Abstract
Management of the axilla in patients with operable breast cancer is still one of the most controversial areas in clinical oncology. The best procedure to examine the lymph nodes is still standard axillary lymph node dissection; nevertheless, the morbidity associated with this procedure is well known. Based on these considerations, it is important for progress in the treatment of operable breast cancer that strategies are found that permit a less invasive method of axillary sampling which does not impair the patient’s quality of life. The technique of sentinel lymph node (SLN) biopsy has recently been proposed for this purpose, with very important results. SLN has now become routine practice in the surgical management of breast cancer, and in many institutions patients with a negative SLN biopsy are spared axillary dissection, while those with a positive SLN biopsy are submitted to axillary node dissection. The good accuracy of SLN biopsy represents a significant advance in the management of primary breast cancer; however, false negative axillary results can occur in a variable percentage of patients, and the contribution of the SLN procedure to the detection of metastases in the internal mammary and supraclavicular lymph nodes is not clear. Among the recently developed imaging modalities, positron emission tomography (PET) with 18F-fluorodeoxyglucose (FDG) has in particular been applied to the study of lymph node metastases in cancer patients. Several clinical studies have been carried out to evaluate the accuracy of PET in the axillary staging of operable primary breast cancer. These studies have sometimes provided conflicting results, either supporting the possibility of using FDG-PET to select patients who need axillary dissection or questioning whether FDG-PET can accurately assess the axillary status in primary breast cancer. All the limitations and the advantages of FDG-PET are discussed in this paper, by examining the performance of scanner technology and the possible causes of the false negative results. In the experience of the authors, comparing FDG-PET with SLN biopsy in the same series of patients, the results seem to indicate that the lower sensitivity of PET is restricted to micrometastases. Of course, this limitation of PET has to be analysed in relation to the importance of such small axillary metastases for the outcome of patients with breast cancer. The added value offered by PET in breast cancer staging in comparison with intraoperative detection of the sentinel node lies in the fact that FDG-PET is a non-invasive procedure that allows, within a single examination, the biological characterisation of breast cancer and viewing of the entire body.
Similar content being viewed by others
References
Copeland EM 3rd. Is axillary dissection necessary for T1 carcinoma of the breast? [editorial]. J Am Coll Surg 1997; 184:397–398.
Haffty BG, Ward B, Pathare P, Salem R, McKhann C, Beinfield M, Fischer D, Reiss M. Reappraisal of the role of axillary lymph node dissection in the conservative treatment of breast cancer. J Clin Oncol 1997; 15:691–700.
Silverstein MJ, Gierson ED, Waisman JR, Senofsky GM, Colbum WJ, Gamagami P. Axillary lymph node dissection for T1a breast carcinoma. Is it still indicated? Cancer 1994; 73:664–667.
Dees EC, Shulman LN, Souba WW, Smith BL. Does information from axillary dissection change treatment in clinically node-negative patients with breast cancer? An algorithm for assessment of impact of axillary dissection. Ann Surg 1997; 226:279–286.
Cabanes PA, Salmon RJ, Vilcoq JR, Durand JC, Fourquet A, Gautier C, Asselain B. Value of axillary dissection in addition to lumpectomy and radiotherapy in early breast cancer. The Breast Carcinoma Collaborative Group of the Institut Curie. Lancet 1992; 339:1245–1248.
Kwan W, Jackson J, Weir LM, Dingee C, McGregor G, Olivotto IA. Chronic arm morbidity after curative breast cancer treatment: prevalence and impact on quality of life. J Clin Oncol 2002; 20:4242–4228.
Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220:398–401.
Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, Shriver C, Feldman S, Kusminsky R, Gadd M, Kuhn J, Harlow S, Beitsch P. The sentinel node in breast cancer: a multicenter validation study. N Engl J Med 1998; 339:941–946.
Veronesi U, Paganelli G, Viale G, Galimberti V, Luini A, Zurrida S, Robertson C, Sacchini V, Veronesi P, Orvieto E, De cicco C, Intra M, Tosi G, Scarpa D. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst 1999; 91:368–373.
Chao C, McMasters K. The current status of sentinel lymph node biopsy for breast cancer. Adv Surg 2002; 36:167–192.
Jakub JW, Pendas S, Reintgen DS. Current status of sentinel lymph node mapping and biopsy: facts and controversies. Oncologist 2003; 8:59–68.
Gerber B, Krause A, Mueller H, Richter D, Reimer T, Makovitzky J, Herrnring C, Jeschke U, Kundt G, Friese K. Simultaneous immunohistochemical detection of tumour cells in lymph nodes and bone marrow aspirates in breast cancer and its correlation with other prognostic factors J Clin Oncol 2001; 19:960–971.
Klauber-DeMore N, Bevilacqua JL, Van Zee KJ, Borgen P, Cody HS 3rd. Comprehensive review of the management of internal mammary lymph node metastases in breast cancer. J Am Coll Surg 2001; 193:547–555.
Bombardieri E, Crippa F, Baio SM, Peeters BA, Greco M, Pauwels EK. Nuclear medicine advances in breast cancer imaging. Tumori 2001; 87:277–287.
Carrington B. Lymph nodes. In: Husband JES, Rezneck RH, eds. Imaging in oncology, vol 2, part V. Metastases. Oxford: ISIS Mediac Media; 1998:729–748.
Wahl RL, Kaminski MS, Ethier SP, Hutchins GD. The potential of 2-deoxy-2[18F]fluoro-d-glucose (FDG) for the detection of tumor involvement in lymph nodes. J Nucl Med 1990; 31:1831–1835.
Adler LP, Faulhaber PF, Schnur KC, Al-Kasi NL, Shenk RR. Axillary lymph node metastases: screening with [F-18]2-deoxy-2-fluoro-d-glucose (FDG) PET. Radiology 1997; 203:323–327.
Utech CI, Young CS, Winter PF. Prospective evaluation of fluorine-18 fluorodeoxyglucose positron emission tomography in breast cancer for staging of the axilla related to surgery and immunocytochemistry. Eur J Nucl Med 1996; 23:1588–1593.
Greco M, Crippa F, Agresti R, Seregni E, Gerali A, Giovanazzi R, Micheli A, Asero S, Ferraris C, Gennaro M, Bombardieri E, Cascinelli N. Axillary lymph node staging in breast cancer by 2-fluoro-2-deoxy-d-glucose positron emission tomography: clinical evaluation and alternative management. J Natl Cancer Inst 2001; 93:630–635.
Crowe JP Jr, Adler LP, Shenk RR, Sunshine J. Positron emission tomography and breast masses: comparison with clinical, mammographic, and pathological findings. Ann Surg Oncol 1994; 1:132–140.
Noh DY, Yun IJ, Kim JS, Kang HS, Lee DS, Chung JK, Lee MC, Youn YK, Oh SK, Choe KJ. Diagnostic value of positron emission tomography for detecting breast cancer. World J Surg 1998; 22:223–227.
Smith IC, Ogston KN, Whitford P, Smith FW, Sharp P, Norton M, Miller ID, Ah-See AK, Heys SD, Jibril JA, Eremin O. Staging of the axilla in breast cancer: accurate in vivo assessment using positron emission tomography with 2-(fluorine-18)-fluoro-2-deoxy-d-glucose. Ann Surg 1998; 228:220–227.
Scheidhauer K, Scharl A, Pietrzyk U, Wagner R, Göhring UJ, Schomäcker K, Schicha H. Qualitative [18F]FDG positron emission tomography in primary breast cancer: clinical relevance and practicability. Eur J Nucl Med 1996; 23:618–623.
Rieber A, Schirrmeister H, Gabelmann A, Nuessle K, Reske S, Kreienberg R, Brambs HJ, Kuehn T. Pre-operative staging of invasive breast cancer with MR mammography and/or PET: boon or bunk? Br J Radiol 2002; 75:789–798.
Avril N, Dose J, Janicke F, Ziegler S, Romer W, Weber W, Herz M, Nathrath W, Graeff H, Schwaiger M. Assessment of axillary lymph node involvement in breast cancer patients with positron emission tomography using radiolabeled 2-(fluorine-18)-fluoro-2-deoxy-d-glucose. J Natl Cancer Inst 1996; 88:1204–1209.
Whal RL, Siegel BA, Coleman RE, Gatsonis CG. PET Study Group. Prospective multicenter study of axillary nodal staging by positron emission tomography in breast cancer: a report of the staging breast cancer with PET Study Group. J Clin Oncol 2004; 22:277–285.
Kelemen PR, Lowe V, Phillips N. Positron emission tomography and sentinel lymph node dissection in breast cancer. Clin Breast Cancer 2002; 3:73–77.
Guller U, Nitzsche EU, Schirp U, Viehl CT, Torhorst J, Moch H, Langer I, Marti WR, Oertli D, Harder F, Zuber M. Selective axillary surgery in breast cancer patients based on positron emission tomography with18F-fluoro-2-deoxy-d-glucose: not yet! Breast Cancer Res Treat 2002; 71:171–173.
van der Hoeven JJ, Hoekstra OS, Comans EF, Pijpers R, Boom RP, van Geldere D, Meijer S, Lammertsma AA, Teule GJ. Determinants of diagnostic performance of [F-18]fluoro-deoxyglucose positron emission tomography for axillary staging in breast cancer. Ann Surg 2002; 236:619–624.
Lovrics P, Chen V, Coates G, et al. A prospective study of PET scanning, sentinel node biopsy, and standard axillary dissection for axillary staging in patients with early stage breast cancer. Abstract book 24th Annual Cancer Symposium, Society of Surgical Oncology, March, 2001.
Zornoza G. Garcia, Velloso MJ, Sola J, Regueira FM, Pina L, Beorlegui C.18F-FDG PET complemented with sentinel lymph node biopsy in the detection of axillary involvement in breast cancer. Eur J Surg Oncol 2004; 30:15–19.
Jung-Hyun Yang, Nam SJ, Lee TS, Lee HK, Jung SH, Kim BT. Comparison of intraoperative frozen section analysis of sentinel node with preoperative positron emission tomography in the diagnosis of axillary lymph node status in breast cancer patients. Jpn J Clin Oncol 2001; 31:1–6.
Agresti R, Crippa F, Gerali A, Maccauro M, Giovanazzi R, Bombardieri E, Greco M. Lymph node metastases detection by FDG-PET and sentinel node biopsy in breast cancer patients: comparison of these different approaches [abstract]. ESSO Congress, 2004.
Eubank WB, Mankoff DA, Takasugi J, Vesselle H, Eary JF, Shanley TJ, Gralow JR, Charlop A, Ellis GK, Lindsley KL, Austin-Seymour MM, Funkhouser CP, Livingston RB.18Fluorodeoxyglucose positron emission tomography to detect mediastinal or internal mammary metastases in breast cancer. J Clin Oncol 2001; 19:3516–3523.
Crippa F, Seregni E, Agresti R, Chiesa C, Pascali C, Bogni A, Decise D, De Sanctis V, Greco M, Dandone MG, Bombardieri E. Association between [18F]fluorodeoxyglucose uptake and postoperative histopathology, hormone receptor status, thymidine labelling index and p53 in primary breast cancer: a preliminary observation. Eur J Nucl Med 1998; 25:1429–1434.
Avril N, Dose J, Jänicke F, Bense S, Ziegler S, Laubenbacher C, Römer W, Pache H, Herz M, Allgayer B, Nathrath W, Graeff H, Schwaiger M. Metabolic characterization of breast tumours with positron emission tomography using F-18 fluorodeoxyglucose. J Clin Oncol 1996; 14:1848–1857.
Wahl RL, Hutchins GD, Buchsbaum DJ, Liebert M, Grossman HB, Fisher S.18F-2-deoxy-2-fluoro-d-glucose uptake into human tumour xenografts. Feasibility studies for cancer imaging with positron emission tomography. Cancer 1991; 67:1544–1550.
Crippa F, Leutner M, Belli F, Gallino F, Greco M, Pilotti S, Cascinelli N, Bombardieri E. Which kinds of lymph node metastases can FDG PET detect. A clinical study in melanoma. J Nucl Med 2000; 41:1491–1494.
Greco M, Agresti R, Cascinelli N, Casalini P, Giovanazzi R, Maucione A, Tomasic G, Ferraris C, Ammatuna M, Pilotti S, Menard S. Breast cancer patients treated without axillary surgery: clinical implication and biologic analysis. Ann Surg 2000; 232:1–7.
Menard S, Bufalino R, Rilke F, Cascinelli N, Veronesi U, Colnaghi MI. Prognosis based on primary breast carcinoma instead of pathological nodal status. Br J Cancer 1994; 70:709–712.
Acknowledgements
The authors are grateful to Ms. Annaluisa De Simone Sorrentino for her kind editorial collaboration in preparing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Crippa, F., Gerali, A., Alessi, A. et al. FDG-PET for axillary lymph node staging in primary breast cancer. Eur J Nucl Med Mol Imaging 31 (Suppl 1), S97–S102 (2004). https://doi.org/10.1007/s00259-004-1531-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00259-004-1531-z