Elderly Patients with Intracranial Meningioma: Surgical Considerations in 228 Patients with a Comprehensive Analysis of the Literature

Original Article

Elderly Patients with Intracranial Meningioma: Surgical Considerations in 228 Patients with a Comprehensive Analysis of the Literature _ ¨ zmen3, Ebubekir Akpınar5, Murat Imre
rı Canbolat4, Ahmet Akbas¸5, Berk Barıs¸ O Murat S‚ akir Eks¸i1, C¸ag Usseli1, ¨ zduman1,
lu6, Ayc¸a Ers¸en Danyeli2, Koray O Abuzer Gu¨ngo¨r1, Mustafa Gu¨du¨k1, Mehmet Hacıhanefiog M. Necmettin Pamir1

BACKGROUND: Improved life expectancy and advanced diagnostic tools including computed tomography and magnetic resonance imaging have increased the awareness and diagnosis of intracranial meningiomas in the elderly population. The risk/benefit ratio of surgery in elderly patients with intracranial meningioma has not been clearly defined because of the lack of objective measurement tools. We aimed to understand the risk factors associated with postsurgical outcomes and how these risk factors affected postsurgical outcomes in elderly patients with intracranial meningioma.

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METHODS: We retrospectively evaluated 1372 patients, who were operated on for intracranial meningioma, using our prospectively collected database. The same senior author operated on all patients at 2 different tertiary clinics. Patients’ clinical charts, presurgical postcontrast T1-weighted magnetic resonance images, operative reports, and pathology reports were reviewed. The relevant literature was also reviewed.

of Anesthesiologists class was the strongest predictor of postsurgical neurologic complications. A literature review showed higher morbidity and mortality of elderly patients with intracranial meningioma. Initial tumor size and postsurgical MIB-1 labeling index were higher in the elderly patients, both of which were predictors of tumor growth. CONCLUSIONS: Even though elderly patients operated on for intracranial meningioma had higher morbidity and mortality compared with younger patients, surgery is still much more beneficial than wait-and-see strategy in elderly patients.

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RESULTS: Higher age, higher American Society of Anesthesiologists class, presence of comorbidities, tumor location, larger initial tumor size, and presence of peritumoral edema were all associated with postsurgical complications in elderly patients with intracranial meningioma. Age ‡50 years was the strongest predictor of postsurgical systemic complications, whereas higher American Society

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Key words - Elderly - Meningioma - Morbidity - Mortality - Surgery Abbreviations and Acronyms ASA: American Society of Anesthesiologists CRGS: Clinical Radiological Grading System GSS: Geriatric Scoring System KPS: Karnofsky Performance Status MRI: Magnetic resonance imaging SKALE: Sex, Karnofsky Performance Status, American Society of Anesthesiologists Class, Location of Tumor, Peritumoral Edema

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INTRODUCTION

M

eningiomas are assumed to originate from arachnoid cap cells located in the arachnoid villi.1 CBTRUS (Central Brain Tumor Registry in the United States) reported that meningiomas were the most common brain tumors, accounting for 13%e26% of all intracranial tumors. Prevalence of meningiomas was reported as 50.4e70.7 per 100,000 people, and incidence of meningiomas was reported as 1.28e7.8 per 100,000 people per year.2-5 Improved life expectancy and advanced diagnostic tools including computed tomography and magnetic resonance imaging (MRI) increased the awareness and diagnosis of intracranial

From the Departments of 1Neurosurgery and 2Pathology and 3Medical Student, Acıbadem Mehmet Ali Aydınlar University, School of Medicine, Istanbul; 4Vezirköprü State Hospital, Neurosurgery Clinic, Samsun; 5Department of Neurosurgery, Bakırköy Psychiatric Hospital, Health Sciences University, Istanbul, Istanbul; and 6Acıbadem Healthcare Group, Acıbadem Altunizade Hospital, Neurosurgery Clinic, Istanbul, Turkey To whom correspondence should be addressed: Murat S‚ akir Eksxi, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.150 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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Table 1. Comparison of Younger and Elderly Patients Stratified by Demographic, Preoperative Functional Status, Tumor-Related, and Surgery-Related Factors Age-Group (years) <65

‡65

Total (%)

P Value

1144 (83.4)

228 (16.6)

1372 (100)

Not available

Female

849 (74.2)

155 (68)

1004 (73.2)

0.052

Male

295 (25.8)

73 (32)

368 (26.8)

Noneskull base

571 (50)

129 (57)

700 (51)

Skull base

573 (50)

99 (43)

672 (49)

I

1015 (88.7)

196 (86)

1211 (88.3)

IIeIII

129 (11.3)

32 (14)

161 (11.7)

Total Sex

Tumor location 0.06

Tumor grade 0.23

American Society of Anesthesiologists physical status class 1e2

1110 (97)

195 (85.7)

1305 (95.1)

3e5

34 (3)

33 (14.3)

67 (4.9)

<0.001*

Preoperative KPS Score <70

56 (4.9)

17 (7.4)

73 (5.3)


70

1088 (95.1)

211 (92.6)

1299 (94.7)

36.64  16.85

44.64  16.25

37.20  16.89

0.072

Absent

752 (65.7)

70 (30.8)

822 (59.9)

<0.001*

Present

392 (34.3)

158 (69.2)

550 (40.1)

IeII

898 (78.5)

176 (77.19)

1074 (78.28)

IIIeV

246 (21.5)

52 (22.81)

298 (21.72)

Duration of hospital stay (days)

6.10  4.94

6.22  3.13

6.11  4.81

0.399

MIB-1 labeling index (%)

5.14  5.46

6.71  7.60

5.44  5.95

0.120

Largest tumor diameter (mm)

0.115

Edema at the periphery of the tumor

Rate of tumor resection (Simpson grade) 0.662

Values are number (%) except where indicated otherwise. *Statistically significant.

meningiomas in the elderly population.6-8 Elderly patients were described as the ones aged
65 years, and sometimes as those aged
70 years.7,9-27 Intracranial meningiomas were detected 3.5 times higher in patients aged >70 years compared with patients aged 70 years.5 Even though many studies have focused on surgery in elderly patients with intracranial meningioma, indications for surgery and risks associated with surgery in elderly patients with meningioma were inconclusive.18,24,25,28-38 The risk/benefit ratio has not been clearly defined because of the lack of objective measurement tools.36 In this study, we aimed to understand the risk factors associated with postsurgical outcomes and how these risk factors affected postsurgical outcomes in elderly patients (aged
65 years) with intracranial meningioma. We compared data of younger and

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elderly patients operated on for intracranial meningioma. We also analyzed the literature to define the morbidity and mortality of elderly patients who underwent surgery for intracranial meningioma.

METHODS Patient Cohort We retrospectively evaluated 1372 patients who were operated on for intracranial meningioma, using our prospectively collected database. The same senior author (M.N.P.) operated on all patients at 2 different tertiary clinics at Marmara University and Acıbadem MAA University Hospitals between 1986 and 2018. The

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Table 2. Comparison of Patient Age and Patient Presurgical Comorbidities Age (years)

Diabetes Mellitus, n (%)*

Hypertension, n (%)*

Cardiac, n (%)*

Pulmonary, n (%)*

Gastrointestinal, n (%)*

<65

165 (14.4)

299 (26.1)


65

30 (13.2)

122 (53.5)

Total

195 (14.2)

421 (30.7)

121 (8.8)

Renal, n (%)*

P Value

76 (6.6)

93 (8.1)

45 (19.7)

17 (7.5)

216 (18.9)

26 (2.3)

<0.001y

51 (22.2)

17 (7.4)

110 (8.0)

267 (19.5)

43 (3.1)

*% represents the percentage within specified age-group. yStatistically significant.

institutional review board approved this retrospective clinical study (institutional review board approval number 2018-4/15). Study Protocol Doctors (M.S ¸.E., Ç.C., A.A., B.B.Ö., and E.A.), each of who was blind to the others' findings, evaluated patients’ clinical charts,

presurgical postcontrast T1-weighted MRIs, operative reports, and pathology reports to identify age at the time of diagnosis, gender, tumor location, tumor grade and MIB-1 labeling index, patient comorbidities, tumor removal rate, length of hospital stay, and postsurgical neurologic and systemic complications. In case of any conflict, a consensus was reached.

Figure 1. Types of postsurgical neurologic (A) and systemic (B) complications.

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Table 3. Comparison of Gender and Postsurgical Complications Stratified by Age Absent, n (%)

Present, n (%)

<65 Years

‡65 Years

<65 Years

‡65 Years

P Value

Female

716 (62.6)

130 (57)

133 (11.6)

25 (11)

<0.001y

Male

236 (20.6)

46 (20.2)

59 (5.2)

27 (11.8)

Total

952 (83.2)

176 (77.2)

192 (16.8)

52 (22.8)

777 (67.9)

116 (50.9)

72 (6.3)

39 (17.1)

Male

264 (23)

73 (32)

31 (2.8)

0 (0)

Total

1041 (90.9)

189 (82.9)

103 (9.1)

39 (17.1)

Sex Neurologic complications*

Systemic complications* Female

<0.001y

*% represents the percentage within specified age-group. yStatistically significant.

Radiologic and Pathologic Evaluation Tumors were defined as “skull base” and “noneskull base” according to their gross anatomic locations. Tumors located at the convexity dura, falx cerebri, tentorium cerebelli (T3, T4, T5, and T6 according to the Yasargil classification39) and inside the ventricles were classified as noneskull base meningiomas, whereas others including T1, T2, and T7 tentorial meningiomas were classified as skull base meningiomas. The largest linear diameter of tumor was measured in any plane on MRI with
2 views per patient. Peritumoral edema status was defined as present or absent based on T2-weighted images. Tumor resection rate was graded according to the Simpson grade of meningioma resection.40 The resection rates were subdivided simply as

Simpson IeII or Simpson IIIeV. Tumors were graded according to World Health Organization classification. Clinical Evaluation of Patients’ Heath and Functionality Status Patients were categorized according to age-groups for each 5 years (from 50 to 70 years) to identify the effect of age on postsurgical clinical status. The patients’ functional statuses in daily living were re-evaluated using the Karnofsky Performance Status (KPS). The KPS was scored from 0 to 100; 0 corresponds to death, 50e70 corresponds to living at home with assistance, 71e99 corresponds to maintaining daily activities, and 100 corresponds to independent performance.41 Then, the patients with KPS
70 were compared with those with KPS <70.28 Patients’ physical statuses

Table 4. Comparison of Age-Groups and Postsurgical Neurologic and Systemic Complications Neurologic Complications, n (%) Age (years)

Systemic Complications, n (%)

Absent

Present

P Value

Absent

Present

P Value

<50

546 (82.7)

114 (17.3)

0.63

623 (94.4)

37 (5.6)

<0.001*


50

582 (81.8)

130 (18.2)

607 (85.2)

105 (14.8)

<55

745 (83.2)

150 (16.8)


55

383 (80.5)

94 (19.5)

<60

930 (83.3)

187 (16.7)


60

198 (77.8)

57 (22.2)

<65

952 (83.2)

192 (16.8)


65

176 (77.2)

52 (22.8)

<70

1072 (82.5)

227 (17.5)


70

56 (77.8)

17 (22.2)

0.21

822 (91.8)

73 (8.2)

408 (85.6)

69 (14.4)

0.03*

1011 (90.5)

106 (9.5)

219 (85.7)

36 (14.3)

0.03*

1041 (90.9)

103 (9.1)

189 (82.9)

39 (17.1)

0.33

1169 (90.0)

130 (10.0)

61 (83.3)

12 (16.7)

<0.001*

0.03* <0.001*

0.08

*Statistically significant.

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Table 5. Comparison of Presurgical Comorbidities and Postsurgical Complications No Complication, n (%)*

Complications, n (%)*

<65 Years

‡65 Years

<65 Years

‡65 Years

P Value

Diabetes mellitus

152 (92.1)

10 (33.3)

13 (7.9)

20 (66.7)

<0.001y

Hypertension

246 (82.3)

86 (70.5)

53 (17.7)

36 (29.5)

<0.01y

76 (100)

25 (55.6)

0 (0)

20 (44.4)

<0.001y

Comorbidities Neurologic complications

Cardiac Pulmonary

73 (78.5)

17 (100)

20 (21.5)

0 (0)

0.03y

Gastrointestinal

168 (77.8)

40 (78.4)

48 (22.2)

11 (21.6)

0.919

Renal

14 (53.9)

9 (52.9)

12 (46.1)

8 (47.1)

0.953

132 (80)

30 (100)

33 (20)

0 (0)

<0.01y

Hypertension

267 (89.3)

101 (82.8)

32 (10.7)

21 (17.2)

0.06

Cardiac

71 (93.4)

34 (75.6)

5 (6.6)

11 (24.4)

<0.01y

Pulmonary

89 (95.7)

17 (100)

4 (4.3)

0 (0)

1

Gastrointestinal

202 (93.5)

48 (94.1)

14 (6.5)

3 (5.9)

0.874

Renal

23 (88.5)

15 (88.2)

3 (11.5)

2 (11.8)

0.981

Systemic complications Diabetes mellitus

*% represents the percentage within specified age-group. yStatistically significant.

before surgical procedures were defined using American Society of Anesthesiologists (ASA) physical status classification. ASA I represents a normal healthy patient (except the defined illness). ASA II represents a patient with mild systemic disease (includes yet not limited to mild lung disease, well-controlled diabetes mellitus/hypertension, obesity (body mass index 30e40), social alcohol drinker, and current smoker). ASA III represents a patient with severe systemic disease with substantive functional

limitations. ASA IV represents a patient with severe systemic disease with a constant threat to life. A patient who is not expected to survive without the operation is classified as ASA V. ASA VI corresponds to declared brain death status of a patient whose organs are being removed for donor purposes. Hypertension, diabetes mellitus, pulmonary disease, cardiovascular disease, gastrointestinal disease, and renal disease were defined as presurgical comorbidities.

Table 6. Comparison of American Society of Anesthesiologists Class and Postsurgical Complications Absent, n (%) American Society of Anesthesiologists Class

Present, n (%)

<65 Years

‡65 Years

<65 Years

‡65 Years

P Value

<0.001y

Neurologic complications* 1e2

929 (81.2)

162 (71.1)

181 (15.8)

33 (14.5)

3e5

23 (2)

14 (6.1)

11 (1)

19 (8.3)

Total

952 (83.2)

176 (77.2)

192 (16.8)

52 (22.8)

1011 (88.3)

172 (75.4)

99 (8.7)

23 (10.1)

Systemic complications* 1e2 3e5

30 (2.6)

17 (7.5)

4 (0.4)

16 (7)

Total

1041 (90.9)

189 (82.9)

103 (9.1)

39 (17.1)

<0.001y

*% represents the percentage within specified age-group. yStatistically significant.

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Table 7. Comparison of Initial Tumor Size and Postsurgical Complications Largest Tumor Diameter (mm) <65 Years

‡65 Years

Absent

34.91  16.04

43.31  17.41

Present

43.73  18.03

49.10  13.51

Absent

37.28  16.60

45.99  18.45

Present

33.11  18.32

40.16  3.74

Complications

P Value

Neurologic complications 0.025*

Systemic complications 0.310

*Statistically significant.

Follow-Up Patients with grade 1 tumor were regularly followed up at 1 month and yearly thereafter. Patients with higher-grade tumors were followed up at 1 month and biannually thereafter. Mortality within 30 days of index surgery was accepted as perioperative mortality. Clinical and Radiologic Scoring Systems Some clinical and radiologic scoring systems have been developed and used for predicting the postsurgical period of patients with intracranial meningiomas.6 Patients were evaluated using the SKALE (Sex, Karnofsky Performance Status, American Society of Anesthesiologists Class, Location of Tumor, Peritumoral Edema) grading system, Geriatric Scoring System (GSS), and Clinical Radiological Grading System (CRGS). The SKALE grading system evaluates patient’s sex, KPS, ASA, tumor location, and peritumoral edema.36 The GSS evaluates tumor size, tumor location, peritumoral edema, KPS, neurologic deficit, diabetes mellitus, hypertension, and pulmonary disease.31,32 The CRGS evaluates tumor size, tumor location,

peritumoral edema, comorbidities.30

KPS,

neurologic

condition,

and

Literature Review The keywords “meningioma,” “elderly,” and “surgery” were searched in PubMed. References of retrieved articles were analyzed for any relevant content. Number of patients, definition of elderly, rate of postsurgical complications, and 30-day and 1year mortality were evaluated for each article. All relevant articles were analyzed and summarized in 2 tables; one table showed all articles, whereas the other table presented the articles comparing the surgical results of younger and elderly patients with intracranial meningioma from the same clinics. The literature was also reviewed at the end of corresponding tables. Statistical Analysis Data were analyzed using SPSS version 20.0 (IBM Corp., Armonk, New York, USA). Continuous variables were expressed as means and standard deviations, whereas categorical variables were

Table 8. Comparison of Peritumoral Edema and Postsurgical Complications Absent, n (%) Peritumoral Edema

Present, n (%)

<65 Years

‡65 Years

<65 Years

‡65 Years

P Value

<0.001y

Neurologic complications* Absent

642 (56.1)

64 (28.1)

110 (9.6)

6 (2.6)

Present

299 (26.2)

123 (54)

93 (8.1)

35 (15.3)

Total

941 (82.3)

187 (82.1)

203 (17.7)

41 (17.9)

Absent

682 (59.6)

66 (29)

70 (6.1)

4 (1.7)

Present

359 (31.4)

123 (54)

33 (2.9)

35 (15.3)

Total

1041 (91)

189 (83)

103 (9)

39 (17)

Systemic complications* <0.001y

*% represents the percentage within specified age-group. yStatistically significant.

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Table 9. Comparison of Age and Scoring Systems Age (years)

Points

P Value

Sex, Karnofsky Performance Status, American Society of Anesthesiologists Class, Location of Tumor, and Peritumoral Edema Grading System <65

13.70  1.81


65

12.84  1.80

Total

13.63  1.82

0.024*

Geriatric Scoring System <65

19.51  1.91


65

18.15  1.99

Total

19.41  1.94

0.020*

Clinical Radiological Grading System <65

14.20  1.76


65

13.08  2.13

Total

14.12  1.82

0.085

44.64 mm; P ¼ 0.072). Peritumoral edema was seen in 40.1% of the patients. Elderly patients were significantly more likely to have peritumoral edema compared with the younger patients (69.2% vs. 34.3%; P < 0.001). Tumor resection rate was Simpson grade I or II in 78.28% of all patients. Tumor resection rates were Simpson grade IeII in 78.5% of the younger patients and in 77.19% of the elderly patients. Tumor resection rates were Simpson grade IIIeV in 21.5% and 22.81% of the younger and the elderly patients, respectively. There was no significant difference of tumor resection rates between age-groups (P ¼ 0.662). Grade I meningiomas were more prevalent than grade II and III meningiomas (88.3% vs. 11.7%) in the whole cohort. Younger and elderly patients had comparatively similar rates of grade I (88.7% vs. 86%) and grade II or grade III (11.3% vs. 14%; P ¼ 0.23) tumors. Mean MIB-1 labeling index was 5.44% for the whole cohort. MIB-1 labeling index was comparatively higher in the elderly patients, even though the difference was not statistically significant (6.71% vs. 5.14%; P ¼ 0.12; Table 1).

Demographics A total of 1372 patients with intracranial meningioma were evaluated. There were 1004 women (73.2%) and 368 men (26.8%) in this cohort (mean age, 51.9 years; range, 18e100 years). At the time of surgery, 16.6% (n ¼ 228) of these patients were aged
65 years (range, 65e100 years). In our series, noneskull base and skull base meningiomas were seen in 51% (n ¼ 700) and 49% (n ¼ 672) of the patients, respectively (Table 1). Most patients (94%, n ¼ 1290) were symptomatic. The most common symptoms were headache, seizure, and visual disturbances.

ASA Class and KPS Scores In younger patients, 97% (n ¼ 1110) were graded as ASA class 1-2, whereas only 3% (n ¼ 34) were graded as ASA class 3e5. In the elderly patients, 85.7% (n ¼ 195) were graded as ASA class 1-2, whereas 14.3% (n ¼ 33) were graded as ASA class 3e5. Elderly patients had significantly higher ASA scores than did younger patients (P < 0.001; Table 1). In younger patients, 95.1% (n ¼ 1088) had KPS scores
70, whereas 4.9% (n ¼ 56) had KPS scores <70. In the elderly patients, 92.6% (n ¼ 211) had KPS scores
70, whereas 7.4% (n ¼ 17) had KPS scores <70. Agegroups did not significantly differ in terms of KPS scores (P ¼ 0.115; Table 1). Diabetes mellitus was present in 14.4% (n ¼ 165) of the younger patients and 13.2% (n ¼ 30) of the elderly patients. Hypertension was present in 26.1% (n ¼ 299) of the younger patients, and 53.5% (n ¼ 122) of the elderly patients. Cardiac comorbidities were present in 6.6% (n ¼ 76) and 19.7% (n ¼ 45) of the younger and elderly patients, respectively. Pulmonary comorbidities were observed in 8.1% (n ¼ 93) of the younger patients, and in 7.5% (n ¼ 17) of the elderly patients. Gastrointestinal problems were seen in 18.9% (n ¼ 216) and 22.2% (n ¼ 51) of the younger and elderly patients, respectively. Renal disorders were observed in 2.3% (n ¼ 26) of the younger and 7.4% (n ¼ 17) of the elderly patients, respectively. Elderly patients were significantly more likely to have hypertension, cardiac and renal comorbidities in the presurgical period compared with the younger patients (P < 0.001, Table 2).

Tumor Characteristics There were 1144 younger patients (aged <65 years) in the cohort. Fifty percent of the younger patients (n ¼ 571) had noneskull base meningiomas, whereas the other 50% (n ¼ 573) had skull base meningiomas. Noneskull base and skull base meningiomas were detected in 57% (n ¼ 129) and 43% (n ¼ 99) of the elderly patients, respectively. Younger and elderly patients had no significant difference in terms of tumor location (P ¼ 0.06). In 1372 patients, the mean linear diameter of the tumors was 37.2 mm. Younger and elderly patients had no significant difference in terms of the largest linear tumor diameter (36.64 mm vs.

Postsurgical Complications The mean length of hospital stay was 6.11 days for the whole cohort, 6.1 days for younger patients, and 6.22 days for elderly patients (P ¼ 0.399, Table 1). Postsurgical neurologic complications were seen in 17.8% of the patients (n ¼ 244) (Figure 1A). In these 244 patients with postsurgical neurologic complications, 78.7% (n ¼ 192) were younger than 65 years, whereas 21.3% (n ¼ 52) were aged 65 years or older. There was significant difference between agegroups in terms of postsurgical neurologic complications (16.8% vs. 22.8%; P ¼ 0.03). Postsurgical neurologic complications were

*Statistically significant.

presented as numbers and percentages. Data were not distributed normally according to Kolmogorov-Smirnov and Shapiro-Wilk tests. A c2 test or Fisher exact test and a Mann-Whitney U or a 1-way analysis of variance test were used for categorical and continuous variables, respectively. A binary logistic regression test was performed to determine the odds ratio of presurgical risk factors that could predict outcomes. The odds ratios and 95% confidence intervals were calculated for each risk factor. An a value of <0.05 was accepted as significant. RESULTS

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Table 10. Clinical Series of Elderly Patients with Intracranial Meningioma Reported in the Literature Number of Patients

Limit of Seniority (years)

Postsurgical Complications (%)

30-Day Mortality (%)

1-Year Mortality (%)

Timmer et al., 201942

133

55

N/A

N/A

N/A

DelgadoFernandez et al., 201843

110

70

25.5

3.6

4.5

Kolakshyapati et al., 201844

57

65

33

1.8

1.8

Meling et al., 201845

321

70

8.1*

4.7

N/A

Di Cristofori et al., 201846

41

70

14.6*

N/A

N/A

Zoia et al., 201847

107

70

21.5

N/A

N/A

Isobe et al., 201848

265

65

28.3

0.4

0.8

Amano et al., 201811

34

75

14.7*

0

N/A

Dobran et al., 201849

25

80

12*

8

N/A

Slot et al., 20189

23

65

N/A

0

N/A

da Silva and de Freitas, 201810

23

65

26*

8.6

N/A

Zhao et al., 201812

115

65

24.4*

3.9

N/A

Yamamoto et al., 201713

16

75

6.3*, 0y

0

0

Brokinkel et al., 201714

142

65

N/A

7.2

N/A

Diaz et al., 201650

52

65

N/A

5.7

25

Bir et al., 201651

81

70

32.3

1.2

N/A

Troya Castilla et al., 201615

37

70

49

5.4

13.5

Nayeri et al., 201652

45

60

N/A

N/A

N/A

Chen et al., 201528

86

65

N/A

1.2

2.3

Bartek et al., 201516

135

70

N/A

N/A

N/A

Zhang et al., 201553

209

65

N/A

N/A

N/A

Konglund et al., 201354

54

60

33.5*, 11.2y

5.6

9.3

Konglund et al., 201355

51

80

N/A

3.9

15.7

Poon et al., 201317

92

65

69.6

0

4.3

Reference

Continues

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WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.08.150

ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Table 10. Continued Number of Patients

Limit of Seniority (years)

Postsurgical Complications (%)

30-Day Mortality (%)

1-Year Mortality (%)

Schul et al., 201256

164

65

49.4*, 4.9y

3.7

6.7

Cohen-Inbar et al., 201132

120

65

47.2*, 4.4y

N/A

13.7

Grossman et al., 201157

5717

65

11*, 6.5y

3.2

N/A

Pirracchio et al., 201058

46

70

N/A

6.1

N/A

Cohen-Inbar et al., 201031

250

65

59.8

N/A

N/A

Patil et al., 201018

258

70

29.8

12

N/A

Rogne et al., 200959

79

70

N/A

2.5

6.3

Roser et al., 200719

43

70

23.2*, 30.2y

0

0

Boviatsis et al., 200720

108

65

17.9*, 21.8y

6.5

N/A

Riffaud et al., 200760

11

80

9.1

0

9.1

Sacko et al., 200736

74

80

6.8*, 2.7y

0

9.4

Yano et al., 200621

54

70

11.1*, 5.6y

N/A

N/A

D'Andrea et al., 200534

37

80

10.8*, 5.4y

13.5

13.5

Caroli et al., 200530

90

70

N/A

6.7

15.6

Bateman et al., 200522

2304

70

N/A

4

N/A

Nakamura et al., 200523

21

70

23.8*, 28.6y

0

4.8

Sonoda et al., 200561

25

70

16*, 0y

4

N/A

Tucha et al., 200162

33

60

N/A

N/A

N/A

Kuratsu et al., 20007

30

70

23.3

0

N/A

Buhl et al., 200063

66

70

30.3*, 19.7y

7.6

16.7

Black et al., 199824

57

65

7*, 8.8y

1.8

N/A

Lieu and Howng, 199837

36

65

47.2

11.1

N/A

Pompili et al., 199864

37

75

N/A

10.8

N/A

Reference

N/A, not available. *Neurologic complications. ySystemic complications.

WORLD NEUROSURGERY -: e1-e16, - 2019

Continues

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Table 10. Continued Number of Patients

Limit of Seniority (years)

Postsurgical Complications (%)

30-Day Mortality (%)

1-Year Mortality (%)

Proust et al., 199765

39

70

10.3

7.6

N/A

Mastronardi et al., 199566

17

80

5.8

29.4

N/A

Nishizaki et al., 199425

78

70

13

N/A

N/A

McGrail and Ojemann, 199438

56

70

35.7

3.6

N/A

Gijtenbeek et al., 199367

93

60

41

14

N/A

Maurice-Williams and Kitchen, 199226

46

65

13.7

3.9

N/A

Umansky et al., 199268

37

70

37

5.4

N/A

Cornu et al., 199033

96

65

57

16

N/A

Arienta et al., 199029

34

70

44

12

N/A

Awad et al., 198969

75

60

48

6.6

N/A

Djindjian et al., 198835

30

70

47

23

N/A

Jan et al., 198627

35

70

N/A

N/A

N/A

Papo, 198370

54

60

24.1*, 14.8y

55

N/A

12604

55e80

37.11 (23 studies with all complications), 13.25* (21 studies with neurologic complications), 7.07y (15 studies with systemic complications)

4.31 (48 studies reported 30-day mortality)

7.61 (20 studies reported 1-year mortality)

Reference

Total

N/A, not available. *Neurologic complications. ySystemic complications.

seen in 15.7% of women (n ¼ 158), and 23.4% of men (n ¼ 86). In women with postsurgical neurologic complications, 84.2% (n ¼ 133) were aged <65 years, and 15.8% (n ¼ 25) were aged
65 years. In men with postsurgical neurologic complications, 68.6% (n ¼ 59) were aged <65 years, and 31.4% (n ¼ 27) were aged
65 years. Postsurgical neurologic complications were significantly more common in men than in women both in younger (20% vs. 15.7%) and elderly (37% vs. 16.1%; P < 0.001) groups. Postsurgical systemic complications were seen in 10.4% of the patients (n ¼ 142) (Figure 1B). In these 142 patients with postsurgical systemic complications, 72.5% (n ¼ 103) were aged <65 years, whereas 27.5% (n ¼ 39) were aged
65 years. Elderly patients had significantly higher rates of postsurgical systemic

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complications (17.1% vs. 9.1%; P < 0.001). Postsurgical systemic complications were seen in 11.1% of women (n ¼ 111) and 8.4% of men (n ¼ 31). Postsurgical systemic complications were significantly more prevalent in younger men than in younger women (10.6% vs. 8.5%), and in elderly women than in elderly men (25.2% vs. 0%; P < 0.001; Table 3). All patients were divided in 5-year age-groups from 50 to 70 years of age. Elderly patients aged
60 years (22.2% vs. 16.7%; P ¼ 0.03) and
65 years (22.8% vs. 16.8%; P ¼ 0.03) had significantly higher rates of postsurgical neurologic complications. Besides, elderly patients aged
50 years (14.8% vs. 5.6%; P < 0.001),
55 years (14.4% vs. 8.2%; P < 0.001),
60 years (14.3% vs. 9.5%; P ¼ 0.03) and
65 years (17.1% vs. 9.1%; P < 0.001) had

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

significantly higher rates of postsurgical systemic complications (Table 4). Younger and elderly patients were compared in terms of any association between presurgical comorbidities and postsurgical complications. Elderly patients with diabetes mellitus (66.7% vs. 7.9%; P < 0.001), hypertension (29.5% vs. 17.7%; P < 0.01), and cardiac comorbidities (44.4% vs. 0%; P < 0.001), and younger patients with pulmonary comorbidities (21.5% vs. 0%; P ¼ 0.03) had significantly higher rates of postsurgical neurologic complications. Elderly patients with cardiac comorbidities (24.4% vs. 6.6%; P < 0.01), and younger patients with diabetes mellitus (20% vs. 0%; P < 0.01) had significantly higher rates of postsurgical systemic complications (Table 5). Presurgical ASA classes were compared in terms of postsurgical complications. Postsurgical neurologic (44.8% vs. 16.4%; P < 0.001) and systemic (29.9% vs. 9.4%; P < 0.001) complications were significantly more common in patients with higher ASA classes (3e5) (Table 6). Radiologic parameters were compared in terms of postsurgical complications. Elderly patients with noneskull base tumors were more likely to have postsurgical neurologic complications than were those with skull base tumors (18.9% vs. 4%) compared with younger patients (8.7% vs. 8%). The difference in postsurgical neurologic complications between age-groups in terms of tumor location was statistically significant (P < 0.001). However, elderly (7% vs. 10.1%) and younger (2.7% vs. 6.3%) patients had no significant differences in terms of having postsurgical systemic complications based on their tumor locations (P ¼ 0.216). Postsurgical neurologic complications were more commonly detected in patients with larger tumor diameter in both younger (43.73 mm vs. 34.91 mm) and elderly (49.1 mm vs. 43.31 mm) groups (P ¼ 0.025). Tumors were comparatively larger in patients without postsurgical systemic complications both in younger (37.28 mm vs. 33.11 mm) and elderly (45.99 mm vs. 40.16 mm) groups (P ¼ 0.31; Table 7). Peritumoral edema was significantly associated with both postsurgical neurologic (15.3% vs. 2.6%) and systemic complications (15.3% vs. 1.7%) in elderly patients (P < 0.001). No such association was observed in the younger group (Table 8). Scoring Systems The mean SKALE score was 13.63 points (range, 8e16 points), and the mean GSS score was 19.41 points (range, 15e24 points). Younger patients had significantly higher SKALE and GSS scores compared with the elderly patients (SKALE: 13.7 vs. 12.84 points, P ¼ 0.024; GSS: 19.51 vs. 18.15 points, P ¼ 0.020). The mean CRGS score of the cohort was 14.12 points (range, 9e 18 points). Younger patients had higher CRGS scores than did the elderly patients. However, the difference was not statistically significant (14.2 vs. 13.08 points; P ¼ 0.085; Table 9). Predictive Factors of Postsurgical Complications Bivariate regression analysis showed that age
50 years was the strongest predictor of postsurgical systemic complications (odds ratio, 2.98; 95% confidence interval, 1.35e6.58; P ¼ 0.007), whereas higher ASA class (3e5) was the strongest predictor of postsurgical neurologic complications (odds ratio, 4.33; 95% confidence interval, 1.40e13.42; P ¼ 0.011).

WORLD NEUROSURGERY -: e1-e16, - 2019

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

Literature Review In the literature, 60 articles reporting surgery in elderly patients with intracranial meningiomas were published between 1983 and 2019, until the current series. There were 12,604 elderly patients operated on for intracranial meningioma. The limit for seniority ranged between 55 and 80 years. The rates of all complications, of only neurologic complications, and of only systemic complications were 37.11%, 13.25%, and 7.07%, respectively. Thirty-day and 1year mortality of elderly patients operated on for intracranial meningioma were 4.31% (range, 0%e55%) and 7.61% (range, 0%e25%), respectively (Table 10). Twenty-one of those 60 articles compared younger and elderly patients operated on for intracranial meningioma from the same clinics. When only those 21 articles were analyzed together with the present series, there were 3933 elderly and 12,313 younger patients. The limit for seniority ranged from 60 to 75 years. The rates of all complications, of only neurologic complications, and of only systemic complications in elderly patients were 33.64%, 18.33%, and 16.87%, respectively. The same rates in younger patients were 14.7%, 16.42%, and 7.62%, respectively. Thirty-day and 1-year mortality were 5.07% (range, 0%e55%) and 4.79% (range, 0%e13.5%) in the elderly group, and 2.03% (range, 0%e4.6%) and 0.43% (range, 0%e 1.1%) in the younger group (Table 11). DISCUSSION Elder age was defined according to different thresholds. The United Nations describes elderly people as people aged >60 years, whereas the World Health Organization defines 65 years as the border for seniority.6 CBTRUS has reported a recent meningioma incidence of 8/100,000, 49% of which was composed of patients > 65 years. The trend in European data has similarities to U.S. data; 4.4/100,000 in the general population, 11.28/100,000 in patients aged 70e79 years, 11.98/100,000 in patients aged
80 years.71 Incidental detection of intracranial meningioma has been increasing in the elderly, since the world population has been aging and diagnostic imaging tools have advanced.6,72-74 Even though many studies focused on surgery in elderly patients with intracranial meningioma, results were conflicting and variable (Tables 10 and 11).4,7,9-38,42-53 Previously identified risk factors were gender, presurgical general health and neurologic status, tumor location, tumor size, and peritumoral edema.34,36,66 In this respect, 2 questions require clear answers: 1) Should we operate on elderly patients with intracranial meningioma? 2) What kinds of risks are expected in surgery of elderly patients with intracranial meningioma? Should We Operate on Elderly Patients with Intracranial Meningioma? To better define surgical indications in the elderly population, the natural history of incidentally diagnosed meningioma in this age-group should be discussed first. Only a few articles in the literature have presented the natural history of intracranial meningioma.7,8,21,74-81 Articles related to natural history in elderly patients with intracranial meningioma are even rarer in the English literature.74,82,83 Krampla et al.82 conducted MRI scans in patients from the VITA (Vienna Transdanube Aging) trial cohort, which was designed to

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Postsurgical Complications (%)

30-Day Mortality (%)

1-Year Mortality (%)

www.SCIENCEDIRECT.com

Limit of Seniority (years)

Elderly

Younger

Elderly

Present series

228

1144

65

17.9*, 17.1y

17.7*, 9.1y

0.9

0.3

N/A

N/A

Amano et al., 201811

34

104

75

14.7*

19.2*

0

N/A

N/A

N/A

Slot et al., 20189

23

66

65

N/A

N/A

0

3

N/A

N/A

da Silva and de Freitas, 201810

23

23

65

26*

34.7*

8.6

4.3

N/A

N/A

Zhao et al., 201812

115

413

65

24.4*

14.8*

3.9

N/A

N/A

N/A

Yamamoto et al., 201713

16

54

75

6.3*, 0y

24.1*

0

0

0

0

Brokinkel et al., 201714

142

325

65

N/A

N/A

7.2

1

N/A

N/A

Troya Castilla et al., 201615

37

390

70

49

N/A

5.4

N/A

13.5

N/A

Bartek et al., 201516

135

844

70

N/A

N/A

N/A

N/A

N/A

N/A

Poon et al., 201317

92

92

65

69.6

51.1

0

0

4.3

1.1

Patil et al., 201018

258

960

70

29.8

13.1

12

4.6

N/A

N/A

Roser et al., 200719

43

89

70

23.2*, 30.2y

10.1*, 2.2y

0

0

0

0

Boviatsis et al., 200720

108

240

65

17.9*, 21.8y

11.3*, 7.7y

6.5

4.2

N/A

N/A

Yano et al., 200621

54

159

70

11.1*, 5.6y

17*, 3.8y

N/A

N/A

N/A

N/A

Bateman et al., 200522

2304

6557

70

N/A

N/A

4

N/A

N/A

N/A

Nakamura et al., 200523

21

56

70

23.8*, 28.6y

19.6*, 1.8y

0

0

4.8

N/A

Kuratsu et al., 20007

30

166

70

23.3

3.5

0

N/A

N/A

N/A

Black et al., 199824

57

57

65

7*, 8.8y

8.8*, 3.5y

1.8

0

N/A

N/A

Reference

Younger

Elderly

Younger

ORIGINAL ARTICLE

Number of Younger Patients

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

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Number of Elderly Patients

MURAT S ¸ AKIR EKS ¸ I ET AL.

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Table 11. Literature Review of Articles Comparing Elderly and Younger Patients Operated on for Intracranial Meningioma

ORIGINAL ARTICLE

0.43 (3 studies reported 1-year mortality)

establish prognostic criteria for Alzheimer disease. Patients were aged 75 years at the time of the research. These investigators detected intracranial meningioma in 9 women out of 532 patients. None of the patients with incidental intracranial meningioma was symptomatic. All patients were offered regular follow-ups with radiographic tools. One patient opted to be operated on. The tumor was confirmed as meningioma. No complication occurred. One of the remaining 8 tumors (12.5%) progressed within 3.5 years. Arienta et al.83 presented their series of 46 elderly patients (>70 years) with intracranial meningioma. These investigators operated on 34 patients and conservatively followed up the remaining 12 patients, who were not available for surgery because of worse medical condition, small tumor size, and lack of consent by the patient and the family. During their 2year follow-up, 6 of 12 (50%) elderly patients who were conservatively followed up died of tumor-related conditions. Only 2 of 6 remaining patients (33.3%) had unchanged KPS at final follow-up, yet 4 patients (66.7%) deteriorated until final follow-up. The mortality of the conservatively followed up patients (50%) was higher than the mortality of operated patients at both 1 month (11.7%) and 3 months (20.5%) after surgery. In a comprehensive analysis of 40 asymptomatic patients with intracranial meningioma (32 women and 8 men), aged >70 years, tumor growth was observed in 14 patients (35%) at a mean followup time of 32.1 months.74 Five of those 14 patients (35.7%) became symptomatic later. Three patients, who became symptomatic during follow-up, were operated on. The remaining 2 symptomatic patients were followed up because of old age and poor medical condition. One of those 2 patients died of a tumor-related condition 88 months after the initial diagnosis. Six of 9 patients with asymptomatically growing intracranial meningioma were treated using Gamma Knife radiosurgery (Elekta, Stockholm, Sweden). Although Krampla et al.82 reported a 12.5% progression of tumor size, Arienta et al.83 and Niiro et al.74 showed higher rates of progression and tumor growth in elderly patients during their follow-up. Most of the patients in the current series were already symptomatic at their admission to the clinic. Elderly patients had larger initial tumor size and higher MIB-1 labeling index compared with younger patients. Higher MIB-1 index and larger initial tumor size were reported in tumors with growth potential.74,84 Tumor growth rates and tumor-related deaths in elderly patients could not be ignored, when the literature is considered. Elderly patients with intracranial meningioma should be carefully selected for surgery according to their medical condition.

60e75 12313

N/A, not available. *Neurologic complications. ySystemic complications.

3933 Total

Papo, 1983

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

33.64 (6 studies with all 14.7 (3 studies with all 5.07 (18 studies 2.03 (11 studies 4.79 (5 studies complications), 16.42* reported 30-day reported 30-day reported 1-year complications), 18.33* mortality) mortality) mortality) (10 studies (11 studies with neurologic with neurologic complications), 16.87y (8 complications), 7.62y (6 studies with systemic studies with systemic complications) complications)

N/A N/A N/A 55 N/A 60 54

209

24.1*, 14.8y

N/A N/A N/A N/A N/A 70 35

70

Jan et al., 198627

98

N/A

N/A N/A N/A 3.9 N/A 13.7 65 98 46 Maurice-Williams and Kitchen, 199226

70 78 Nishizaki et al., 199425

169

13

N/A

N/A

N/A

N/A

N/A

MURAT S ¸ AKIR EKS ¸ I ET AL.

WORLD NEUROSURGERY -: e1-e16, - 2019

What Kinds of Risks Are Expected in Surgery of Elderly Patients with Intracranial Meningioma? A comparative literature review of elderly and younger patients operated on for intracranial meningioma from the same clinics showed that elderly patients had higher rates of morbidity and mortality compared with younger ones. Some of those studies reported postsurgical neurologic and systemic complications all together and some reported these complications separately. In the studies evaluating postsurgical neurologic and systemic complications all together, postsurgical complications in elderly and younger patients were reported as 33.64% and 14.7%,

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ORIGINAL ARTICLE MURAT S ¸ AKIR EKS ¸ I ET AL.

SURGERY OF ELDERLY PATIENTS WITH MENINGIOMA

respectively.7,15,17,18,25,26 The studies that reported postsurgical neurologic (18.33% vs. 16.42%) and systemic (16.87% vs. 7.62%) complications separately had similar trends.10-13,19-21,23,24,70 In the present series, elderly patients had higher rates of postsurgical complications compared with younger patients. Higher ASA class was the strongest predictor of postsurgical neurologic complications, and older age was the strongest predictor of postsurgical systemic complications. Mortality at 1 month and 1 year was also higher in elderly patients both in the literature and in the present series.10,14,18,20,24 Clinical and radiologic grading systems for predicting the postsurgical outcomes were reported as useful for elderly patients with intracranial meningioma.30,31,36 Caroli et al.30 found that CRGS score <10 was a poor prognostic factor. Sacko et al. stated that only 50% of the patients with SKALE score <8 survived for 1 year after the surgery. Mortality was 10.5% for patients with SKALE scores of 8, 0% for patients with SKALE scores >8.36 Cohen-Inbar et al.31 reported a score of 15 points as the cutoff value for better outcome in GSS. Overall, elderly patients in the present series had lower points than did younger patients on these scoring systems (CRGS, SKALE, and GSS). However, the scores of elderly patients were still higher than the cutoff values of these corresponding scoring systems. Thus, surgery would be beneficial for selected elderly patients with intracranial meningioma, when morbidity and mortality of unoperated elderly patients are taken into account.

REFERENCES 1. Baldi I, Engelhardt J, Bonnet C, et al. Epidemiology of meningiomas. Neurochirurgie. 2018; 64:5-14.

Limitations There are some limitations to the current study. This is a retrospective review of prospectively collected data. The patients who had been conservatively followed up or had been treated with radiosurgery were not included in the cohort to make a comparison. However, important results with a thorough review of the literature ending up with important conclusions and suggestions for surgery in elderly patients with intracranial meningioma were presented.

CONCLUSIONS Elderly patients with intracranial meningioma are usually symptomatic at the time of admission. Tumor growth is expected in those patients with larger initial tumor size and higher MIB-1 labeling index. Even though elderly patients operated on for intracranial meningioma had higher morbidity and mortality compared with younger patients, surgery is still more beneficial than wait-and-see strategy in carefully selected elderly patients.

ACKNOWLEDGMENTS We thank Dr. Emel Ece Özcan-Eks¸i, Ali Durmaz, and Halil Kardas¸ for their efforts in preparation of this manuscript.

8. Oya S, Kim SH, Sade B, Lee JH. The natural history of intracranial meningiomas. J Neurosurg. 2011;114:1250-1256. 9. Slot KM, Peters JVM, Vandertop WP, Verbaan D, Peerdeman SM. Meningioma surgery in younger and older adults: patient profile and surgical outcomes. Eur Geriatr Med. 2018;9:95-101.

2. Duong LM, McCarthy BJ, McLendon RE, et al. Descriptive epidemiology of malignant and nonmalignant primary spinal cord, spinal meninges, and cauda equina tumors, United States, 2004-2007. Cancer. 2012;118:4220-4227.

10. da Silva CE, de Freitas PEP. Surgical removal of skull base meningiomas in symptomatic elderly patients. World Neurosurg. 2018;120:e1149-e1155.

3. Davis FG, Kupelian V, Freels S, McCarthy B, Surawicz T. Prevalence estimates for primary brain tumors in the United States by behavior and major histology groups. Neuro Oncol. 2001;3:152-158.

11. Amano T, Nakamizo A, Michiwaki Y, Matsuo S, Fujioka Y, Nagata S. Surgical outcome in elderly patients with intracranial meningioma. J Clin Neurosci. 2018;56:63-66.

4. Porter KR, McCarthy BJ, Freels S, Kim Y, Davis FG. Prevalence estimates for primary brain tumors in the United States by age, gender, behavior, and histology. Neuro Oncol. 2010;12: 520-527.

12. Zhao X, Zhao D, Wu Y, et al. Meningioma in the elderly: characteristics, prognostic factors, and surgical strategy. J Clin Neurosci. 2018;56:143-149.

5. Louis DN, Scheithauer BW, Budka H, von Deimling A, Kepes JJ. Meningiomas. In: Kleihues P, Cavenee WK, eds. Pathology and Genetics of Tumours of the Nervous System: World Health Organisation Classification of Tumours. Lyon: IARC Press; 2000:175-184. 6. Ikawa F, Kinoshita Y, Takeda M, et al. Review of current evidence regarding surgery in elderly patients with meningioma. Neurol Med Chir (Tokyo). 2017;57:521-533. 7. Kuratsu J, Kochi M, Ushio Y. Incidence and clinical features of asymptomatic meningiomas. J Neurosurg. 2000;92:766-770.

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13. Yamamoto J, Takahashi M, Idei M, et al. Clinical features and surgical management of intracranial meningiomas in the elderly. Oncol Lett. 2017;14: 909-917. 14. Brokinkel B, Holling M, Spille DC, et al. Surgery for meningioma in the elderly and long-term survival: comparison with an age- and sexmatched general population and with younger patients. J Neurosurg. 2017;126:1201-1211. 15. Troya Castilla M, Chocron Gonzalez Y, Marquez Rivas FJ. [Complications and outcomes in the elderly with intracranial meningioma]. Rev Esp Geriatr Gerontol. 2016;51:82-87 [in Spanish]. 16. Bartek J Jr, Sjavik K, Forander P, et al. Predictors of severe complications in intracranial

meningioma surgery: a population-based multicenter study. World Neurosurg. 2015;83:673-678. 17. Poon MT, Fung LH, Pu JK, Leung GK. Outcome comparison between younger and older patients undergoing intracranial meningioma resections. J Neurooncol. 2013;114:219-227. 18. Patil CG, Veeravagu A, Lad SP, Boakye M. Craniotomy for resection of meningioma in the elderly: a multicentre, prospective analysis from the National Surgical Quality Improvement Program. J Neurol Neurosurg Psychiatry. 2010;81:502-505. 19. Roser F, Ebner FH, Ritz R, Samii M, Tatagiba MS, Nakamura M. Management of skull based meningiomas in the elderly patient. J Clin Neurosci. 2007;14:224-228. 20. Boviatsis EJ, Bouras TI, Kouyialis AT, Themistocleous MS, Sakas DE. Impact of age on complications and outcome in meningioma surgery. Surg Neurol. 2007;68:407-411 [discussion 411]. 21. Yano S, Kuratsu J, Kumamoto Brain Tumor Research Group. Indications for surgery in patients with asymptomatic meningiomas based on an extensive experience. J Neurosurg. 2006;105: 538-543. 22. Bateman BT, Pile-Spellman J, Gutin PH, Berman MF. Meningioma resection in the elderly: nationwide inpatient sample, 1998-2002. Neurosurgery. 2005;57:866-872 [discussion 866-872]. 23. Nakamura M, Roser F, Dormiani M, Vorkapic P, Samii M. Surgical treatment of cerebellopontine angle meningiomas in elderly patients. Acta

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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 13 June 2019; accepted 22 August 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.150 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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