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. 2022 Mar 2;3(3):CD013387.
doi: 10.1002/14651858.CD013387.pub2.

Diagnostic test accuracy and cost-effectiveness of tests for codeletion of chromosomal arms 1p and 19q in people with glioma

Alexandra McAleenan  1 , Hayley E Jones  1 , Ashleigh Kernohan  2 , Tomos Robinson  3 , Lena Schmidt  1 , Sarah Dawson  1 , Claire Kelly  1 , Emmelyn Spencer Leal  1 , Claire L Faulkner  4 , Abigail Palmer  4 , Christopher Wragg  4 , Sarah Jefferies  5 , Sebastian Brandner  6   7 , Luke Vale  8 , Julian Pt Higgins  1 , Kathreena M Kurian  9
Affiliations

Diagnostic test accuracy and cost-effectiveness of tests for codeletion of chromosomal arms 1p and 19q in people with glioma

Alexandra McAleenan et al. Cochrane Database Syst Rev. .

Abstract

Background: Complete deletion of both the short arm of chromosome 1 (1p) and the long arm of chromosome 19 (19q), known as 1p/19q codeletion, is a mutation that can occur in gliomas. It occurs in a type of glioma known as oligodendroglioma and its higher grade counterpart known as anaplastic oligodendroglioma. Detection of 1p/19q codeletion in gliomas is important because, together with another mutation in an enzyme known as isocitrate dehydrogenase, it is needed to make the diagnosis of an oligodendroglioma. Presence of 1p/19q codeletion also informs patient prognosis and prediction of the best drug treatment. The main two tests in use are fluorescent in situ hybridisation (FISH) and polymerase chain reaction (PCR)-based loss of heterozygosity (LOH) assays (also known as PCR-based short tandem repeat or microsatellite analysis). Many other tests are available. None of the tests is perfect, although PCR-based LOH is expected to have very high sensitivity.

Objectives: To estimate the sensitivity and specificity and cost-effectiveness of different deoxyribonucleic acid (DNA)-based techniques for determining 1p/19q codeletion status in glioma.

Search methods: We searched MEDLINE, Embase and BIOSIS up to July 2019. There were no restrictions based on language or date of publication. We sought economic evaluation studies from the results of this search and using the National Health Service Economic Evaluation Database.

Selection criteria: We included cross-sectional studies in adults with glioma or any subtype of glioma, presenting raw data or cross-tabulations of two or more DNA-based tests for 1p/19q codeletion. We also sought economic evaluations of these tests.

Data collection and analysis: We followed procedures outlined in the Cochrane Handbook for Diagnostic Test Accuracy Reviews. Two review authors independently screened titles/abstracts/full texts, performed data extraction, and undertook applicability and risk of bias assessments using QUADAS-2. Meta-analyses used the hierarchical summary ROC model to estimate and compare test accuracy. We used FISH and PCR-based LOH as alternate reference standards to examine how tests compared with those in common use, and conducted a latent class analysis comparing FISH and PCR-based LOH. We constructed an economic model to evaluate cost-effectiveness.

Main results: We included 53 studies examining: PCR-based LOH, FISH, single nucleotide polymorphism (SNP) array, next-generation sequencing (NGS), comparative genomic hybridisation (CGH), array comparative genomic hybridisation (aCGH), multiplex-ligation-dependent probe amplification (MLPA), real-time PCR, chromogenic in situ hybridisation (CISH), mass spectrometry (MS), restriction fragment length polymorphism (RFLP) analysis, G-banding, methylation array and NanoString. Risk of bias was low for only one study; most gave us concerns about how patients were selected or about missing data. We had applicability concerns about many of the studies because only patients with specific subtypes of glioma were included. 1520 participants contributed to analyses using FISH as the reference, 1304 participants to analyses involving PCR-based LOH as the reference and 262 participants to analyses of comparisons between methods from studies not including FISH or PCR-based LOH. Most evidence was available for comparison of FISH with PCR-based LOH (15 studies, 915 participants): PCR-based LOH detected 94% of FISH-determined codeletions (95% credible interval (CrI) 83% to 98%) and FISH detected 91% of codeletions determined by PCR-based LOH (CrI 78% to 97%). Of tumours determined not to have a deletion by FISH, 94% (CrI 87% to 98%) had a deletion detected by PCR-based LOH, and of those determined not to have a deletion by PCR-based LOH, 96% (CrI 90% to 99%) had a deletion detected by FISH. The latent class analysis suggested that PCR-based LOH may be slightly more accurate than FISH. Most other techniques appeared to have high sensitivity (i.e. produced few false-negative results) for detection of 1p/19q codeletion when either FISH or PCR-based LOH was considered as the reference standard, although there was limited evidence. There was some indication of differences in specificity (false-positive rate) with some techniques. Both NGS and SNP array had high specificity when considered against FISH as the reference standard (NGS: 6 studies, 243 participants; SNP: 6 studies, 111 participants), although we rated certainty in the evidence as low or very low. NGS and SNP array also had high specificity when PCR-based LOH was considered the reference standard, although with much more uncertainty as these results were based on fewer studies (just one study with 49 participants for NGS and two studies with 33 participants for SNP array). G-banding had low sensitivity and specificity when PCR-based LOH was the reference standard. Although MS had very high sensitivity and specificity when both FISH and PCR-based LOH were considered the reference standard, these results were based on only one study with a small number of participants. Real-time PCR also showed high specificity with FISH as a reference standard, although there were only two studies including 40 participants. We found no relevant economic evaluations. Our economic model using FISH as the reference standard suggested that the resource-optimising test depends on which measure of diagnostic accuracy is most important. With FISH as the reference standard, MLPA is likely to be cost-effective if society was willing to pay GBP 1000 or less for a true positive detected. However, as the value placed on a true positive increased, CISH was most cost-effective. Findings differed when the outcome measure changed to either true negative detected or correct diagnosis. When PCR-based LOH was used as the reference standard, MLPA was likely to be cost-effective for all measures of diagnostic accuracy at lower threshold values for willingness to pay. However, as the threshold values increased, none of the tests were clearly more likely to be considered cost-effective.

Authors' conclusions: In our review, most techniques (except G-banding) appeared to have good sensitivity (few false negatives) for detection of 1p/19q codeletions in glioma against both FISH and PCR-based LOH as a reference standard. However, we judged the certainty of the evidence low or very low for all the tests. There are possible differences in specificity, with both NGS and SNP array having high specificity (fewer false positives) for 1p/19q codeletion when considered against FISH as the reference standard. The economic analysis should be interpreted with caution due to the small number of studies.

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Conflict of interest statement

AM: none HEJ: none AK: none TR: none LS: none SD: none CK: none ESL: none CLF: none AP: none CW: none SJ: none SB: none LV: none JPTH: none KMK: none

Figures

1
1
Combinations of chromosomal deletions in oligodendrogliomas and the corresponding signals in fluorescent in situ hybridisation (FISH) in a schematic representation. In all parts of the figure, chromosome 1 and chromosome 19 are presented in separate frames to visualise the combination of FISH signals. The 1p probes and the 19q probes are red, and the reference probes (1q and 19p) are green. The approximate labelling sites are indicated in the chromosomal schematics. An unrelated chromosome (2) is also shown. Below each frame a schematic representation of the nuclear hybridisation signals as they appear on FISH images. (A): normal cell with diploid set of chromosomes. There are two red signals each, for chromosomal arms 1p and 19q, as well as two green signals each for chromosomal arms 1q and 19p. (B): the most common constellation in oligodendrogliomas with absolute 1p/19q codeletion in a diploid set of chromosomes. Loss of one red signal in chromosome 1p and in 19q and two green signals for each 1q and 19p. (C): relative codeletion with example of polysomy of chromosome 19 and chromosome 2. (D): 1p/19q codeletion in tetraploid cells, resulting in two red and four green signals for both, 1p and 19q tests. (E): complex deletion patterns can be found in a small proportion of oligodendrogliomas, often associated with anaplastic histological types. In this example, there are diploid cells (left, 30%), triploid cells (centre, 30%) and tetraploid cells (right, 40%).
2
2
PRISMA flow chart.
3
3
Network plot of the included studies. The size of the circles represents the number of test results for a test category. The thickness of the lines is proportional to the number of studies making the comparison. Note that the FISH and PCR circles include comparison within test categories. aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; CISH: chromogenic in situ hybridisation; FISH: fluorescence in situ hybridisation; LOH: loss of heterozygosity; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; NGS: next‐generation sequencing; PCR: polymerase chain reaction; RFLP: restriction fragment length polymorphism; RT: real‐time; SNP: single nucleotide polymorphism.
4
4
Graphical representation of regions analysed in studies comparing four tests (panel A) and studies comparing three tests (panel B), as listed in Appendix 6 (Tables A6.1 and A6.2). The top of the figure indicates a graphical representation of chromosome 1 (adapted from the GRCh38/hg38 assembly). The figure legend indicates the different methods, with different colour codes for FISH, depending on the origin or manufacturer of the probes. In each section, the first author of the study is represented on top, and the techniques on the left of the table. The graphical representation indicates the position of the probe or primer on the chromosome. aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; CISH: chromogenic in situ hybridisation; FISH: fluorescence in situ hybridisation; LOH: loss of heterozygosity; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; NGS: next‐generation sequencing; PCR: polymerase chain reaction; RT‐PCR: real‐time polymerase chain reaction; SNP: single nucleotide polymorphism.
5
5
Graphical representation of regions analysed in studies comparing two tests, as listed in Appendix 6 (Table A6.3). For legend to symbols, see Figure 4. Studies that are already represented in the three‐ or four‐test comparisons are omitted (see footnotes). Studies comparing FISH with FISH used different parameters, see Table A6.3 for details. aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; CISH: chromogenic in situ hybridisation; FISH: fluorescence in situ hybridisation; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; NGS: next‐generation sequencing; PCR: polymerase chain reaction; SNP: single nucleotide polymorphism.
6
6
Comparative listing of all studies using FISH (panel A) and all studies using PCR‐based LOH (panel B). Studies appear in alphabetical order of first author. For legend to symbols, see Figure 4. FISH: fluorescence in situ hybridisation; PCR: polymerase chain reaction.
7
7
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; CISH: chromogenic in situ hybridisation; FISH: fluorescence in situ hybridisation; LOH: loss of heterozygosity; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; NGS: next‐generation sequencing; PCR: polymerase chain reaction; RFLP: restriction fragment length polymorphism; SNP: single nucleotide polymorphism. Note: Horbinski 2012 used two FISH variants. The judgements for variant 1 are shown (cut‐off: target‐ploidy control ratio was less than 0.87, with at least 20% of nuclei showing deletion). Hatanpaa 2003a and Hatanpaa 2003b used two PCR‐based LOH variants. The judgements shown are for PCR compared with normal DNA.
8
8
Forest plot of tests: 1 PCR‐based LOH (against FISH), 2 SNP array (against FISH), 3 NGS (against FISH), 4 CGH (against FISH), 5 aCGH (against FISH), 6 MLPA (against FISH), 7 real‐time PCR (against FISH), 8 CISH (against FISH), 9 MS (against FISH), 10 NanoString (against FISH). aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; CI: confidence interval; CISH: chromogenic in situ hybridisation; FISH: fluorescence in situ hybridisation; FN: false negative; FP: false positive; LOH: loss of heterozygosity; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; PCR: polymerase chain reaction; SNP: single nucleotide polymorphism; TN: true negative; TP: true positive.
9
9
Receiver operating characteristic plots obtained using FISH as the reference standard (panel A) and PCR‐based LOH as the reference standard (panel B) for tests with four or more studies and variation in both sensitivity and specificity. Summary estimates of sensitivity and specificity with 95% credible regions are included along with a hierarchical summary receiver operating characteristic (HSROC) line. CGH: comparative genomic hybridisation; FISH: fluorescence in situ hybridisation; LOH: loss of heterozygosity; PCR: polymerase chain reaction; SNP: single nucleotide polymorphism.
1
1. Test
CISH (against FISH)
2
2. Test
PCR‐based LOH (against FISH)
3
3. Test
Real‐time PCR (against FISH)
4
4. Test
MLPA (against FISH)
5
5. Test
CGH (against FISH)
6
6. Test
aCGH (against FISH)
7
7. Test
SNP array (against FISH)
8
8. Test
NGS (against FISH)
9
9. Test
MS (against FISH)
10
10. Test
NanoString (against FISH)
10
10
Forest plot of tests: 11 FISH (against PCR‐based LOH), 12 CGH (against PCR‐based LOH), 13 aCGH (against PCR‐based LOH), 14 SNP array (against PCR‐based LOH), 15 NGS (against PCR‐based LOH), 16 G‐banding (against PCR‐based LOH), 17 MLPA (against PCR‐based LOH), 18 real‐time PCR (against PCR‐based LOH), 19 MS (against PCR‐based LOH). aCGH: array comparative genomic hybridisation; CGH: comparative genomic hybridisation; FISH: fluorescence in situ hybridisation; FN: false negative; FP: false positive; LOH: loss of heterozygosity; MLPA: multiplex‐ligation‐dependent probe amplification; MS; mass spectrometry; NGS: next‐generation sequencing; PCR: polymerase chain reaction; SNP: single nucleotide polymorphism; TN: true negative; TP: true positive.
11
11. Test
FISH (against PCR‐based LOH)
12
12. Test
Real‐time PCR (against PCR‐based LOH)
13
13. Test
MLPA (against PCR‐based LOH)
14
14. Test
CGH (against PCR‐based LOH)
15
15. Test
aCGH (against PCR‐based LOH)
16
16. Test
SNP array (against PCR‐based LOH)
17
17. Test
NGS (against PCR‐based LOH)
18
18. Test
MS (against PCR‐based LOH)
19
19. Test
G‐banding (against PCR‐based LOH)
20
20. Test
CGH (against MLPA)
21
21. Test
Methylation array (against MLPA)
22
22. Test
G‐banding (against CGH)
23
23. Test
G‐banding (against RFLP)
11
11
Economic model CISH: chromogenic in situ hybridisation; MLPA: multiplex‐ligation‐dependent probe amplification; RT‐PCR: real‐time polymerase chain reaction.
12
12
Risk of bias and applicability concerns summary for studies that assessed at least two FISH variants: review authors' judgements about each domain for each included study. Note: the judgements for FISH variant 1 for Horbinski 2012 are shown in Figure 7. FISH: fluorescence in situ hybridisation.
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References

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    1. Lhotska H.Unbalanced changes in cancer cells genome and its role in cancer pathogenesis [PhD thesis] [Nebalancované zm?ny v genomu nádorových bun?k a jejich úloha v patogenezi onemocn?ní]. Prague (Czech Republic): Univerzita Karlova, 2017.
Mohapatra 2006 {published data only}
    1. Mohapatra G, Betensky RA, Miller ER, Carey B, Gaumont LD, Engler DA, et al.Glioma test array for use with formalin-fixed, paraffin-embedded tissue: array comparative genomic hybridization correlates with loss of heterozygosity and fluorescence in situ hybridization. 97th Annual Meeting of the American Association for Cancer Research; 2006 April 1-5; Washington (DC). - PMC - PubMed
    1. Mohapatra G, Betensky RA, Miller ER, Carey B, Gaumont LD, Engler DA, et al.Glioma test array for use with formalin-fixed, paraffin-embedded tissue: array comparative genomic hybridization correlates with loss of heterozygosity and fluorescence in situ hybridization. Journal of Molecular Diagnostics 2006;8(2):268-76. - PMC - PubMed
Na 2019 {published data only}
    1. Na K, Kim HS, Shim HS, Chang JH, Kang SG, Kim SH.Targeted next-generation sequencing panel (TruSight Tumor 170) in diffuse glioma: a single institutional experience of 135 cases. Journal of Neuro-Oncology 2019;142(3):445-54. - PubMed
Natte 2005 {published data only}
    1. Natte R, Eijk R, Eilers P, Cleton-Jansen AM, Oosting J, Kouwenhove M, et al.Multiplex ligation-dependent probe amplification for the detection of 1p and 19q chromosomal loss in oligodendroglial tumors. Brain Pathology 2005;15(3):192-7. - PMC - PubMed
Nigro 2001 {published data only}
    1. Nigro JM, Takahashi MA, Ginzinger DG, Law M, Passe S, Jenkins RB, et al.Detection of 1p and 19q loss in oligodendroglioma by quantitative microsatellite analysis, a real-time quantitative polymerase chain reaction assay. American Journal of Pathology 2001;158(4):1253-62. - PMC - PubMed
Park 2019 {published data only}
    1. Park H, Chun SM, Shim J, Oh JH, Cho EJ, Hwang HS, et al.Detection of chromosome structural variation by targeted next-generation sequencing and a deep learning application. Scientific Reports 2019;9(1):3644. - PMC - PubMed
Paxton 2015 {published data only}
    1. Paxton CN, Rowe LR, South ST.Observations of the genomic landscape beyond 1p19q deletions and EGFR amplification in Glioma. Cytogenetic and Genome Research 2014;142(3):247. - PMC - PubMed
    1. Paxton CN, Rowe LR, South ST.Observations of the genomic landscape beyond 1p19q deletions and EGFR amplification in glioma. Molecular Cytogenetics 2015;8:60. - PMC - PubMed
Pesenti 2017 {published data only}
    1. Pesenti C, Paganini L, Fontana L, Veniani E, Runza L, Ferrero S, et al.Mass spectrometry-based assay for the molecular diagnosis of glioma: concomitant detection of chromosome 1p/19q codeletion, and IDH1, IDH2, and TERT mutation status. Oncotarget 2017;8(34):57134-48. - PMC - PubMed
Ransom 1992a {published data only}
    1. Ransom DT, Ritland SR, Kimmel DW, Moertel CA, Dahl RJ, Scheithauer BW, et al.Cytogenetic and loss of heterozygosity studies in ependymomas, pilocytic astrocytomas, and oligodendrogliomas. Genes Chromosomes and Cancer 1992;5(4):348-56. - PubMed
Ransom 1992b {published data only}
    1. Ransom DT, Ritland SR, Moertel CA, Dahl RJ, O'Fallon JR, Scheithauer BW, et al.Correlation of cytogenetic analysis and loss of heterozygosity studies in human diffuse astrocytomas and mixed oligo-astrocytomas. Genes Chromosomes and Cancer 1992;5(4):357-74. - PubMed
Scheie 2006 {published data only}
    1. Scheie D, Andresen PA, Cvancarova M, Bo AS, Helseth E, Skullerud K, et al.Fluorescence in situ hybridization (FISH) on touch preparations: a reliable method for detecting loss of heterozygosity at 1p and 19q in oligodendroglial tumors. American Journal of Surgical Pathology 2006;30(7):828-37. - PubMed
    1. Scheie D.1p/19q loss in oligodendroglial tumors-methodological, histological, radiological and clinical aspects. Clinical Neuropathology 2012;31(6):464.
    1. Scheie D.1p/19q-loss in Oligodendroglial Tumours. Methodological, Histological, Radiological and Clinical Aspects [PhD thesis]. Oslo (Norway): University of Oslo, 2012. [ISBN:9788282641883]
Schrock 1994 {published data only}
    1. Schrock E, Thiel G, Lozanova T, du Manoir S, Meffert MC, Jauch A, et al.Comparative genomic hybridization of human malignant gliomas reveals multiple amplification sites and nonrandom chromosomal gains and losses. American Journal of Pathology 1994;144(6):1203-18. - PMC - PubMed
Senetta 2013 {published data only}
    1. Senetta R, Verdun di Cantogno L, Chiusa L, Castellano I, Gugliotta P, Sapino A, et al.A "weighted" fluorescence in situ hybridization strengthens the favorable prognostic value of 1p/19q codeletion in pure and mixed oligodendroglial tumors. Journal of Neuropathology & Experimental Neurology 2013;72(5):432-41. - PMC - PubMed
Sim 2018a {published data only}
    1. Sim J, Nam DH, Kim Y, Lee IH, Choi JW, Sa JK, et al.Comparison of 1p and 19q status of glioblastoma by whole exome sequencing, array-comparative genomic hybridization, and fluorescence in situ hybridization. Medical Oncology 2018;35(5):60. - PubMed
    1. Suh YL, Sim J.Comparison of 1p19q status by FISH and whole exome sequencing and/or array-CGH in glioblastoma. Clinical Neuropathology 2016;35(4):228.
Sim 2018b {published data only}
    1. Sim J, Nam DH, Kim Y, Lee IH, Choi JW, Sa JK, et al.Comparison of 1p and 19q status of glioblastoma by whole exome sequencing, array-comparative genomic hybridization, and fluorescence in situ hybridization. Medical Oncology 2018;35(5):60. - PubMed
    1. Suh YL, Sim J.Comparison of 1p19q status by FISH and whole exome sequencing and/or array-CGH in glioblastoma. Clinical Neuropathology 2016;35(4):228.
Smith 1999 {published data only}
    1. Smith JS, Alderete B, Minn Y, Borell TJ, Perry A, Mohapatra G, et al.Localization of common deletion regions on 1p and 19q in human gliomas and their association with histological subtype. Oncogene 1999;18(28):4144-52. - PubMed
Srebotnik‐Kirbis 2016 {published data only}
    1. Limbaeck-Stokin C, Srebotnik-Kirbis I, Zupan A, Glavac D, Popovic M.Brush cytology for FISH based detection of 1p/19q loss in oligodendroglial tumors. Clinical Neuropathology 2012;31(4):256.
    1. Srebotnik-Kirbis I, Limback-Stokin C.Application of brush cytology for FISH-based detection of 1p/19q codeletion in oligodendroglial tumors. Journal of Neuro-Oncology 2016;129(3):415-22. - PubMed
Thakur 2012 {published data only}
    1. Thakur S, Alvarez K, Weindel M, Li MM, Monzon FA.Validation of affymetrix 250K Nsp arrays for clinical use in the evaluation of genomic copy number alteration and loss of heterozygosity in cancer. Journal of Molecular Diagnostics 2012;14(6):707-8.
Thomas 2017 {published data only}
    1. Thomas AA, Abrey LE, Terziev R, Raizer J, Martinez NL, Forsyth P, et al.Multicenter phase II study of temozolomide and myeloablative chemotherapy with autologous stem cell transplant for newly diagnosed anaplastic oligodendroglioma. Neuro-Oncology 2017;19(10):1380-90. - PMC - PubMed
Tsiatis 2010 {published data only}
    1. Tsiatis AC, Hafez MJ, Jedlicka AE, Maitra A, Murphy KM, Eshleman JR.Use of SNP arrays to assess loss of heterozygosity in gliomas. 101st Annual Meeting of American Association for Cancer Research; 2010 April 17-21; Washington (DC). [DOI: 10.1158/1538-7445.AM10-1781] - DOI
Uchida 2019 {published data only}
    1. Uchida H, Yonezawa H, Hirano H, Yoshimoto K.Usefulness and pitfalls of 1p/ 19q-codeletion analysis by FISH method in glioblastoma. Brain Pathology 2019;29(Suppl 1):120.
Wiestler 2014 {published data only}
    1. Wiestler B, Capper D, Hovestadt V, Sill M, Jones D, Hartmann C, et al.Assessing CpG island methylator phenotype, 1p/19q codeletion, and MGMT promoter methylation from epigenome-wide data in the biomarker cohort of the NOA-04 trial. Neuro-Oncology 2014;16(12):1630-8. - PMC - PubMed
    1. Wiestler B, Capper D, Hovestadt V, Sill M, Jones D, Hartmann C, et al.Determining the glioma CpG island methylator phenotype, 1p/19q codeletion, and MGMT promoter methylation from epigenome-wide methylation data in the biomarker cohort of the NOA-04 trial. Journal of Clinical Oncology 2014;32:15. [DOI: 10.1200/jco.2014.32.15_suppl.2017] - DOI - PMC - PubMed

References to studies excluded from this review

Afyounian 2017 {published data only}
    1. Afyounian E, Annala M, Nykter M.Segmentum: a tool for copy number analysis of cancer genomes. BMC Bioinformatics 2017;18(1):215. - PMC - PubMed
Alentorn 2014 {published data only}
    1. Alentorn A, Thuijl HF, Marie Y, Alshehhi H, Carpentier C, Boisselier B, et al.Clinical value of chromosome arms 19q and 11p losses in low-grade gliomas. Neuro-Oncology 2014;16(3):400-8. - PMC - PubMed
Aoki 2015a {published data only}
    1. Aoki K, Suzuki H, Nakamura H, Motomura K, Mizoguchi M, Abe T, et al.Prognostic model of lower grade gliomas. Journal of Clinical Oncology 2015;33(15 Suppl 1):2038.
Aoki 2015b {published data only}
    1. Aoki K, Suzuki H, Nakamura H, Motomura K, Ohka F, Mizoguchi M, et al.Prognostic significance of genetic alterations from comprehensive analysis in lower-grade gliomas. Neuro-Oncology 2015;5:v91.
Assem 2009 {published data only}
    1. Assem M, Sibenaller Z, Marner J, Bair T, Ryken TC.Genomic profiling as a tool to improve diagnosis and treatment of malignant gliomas. Proceedings of the American Association for Cancer Research Annual Meeting 2009;50:341.
Assem 2012 {published data only}
    1. Assem M, Sibenaller Z, Agarwal S, Al-Keilani MS, Alqudah MA, Ryken TC.Enhancing diagnosis, prognosis, and therapeutic outcome prediction of gliomas using genomics. Omics a Journal of Integrative Biology 2012;16(3):113-22. - PMC - PubMed
Bady 2013 {published data only}
    1. Bady P, Kurscheid S, Delorenzi M, Hegi ME.The genetic and epigenetic context of MGMT methylation in glioma may impact the predictive and prognostic value. Neuro-Oncology 2013;3:iii141-2.
Ballester 2017 {published data only}
    1. Ballester LY, Huse JT, Tang G, Fuller GN.Molecular classification of adult diffuse gliomas: conflicting IDH1/IDH2, ATRX, and 1p/19q results. Human Pathology 2017;69:15-22. - PubMed
Becker 2017 {published data only}
    1. Becker AP, Bell EH, Fleming J, McElroy JP, Fabian D, Beyer S, et al.Comprehensive assessment of ATRX mutation, protein expression, and alternative lengthening of telomeres (ALT) phenotype in grade II and III gliomas. Journal of Clinical Oncology 2017;35(15 Suppl 1):2064.
Bienkowski 2018 {published data only}
    1. Bienkowski M, Wohrer A, Moser P, Kitzwogerer M, Ricken G, Strobel T, et al.Molecular diagnostic testing of diffuse gliomas in the real-life setting: a practical approach. Clinical Neuropathology 2018;37(4):166-77. - PMC - PubMed
Boudreau 2004 {published data only}
    1. Boudreau CR, Liau LM.Molecular characterization of brain tumors. Clinical Neurosurgery 2004;51:81-90. - PubMed
Brat 2015 {published data only}
    1. Brat DJ, Fehrenbach A, Finocchiaro G, Verhaak RG, Friedman W, Al-Dape KD, et al.Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. New England Journal of Medicine 2015;372(26):2481-98. - PMC - PubMed
Buckley 2011 {published data only}
    1. Buckley PG, Alcock L, Heffernan J, Woods J, Brett F, Stallings RL, et al.Loss of chromosome 1p/19q in oligodendroglial tumors: refinement of chromosomal critical regions and evaluation of internexin immunostaining as a surrogate marker. Journal of Neuropathology & Experimental Neurology 2011;70(3):177-82. - PubMed
Burgenske 2017 {published data only}
    1. Burgenske D, Eckel-Passow J, Decker P, Kosel M, Youland R, Remonde D, et al.Clinical and molecular analyses of long term survivors of glioblastoma. Neuro-Oncology 2017;19(Suppl 6):vi98.
Bystricka 2011 {published data only}
    1. Bystricka D, Zemanova Z, Kramar F, Lizcova L, Ransdorfova S, Dostalova-Merkerova M, et al.Genomic changes in 37 patients with low-grade diffuse gliomas. Chromosome Research 2011;1:S146-7.
Carrato 2006 {published data only}
    1. Carrato C, Beyer K, Zamora L, Granada I, Roussos I, Balana C, et al.1p/19q loss in gliomas: microsatellite amplification in comparison with FISH. Laboratory Investigation 2006;86(Suppl 1):284A.
Carrato 2010 {published data only}
    1. Carrato C, Beyer K, Md L, Domingo-Sabat M, Lopez MT, Ariza A.A rapid, user-friendly approach for distinguishing between partial and complete 1p/19q losses in gliomas. Brain Pathology 2010;1:60.
Carter 2016 {published data only}
    1. Carter JH, McNulty S, Cottrell C, Heusel J.Targeted NGS in molecular subtyping of lower-grade diffuse gliomas: application of the WHO's 2016 revised criteria for CNS tumors. Journal of Molecular Diagnostics 2016;18(6):1009. - PubMed
Castilla 2003 {published data only}
    1. Castilla EA, Prayson RA, Hartke M, Staugaitis SM, Barnett GH, Tubbs RR.Discordance in allelic losses on chromosomes 1p and 19q in gliomas. Modern Pathology 2003;16(1):289A.
Chernova 2003 {published data only}
    1. Chernova OB, Barnett GH, Cowell JK.Rapid detection of allelic losses in brain tumours using microsatellite repeat markers and high-performance liquid chromatography. British Journal of Cancer 2003;88(12):1889-93. - PMC - PubMed
Cieply 2005 {published data only}
    1. Cieply KM, Sherer C, Hunt J, Hamilton RL.Assessment of 1p and 19q status in pediatric oligodendrogliomas by FISH. Journal of Molecular Diagnostics 2005;7(5):688.
Durand 2010 {published data only}
    1. Durand KS, Guillaudeau A, Weinbreck N, De Armas R, Robert S, Chaunavel A, et al.1p19q LOH patterns and expression of p53 and Olig2 in gliomas: relation with histological types and prognosis. Modern Pathology 2010;23(4):619-28. - PubMed
Eckel‐Passow 2017 {published data only}
    1. Eckel-Passow J, Decker P, Hughes E, Kollmeyer T, Kosel M, Burgenske D, et al.Clinical sensitivity and specificity of illumina methylation array for classifying adult gliomas into who groups. Neuro-Oncology 2017;19(Suppl 6):vi181.
Fontaine 2007 {published data only}
    1. Fontaine D, Monnot S, Vandenbos F, Paquis P, Michiels JF, Bannwarth S, et al.DNA extraction by FTATM technology: application for rapid detection of 1p/19q deletions in gliomas. Neuropathology and Applied Neurobiology 2007;33(3):360-3. - PubMed
Franco‐Hernandez 2009a {published data only}
    1. Franco-Hernandez C, Martinez-Glez V, Campos JM, Isla A, Vaquero J, Gutiérrez M, et al.Allelic status of 1p and 19q in oligodendrogliomas and glioblastomas: multiplex ligation-dependent probe amplification versus loss of heterozygosity. Cancer Genetics & Cytogenetics 2009;190(2):93-6. - PubMed
Franco‐Hernandez 2009b {published data only}
    1. Franco-Hernandez C, Martinez-Glez V, Torres-Martin M, Campos JM, Isla A, Vaquero J, et al.Identification of genetic alterations by multiple ligation-dependent probe amplification (MLPA) analysis in oligodendrogliomas. Neurocirugia (Asturias, Spain) 2009;20(2):117-23. - PubMed
French 2005 {published data only}
    1. French PJ, Swagemakers SM, Nagel JH, Kouwenhoven MC, Brouwer E, van der Spek, et al.Gene expression profiles associated with treatment response in oligodendrogliomas. Cancer Research 2005;65(24):11335-44. - PubMed
Garber 2016 {published data only}
    1. Garber ST, Hashimoto Y, Weathers SP, Xiu J, Gatalica Z, Verhaak RG, et al.Immune checkpoint blockade as a potential therapeutic target: surveying CNS malignancies. Neuro-Oncology 2016;18(10):1357-66. - PMC - PubMed
Hartmann 2005 {published data only}
    1. Hartmann C, Mueller W, Lass U, Kamel-Reid S, Deimling A.Molecular genetic analysis of oligodendroglial tumors. Journal of Neuropathology & Experimental Neurology 2005;64(1):10-4. - PubMed
Hashimoto 2002 {published data only}
    1. Hashimoto N, Murakami M, Sasajima H, Takahashi Y, Mineura K.Diagnostic molecular genetics and its application to clinical decision in brain tumors. In: Watanabe K, editors(s). Developments in Neuroscience, Proceedings. 1247 edition. Amsterdam (the Netherlands): Elsevier Science Bv, 2002:221-9.
Hench 2018 {published data only}
    1. Hench J, Bihl M, Bratic Hench I, Hoffmann P, Tolnay M, Bösch Al Jadooa N, et al.Satisfying your neuro-oncologist: a fast approach to routine molecular glioma diagnostics. Neuro-Oncology 2018;20(12):1682-3. - PMC - PubMed
Horbinski 2008 {published data only}
    1. Horbinski C, Dacic S, Cieply K, Brat DJ, McClendon RE, Chu CT.Chordoid glioma: molecular characterization of four cases. Laboratory Investigation 2008;88(Suppl 1):321A.
Horbinski 2011 {published data only}
    1. Horbinski C, Nikiforova M, Hobbs J, Cieply K, Hamilton R.Prospective comparison of FISH versus PCR-based microsatellite LOH in the evaluation of gliomas for 1p/19q codeletion. Journal of Neuropathology and Experimental Neurology 2011;70(6):526.
Ida 2018 {published data only}
    1. Ida C, Zepeda-Mendoza C, Praska C, Balcom J, Swanson K, Barr Fritcher E, et al.Recurrent unusual patterns in clinical molecular profiling of adult diffuse gliomas. Journal of Neuropathology and Experimental Neurology 2018;77(6):482.
Idbaih 2008 {published data only}
    1. Idbaih A, Kouwenhoven M, Jeuken J, Carpentier C, Gorlia T, Kros JM, et al.Chromosome 1p loss evaluation in anaplastic oligodendrogliomas. Neuropathology 2008;28(4):440-3. - PubMed
Joo 2013 {published data only}
    1. Joo M, Park SH, Chang SH, Kim H, Choi CY, Lee CH, et al.Cytogenetic and molecular genetic study on granular cell glioblastoma: a case report. Human Pathology 2013;44(2):282-8. - PubMed
Juratli 2012 {published data only}
    1. Juratli TA, Kirsch M, Geiger K, Klink B, Leipnitz E, Pinzer T, et al.The prognostic value of IDH mutations and MGMT promoter status in secondary high-grade gliomas. Journal of Neuro-Oncology 2012;110(3):325-33. - PubMed
Kamoun 2015 {published data only}
    1. Kamoun A, Ducray F, Dehais C, Idbaih A, Elarouci N, Letouze E, et al.Integrated genomic analysis of oligodendroglial tumors identifies distinct molecular subgroups within 1p/19q co-deleted oligodendrogliomas. Neuro-Oncology 2015;5:v95.
Kashofer 2018 {published data only}
    1. Kashofer K, Halbwedl I, Winter E, Hoefler G, Asslaber M.Expanding on WHO guideline compliant molecular testing of central nervous system tumours by low density whole genome sequencing. Virchows Archiv 2018;473(Suppl 1):s28.
Kim 2016 {published data only}
    1. Kim L, Xiu J, Judy K, Evans J, Andrews D, Farrell C.Results of molecular profiling for recurrent malignant gliomas reveal significant changes in biomarkers compared to mostly treatment naive tumors that could impact treatment decision. Neuro-Oncology 2016;18(Suppl 6):vi117-8.
Kitange 2004 {published data only}
    1. Kitange GJ, Misra A, Law M, Passe S, Kollymeyer T, Mauer M, et al.Analysis of genetic dosage anomalies using comparative genomic hybridization array (CGHa) in human oligodendrogliomas. Proceedings of the American Association for Cancer Research Annual Meeting 2004;45:386.
Kitange 2005 {published data only}
    1. Kitange G, Misra A, Law M, Passe S, Kollmeyer TM, Maurer M, et al.Chromosomal imbalances detected by array comparative genomic hybridization in human oligodendrogliomas and mixed oligoastrocytomas. Genes, Chromosomes & Cancer 2005;42(1):68-77. - PubMed
Klink 2010 {published data only}
    1. Klink B, Schlingelhof B, Klink M, Stout-Weider K, Patt S, Schrock E.Glioblastomas with oligodendroglial component – common origin of the different histological parts and genetic subclassification. Analytical Cellular Pathology 2010;33(1):37-54. - PMC - PubMed
Klink 2011 {published data only}
    1. Klink B, Schlingelhof B, Klink M, Stout-Weider K, Patt S, Schrock E.Glioblastomas with oligodendroglial component-common origin of the different histological parts and genetic subclassification. Cellular Oncology 2011;34(3):261-75. - PubMed
Kouwenhoven 2009 {published data only}
    1. Kouwenhoven MC, Gorlia T, Kros JM, Ibdaih A, Brandes AA, Bromberg JE, et al.Molecular analysis of anaplastic oligodendroglial tumors in a prospective randomized study: a report from EORTC study 26951. Neuro-Oncology 2009;11(6):737-46. - PMC - PubMed
Kuo 2009 {published data only}
    1. Kuo LT, Kuo KT, Lee MJ, Wei CC, Scaravilli F, Tsai JC, et al.Correlation among pathology, genetic and epigenetic profiles, and clinical outcome in oligodendroglial tumors. International Journal of Cancer 2009;124(12):2872-9. - PubMed
Kuo 2013 {published data only}
    1. Kuo LT, Tsai SY, Chang CC, Kuo KT, Huang AP, Tsai JC, et al.Genetic and epigenetic alterations in primary-progressive paired oligodendroglial tumors. PLoS One 2013;8(6):e67139. - PMC - PubMed
Kwon 2019 {published data only}
    1. Kwon MJ, Suh YL, Cho H, Kang SY.Molecular subgrouping of gliomatosis cerebri according to the 2016 World Health Organization classification of tumors of the central nervous system. Brain Pathology 2019;29(Suppl 1):43-4.
Lautenschlaeger 2013 {published data only}
    1. Lautenschlaeger T, Juratli TA, McElroy J, Meng W, Huebner A, Geiger KD, et al.Genome-wide CNV analysis identifies loci putatively associated with delayed time to first recurrence in IDH-mutant low-grade astrocytomas. Neuro-Oncology 2013;3:iii145.
Levine 2018 {published data only}
    1. Levine AB, Yip S.Implementation of the 2016 who classification for infiltrating glioma: the VGH experience. Laboratory Investigation 2018;98(Suppl 1):660.
Liu 2014 {published data only}
    1. Liu EZ, Abreu FB, Hickey WF, Ronan LK, Fadul CE, Otis L, et al.Development of a 1p19q LOH assay for glioma patients using capillary electrophoresis. Journal of Molecular Diagnostics 2014;16(6):789.
Magnani 2003 {published data only}
    1. Magnani I, Moroni RF, Beghini A, Larizza L.Multiple alterations of chromosome arms 1p and 19q detected by FISH analysis correlate with LOH heterogeneity in gliomas. Annales de Genetique 2003;46(2-3):165.
Martinez 2005 {published data only}
    1. Martinez R, Schackert HK, Kirsch M, Paulus W, Joos S, Schackert G.Comparative genetic analysis of metachronous anaplastic oligoastrocytomas with extended recurrence-free interval. Journal of Neuro-Oncology 2005;72(2):95-102. - PubMed
Marucci 2012 {published data only}
    1. Marucci G, Di Oto, Farnedi A, Panzacchi R, Ligorio C, Foschini MP.Nogo-A: a useful marker for the diagnosis of oligodendroglioma and for identifying 1p19q codeletion. Human Pathology 2012;43(3):374-80. - PubMed
McDonald 2005 {published data only}
    1. McDonald JM, See SJ, Tremont IW, Colman H, Gilbert MR, Groves M, et al.The prognostic impact of histology and 1p/19q status in anaplastic oligodendroglial tumors. Cancer 2005;104(7):1468-77. - PubMed
Mohapatra 2011 {published data only}
    1. Mohapatra G, Engler DA, Starbuck KD, Kim JC, Bernay DC, Scangas GA, et al.Genome-wide comparison of paired fresh frozen and formalin-fixed paraffin-embedded gliomas by custom BAC and oligonucleotide array comparative genomic hybridization: facilitating analysis of archival gliomas. Acta Neuropathologica 2011;121(4):529-43. - PMC - PubMed
Molinari 2010 {published data only}
    1. Molinari C, Iorio P, Medri L, Ballardini M, Guiducci G, Cremonini AM, et al.Chromosome 1p and 19q evaluation in low-grade oligodendrogliomas: a descriptive study. International Journal of Molecular Medicine 2010;25(1):145-51. - PubMed
Mrachek 2018 {published data only}
    1. Mrachek EK, Batchala P, Patel S, Fadul C, Schiff D, Williams E, et al.Neuroradiology concordance with neuropathology in predicting 1p/19q-codeletion in IDH-mutant lower-grade gliomas. Journal of Neuropathology and Experimental Neurology 2018;77(6):483.
Mur 2013 {published data only}
    1. Mur P, Mollejo M, Ruano Y, Lope AR, Fiano C, García JF, et al.Codeletion of 1p and 19q determines distinct gene methylation and expression profiles in IDH-mutated oligodendroglial tumors. Acta Neuropathologica 2013;126(2):277-89. - PubMed
Myung 2011 {published data only}
    1. Myung JK, Byeon SJ, Kim B, Suh J, Kim SK, Park CK, et al.Papillary glioneuronal tumors: a review of clinicopathologic and molecular genetic studies. American Journal of Surgical Pathology 2011;35(12):1794-805. - PubMed
Narasimhaiah 2010 {published data only}
    1. Narasimhaiah DA, Godfraind C.Fluorescence in situ hybridization (FISH) for 1p/19q in oligodendrogliomas – the need for consensus criteria and uniform guidelines. Brain Pathology 2010;1:55.
Neill 2015 {published data only}
    1. Neill S, Hill K, Adewumi D, Holder C, Rossi M, Schniederjan M.Disseminated oligodendroglioma-like leptomeningeal neoplasm in a 31 year-old patient. Journal of Neuropathology and Experimental Neurology 2015;74(6):635.
Nielsen 2007 {published data only}
    1. Nielsen KV, Rasmussen BB, Balslev E, Poulsen TS, Schonau A, Ejlertsen B.Loss of heterozygosity on chromosomes 1 and 19 in primary brain tumors. Ugeskrift for Laeger 2007;169(2):147. - PubMed
Parizi‐Robinson 2004 {published data only}
    1. Parizi-Robinson M, Hatanpaa K, Yegappan M, Siegelman MH.Molecular diagnosis of oligodendrogliomas using capillary electrophoresis to detect loss of heterozygosity on chromosomes 1p and 19q. Journal of Molecular Diagnostics 2004;6(4):428.
Payne 2008 {published data only}
    1. Payne C, Parkinson J, Cook R, Wheeler H, Robinson B, McDonald K.Oligodendrogliomas with LOH 1P/19Q: identifying genes associated with therapeutic sensitivity. Neuro-Oncology 2008;10(5):802.
Pekmezci 2016 {published data only}
    1. Pekmezci M, Walsh KM, Molinaro A, Decker PA, Hansen HM, Sicotto H, et al.Molecularly defined adult gliomas with known ATRX status: does TERT have an additional prognostic role. Laboratory Investigation 2016;1:435A.
Pietsch 2015 {published data only}
    1. Pietsch T, Gessi M, Muhlen A, Dörner E, Last A, Sundar P.Implementation of next generation copy number and mutational analysis in routine neuropathology: molecular inversion profiling is a helpful tool in differential diagnostics and prognostification of pediatric brain tumors. Neuro-Oncology 2015;3:iii30-iii.
Pina‐Oviedo 2012 {published data only}
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References to ongoing studies

ACTRN12618000006246 {unpublished data only}
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