Gross-total resection outcomes in an elderly population with glioblastoma: a SEER-based analysis

Clinical article

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Object

There is limited information on the relationship between patient age and the clinical benefit of resection in patients with glioblastoma. The purpose of this study was to use a population-based database to determine whether patient age influences the frequency that gross-total resection (GTR) is performed, and also whether GTR is associated with survival difference in different age groups.

Methods

The authors identified 20,705 adult patients with glioblastoma in the Surveillance, Epidemiology, and End Results (SEER) registry (1998–2009). Surgical practice patterns were defined by the categories of no surgery, subtotal resection (STR), and GTR. Kaplan-Meier and multivariate Cox regression analyses were used to assess the pattern of surgical practice and overall survival.

Results

The frequency that GTR was achieved in patients with glioblastoma decreased in a stepwise manner as a function of patient age (from 36% [age 18–44 years] to 24% [age ≥ 75]; p < 0.001). For all age groups, glioblastoma patients who were selected for and underwent GTR showed a 2- to 3-month improvement in overall survival (p < 0.001) relative to those who underwent STR. These trends remained true after a multivariate analysis that incorporated variables including ethnicity, sex, year of diagnosis, tumor size, tumor location, and radiotherapy status.

Conclusions

Gross-total resection is associated with improved overall survival, even in elderly patients with glioblastoma. As such, surgical decisions should be individually tailored to the patient rather than an adherence to age as the sole clinical determinant.

Abbreviations used in this paper:GTR = gross-total resection; HR = hazard ratio; OR = odds ratio; SEER = Surveillance, Epidemiology, and End Results; STR = subtotal resection.

Whether more extensive glioblastoma resection translates into survival benefit remains a central question in neurooncology.5,11,17,18 Autopsy studies revealed glioblastoma as an aggressively infiltrative disease, with tumor cells found more than 2 cm from the regions of contrast enhancement.12,26 As such, complete surgical excision of glioblastoma cannot be achieved without extended removal of inherently eloquent human cerebrum.2,14 The incremental gain of mitigating tumor burden versus the risks of an extended removal warrants thoughtful deliberation and clinical validation.

Unfortunately, the clinical benefit of glioblastoma resection is not one easily amenable to randomized clinical trial design. The complexities of surgical planning/execution, the inherent molecular heterogeneity of glioblastomas, the varied clinical presentations and neuroanatomy, as well as the general rarity of glioblastoma9,13,16 constitute formidable barriers to a meaningful clinical trial. However, there is mounting evidence from carefully documented single-institution experiences that suggest maximal glioblastoma resection is associated with survival benefit.5,11,17,18 In this regard, there is an emerging consensus that “maximal safe resection” should be attempted in glioblastoma surgery.

In clinical practice, the principle of maximal safe resection is often balanced against the notion of “do no harm,” particularly as it pertains to elderly patients with glioblastoma. Some oncology practitioners have advanced the notion that glioblastoma in patients older than 70 years of age derive little value from resection, chemotherapy, or radiation therapy.19 As such, many practitioners have strongly advocated against aggressive treatment in the elderly population on the grounds of treatment-related toxicity.8 Accordingly, studies reveal that elderly patients with glioblastoma are less likely to receive the treatments offered to their younger counterparts.6

In this context, the study aims to determine the impact of age on neurosurgical treatment of glioblastoma patients. The Surveillance, Epidemiology, and End Results (SEER) registry was used to determine whether patient age influences the frequency that gross-total resection (GTR, as defined by the complete removal of the contrast-enhancing lesion) is achieved in patients with glioblastoma. The impact that age has on the overall survival of patients with glioblastoma undergoing GTR was also assessed. We used the SEER registry for our study because the data set is broadly representative of the oncology care provided to the entire US population and includes data from patients treated at both academic and nonacademic institutions. Furthermore, the registry offers access to data related to glioblastoma patients on a scale that cannot be matched by any single institutional experience.

Methods

Data Source

Data for this study was obtained from the SEER public-use database. This database was established by the National Cancer Institute in Bethesda, Maryland, to collect cancer incidence and survival data from 18 population-based cancer registries in distinct geographic areas. The SEER database currently represents 28% of the US population22 and the demographic of the database is broadly representative of the general US population, and includes data from both academic and nonacademic institutions. As a cancer registry, the SEER database is considered the gold-standard database in which independent verifications of collected variables were performed.22

Study Period and Extent of Resection

Data from 1998 to 2009 were used for this study. Pertaining to the extent of resection, there were no reliable codes that could be uniformly applied to all time periods. Surgical codes that consistently capture the relevant categories of resection (no surgery, partial resection/local excision, and GTR) were available only for the time period of 1998 to 2009. Detailed surgical code definitions used in this study can be found in the SEER Program Coding and Staging Manual 2007 with 2008 Revisions (Appendix C, Part 6, for Site Specific Coding Modules C64.9–C80.9, found on page C-939; http://seer.cancer.gov/tools/codingmanuals/historical.html).

Study Sample and Variables

A total of 20,705 adult patients (age ≥ 18 years) were identified with the diagnoses of glioblastoma (ICD-O-3 histology codes: 9440 Glioblastoma, Not Otherwise Specified; 9441 Giant Cell Glioblastoma; 9442 Gliosarcoma; and ICD-O-3 topology codes C71.0–C71.9) from 1998 to 2009. These codes were selected based on previous SEER-based glioblastoma studies.7,25 Glioblastoma patients with a second malignancy were excluded because our study was interested in the clinical course of glioblastoma patients in the absence of a second malignancy.

Demographic and clinical variables included age (by category: 18–44, 45–59, 60–74, or 75 years and above), race/ethnicity (White, Black, Asian/Pacific Islander, Hispanic, American Indian/Alaskan Native, or Other/Unknown), sex (male or female), year of diagnosis, tumor size (by category: < 5 cm, 5–7 cm, or > 7 cm), tumor location (based on topology site codes), radiotherapy status, and surgical treatment received.

With regard to the extent of tumor resection, all identified patients were coded in the SEER registry as having received no surgery (Code 00), local excision/biopsy (Code 20), partial resection (Code 40), GTR (Code 55), or unknown (all other codes). It should be noted that there is ambiguity with respect to the extent of resection achieved in an excisional biopsy versus a partial resection. For the practice pattern portion of the analyses, we analyzed the data based on the 5 categories. For the survival analysis, we collapsed the local excision/biopsy and partial resection categories into a single category termed subtotal resection (STR), because these 2 categories exhibited similar survival curves that were distinct from those of no surgery and GTR. Based on communications with the SEER registry, GTR was coded based on radiographic reports documenting the absence of enhancement on postoperative MRI. The primary endpoint was overall survival, defined as time in months from diagnosis until death (due to all causes).

Statistical Analyses

Surgical practice patterns were assessed within age category subsets. Comparisons of differences in demographic and clinical variables by GTR status were performed using a Pearson chi-square test or t-test as appropriate. Multivariate logistic regression modeling was used with GTR status as the dependent variable to obtain an odds ratio (OR) for receiving a GTR adjusted for patient demographics, tumor characteristics, year of diagnosis, and radiotherapy. Survival analyses by surgical status (no surgery, STR, or GTR) were evaluated using the Kaplan-Meier method and compared using a log-rank test. Hazard ratios (HRs) were calculated using a multivariate Cox proportional hazards model adjusting for the same covariates noted above using STR as the reference group. The level of statistical significance for all analyses was set at p < 0.05.

A subset analysis was also performed to investigate any impact from the introduction of radiation/temozolomide as the standard of care in 2005 on the association between GTR and survival. To accomplish this, subset analysis was performed by dividing patients into 2 time periods, 2002–2005 (the pre-temozolomide years) and 2006–2009 (the post-temozolomide years), and performing multivariate Cox regressions within these 2 subgroups.

Results

Patterns of Practice for Surgical Excision

All demographic data and clinical characteristics are displayed in Table 1. The distribution of surgical treatments for patients diagnosed with glioblastomas is represented in Fig. 1. These data were stratified by age category subsets in Fig. 2.

Fig. 1.
Fig. 1.

Distribution of surgical treatments provided to the overall cohort of 20,705 patients diagnosed with glioblastoma.

Fig. 2.
Fig. 2.

Practice patterns of surgical treatments by different age categories. The “Partial Resection” and “Local Excision/Biopsy” categories (asterisks) exhibited similar survival curves and were thus collapsed into the STR category for subsequent analyses.

TABLE 1:

Patient characteristics according to GTR*

VariableOverall CohortNo GTRGTRp Value
no. of patients (%)20,705 (100)14,548 (70.3)6157 (29.7)
median age in yrs (IQR)62 (52–71)62 (53–72)60 (51–70)
mean age ± SD in yrs61.3 ± 13.361.9 ± 13.359.7 ± 13.3<0.001
age category in yrs (%)<0.001
 18–442199 (10.6)1408 (9.7)791 (12.9)
 45–596822 (33.0)4628 (31.8)2194 (35.6)
 60–748053 (38.9)5763 (39.6)2290 (37.2)
 ≥753631 (17.5)2749 (18.9)882 (14.3)
race (%)0.008
 white16,783 (81.1)11,716 (80.5)5067 (82.3)
 black1113 (5.4)835 (5.7)278 (4.5)
 Asian/Pacific Islander771 (3.7)539 (3.7)232 (3.8)
 Hispanic1947 (9.4)1391 (9.6)556 (9.0)
 American Indian/Alaskan Native59 (0.3)44 (0.3)15 (0.2)
 other/unknown, non-Hispanic32 (0.2)23 (0.2)9 (0.2)
marital status (%)<0.001
 single2579 (12.8)1821 (12.9)758 (12.6)
 married13,523 (67.3)9348 (66.4)4175 (69.4)
 separated, divorced, widowed3999 (19.9)2914 (20.7)1085 (18.0)
sex (%)0.922
 male12,146 (58.7)8531 (58.6)3615 (58.7)
 female8559 (41.3)6017 (41.4)2542 (41.3)
tumor size in cm (%)<0.001
 <58858 (56.9)5880 (55.3)2978 (60.4)
 5–75339 (34.3)3744 (35.2)1595 (32.4)
 >71370 (8.8)1014 (9.5)356 (7.2)
tumor site (%)<0.001
 cerebrum745 (3.6)698 (4.8)47 (0.8)
 frontal lobe5506 (26.6)3751 (25.8)1755 (28.5)
 temporal lobe5046 (24.4)3177 (21.8)1869 (30.4)
 parietal lobe3485 (16.8)2435 (16.7)1050 (17.1)
 occipital lobe905 (4.4)558 (3.8)347 (5.6)
 ventricle, NOS85 (0.4)71 (0.5)14 (0.2)
 cerebellum, NOS138 (0.7)92 (0.6)46 (0.8)
 brain stem95 (0.5)87 (0.6)8 (0.1)
 overlapping lesion of brain3613 (17.5)2738 (18.8)875 (14.2)
 brain, NOS1087 (5.3)941 (6.5)146 (2.4)
year of diagnosis (%)<0.001
 1998795 (3.8)610 (4.2)185 (3.0)
 1999877 (4.2)649 (4.5)228 (3.7)
 20001735 (8.4)1309 (9.0)426 (6.9)
 20011721 (8.3)1288 (8.9)433 (7.0)
 20021781 (8.6)1321 (9.1)460 (7.5)
 20031870 (9.0)1182 (8.1)688 (11.2)
 20041969 (9.5)1219 (8.4)750 (12.2)
 20051960 (9.5)1207 (8.3)753 (12.2)
 20061878 (9.1)1163 (8.0)715 (11.6)
 20072032 (9.8)1352 (9.3)680 (11.0)
 20082058 (9.9)1611 (11.1)447 (7.3)
 20092029 (9.8)1637 (11.3)392 (6.4)
radiotherapy (%)<0.001
 no5082 (25.2)3981 (28.1)1101 (18.3)
 yes15,114 (74.8)10,205 (71.9)4909 (81.7)
overall mortality (%)<0.001
 alive2884 (13.9)1936 (13.3)948 (15.4)
 died17,821 (86.1)12,612 (86.7)5209 (84.6)

IQR = interquartile range; NOS = not otherwise specified.

The frequency that GTR was achieved decreased in a stepwise manner as a function of patient age. There was a significant decrease from 36.0% with GTR in patients aged 18–44 years relative to 24.3% with GTR in patients aged ≥ 75 years (p < 0.001; Fig. 2). Similarly, the prevalence of any surgery (GTR, partial resection, or excision/biopsy) decreased in a stepwise manner as a function of age (82.6% for ages 18–44 years vs 65.6% for ages ≥ 75 years; p < 0.001). In a multivariate analysis that compared patients with and without GTR, increasing age was associated with a reduced likelihood of receiving a GTR. As shown in Table 2, each older age category had statistically significant reduced odds of receiving a GTR. For instance, the likelihood of a GTR for the subset of glioblastoma patients aged ≥ 75 years was 0.5 (95% CI 0.43–0.58) relative to patients aged 18–44 years.

TABLE 2:

Adjusted odds ratios of receiving a GTR

VariableOR (95% CI)p Value
age category (yrs)
 18–441.00 (referent)
 45–590.71 (0.63–0.81)<0.001
 60–740.62 (0.55–0.71)<0.001
 ≥750.50 (0.43–0.58)<0.001
race
 white1.00 (referent)
 black0.83 (0.69–0.98)0.030
 Asian/Pacific Islander0.99 (0.83–1.20)0.969
 Hispanic0.88 (0.77–0.99)0.041
 American Indian/Alaskan Native0.68 (0.32–1.42)0.301
 other/unknown, non-Hispanic1.39 (0.49–4.00)0.538
marital status
 single1.00 (referent)
 married1.08 (0.96–1.21)0.214
 separated, divorced, widowed1.03 (0.90–1.18)0.696
sex
 male1.00 (referent)
 female1.05 (0.98–1.13)0.187
tumor size (cm)
 <51.00 (referent)
 5–70.80 (0.74–0.87)<0.001
 >70.66 (0.57–0.76)<0.001
tumor site
 cerebrum0.13 (0.09–0.18)<0.001
 frontal lobe1.00 (referent)
 temporal lobe1.29 (1.17–1.42)<0.001
 parietal lobe0.91 (0.82–1.02)0.109
 occipital lobe1.37 (1.15–1.63)<0.001
 ventricle, NOS0.38 (0.19–0.77)0.007
 cerebellum, NOS1.12 (0.72–1.75)0.601
 brain stem0.14 (0.06–0.36)<0.001
 overlapping lesion of brain0.71 (0.64–0.79)<0.001
 brain, NOS0.42 (0.33–0.53)<0.001
year of diagnosis
 19981.00 (referent)
 19991.32 (0.99–1.74)0.055
 20001.19 (0.93–1.53)0.176
 20011.22 (0.95–1.56)0.124
 20021.31 (1.02–1.67)0.033
 20032.07 (1.63–2.63)<0.001
 20042.29 (1.81–2.90)<0.001
 20052.17 (1.72–2.74)<0.001
 20062.23 (1.76–2.82)<0.001
 20071.77 (1.40–2.23)<0.001
 20080.93 (0.73–1.18)0.527
 20090.80 (0.63–1.01)0.064
radiotherapy
 no1.00 (referent)
 yes1.52 (1.39–1.67)<0.001

Association Between Surgical Treatment for Glioblastoma and Survival as a Function of Age

There was a significant improvement in overall survival with patients receiving either GTR or STR relative to patients receiving no surgery, across all ages (p < 0.001; Fig. 3), with overall median survival of 13 months for patients with GTR, 9 months for patients with STR, and 4 months for patients without surgical intervention.

Fig. 3.
Fig. 3.

Kaplan-Meier curves for each age category, comparing patients receiving GTR (short dashed line), STR (long dashed line), and no surgical treatment (solid line).

Pertaining to age, there were 2 general trends emerging from our analysis. First, there was a general trend of decreased survival with advanced age, independent of surgical intervention. For nonsurgical patients, the median survival times were 11, 7, 4, and 3 months for ages 18–44, 45–59, 60–74, and ≥ 75 years, respectively. For the STR patients, the median survival times were 18, 12, 7, and 4 months for ages 18–44, 45–59, 60–74, and ≥ 75 years, respectively. For the GTR patients, the median survival times were 21, 15, 10, and 6 months for ages 18–44, 45–59, 60–74, and ≥ 75 years, respectively. These findings are generally consistent with previous studies associating age with overall survival in patients with glioblastoma.27

The second general trend was that GTR and STR were both associated with improved overall survival relative to nonsurgical treatment in all age groups. Irrespective of age, the overall survival of patients with GTR was superior to that of patients with STR by approximately 2–3 months. For instance, relative to the STR patients, GTR patients between the ages of 18 and 44 years exhibited a 3-month improvement in median survival. Similarly, for patients with glioblastoma aged ≥ 75 years, those who underwent GTR showed a 2-month increase in median survival relative to the STR patients.

The association of GTR and STR with improved survival remained robust and statistically significant across all age groups (Fig. 3). Accordingly, multivariate analysis demonstrated improved survival in patients receiving GTR relative to STR, and STR relative to no surgery, irrespective of patient age (Table 3), after adjusting for race/ethnicity, sex, year of diagnosis, tumor size (< 5 cm, 5–7 cm, or > 7 cm), tumor location (based on topology site codes), and radiotherapy status.

TABLE 3:

Multivariate adjusted HRs with 95% CIs for patients with glioblastoma

Age CategoryHR (95% CI)p Value
18–44 yrs
 no surgery1.70 (1.39–2.08)<0.001
 STR(referent)
 GTR0.86 (0.75–0.98)0.024
45–59 yrs
 no surgery1.68 (1.52–1.84)<0.001
 STR(referent)
 GTR0.82 (0.77–0.89)<0.001
60–74 yrs
 no surgery1.66 (1.53–1.79)<0.001
 STR(referent)
 GTR0.79 (0.74–0.84)<0.001
≥75 yrs
 no surgery1.55 (1.40–1.72)<0.001
 STR(referent)
 GTR0.78 (0.70–0.86)<0.001

It is conceivable that the introduction of concurrent radiation/temozolomide therapy in 2005 may have impacted the clinical practice of GTR and the overall survival of patients who underwent GTR. To assess this possibility, we performed a subset analysis by separately analyzing patients treated from 2002 to 2005 and from 2006 to 2009 (Table 4). This analysis showed that the proportion of patients who received GTR only slightly declined during these two time periods. Furthermore, a multivariate Cox regression analysis revealed that the confidence interval of the adjusted HR associated with GTR significantly overlapped between the two time periods. These results suggest that the overall survival benefit associated with GTR was not significantly affected by the introduction of radiation/temozolomide therapy.

TABLE 4:

Multivariate adjusted HRs with 95% CIs for patients with glioblastoma before and after temozolomide

Age GroupBefore Temozolomide (2002–2005)After Temozolomide (2006–2009)
 n (%)HR (95% CI)p Valuen (%)HR (95% CI)p Value
<75 yrs
 no surgery1208 (16.2)1.60 (1.46–1.75)<0.0011231 (15.8)1.85 (1.69–2.04)<0.001
 STR2675 (35.9)(referent)3311 (42.5)(referent)
 GTR2253 (30.2)0.78 (0.73–0.84)<0.0011937 (24.9)0.80 (0.74–0.87)<0.001
≥75 yrs
 no surgery410 (5.5)1.67 (1.40–1.99)<0.001433 (5.6)1.44 (1.22–1.70)<0.001
 STR507 (6.8)(referent)580 (7.4)(referent)
 GTR398 (5.3)0.81 (0.69–0.95)0.01297 (3.8)0.72 (0.60–0.86)<0.001

Discussion

Despite the aggressive infiltrative nature of glioblastoma, there is mounting evidence that maximal surgical cytoreduction contributes to improvement in overall survival and quality of life, as well as clinical response to temozolomide and radiation therapy.10,20,21 This study provides data to further support this thesis using data available through the SEER database. As a cancer registry, SEER is considered the gold-standard database, in which independent verifications of collected variables were performed.22 Moreover, the available data suggest that the data captured in SEER is highly representative of the US population and includes patients treated at both academic and nonacademic institutions. Using this SEER database, we demonstrated that patients with glioblastoma who underwent GTR exhibited significantly prolonged overall survival relative to those without surgical intervention or with STR, after accounting for a host of variables including tumor location, size, and radiation therapy. It is important to note that the study design does not allow the inference that GTR independently contributed to the prolonged survival for patients with glioblastoma. The many factors involved in patient selection may also have contributed to the association with overall survival. Instead, our results indicate that glioblastoma patients who are selected for GTR and in whom GTR is achieved fare better clinically relative to those in whom GTR was not achieved or attempted. Interestingly, the 2- to 3-month survival difference between GTR and STR patients observed in the SEER database is largely consistent with previously published case series that explored this issue.5,11,17,18

Within the context of this interpretation, the data suggest that survival benefits associated with GTR persisted in all age groups. In patients aged < 75 years, patients who underwent GTR survived 3 months longer than those who underwent STR after correcting for pertinent variables available in SEER (p < 0.001; see Methods). The magnitude of this survival benefit in patients aged ≥ 75 years was reduced to 2 months (p < 0.001). Overall, the data support the general principle that the decision to operate in patients with glioblastoma should not be based on age alone. In appropriately selected patients, our data suggest that GTR may be of clinical benefit, despite advanced age. Such benefit must be judiciously weighed against the general trend of decreased survival in the elderly glioblastoma patient as well as the impact of surgery on the quality of life for the surviving patient.1 Studies directed toward understanding these factors are sorely needed.

A rather striking finding in this study is that between 15% and 30% of the glioblastoma patients received no surgeries of any form, suggesting that the patients were triaged to palliation or were treated based on imaging data. This practice is potentially problematic because it is not always possible to definitively distinguish glioblastoma from cerebral metastases, abscesses, inflammatory diseases, or other ring-enhancing intracranial lesions.3,4,15,23 In 1 study, nearly 20% of radiographic lesions believed to be glioblastoma by experienced neuroradiologists were found to be cerebral abscesses or cerebral metastases at the time of biopsy.23 To the extent that effective treatments exist for many diagnoses that present as ring-enhancing intracranial lesions, we propose that glioblastoma treatment be performed only after tissue diagnosis, particularly given the overall safety of needle-based stereotactic biopsies.24

There are a number of limitations inherent within this population-based study. First, the study constitutes a retrospective review of a population-based cancer registry and is subject to the various biases and flaws inherent within such a study design. Most notably, information relating to the clinical condition of the patient (such as performance status or medical comorbidities), the location of the tumor in relation to eloquent cerebrum, subsequent chemotherapeutic regimens, and quality of life measures were not available in the SEER database. Because these clinical variables are routinely used for surgical decision making, it is conceivable that they contributed to the poorer prognosis of patients who did not undergo GTR. Nevertheless, this inherent flaw does not nullify our conclusion that patients who were selected for and underwent GTR fare better than the other patients. Second, the surgery codes used in SEER have an element of ambiguity in terms of the definition of an excisional biopsy versus a partial resection. To the extent that the overall survival of patients in these 2 categories was similar to one another but distinct from those with no surgery or GTR, the patients in these categories were combined into 1 group in the survival analysis. Finally, information on how resection impacts quality of life was unavailable in the SEER data set.

An open question that remains from this study is whether we should be more aggressively pursuing resection in the elderly population with glioblastoma. We do not believe that all elderly patients with glioblastoma should be treated as a generic category of patients, to be aggressively operated on or to be left to palliation. Many authors have used the observation that advanced age is a poor prognostic factor to advance the agenda for palliation in elderly patients with glioblastoma.6,8,19 In this study we provide data that a subset of the elderly potentially benefits from GTR as a counterpoint to this fatalistic literature. We believe that thoughtful discussion with the patient or family members should be held in terms of the potential survival benefits of GTR in the context of the patient's expectations and potential impact of the surgery on quality of life. Ultimately, each surgical decision should be tailored to the individual patient and grounded in the existing literature.

Conclusions

Within the limitations inherent in any cancer registry–based study, we demonstrate that nearly one-third of patients with glioblastoma do not undergo surgery for procurement of definitive tissue diagnosis, and independent of age, patients who were selected to undergo GTR and underwent GTR exhibited longer overall survival relative to those in whom GTR was not achieved or attempted. These findings, when taken in the context of the larger literature base, suggest the critical need for tissue diagnosis prior to chemotherapy/radiation treatment as well as judicious patient selection in terms of resection.

Disclosure

Dr. Talamini serves as a consultant to Guidepoint Global and has direct stock ownership in Leading Biosciences.

Author contributions to the study and manuscript preparation include the following. Conception and design: Chen, Noorbakhsh, Marcus, McCutcheon, Gonda, Chang, Carter. Acquisition of data: Noorbakhsh. Analysis and interpretation of data: Chen, Noorbakhsh, Tang, Marcus, McCutcheon. Drafting the article: Chen, Noorbakhsh, Tang. 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: Chen. Statistical analysis: Noorbakhsh. Administrative/technical/material support: Chen. Study supervision: Chen, Talamini, Chang, Carter.

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    Sanai NPolley MYMcDermott MWParsa ATBerger MS: An extent of resection threshold for newly diagnosed glioblastomas. Clinical article. J Neurosurg 115:382011

  • 19

    Sijben AEMcIntyre JBRoldán GBEasaw JCYan EForsyth PA: Toxicity from chemoradiotherapy in older patients with glioblastoma multiforme. J Neurooncol 89:971032008

  • 20

    Stark AMvan de Bergh JHedderich JMehdorn HMNabavi A: Glioblastoma: clinical characteristics, prognostic factors and survival in 492 patients. Clin Neurol Neurosurg 114:8408452012

  • 21

    Stupp RMason WPvan den Bent MJWeller MFisher BTaphoorn MJ: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:9879962005

  • 22

    : (http://seer.cancer.gov/data/

  • 23

    Vuorinen VHinkka SFärkkilä MJääskeläinen J: Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir (Wien) 145:5102003

  • 24

    Waters JDGonda DDReddy HKasper EMWarnke PCChen CC: Diagnostic yield of stereotactic needle-biopsies of sub-cubic centimeter intracranial lesions. Surg Neurol Int 4:Suppl 3S176S1812013

  • 25

    Wrensch MRice TMiike RMcMillan ALamborn KRAldape K: Diagnostic, treatment, and demographic factors influencing survival in a population-based study of adult glioma patients in the San Francisco Bay Area. Neuro Oncol 8:12262006

  • 26

    Yamahara TNuma YOishi TKawaguchi TSeno TAsai A: Morphological and flow cytometric analysis of cell infiltration in glioblastoma: a comparison of autopsy brain and neuroimaging. Brain Tumor Pathol 27:81872010

  • 27

    Zhou CLiu LSong YLiu HLi TGong Q: Anterior and posterior vertebral column resection for severe and rigid idiopathic scoliosis. Eur Spine J 20:172817342011

Article Information

Mr. Noorbakhsh and Ms. Tang contributed equally to this work. Drs. Chang, Carter, and Chen share senior authorship of this work.

Address correspondence to: Clark Chen, M.D., Ph.D., Division of Neurosurgery, University of California, San Diego, 3855 Health Science Dr.,  0987, La Jolla, CA 92093-0987. email: clarkchen@ucsd.edu.

Please include this information when citing this paper: published online November 8, 2013; DOI: 10.3171/2013.9.JNS13877.

© AANS, except where prohibited by US copyright law."

Headings

Figures

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    Distribution of surgical treatments provided to the overall cohort of 20,705 patients diagnosed with glioblastoma.

  • View in gallery

    Practice patterns of surgical treatments by different age categories. The “Partial Resection” and “Local Excision/Biopsy” categories (asterisks) exhibited similar survival curves and were thus collapsed into the STR category for subsequent analyses.

  • View in gallery

    Kaplan-Meier curves for each age category, comparing patients receiving GTR (short dashed line), STR (long dashed line), and no surgical treatment (solid line).

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Sanai NPolley MYMcDermott MWParsa ATBerger MS: An extent of resection threshold for newly diagnosed glioblastomas. Clinical article. J Neurosurg 115:382011

19

Sijben AEMcIntyre JBRoldán GBEasaw JCYan EForsyth PA: Toxicity from chemoradiotherapy in older patients with glioblastoma multiforme. J Neurooncol 89:971032008

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Stark AMvan de Bergh JHedderich JMehdorn HMNabavi A: Glioblastoma: clinical characteristics, prognostic factors and survival in 492 patients. Clin Neurol Neurosurg 114:8408452012

21

Stupp RMason WPvan den Bent MJWeller MFisher BTaphoorn MJ: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:9879962005

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: (http://seer.cancer.gov/data/

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Vuorinen VHinkka SFärkkilä MJääskeläinen J: Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir (Wien) 145:5102003

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Waters JDGonda DDReddy HKasper EMWarnke PCChen CC: Diagnostic yield of stereotactic needle-biopsies of sub-cubic centimeter intracranial lesions. Surg Neurol Int 4:Suppl 3S176S1812013

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Wrensch MRice TMiike RMcMillan ALamborn KRAldape K: Diagnostic, treatment, and demographic factors influencing survival in a population-based study of adult glioma patients in the San Francisco Bay Area. Neuro Oncol 8:12262006

26

Yamahara TNuma YOishi TKawaguchi TSeno TAsai A: Morphological and flow cytometric analysis of cell infiltration in glioblastoma: a comparison of autopsy brain and neuroimaging. Brain Tumor Pathol 27:81872010

27

Zhou CLiu LSong YLiu HLi TGong Q: Anterior and posterior vertebral column resection for severe and rigid idiopathic scoliosis. Eur Spine J 20:172817342011

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