Impact of preoperative endovascular embolization on immediate meningioma resection outcomes

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OBJECTIVE

Preoperative embolization of meningiomas can facilitate their resection when they are difficult to remove. The optimal use and timing of such a procedure remains controversial given the risk of embolization-linked morbidity in select clinical settings. In this work, the authors used a large national database to study the impact of immediate preoperative embolization on the immediate outcomes of meningioma resection.

METHODS

Meningioma patients who had undergone elective resection were identified in the National (Nationwide) Inpatient Sample (NIS) for the period 2002–2014. Patients who had undergone preoperative embolization were propensity score matched to those who had not, adjusting for patient and hospital characteristics. Associations between preoperative embolization and morbidity, mortality, and nonroutine discharge were investigated.

RESULTS

Overall, 27,008 admissions met the inclusion criteria, and 633 patients (2.34%) had undergone preoperative embolization and 26,375 (97.66%) had not. The embolization group was younger (55.17 vs 57.69 years, p < 0.001) with a lower proportion of females (63.5% vs 69.1%, p = 0.003), higher Charlson Comorbidity Index (p = 0.002), and higher disease severity (p < 0.001). Propensity score matching retained 413 embolization and 413 nonembolization patients. In the matched cohort, preoperative embolization was associated with increased rates of cerebral edema (25.2% vs 17.7%, p = 0.009), posthemorrhagic anemia or transfusion (21.8% vs 13.8%, p = 0.003), and nonroutine discharge (42.8% vs 35.7%, p = 0.039). There was no difference in mortality (≤ 2.4% vs ≤ 2.4%, p = 0.82). Among the embolization patients, the mean interval from embolization to resection was 1.49 days. On multivariate analysis, a longer interval was significantly associated with nonroutine discharge (OR 1.33, p = 0.004) but not with complications or mortality.

CONCLUSIONS

Relative to meningioma patients who do not undergo preoperative embolization in the same admission, those who do have higher rates of cerebral edema and nonroutine discharge but not higher rates of stroke or death. Thus, meningiomas requiring preoperative embolization represent a distinct clinical entity that requires prolonged, more complex care. Further, among embolization patients, the timing of resection did not affect the risk of in-hospital complications, suggesting that the timing of surgery can be determined according to surgeon discretion.

ABBREVIATIONS APR-DRG = All-Patient Refined Diagnosis-Related Group; CCI = Charlson Comorbidity Index; HCUP = Healthcare Cost and Utilization Project; NIS = National (Nationwide) Inpatient Sample.

Abstract

OBJECTIVE

Preoperative embolization of meningiomas can facilitate their resection when they are difficult to remove. The optimal use and timing of such a procedure remains controversial given the risk of embolization-linked morbidity in select clinical settings. In this work, the authors used a large national database to study the impact of immediate preoperative embolization on the immediate outcomes of meningioma resection.

METHODS

Meningioma patients who had undergone elective resection were identified in the National (Nationwide) Inpatient Sample (NIS) for the period 2002–2014. Patients who had undergone preoperative embolization were propensity score matched to those who had not, adjusting for patient and hospital characteristics. Associations between preoperative embolization and morbidity, mortality, and nonroutine discharge were investigated.

RESULTS

Overall, 27,008 admissions met the inclusion criteria, and 633 patients (2.34%) had undergone preoperative embolization and 26,375 (97.66%) had not. The embolization group was younger (55.17 vs 57.69 years, p < 0.001) with a lower proportion of females (63.5% vs 69.1%, p = 0.003), higher Charlson Comorbidity Index (p = 0.002), and higher disease severity (p < 0.001). Propensity score matching retained 413 embolization and 413 nonembolization patients. In the matched cohort, preoperative embolization was associated with increased rates of cerebral edema (25.2% vs 17.7%, p = 0.009), posthemorrhagic anemia or transfusion (21.8% vs 13.8%, p = 0.003), and nonroutine discharge (42.8% vs 35.7%, p = 0.039). There was no difference in mortality (≤ 2.4% vs ≤ 2.4%, p = 0.82). Among the embolization patients, the mean interval from embolization to resection was 1.49 days. On multivariate analysis, a longer interval was significantly associated with nonroutine discharge (OR 1.33, p = 0.004) but not with complications or mortality.

CONCLUSIONS

Relative to meningioma patients who do not undergo preoperative embolization in the same admission, those who do have higher rates of cerebral edema and nonroutine discharge but not higher rates of stroke or death. Thus, meningiomas requiring preoperative embolization represent a distinct clinical entity that requires prolonged, more complex care. Further, among embolization patients, the timing of resection did not affect the risk of in-hospital complications, suggesting that the timing of surgery can be determined according to surgeon discretion.

Meningiomas are frequently hypervascular, and preoperative embolization of dural feeding arteries, especially for large tumors or lesions with surgically inaccessible vascular supplies, can facilitate resection and decrease operative blood loss and surgical complications.6,7,11,13,15,16,25,27,28 Nonetheless, the ideal use of preoperative meningioma embolization is controversial34 as it can also lead to edema, hemorrhage, stroke, and cranial nerve palsies.20,23,30 Nonneurological complications related to endovascular therapy can occur as well and include groin hematoma, femoral pseudoaneurysm, and arteriovenous fistula.22 Overall complication rates up to 8.3% have been reported in embolization for meningiomas.13

The optimal time interval between tumor embolization and resection is also unknown. Some studies have recommended a minimum of 24 hours if the goal is to simply maximize tumor devascularization and reduce operative blood loss and at least a week when trying to optimize tumor resectability and decrease edema.10,19,33 In contrast, other authors have suggested intervals of less than a week to reduce the opportunity for tumor revascularization.26,30 In the current work, using a large national database, we studied the impact of immediate preoperative embolization on the immediate outcomes of meningioma resection.

Methods

A retrospective observational study was performed using the National (Nationwide) Inpatient Sample (NIS) for the period between 2002 and 2014. The NIS is a database publicly available through the Healthcare Cost and Utilization Project (HCUP; https://www.hcup-us.ahrq.gov/nisoverview.jsp). It is the largest administrative all-payer database in the US, representing a 20% stratified sample of all US hospital discharges. Patient diagnoses and treatments are recorded using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes.

Inclusion and Exclusion Criteria

The database was queried for all meningioma patients (diagnosis codes: 192.1, 225.2, 237.6) who had undergone craniotomy (procedure code: 01.51). Patients undergoing tumor embolization (procedure code: 39.72) in the same admission were identified. The NIS provides a “PRDAYn” variable that identifies on which day of hospitalization each procedure occurs. Therefore, patients with a PRDAYn missing for embolization or resection or patients who had an embolization day following the resection day were excluded in order to identify the preoperative embolization patients.

The primary exposure of interest was preoperative embolization for meningioma. Patient variables included tumor histology (benign or malignant), age, sex, race (white, black, Hispanic, Asian or Pacific Islander, or other), Charlson Comorbidity Index (CCI), insurance status (Medicare or private, Medicaid, or no coverage), and zip code income quartile. Admissions were categorized as elective or nonelective. The All-Patient Refined Diagnosis-Related Group (APR-DRG) index was used to represent disease severity.3 Hospital variables included region (Northeast, Midwest, South, West), location and teaching status (rural, urban nonteaching, urban teaching), and size (small, medium, or large).

Studied outcomes included morbidity, mortality, and discharge disposition. Complications were derived from previously defined adverse events of meningioma resection1 and endovascular embolization, including hematoma complicating a procedure, cerebral infarction or hemorrhage, hydrocephalus, cerebral edema, cranial nerve palsy, meningitis or cerebral venous thrombosis, venous embolism, blood transfusion, and mechanical ventilation. Discharge disposition was categorized as routine, nonroutine (discharge to skilled nursing facility, acute rehabilitation facility, hospice, short-term hospital, or home health care), or in-hospital death.

Statistical Analysis

Statistical analysis was performed using Stata/MP version 14.1 (StataCorp LLC). Continuous variables are presented as the means ± standard deviations, and categorical variables are presented as counts with corresponding percentages. Independent samples t-tests and Wilcoxon rank-sum tests were used to detect group differences for normally and nonnormally distributed continuous variables, respectively. The chi-square test was used for categorical variables, and ordinal logistic regression was used for ordinal variables. Multivariate logistic regression analyses were completed to determine the impact of the interval between embolization and resection on these outcomes. Statistical significance was defined as α = 0.05, and all tests were 2-sided. In accordance with the HCUP data use agreement, cells containing ≤ 10 patients are not reported as a patient privacy precaution.

Given significant differences between the embolization and nonembolization patient cohorts, we used propensity score matching to adjust for differences in patient and hospital characteristics. Multivariate logistic regression was used to estimate the propensity of preoperative embolization (compared with no preoperative embolization). Covariates were selected a priori and included age, sex, race, insurance status, zip code income quartile, CCI, APR-DRG index, elective status of the admission, hospital size, hospital region, hospital location, and hospital teaching status. Matched propensity score analysis was completed with a 1:1 nearest neighbor algorithm without replacement using the TEFFECTS and PSMATCH2 software modules in Stata.14 These matching methods were selected to minimize bias.2 Patients who had undergone preoperative embolization were then matched to patients who had not, according to the propensity score. Following propensity score matching, rates of adverse outcomes were compared using chi-square tests.

Results

Overall, 27,008 meningioma admissions met the inclusion criteria, and 633 patients (2.34%) had undergone preoperative embolization and 26,375 (97.66%) had not. Baseline characteristics for both the overall and the propensity score–matched cohorts are shown in Tables 1 and 2. Several baseline differences were observed in the overall cohort, including a lower age (55.17 vs 57.69 years, p < 0.001) and a smaller proportion of females (63.5% vs 69.1%, p = 0.003) among the embolization patients. The embolization patients also had higher CCIs (OR 1.27, p = 0.002) and APR-DRG disease severity (OR 1.68, p < 0.001).

TABLE 1.

Patient and hospital characteristics in the entire study cohort

VariableNo EmbolizationEmbolizationp Value
No. of patients26,375633
Mean age in yrs57.6872 ± 14.721455.1738 ± 14.2948<0.001
Sex0.003
 Male8,102 (30.9)*231 (36.5)
 Female18,127 (69.1)*402 (63.5)
Race<0.001
 White15,970 (72.7)*333 (62.9)*
 Black2,458 (11.2)*60 (11.3)*
 Hispanic1,972 (9.0)*60 (11.3)*
 Asian or Pacific Islander782 (3.6)*42 (7.9)*
 Other790 (3.6)*34 (6.4)*
Insurance0.001
 Medicare or private22,237 (87.6)*500 (82.8)*
 Medicaid2,252 (8.9)*72 (11.9)*
 None888 (3.5)*32 (5.3)*
Zip code income quartile0.008
 14,408 (22.3)*122 (19.8)*
 24,889 (24.8)*128 (20.8)*
 35,090 (25.8)*168 (27.3)*
 45,340 (27.1)*198 (32.1)*
CCI0.008
 016,122 (61.1)351 (55.5)
 1–28,230 (31.2)219 (34.6)
 >22,023 (7.7)63 (10.0)
Severity of illness<0.001
 Minor loss of function8,307 (38.8)*179 (28.3)*
 Moderate loss of function8,355 (39.1)*242 (38.3)*
 Major loss of function3,443 (16.1)*151 (23.9)*
 Extreme loss of function1,278 (6.0)*60 (9.5)*
Histology0.88
 Benign25,028 (95.7)*599 (95.5)*
 Malignant1,137 (4.3)*28 (4.5)*
Admission type<0.001
 Nonelective5,479 (25.4)*285 (45.3)*
 Elective16,055 (74.6)*344 (54.7)*
Hospital region<0.001
 Northeast4,565 (18.7)*91 (16.3)*
 Midwest4,466 (18.3)*81 (14.5)*
 South9,162 (37.5)*171 (30.7)*
 West6,208 (25.4)*214 (38.4)*
Location & teaching status of hospital<0.001
 Urban teaching18,708 (77.1)*501 (89.9)*
 Urban nonteaching4,990 (20.6)*56 (10.1)*
 Rural557 (2.3)*≤10 (≤1.8)*
Bed size of hospital<0.001
 Large18,684 (77.0)*465 (83.5)*
 Medium4,100 (16.9)*51 (9.2)*
 Small1,471 (6.1)*41 (7.4)*

Values expressed as the mean ± standard deviation or as number (%), unless indicated otherwise.

Data missing for some cases; therefore, values do not reflect total study population.

TABLE 2.

Patient and hospital characteristics in the propensity score–matched sample

VariableNo EmbolizationEmbolizationp Value
No. of patients413413
Mean age in yrs54.5036 ± 15.112555.7554 ± 13.9340.22
Sex0.83
 Male149 (36.1)152 (36.8)
 Female264 (63.9)261 (63.2)
Race0.26
 White265 (64.2)260 (63.0)
 Black52 (12.6)53 (12.8)
 Hispanic56 (13.6)46 (11.1)
 Asian or Pacific Islander19 (4.6)34 (8.2)
 Other21 (5.1)20 (4.8)
Insurance0.90
 Medicare or private342 (82.8)344 (83.3)
 Medicaid47 (11.4)48 (11.6)
 None24 (5.8)21 (5.1)
Zip code income quartile0.85
 193 (22.5)83 (20.1)
 293 (22.5)95 (23.0)
 3104 (25.2)105 (25.4)
 4123 (29.8)130 (31.5)
CCI0.18
 0249 (60.3)238 (57.6)
 1–2135 (32.7)131 (31.7)
 >229 (7.0)44 (10.7)
Severity of illness0.71
 Minor loss of function109 (26.4)114 (27.6)
 Moderate loss of function177 (42.9)161 (39.0)
 Major loss of function91 (22.0)97 (23.5)
 Extreme loss of function36 (8.7)41 (9.9)
Histology0.51
 Benign396 (95.9)392 (94.9)
 Malignant17 (4.1)21 (5.1)
Admission type0.57
 Nonelective185 (44.8)177 (42.9)
 Elective228 (55.2)236 (57.1)
Hospital region0.006
 Northeast62 (15.0)79 (19.1)
 Midwest53 (12.8)31 (7.5)
 South160 (38.7)136 (32.9)
 West138 (33.4)167 (40.4)
Location & teaching status of hospital1.00
 Urban teaching365 (88.4)365 (88.4)
 Urban nonteaching48 (11.6)48 (11.6)
Bed size of hospital0.50
 Large340 (82.3)342 (82.8)
 Medium49 (11.9)41 (9.9)
 Small24 (5.8)30 (7.3)

Values expressed as the mean ± standard deviation or as number (%), unless indicated otherwise.

Unmatched Cohort

In the overall cohort, preoperative embolization was associated with significantly increased rates of hematoma complicating a procedure (3.6% vs 1.7%, p < 0.001), infarction or hemorrhage (7.6% vs 3.8%, p < 0.001), hydrocephalus (8.8% vs 4.1%, p < 0.001), cerebral edema (27.6% vs 11.8%, p < 0.001), meningitis or cerebral venous thrombosis (≤ 1.6% vs 0.6%, p = 0.049), and venous embolism (3.8% vs 1.8%, p < 0.001). Embolization patients also had higher rates of posthemorrhagic anemia or transfusion (21.8% vs 11.4%, p < 0.001), mechanical ventilation (9.0% vs 5.6%, p < 0.001), and nonroutine discharge (42.0% vs 33.3%, p < 0.001). There were no differences in the rates of cranial nerve palsy or death (Table 3).

TABLE 3.

Outcomes in the full patient sample

VariableNo EmbolizationEmbolizationp Value
No. of patients26,375633
Hematoma complicating a procedure447 (1.7)23 (3.6)<0.001
Cerebral infarction or hemorrhage1,009 (3.8)48 (7.6)<0.001
Hydrocephalus or performance of ventriculostomy1,082 (4.1)56 (8.8)<0.001
Cerebral edema3,121 (11.8)175 (27.6)<0.001
Cranial nerve palsy621 (2.4)21 (3.3)0.12
Posthemorrhagic anemia or transfusion3,001 (11.4)138 (21.8)<0.001
Meningitis or cerebral venous thrombosis166 (0.6)≤10 (≤1.6)0.049
Venous embolism or placement of IVC filter483 (1.8)24 (3.8)<0.001
Mechanical ventilation1,472 (5.6)57 (9.0)<0.001
Nonroutine discharge8,649 (33.3)*260 (42.0)*<0.001
Death during hospitalization366 (1.4)12 (1.9%)0.28

IVC = inferior vena cava.

Values expressed as number (%), unless indicated otherwise.

Data missing for some cases; therefore, values do not reflect total study population.

Interval Analysis

Univariate and multivariate logistic regression analyses restricted to embolization patients were completed to determine the impact of the interval (days) before resection on adverse outcomes. The mean interval was 1.49 days (range 0–20 days). Covariates included the patient and hospital factors previously described. On univariate analysis, a longer interval was significantly associated with an increased risk for infarction or hemorrhage (OR 1.14, p = 0.022) and nonroutine discharge (OR 1.31, p < 0.001). On adjusted analysis, only the association with nonroutine discharge remained significant (OR 1.33, p = 0.004).

Matched Cohort

After 1:1 propensity score matching, 413 embolization patients and 413 nonembolization patients were retained for comparison (Table 2). In this matched cohort, preoperative embolization was associated with increased rates of cerebral edema (25.2% vs 17.7%, p = 0.009), posthemorrhagic anemia or transfusion (21.8% vs 13.8%, p = 0.003), and nonroutine discharge (42.8% vs 35.7%, p = 0.039). There were no other significant associations (Table 4).

TABLE 4.

Outcomes in the propensity score–matched patient sample

VariableNo EmbolizationEmbolizationp Value
No. of patients413413
Hematoma complicating a procedure≤10 (≤2.4)16 (3.9)0.057
Cerebral infarction or hemorrhage24 (5.8)24 (5.8)1.00
Hydrocephalus or performance of ventriculostomy31 (7.5)37 (9.0)0.45
Cerebral edema73 (17.7)104 (25.2)0.009
Cranial nerve palsy13 (3.1)14 (3.4)0.84
Posthemorrhagic anemia or transfusion57 (13.8)90 (21.8)0.003
Meningitis or cerebral venous thrombosis≤10 (≤2.4)≤10 (≤2.4)0.31
Venous embolism or placement of IVC filter11 (2.7)15 (3.6)0.43
Mechanical ventilation41 (9.9)38 (9.2)0.72
Nonroutine discharge144 (35.7)*173 (42.8)*0.039
Death during hospitalization≤10 (≤2.4)≤10 (≤2.4)0.82

Values expressed as number (%), unless indicated otherwise.

Data missing for some cases; therefore, values do not reflect total study population.

Discussion

Using the NIS database, we completed a retrospective analysis of meningioma patients who had undergone resection with or without immediate preoperative embolization. Consistent with its goal of decreasing surgical complexity, preoperative embolization was more likely to be performed in patients with comorbid conditions and higher disease severity indices. When adjusting for hospital and patient factors (excluding tumor-specific information not in the NIS database, such as size, location, and arterial feeders), we found that patients who had undergone preoperative embolization had a 47% increased risk of cerebral edema, 92% increased risk of posthemorrhagic anemia or transfusion, and 7% increased risk for nonroutine discharge. In contrast, there were no differences for other complications, such as cranial nerve palsy, cerebral infarction or hemorrhage, and death.

Because preoperative embolization is more likely to be performed for large,29 vascular meningiomas with difficult-to-access feeding arteries,12 the increased risks for cerebral edema, blood loss, and adverse discharge are not necessarily surprising. Nonetheless, such tumor characteristics represent a confounding variable by indication, where a variable is associated with both the exposure and the outcome.31,32 While our use of propensity score matching minimized confounding of the measured variables available in the NIS database, it did not preclude confounding by unmeasured variables, such as individual surgeon preferences or tumor characteristics. Given this limitation, our data suggest that complex meningiomas thought to require preoperative embolization represent a clinical entity distinct from those meningiomas that appear resectable without preoperative treatment. Nonetheless, preoperative embolization and resection of such complex meningiomas can be safely performed in the majority of cases.

The higher rate of cerebral edema we observed in the embolization patients (25.2% vs 17.7% in the matched cohort) is consistent with rates in prior studies8,21,36,37 and likely results from a combination of the increased complexity of tumors selected for embolization and an effect of the embolization itself.34 Pretreatment edema exists in up to two-thirds of meningioma patients and varies with tumor location, tumor size, and extent of cortical damage.8,17,18,24 Larger meningiomas and those located in the frontal convexity or middle third falx have been shown to have significantly greater edema.24 Therefore, while embolization is known to be associated with cerebral edema,34 many of the patients in our study probably had baseline edema before embolization or resection. Unfortunately, the timing and cause of this edema cannot be directly ascertained from our data set. However, abnormal imaging results (such as cerebral edema) are only coded for billing and only appear in the NIS database with documented clinical significance,9 and those patients with baseline symptomatic edema not reflected in the CCI and APR-DRG index were almost certainly more likely to have had deeper or larger tumors that would be selected for preoperative embolization.

To our knowledge, this is the first report of a greater incidence of nonroutine discharge disposition among meningioma patients who underwent preoperative embolization than that among nonembolized patients. Because this finding persisted on adjusted analysis—unlike complications of embolization, such as stroke or hemorrhage—it probably represents a meaningful clinical impact of the increased complexity of tumors selected for embolization. Therefore, further care of cerebral edema in complex meningioma patients may be required for clinical manifestations such as nausea and vomiting, altered mental status, or decreased respiratory drive. Prolonged care following hospital discharge also probably increases costs for both patients and health care systems and should be considered when planning treatment.

Together, our data suggest that meningiomas selected for preoperative embolization represent a subset of high-risk tumors and that patients with these tumors have extra clinical needs. Surgical and postoperative care for these patients should be planned accordingly and the costs perhaps reimbursed differently than those for simple meningiomas. Future longitudinal studies are needed to determine if there are associations between preoperative embolization and long-term outcomes for meningioma patients.

The interval between embolization and craniotomy is also a controversial topic, with mixed recommendations and evidence for impact on efficacy or patient outcomes.4,5,10,12,19,30,35 However, embolization and resection are usually completed within 72 hours of each other and within the same hospital stay.11 In the current analysis, we identified delayed resection as a risk factor for cerebral infarction or hemorrhage, although this relation did not persist on multivariate analysis. However, there was a significant association between a longer interval and nonroutine discharge on both unadjusted and adjusted analyses. Given that delayed resection does not appear to be associated with an increased risk of in-hospital complications, the timing of surgery following embolization can be largely determined according to surgeon discretion.

There are several limitations to retrospective analyses utilizing a large administrative database as well as the risk of confounding by indication, as discussed above. Specifically, the NIS does not contain information about a patient’s baseline neurological status and long-term outcome or about procedural details, such the particle size and type of embolic agent. However, the object of this study was to assess the overall risk of adverse in-hospital outcomes for preoperative embolization patients relative to that for nonembolization patients, and therefore we did not require this information. An additional limitation related to our study design is our assessment of preoperative embolizations only performed in the same admission as the craniotomy. In some cases, patients undergo embolization and are discharged for variable lengths of time before being readmitted for resection. Although this was probably true for only a minority of cases, these types of patients may have been misclassified as nonembolization patients, likely biasing comparisons between groups toward the null. Large database analyses of meningioma patients would be improved by the availability of longitudinal data on postdischarge complications and tumor recurrence. Furthermore, data on tumor characteristics such as size, feeding arteries, and location would enable more precise matching of embolization and nonembolization patients for analysis.

Conclusions

Meningiomas requiring preoperative embolization likely represent a distinct clinical entity with greater treatment complexity and higher risks. These findings have important implications for the management of and reimbursement structure for these complex tumors.

Acknowledgments

The project described was partially supported by the National Institutes of Health Predoctoral Grant No. TL1TR001443 (M.G.B. and P.A.).

Disclosures

Dr. Pannell has been a consultant for Stryker.

Author Contributions

Conception and design: all authors. Acquisition of data: Brandel, Lopez Ramos. Analysis and interpretation of data: Brandel, Lopez Ramos. Drafting the article: Brandel, Rennert. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Khalessi. Statistical analysis: Brandel. Administrative/technical/material support: Wali, Santiago-Dieppa, Steinberg, Abraham. Study supervision: Khalessi, Rennert, Santiago-Dieppa, Pannell.

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    Lobato RDAlday RGómez PARivas JJDomínguez JCabrera A: Brain oedema in patients with intracranial meningioma. Correlation between clinical, radiological, and histological factors and the presence and intensity of oedema. Acta Neurochir (Wien) 138:4854941996

  • 25

    Macpherson P: The value of pre-operative embolisation of meningioma estimated subjectively and objectively. Neuroradiology 33:3343371991

  • 26

    Manelfe CLasjaunias PRuscalleda J: Preoperative embolization of intracranial meningiomas. AJNR Am J Neuroradiol 7:9639721986

  • 27

    Oka HKurata AKawano NSaegusa HKobayashi IOhmomo T: Preoperative superselective embolization of skull-base meningiomas: indications and limitations. J Neurooncol 40:67711998

  • 28

    Quiñones-Hinojosa AKaprealian TChaichana KLSanai NParsa ATBerger MS: Pre-operative factors affecting resectability of giant intracranial meningiomas. Can J Neurol Sci 36:6236302009

  • 29

    Raper DMStarke RMHenderson F JrDing DSimon SEvans AJ: Preoperative embolization of intracranial meningiomas: efficacy, technical considerations, and complications. AJNR Am J Neuroradiol 35:179818042014

  • 30

    Richter HPSchachenmayr W: Preoperative embolization of intracranial meningiomas. Neurosurgery 13:2612681983

  • 31

    Rush BRousseau JSekhon MSGriesdale DE: Craniotomy versus craniectomy for acute traumatic subdural hematoma in the United States: a national retrospective cohort analysis. World Neurosurg 88:25312016

  • 32

    Salas MHofman AStricker BH: Confounding by indication: an example of variation in the use of epidemiologic terminology. Am J Epidemiol 149:9819831999

  • 33

    Shi ZSFeng LJiang XBHuang QYang ZHuang ZS: Therapeutic embolization of meningiomas with Onyx for delayed surgical resection. Surg Neurol 70:4784812008

  • 34

    Singla ADeshaies EMMelnyk VToshkezi GSwarnkar AChoi H: Controversies in the role of preoperative embolization in meningioma management. Neurosurg Focus 35(6):E172013

  • 35

    Teasdale EPatterson JMcLellan DMacpherson P: Subselective preoperative embolization for meningiomas. A radiological and pathological assessment. J Neurosurg 60:5065111984

  • 36

    Wakhloo AKJuengling FDVan Velthoven VSchumacher MHennig JSchwechheimer K: Extended preoperative polyvinyl alcohol microembolization of intracranial meningiomas: assessment of two embolization techniques. AJNR Am J Neuroradiol 14:5715821993

  • 37

    Yasui KShoda YSuyama TNuma YAmanouchi YYKawamoto K: Preoperative embolization for meningioma using lipiodol. Interv Neuroradiol 4 (Suppl 1):63661998

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Article Information

Correspondence Alexander A. Khalessi: University of California, San Diego, La Jolla, CA. akhalessi@ucsd.edu.

INCLUDE WHEN CITING DOI: 10.3171/2018.1.FOCUS17751.

Disclosures Dr. Pannell has been a consultant for Stryker.

© AANS, except where prohibited by US copyright law.

Headings

References

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Ambekar SSharma MMadhugiri VSNanda A: Trends in intracranial meningioma surgery and outcome: a Nationwide Inpatient Sample database analysis from 2001 to 2010. J Neurooncol 114:2993072013

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Austin PC: Statistical criteria for selecting the optimal number of untreated subjects matched to each treated subject when using many-to-one matching on the propensity score. Am J Epidemiol 172:109210972010

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Djindjian RCophignon JThéron JMerland JJHoudart R: Embolization by superselective arteriography from the femoral route in neuroradiology. Review of 60 cases. 1. Technique, indications, complications. Neuroradiology 6:20261973

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Dubel GJAhn SHSoares GM: Contemporary endovascular embolotherapy for meningioma. Semin Intervent Radiol 30:2632772013

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Garrido MMKelley ASParis JRoza KMeier DEMorrison RS: Methods for constructing and assessing propensity scores. Health Serv Res 49:170117202014

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Gruber AKiller MMazal PBavinzski GRichling B: Preoperative embolization of intracranial meningiomas: a 17-years single center experience. Minim Invasive Neurosurg 43:18292000

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Haider ASRana HLee LKShail MSLeonard DKhan U: Large transcalvarial meningioma: surgical resection aided by preoperative embolization. Cureus 9:e12292017

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Hou JKshettry VRSelman WRBambakidis NC: Peritumoral brain edema in intracranial meningiomas: the emergence of vascular endothelial growth factor-directed therapy. Neurosurg Focus 35(6):E22013

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Kai YHamada JMorioka MYano STodaka TUshio Y: Appropriate interval between embolization and surgery in patients with meningioma. AJNR Am J Neuroradiol 23:1391422002

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Kallmes DFEvans AJKaptain GJMathis JMJensen MEJane JA: Hemorrhagic complications in embolization of a meningioma: case report and review of the literature. Neuroradiology 39:8778801997

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Kasuya HShimizu TSasahara ATakakura K: Phenytoin as a liquid material for embolisation of tumours. Neuroradiology 41:3203231999

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Kominami SWatanabe ASuzuki MMizunari TKobayashi STeramoto A: Preoperative embolization of meningiomas with N-butyl cyanoacrylate. Interv Neuroradiol 18:1331392012

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Lefkowitz MGiannotta SLHieshima GHigashida RHalbach VDowd C: Embolization of neurosurgical lesions involving the ophthalmic artery. Neurosurgery 43:129813031998

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Lobato RDAlday RGómez PARivas JJDomínguez JCabrera A: Brain oedema in patients with intracranial meningioma. Correlation between clinical, radiological, and histological factors and the presence and intensity of oedema. Acta Neurochir (Wien) 138:4854941996

25

Macpherson P: The value of pre-operative embolisation of meningioma estimated subjectively and objectively. Neuroradiology 33:3343371991

26

Manelfe CLasjaunias PRuscalleda J: Preoperative embolization of intracranial meningiomas. AJNR Am J Neuroradiol 7:9639721986

27

Oka HKurata AKawano NSaegusa HKobayashi IOhmomo T: Preoperative superselective embolization of skull-base meningiomas: indications and limitations. J Neurooncol 40:67711998

28

Quiñones-Hinojosa AKaprealian TChaichana KLSanai NParsa ATBerger MS: Pre-operative factors affecting resectability of giant intracranial meningiomas. Can J Neurol Sci 36:6236302009

29

Raper DMStarke RMHenderson F JrDing DSimon SEvans AJ: Preoperative embolization of intracranial meningiomas: efficacy, technical considerations, and complications. AJNR Am J Neuroradiol 35:179818042014

30

Richter HPSchachenmayr W: Preoperative embolization of intracranial meningiomas. Neurosurgery 13:2612681983

31

Rush BRousseau JSekhon MSGriesdale DE: Craniotomy versus craniectomy for acute traumatic subdural hematoma in the United States: a national retrospective cohort analysis. World Neurosurg 88:25312016

32

Salas MHofman AStricker BH: Confounding by indication: an example of variation in the use of epidemiologic terminology. Am J Epidemiol 149:9819831999

33

Shi ZSFeng LJiang XBHuang QYang ZHuang ZS: Therapeutic embolization of meningiomas with Onyx for delayed surgical resection. Surg Neurol 70:4784812008

34

Singla ADeshaies EMMelnyk VToshkezi GSwarnkar AChoi H: Controversies in the role of preoperative embolization in meningioma management. Neurosurg Focus 35(6):E172013

35

Teasdale EPatterson JMcLellan DMacpherson P: Subselective preoperative embolization for meningiomas. A radiological and pathological assessment. J Neurosurg 60:5065111984

36

Wakhloo AKJuengling FDVan Velthoven VSchumacher MHennig JSchwechheimer K: Extended preoperative polyvinyl alcohol microembolization of intracranial meningiomas: assessment of two embolization techniques. AJNR Am J Neuroradiol 14:5715821993

37

Yasui KShoda YSuyama TNuma YAmanouchi YYKawamoto K: Preoperative embolization for meningioma using lipiodol. Interv Neuroradiol 4 (Suppl 1):63661998

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