Skip to main content

Advertisement

Log in

Prediction of breast cancer recurrence using lymph node metabolic and volumetric parameters from 18F-FDG PET/CT in operable triple-negative breast cancer

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

Triple-negative breast cancer has a poor prognosis. We evaluated several metabolic and volumetric parameters from preoperative 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET)/computed tomography (CT) in the prognosis of triple-negative breast cancer and compared them with current clinicopathologic parameters.

Methods

A total of 228 patients with triple-negative breast cancer (mean age 47.0 ± 10.8 years, all women) who had undergone preoperative PET/CT were included. The PET/CT metabolic parameters evaluated included maximum, peak, and mean standardized uptake values (SUVmax, SUVpeak, and SUVmean, respectively). The volumetric parameters evaluated included metabolic tumor volume (MTV) and total lesion glycolysis (TLG). Metabolic and volumetric parameters were evaluated separately for tumor (T) and lymph nodes (N). The prognostic value of these parameters was compared with that of clinicopathologic parameters.

Results

All lymph node metabolic and volumetric parameters showed significant differences between patients with and without recurrence. However, tumor metabolic and volumetric parameters showed no significant differences. In a univariate survival analysis, all lymph node metabolic and volumetric parameters (SUVmax-N, SUVpeak-N, SUVmean-N, MTV-N, and TLG-N; all P < 0.001), T stage (P = 0.010), N stage (P < 0.001), and TNM stage (P < 0.001) were significant parameters. In a multivariate survival analysis, SUVmax-N (P = 0.005), MTV (P = 0.008), and TLG (P = 0.006) with TNM stage (all P < 0.001) were significant parameters.

Conclusions

Lymph node metabolic and volumetric parameters were significant predictors of recurrence in patients with triple-negative breast cancer after surgery. Lymph node metabolic and volumetric parameters were useful parameters for evaluating prognosis in patients with triple-negative breast cancer by 18F-FDG PET/CT, rather than tumor parameters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.

    Article  PubMed  Google Scholar 

  2. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747–52.

    Article  CAS  PubMed  Google Scholar 

  3. Prat A, Adamo B, Cheang MC, Anders CK, Carey LA, Perou CM. Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist. 2013;18:123–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121:2750–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Groheux D, Cochet A, Humbert O, Alberini J-L, Hindié E, Mankoff D. 18F-FDG PET/CT for staging and restaging of breast cancer. J Nucl Med. 2016;57:17S–26S.

    Article  CAS  PubMed  Google Scholar 

  6. Groheux D, Mankoff D, Espié M, Hindié E. 18F-FDG PET/CT in the early prediction of pathological response in aggressive subtypes of breast cancer: review of the literature and recommendations for use in clinical trials. Eur J Nucl Med Mol Imaging. 2016;43:983–93.

    Article  CAS  PubMed  Google Scholar 

  7. Jo I, Zeon SK, Kim SH, Kim HW, Kang SH, Kwon SY, et al. Correlation of primary tumor FDG uptake with clinicopathologic prognostic factors in invasive ductal carcinoma of the breast. Nucl Med Mol Imaging. 2015;49:19–25.

    Article  CAS  PubMed  Google Scholar 

  8. Groheux D, Hindié E, Delord M, Giacchetti S, Hamy A-S, de Bazelaire C, et al. Prognostic impact of 18FDG-PET-CT findings in clinical stage III and IIB breast cancer. J Natl Cancer Inst. 2012;19:1879–87.

    Article  Google Scholar 

  9. Chang JS, Lee J, Kim HJ, Kim KH, Yun M, Kim SI, et al. 18F-FDG/PET may help to identify a subgroup of patients with T1-T2 breast cancer and 1–3 positive lymph nodes who are at a high risk of recurrence after mastectomy. Cancer Res Treat. 2016;48:508–17.

    Article  CAS  PubMed  Google Scholar 

  10. Basu S, Chen W, Tchou J, Mavi A, Cermik T, Czerniecki B, et al. Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters. Cancer. 2008;112:995–1000.

    Article  CAS  PubMed  Google Scholar 

  11. Groheux D, Giacchetti S, Moretti J-L, Porcher R, Espié M, Lehmann-Che J, et al. Correlation of high 18F-FDG uptake to clinical, pathological and biological prognostic factors in breast cancer. Eur J Nucl Med Mol Imaging. 2011;38:426–35.

    Article  PubMed  Google Scholar 

  12. Vicente AMG, Castrejón ÁS, Martín AL, López-Muñiz IC, Madero VM, Sánchez MMM, et al. Molecular subtypes of breast cancer: metabolic correlation with 18F-FDG PET/CT. Eur J Nucl Med Mol Imaging. 2013;40:1304–11.

    Article  Google Scholar 

  13. Marinelli B, Espinet-Col C, Ulaner GA, McArthur HL, Gonen M, Jochelson M, et al. Prognostic value of FDG PET/CT-based metabolic tumor volumes in metastatic triple negative breast cancer patients. Am J Nucl Med Mol Imaging. 2016;6:120–7.

    PubMed  PubMed Central  Google Scholar 

  14. Hyun SH, Ahn HK, Park YH, Im Y-H, Kil WH, Lee JE, et al. Volume-based metabolic tumor response to neoadjuvant chemotherapy is associated with an increased risk of recurrence in breast cancer. Radiology. 2014;275:235–44.

    Article  PubMed  Google Scholar 

  15. Son SH, Lee S-W, Jeong SY, Song B-I, Chae YS, Ahn B-C, et al. Whole-body metabolic tumor volume, as determined by 18F-FDG PET/CT, as a prognostic factor of outcome for patients with breast cancer who have distant metastasis. AJR Am J Roentgenol. 2015;205:878–85.

    Article  PubMed  Google Scholar 

  16. Kim J, Yoo SW, Kang S-R, Cho S-G, Oh J-R, Chong A, et al. Prognostic significance of metabolic tumor volume measured by 18F-FDG PET/CT in operable primary breast cancer. Nucl Med Mol Imaging. 2012;46:278–85.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Song B-I, Lee S-W, Jeong SY, Chae YS, Lee WK, Ahn B-C, et al. 18F-FDG uptake by metastatic axillary lymph nodes on pretreatment PET/CT as a prognostic factor for recurrence in patients with invasive ductal breast cancer. J Nucl Med. 2012;53:1337–44.

    Article  CAS  PubMed  Google Scholar 

  18. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19:403–10.

    Article  CAS  PubMed  Google Scholar 

  19. Hammond MEH, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version). Arch Pathol Lab Med. 2010;134:e48–72.

    CAS  PubMed  Google Scholar 

  20. Wolff AC, Hammond MEH, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. Arch Pathol Lab Med. 2007;131:18–43.

    CAS  PubMed  Google Scholar 

  21. Budczies J, Klauschen F, Sinn BV, Győrffy B, Schmitt WD, Darb-Esfahani S, et al. Cutoff finder: a comprehensive and straightforward web application enabling rapid biomarker cutoff optimization. PLoS One. 2012;7:e51862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Groheux D, Giacchetti S, Delord M, Hindié E, Vercellino L, Cuvier C, et al. 18F-FDG PET/CT in staging patients with locally advanced or inflammatory breast cancer: comparison to conventional staging. J Nucl Med. 2013;54:5–11.

    Article  PubMed  Google Scholar 

  23. Groheux D, Hindié E, Giacchetti S, Delord M, Hamy A-S, de Roquancourt A, et al. Triple-negative breast cancer: early assessment with 18F-FDG PET/CT during neoadjuvant chemotherapy identifies patients who are unlikely to achieve a pathologic complete response and are at a high risk of early relapse. J Nucl Med. 2012;53:249–54.

    Article  CAS  PubMed  Google Scholar 

  24. Groheux D, Giacchetti S, Delord M, de Roquancourt A, Merlet P, Hamy A, et al. Prognostic impact of 18F-FDG PET/CT staging and of pathological response to neoadjuvant chemotherapy in triple-negative breast cancer. Eur J Nucl Med Mol Imaging. 2015;42:377–85.

    Article  CAS  PubMed  Google Scholar 

  25. Humbert O, Riedinger J-M, Charon-Barra C, Berriolo-Riedinger A, Desmoulins I, Lorgis V, et al. Identification of biomarkers including 18FDG-PET/CT for early prediction of response to neoadjuvant chemotherapy in triple-negative breast cancer. Clin Cancer Res. 2015;21:5460–8.

    Article  CAS  PubMed  Google Scholar 

  26. Koo HR, Park JS, Kang KW, Han W, Park IA, Moon WK. Correlation between 18F-FDG uptake on PET/CT and prognostic factors in triple-negative breast cancer. Eur Radiol. 2015;25:3314–21.

    Article  PubMed  Google Scholar 

  27. Aogi K, Kadoya T, Sugawara Y, Kiyoto S, Shigematsu H, Masumoto N, et al. Utility of 18F FDG-PET/CT for predicting prognosis of luminal-type breast cancer. Breast Cancer Res Treat. 2015;150:209–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yue Y, Cui X, Bose S, Audeh W, Zhang X, Fraass B. Stratifying triple-negative breast cancer prognosis using 18F-FDG-PET/CT imaging. Breast Cancer Res Treat. 2015;153:607–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lucignani G. SUV and segmentation: pressing challenges in tumour assessment and treatment. Eur J Nucl Med Mol Imaging. 2009;36:715–20.

    Article  PubMed  Google Scholar 

  30. Thie JA. Understanding the standardized uptake value, its methods, and implications for usage. J Nucl Med. 2004;45:1431–4.

    PubMed  Google Scholar 

  31. Hyun SH, Choi JY, Shim YM, Kim K, Lee SJ, Cho YS, et al. Prognostic value of metabolic tumor volume measured by 18F-fluorodeoxyglucose positron emission tomography in patients with esophageal carcinoma. Ann Surg Oncol. 2010;17:115–22.

    Article  PubMed  Google Scholar 

  32. Chen HH, Chiu N-T, Su W-C, Guo H-R, Lee B-F. Prognostic value of whole-body total lesion glycolysis at pretreatment FDG PET/CT in non–small cell lung cancer. Radiology. 2012;264:559–66.

    Article  PubMed  Google Scholar 

  33. Pak K, Cheon GJ, Nam H-Y, Kim S-J, Kang KW, Chung J-K, 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;55:884–90.

    Article  CAS  PubMed  Google Scholar 

  34. Ferguson DJ, Meier P, Karrison T, Dawson PJ, Straus FH, Lowenstein FE. Staging of breast cancer and survival rates: an assessment based on 50 years of experience with radical mastectomy. JAMA. 1982;248:1337–41.

    Article  CAS  PubMed  Google Scholar 

  35. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363:1938–48.

    Article  CAS  PubMed  Google Scholar 

  36. Liao C-T, Chang JT-C, Wang H-M, Ng S-H, Hsueh C, Lee L-Y, et al. Preoperative [18F]fluorodeoxyglucose positron emission tomography standardized uptake value of neck lymph nodes predicts neck cancer control and survival rates in patients with oral cavity squamous cell carcinoma and pathologically positive lymph nodes. Int J Radiat Oncol Biol Phys. 2009;74:1054–61.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keon Wook Kang.

Ethics declarations

Funding

This research was supported by the Basic Science Research Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2009-0093820), and by a grant from the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HI14C1072).

Conflicts of interest

None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the principles of the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, Yi., Kim, Y.J., Paeng, J.C. et al. Prediction of breast cancer recurrence using lymph node metabolic and volumetric parameters from 18F-FDG PET/CT in operable triple-negative breast cancer. Eur J Nucl Med Mol Imaging 44, 1787–1795 (2017). https://doi.org/10.1007/s00259-017-3748-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00259-017-3748-7

Keywords

Navigation