

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    Abla AALawton MT: Anterior cerebral artery bypass for complex aneurysms: an experience with intracranial-intracranial reconstruction and review of bypass options. J Neurosurg 120:136413772014

  • 2

    Abla AAMcDougall CMBreshears JDLawton MT: Intracranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients. J Neurosurg 124:127512862016

  • 3

    Alshekhlee AMehta SEdgell RCVora NFeen EMohammadi A: Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke 41:147114762010

  • 4

    Becske TBrinjikji WPotts MBKallmes DFShapiro MMoran CJ: Long-term clinical and angiographic outcomes following Pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the Pipeline for Uncoilable or Failed Aneurysms trial. Neurosurgery 80:40482017

  • 5

    Becske TKallmes DFSaatci IMcDougall CGSzikora ILanzino G: Pipeline for Uncoilable or Failed Aneurysms: results from a multicenter clinical trial. Radiology 267:8588682013

  • 6

    Benet ATabani HBang JSMeybodi ATLawton MT: Occipital artery to anterior inferior cerebellar artery bypass with radial artery interposition graft for vertebrobasilar insufficiency: 3-dimensional operative video. Oper Neurosurg (Hagerstown) 13:6412017

  • 7

    Brinjikji WRabinstein AANasr DMLanzino GKallmes DFCloft HJ: Better outcomes with treatment by coiling relative to clipping of unruptured intracranial aneurysms in the United States, 2001-2008. AJNR Am J Neuroradiol 32:107110752011

  • 8

    Brown RD JrBroderick JP: Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurol 13:3934042014

  • 9

    Burkhardt JKWinkler ETabani HGandhi SBenet ALawton MT: A2 anterior cerebral artery-to-A3 anterior cerebral artery interpositional bypass with radial artery graft for a ruptured mycotic fusiform aneurysm: 2-dimensional operative video. Oper Neurosurg (Hagerstown) 15:6012018

  • 10

    Cowan JA JrZiewacz JDimick JBUpchurch GR JrThompson BG: Use of endovascular coil embolization and surgical clip occlusion for cerebral artery aneurysms. J Neurosurg 107:5305352007

  • 11

    Czabanka MAli MSchmiedek PVajkoczy PLawton MT: Vertebral artery-posterior inferior cerebellar artery bypass using a radial artery graft for hemorrhagic dissecting vertebral artery aneurysms: surgical technique and report of 2 cases. J Neurosurg 114:107410792011

  • 12

    Elixhauser ASteiner CHarris DRCoffey RM: Comorbidity measures for use with administrative data. Med Care 36:8271998

  • 13

    Fiorella DLylyk PSzikora IKelly MEAlbuquerque FCMcDougall CG: Curative cerebrovascular reconstruction with the Pipeline embolization device: the emergence of definitive endovascular therapy for intracranial aneurysms. J Neurointerv Surg 10 (Suppl 1):i9–i182018

  • 14

    Hwang JSHyun MKLee HJChoi JEKim JHLee NR: Endovascular coiling versus neurosurgical clipping in patients with unruptured intracranial aneurysm: a systematic review. BMC Neurol 12:992012

  • 15

    Kalakoti PMissios SMaiti TKonar SBir SBollam P: Inpatient outcomes and postoperative complications after primary versus revision lumbar spinal fusion surgeries for degenerative lumbar disc disease: a National (Nationwide) Inpatient Sample Analysis, 2002-2011. World Neurosurg 85:1141242016

  • 16

    Kourtis APBansil PPosner SFJohnson CJamieson DJ: Trends in hospitalizations of HIV-infected children and adolescents in the United States: analysis of data from the 1994-2003 Nationwide Inpatient Sample. Pediatrics 120:e236e2432007

  • 17

    Lawton MTAbla AARutledge WCBenet AZador ZRayz VL: Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: a work in progress. Neurosurgery 79:83992016

  • 18

    Lee CHTsai STChiu TL: Superficial temporal artery-middle cerebral artery bypass for the treatment of complex middle cerebral artery aneurysms. Ci Ji Yi Xue Za Zhi 30:1101152018

  • 19

    Li JShen BMa CLiu LRen LFang Y: 3D contrast enhancement-MR angiography for imaging of unruptured cerebral aneurysms: a hospital-based prevalence study. PLoS One 9:e1141572014

  • 20

    Li MHChen SWLi YDChen YCCheng YSHu DJ: Prevalence of unruptured cerebral aneurysms in Chinese adults aged 35 to 75 years: a cross-sectional study. Ann Intern Med 159:5145212013

  • 21

    Lylyk PMiranda CCeratto RFerrario AScrivano ELuna HR: Curative endovascular reconstruction of cerebral aneurysms with the Pipeline embolization device: the Buenos Aires experience. Neurosurgery 64:6326432009

  • 22

    Makarov DVLoeb SLandman ABNielsen MEGross CPLeslie DL: Regional variation in total cost per radical prostatectomy in the healthcare cost and utilization project Nationwide Inpatient Sample database. J Urol 183:150415092010

  • 23

    McCutcheon BAChang DCMarcus LGonda DDNoorbakhsh AChen CC: Treatment biases in traumatic neurosurgical care: a retrospective study of the Nationwide Inpatient Sample from 1998 to 2009. J Neurosurg 123:4064142015

  • 24

    McDougall CGSpetzler RFZabramski JMPartovi SHills NKNakaji P: The Barrow Ruptured Aneurysm Trial. J Neurosurg 116:1351442012

  • 25

    Mocco JBrown RD JrTorner JCCapuano AWFargen KMRaghavan ML: Aneurysm morphology and prediction of rupture: an International Study of Unruptured Intracranial Aneurysms analysis. Neurosurgery 82:4914962018

  • 26

    Molyneux AKerr RStratton ISandercock PClarke MShrimpton J: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:126712742002

  • 27

    Molyneux AJKerr RSYu LMClarke MSneade MYarnold JA: 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 366:8098172005

  • 28

    Opila TGeorge AEl-Ghanem MSouayah N: Trends in outcomes and hospitalization charges of infant botulism in the United States: a comparative analysis between Kids’ Inpatient Database and National Inpatient Sample. Pediatr Neurol 67:53582017

  • 29

    Quan HSundararajan VHalfon PFong ABurnand BLuthi JC: Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med Care 43:113011392005

  • 30

    Raper DMDing DPeterson ECCrowley RWLiu KCChalouhi N: Cavernous carotid aneurysms: a new treatment paradigm in the era of flow diversion. Expert Rev Neurother 17:1551632017

  • 31

    Ruan CLong HSun HHe MYang KZhang H: Endovascular coiling vs. surgical clipping for unruptured intracranial aneurysm: a meta-analysis. Br J Neurosurg 29:4854922015

  • 32

    Schraufnagel DRajaee SMillham FH: How many sunsets? Timing of surgery in adhesive small bowel obstruction: a study of the Nationwide Inpatient Sample. J Trauma Acute Care Surg 74:1811892013

  • 33

    Sekhar LNDuff JMKalavakonda COlding M: Cerebral revascularization using radial artery grafts for the treatment of complex intracranial aneurysms: techniques and outcomes for 17 patients. Neurosurgery 49:6466592001

  • 34

    Sharma MBrown BMadhugiri VCuellar-Saenz HSonig AAmbekar S: Unruptured intracranial aneurysms: comparison of perioperative complications, discharge disposition, outcome, and effect of calcification, between clipping and coiling: a single institution experience. Neurol India 61:2702762013

  • 35

    Siddiqui AHAbla AAKan PDumont TMJahshan SBritz GW: Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg 116:125812662012

  • 36

    Smith TRCote DJDasenbrock HHHamade YJZammar SGEl Tecle NE: Comparison of the efficacy and safety of endovascular coiling versus microsurgical clipping for unruptured middle cerebral artery aneurysms: a systematic review and meta-analysis. World Neurosurg 84:9429532015

  • 37

    Spetzler RFMcDougall CGAlbuquerque FCZabramski JMHills NKPartovi S: The Barrow Ruptured Aneurysm Trial: 3-year results. J Neurosurg 119:1461572013

  • 38

    Spetzler RFMcDougall CGZabramski JMAlbuquerque FCHills NKRussin JJ: The Barrow Ruptured Aneurysm Trial: 6-year results. J Neurosurg 123:6096172015

  • 39

    Spetzler RFSchuster HRoski RA: Elective extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. J Neurosurg 53:22271980

  • 40

    Starke RMTurk ADing DCrowley RWLiu KCChalouhi N: Technology developments in endovascular treatment of intracranial aneurysms. J Neurointerv Surg 8:1351442016

  • 41

    Sundt TM JrPiepgras DGHouser OWCampbell JK: Interposition saphenous vein grafts for advanced occlusive disease and large aneurysms in the posterior circulation. J Neurosurg 56:2052151982

  • 42

    Sundt TM JrPiepgras DGMarsh WRFode NC: Saphenous vein bypass grafts for giant aneurysms and intracranial occlusive disease. J Neurosurg 65:4394501986

  • 43

    Tayebi Meybodi AHuang WBenet AKola OLawton MT: Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization. J Neurosurg 127:4634792017

  • 44

    Tripathi BArora SKumar VAbdelrahman MLahewala SDave M: Temporal trends of in-hospital complications associated with catheter ablation of atrial fibrillation in the United States: an update from Nationwide Inpatient Sample database (2011-2014). J Cardiovasc Electrophysiol 29:7157242018

  • 45

    Vishteh AGMarciano FFDavid CASchievink WIZabramski JMSpetzler RF: Long-term graft patency rates and clinical outcomes after revascularization for symptomatic traumatic internal carotid artery dissection. Neurosurgery 43:7617681998

  • 46

    Wiebers DOWhisnant JPHuston J IIIMeissner IBrown RD JrPiepgras DG: Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:1031102003

  • 47

    Yasargil MGKrayenbuhl HAJacobson JH II: Microneurosurgical arterial reconstruction. Surgery 67:2212331970

  • 48

    Yasargil MGYonekawa Y: Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery 1:22241977

  • 49

    Yoon SBurkhardt JKLawton MT: Long-term patency in cerebral revascularization surgery: an analysis of a consecutive series of 430 bypasses. J Neurosurg [epub ahead of print August 24 2018. DOI: 10.3171/2018.3.JNS172158]

  • 50

    Zammar SGBuell TJChen CJCrowley RWDing DGriessenauer CJ: Outcomes after off-label use of the Pipeline embolization device for intracranial aneurysms: a multicenter cohort study. World Neurosurg 115:e200e2052018

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

Correspondence Dale Ding: University of Louisville School of Medicine, Louisville, KY. daleding1234@gmail.com.

INCLUDE WHEN CITING DOI: 10.3171/2018.11.FOCUS18504.

Disclosures Dr. Williams has served as a consultant for Monteris.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Rate of primary bypasses performed for primary UIAs per year, 1998–2015.

  • View in gallery

    Results from Joinpoint Regression Software. Red boxes indicate observed percentage of UIA patients undergoing bypass; blue line indicates 1998–2015 slope = -0.01. Slope is significantly different from 0 at alpha = 0.05 level. Final selected model: 0 Joinpoints.

References

1

Abla AALawton MT: Anterior cerebral artery bypass for complex aneurysms: an experience with intracranial-intracranial reconstruction and review of bypass options. J Neurosurg 120:136413772014

2

Abla AAMcDougall CMBreshears JDLawton MT: Intracranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients. J Neurosurg 124:127512862016

3

Alshekhlee AMehta SEdgell RCVora NFeen EMohammadi A: Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke 41:147114762010

4

Becske TBrinjikji WPotts MBKallmes DFShapiro MMoran CJ: Long-term clinical and angiographic outcomes following Pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the Pipeline for Uncoilable or Failed Aneurysms trial. Neurosurgery 80:40482017

5

Becske TKallmes DFSaatci IMcDougall CGSzikora ILanzino G: Pipeline for Uncoilable or Failed Aneurysms: results from a multicenter clinical trial. Radiology 267:8588682013

6

Benet ATabani HBang JSMeybodi ATLawton MT: Occipital artery to anterior inferior cerebellar artery bypass with radial artery interposition graft for vertebrobasilar insufficiency: 3-dimensional operative video. Oper Neurosurg (Hagerstown) 13:6412017

7

Brinjikji WRabinstein AANasr DMLanzino GKallmes DFCloft HJ: Better outcomes with treatment by coiling relative to clipping of unruptured intracranial aneurysms in the United States, 2001-2008. AJNR Am J Neuroradiol 32:107110752011

8

Brown RD JrBroderick JP: Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurol 13:3934042014

9

Burkhardt JKWinkler ETabani HGandhi SBenet ALawton MT: A2 anterior cerebral artery-to-A3 anterior cerebral artery interpositional bypass with radial artery graft for a ruptured mycotic fusiform aneurysm: 2-dimensional operative video. Oper Neurosurg (Hagerstown) 15:6012018

10

Cowan JA JrZiewacz JDimick JBUpchurch GR JrThompson BG: Use of endovascular coil embolization and surgical clip occlusion for cerebral artery aneurysms. J Neurosurg 107:5305352007

11

Czabanka MAli MSchmiedek PVajkoczy PLawton MT: Vertebral artery-posterior inferior cerebellar artery bypass using a radial artery graft for hemorrhagic dissecting vertebral artery aneurysms: surgical technique and report of 2 cases. J Neurosurg 114:107410792011

12

Elixhauser ASteiner CHarris DRCoffey RM: Comorbidity measures for use with administrative data. Med Care 36:8271998

13

Fiorella DLylyk PSzikora IKelly MEAlbuquerque FCMcDougall CG: Curative cerebrovascular reconstruction with the Pipeline embolization device: the emergence of definitive endovascular therapy for intracranial aneurysms. J Neurointerv Surg 10 (Suppl 1):i9–i182018

14

Hwang JSHyun MKLee HJChoi JEKim JHLee NR: Endovascular coiling versus neurosurgical clipping in patients with unruptured intracranial aneurysm: a systematic review. BMC Neurol 12:992012

15

Kalakoti PMissios SMaiti TKonar SBir SBollam P: Inpatient outcomes and postoperative complications after primary versus revision lumbar spinal fusion surgeries for degenerative lumbar disc disease: a National (Nationwide) Inpatient Sample Analysis, 2002-2011. World Neurosurg 85:1141242016

16

Kourtis APBansil PPosner SFJohnson CJamieson DJ: Trends in hospitalizations of HIV-infected children and adolescents in the United States: analysis of data from the 1994-2003 Nationwide Inpatient Sample. Pediatrics 120:e236e2432007

17

Lawton MTAbla AARutledge WCBenet AZador ZRayz VL: Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: a work in progress. Neurosurgery 79:83992016

18

Lee CHTsai STChiu TL: Superficial temporal artery-middle cerebral artery bypass for the treatment of complex middle cerebral artery aneurysms. Ci Ji Yi Xue Za Zhi 30:1101152018

19

Li JShen BMa CLiu LRen LFang Y: 3D contrast enhancement-MR angiography for imaging of unruptured cerebral aneurysms: a hospital-based prevalence study. PLoS One 9:e1141572014

20

Li MHChen SWLi YDChen YCCheng YSHu DJ: Prevalence of unruptured cerebral aneurysms in Chinese adults aged 35 to 75 years: a cross-sectional study. Ann Intern Med 159:5145212013

21

Lylyk PMiranda CCeratto RFerrario AScrivano ELuna HR: Curative endovascular reconstruction of cerebral aneurysms with the Pipeline embolization device: the Buenos Aires experience. Neurosurgery 64:6326432009

22

Makarov DVLoeb SLandman ABNielsen MEGross CPLeslie DL: Regional variation in total cost per radical prostatectomy in the healthcare cost and utilization project Nationwide Inpatient Sample database. J Urol 183:150415092010

23

McCutcheon BAChang DCMarcus LGonda DDNoorbakhsh AChen CC: Treatment biases in traumatic neurosurgical care: a retrospective study of the Nationwide Inpatient Sample from 1998 to 2009. J Neurosurg 123:4064142015

24

McDougall CGSpetzler RFZabramski JMPartovi SHills NKNakaji P: The Barrow Ruptured Aneurysm Trial. J Neurosurg 116:1351442012

25

Mocco JBrown RD JrTorner JCCapuano AWFargen KMRaghavan ML: Aneurysm morphology and prediction of rupture: an International Study of Unruptured Intracranial Aneurysms analysis. Neurosurgery 82:4914962018

26

Molyneux AKerr RStratton ISandercock PClarke MShrimpton J: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:126712742002

27

Molyneux AJKerr RSYu LMClarke MSneade MYarnold JA: 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 366:8098172005

28

Opila TGeorge AEl-Ghanem MSouayah N: Trends in outcomes and hospitalization charges of infant botulism in the United States: a comparative analysis between Kids’ Inpatient Database and National Inpatient Sample. Pediatr Neurol 67:53582017

29

Quan HSundararajan VHalfon PFong ABurnand BLuthi JC: Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med Care 43:113011392005

30

Raper DMDing DPeterson ECCrowley RWLiu KCChalouhi N: Cavernous carotid aneurysms: a new treatment paradigm in the era of flow diversion. Expert Rev Neurother 17:1551632017

31

Ruan CLong HSun HHe MYang KZhang H: Endovascular coiling vs. surgical clipping for unruptured intracranial aneurysm: a meta-analysis. Br J Neurosurg 29:4854922015

32

Schraufnagel DRajaee SMillham FH: How many sunsets? Timing of surgery in adhesive small bowel obstruction: a study of the Nationwide Inpatient Sample. J Trauma Acute Care Surg 74:1811892013

33

Sekhar LNDuff JMKalavakonda COlding M: Cerebral revascularization using radial artery grafts for the treatment of complex intracranial aneurysms: techniques and outcomes for 17 patients. Neurosurgery 49:6466592001

34

Sharma MBrown BMadhugiri VCuellar-Saenz HSonig AAmbekar S: Unruptured intracranial aneurysms: comparison of perioperative complications, discharge disposition, outcome, and effect of calcification, between clipping and coiling: a single institution experience. Neurol India 61:2702762013

35

Siddiqui AHAbla AAKan PDumont TMJahshan SBritz GW: Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. J Neurosurg 116:125812662012

36

Smith TRCote DJDasenbrock HHHamade YJZammar SGEl Tecle NE: Comparison of the efficacy and safety of endovascular coiling versus microsurgical clipping for unruptured middle cerebral artery aneurysms: a systematic review and meta-analysis. World Neurosurg 84:9429532015

37

Spetzler RFMcDougall CGAlbuquerque FCZabramski JMHills NKPartovi S: The Barrow Ruptured Aneurysm Trial: 3-year results. J Neurosurg 119:1461572013

38

Spetzler RFMcDougall CGZabramski JMAlbuquerque FCHills NKRussin JJ: The Barrow Ruptured Aneurysm Trial: 6-year results. J Neurosurg 123:6096172015

39

Spetzler RFSchuster HRoski RA: Elective extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. J Neurosurg 53:22271980

40

Starke RMTurk ADing DCrowley RWLiu KCChalouhi N: Technology developments in endovascular treatment of intracranial aneurysms. J Neurointerv Surg 8:1351442016

41

Sundt TM JrPiepgras DGHouser OWCampbell JK: Interposition saphenous vein grafts for advanced occlusive disease and large aneurysms in the posterior circulation. J Neurosurg 56:2052151982

42

Sundt TM JrPiepgras DGMarsh WRFode NC: Saphenous vein bypass grafts for giant aneurysms and intracranial occlusive disease. J Neurosurg 65:4394501986

43

Tayebi Meybodi AHuang WBenet AKola OLawton MT: Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization. J Neurosurg 127:4634792017

44

Tripathi BArora SKumar VAbdelrahman MLahewala SDave M: Temporal trends of in-hospital complications associated with catheter ablation of atrial fibrillation in the United States: an update from Nationwide Inpatient Sample database (2011-2014). J Cardiovasc Electrophysiol 29:7157242018

45

Vishteh AGMarciano FFDavid CASchievink WIZabramski JMSpetzler RF: Long-term graft patency rates and clinical outcomes after revascularization for symptomatic traumatic internal carotid artery dissection. Neurosurgery 43:7617681998

46

Wiebers DOWhisnant JPHuston J IIIMeissner IBrown RD JrPiepgras DG: Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:1031102003

47

Yasargil MGKrayenbuhl HAJacobson JH II: Microneurosurgical arterial reconstruction. Surgery 67:2212331970

48

Yasargil MGYonekawa Y: Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery 1:22241977

49

Yoon SBurkhardt JKLawton MT: Long-term patency in cerebral revascularization surgery: an analysis of a consecutive series of 430 bypasses. J Neurosurg [epub ahead of print August 24 2018. DOI: 10.3171/2018.3.JNS172158]

50

Zammar SGBuell TJChen CJCrowley RWDing DGriessenauer CJ: Outcomes after off-label use of the Pipeline embolization device for intracranial aneurysms: a multicenter cohort study. World Neurosurg 115:e200e2052018

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