Role of traditional CHO PET parameters in distinguishing IDH, TERT and MGMT alterations in primary diffuse gliomas

Springer Science and Business Media LLC - Tập 35 - Trang 493-503 - 2021
Ziren Kong1,2, Yucheng Zhang3, Delin Liu2, Penghao Liu1, Yixin Shi2, Yaning Wang1, Dachun Zhao4, Xin Cheng2, Yu Wang1, Wenbin Ma1
1Department of Neurosurgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
2Department of Nuclear Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
3Institute of Nuclear and New Energy Technology, Tsinghua University, Beijing, China
4Department of Pathology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

Tóm tắt

Isocitrate dehydrogenase (IDH) mutation, telomerase reverse transcriptase (TERT) promoter mutation and O6-methylguanine-DNA methyltransferase (MGMT) promoter methylation status are diagnostic, prognostic, predictive and therapeutic biomarkers for primary diffuse gliomas, and this study aimed to explore the relationship between choline (CHO) positron emission tomography (PET) parameters and these molecular alterations. Twenty-eight patients who were histopathologically diagnosed with primary diffuse glioma and underwent presurgical CHO PET/CT were retrospectively analyzed, and IDH, TERT and MGMT alterations were examined. The volume of interest (VOI) was semiautomatically defined based on standardized uptake value (SUV) thresholds, and 5 traditional CHO parameters, namely, SUVmax, SUVmean, metabolic tumor volume (MTV), total lesion CHO uptake (TLC) and tumor-to-normal contralateral cortex activity ratio (T/N ratio), were calculated. Wilcoxon rank-sum tests and receiver operating characteristic (ROC) curves were applied to evaluate the differences and performances of the CHO parameters, and their capability to stratify patient prognosis was also evaluated. All 5 parameters were significantly higher in IDH-wildtype gliomas than in IDH-mutant gliomas (p = 0.0001–0.037), and SUVmax, SUVmean, TLC and the T/N ratio exhibited good performances in distinguishing the IDH status (areas under the ROC curve (AUCs) 0.856–0.918, accuracies 0.857–0.893) as well as stratifying patient prognosis. Although the differences and performances of the traditional parameters in distinguishing diverse TERT and MGMT statuses were moderate in the whole population, the T/N ratio and TLC displayed certain predictive value in discriminating the TERT status in the IDH-mutant and IDH-wildtype subgroups (p = 0.028–0.048, AUCs 0.857–0.860, accuracies 0.800–0.917, respectively). Traditional CHO PET parameters are capable of distinguishing IDH but not TERT or MGMT alterations in the whole population. In accordance with the clinical understanding of TERT promoter mutations, the T/N ratio and TLC can also discriminate the TERT status in IDH subgroups.

Tài liệu tham khảo

Lapointe S, Perry A, Butowski NA. Primary brain tumours in adults. Lancet. 2018;392:432–46. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370:699–708. Wick W, Roth P, Hartmann C, Hau P, Nakamura M, Stockhammer F, et al. Long-term analysis of the NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with PCV or temozolomide. Neuro Oncol. 2016;18:1529–37. Buckner JC, Shaw EG, Pugh SL, Chakravarti A, Gilbert MR, Barger GR, et al. Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med. 2016;374:1344–55. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 world health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–20. Waitkus MS, Diplas BH, Yan H. Isocitrate dehydrogenase mutations in gliomas. Neuro Oncol. 2016;18:16–26. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360:765–73. Arita H, Narita Y, Takami H, Fukushima S, Matsushita Y, Yoshida A, et al. TERT promoter mutations rather than methylation are the main mechanism for TERT upregulation in adult gliomas. Acta Neuropathol. 2013;126:939–41. Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, et al. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med. 2015;372:2481–98. Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med. 2015;372:2499–508. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003. Arita H, Yamasaki K, Matsushita Y, Nakamura T, Shimokawa A, Takami H, et al. A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas. Acta Neuropathol Commun. 2016;4:79. Kim MM, Parolia A, Dunphy MP, Venneti S. Non-invasive metabolic imaging of brain tumours in the era of precision medicine. Nat Rev Clin Oncol. 2016;13:725–39. Giovannini E, Lazzeri P, Milano A, Gaeta MC, Ciarmiello A. Clinical applications of choline PET/CT in brain tumors. Curr Pharm Des. 2015;21:121–7. Hara T, Kosaka N, Shinoura N, Kondo T. PET imaging of brain tumor with [methyl-11C]choline. J Nucl Med. 1997;38:842–7. Ohtani T, Kurihara H, Ishiuchi S, Saito N, Oriuchi N, Inoue T, et al. Brain tumour imaging with carbon-11 choline: comparison with FDG PET and gadolinium-enhanced MR imaging. Eur J Nucl Med. 2001;28:1664–70. Tian M, Zhang H, Oriuchi N, Higuchi T, Endo K. Comparison of 11C-choline PET and FDG PET for the differential diagnosis of malignant tumors. Eur J Nucl Med Mol Imaging. 2004;31:1064–72. Kato T, Shinoda J, Nakayama N, Miwa K, Okumura A, Yano H, et al. Metabolic assessment of gliomas using 11C-methionine, [18F] fluorodeoxyglucose, and 11C-choline positron-emission tomography. AJNR Am J Neuroradiol. 2008;29:1176–82. Garcia Vicente AM, Perez-Beteta J, Amo-Salas M, Pena Pardo FJ, Villena Martin M, Sandoval Valencia H, et al. 18F-Fluorocholine PET/CT in the prediction of molecular subtypes and prognosis for gliomas. Clin Nucl Med. 2019;44:e548–58. Takei H, Shinoda J, Ikuta S, Maruyama T, Muragaki Y, Kawasaki T, et al. Usefulness of positron emission tomography for differentiating gliomas according to the 2016 World Health Organization classification of tumors of the central nervous system. J Neurosurg. 2019;133:1010–9. Hara T, Kosaka N, Kishi H. Development of 18F-fluoroethylcholine for cancer imaging with PET: synthesis, biochemistry, and prostate cancer imaging. J Nucl Med. 2002;43:187–99. Horbinski C, Kofler J, Kelly LM, Murdoch GH, Nikiforova MN. Diagnostic use of IDH1/2 mutation analysis in routine clinical testing of formalin-fixed, paraffin-embedded glioma tissues. J Neuropathol Exp Neurol. 2009;68:1319–25. Chan AK, Yao Y, Zhang Z, Chung NY, Liu JS, Li KK, et al. TERT promoter mutations contribute to subset prognostication of lower-grade gliomas. Mod Pathol. 2015;28:177–86. Reifenberger G, Hentschel B, Felsberg J, Schackert G, Simon M, Schnell O, et al. Predictive impact of MGMT promoter methylation in glioblastoma of the elderly. Int J Cancer. 2012;131:1342–50. Fedorov A, Beichel R, Kalpathy-Cramer J, Finet J, Fillion-Robin JC, Pujol S, et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging. 2012;30:1323–41. Yang P, Cai J, Yan W, Zhang W, Wang Y, Chen B, et al. Classification based on mutations of TERT promoter and IDH characterizes subtypes in grade II/III gliomas. Neuro Oncol. 2016;18:1099–108. Mellinghoff IK, Ellingson BM, Touat M, Maher E, De La Fuente MI, Holdhoff M, et al. Ivosidenib in isocitrate dehydrogenase 1-mutated advanced glioma. J Clin Oncol. 2020;2020:1903327. Molinaro AM, Hervey-Jumper S, Morshed RA, Young J, Han SJ, Chunduru P, et al. Association of maximal extent of resection of contrast-enhanced and non-contrast-enhanced tumor with survival within molecular subgroups of patients with newly diagnosed glioblastoma. JAMA Oncol. 2020;6:495–503. Kong Z, Jiang C, Zhang Y, Liu S, Liu D, Liu Z, et al. Thin-slice magnetic resonance imaging-based radiomics signature predicts chromosomal 1p/19q Co-deletion status in Grade II and III Gliomas. Front Neurol. 2020;11:551771. Arita H, Narita Y, Fukushima S, Tateishi K, Matsushita Y, Yoshida A, et al. Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Acta Neuropathol. 2013;126:267–76. Arita H, Matsushita Y, Machida R, Yamasaki K, Hata N, Ohno M, et al. TERT promoter mutation confers favorable prognosis regardless of 1p/19q status in adult diffuse gliomas with IDH1/2 mutations. Acta Neuropathol Commun. 2020;8:201. Brat DJ, Aldape K, Colman H, Holland EC, Louis DN, Jenkins RB, et al. cIMPACT-NOW update 3: recommended diagnostic criteria for “Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV.” Acta Neuropathol. 2018;136:805–10. Gorlia T, van den Bent MJ, Hegi ME, Mirimanoff RO, Weller M, Cairncross JG, et al. Nomograms for predicting survival of patients with newly diagnosed glioblastoma: prognostic factor analysis of EORTC and NCIC trial 26981–22981/CE3. Lancet Oncol. 2008;9:29–38. van den Bent MJ, Dubbink HJ, Sanson M, van der Lee-Haarloo CR, Hegi M, Jeuken JW, et al. MGMT promoter methylation is prognostic but not predictive for outcome to adjuvant PCV chemotherapy in anaplastic oligodendroglial tumors: a report from EORTC Brain Tumor Group Study 26951. J Clin Oncol. 2009;27:5881–6. van den Bent MJ, Baumert B, Erridge SC, Vogelbaum MA, Nowak AK, Sanson M, et al. Interim results from the CATNON trial (EORTC study 26053–22054) of treatment with concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: a phase 3, randomised, open-label intergroup study. Lancet. 2017;390:1645–53. Bell EH, Zhang P, Fisher BJ, Macdonald DR, McElroy JP, Lesser GJ, et al. Association of MGMT promoter methylation status with survival outcomes in patientswith high-risk glioma treated with radiotherapy and temozolomide: an analysis from the NRG oncology/RTOG 0424. JAMA Oncol. 2018;2018:5. Okita Y, Shofuda T, Kanematsu D, Yoshioka E, Kodama Y, Mano M, et al. The association between 11C-methionine uptake, IDH gene mutation, and MGMT promoter methylation in patients with grade II and III gliomas. Clin Radiol. 2020;2020:5. Kong Z, Lin Y, Jiang C, Li L, Liu Z, Wang Y, et al. 18F-FDG-PET-based Radiomics signature predicts MGMT promoter methylation status in primary diffuse glioma. Cancer Imaging. 2019;19:58. Suchorska B, Weller M, Tabatabai G, Senft C, Hau P, Sabel MC, et al. Complete resection of contrast-enhancing tumor volume is associated with improved survival in recurrent glioblastoma-results from the DIRECTOR trial. Neuro Oncol. 2016;18:549–56. Duffau H, Taillandier L. New concepts in the management of diffuse low-grade glioma: proposal of a multistage and individualized therapeutic approach. Neuro Oncol. 2015;17:332–42. Kong Z, Jiang C, Zhu R, Feng S, Wang Y, Li J, et al. 18F-FDG-PET-based radiomics features to distinguish primary central nervous system lymphoma from glioblastoma. Neuroimage Clin. 2019;23:101912. Ohno M, Narita Y. A case of glioblastoma invasion clearly demonstrated on 11C-methionine positron emission tomography. Jpn J Clin Oncol. 2013;43:448. Yamauchi T, Ohno M, Matsushita Y, Takahashi M, Miyakita Y, Kitagawa Y, et al. Radiological characteristics based on isocitrate dehydrogenase mutations and 1p/19q codeletion in grade II and III gliomas. Brain Tumor Pathol. 2018;35:148–58. Tanaka K, Yamamoto Y, Maeda Y, Yamamoto H, Kudomi N, Kawai N, et al. Correlation of 4’-[methyl-11C]-thiothymidine uptake with Ki-67 immunohistochemistry and tumor grade in patients with newly diagnosed gliomas in comparison with 11C-methionine uptake. Ann Nucl Med. 2016;30:89–96. Toriihara A, Ohtake M, Tateishi K, Hino-Shishikura A, Yoneyama T, Kitazume Y, et al. Prognostic implications of 62Cu-diacetyl-bis (N(4)-methylthiosemicarbazone) PET/CT in patients with glioma. Ann Nucl Med. 2018;32:264–71.