CC BY-NC-ND 4.0 · Indian Journal of Neurosurgery 2022; 11(02): 104-117
DOI: 10.1055/s-0042-1742333
Review Article

Utility of Administrative Databases and Big Data on Understanding Glioma Treatment—A Systematic Review

Monica-Rae Owens
1   Department of Neurosurgery, University of Utah, Utah, United States
,
Sarah Nguyen
1   Department of Neurosurgery, University of Utah, Utah, United States
,
2   University of Utah Health Care, University of Utah Health Hospitals and Clinics, Utah, United States
› Author Affiliations
Funding None.
 

Abstract

Background Gliomas are a heterogeneous group of tumors where large multicenter clinical and genetic studies have become increasingly popular in their understanding. We reviewed and analyzed the findings from large databases in gliomas, seeking to understand clinically relevant information.

Methods A systematic review was performed for gliomas studied using large administrative databases up to January 2020 (e.g., National Inpatient Sample [NIS], National Surgical Quality Improvement Program [NSQIP], and Surveillance, Epidemiology, and End Results Program [SEER], National Cancer Database [NCDB], and others).

Results Out of 390 screened studies, 122 were analyzed. Studies included a wide range of gliomas including low- and high-grade gliomas. The SEER database (n = 83) was the most used database followed by NCDB (n = 28). The most common pathologies included glioblastoma multiforme (GBM) (n = 67), with the next category including mixes of grades II to IV glioma (n = 31). Common study themes involved evaluation of descriptive epidemiological trends, prognostic factors, comparison of different pathologies, and evaluation of outcome trends over time. Persistent health care disparities in patient outcomes were frequently seen depending on race, marital status, insurance status, hospital volume, and location, which did not change over time. Most studies showed improvement in survival because of advances in surgical and adjuvant treatments.

Conclusions This study helps summarize the use of clinical administrative databases in gliomas research, informing on socioeconomic issues, surgical outcomes, and adjuvant treatments over time on a national level. Large databases allow for some study questions that would not be possible with single institution data; however, limitations remain in data curation, analysis, and reporting methods.


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Introduction

Gliomas encompass the second most common type of brain tumor in the United States, while glioblastoma multiforme (GBM) accounts for the most common malignant primary brain tumor.[1] Multiple advances in treatment, including earlier imaging and detection, safer surgical resection, and adjuvant radiochemotherapy (RCT) have improved disease treatment.[2] Clinical variables, such as age and surgical resection, in addition to genetic factors have been helpful in stratifying patient risk. However, there remains heterogeneity in the outcomes of patients and treatment response.

The rise in the use of administrative databases and big data has been notable in neurosurgery, but their impact on glioma understanding remains limited.[3] These studies often show multiple associative findings due to their significant sample sizes without distinction between statistical and clinical significance. Moreover, the clinical impact of these studies remains unclear. The purpose of this review was to accumulate and compare the lessons learned from big data regarding gliomas and identify future challenges for exploration.


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Methods

We aimed to evaluate the impact of multicenter, publicly available administrative databases on clinically relevant information in the treatment of gliomas. A literature search of PubMed was performed using the following search terms: (National Surgical Quality Improvement Program OR NSQIP OR National Inpatient Sample OR NIS OR HCUP-NIS OR Kid's Inpatient Database OR HCUP-KID OR Surveillance, Epidemiology, and End Results Program OR SEER OR Pediatric Health Information Systems OR PHIS OR MarketScan OR Administrative database OR SEER OR SEER-Medicare OR CBTRUS OR NCDB OR NRD OR SID OR SASD OR CMS OR Vizient OR Premier OR PearlDiver OR Optum) AND (glioma OR glioblastoma OR astrocytoma OR oligodendroglioma OR anaplastic astrocytoma OR anaplastic oligodendroglioma [AO]). References from manuscripts were also reviewed to identify relevant studies.

Studies up to January 2020 and English-only manuscripts were included. Studies were reviewed independently by two reviewers (M.O., M.K.) to exclude case reports, reviews, and laboratory studies. The main study findings including prognostic factors, sample number, database type, World Health Organization (WHO) tumor status, tumor types, surgical complications, and surgical outcomes were noted. Papers were narrowed to those discussing low-grade glioma (LGG), including grade II gliomas, astrocytoma and oligodendroglioma, as well as high-grade gliomas (HGG), including anaplastic astrocytoma (AA), anaplastic oligodendroglioma (AO), and GBM. Studies used a combination of histological and molecular classification, depending on the year of study. Several studies incorporated other glioma types that were excluded ([Supplemental discussion], [Fig. S1], [Table S1]). The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were used to draft this manuscript. Descriptive statistics are demonstrated where relevant.


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Results

A total of 390 studies were screened and narrowed down to 122 studies ([Fig. 1]). Studies included AA only (n = 2), AA with other pathologies (n = 3), AO only (n = 2), GBM (n = 67), grades II to IV glioma (n = 31), grade II glioma (n = 3), HGG (n = 7), mix of high-grade tumors (n = 1), and oligodendroglioma (n = 6) ([Table 1]). The most common databases included the NCDB (n = 28) and SEER databases (n = 83). A further breakdown of all studies into LGG and HGG was performed ([Figs. S1–S3]).

Zoom Image
Fig. 1 The Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) flow diagram of selected studies.
Table 1

Studies evaluating administrative studies/big data in LGG and HGG

Database used

Patient pathology

Sample size

Study year

Study findings

Reference

NCDB

AA

4,807

2004–2013

Prognostic factors: RCT, age, private insurance, higher income

Shin[40]

SEER

AA

3,202

1973–2006

5-year OS 23.6%; prognostic factor: age (only 3 years postdiagnosis); 5 year survival unchanged over time

Smoll[43]

SEER

AA, AO

1,939

1973–2013

Prognostic factors: age, tumor site, marital status, EOR, histology, RT, surgery

Zhao[44]

SEER

AA, AO

390

1990–2008

Evaluated patients > 70 years of age; median OS 11 month; prognostic factors: EOR, RT, gender, marital status

Mukherjee[38]

SEER

AA, GBM

24717

1999–2010

Median OS (AA versus GBM with GTR) 64 versus 13 months; prognostic factors: EOR

Padwal[39]

NCDB

AO

1,643

2004–2013

Prognostic factors: race, age, RCT

Shin[42]

NCDB

AO

1,692

2004–2013

5-year OS 59.8%; prognostic factors: RCT, single-agent chemotherapy

Shin[41]

NCDB

GBM

100,672

1998–2011

Median OS 7.5 months; prognostic factor: age, tumor histology, race, gender, education, insurance status, EOR, RCT, tumor location

Dressler[56]

NCDB

GBM

60,672

2004–2013

Median OS 8.1 months; prognostic factors: TMZ, high volume facility treatment; 2-month survival benefit in high-volume centers

Aulakh[55]

NCDB

GBM

738

2010–2012

Median OS (RCT) 15.6 months, 2-year OS 25.9%; limited benefit of RT in patients with MGMT methylation

Lee[60]

NCDB

GBM

448

2010–2013

Median OS (RCT) 8.7 months; prognostic factors: age, EOR, RCT;

Malakhov[59]

NCDB

GBM

4,598

1998–2011

Prognostic factor: long-course radiotherapy compared with short-course radiotherapy

Mak[58]

NCDB

GBM

114,979

1998–2012

Prognostic factor: RCT compared with radiation alone

Glaser[57]

NCDB

GBM

114,979

1998–2012

Prognostic factors: disparities in standard of care secondary to race, insurance status and institution of treatment

Rhome[65]

NCDB

GBM

5,252

2004–2012

Prognostic factor: single-agent chemotherapy with radiotherapy in elderly patients

Huang[111]

NCDB

GBM

89,839

2004–2013

Prognostic factor: patients treated in academic/research programs, high-volume centers

Hauser[64]

NCDB

GBM

27,865

2004–2013

Prognostic factor: GTR; no survival benefit of STR over biopsy

Trifiletti[67]

NCDB

GBM

1,223

2004–2014

Dose escalation not associated with survival; prognostic factors: age, comorbidity score, hospital volume (noncommunity centers), education level, income, insurance status, race, gender

Wegner[68]

NCDB

GBM

45,942

2004–2015

Prognostic factor: younger age, female gender, black ethnicity, higher KPS, and GTR over STR; delay > 8 weeks for radiochemotherapy detrimental after GTR; delay < 4 weeks for radiochemotherapy detrimental after STR

Buszek[62]

NCDB

GBM

45,268

2004–2016

Median OS was 12.8 months vs 8.3 months for patients with unifocal GBM or multifocal GBM; prognostic factor: radiochemotherapy; radiochemotherapy beneficial even if multifocal

Haque[63]

NCDB

GBM

13,489

2005–2012

Prognostic factors: delay in radiochemotherapy treatment

Yusuf[76]

NCDB

GBM

1,479

2006–2011

Prognostic factor: radiochemotherapy compared with radiation alone

Kole[66]

NCDB

GBM

12,725

2010–2012

Median OS (MGMTme versus MGMT-) 20 versus 15 months; prognostic factors: RCT in MGMTme tumors

Lee[61]

NCDB; RTOG

GBM

40,396

1974–2002

Survival for patients in the RTOG database exceeded survival in patients in the NCDB group likely because patients in the RTOG database come from clinical trials which have specific enrollment criteria; prognostic factor: age

Siker[73]

SEER

GBM

9,103

1973–2006

Prognostic factor: age, marital status, resection

Walker[75]

SEER

GBM

21,783

1973–2007

Prognostic factors: EOR, RT

Zinn[77]

SEER

GBM

34,664

1973–2008

Prognostic factor: race (Asian/Pacific Islander), surgical resection, age, RT; improved survival over time

Thumma[74]

SEER

GBM

51,518

1973–2014

Prognostic factor: no prior history of cancer

Al-Husseini[70]

SEER

GBM

60,456

1973–2015

Prognostic factors: age, tumor size, tumor location, GTR, radiation, chemotherapy, brachytherapy

Bartek[72]

SEER

GBM

25,117

1985–2014

Prognostic factors: Hispanic Latino (GBM and GBM-GC), age, gender

Bin Abdulrahman [120]

SEER

GBM

10,987

1988–2001

Prognostic factors: marital status

Chang[78]

SEER

GBM

1,530

1991–1999

Prognostic factor: race

Barnholtz-Sloan [71]

SEER

GBM

1,375

1991–2002

Median time post-resection to initiation of RT was 15 days; no impact of wait time on OS

Lai[121]

SEER

GBM

1,273

1991–2007

No difference in patient outcomes between low- and high-readmission rate hospitals

Nuno[117]

SEER

GBM

19,674

1993–2007

Improved survival over time

Darefsky[80]

SEER

GBM

4,137

1994–2002

Prognostic factors: age, marital status, and comorbidities

Iwamoto[81]

SEER

GBM

1,652

1995–2009

Median OS of 7.4, 5.9 and 5.6 months for TMZ/RT, RT alone (2005–2009) and RT alone (1995–1999), respectively; benefit of TMZ addition to RT in later years

Arvold[98]

SEER

GBM

3,963

1997–2010

GTR supported as initial treatment and for recurrence

Chen[122]

SEER

GBM

3,784

1997–2010

Patients with postop infections showed no significant difference in survival

Chen[123]

SEER

GBM

22,777

1998–2007

Factors associated with omission of RT included older age, lower annual income, African–American race, Hispanic race, Asian–American race, unmarried status, and STR/Bx; use of radiation associated with improved OS

Aizer[69]

SEER

GBM

10,022

1998–2008

Patients surviving past 2 years have favorable conditional probability of survival

Johnson[83]

SEER

GBM

20,705

1998–2009

Benefit of 2–3 months survival after GTR in all age groups; lower rate of GTR in older patients

Noorbakhsh[86]

SEER

GBM

342

1998–2009

Median OS 12 months; prognostic factors: EOR

Adams[82]

SEER

GBM

6,039

1999–2010

Prognostic factors: gender (female), married patients, ethnicity

Shah[89]

SEER

GBM

13,932

2000–2008

Benefit of TMZ to survival over time

Johnson[84]

SEER

GBM

6,586

2000–2008

Prognostic factor: gender (female)

Tian[90]

SEER

GBM

20,879

2000–2009

Benefit of TMZ and BZM to survival over time

Wachtel[91]

SEER

GBM

302

2000–2010

Prognostic factors: supratentorial location, GTR, and later year of diagnosis

Lam[85]

SEER

GBM

14,675

2000–2010

Median OS 11 months; prognostic factors: age, gender, marriage status, race (non-Hispanics), region (northeast), nonlateralizing, small (< 3 cm), adjuvant radiation

Pan[87]

SEER

GBM

26,481

2000–2010

Prognostic factors: age, gender, race (non-White), socioeconomic status

Porter[88]

SEER

GBM

28,933

2000–2013

Improved survival with TMZ with radiation and adjuvant TMZ and then BEV after FDA approval

Zhu[92]

SEER

GBM

20,550

2000–2013

Prognostic factors: tumor size (< 5 cm), EOR, RCT

Shu[96]

SEER

GBM

6,919

2001–2006

Benefit of TMZ to survival over time

Koshy[94]

SEER

GBM

11,189

2001–2006

Cure fraction of 12% for young adults at 10 years

Smoll[97]

SEER

GBM

21,184

2001–2011

Prognostic factors: race (Latinos); possibly greater incidence of GBM-GC in Latinos

Shabihkhani[95]

SEER

GBM

5,991

2004–2008

Prognostic factors: age, marital status, median income; factors led to increased GTR and RT

Aneja[93]

SEER

GBM

24,262

2004–2013

Regional differences in survival and incidence in the US; prognostic factors: age, marital status, race, tumor laterality, WHO grade, disease extent, tumor size, tumor extension, RCT

Xu[119]

SEER

GBM

24,348

2004–2013

Median survival 15, 15 and 5 months for pediatric, adult, and elderly, respectively

Li[116]

SEER

GBM

30,767

2004–2015

Prognostic factors: marriage, age, race, middle-income counties

Xie[52]

SEER

GBM

5,607

2006–2010

Median OS of 8, 7, and 9 months in 2006, 2008, and 2010, respectively; improved survival with BZM

Johnson[105]

SEER

GBM

2,603

2006–2011

Benefit of BZM to survival

Davies[102]

SEER

GBM

13,665

2007–2012

Prognostic factors: insurance status, RT, marital status; improved OS over time

Rong[110]

SEER

GBM

3,473

2010–2014

Prognostic factors: race (Asian–Pacific Islander)

Bohn[101]

SEER; Broad Institute Genotype Tissue Expression project; UCSF 10K Immunomes-database

GBM

1973–2016

Increased expression of immunoregulatory molecules in the elderly

Ladomersky[106]

SEER; Medicare database

GBM

5,029

1999–2007

Median survival was 4.9 months

Arvold[99]

ACS-NSQIP

GBM

1,016

2012–2016

Patients' aged 65–89 years included; 3.4% 30-day death rate; 5.7% severe complication rate; 33% change in living disposition rate

Rahmani[109]

California Office of Statewide Health Planning & Development inpatient-discharge administrative database

GBM

18,506

1995–2010

13.2% 30-day readmission rate; each readmission represented an additional $20,296 in median hospital charges on top of the $72,029 in charges for the index neurosurgical admission

Marcus[107]

MarketScan

GBM

14,037

2007–2016

Functional mapping associated with decreased complications, reoperations, emergency department visits, and shorter lengths of stay; no difference in charges with functional versus no mapping

Pendharkar[108]

SEER

GBM

48748

2000–2013

Multiple primary tumors associated with female gender, White race, smaller tumors

Nguyen[112]

SEER

GBM

12,437

2002–2011

Hospice enrollment associated with older age, female gender, higher education, White race, lower median income

Forst[104]

Los Angeles County Cancer Surveillance Program, CCR, and SEER

GBM

38,567

1996–2006

Increased incidence of frontal, temporal and cerebellar GBM over time compared with other locations

Zada[113]

SEER

GBM

21,493

1973–1997

Prognostic factor: race (white)

Barnholtz-Sloan [100]

SEER

GBM

1,181

1973–2015

Prognostic factors (for secondary malignancy): age, race, differentiated grade of cancer tissue, marital status, WHO grade, latency

Wang[118]

SEER

GBM

37,581

2001–2011

Median OS 14 versus 11 months of metropolitan versus non-metropolitan; prognostic factors: urban area

Delavar[103]

FCDS

Glioma

14,092

1981–2013

Diagnostic factor: race (Caucasian more likely), age (older), gender (male), smoking status, insurance status

Persaud-Sharma [15]

NCDB

Glioma

49,405

2004–2013

Proton beam therapy better median and 5-year OS compared with other radiation therapy

Jhaveri[17]

NCDB

Glioma

5,036

2010–2014

Prognostic factors: female gender (GBMs)

Gittleman[20]

NIS

Glioma

21,384

2005–2011

Identified perioperative complication risk: age, coagulopathy, CAD, CHF, smoking

Missios[37]

SEER

Glioma

5,956

1973–2010

Prognostic factor: race (White)

Samaan[21]

SEER

Glioma

49,124

1973–2014

Increased incidence of GBM versus non-GBM over time

Li[18]

SEER

Glioma

389,415

1973–2014

Increased risk of gliomas in younger women after breast cancer treatment

Mezencev[14]

SEER

Glioma

58,700

1975–2016

Prognostic factor: age

Zhou[124]

SEER

Glioma

22,427

1977–2000

Prognostic factors: age, gender, year of diagnosis; diagnostic factors: age, gender, later year of diagnosis

Hess[16]

SEER

Glioma

24,340

1992–2007

Diagnostic factors: age, race (non-Hispanic White)

Dubrow[13]

SEER

Glioma

1,067

1994–2002

Median OS 9, 4, 57 and 9 months for low-grade glioma, AA, OG, and AO, respectively; prognostic factors: age, WHO grade

Iwamoto[25]

SEER

Glioma

9,385

1999–2010

Improved survival for grade II and III gliomas over time

Dong[24]

SEER

Glioma

24,230

2000–2006

Greater incidence gliomas in counties with higher socioeconomic status

Plascak[19]

SEER

Glioma

617

2000–2014

Prognostic factor: marital status

Long[26]

SEER

Glioma

244,808

2000–2014

Prognostic factor: race; non-Hispanic whites showed lower survival

Ostrom[1]

SEER

Glioma

43,324

2000–2016

Prognostic factor: marital status

Xie[28]

SEER

Glioma

50,170

2003–2012

Prognostic factor: socioeconomic status

Deb[23]

SEER

Glioma

10,591

2005–2013

Prognostic factor: age, race (White), noncerebral tumor sites

Sun[51]

SEER; Medicare database

Glioma

1,958

1991–1999

Prognostic factors: age, EOR, RT

Barnholtz-Sloan [50]

NCDB

Glioma

1,029

2004–2012

No difference between single- and multiagent chemotherapy

Haque[125]

NCDB

Glioma

2,253

2004–2013

Prognostic factor: RCT

Wu[27]

NCDB

Glioma

5,539

2004–2014

Prognostic factor: high-volume facility

Zhu[29]

NCDB

Glioma

1,952

2010–2012

Prognostic factor: histology, RT

Youseff[36]

NCDB

Glioma

1,032

2010–2013

Prognostic factor: WHO grade, tumor size

Jairam[32]

SEER

Glioma

2,009

1973–2001

Prognostic factor: gender (female), age, race (White), WHO grade, later year of diagnosis; improved survival over time

Claus[30]

SEER

Glioma

2,825

1973–2011

Indicated lack of OS improvement for LGG; suggested importance of molecular markers

Claus[31]

SEER

Glioma

42,622

2000–2013

Evaluated primary and secondary GBM

Nguyen[34]

SEER

Glioma

5,037

2001–2006

Patients diagnosed with LGG 17X more likely to die than general population; older patients with LGG 31X more likely to die than young adults in first year

Smoll[35]

SEER

Glioma

3,732

2004–2013

Prognostic factors: age, marital status, tumor site, histological type, tumor size, surgery, and sex

Zhao[22]

SEER

Glioma

561

2006–2012

Prognostic factor: EOR

Diaz-Aguilar[126]

SEER, TCGA

Glioma

1,278

1999–2016

Overlap of risk genes in Alzheimer disease and gliomas (TREM2, SPI1, CD33, and INPP5D)

Lehrer[33]

NCDB

Grade II glioma

1,054

2004–2013

RCT not associated with higher survival in comparison to chemotherapy alone

Jhaveri[17]

SEER

Grade II glioma

1,980

1999–2010

Prognostic factors: frontal lobe location, EOR, age

Alattar[5]

SEER

Grade II glioma

4,113

1999–2010

Prognostic factors: EOR

Schupper[6]

CSP

HGG

2,743

1990–2000

5-year OS 6%; median OS 6.6 months; improved survival over time; prognostic factors: age, WHO grade, tumor site, primary treatment, year of treatment, academic hospital

Tsao-Wei[45]

PMSI

HGG

1,659

2010–2018

Median OS was 1.4 years; prognostic factors: carmustine wafer, age, gender, recurrent disease

Champeaux[46]

MarketScan and Medicare supplemental health claims database

HGG

2,157

2009–2015

No significant association between use of BEV and occurrence of thromboembolic events

Lee[53]

SEER

HGG

154

1973–2013

Median OS 10 months; prognostic factors: non-brainstem location, RT

Maxwell[47]

SEER

HGG

353

1973–2015

Prognostic factors: age; no tumor-related characteristics were associated with survival

Yang[49]

SEER

HGG

14,461

1998–2007

Prognostic factor: WHO grade, RT

Rusthoven[48]

SEER

HGG

3,706

2000–2013

Median OS 14.3 month; 5-year OS 6.2%; prognostic factor: age, location (unilateral), EOR, RT

Xia[127]

ACS-NSQIP

Mix of malignant brain tumor

4,407

2007–2012

Perioperative steroid use associated with shorter hospitalization and increased readmission; no adverse events with steroid use

Alan[54]

CBTRUS

Oligodendroglioma

2000–2013

OD and AOD showed decreased incidence over time

Achey[7]

SEER

Oligodendroglioma

762

1973–2012

Prognostic factors: age, gender, race; improved survival over time

Furst[12]

SEER

Oligodendroglioma

7,001

1973–2013

Prognostic factor age

Lau[11]

SEER

Oligodendroglioma

3,406

1999–2010

Prognostic factors: EOR; limited benefit for GTR in OG compared to AA or GBM

Alattar[8]

SEER

Oligodendroglioma

3,880

1999–2012

Improved survival over time

Brandel[9]

SEER

Oligodendroglioma

3,135

2004–2013

Prognostic factors: EOR

Kinslow[10]

Abbreviations: AA anaplastic astrocytoma; AO, anaplastic oligodendroglioma; ACS-NSQIP, American College of Surgeons National Surgical Quality Improvement Program database; BZM, bevacizumab; CA, California; CBTRUS, Central Brain Tumor Registry of the United States; CAD, coronary artery disease; CCR, California Cancer Registry; CHF, congestive heart failure; CSP, Cancer Surveillance Program; EOR, extent-of-resection; FCDS, Florida Cancer Data Registry; GBM, glioblastoma multiforme; GTR, gross total resection; HGG, high-grade glioma; LGG, low-grade glioma; NCDB, National Cancer Database; NIS, National Inpatient Sample; OS, overall survival; PMSI, French medico-administrative national database; RT, radiotherapy; RTOG, Radiation Therapy Oncology Group; SEE, Southern and Eastern Europe Tumor Registry; SEER, Surveillance, Epidemiology and End Results Database; TCGA, The Cancer Genome Atlas; TMZ, temozolomide; UCSF, University of California - San Francisco.


Low Grade Glioma

LGGs were evaluated as an aggregate group in three studies. One study on grade II gliomas showed that RCT did not improve survival compared with chemotherapy alone,[4] and two others showed that greater extent of resection (EOR) improved prognosis.[5] [6] Unfortunately, these studies were limited by aggregating all LGGs, which often behave distinctly.

Six studies specifically evaluated oligodendroglioma,[7] [8] [9] [10] [11] [12] with two of these studies showing improved survival over the preceding 10 years (e.g., 2004–2013) mainly as a function of improved surgery and RCT.[9] [12] Achey et al evaluated the age-adjusted incidence rate from the Central Brain Tumor Registry of the United States from 2000 to 2013.[7] A decreased incidence of oligodendroglioma and AO was seen, although this was possibly because of recent changes in molecular classification. Prognostic factors impacting survival for oligodendrogliomas in other studies included age, sex, race, and EOR.[8] [10] [11] [12] Alattar et al evaluated 3,406 patients with oligodendroglioma from 1999 to 2010 using the SEER database and demonstrated an improvement in OS after gross-total resection compared with AA or GBM.[8] This finding was confirmed by Kinslow et al in their evaluation of 3135 cases from the SEER database data from 2004 to 2013; they also showed that EOR impacted survival in both oligodendroglioma and AO.[10]

Multiple studies have evaluated glioma by including either LGG as a broad category or comparing LGG with HGG.[1] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] [37] Several studies evaluated the epidemiology of gliomas and demonstrated increased likelihood in Caucasians, older, or male patients, patients with prior smoking history, women with prior breast cancer treatment, and insured patients.[13] [14] [15] [16] [19] Plascak et al evaluated 24,230 glioma patients using the SEER database between 2000 and 2006; they showed a greater incidence of gliomas in countries with higher socioeconomic status, which suggested unequal distribution of diagnostic resources.[19] Another study using the SEER database noted a decreasing incidence of gliomas and suggested there was a shift to increased diagnosis of GBM by pathological criteria over time.[18] The vast majority of studies involving glioma have looked at prognostic factors. These studies have suggested that White race, younger age, more recent diagnosis, lower WHO grade or histology, marital status, better socioeconomic status, EOR, radiotherapy, radiochemotherapy, treatment at high-volume facilities, and tumor size positively impact patient prognosis.[1] [4] [16] [17] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] Missios et al evaluated 21,384 cases of glioma between 2005 and 2011 using the National Inpatient Sample (NIS) database and showed that perioperative complications were increased by greater age, coagulopathy, coronary artery disease, congestive heart failure, and smoking history.[37]

Although these studies have had an impact by identifying consistent risk and prognostic factors, they are limited by aggregating glioma types, mostly as a limitation of lacking molecular data in nearly all multicenter databases. Moreover, both epidemiology and prognostic factor studies suggest geographic differences in outcomes because of medical resources and facilities but do little to address these inequalities or report in sufficient detail to confer actionable insight. Despite improve standardization of glioma treatment with clinical guidelines, treatment variation likely still occurs, which is impacted by patient socioeconomics and remains poorly understood.


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High-Grade Glioma

Several studies have evaluated and compared outcomes for AA and AO. Prognostic factors for AA included age, RCT, private insurance, higher income, tumor site, marital status, EOR, histology, and treatment with RT.[38] [39] [40] [41] [42] [43] [44] Smoll et al specifically looked at 3,202 patients with AA between 1973 and 2006 in the SEER database, showing worsened mortality compared with matched controls.[43] A 5- and 10-year overall survival (OS) of 23.6% and 15.1% was identified, respectively. Age significantly impacted prognosis, however, improvement in survival was not seen over the study time period. In contrast, Shin et al evaluated 1,692 patients with AO via the NCDB database between 2004 and 2013.[41] An overall 5-year of 59.8% was seen and significant benefits in survival were seen from RCT or single-agent chemotherapy. Patients were more likely to receive adjuvant RCT if treated in later time epochs, were male, had private insurance, or had ≥ $63,000 median income. While the survival benefit from AOs compared with AAs were not unexpected, differences in treatment with RCT often depended on socioeconomic factors.

HGG also represent a diverse group of studied pathologies commonly aggregated in database studies. Tsao-Wei et al showed improved survival in HGG in Los Angeles County over time between 1990 and 2000.[45] In addition, this study showed relative improvement in survival of GBM compared with grade III gliomas over the same time period despite an OS of 6% at 5-years for the study group. Several other studies regarding HGG have studied several prognostic factors including age, gender, recurrent disease, tumor location, WHO grade, primary treatment, RT, and EOR.[28] [45] [46] [47] [48] [49] [50] [51] [52] Another study by Lee et al showed no association between bevacizumab use and thromboembolic events.[53] One study evaluated 4,407 patients via the NSQIP database who underwent resection of a malignant brain tumor between 2007 and 2012. This study included metastatic tumors (n = 1611) and malignant gliomas (n = 2796).[54] Steroid use was found to decrease hospital length of stay but increase risk of readmission in an unmatched case-control analysis; however, these findings were not confirmed on a propensity matched analysis.


#

Glioblastoma

Studies on GBM encompass the largest topic of database analysis in gliomas. A total of 68 studies were published between 2002 and 2020 ([Table 1]). Studies evaluating prognostic factors showed that age, tumor histology, molecular markers, race, sex, education, marital status, treatment in high-volume and/or urban centers, insurance status, EOR, RCT, and tumor location impacted outcomes.[52] [55] [56] [57] [58] [59] [60] [61] [62] [63] [64] [65] [66] [67] [68] [69] [70] [71] [72] [73] [74] [75] [76] [77] [78] [79] [80] [81] [82] [83] [84] [85] [86] [87] [88] [89] [90] [91] [92] [93] [94] [95] [96] [97] [98] [99] [100] [101] [102] [103] [104] [105] [106] [107] [108] [109] [110] [111] Although a few studies simply described general demographic changes of GBMs,[112] [113] most studied specific questions.[52] [55] [56] [57] [58] [59] [60] [61] [62] [63] [64] [65] [66] [67] [68] [69] [70] [71] [72] [73] [74] [75] [76] [77] [78] [79] [80] [81] [82] [83] [84] [85] [86] [87] [88] [89] [90] [91] [93] [94] [95] [96] [97] [98] [99] [100] [101] [102] [103] [104] [105] [106] [107] [108] [109] [110] [114] [115] [116] Most studies also demonstrated improved survival over time, which was likely associated with an increased use of RCT, temozolomide, and adjuvant treatments, such as bevacizumab, but could not deliver more granular specifics.

The impact of facility type and location on outcome after GBM treatment has been evaluated by several studies. Aulakh et al[55] evaluated 60,672 patients in the NCDB from 2004 to 2013, demonstrating that treatment in a high-volume facility, along with temozolomide treatment, improved survival. In fact, treatment in a high-volume center conferred a 2-month OS benefit. Another study by Hauser et al[64] evaluating 89,839 patients in the NCDB from 2004 to 2013 suggested better outcomes for patients treated in academic centers, and a study by Delavar et al.[103] evaluating 37,581 patients between 2001 and 2011 showed a 3-month improvement in OS for patients living in metropolitan areas compared with nonmetropolitan areas. Other studies support the impact of institution type on treatment accessibility and outcome.[65] [68] Nuno et al[117] evaluated 1,273 patients in the SEER database between 1991 and 2007 to compare hospitals with low and high rates of readmission after GBM treatment. No differences were seen in patient outcomes such as complications, nonroutine discharge, length of stay, EOR, or OS. Thus, facility characteristics, such as patient volume and facility location, seemed to impact outcome.

Several studies have evaluated the impact on outcome of socioeconomic factors, namely, marital status, race/ethnicity, and insurance status. Several studies have shown the positive impact of marriage on outcome after GBM.[52] [56] [68] [69] [75] [78] [87] [89] [104] [110] [118] Several studies have shown the impact of race on outcome, primarily demonstrating that non-White races fared worse.[52] [69] [71] [74] [87] [89] [95] [100] [101] [104] [118] [119] Aizer et al[69] studied 22,777 patients between 1998 and 2007 via the SEER database and showed that factors associated with omission of RT included African-American and Asian-American races, unmarried status, and lower annual income. Other factors associated with reduced likelihood of RT included older age and subtotal resection/biopsy. Forst et al[104] evaluated 12,437 patients via the SEER database between 2002 and 2011, showing that hospice enrollment was associated with higher education, White race, and lower median income among other factors. Studying 13,665 patients in the SEER database between 2007 and 2012, Rong et al[110] showed that insurance status highly affected prognosis. Patients who were uninsured or had Medicaid coverage were likely to be younger and unmarried and to present with larger tumors. In addition, incremental survival benefits from 2007 through 2011 were seen in insured patients but not uninsured patients.


#
#

Discussion

An evaluation of the use of administrative databases and big data in the study of gliomas demonstrated 122 studies across a wide range of pathologies and clinical questions. While we aimed to characterize the important prognostic factors seen across various geographic locales and significant time frames, there remained limitations in the granular study details important to clinical applicability. Several factors, including age, tumor grade and histology, as well as surgical EOR and adjuvant therapies, were reliably impactful on patient survival which were unsurprising. More specific patient situations or treatments that offer insight to treatment could often not be determined based on the database structure. Other prognostic factors often were not reproducible among different studies. Numerous studies show improvement in survival rates over time and loosely attribute this to improved surgical technique and optimal timing of adjuvant RCT. But the impact of specific treatment changes could not be identified from these databases. The incorporation of molecular diagnostics in the discussion of these patients was commonly lacking and multiple studies combined different pathologies or WHO grade tumors to report findings.

One of the major advantages of large databases is the ability to compare across variation of socioeconomic factors, such as race, marital status, and insurance status, which would not be possible for many individual centers which have more homogeneous patient populations. This allows tracking of outcomes in disadvantaged patients and raises awareness for the patient management. In addition, some studies have shown the improvement of survival for patients in high-volume centers or metropolitan areas, suggesting variation in care delivery. However, the major disadvantage of large databases involves higher level of detail regarding patients and tumor types. These group of studies also did not indicate avenues to improve on health care disparities despite detecting them multiple times.

Improved analysis of large administrative databases is still needed. Despite some reported benefits, large databases are generally not designed to address all clinically relevant study questions with precision. One example of this is that different studies can show contradictory results for various prognostic factors. This may be likely a result of patient heterogeneity or the statistical analysis performed. Use of traditional statistical methods have the potential to identify statistically significant but not clinically relevant findings. Improvements are needed in our ability to analyze data from large administrative databases to ensure we can answer impactful questions and recognize reproducible epidemiologic patterns. Use of uniform reporting criteria for these studies, such as the STROBE criteria, is also necessary to improve the quality of these studies.


#

Conclusions

This study helped identify databases involved in the understanding of treatment for various gliomas. Descriptive information regarding the involved databases is provided. Consistent prognostic factors included age, tumor grade, histology, and EOR. While improvement in survival was seen over time, it was unclear which treatments specifically impacted this. In addition, marked socioeconomic, and racial disparities in health care persisted over time for a variety of pathologies. Administrative databases were also limited in integrating updates in molecular tumor subtypes. The application of insights from research databases to impact patient care remains inadequate.


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Conflict of Interest

None declared.

Supplementary Material

  • References

  • 1 Ostrom QT, Cote DJ, Ascha M, Kruchko C, Barnholtz-Sloan JS. Adult glioma incidence and survival by race or ethnicity in the United States From 2000 to 2014. JAMA Oncol 2018; 4 (09) 1254-1262
  • 2 Karsy M, Neil JA, Guan J, Mahan MA, Colman H, Jensen RL. A practical review of prognostic correlations of molecular biomarkers in glioblastoma. Neurosurg Focus 2015; 38 (03) E4
  • 3 Oravec CS, Motiwala M, Reed K. et al. Big data research in neurosurgery: a critical look at this popular new study design. Neurosurgery 2018; 82 (05) 728-746
  • 4 Jhaveri J, Liu Y, Chowdhary M. et al. Is less more? Comparing chemotherapy alone with chemotherapy and radiation for high-risk grade 2 glioma: an analysis of the National Cancer Data Base. Cancer 2018; 124 (06) 1169-1178
  • 5 Alattar AA, Carroll KT, Bryant AK. et al. Prognostic importance of age, tumor location, and tumor grade in grade II astrocytomas: An Integrated Analysis of the Cancer Genome Atlas and the Surveillance, Epidemiology, and End Results Database. World Neurosurg 2019; 121: e411-e418
  • 6 Schupper AJ, Hirshman BR, Carroll KT, Ali MA, Carter BS, Chen CC. Effect of Gross Total Resection in World Health Organization Grade II Astrocytomas: SEER-Based Survival Analysis. World Neurosurg 2017; 103: 741-747
  • 7 Achey RL, Khanna V, Ostrom QT, Kruchko C, Barnholtz-Sloan JS. Incidence and survival trends in oligodendrogliomas and anaplastic oligodendrogliomas in the United States from 2000 to 2013: a CBTRUS Report. J Neurooncol 2017; 133 (01) 17-25
  • 8 Alattar AA, Brandel MG, Hirshman BR. et al. Oligodendroglioma resection: a Surveillance, Epidemiology, and End Results (SEER) analysis. J Neurosurg 2018; 128 (04) 1076-1083
  • 9 Brandel MG, Alattar AA, Hirshman BR. et al. Survival trends of oligodendroglial tumor patients and associated clinical practice patterns: a SEER-based analysis. J Neurooncol 2017; 133 (01) 173-181
  • 10 Kinslow CJ, Garton ALA, Rae AI. et al. Extent of resection and survival for oligodendroglioma: a U.S. population-based study. J Neurooncol 2019; 144 (03) 591-601
  • 11 Lau CS, Mahendraraj K, Chamberlain RS. Oligodendrogliomas in pediatric and adult patients: an outcome-based study from the Surveillance, Epidemiology, and End Result database. Cancer Manag Res 2017; 9: 159-166
  • 12 Furst T, Hoffman H, Chin LS. All-cause and tumor-specific mortality trends in geriatric oligodendroglioma (OG) patients: A surveillance, epidemiology, and end results (SEER) analysis. J Clin Neurosci 2020; 73: 94-100
  • 13 Dubrow R, Darefsky AS. Demographic variation in incidence of adult glioma by subtype, United States, 1992-2007. BMC Cancer 2011; 11: 325
  • 14 Mezencev R. Epidemiology of gliomas in women diagnosed with breast cancer supports the protective role of estrogenic exposure. Bratisl Lek Listy 2018; 119 (08) 463-468
  • 15 Persaud-Sharma D, Burns J, Trangle J. et al. Demographic variation in the frequency of gliomas in Florida. Medicina (Kaunas) 2019; 55 (01) E5
  • 16 Hess KR, Broglio KR, Bondy ML. Adult glioma incidence trends in the United States, 1977-2000. Cancer 2004; 101 (10) 2293-2299
  • 17 Jhaveri J, Cheng E, Tian S. et al. Proton vs. Photon Radiation Therapy for Primary Gliomas: An Analysis of the National Cancer Data Base. Front Oncol 2018; 8: 440
  • 18 Li K, Lu D, Guo Y. et al. Trends and patterns of incidence of diffuse glioma in adults in the United States, 1973-2014. Cancer Med 2018; 7 (10) 5281-5290
  • 19 Plascak JJ, Fisher JL. Area-based socioeconomic position and adult glioma: a hierarchical analysis of surveillance epidemiology and end results data. PLoS One 2013; 8 (04) e60910
  • 20 Gittleman H, Ostrom QT, Stetson LC. et al. Sex is an important prognostic factor for glioblastoma but not for nonglioblastoma. Neurooncol Pract 2019; 6 (06) 451-462
  • 21 Samaan MC, Akhtar-Danesh N. The impact of age and race on longevity in pediatric astrocytic tumors: A population-based study. Pediatr Blood Cancer 2015; 62 (09) 1567-1571
  • 22 Zhao YY, Chen SH, Hao Z, Zhu HX, Xing ZL, Li MH. A nomogram for predicting individual prognosis of patients with low-grade glioma. World Neurosurg 2019; 130: e605-e612
  • 23 Deb S, Pendharkar AV, Schoen MK, Altekruse S, Ratliff J, Desai A. The effect of socioeconomic status on gross total resection, radiation therapy and overall survival in patients with gliomas. J Neurooncol 2017; 132 (03) 447-453
  • 24 Dong X, Noorbakhsh A, Hirshman BR. et al. Survival trends of grade I, II, and III astrocytoma patients and associated clinical practice patterns between 1999 and 2010: A SEER-based analysis. Neurooncol Pract 2016; 3 (01) 29-38
  • 25 Iwamoto FM, Reiner AS, Nayak L, Panageas KS, Elkin EB, Abrey LE. Prognosis and patterns of care in elderly patients with glioma. Cancer 2009; 115 (23) 5534-5540
  • 26 Long S, Li M, Ou S, Li G. The effect of marital status on glioma patient survival: analysis of 617 cases: A SEER-based study. Medicine (Baltimore) 2018; 97 (52) e13900
  • 27 Wu J, Neale N, Huang Y. et al. Comparison of Adjuvant Radiation Therapy Alone and Chemotherapy Alone in Surgically Resected Low-Grade Gliomas: Survival Analyses of 2253 Cases from the National Cancer Data Base. World Neurosurg 2018; 112: e812-e822
  • 28 Xie JC, Yang S, Liu XY, Zhao YX. Marital status is associated with survival of patients with astrocytoma. J Clin Neurosci 2018; 56: 79-87
  • 29 Zhu P, Du XL, Blanco AI. et al. Impact of facility type and volume in low-grade glioma outcomes. J Neurosurg (e-pub ahead of print)
  • 30 Claus EB, Black PM. Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas: data from the SEER program, 1973-2001. Cancer 2006; 106 (06) 1358-1363
  • 31 Claus EB, Walsh KM, Wiencke JK. et al. Survival and low-grade glioma: the emergence of genetic information. Neurosurg Focus 2015; 38 (01) E6
  • 32 Jairam V, Kann BH, Park HS. et al. Defining an Intermediate-risk Group for Low-grade Glioma: A National Cancer Database Analysis. Anticancer Res 2019; 39 (06) 2911-2918
  • 33 Lehrer S. Glioma and Alzheimer's disease. J Alzheimers Dis Rep 2018; 2 (01) 213-218
  • 34 Nguyen HS, Best B, Doan NB. et al. Glioblastoma in the setting of prior lower grade gliomas - insights from SEER database. Oncotarget 2018; 9 (70) 33271-33277
  • 35 Smoll NR, Gautschi OP, Schatlo B, Schaller K, Weber DC. Relative survival of patients with supratentorial low-grade gliomas. Neuro-oncol 2012; 14 (08) 1062-1069
  • 36 Youssef I, Lee A, Garay EL, Becker DJ, Schreiber D. Patterns of care and outcomes of postoperative radiation for low-grade gliomas in United States hospitals. J Clin Neurosci 2018; 58: 124-129
  • 37 Missios S, Kalakoti P, Nanda A, Bekelis K. Craniotomy for glioma resection: a predictive model. World Neurosurg 2015; 83 (06) 957-964
  • 38 Mukherjee D, Sarmiento JM, Nosova K. et al. Effectiveness of radiotherapy for elderly patients with anaplastic gliomas. J Clin Neurosci 2014; 21 (05) 773-778
  • 39 Padwal JA, Dong X, Hirshman BR, Hoi-Sang U, Carter BS, Chen CC. Superior efficacy of gross total resection in anaplastic astrocytoma patients relative to glioblastoma patients. World Neurosurg 2016; 90: 186-193
  • 40 Shin JY, Diaz AZ. Anaplastic astrocytoma: prognostic factors and survival in 4807 patients with emphasis on receipt and impact of adjuvant therapy. J Neurooncol 2016; 129 (03) 557-565
  • 41 Shin JY, Diaz AZ. Utilization and impact of adjuvant therapy in anaplastic oligodendroglioma: an analysis on 1692 patients. J Neurooncol 2016; 129 (03) 567-575
  • 42 Shin JY, Yoon JK, Diaz AZ. Racial disparities in anaplastic oligodendroglioma: An analysis on 1643 patients. J Clin Neurosci 2017; 37: 34-39
  • 43 Smoll NR, Hamilton B. Incidence and relative survival of anaplastic astrocytomas. Neuro-oncol 2014; 16 (10) 1400-1407
  • 44 Zhao YY, Wan QS, Hao Z, Zhu HX, Xing ZL, Li MH. Clinical nomogram for predicting the survival of patients with cerebral anaplastic gliomas. Medicine (Baltimore) 2020; 99 (10) e19416
  • 45 Tsao-Wei DD, Hu J, Groshen SG, Chamberlain MC. Conditional survival of high-grade glioma in Los Angeles County during the year 1990-2000. J Neurooncol 2012; 110 (01) 145-152
  • 46 Champeaux C, Weller J. Implantation of carmustine wafers (Gliadel) for high-grade glioma treatment. A 9-year nationwide retrospective study. J Neurooncol 2020; 147 (01) 159-169
  • 47 Maxwell R, Luksik AS, Garzon-Muvdi T. et al. Population-based study determining predictors of cancer-specific mortality and survival in pediatric high-grade brainstem glioma. World Neurosurg 2018; 119: e1006-e1015
  • 48 Rusthoven CG, Carlson JA, Waxweiler TV. et al. The impact of adjuvant radiation therapy for high-grade gliomas by histology in the United States population. Int J Radiat Oncol Biol Phys 2014; 90 (04) 894-902
  • 49 Yang W, Xu T, Garzon-Muvdi T, Jiang C, Huang J, Chaichana KL. Survival of Ventricular and Periventricular High-Grade Gliomas: A Surveillance, Epidemiology, and End Results Program-Based Study. World Neurosurg 2018; 111: e323-e334
  • 50 Barnholtz-Sloan JS, Williams VL, Maldonado JL. et al. Patterns of care and outcomes among elderly individuals with primary malignant astrocytoma. J Neurosurg 2008; 108 (04) 642-648
  • 51 Sun Y, Xiong ZY, Yan PF, Jiang LL, Nie CS, Wang X. Characteristics and prognostic factors of age-stratified high-grade intracranial glioma patients: a population-based analysis. Bosn J Basic Med Sci 2019; 19 (04) 375-383
  • 52 Xie JC, Yang S, Liu XY, Zhao YX. Effect of marital status on survival in glioblastoma multiforme by demographics, education, economic factors, and insurance status. Cancer Med 2018; 7 (08) 3722-3742
  • 53 Lee I, Adimadhyam S, Nutescu EA. et al. Bevacizumab use and the risk of arterial and venous thromboembolism in patients with high-grade gliomas: a nested case-control study. Pharmacotherapy 2019; 39 (09) 921-928
  • 54 Alan N, Seicean A, Seicean S, Neuhauser D, Benzel EC, Weil RJ. Preoperative steroid use and the incidence of perioperative complications in patients undergoing craniotomy for definitive resection of a malignant brain tumor. J Clin Neurosci 2015; 22 (09) 1413-1419
  • 55 Aulakh S, DeDeo MR, Free J. et al. Survival trends in glioblastoma and association with treating facility volume. J Clin Neurosci 2019; 68: 271-274
  • 56 Dressler EV, Liu M, Garcia CR. et al. Patterns and disparities of care in glioblastoma. Neurooncol Pract 2019; 6 (01) 37-46
  • 57 Glaser SM, Dohopolski MJ, Balasubramani GK, Flickinger JC, Beriwal S. Glioblastoma multiforme (GBM) in the elderly: initial treatment strategy and overall survival. J Neurooncol 2017; 134 (01) 107-118
  • 58 Mak KS, Agarwal A, Qureshi MM, Truong MT. Hypofractionated short-course radiotherapy in elderly patients with glioblastoma multiforme: an analysis of the National Cancer Database. Cancer Med 2017; 6 (06) 1192-1200
  • 59 Malakhov N, Lee A, Garay E, Becker DJ, Schreiber D. Patterns of care and outcomes for glioblastoma in patients with poor performance status. J Clin Neurosci 2018; 52: 66-70
  • 60 Lee A, Malakhov N, Sheth N, Wang A, Han P, Schreiber D. Patterns of care and outcomes of chemoradiation versus radiation alone for MGMT promoter unmethylated glioblastoma. Clin Neurol Neurosurg 2018; 170: 127-131
  • 61 Lee A, Youssef I, Osborn VW, Safdieh J, Becker DJ, Schreiber D. The utilization of MGMT promoter methylation testing in United States hospitals for glioblastoma and its impact on prognosis. J Clin Neurosci 2018; 51: 85-90
  • 62 Buszek SM, Al Feghali KA, Elhalawani H, Chevli N, Allen PK, Chung C. Optimal Timing of Radiotherapy Following Gross Total or Subtotal Resection of Glioblastoma: A Real-World Assessment using the National Cancer Database. Sci Rep 2020; 10 (01) 4926
  • 63 Haque W, Thong Y, Verma V, Rostomily R, Brian Butler E, Teh BS. Patterns of management and outcomes of unifocal versus multifocal glioblastoma. J Clin Neurosci 2020; 74: 155-159
  • 64 Hauser A, Dutta SW, Showalter TN, Sheehan JP, Grover S, Trifiletti DM. Impact of academic facility type and volume on post-surgical outcomes following diagnosis of glioblastoma. J Clin Neurosci 2018; 47: 103-110
  • 65 Rhome R, Fisher R, Hormigo A, Parikh RR. Disparities in receipt of modern concurrent chemoradiotherapy in glioblastoma. J Neurooncol 2016; 128 (02) 241-250
  • 66 Kole AJ, Park HS, Yeboa DN. et al. Concurrent chemoradiotherapy versus radiotherapy alone for “biopsy-only” glioblastoma multiforme. Cancer 2016; 122 (15) 2364-2370
  • 67 Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN. Prognostic implications of extent of resection in glioblastoma: analysis from a large database. World Neurosurg 2017; 103: 330-340
  • 68 Wegner RE, Abel S, Horne ZD. et al. National trends in radiation dose escalation for glioblastoma. Radiat Oncol J 2019; 37 (01) 13-21
  • 69 Aizer AA, Ancukiewicz M, Nguyen PL, Shih HA, Loeffler JS, Oh KS. Underutilization of radiation therapy in patients with glioblastoma: predictive factors and outcomes. Cancer 2014; 120 (02) 238-243
  • 70 Al-Husseini MJ, Saad AM, El-Shewy KM. et al. Prior malignancy impact on survival outcomes of glioblastoma multiforme; population-based study. Int J Neurosci 2019; 129 (05) 447-454
  • 71 Barnholtz-Sloan JS, Maldonado JL, Williams VL. et al. Racial/ethnic differences in survival among elderly patients with a primary glioblastoma. J Neurooncol 2007; 85 (02) 171-180
  • 72 Bartek Jr J, Alattar AA, Dhawan S. et al. Receipt of brachytherapy is an independent predictor of survival in glioblastoma in the Surveillance, Epidemiology, and End Results database. J Neurooncol 2019; 145 (01) 75-83
  • 73 Siker ML, Wang M, Porter K. et al. Age as an independent prognostic factor in patients with glioblastoma: a Radiation Therapy Oncology Group and American College of Surgeons National Cancer Data Base comparison. J Neurooncol 2011; 104 (01) 351-356
  • 74 Thumma SR, Fairbanks RK, Lamoreaux WT. et al. Effect of pretreatment clinical factors on overall survival in glioblastoma multiforme: a Surveillance Epidemiology and End Results (SEER) population analysis. World J Surg Oncol 2012; 10: 75
  • 75 Walker GV, Li J, Mahajan A. et al. Decreasing radiation therapy utilization in adult patients with glioblastoma multiforme: a population-based analysis. Cancer 2012; 118 (18) 4538-4544
  • 76 Yusuf MB, Gaskins J, Amsbaugh MJ, Woo S, Burton E. Survival impact of prolonged postoperative radiation therapy for patients with glioblastoma treated with combined-modality therapy. Neurooncol Pract 2019; 6 (02) 112-123
  • 77 Zinn PO, Colen RR, Kasper EM, Burkhardt JK. Extent of resection and radiotherapy in GBM: A 1973 to 2007 surveillance, epidemiology and end results analysis of 21,783 patients. Int J Oncol 2013; 42 (03) 929-934
  • 78 Chang SM, Barker II FG. Marital status, treatment, and survival in patients with glioblastoma multiforme: a population based study. Cancer 2005; 104 (09) 1975-1984
  • 79 Chen JH, Huang CY, Lee YC. et al. Comparative cost analysis for the surgical and endovascular treatment of ruptured intracranial aneurysms in Taiwan: a nationwide population-based cohort study. World Neurosurg 2018; 116: e485-e490
  • 80 Darefsky AS, King Jr JT, Dubrow R. Adult glioblastoma multiforme survival in the temozolomide era: a population-based analysis of Surveillance, Epidemiology, and End Results registries. Cancer 2012; 118 (08) 2163-2172
  • 81 Iwamoto FM, Reiner AS, Panageas KS, Elkin EB, Abrey LE. Patterns of care in elderly glioblastoma patients. Ann Neurol 2008; 64 (06) 628-634
  • 82 Adams H, Adams HH, Jackson C, Rincon-Torroella J, Jallo GI, Quiñones-Hinojosa A. Evaluating extent of resection in pediatric glioblastoma: a multiple propensity score-adjusted population-based analysis. Childs Nerv Syst 2016; 32 (03) 493-503
  • 83 Johnson DR, Ma DJ, Buckner JC, Hammack JE. Conditional probability of long-term survival in glioblastoma: a population-based analysis. Cancer 2012; 118 (22) 5608-5613
  • 84 Johnson DR, O'Neill BP. Glioblastoma survival in the United States before and during the temozolomide era. J Neurooncol 2012; 107 (02) 359-364
  • 85 Lam S, Lin Y, Zinn P, Su J, Pan IW. Patient and treatment factors associated with survival among pediatric glioblastoma patients: A Surveillance, Epidemiology, and End Results study. J Clin Neurosci 2018; 47: 285-293
  • 86 Noorbakhsh A, Tang JA, Marcus LP. et al. Gross-total resection outcomes in an elderly population with glioblastoma: a SEER-based analysis. J Neurosurg 2014; 120 (01) 31-39
  • 87 Pan IW, Ferguson SD, Lam S. Patient and treatment factors associated with survival among adult glioblastoma patients: A USA population-based study from 2000-2010. J Clin Neurosci 2015; 22 (10) 1575-1581
  • 88 Porter AB, Lachance DH, Johnson DR. Socioeconomic status and glioblastoma risk: a population-based analysis. Cancer Causes Control 2015; 26 (02) 179-185
  • 89 Shah BK, Bista A, Sharma S. Survival trends in elderly patients with glioblastoma in the United States: a population-based study. Anticancer Res 2016; 36 (09) 4883-4886
  • 90 Tian M, Ma W, Chen Y. et al. Impact of gender on the survival of patients with glioblastoma. Biosci Rep 2018; 38 (06) BSR20180752
  • 91 Wachtel MS, Yang S. Odds of death after glioblastoma diagnosis in the United States by chemotherapeutic era. Cancer Med 2014; 3 (03) 660-666
  • 92 Zhu P, Du XL, Lu G, Zhu JJ. Survival benefit of glioblastoma patients after FDA approval of temozolomide concomitant with radiation and bevacizumab: A population-based study. Oncotarget 2017; 8 (27) 44015-44031
  • 93 Aneja S, Khullar D, Yu JB. The influence of regional health system characteristics on the surgical management and receipt of post operative radiation therapy for glioblastoma multiforme. J Neurooncol 2013; 112 (03) 393-401
  • 94 Koshy M, Villano JL, Dolecek TA. et al. Improved survival time trends for glioblastoma using the SEER 17 population-based registries. J Neurooncol 2012; 107 (01) 207-212
  • 95 Shabihkhani M, Telesca D, Movassaghi M. et al. Incidence, survival, pathology, and genetics of adult Latino Americans with glioblastoma. J Neurooncol 2017; 132 (02) 351-358
  • 96 Shu C, Yan X, Zhang X, Wang Q, Cao S, Wang J. Tumor-induced mortality in adult primary supratentorial glioblastoma multiforme with different age subgroups. Future Oncol 2019; 15 (10) 1105-1114
  • 97 Smoll NR, Schaller K, Gautschi OP. The cure fraction of glioblastoma multiforme. Neuroepidemiology 2012; 39 (01) 63-69
  • 98 Arvold ND, Cefalu M, Wang Y, Zigler C, Schrag D, Dominici F. Comparative effectiveness of radiotherapy with vs. without temozolomide in older patients with glioblastoma. J Neurooncol 2017; 131 (02) 301-311
  • 99 Arvold ND, Wang Y, Zigler C, Schrag D, Dominici F. Hospitalization burden and survival among older glioblastoma patients. Neuro-oncol 2014; 16 (11) 1530-1540
  • 100 Barnholtz-Sloan JS, Sloan AE, Schwartz AG. Racial differences in survival after diagnosis with primary malignant brain tumor. Cancer 2003; 98 (03) 603-609
  • 101 Bohn A, Braley A, Rodriguez de la Vega P, Zevallos JC, Barengo NC. The association between race and survival in glioblastoma patients in the US: a retrospective cohort study. PLoS One 2018; 13 (06) e0198581
  • 102 Davies J, Reyes-Rivera I, Pattipaka T. et al. Survival in elderly glioblastoma patients treated with bevacizumab-based regimens in the United States. Neurooncol Pract 2018; 5 (04) 251-261
  • 103 Delavar A, Al Jammal OM, Maguire KR, Wali AR, Pham MH. The impact of rural residence on adult brain cancer survival in the United States. J Neurooncol 2019; 144 (03) 535-543
  • 104 Forst D, Adams E, Nipp R. et al. Hospice utilization in patients with malignant gliomas. Neuro-oncol 2018; 20 (04) 538-545
  • 105 Johnson DR, Leeper HE, Uhm JH. Glioblastoma survival in the United States improved after Food and Drug Administration approval of bevacizumab: a population-based analysis. Cancer 2013; 119 (19) 3489-3495
  • 106 Ladomersky E, Scholtens DM, Kocherginsky M. et al. The coincidence between increasing age, immunosuppression, and the incidence of patients with glioblastoma. Front Pharmacol 2019; 10: 200
  • 107 Marcus LP, McCutcheon BA, Noorbakhsh A. et al. Incidence and predictors of 30-day readmission for patients discharged home after craniotomy for malignant supratentorial tumors in California (1995-2010). J Neurosurg 2014; 120 (05) 1201-1211
  • 108 Pendharkar AV, Rezaii PG, Ho AL, Sussman ES, Li G, Desai AM. Functional mapping for glioma surgery: a propensity-matched analysis of outcomes and cost. World Neurosurg 2020; 137: e328-e335
  • 109 Rahmani R, Tomlinson SB, Santangelo G. et al. Risk factors associated with early adverse outcomes following craniotomy for malignant glioma in older adults. J Geriatr Oncol 2020; 11 (04) 694-700
  • 110 Rong X, Yang W, Garzon-Muvdi T. et al. Influence of insurance status on survival of adults with glioblastoma multiforme: A population-based study. Cancer 2016; 122 (20) 3157-3165
  • 111 Huang J, Samson P, Perkins SM. et al. Impact of concurrent chemotherapy with radiation therapy for elderly patients with newly diagnosed glioblastoma: a review of the National Cancer Data Base. J Neurooncol 2017; 131 (03) 593-601
  • 112 Nguyen HS, Doan NB, Gelsomino M. et al. Management and survival trends for adult patients with malignant gliomas in the setting of multiple primary tumors: a population based analysis. J Neurooncol 2019; 141 (01) 213-221
  • 113 Zada G, Bond AE, Wang YP, Giannotta SL, Deapen D. Incidence trends in the anatomic location of primary malignant brain tumors in the United States: 1992-2006. World Neurosurg 2012; 77 (3-4): 518-524
  • 114 Huang LE, Cohen AL, Colman H, Jensen RL, Fults DW, Couldwell WT. IGFBP2 expression predicts IDH-mutant glioma patient survival. Oncotarget 2017; 8 (01) 191-202
  • 115 Chen LF, Yang Y, Ma XD. et al. Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 2017; 27 (05) 696-706
  • 116 Li X, Li Y, Cao Y. et al. Risk of subsequent cancer among pediatric, adult and elderly patients following a primary diagnosis of glioblastoma multiforme: a population-based study of the SEER database. Int J Neurosci 2017; 127 (11) 1005-1011
  • 117 Nuño M, Ly D, Mukherjee D, Ortega A, Black KL, Patil CG. Quality of surgical care and readmission in elderly glioblastoma patients. Neurooncol Pract 2014; 1 (02) 33-39
  • 118 Wang W. Increased incidence of second primary malignancy in patients with malignant astrocytoma: a population-based study. Biosci Rep 2019; 39 (06) BSR20181968
  • 119 Xu H, Chen J, Xu H, Qin Z. Geographic variations in the incidence of glioblastoma and prognostic factors predictive of overall survival in US adults from 2004-2013. Front Aging Neurosci 2017; 9: 352
  • 120 Bin Abdulrahman AK, Bin Abdulrahman KA, Bukhari YR, Faqihi AM, Ruiz JG. Association between giant cell glioblastoma and glioblastoma multiforme in the United States: A retrospective cohort study. Brain Behav 2019; 9 (10) e01402
  • 121 Lai R, Hershman DL, Doan T, Neugut AI. The timing of cranial radiation in elderly patients with newly diagnosed glioblastoma multiforme. Neuro-oncol 2010; 12 (02) 190-198
  • 122 Chen YR, Sole J, Ugiliweneza B. et al. National trends for reoperation in older patients with glioblastoma. World Neurosurg 2018; 113: e179-e189
  • 123 Chen YR, Ugiliweneza B, Burton E, Woo SY, Boakye M, Skirboll S. The effect of postoperative infection on survival in patients with glioblastoma. J Neurosurg 2017; 127 (04) 807-811
  • 124 Zhou X, Zhang S, Niu X. et al. Risk factors for early mortality among patients with glioma: a population-based study. World Neurosurg 2020; 136: e496-e503
  • 125 Haque W, Verma V, Butler EB, Teh BS. Patterns of care and outcomes of multi-agent versus single-agent chemotherapy as part of multimodal management of low grade glioma. J Neurooncol 2017; 133 (02) 369-375
  • 126 Diaz-Aguilar D, ReFaey K, Clifton W. et al. Prognostic factors and survival in low grade gliomas of the spinal cord: A population-based analysis from 2006 to 2012. J Clin Neurosci 2019; 61: 14-21
  • 127 Xia Y, Liao W, Huang S. et al. Nomograms for Predicting the Overall and Cancer-Specific Survival of Patients with High-Grade Glioma: A Surveillance, Epidemiology, and End Results Study. Turk Neurosurg 2020; 30 (01) 48-59

Address for correspondence

Michael Karsy, MD, PhD, MSc
University of Utah Health Care, University of Utah Health Hospitals and Clinics
UT
United States   

Publication History

Article published online:
08 February 2022

© 2022. Neurological Surgeons' Society of India. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Ostrom QT, Cote DJ, Ascha M, Kruchko C, Barnholtz-Sloan JS. Adult glioma incidence and survival by race or ethnicity in the United States From 2000 to 2014. JAMA Oncol 2018; 4 (09) 1254-1262
  • 2 Karsy M, Neil JA, Guan J, Mahan MA, Colman H, Jensen RL. A practical review of prognostic correlations of molecular biomarkers in glioblastoma. Neurosurg Focus 2015; 38 (03) E4
  • 3 Oravec CS, Motiwala M, Reed K. et al. Big data research in neurosurgery: a critical look at this popular new study design. Neurosurgery 2018; 82 (05) 728-746
  • 4 Jhaveri J, Liu Y, Chowdhary M. et al. Is less more? Comparing chemotherapy alone with chemotherapy and radiation for high-risk grade 2 glioma: an analysis of the National Cancer Data Base. Cancer 2018; 124 (06) 1169-1178
  • 5 Alattar AA, Carroll KT, Bryant AK. et al. Prognostic importance of age, tumor location, and tumor grade in grade II astrocytomas: An Integrated Analysis of the Cancer Genome Atlas and the Surveillance, Epidemiology, and End Results Database. World Neurosurg 2019; 121: e411-e418
  • 6 Schupper AJ, Hirshman BR, Carroll KT, Ali MA, Carter BS, Chen CC. Effect of Gross Total Resection in World Health Organization Grade II Astrocytomas: SEER-Based Survival Analysis. World Neurosurg 2017; 103: 741-747
  • 7 Achey RL, Khanna V, Ostrom QT, Kruchko C, Barnholtz-Sloan JS. Incidence and survival trends in oligodendrogliomas and anaplastic oligodendrogliomas in the United States from 2000 to 2013: a CBTRUS Report. J Neurooncol 2017; 133 (01) 17-25
  • 8 Alattar AA, Brandel MG, Hirshman BR. et al. Oligodendroglioma resection: a Surveillance, Epidemiology, and End Results (SEER) analysis. J Neurosurg 2018; 128 (04) 1076-1083
  • 9 Brandel MG, Alattar AA, Hirshman BR. et al. Survival trends of oligodendroglial tumor patients and associated clinical practice patterns: a SEER-based analysis. J Neurooncol 2017; 133 (01) 173-181
  • 10 Kinslow CJ, Garton ALA, Rae AI. et al. Extent of resection and survival for oligodendroglioma: a U.S. population-based study. J Neurooncol 2019; 144 (03) 591-601
  • 11 Lau CS, Mahendraraj K, Chamberlain RS. Oligodendrogliomas in pediatric and adult patients: an outcome-based study from the Surveillance, Epidemiology, and End Result database. Cancer Manag Res 2017; 9: 159-166
  • 12 Furst T, Hoffman H, Chin LS. All-cause and tumor-specific mortality trends in geriatric oligodendroglioma (OG) patients: A surveillance, epidemiology, and end results (SEER) analysis. J Clin Neurosci 2020; 73: 94-100
  • 13 Dubrow R, Darefsky AS. Demographic variation in incidence of adult glioma by subtype, United States, 1992-2007. BMC Cancer 2011; 11: 325
  • 14 Mezencev R. Epidemiology of gliomas in women diagnosed with breast cancer supports the protective role of estrogenic exposure. Bratisl Lek Listy 2018; 119 (08) 463-468
  • 15 Persaud-Sharma D, Burns J, Trangle J. et al. Demographic variation in the frequency of gliomas in Florida. Medicina (Kaunas) 2019; 55 (01) E5
  • 16 Hess KR, Broglio KR, Bondy ML. Adult glioma incidence trends in the United States, 1977-2000. Cancer 2004; 101 (10) 2293-2299
  • 17 Jhaveri J, Cheng E, Tian S. et al. Proton vs. Photon Radiation Therapy for Primary Gliomas: An Analysis of the National Cancer Data Base. Front Oncol 2018; 8: 440
  • 18 Li K, Lu D, Guo Y. et al. Trends and patterns of incidence of diffuse glioma in adults in the United States, 1973-2014. Cancer Med 2018; 7 (10) 5281-5290
  • 19 Plascak JJ, Fisher JL. Area-based socioeconomic position and adult glioma: a hierarchical analysis of surveillance epidemiology and end results data. PLoS One 2013; 8 (04) e60910
  • 20 Gittleman H, Ostrom QT, Stetson LC. et al. Sex is an important prognostic factor for glioblastoma but not for nonglioblastoma. Neurooncol Pract 2019; 6 (06) 451-462
  • 21 Samaan MC, Akhtar-Danesh N. The impact of age and race on longevity in pediatric astrocytic tumors: A population-based study. Pediatr Blood Cancer 2015; 62 (09) 1567-1571
  • 22 Zhao YY, Chen SH, Hao Z, Zhu HX, Xing ZL, Li MH. A nomogram for predicting individual prognosis of patients with low-grade glioma. World Neurosurg 2019; 130: e605-e612
  • 23 Deb S, Pendharkar AV, Schoen MK, Altekruse S, Ratliff J, Desai A. The effect of socioeconomic status on gross total resection, radiation therapy and overall survival in patients with gliomas. J Neurooncol 2017; 132 (03) 447-453
  • 24 Dong X, Noorbakhsh A, Hirshman BR. et al. Survival trends of grade I, II, and III astrocytoma patients and associated clinical practice patterns between 1999 and 2010: A SEER-based analysis. Neurooncol Pract 2016; 3 (01) 29-38
  • 25 Iwamoto FM, Reiner AS, Nayak L, Panageas KS, Elkin EB, Abrey LE. Prognosis and patterns of care in elderly patients with glioma. Cancer 2009; 115 (23) 5534-5540
  • 26 Long S, Li M, Ou S, Li G. The effect of marital status on glioma patient survival: analysis of 617 cases: A SEER-based study. Medicine (Baltimore) 2018; 97 (52) e13900
  • 27 Wu J, Neale N, Huang Y. et al. Comparison of Adjuvant Radiation Therapy Alone and Chemotherapy Alone in Surgically Resected Low-Grade Gliomas: Survival Analyses of 2253 Cases from the National Cancer Data Base. World Neurosurg 2018; 112: e812-e822
  • 28 Xie JC, Yang S, Liu XY, Zhao YX. Marital status is associated with survival of patients with astrocytoma. J Clin Neurosci 2018; 56: 79-87
  • 29 Zhu P, Du XL, Blanco AI. et al. Impact of facility type and volume in low-grade glioma outcomes. J Neurosurg (e-pub ahead of print)
  • 30 Claus EB, Black PM. Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas: data from the SEER program, 1973-2001. Cancer 2006; 106 (06) 1358-1363
  • 31 Claus EB, Walsh KM, Wiencke JK. et al. Survival and low-grade glioma: the emergence of genetic information. Neurosurg Focus 2015; 38 (01) E6
  • 32 Jairam V, Kann BH, Park HS. et al. Defining an Intermediate-risk Group for Low-grade Glioma: A National Cancer Database Analysis. Anticancer Res 2019; 39 (06) 2911-2918
  • 33 Lehrer S. Glioma and Alzheimer's disease. J Alzheimers Dis Rep 2018; 2 (01) 213-218
  • 34 Nguyen HS, Best B, Doan NB. et al. Glioblastoma in the setting of prior lower grade gliomas - insights from SEER database. Oncotarget 2018; 9 (70) 33271-33277
  • 35 Smoll NR, Gautschi OP, Schatlo B, Schaller K, Weber DC. Relative survival of patients with supratentorial low-grade gliomas. Neuro-oncol 2012; 14 (08) 1062-1069
  • 36 Youssef I, Lee A, Garay EL, Becker DJ, Schreiber D. Patterns of care and outcomes of postoperative radiation for low-grade gliomas in United States hospitals. J Clin Neurosci 2018; 58: 124-129
  • 37 Missios S, Kalakoti P, Nanda A, Bekelis K. Craniotomy for glioma resection: a predictive model. World Neurosurg 2015; 83 (06) 957-964
  • 38 Mukherjee D, Sarmiento JM, Nosova K. et al. Effectiveness of radiotherapy for elderly patients with anaplastic gliomas. J Clin Neurosci 2014; 21 (05) 773-778
  • 39 Padwal JA, Dong X, Hirshman BR, Hoi-Sang U, Carter BS, Chen CC. Superior efficacy of gross total resection in anaplastic astrocytoma patients relative to glioblastoma patients. World Neurosurg 2016; 90: 186-193
  • 40 Shin JY, Diaz AZ. Anaplastic astrocytoma: prognostic factors and survival in 4807 patients with emphasis on receipt and impact of adjuvant therapy. J Neurooncol 2016; 129 (03) 557-565
  • 41 Shin JY, Diaz AZ. Utilization and impact of adjuvant therapy in anaplastic oligodendroglioma: an analysis on 1692 patients. J Neurooncol 2016; 129 (03) 567-575
  • 42 Shin JY, Yoon JK, Diaz AZ. Racial disparities in anaplastic oligodendroglioma: An analysis on 1643 patients. J Clin Neurosci 2017; 37: 34-39
  • 43 Smoll NR, Hamilton B. Incidence and relative survival of anaplastic astrocytomas. Neuro-oncol 2014; 16 (10) 1400-1407
  • 44 Zhao YY, Wan QS, Hao Z, Zhu HX, Xing ZL, Li MH. Clinical nomogram for predicting the survival of patients with cerebral anaplastic gliomas. Medicine (Baltimore) 2020; 99 (10) e19416
  • 45 Tsao-Wei DD, Hu J, Groshen SG, Chamberlain MC. Conditional survival of high-grade glioma in Los Angeles County during the year 1990-2000. J Neurooncol 2012; 110 (01) 145-152
  • 46 Champeaux C, Weller J. Implantation of carmustine wafers (Gliadel) for high-grade glioma treatment. A 9-year nationwide retrospective study. J Neurooncol 2020; 147 (01) 159-169
  • 47 Maxwell R, Luksik AS, Garzon-Muvdi T. et al. Population-based study determining predictors of cancer-specific mortality and survival in pediatric high-grade brainstem glioma. World Neurosurg 2018; 119: e1006-e1015
  • 48 Rusthoven CG, Carlson JA, Waxweiler TV. et al. The impact of adjuvant radiation therapy for high-grade gliomas by histology in the United States population. Int J Radiat Oncol Biol Phys 2014; 90 (04) 894-902
  • 49 Yang W, Xu T, Garzon-Muvdi T, Jiang C, Huang J, Chaichana KL. Survival of Ventricular and Periventricular High-Grade Gliomas: A Surveillance, Epidemiology, and End Results Program-Based Study. World Neurosurg 2018; 111: e323-e334
  • 50 Barnholtz-Sloan JS, Williams VL, Maldonado JL. et al. Patterns of care and outcomes among elderly individuals with primary malignant astrocytoma. J Neurosurg 2008; 108 (04) 642-648
  • 51 Sun Y, Xiong ZY, Yan PF, Jiang LL, Nie CS, Wang X. Characteristics and prognostic factors of age-stratified high-grade intracranial glioma patients: a population-based analysis. Bosn J Basic Med Sci 2019; 19 (04) 375-383
  • 52 Xie JC, Yang S, Liu XY, Zhao YX. Effect of marital status on survival in glioblastoma multiforme by demographics, education, economic factors, and insurance status. Cancer Med 2018; 7 (08) 3722-3742
  • 53 Lee I, Adimadhyam S, Nutescu EA. et al. Bevacizumab use and the risk of arterial and venous thromboembolism in patients with high-grade gliomas: a nested case-control study. Pharmacotherapy 2019; 39 (09) 921-928
  • 54 Alan N, Seicean A, Seicean S, Neuhauser D, Benzel EC, Weil RJ. Preoperative steroid use and the incidence of perioperative complications in patients undergoing craniotomy for definitive resection of a malignant brain tumor. J Clin Neurosci 2015; 22 (09) 1413-1419
  • 55 Aulakh S, DeDeo MR, Free J. et al. Survival trends in glioblastoma and association with treating facility volume. J Clin Neurosci 2019; 68: 271-274
  • 56 Dressler EV, Liu M, Garcia CR. et al. Patterns and disparities of care in glioblastoma. Neurooncol Pract 2019; 6 (01) 37-46
  • 57 Glaser SM, Dohopolski MJ, Balasubramani GK, Flickinger JC, Beriwal S. Glioblastoma multiforme (GBM) in the elderly: initial treatment strategy and overall survival. J Neurooncol 2017; 134 (01) 107-118
  • 58 Mak KS, Agarwal A, Qureshi MM, Truong MT. Hypofractionated short-course radiotherapy in elderly patients with glioblastoma multiforme: an analysis of the National Cancer Database. Cancer Med 2017; 6 (06) 1192-1200
  • 59 Malakhov N, Lee A, Garay E, Becker DJ, Schreiber D. Patterns of care and outcomes for glioblastoma in patients with poor performance status. J Clin Neurosci 2018; 52: 66-70
  • 60 Lee A, Malakhov N, Sheth N, Wang A, Han P, Schreiber D. Patterns of care and outcomes of chemoradiation versus radiation alone for MGMT promoter unmethylated glioblastoma. Clin Neurol Neurosurg 2018; 170: 127-131
  • 61 Lee A, Youssef I, Osborn VW, Safdieh J, Becker DJ, Schreiber D. The utilization of MGMT promoter methylation testing in United States hospitals for glioblastoma and its impact on prognosis. J Clin Neurosci 2018; 51: 85-90
  • 62 Buszek SM, Al Feghali KA, Elhalawani H, Chevli N, Allen PK, Chung C. Optimal Timing of Radiotherapy Following Gross Total or Subtotal Resection of Glioblastoma: A Real-World Assessment using the National Cancer Database. Sci Rep 2020; 10 (01) 4926
  • 63 Haque W, Thong Y, Verma V, Rostomily R, Brian Butler E, Teh BS. Patterns of management and outcomes of unifocal versus multifocal glioblastoma. J Clin Neurosci 2020; 74: 155-159
  • 64 Hauser A, Dutta SW, Showalter TN, Sheehan JP, Grover S, Trifiletti DM. Impact of academic facility type and volume on post-surgical outcomes following diagnosis of glioblastoma. J Clin Neurosci 2018; 47: 103-110
  • 65 Rhome R, Fisher R, Hormigo A, Parikh RR. Disparities in receipt of modern concurrent chemoradiotherapy in glioblastoma. J Neurooncol 2016; 128 (02) 241-250
  • 66 Kole AJ, Park HS, Yeboa DN. et al. Concurrent chemoradiotherapy versus radiotherapy alone for “biopsy-only” glioblastoma multiforme. Cancer 2016; 122 (15) 2364-2370
  • 67 Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN. Prognostic implications of extent of resection in glioblastoma: analysis from a large database. World Neurosurg 2017; 103: 330-340
  • 68 Wegner RE, Abel S, Horne ZD. et al. National trends in radiation dose escalation for glioblastoma. Radiat Oncol J 2019; 37 (01) 13-21
  • 69 Aizer AA, Ancukiewicz M, Nguyen PL, Shih HA, Loeffler JS, Oh KS. Underutilization of radiation therapy in patients with glioblastoma: predictive factors and outcomes. Cancer 2014; 120 (02) 238-243
  • 70 Al-Husseini MJ, Saad AM, El-Shewy KM. et al. Prior malignancy impact on survival outcomes of glioblastoma multiforme; population-based study. Int J Neurosci 2019; 129 (05) 447-454
  • 71 Barnholtz-Sloan JS, Maldonado JL, Williams VL. et al. Racial/ethnic differences in survival among elderly patients with a primary glioblastoma. J Neurooncol 2007; 85 (02) 171-180
  • 72 Bartek Jr J, Alattar AA, Dhawan S. et al. Receipt of brachytherapy is an independent predictor of survival in glioblastoma in the Surveillance, Epidemiology, and End Results database. J Neurooncol 2019; 145 (01) 75-83
  • 73 Siker ML, Wang M, Porter K. et al. Age as an independent prognostic factor in patients with glioblastoma: a Radiation Therapy Oncology Group and American College of Surgeons National Cancer Data Base comparison. J Neurooncol 2011; 104 (01) 351-356
  • 74 Thumma SR, Fairbanks RK, Lamoreaux WT. et al. Effect of pretreatment clinical factors on overall survival in glioblastoma multiforme: a Surveillance Epidemiology and End Results (SEER) population analysis. World J Surg Oncol 2012; 10: 75
  • 75 Walker GV, Li J, Mahajan A. et al. Decreasing radiation therapy utilization in adult patients with glioblastoma multiforme: a population-based analysis. Cancer 2012; 118 (18) 4538-4544
  • 76 Yusuf MB, Gaskins J, Amsbaugh MJ, Woo S, Burton E. Survival impact of prolonged postoperative radiation therapy for patients with glioblastoma treated with combined-modality therapy. Neurooncol Pract 2019; 6 (02) 112-123
  • 77 Zinn PO, Colen RR, Kasper EM, Burkhardt JK. Extent of resection and radiotherapy in GBM: A 1973 to 2007 surveillance, epidemiology and end results analysis of 21,783 patients. Int J Oncol 2013; 42 (03) 929-934
  • 78 Chang SM, Barker II FG. Marital status, treatment, and survival in patients with glioblastoma multiforme: a population based study. Cancer 2005; 104 (09) 1975-1984
  • 79 Chen JH, Huang CY, Lee YC. et al. Comparative cost analysis for the surgical and endovascular treatment of ruptured intracranial aneurysms in Taiwan: a nationwide population-based cohort study. World Neurosurg 2018; 116: e485-e490
  • 80 Darefsky AS, King Jr JT, Dubrow R. Adult glioblastoma multiforme survival in the temozolomide era: a population-based analysis of Surveillance, Epidemiology, and End Results registries. Cancer 2012; 118 (08) 2163-2172
  • 81 Iwamoto FM, Reiner AS, Panageas KS, Elkin EB, Abrey LE. Patterns of care in elderly glioblastoma patients. Ann Neurol 2008; 64 (06) 628-634
  • 82 Adams H, Adams HH, Jackson C, Rincon-Torroella J, Jallo GI, Quiñones-Hinojosa A. Evaluating extent of resection in pediatric glioblastoma: a multiple propensity score-adjusted population-based analysis. Childs Nerv Syst 2016; 32 (03) 493-503
  • 83 Johnson DR, Ma DJ, Buckner JC, Hammack JE. Conditional probability of long-term survival in glioblastoma: a population-based analysis. Cancer 2012; 118 (22) 5608-5613
  • 84 Johnson DR, O'Neill BP. Glioblastoma survival in the United States before and during the temozolomide era. J Neurooncol 2012; 107 (02) 359-364
  • 85 Lam S, Lin Y, Zinn P, Su J, Pan IW. Patient and treatment factors associated with survival among pediatric glioblastoma patients: A Surveillance, Epidemiology, and End Results study. J Clin Neurosci 2018; 47: 285-293
  • 86 Noorbakhsh A, Tang JA, Marcus LP. et al. Gross-total resection outcomes in an elderly population with glioblastoma: a SEER-based analysis. J Neurosurg 2014; 120 (01) 31-39
  • 87 Pan IW, Ferguson SD, Lam S. Patient and treatment factors associated with survival among adult glioblastoma patients: A USA population-based study from 2000-2010. J Clin Neurosci 2015; 22 (10) 1575-1581
  • 88 Porter AB, Lachance DH, Johnson DR. Socioeconomic status and glioblastoma risk: a population-based analysis. Cancer Causes Control 2015; 26 (02) 179-185
  • 89 Shah BK, Bista A, Sharma S. Survival trends in elderly patients with glioblastoma in the United States: a population-based study. Anticancer Res 2016; 36 (09) 4883-4886
  • 90 Tian M, Ma W, Chen Y. et al. Impact of gender on the survival of patients with glioblastoma. Biosci Rep 2018; 38 (06) BSR20180752
  • 91 Wachtel MS, Yang S. Odds of death after glioblastoma diagnosis in the United States by chemotherapeutic era. Cancer Med 2014; 3 (03) 660-666
  • 92 Zhu P, Du XL, Lu G, Zhu JJ. Survival benefit of glioblastoma patients after FDA approval of temozolomide concomitant with radiation and bevacizumab: A population-based study. Oncotarget 2017; 8 (27) 44015-44031
  • 93 Aneja S, Khullar D, Yu JB. The influence of regional health system characteristics on the surgical management and receipt of post operative radiation therapy for glioblastoma multiforme. J Neurooncol 2013; 112 (03) 393-401
  • 94 Koshy M, Villano JL, Dolecek TA. et al. Improved survival time trends for glioblastoma using the SEER 17 population-based registries. J Neurooncol 2012; 107 (01) 207-212
  • 95 Shabihkhani M, Telesca D, Movassaghi M. et al. Incidence, survival, pathology, and genetics of adult Latino Americans with glioblastoma. J Neurooncol 2017; 132 (02) 351-358
  • 96 Shu C, Yan X, Zhang X, Wang Q, Cao S, Wang J. Tumor-induced mortality in adult primary supratentorial glioblastoma multiforme with different age subgroups. Future Oncol 2019; 15 (10) 1105-1114
  • 97 Smoll NR, Schaller K, Gautschi OP. The cure fraction of glioblastoma multiforme. Neuroepidemiology 2012; 39 (01) 63-69
  • 98 Arvold ND, Cefalu M, Wang Y, Zigler C, Schrag D, Dominici F. Comparative effectiveness of radiotherapy with vs. without temozolomide in older patients with glioblastoma. J Neurooncol 2017; 131 (02) 301-311
  • 99 Arvold ND, Wang Y, Zigler C, Schrag D, Dominici F. Hospitalization burden and survival among older glioblastoma patients. Neuro-oncol 2014; 16 (11) 1530-1540
  • 100 Barnholtz-Sloan JS, Sloan AE, Schwartz AG. Racial differences in survival after diagnosis with primary malignant brain tumor. Cancer 2003; 98 (03) 603-609
  • 101 Bohn A, Braley A, Rodriguez de la Vega P, Zevallos JC, Barengo NC. The association between race and survival in glioblastoma patients in the US: a retrospective cohort study. PLoS One 2018; 13 (06) e0198581
  • 102 Davies J, Reyes-Rivera I, Pattipaka T. et al. Survival in elderly glioblastoma patients treated with bevacizumab-based regimens in the United States. Neurooncol Pract 2018; 5 (04) 251-261
  • 103 Delavar A, Al Jammal OM, Maguire KR, Wali AR, Pham MH. The impact of rural residence on adult brain cancer survival in the United States. J Neurooncol 2019; 144 (03) 535-543
  • 104 Forst D, Adams E, Nipp R. et al. Hospice utilization in patients with malignant gliomas. Neuro-oncol 2018; 20 (04) 538-545
  • 105 Johnson DR, Leeper HE, Uhm JH. Glioblastoma survival in the United States improved after Food and Drug Administration approval of bevacizumab: a population-based analysis. Cancer 2013; 119 (19) 3489-3495
  • 106 Ladomersky E, Scholtens DM, Kocherginsky M. et al. The coincidence between increasing age, immunosuppression, and the incidence of patients with glioblastoma. Front Pharmacol 2019; 10: 200
  • 107 Marcus LP, McCutcheon BA, Noorbakhsh A. et al. Incidence and predictors of 30-day readmission for patients discharged home after craniotomy for malignant supratentorial tumors in California (1995-2010). J Neurosurg 2014; 120 (05) 1201-1211
  • 108 Pendharkar AV, Rezaii PG, Ho AL, Sussman ES, Li G, Desai AM. Functional mapping for glioma surgery: a propensity-matched analysis of outcomes and cost. World Neurosurg 2020; 137: e328-e335
  • 109 Rahmani R, Tomlinson SB, Santangelo G. et al. Risk factors associated with early adverse outcomes following craniotomy for malignant glioma in older adults. J Geriatr Oncol 2020; 11 (04) 694-700
  • 110 Rong X, Yang W, Garzon-Muvdi T. et al. Influence of insurance status on survival of adults with glioblastoma multiforme: A population-based study. Cancer 2016; 122 (20) 3157-3165
  • 111 Huang J, Samson P, Perkins SM. et al. Impact of concurrent chemotherapy with radiation therapy for elderly patients with newly diagnosed glioblastoma: a review of the National Cancer Data Base. J Neurooncol 2017; 131 (03) 593-601
  • 112 Nguyen HS, Doan NB, Gelsomino M. et al. Management and survival trends for adult patients with malignant gliomas in the setting of multiple primary tumors: a population based analysis. J Neurooncol 2019; 141 (01) 213-221
  • 113 Zada G, Bond AE, Wang YP, Giannotta SL, Deapen D. Incidence trends in the anatomic location of primary malignant brain tumors in the United States: 1992-2006. World Neurosurg 2012; 77 (3-4): 518-524
  • 114 Huang LE, Cohen AL, Colman H, Jensen RL, Fults DW, Couldwell WT. IGFBP2 expression predicts IDH-mutant glioma patient survival. Oncotarget 2017; 8 (01) 191-202
  • 115 Chen LF, Yang Y, Ma XD. et al. Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 2017; 27 (05) 696-706
  • 116 Li X, Li Y, Cao Y. et al. Risk of subsequent cancer among pediatric, adult and elderly patients following a primary diagnosis of glioblastoma multiforme: a population-based study of the SEER database. Int J Neurosci 2017; 127 (11) 1005-1011
  • 117 Nuño M, Ly D, Mukherjee D, Ortega A, Black KL, Patil CG. Quality of surgical care and readmission in elderly glioblastoma patients. Neurooncol Pract 2014; 1 (02) 33-39
  • 118 Wang W. Increased incidence of second primary malignancy in patients with malignant astrocytoma: a population-based study. Biosci Rep 2019; 39 (06) BSR20181968
  • 119 Xu H, Chen J, Xu H, Qin Z. Geographic variations in the incidence of glioblastoma and prognostic factors predictive of overall survival in US adults from 2004-2013. Front Aging Neurosci 2017; 9: 352
  • 120 Bin Abdulrahman AK, Bin Abdulrahman KA, Bukhari YR, Faqihi AM, Ruiz JG. Association between giant cell glioblastoma and glioblastoma multiforme in the United States: A retrospective cohort study. Brain Behav 2019; 9 (10) e01402
  • 121 Lai R, Hershman DL, Doan T, Neugut AI. The timing of cranial radiation in elderly patients with newly diagnosed glioblastoma multiforme. Neuro-oncol 2010; 12 (02) 190-198
  • 122 Chen YR, Sole J, Ugiliweneza B. et al. National trends for reoperation in older patients with glioblastoma. World Neurosurg 2018; 113: e179-e189
  • 123 Chen YR, Ugiliweneza B, Burton E, Woo SY, Boakye M, Skirboll S. The effect of postoperative infection on survival in patients with glioblastoma. J Neurosurg 2017; 127 (04) 807-811
  • 124 Zhou X, Zhang S, Niu X. et al. Risk factors for early mortality among patients with glioma: a population-based study. World Neurosurg 2020; 136: e496-e503
  • 125 Haque W, Verma V, Butler EB, Teh BS. Patterns of care and outcomes of multi-agent versus single-agent chemotherapy as part of multimodal management of low grade glioma. J Neurooncol 2017; 133 (02) 369-375
  • 126 Diaz-Aguilar D, ReFaey K, Clifton W. et al. Prognostic factors and survival in low grade gliomas of the spinal cord: A population-based analysis from 2006 to 2012. J Clin Neurosci 2019; 61: 14-21
  • 127 Xia Y, Liao W, Huang S. et al. Nomograms for Predicting the Overall and Cancer-Specific Survival of Patients with High-Grade Glioma: A Surveillance, Epidemiology, and End Results Study. Turk Neurosurg 2020; 30 (01) 48-59

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Fig. 1 The Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) flow diagram of selected studies.