Prognostic value of maximum standard uptake value, metabolic tumor volume, and total lesion glycolysis of positron emission tomography/computed tomography in patients with breast cancer: A systematic review and meta-analysis

Autoři: Weibo Wen aff001;  Dongchun Xuan aff001;  Yulai Hu aff002;  Xiangdan Li aff002;  Lan Liu aff003;  Dongyuan Xu aff002
Působiště autorů: Department of Nuclear Medicine, Affiliated hospital of Yanbian University, Yanji, Jilin Province, China aff001;  Center of Morphological Experiment, Medical College of Yanbian University, Yanji, Jilin Province, China aff002;  Department of Pathology, Affiliated hospital of Yanbian University, Yanji, Jilin Province, China aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article



A comprehensive systematic review of the literature was conducted on parameters from 18 F-FDG PET and a meta-analysis of the prognostic value of the maximal standard uptake value (SUVmax), metabolic tumor volume (MTV) and total lesional glycolysis (TLG) in patients with breast cancer (BC).

Patients and methods

Relevant English articles from PubMed, EMBASE, and the Cochrane Library were retrieved. Pooled hazard ratios (HRs) were used to assess the prognostic value of SUVmax, MTV, and TLG.


A total of 20 primary studies with 3115 patients with BC were included. The combined HRs (95% confidence interval [CI] of higher SUVmax and higher TLG for event-free survival (EFS) were 1.53 (95% CI, 1.25–1.89, P = 0.0006) and 5.94 (95% CI, 2.57–13.71, P = 0.97), respectively. Regarding the overall survival (OS), the combined HRs were 1.22 (95%CI, 1.02–1.45, P = 0.0006) with higher SUVmax, and 2.91(95% CI, 1.75–4.85, P = 0.44) with higher MTV. Higher MTV showed no correlation with EFS [1.31(95% CI, 0.65–2.65, P = 0.18)] and similarly higher TLG showed no correlation with OS [1.20(95% CI, 0.65–2.23, P = 0.45)]. Subgroup analysis showed that SUVmax, with a median value of 5.55 was considered as a significant risk factor for both EFS and OS in BC patients.


Despite clinically heterogeneous BC patients and adoption of various methods between studies, the present meta-analysis results confirmed that patients with high SUVmax are at high risk of adverse events or death in BC patients, high MTV predicted a high risk of death and high TLG predicted a high risk of adverse events.

Klíčová slova:

Adverse events – Breast cancer – Cancer treatment – Glycolysis – Positron emission tomography – Prognosis – Publication ethics


1. Jung NY, Kim SH, Choi BB, Kim SH, Sung MS. Associations between the standardized uptake value of (18)F-FDG PET/CT and the prognostic factors of invasive lobular carcinoma: in comparison with invasive ductal carcinoma. World J Surg Oncol. 2015;13:113. Epub 2015/04/19. doi: 10.1186/s12957-015-0522-9 25889560; PubMed Central PMCID: PMC4371618.

2. Gallamini A, Zwarthoed C, Borra A. Positron Emission Tomography (PET) in Oncology. Cancers (Basel). 2014;6(4):1821–89. Epub 2014/10/01. doi: 10.3390/cancers6041821 25268160; PubMed Central PMCID: PMC4276948.

3. Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54. Epub 2014/12/03. doi: 10.1007/s00259-014-2961-x 25452219; PubMed Central PMCID: PMC4315529.

4. Lee JW, Kang CM, Choi HJ, Lee WJ, Song SY, Lee JH, et al. Prognostic Value of Metabolic Tumor Volume and Total Lesion Glycolysis on Preoperative (1)(8)F-FDG PET/CT in Patients with Pancreatic Cancer. J Nucl Med. 2014;55(6):898–904. Epub 2014/04/09. doi: 10.2967/jnumed.113.131847 24711649.

5. 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(8):1191–8. Epub 2015/06/06. doi: 10.2967/jnumed.115.159913 26045311.

6. Kitajima K, Miyoshi Y, Yamano T, Odawara S, Higuchi T, Yamakado K. Prognostic value of FDG-PET and DWI in breast cancer. Ann Nucl Med. 2018;32(1):44–53. Epub 2017/11/15. doi: 10.1007/s12149-017-1217-9 29134565.

7. Cha J, Park HS, Kim D, Kim HJ, Kim MJ, Cho YU, et al. A hierarchical prognostic model for risk stratification in patients with early breast cancer according to (18) F-fludeoxyglucose uptake and clinicopathological parameters. Cancer Med. 2018;7(4):1127–34. Epub 2018/02/27. doi: 10.1002/cam4.1394 29479851; PubMed Central PMCID: PMC5911607.

8. Carkaci S, Sherman CT, Ozkan E, Adrada BE, Wei W, Rohren EM, et al. (18)F-FDG PET/CT predicts survival in patients with inflammatory breast cancer undergoing neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2013;40(12):1809–16. Epub 2013/07/24. doi: 10.1007/s00259-013-2506-8 23877633.

9. Cochet A, Dygai-Cochet I, Riedinger JM, Humbert O, Berriolo-Riedinger A, Toubeau M, et al. (1)(8)F-FDG PET/CT provides powerful prognostic stratification in the primary staging of large breast cancer when compared with conventional explorations. Eur J Nucl Med Mol Imaging. 2014;41(3):428–37. Epub 2013/11/08. doi: 10.1007/s00259-013-2595-4 24196916.

10. Moher D LA, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009; 151: 264–9. 2009.

11. Carkaci S, Sherman CT, Ozkan E, Adrada BE, Wei TY. F-18-FDG PET/CT predicts survival in patients with inflammatory breast cancer undergoing neoadjuvant chemotherapy. European Journal of Nuclear Medicine & Molecular Imaging. 2013;40(12):1809–16.

12. Ahn SG, Lee M, Jeon TJ, Han K, Lee HM, Lee SA, et al. [18F]-fluorodeoxyglucose positron emission tomography can contribute to discriminate patients with poor prognosis in hormone receptor-positive breast cancer. PLoS One. 2014;9(8):e105905. Epub 2014/08/29. doi: 10.1371/journal.pone.0105905 25167062; PubMed Central PMCID: PMC4148332.

13. Kim YH, Yoon HJ, Kim Y, Kim BS. Axillary Lymph Node-to-Primary Tumor Standard Uptake Value Ratio on Preoperative (18)F-FDG PET/CT: A Prognostic Factor for Invasive Ductal Breast Cancer. J Breast Cancer. 2015;18(2):173–80. Epub 2015/07/15. doi: 10.4048/jbc.2015.18.2.173 26155294; PubMed Central PMCID: PMC4490267.

14. Hyun SH, Ahn HK, Lee JH, Choi JY, Kim BT, Park YH, et al. Body Mass Index with Tumor 18F-FDG Uptake Improves Risk Stratification in Patients with Breast Cancer. PLoS One. 2016;11(10):e0165814. Epub 2016/11/01. doi: 10.1371/journal.pone.0165814 27798667; PubMed Central PMCID: PMC5087879 Young Choi, Byung-Tae Kim, Yeon Hee Park, Young-Hyuck Im, Jeong Eon Lee, Seok Jin Nam, and Kyung-Han Lee are employed by Samsung Medical Center, which is administratively separate from the Samsung Corporation. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

15. Chen S, Ibrahim NK, Yan Y, Wong ST, Wang H, Wong FC. Complete Metabolic Response on Interim (18)F-Fluorodeoxyglucose Positron Emission Tomography/Computed Tomography to Predict Long-Term Survival in Patients with Breast Cancer Undergoing Neoadjuvant Chemotherapy. Oncologist. 2017;22(5):526–34. Epub 2017/04/06. doi: 10.1634/theoncologist.2016-0334 28377466; PubMed Central PMCID: PMC5423520.

16. Yoo J, Yoon HJ, Kim BS. Prognostic Value of Percentage Change in Metabolic Parameters as Measured by Dual-Time Point (18)F-FDG PET/CT in Premenopausal Women with Invasive Ductal Breast Carcinoma. J Womens Health (Larchmt). 2017;26(10):1131–7. Epub 2017/05/13. doi: 10.1089/jwh.2016.6256 28498790.

17. Zhao Y, Liu C, Zhang Y, Gong C, Li Y, Xie Y, et al. Prognostic Value of Tumor Heterogeneity on 18F-FDG PET/CT in HR+HER2- Metastatic Breast Cancer Patients receiving 500 mg Fulvestrant: a retrospective study. Sci Rep. 2018;8(1):14458. Epub 2018/09/29. doi: 10.1038/s41598-018-32745-z 30262849; PubMed Central PMCID: PMC6160449.

18. Kadoya T, Aogi K, Kiyoto S, Masumoto N, Okada M. Role of maximum standardized uptake value in fluorodeoxyglucose positron emission tomography/computed tomography predicts malignancy grade and prognosis of operable breast cancer: A multi-institute study. Breast Cancer Research & Treatment. 2013;141(2).

19. Jian Z, Zhen J, Joseph R, Zhang YJ, Min Z, Zhang YP, et al. The maximum standardized uptake value of 18 F-FDG PET scan to determine prognosis of hormone-receptor positive metastatic breast cancer. BMC Cancer. 2013;13(1):42.

20. Garcia Vicente AM, Soriano Castrejon A, Lopez-Fidalgo JF, Amo-Salas M, Munoz Sanchez Mdel M, Alvarez Cabellos R, et al. Basal (1)(8)F-fluoro-2-deoxy-D-glucose positron emission tomography/computed tomography as a prognostic biomarker in patients with locally advanced breast cancer. Eur J Nucl Med Mol Imaging. 2015;42(12):1804–13. Epub 2015/07/15. doi: 10.1007/s00259-015-3102-x 26156534.

21. Chen S, Ibrahim NK, Yan Y, Wong ST, Wang H, Wong FC. Risk stratification in patients with advanced-stage breast cancer by pretreatment [(18) F]FDG PET/CT. Cancer. 2015;121(22):3965–74. Epub 2015/08/08. doi: 10.1002/cncr.29565 26249241.

22. Son SH, Lee SW, Jeong SY, Song BI, Chae YS, Ahn BC, et al. Whole-Body Metabolic Tumor Volume, as Determined by (18)F-FDG PET/CT, as a Prognostic Factor of Outcome for Patients With Breast Cancer Who Have Distant Metastasis. AJR Am J Roentgenol. 2015;205(4):878–85. Epub 2015/07/24. doi: 10.2214/AJR.14.13906 26204115.

23. Taghipour M, Wray R, Sheikhbahaei S, Wright JL, Subramaniam RM. FDG Avidity and Tumor Burden: Survival Outcomes for Patients With Recurrent Breast Cancer. AJR Am J Roentgenol. 2016;206(4):846–55. Epub 2016/03/24. doi: 10.2214/AJR.15.15106 27003053.

24. Kim J, Yoo SW, Kang SR, Cho SG, Oh JR, Chong A, et al. Prognostic Significance of Metabolic Tumor Volume Measured by (18)F-FDG PET/CT in Operable Primary Breast Cancer. Nucl Med Mol Imaging. 2012;46(4):278–85. Epub 2012/12/01. doi: 10.1007/s13139-012-0161-9 24900075; PubMed Central PMCID: PMC4043062.

25. Marinelli B, Espinet-Col C, Ulaner GA, Mcarthur HL, Weber WA. Prognostic value of FDG PET/CT-based metabolic tumor volumes in metastatic triple negative breast cancer patients. American Journal of Nuclear Medicine & Molecular Imaging. 2016;6(2):120–7.

26. Kim TH, Yoon JK, Kang DK, Kang SY, Jung YS, Han S, et al. Value of volume-based metabolic parameters for predicting survival in breast cancer patients treated with neoadjuvant chemotherapy. Medicine (Baltimore). 2016;95(41):e4605. Epub 2016/10/16. doi: 10.1097/MD.0000000000004605 27741099; PubMed Central PMCID: PMC5072926.

27. Son SH, Kim DH, Hong CM, Kim CY, Jeong SY, Lee SW, et al. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC Cancer,14,1(2014-08-12). 2014;14(1):585.

28. Pak K, Cheon GJ, Nam HY, Kim SJ, Kang KW, Chung JK, et al. Prognostic value of metabolic tumor volume and total lesion glycolysis in head and neck cancer: a systematic review and meta-analysis. J Nucl Med. 2014;55(6):884–90. Epub 2014/04/23. doi: 10.2967/jnumed.113.133801 24752671.

29. Sarker A, Im H-J, Cheon GJ, Hoon Chung H, Kang K, Chung J-K, et al. Prognostic Implications of the SUVmax of Primary Tumors and Metastatic Lymph Node Measured by 18F-FDG PET in Patients With Uterine Cervical Cancer: A Meta-analysis2015.

30. Im HJ, Pak K, Cheon GJ, Kang KW, Kim SJ, Kim IJ, et al. Prognostic value of volumetric parameters of (18)F-FDG PET in non-small-cell lung cancer: a meta-analysis. Eur J Nucl Med Mol Imaging. 2015;42(2):241–51. Epub 2014/09/07. doi: 10.1007/s00259-014-2903-7 25193652.

31. Zhao Q, Feng Y, Mao X, Qie M. Prognostic value of fluorine-18-fluorodeoxyglucose positron emission tomography or PET-computed tomography in cervical cancer: a meta-analysis. International journal of gynecological cancer: official journal of the International Gynecological Cancer Society. 2013;23(7):1184–90. doi: 10.1097/IGC.0b013e31829ee012 23851677.

32. Geus-Oei LF, Oyen WJ. Predictive and prognostic value of FDG-PET. Cancer Imaging. 2008;8:70–80. Epub 2008/04/09. doi: 10.1102/1470-7330.2008.0010 18390390; PubMed Central PMCID: PMC2324370.

33. Chang KP, Tsang NM, Liao CT, Hsu CL, Chung MJ, Lo CW, et al. Prognostic significance of 18F-FDG PET parameters and plasma Epstein-Barr virus DNA load in patients with nasopharyngeal carcinoma. Journal of nuclear medicine: official publication, Society of Nuclear Medicine. 2012;53(1):21–8. doi: 10.2967/jnumed.111.090696 22213820.

34. Yang Z, Shi Q, Zhang Y, Pan H, Yao Z, Hu S, et al. Pretreatment (18)F-FDG uptake heterogeneity can predict survival in patients with locally advanced nasopharyngeal carcinoma—a retrospective study. Radiation oncology (London, England). 2015;10:4. doi: 10.1186/s13014-014-0268-5 25566697.

35. Cheng L, Davison DD, Adams J, Lopez-Beltran A, Wang L, Montironi R, et al. Biomarkers in bladder cancer: translational and clinical implications. Critical reviews in oncology/hematology. 2014;89(1):73–111. doi: 10.1016/j.critrevonc.2013.08.008 24029603.

36. Ng SH, Chan SC, Yen TC, Chang JT, Liao CT, Ko SF, et al. Staging of untreated nasopharyngeal carcinoma with PET/CT: comparison with conventional imaging work-up. Eur J Nucl Med Mol Imaging. 2009;36(1):12–22. doi: 10.1007/s00259-008-0918-7 18704401.

37. Xia Q, Liu J, Wu C, Song S, Tong L, Huang G, et al. Prognostic significance of (18)FDG PET/CT in colorectal cancer patients with liver metastases: a meta-analysis. Cancer Imaging. 2015;15:19. Epub 2015/11/22. doi: 10.1186/s40644-015-0055-z 26589835; PubMed Central PMCID: PMC4654916.

38. Graham MM, Wahl RL, Hoffman JM, Yap JT, Sunderland JJ, Boellaard R, et al. Summary of the UPICT Protocol for 18F-FDG PET/CT Imaging in Oncology Clinical Trials. J Nucl Med. 2015;56(6):955–61. Epub 2015/04/18. doi: 10.2967/jnumed.115.158402 25883122; PubMed Central PMCID: PMC4587663.

39. Fukukita H, Suzuki K, Matsumoto K, Terauchi T, Daisaki H, Ikari Y, et al. Japanese guideline for the oncology FDG-PET/CT data acquisition protocol: synopsis of Version 2.0. Ann Nucl Med. 2014;28(7):693–705. Epub 2014/05/27. doi: 10.1007/s12149-014-0849-2 24859759; PubMed Central PMCID: PMC4332454.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden