Advertisement

Predictive value of primary tumor parameters using 18F-FDG PET/CT for occult lymph node metastasis in breast cancer with clinically negative axillary lymph node

  • Jang Yoo
  • Bom Sahn Kim
  • Hai-Jeon Yoon
Original Article

Abstract

Objective

This study aimed to demonstrate the clinical significance of total lesion glycolysis (TLG) of primary breast cancer using 18F-FDG PET/CT to predict axillary lymph node (ALN) metastasis in invasive ductal breast cancer (IDC) with a clinically negative axillary lymph node (cN-ALN).

Methods

135 patients, newly diagnosed with IDC with CN-ALN between July 2016 and October 2017, were retrospectively enrolled. We estimated primary tumor PET/CT parameters including the maximum standard uptake value (SUVmax), metabolic tumor volume (MTV), and TLG, as well as clinicopathologic findings. All patients received breast surgery followed by pathologic axillary lymph node examination.

Results

Of the 135 patients, 31 (23.0%) were diagnosed with pathologically proven metastatic ALN. In univariate analysis, SUVmax, MTV, and TLG of the primary breast tumor were correlated with metastatic ALN along with tumor size, lymphovascular invasion, CD34, and D2-40. On multivariate analysis, TLG (> 5.74, p = 0.009) had independent significance for predicting ALN metastasis in IDC with cN-ALN.

Conclusion

We demonstrated that TLG of primary tumors can be useful in predicting pathologic ALN metastasis in IDC patients with cN-ALN.

Keywords

Invasive ductal breast cancer Clinically negative axillary lymph node 18F-FDG PET/CT Total lesion glycolysis 

Notes

Acknowledgements

This research was supported by grants from the National Research Foundation (2015R1C1A1A02037051, 2018R1D1A1B07045321) of South Korea.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. 1.
    Schiffman SC, McMasters KM, Scoggins CR, Martin RC, Chagpar AB. Lymph node ratio: a proposed refinement of current axillary staging in breast cancer patients. J Am Coll Surg. 2011;213:45–52 (discussion 52–53).CrossRefPubMedGoogle Scholar
  2. 2.
    de Boer M, van Dijck JA, Bult P, Borm GF, Tjan-Heijnen VC. Breast cancer prognosis and occult lymph node metastases, isolated tumor cells, and micrometastases. J Natl Cancer Inst. 2010;102:410–25.CrossRefPubMedGoogle Scholar
  3. 3.
    Amersi F, Hansen NM. The benefits and limitations of sentinel lymph node biopsy. Curr Treat Options Oncol. 2006;7:141–51.CrossRefPubMedGoogle Scholar
  4. 4.
    Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, et al. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11:927–33.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Veronesi U, Viale G, Paganelli G, Zurrida S, Luini A, Galimberti V, et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg. 2010;251:595–600.CrossRefPubMedGoogle Scholar
  6. 6.
    De Groef A, Van Kampen M, Tieto E, Schonweger P, Christiaens MR, Neven P, et al. Arm lymphoedema and upper limb impairments in sentinel node-negative breast cancer patients: a one year follow-up study. Breast. 2016;29:102–8.CrossRefPubMedGoogle Scholar
  7. 7.
    Gebruers N, Verbelen H, De Vrieze T, Coeck D, Tjalma W. Incidence and time path of lymphedema in sentinel node negative breast cancer patients: a systematic review. Arch Phys Med Rehabil. 2015;96:1131–9.CrossRefPubMedGoogle Scholar
  8. 8.
    Crippa F, Gerali A, Alessi A, Agresti R, Bombardieri E. FDG-PET for axillary lymph node staging in primary breast cancer. Eur J Nucl Med Mol Imaging. 2004;31(Suppl 1):97–102.CrossRefGoogle Scholar
  9. 9.
    Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a metaanalysis. Cancer. 2006;106:4–16.CrossRefPubMedGoogle Scholar
  10. 10.
    Lyman GH, Temin S, Edge SB, Newman LA, Turner RR, Weaver DL, et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2014;32:1365–83.CrossRefPubMedGoogle Scholar
  11. 11.
    Wilke LG, McCall LM, Posther KE, Whitworth PW, Reintgen DS, Leitch AM, et al. Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol. 2006;13:491–500.CrossRefPubMedGoogle Scholar
  12. 12.
    Dialani V, Chadashvili T, Slanetz PJ. Role of imaging in neoadjuvant therapy for breast cancer. Ann Surg Oncol. 2015;22:1416–24.CrossRefPubMedGoogle Scholar
  13. 13.
    Lavayssiere R, Cabee AE, Filmont JE. Positron emission tomography (PET) and breast cancer in clinical practice. Eur J Radiol. 2009;69:50–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Wang Y, Zhang C, Liu J, Huang G. Is 18F-FDG PET accurate to predict neoadjuvant therapy response in breast cancer? A meta-analysis. Breast Cancer Res Treat. 2012;131:357–69.CrossRefPubMedGoogle Scholar
  15. 15.
    Jung NY, Kim SH, Kang BJ, Park SY, Chung MH. The value of primary tumor (18)F-FDG uptake on preoperative PET/CT for predicting intratumoral lymphatic invasion and axillary nodal metastasis. Breast Cancer. 2016;23:712–7.CrossRefPubMedGoogle Scholar
  16. 16.
    Kim JY, Lee SH, Kim S, Kang T, Bae YT. Tumour 18 F-FDG Uptake on preoperative PET/CT may predict axillary lymph node metastasis in ER-positive/HER2-negative and HER2-positive breast cancer subtypes. Eur Radiol. 2015;25:1172–81.CrossRefPubMedGoogle Scholar
  17. 17.
    Seok JW, Kim Y, An YS, Kim BS. The clinical value of tumor FDG uptake for predicting axillary lymph node metastasis in breast cancer with clinically negative axillary lymph nodes. Ann Nucl Med. 2013;27:546–53.CrossRefPubMedGoogle Scholar
  18. 18.
    An YS, Kang DK, Jung Y, Kim TH. Volume-based metabolic parameter of breast cancer on preoperative 18F-FDG PET/CT could predict axillary lymph node metastasis. Medicine. 2017;96:e8557.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    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;121:3965–74.CrossRefPubMedGoogle Scholar
  20. 20.
    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.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200.CrossRefPubMedGoogle Scholar
  22. 22.
    Choi WH, Yoo IR, O JH, Kim SH, Chung SK. The value of dual-time-point 18F-FDG PET/CT for identifying axillary lymph node metastasis in breast cancer patients. Br J Radiol. 2011;84(1003):593–9.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Deurloo EE, Tanis PJ, Gilhuijs KG, Muller SH, Kroger R, Peterse JL, et al. Reduction in the number of sentinel lymph node procedures by preoperative ultrasonography of the axilla in breast cancer. Eur J Cancer. 2003;39(8):1068–73.CrossRefPubMedGoogle Scholar
  24. 24.
    Kvistad KA, Rydland J, Smethurst HB, Lundgren S, Fjosne HE, Haraldseth O. Axillary lymph node metastases in breast cancer: preoperative detection with dynamic contrast-enhanced MRI. Eur Radiol. 2000;10(9):1464–71.CrossRefPubMedGoogle Scholar
  25. 25.
    Nori J, Vanzi E, Bazzocchi M, Bufalini FN, Distante V, Branconi F, et al. Role of axillary ultrasound examination in the selection of breast cancer patients for sentinel node biopsy. Am J Surg. 2007;193(1):16–20.CrossRefPubMedGoogle Scholar
  26. 26.
    Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol. 2013;31:3997–4013.CrossRefPubMedGoogle Scholar
  27. 27.
    Petric M, Martinez S, Acevedo F, Oddo D, Artigas R, Camus M, et al. Correlation between Ki67 and histological grade in breast cancer patients treated with preoperative chemotherapy. Asian Pac J Cancer Prev. 2014;15:10277–80.CrossRefPubMedGoogle Scholar
  28. 28.
    Van den Eynden GG, Van der Auwera I, Van Laere SJ, Colpaert CG, van Dam P, Dirix LY, et al. Distinguishing blood and lymph vessel invasion in breast cancer: a prospective immunohistochemical study. Br J Cancer. 2006;94:1643–9.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Yoo J, Kim BS, Chung J, Yoon HJ. Percentage change of primary tumor on 18F-FDG PET/CT as a prognostic factor for invasive ductal breast cancer with axillary lymph node metastasis: comparison with MRI. Medicine (Baltimore). 2017;96:e7657.CrossRefGoogle Scholar
  30. 30.
    Lee JW, Cho A, Lee JH, Yun M, Lee JD, Kim YT, et al. The role of metabolic tumor volume and total lesion glycolysis on 18F-FDG PET/CT in the prognosis of epithelial ovarian cancer. Eur J Nucl Med Mol Imaging. 2014;41:1898–906.CrossRefPubMedGoogle Scholar
  31. 31.
    Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 2013;36:27–46.CrossRefGoogle Scholar
  32. 32.
    Chung MJ, Lee JH, Kim SH, Suh YJ, Choi HJ. Simple prediction model of axillary lymph node positivity after analyzing molecular and clinical factors in early breast cancer. Medicine. 2016;95:e3689.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Yoshihara E, Smeets A, Laenen A, Reynders A, Soens J, Van Ongeval C, et al. Predictors of axillary lymph node metastases in early breast cancer and their applicability in clinical practice. Breast. 2013;22:357–61.CrossRefPubMedGoogle Scholar
  34. 34.
    Ahn JH, Son EJ, Kim JA, Youk JH, Kim EK, Kwak JY, et al. The role of ultrasonography and FDG-PET in axillary lymph node staging of breast cancer. Acta Radiol. 2010;51:859–65.CrossRefPubMedGoogle Scholar
  35. 35.
    Valente SA, Levine GM, Silverstein MJ, Rayhanabad JA, Weng-Grumley JG, Ji L, et al. Accuracy of predicting axillary lymph node positivity by physical examination, mammography, ultrasonography, and magnetic resonance imaging. Ann Surg Oncol. 2012;19:1825–30.CrossRefPubMedGoogle Scholar
  36. 36.
    Gradishar WJ, Anderson BO, Balassanian R, Blair SL, Burstein HJ, Cyr A, et al. Invasive breast cancer version 1.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2016;14:324–54.CrossRefPubMedGoogle Scholar
  37. 37.
    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 18F-fludeoxyglucose uptake and clinicopathological parameters. Cancer Med. 2018;7:1127–34.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Japanese Society of Nuclear Medicine 2018

Authors and Affiliations

  1. 1.Department of Nuclear Medicine, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea
  2. 2.Department of Nuclear MedicineEwha Womans University School of MedicineSeoulSouth Korea

Personalised recommendations