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Relationship between 18F-FDG PET/CT Semi-Quantitative Parameters and International Association for the Study of Lung Cancer, American Thoracic Society/European Respiratory Society Classification in Lung Adenocarcinomas

  • Lihong Bu (PET/CT/MRI and Molecular Imaging Center, Renmin Hospital of Wuhan University) ;
  • NingTu (PET/CT/MRI and Molecular Imaging Center, Renmin Hospital of Wuhan University) ;
  • Ke Wang (PET/CT/MRI and Molecular Imaging Center, Renmin Hospital of Wuhan University) ;
  • Ying Zhou (PET/CT/MRI and Molecular Imaging Center, Renmin Hospital of Wuhan University) ;
  • Xinli Xie (Department of Nuclear Medicine, The First Affiliated Hospital of Zhengzhou University) ;
  • Xingmin Han (Department of Nuclear Medicine, The First Affiliated Hospital of Zhengzhou University) ;
  • Huiqin Lin (Department of Thoracic Surgery, Renmin Hospital of Wuhan University) ;
  • Hongyan Feng (PET/CT/MRI and Molecular Imaging Center, Renmin Hospital of Wuhan University)
  • Received : 2021.02.22
  • Accepted : 2021.09.26
  • Published : 2022.01.01

Abstract

Objective: To investigate the relationship between 18F-FDG PET/CT semi-quantitative parameters and the International Association for the Study of Lung Cancer, American Thoracic Society/European Respiratory Society (IASLC/ATS/ERS) histopathologic classification, including histological subtypes, proliferation activity, and somatic mutations. Materials and Methods: This retrospective study included 419 patients (150 males, 269 females; median age, 59.0 years; age range, 23.0-84.0 years) who had undergone surgical removal of stage IA-IIIA lung adenocarcinoma and had preoperative PET/CT data of lung tumors. The maximum standardized uptake values (SUVmax), background-subtracted volume (BSV), and background-subtracted lesion activity (BSL) derived from PET/CT were measured. The IASLC/ATS/ERS subtypes, Ki67 score, and epidermal growth factor/anaplastic lymphoma kinase (EGFR/ALK) mutation status were evaluated. The PET/CT semi-quantitative parameters were compared between the tumor subtypes using the Mann-Whitney U test or the Kruskal-Wallis test. The optimum cutoff values of the PET/CT semi-quantitative parameters for distinguishing the IASLC/ATS/ERS subtypes were calculated using receiver operating characteristic curve analysis. The correlation between the PET/CT semi-quantitative parameters and pathological parameters was analyzed using Spearman's correlation. Statistical significance was set at p < 0.05. Results: SUVmax, BSV, and BSL values were significantly higher in invasive adenocarcinoma (IA) than in minimally IA (MIA), and the values were higher in MIA than in adenocarcinoma in situ (AIS) (all p < 0.05). Remarkably, an SUVmax of 0.90 and a BSL of 3.62 were shown to be the optimal cutoff values for differentiating MIA from AIS, manifesting as pure ground-glass nodules with 100% sensitivity and specificity. Metabolic-volumetric parameters (BSV and BSL) were better potential independent factors than metabolic parameters (SUVmax) in differentiating growth patterns. SUVmax and BSL, rather than BSV, were strongly or moderately correlated with Ki67 in most subtypes, except for the micropapillary and solid predominant groups. PET/CT parameters were not correlated with EGFR/ALK mutation status. Conclusion: As noninvasive surrogates, preoperative PET/CT semi-quantitative parameters could imply IASLC/ATS/ERS subtypes and Ki67 index and thus may contribute to improved management of precise surgery and postoperative adjuvant therapy.

Keywords

Acknowledgement

This work was supported in part, by the National Science Foundation of China (81871419 to Dr. Bu, 81701735 to Dr. Feng), Seed project in Sino foreign joint research platform of Wuhan University (2309-413100006 to Dr. Bu), Hubei Provincial Natural Science Foundation of China (2017CFB781 to Dr. Bu), Chinese Society of Clinical Oncology Foundation (Y-HR2016-44 to Dr. Bu), Hubei Provincial Health Department (WJ2017M012 to Dr. Bu) and Young Teachers' Independent Research Funding of Wuhan University (2042019kf0054 to Dr. Tu). This was not an industry supported study.

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394-424
  2. Ettinger DS, Wood DE, Aggarwal C, Aisner DL, Akerley W, Bauman JR, et al. NCCN guidelines insights: non-small cell lung cancer, version 1.2020. J Natl Compr Canc Netw 2019;17:1464-1472
  3. Travis WD, Brambilla E, Nicholson AG, Yatabe Y, Austin JHM, Beasley MB, et al. The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol 2015;10:1243-1260
  4. Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 2011;6:244-285
  5. Noguchi M. Stepwise progression of pulmonary adenocarcinoma--clinical and molecular implications. Cancer Metastasis Rev 2010;29:15-21
  6. Fang W, Xiang Y, Zhong C, Chen Q. The IASLC/ATS/ERS classification of lung adenocarcinoma-a surgical point of view. J Thorac Dis 2014;6:S552-S560
  7. Van Schil PE, Asamura H, Rusch VW, Mitsudomi T, Tsuboi M, Brambilla E, et al. Surgical implications of the new IASLC/ATS/ERS adenocarcinoma classification. Eur Respir J 2012;39:478-486
  8. Zugazagoitia J, Enguita AB, Nunez JA, Iglesias L, Ponce S. The new IASLC/ATS/ERS lung adenocarcinoma classification from a clinical perspective: current concepts and future prospects. J Thorac Dis 2014;6:S526-S536
  9. Chiu CH, Yeh YC, Lin KH, Wu YC, Lee YC, Chou TY, et al. Histological subtypes of lung adenocarcinoma have differential 18F-fluorodeoxyglucose uptakes on the positron emission tomography/computed tomography scan. J Thorac Oncol 2011;6:1697-1703
  10. Nakamura H, Saji H, Shinmyo T, Tagaya R, Kurimoto N, Koizumi H, et al. Close association of IASLC/ATS/ERS lung adenocarcinoma subtypes with glucose-uptake in positron emission tomography. Lung Cancer 2015;87:28-33
  11. Satoh Y, Onishi H, Nambu A, Araki T. Volume-based parameters measured by using FDG PET/CT in patients with stage I NSCLC treated with stereotactic body radiation therapy: prognostic value. Radiology 2014;270:275-281
  12. Boellaard R. Standards for PET image acquisition and quantitative data analysis. J Nucl Med 2009;50 Suppl 1:11S-20S
  13. Zhu L, Li X, Wang J, Fu Q, Liu J, Ma W, et al. Value of metabolic parameters in distinguishing primary mediastinal lymphomas from thymic epithelial tumors. Cancer Biol Med 2020;17:468-477
  14. Korkmaz U, Hacioglu MB, Kostek O, Sut N, Kodaz H, Erdogan B, et al. The relationship between FDG PET/CT-defined metabolic parameters and the histopathological subtype of oesophageal carcinomas. Pol J Radiol 2020;85:e254-e260
  15. Husby JA, Reitan BC, Biermann M, Trovik J, Bjorge L, Magnussen IJ, et al. Metabolic tumor volume on 18F-FDG PET/CT improves preoperative identification of high-risk endometrial carcinoma patients. J Nucl Med 2015;56:1191-1198
  16. Liao S, Penney BC, Wroblewski K, Zhang H, Simon CA, Kampalath R, et al. Prognostic value of metabolic tumor burden on 18F-FDG PET in nonsurgical patients with non-small cell lung cancer. Eur J Nucl Med Mol Imaging 2012;39:27-38
  17. Chen HH, Chiu NT, Su WC, Guo HR, Lee BF. Prognostic value of whole-body total lesion glycolysis at pretreatment FDG PET/CT in non-small cell lung cancer. Radiology 2012;264:559-566
  18. Burger IA, Vargas HA, Apte A, Beattie BJ, Humm JL, Gonen M, et al. PET quantification with a histogram derived total activity metric: superior quantitative consistency compared to total lesion glycolysis with absolute or relative SUV thresholds in phantoms and lung cancer patients. Nucl Med Biol 2014;41:410-418
  19. Burger IA, Vargas HA, Beattie BJ, Goldman DA, Zheng J, Larson SM, et al. How to assess background activity: introducing a histogram-based analysis as a first step for accurate one-step PET quantification. Nucl Med Commun 2014;35:316-324
  20. Burger IA, Casanova R, Steiger S, Husmann L, Stolzmann P, Huellner MW, et al. 18F-FDG PET/CT of non-small cell lung carcinoma under neoadjuvant chemotherapy: background-based adaptive-volume metrics outperform TLG and MTV in predicting histopathologic response. J Nucl Med 2016;57:849-854
  21. Xu W, Yu S, Ma Y, Liu C, Xin J. Effect of different segmentation algorithms on metabolic tumor volume measured on 18F-FDG PET/CT of cervical primary squamous cell carcinoma. Nucl Med Commun 2017;38:259-265
  22. Wang XY, Zhao YF, Liu Y, Yang YK, Zhu Z, Wu N. Comparison of different automated lesion delineation methods for metabolic tumor volume of 18F-FDG PET/CT in patients with stage I lung adenocarcinoma. Medicine (Baltimore) 2017;96:e9365
  23. Dias-Santagata D, Akhavanfard S, David SS, Vernovsky K, Kuhlmann G, Boisvert SL, et al. Rapid targeted mutational analysis of human tumours: a clinical platform to guide personalized cancer medicine. EMBO Mol Med 2010;2:146-158
  24. Qi L, Lu W, Yang L, Tang W, Zhao S, Huang Y, et al. Qualitative and quantitative imaging features of pulmonary subsolid nodules: differentiating invasive adenocarcinoma from minimally invasive adenocarcinoma and preinvasive lesions. J Thorac Dis 2019;11:4835-4846
  25. Eriguchi D, Shimada Y, Imai K, Furumoto H, Okano T, Masuno R, et al. Predictive accuracy of lepidic growth subtypes in early-stage adenocarcinoma of the lung by quantitative CT histogram and FDG-PET. Lung Cancer 2018;125:14-21
  26. Nishii K, Bessho A, Fukamatsu N, Ogata Y, Hosokawa S, Sakugawa M, et al. Statistical analysis of 18F-fluorodeoxyglucose positron-emission tomography/computed tomography ground-glass nodule findings. Mol Clin Oncol 2018;9:279-282
  27. Lee HJ, Lee CH, Jeong YJ, Chung DH, Goo JM, Park CM, et al. IASLC/ATS/ERS international multidisciplinary classification of lung adenocarcinoma: novel concepts and radiologic implications. J Thorac Imaging 2012;27:340-353
  28. Godoy MC, Naidich DP. Overview and strategic management of subsolid pulmonary nodules. J Thorac Imaging 2012;27:240-248
  29. Shao X, Niu R, Jiang Z, Shao X, Wang Y. Role of PET/CT in management of early lung adenocarcinoma. AJR Am J Roentgenol 2020;214:437-445
  30. Lee HY, Jeong JY, Lee KS, Yi CA, Kim BT, Kang H, et al. Histopathology of lung adenocarcinoma based on new IASLC/ATS/ERS classification: prognostic stratification with functional and metabolic imaging biomarkers. J Magn Reson Imaging 2013;38:905-913
  31. Gormsen LC, Vendelbo MH, Pedersen MA, Haraldsen A, Hjorthaug K, Bogsrud TV, et al. A comparative study of standardized quantitative and visual assessment for predicting tumor volume and outcome in newly diagnosed diffuse large B-cell lymphoma staged with 18F-FDG PET/CT. EJNMMI Res 2019;9:36
  32. Castello A, Rossi S, Mazziotti E, Toschi L, Lopci E. Hyperprogressive disease in patients with non-small cell lung cancer treated with checkpoint inhibitors: the role of 18F-FDG PET/CT. J Nucl Med 2020;61:821-826
  33. Del Gobbo A, Pellegrinelli A, Gaudioso G, Castellani M, Zito Marino F, Franco R, et al. Analysis of NSCLC tumour heterogeneity, proliferative and 18F-FDG PET indices reveals Ki67 prognostic role in adenocarcinomas. Histopathology 2016;68:746-751
  34. Shen G, Ma H, Pang F, Ren P, Kuang A. Correlations of 18F-FDG and 18F-FLT uptake on PET with Ki-67 expression in patients with lung cancer: a meta-analysis. Acta Radiol 2018;59:188-195
  35. Sauter AW, Winterstein S, Spira D, Hetzel J, Schulze M, Mueller M, et al. Multifunctional profiling of non-small cell lung cancer using 18F-FDG PET/CT and volume perfusion CT. J Nucl Med 2012;53:521-529
  36. Nishimukai A, Inoue N, Kira A, Takeda M, Morimoto K, Araki K, et al. Tumor size and proliferative marker geminin rather than Ki67 expression levels significantly associated with maximum uptake of 18F-deoxyglucose levels on positron emission tomography for breast cancers. PLoS One 2017;12:e0184508
  37. Incoronato M, Grimaldi AM, Cavaliere C, Inglese M, Mirabelli P, Monti S, et al. Relationship between functional imaging and immunohistochemical markers and prediction of breast cancer subtype: a PET/MRI study. Eur J Nucl Med Mol Imaging 2018;45:1680-1693
  38. Morawitz J, Kirchner J, Martin O, Bruckmann NM, Dietzel F, Li Y, et al. Prospective correlation of prognostic immunohistochemical markers with SUV and ADC derived from dedicated hybrid breast 18F-FDG PET/MRI in women with newly diagnosed breast cancer. Clin Nucl Med 2021;46:201-205
  39. Parent EE, Benayoun M, Ibeanu I, Olson JJ, Hadjipanayis CG, Brat DJ, et al. [18F]Fluciclovine PET discrimination between high- and low-grade gliomas. EJNMMI Res 2018;8:67
  40. Chang CC, Cho SF, Chen YW, Tu HP, Lin CY, Chang CS. SUV on dual-phase FDG PET/CT correlates with the Ki-67 proliferation index in patients with newly diagnosed non-Hodgkin lymphoma. Clin Nucl Med 2012;37:e189-e195
  41. Mu W, Jiang L, Zhang J, Shi Y, Gray JE, Tunali I, et al. Noninvasive decision support for NSCLC treatment using PET/CT radiomics. Nat Commun 2020;11:5228
  42. Yip SS, Kim J, Coroller TP, Parmar C, Velazquez ER, Huynh E, et al. Associations between somatic mutations and metabolic imaging phenotypes in non-small cell lung cancer. J Nucl Med 2017;58:569-576
  43. Zhang J, Zhao X, Zhao Y, Zhang J, Zhang Z, Wang J, et al. Value of pre-therapy 18F-FDG PET/CT radiomics in predicting EGFR mutation status in patients with non-small cell lung cancer. Eur J Nucl Med Mol Imaging 2020;47:1137-1146
  44. Kim YI, Paeng JC, Park YS, Cheon GJ, Lee DS, Chung JK, et al. Relation of EGFR mutation status to metabolic activity in localized lung adenocarcinoma and its influence on the use of FDG PET/CT parameters in prognosis. AJR Am J Roentgenol 2018;210:1346-1351
  45. Zhu L, Yin G, Chen W, Li X, Yu X, Zhu X, et al. Correlation between EGFR mutation status and F18 -fluorodeoxyglucose positron emission tomography-computed tomography image features in lung adenocarcinoma. Thorac Cancer 2019;10:659-664
  46. Jiang L, Mino-Kenudson M, Roden AC, Rosell R, Molina MA, Flores RM, et al. Association between the novel classification of lung adenocarcinoma subtypes and EGFR/KRAS mutation status: a systematic literature review and pooled-data analysis. Eur J Surg Oncol 2019;45:870-876