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Axillary Staging in the Neoadjuvant Setting

  • Breast Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Neoadjuvant chemotherapy (NAC) is increasingly being used in the treatment of locally advanced breast cancer as well as for early breast cancer. Axillary lymph node dissection has been the standard method of staging the axilla in the neoadjuvant setting. Since the sentinel lymph node biopsy was introduced in the early 1990s, less invasive approaches to axillary staging in patients undergoing neoadjuvant therapy have been proposed. In this review, we discuss the effects of NAC, the imaging modalities that have been used to evaluate the axillary lymph nodes, and the role and timing of sentinel lymph node biopsy in the neoadjuvant setting. Finally, we propose a treatment algorithm for patients undergoing NAC on the basis of the current data.

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References

  1. Kaufmann M, von Minckwitz G, Bear HD, et al. Recommendations from an international expert panel on the use of neoadjuvant (primary) systemic treatment of operable breast cancer: new perspectives, 2006. Ann Oncol. 2007;18:1927–34.

    Article  PubMed  CAS  Google Scholar 

  2. Fisher B, Brown A, Mamounas E, et al. Effect of preoperative chemotherapy on local-regional disease in women with operable breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-18. J Clin Oncol. 1997;15:2483–93.

    PubMed  CAS  Google Scholar 

  3. Mamounas EP. Sentinel lymph node biopsy after neoadjuvant systemic therapy. Surg Clin North Am. 2003;83:931–42.

    Article  PubMed  Google Scholar 

  4. Kuerer HM, Sahin AA, Hunt KK, et al. Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg. 1999;230:72–8.

    Article  PubMed  CAS  Google Scholar 

  5. Singletary SE, Connolly JL. Breast cancer staging: working with the sixth edition of the AJCC Cancer Staging Manual. CA Cancer J Clin. 2006;56:37–47.

    Article  PubMed  Google Scholar 

  6. Carey LA, Metzger R, Dees EC, et al. American Joint Committee on Cancer tumor-node-metastasis stage after neoadjuvant chemotherapy and breast cancer outcome. J Natl Cancer Inst. 2005;97:1137–42.

    Article  PubMed  Google Scholar 

  7. Kuerer HM, Newman LA, Smith TL, et al. Clinical course of breast cancer patients with complete pathologic primary tumor and axillary lymph node response to doxorubicin-based neoadjuvant chemotherapy. J Clin Oncol. 1999;17:460–9.

    PubMed  CAS  Google Scholar 

  8. Vassallo P, Wernecke K, Roos N, Peters PE. Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology. 1992:215–20.

  9. Feu J, Tresserra F, Fabregas R, et al. Metastatic breast carcinoma in axillary lymph nodes: in vitro US detection. Radiology. 1997;205:831–5.

    PubMed  CAS  Google Scholar 

  10. Klauber-Demore N, Kuzmiak C, Rager EL, et al. High-resolution axillary ultrasound is a poor prognostic test for determining pathologic lymph node status in patients undergoing neoadjuvant chemotherapy for locally advanced breast cancer. Am J Surg. 2004;188:386–9.

    Article  PubMed  Google Scholar 

  11. Oruwari JU, Chung MA, Koelliker S, Steinhoff MM, Cady B. Axillary staging using ultrasound-guided fine needle aspiration biopsy in locally advanced breast cancer. Am J Surg. 2002;184:307–9.

    Article  PubMed  Google Scholar 

  12. Vlastos G, Fornage BD, Mirza NQ, et al. The correlation of axillary ultrasonography with histologic breast cancer downstaging after induction chemotherapy. Am J Surg. 2000;179:446–52.

    Article  PubMed  CAS  Google Scholar 

  13. Kuerer HM, Newman LA, Fornage BD, et al. Role of axillary lymph node dissection after tumor downstaging with induction chemotherapy for locally advanced breast cancer. Ann Surg Oncol. 1998;5:673–80.

    Article  PubMed  CAS  Google Scholar 

  14. Krishnamurthy S, Sneige N, Bedi DG, et al. Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer. 2002;95:982–8.

    Article  PubMed  Google Scholar 

  15. Alkuwari E, Auger M. Accuracy of fine-needle aspiration cytology of axillary lymph nodes in breast cancer patients: a study of 115 cases with cytologic-histologic correlation. Cancer. 2008;114:89–93.

    Article  PubMed  Google Scholar 

  16. Bonnema J, van Geel AN, van Ooijen B, et al. Ultrasound-guided aspiration biopsy for detection of nonpalpable axillary node metastases in breast cancer patients: new diagnostic method. World J Surg. 1997;21:270–4.

    Article  PubMed  CAS  Google Scholar 

  17. Koelliker SL, Chung MA, Mainiero MB, Steinhoff MM, Cady B. Axillary lymph nodes: US-guided fine-needle aspiration for initial staging of breast cancer—correlation with primary tumor size. Radiology. 2008;246:81–9.

    Article  PubMed  Google Scholar 

  18. de Kanter AY, van Eijck CH, van Geel AN, et al. Multicentre study of ultrasonographically guided axillary node biopsy in patients with breast cancer. Br J Surg. 1999;86:1459–62.

    Article  PubMed  Google Scholar 

  19. Boughey JC, Middleton LP, Harker L, et al. Utility of ultrasound and fine-needle aspiration biopsy of the axilla in the assessment of invasive lobular carcinoma of the breast. Am J Surg. 2007;194:450–5.

    Article  PubMed  Google Scholar 

  20. Kvistad KA, Rydland J, Smethurst HB, et al. Axillary lymph node metastases in breast cancer: preoperative detection with dynamic contrast-enhanced MRI. Eur Radiol. 2000;10:1464–71.

    Article  PubMed  CAS  Google Scholar 

  21. Luciani A, Dao TH, Lapeyre M, et al. Simultaneous bilateral breast and high-resolution axillary MRI of patients with breast cancer: preliminary results. AJR Am J Roentgenol. 2004;182:1059–67.

    PubMed  Google Scholar 

  22. Memarsadeghi M, Riedl CC, Kaneider A, et al. Axillary lymph node metastases in patients with breast carcinomas: assessment with nonenhanced versus uspio-enhanced MR imaging. Radiology. 2006;241:367–77.

    Article  PubMed  Google Scholar 

  23. Wahl RL, Cody RL, Hutchins GD, Mudgett EE. Primary and metastatic breast carcinoma: initial clinical evaluation with PET with the radiolabeled glucose analogue 2-[F-18]-fluoro-2-deoxy-D-glucose. Radiology. 1991;179:765–70.

    PubMed  CAS  Google Scholar 

  24. Nieweg OE, Kim EE, Wong WH, et al. Positron emission tomography with fluorine-18-deoxyglucose in the detection and staging of breast cancer. Cancer. 1993;71:3920–5.

    Article  PubMed  CAS  Google Scholar 

  25. Avril N, Dose J, Janicke F, et al. Metabolic characterization of breast tumors with positron emission tomography using F-18 fluorodeoxyglucose. J Clin Oncol. 1996;14:1848–57.

    PubMed  CAS  Google Scholar 

  26. Greco M, Crippa F, Agresti R, et al. 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;93:630–5.

    Article  PubMed  CAS  Google Scholar 

  27. Wahl RL, Siegel BA, Coleman RE, Gatsonis CG. 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;22:277–85.

    Article  PubMed  Google Scholar 

  28. 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.

    Article  PubMed  Google Scholar 

  29. Chung MH, Ye W, Giuliano AE. Role for sentinel lymph node dissection in the management of large (> or = 5 cm) invasive breast cancer. Ann Surg Oncol. 2001;8:688–92.

    PubMed  CAS  Google Scholar 

  30. Lyman GH, Giuliano AE, Somerfield MR, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23:7703–20.

    Article  PubMed  Google Scholar 

  31. Piato JR, Barros AC, Pincerato KM, Sampaio AP, Pinotti JA. Sentinel lymph node biopsy in breast cancer after neoadjuvant chemotherapy. A pilot study. Eur J Surg Oncol. 2003;29:118–20.

    Article  PubMed  Google Scholar 

  32. Hunt KK, Yi M, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy is accurate and reduces the need for axillary dissection in breast cancer patients. Ann Surg. 27 Aug 2009 [Epub ahead of print].

  33. Tafra L, Verbanac KM, Lannin DR. Preoperative chemotherapy and sentinel lymphadenectomy for breast cancer. Am J Surg. 2001;182:312–5.

    Article  PubMed  CAS  Google Scholar 

  34. Xing Y, Foy M, Cox DD, et al. Meta-analysis of sentinel lymph node biopsy after preoperative chemotherapy in patients with breast cancer. Br J Surg. 2006;93:539–46.

    Article  PubMed  CAS  Google Scholar 

  35. Mamounas EP, Brown A, Anderson S, et al. Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol. 2005;23:2694–702.

    Article  PubMed  Google Scholar 

  36. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391–8.

    Article  PubMed  CAS  Google Scholar 

  37. Roumen RM, Valkenburg JG, Geuskens LM. Lymphoscintigraphy and feasibility of sentinel node biopsy in 83 patients with primary breast cancer. Eur J Surg Oncol. 1997;23:495–502.

    Article  PubMed  CAS  Google Scholar 

  38. Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer—a multicenter validation study. N Engl J Med. 1998;339:941–6.

    Article  PubMed  CAS  Google Scholar 

  39. Crossin JA, Johnson AC, Stewart PB, Turner WW Jr. Gamma-probe-guided resection of the sentinel lymph node in breast cancer. Am Surg. 1998;64:666–8.

    PubMed  CAS  Google Scholar 

  40. Snider H, Dowlatshahi K, Fan M, et al. Sentinel node biopsy in the staging of breast cancer. Am J Surg. 1998;176:305–10.

    Article  PubMed  CAS  Google Scholar 

  41. O’Hea BJ, Hill AD, El-Shirbiny AM, et al. Sentinel lymph node biopsy in breast cancer: initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg. 1998;186:423–7.

    Article  PubMed  Google Scholar 

  42. Cox CE, Bass SS, McCann CR, et al. Lymphatic mapping and sentinel lymph node biopsy in patients with breast cancer. Annu Rev Med. 2000;51:525–42.

    Article  PubMed  CAS  Google Scholar 

  43. Noguchi M, Motomura K, Imoto S, et al. A multicenter validation study of sentinel lymph node biopsy by the Japanese Breast Cancer Society. Breast Cancer Res Treat. 2000;63:31–40.

    Article  PubMed  CAS  Google Scholar 

  44. Lauridsen MC, Garne JP, Hessov I, et al. Sentinel lymph node biopsy in breast cancer—the Aarhus experience. Acta Oncol. 2000;39:421–2.

    Article  PubMed  CAS  Google Scholar 

  45. Fraile M, Rull M, Julian FJ, et al. Sentinel node biopsy as a practical alternative to axillary lymph node dissection in breast cancer patients: an approach to its validity. Ann Oncol. 2000;11:701–5.

    Article  PubMed  CAS  Google Scholar 

  46. Molland JG, Dias MM, Gillett DJ. Sentinel node biopsy in breast cancer: results of 103 cases. Aust N Z J Surg. 2000;70:98–102.

    Article  PubMed  CAS  Google Scholar 

  47. Canavese G, Gipponi M, Catturich A, et al. Technical issues and pathologic implications of sentinel lymph node biopsy in early-stage breast cancer patients. J Surg Oncol. 2001;77:81–7.

    Article  PubMed  CAS  Google Scholar 

  48. Schrenk P, Wayand W. Sentinel-node biopsy in axillary lymph-node staging for patients with multicentric breast cancer. Lancet. 2001;357(9250):122.

    Article  PubMed  CAS  Google Scholar 

  49. Giuliano AE, Haigh PI, Brennan MB, et al. Prospective observational study of sentinel lymphadenectomy without further axillary dissection in patients with sentinel node-negative breast cancer. J Clin Oncol. 2000;18:2553–9.

    PubMed  CAS  Google Scholar 

  50. Sabel MS, Schott AF, Kleer CG, et al. Sentinel node biopsy prior to neoadjuvant chemotherapy. Am J Surg. 2003;186:102–5.

    Article  PubMed  Google Scholar 

  51. Ollila DW, Neuman HB, Sartor C, Carey LA, Klauber-Demore N. Lymphatic mapping and sentinel lymphadenectomy prior to neoadjuvant chemotherapy in patients with large breast cancers. Am J Surg. 2005;190:371–5.

    Article  PubMed  Google Scholar 

  52. Jones JL, Zabicki K, Christian RL, et al. A comparison of sentinel node biopsy before and after neoadjuvant chemotherapy: timing is important. Am J Surg. 2005;190:517–20.

    Article  PubMed  Google Scholar 

  53. Bonadonna G, Valagussa P, Brambilla C, et al. Primary chemotherapy in operable breast cancer: eight-year experience at the Milan Cancer Institute. J Clin Oncol. 1998;16:93–100.

    PubMed  CAS  Google Scholar 

  54. Cutler SJ, Axtell LM, Schottenfeld D, Farrow JH. Clinical assessment of lymph nodes in carcinoma of the breast. Surg Gynecol Obstet. 1970;131:41–52.

    PubMed  CAS  Google Scholar 

  55. Fisher B, Wolmark N, Bauer M, Redmond C, Gebhardt M. The accuracy of clinical nodal staging and of limited axillary dissection as a determinant of histologic nodal status in carcinoma of the breast. Surg Gynecol Obstet. 1981;152:765–72.

    PubMed  CAS  Google Scholar 

  56. Sacre RA. Clinical evaluation of axillar lymph nodes compared to surgical and pathological findings. Eur J Surg Oncol. 1986;12:169–73.

    PubMed  CAS  Google Scholar 

  57. de Freitas R Jr, Costa MV, Schneider SV, Nicolau MA, Marussi E. Accuracy of ultrasound and clinical examination in the diagnosis of axillary lymph node metastases in breast cancer. Eur J Surg Oncol. 1991;17:240–4.

    PubMed  Google Scholar 

  58. Vaidya JS, Vyas JJ, Thakur MH, Khandelwal KC, Mittra I. Role of ultrasonography to detect axillary node involvement in operable breast cancer. Eur J Surg Oncol. 1996;22:140–3.

    Article  PubMed  CAS  Google Scholar 

  59. Miller AR, Thomason VE, Yeh IT, et al. Analysis of sentinel lymph node mapping with immediate pathologic review in patients receiving preoperative chemotherapy for breast carcinoma. Ann Surg Oncol. 2002;9:243–7.

    Article  PubMed  Google Scholar 

  60. Haid A, Tausch C, Lang A, et al. Is sentinel lymph node biopsy reliable and indicated after preoperative chemotherapy in patients with breast carcinoma? Cancer. 2001;92:1080–4.

    Article  PubMed  CAS  Google Scholar 

  61. Julian TB, Dusi D, Wolmark N. Sentinel node biopsy after neoadjuvant chemotherapy for breast cancer. Am J Surg. 2002;184:315–7.

    Article  PubMed  Google Scholar 

  62. Brady EW. Sentinel lymph node mapping following neoadjuvant chemotherapy for breast cancer. Breast J. 2002;8:97–100.

    Article  PubMed  Google Scholar 

  63. Tanaka Y, Maeda H, Ogawa Y, et al. Sentinel node biopsy in breast cancer patients treated with neoadjuvant chemotherapy. Oncol Rep. 2006;15:927–31.

    PubMed  Google Scholar 

  64. Balch GC, Mithani SK, Richards KR, Beauchamp RD, Kelley MC. Lymphatic mapping and sentinel lymphadenectomy after preoperative therapy for stage II and III breast cancer. Ann Surg Oncol. 2003;10:616–21.

    Article  PubMed  Google Scholar 

  65. Yu JC, Hsu GC, Hsieh CB, Yu CP, Chao TY. Role of sentinel lymphadenectomy combined with intraoperative ultrasound in the assessment of locally advanced breast cancer after neoadjuvant chemotherapy. Ann Surg Oncol. 2007;14:174–80.

    Article  PubMed  Google Scholar 

  66. Tausch C, Konstantiniuk P, Kugler F, et al. Sentinel lymph node biopsy after preoperative chemotherapy for breast cancer: findings from the Austrian Sentinel Node Study Group. Ann Surg Oncol. 2008;15:3378–83.

    Article  PubMed  Google Scholar 

  67. Newman EA, Sabel MS, Nees AV, et al. Sentinel lymph node biopsy performed after neoadjuvant chemotherapy is accurate in patients with documented node-positive breast cancer at presentation. Ann Surg Oncol. 2007;14:2946–52.

    Article  PubMed  Google Scholar 

  68. Schwartz GF, Meltzer AJ. Accuracy of axillary sentinel lymph node biopsy following neoadjuvant (induction) chemotherapy for carcinoma of the breast. Breast J. 2003;9:374–9.

    Article  PubMed  Google Scholar 

  69. Kang SH, Kang JH, Choi EA, Lee ES. Sentinel lymph node biopsy after neoadjuvant chemotherapy. Breast Cancer. 2004;11:233–41.

    Article  PubMed  Google Scholar 

  70. Classe JM, Bordes V, Campion L, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy for advanced breast cancer: results of Ganglion Sentinelle et Chimiotherapie Neoadjuvante, a French prospective multicentric study. J Clin Oncol. 2009;27:726–32.

    Article  PubMed  Google Scholar 

  71. Breslin TM, Cohen L, Sahin A, et al. Sentinel lymph node biopsy is accurate after neoadjuvant chemotherapy for breast cancer. J Clin Oncol. 2000;18:3480–6.

    PubMed  CAS  Google Scholar 

  72. Stearns V, Ewing CA, Slack R, et al. Sentinel lymphadenectomy after neoadjuvant chemotherapy for breast cancer may reliably represent the axilla except for inflammatory breast cancer. Ann Surg Oncol. 2002;9:235–42.

    Article  PubMed  Google Scholar 

  73. Gimbergues P, Abrial C, Durando X, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy is accurate in breast cancer patients with a clinically negative axillary nodal status at presentation. Ann Surg Oncol. 2008;15:1316–21.

    Article  PubMed  CAS  Google Scholar 

  74. Lee S, Kim EY, Kang SH, et al. Sentinel node identification rate, but not accuracy, is significantly decreased after pre-operative chemotherapy in axillary node–positive breast cancer patients. Breast Cancer Res Treat. 2007;102:283–8.

    Article  PubMed  CAS  Google Scholar 

  75. Kinoshita T, Takasugi M, Iwamoto E, et al. Sentinel lymph node biopsy examination for breast cancer patients with clinically negative axillary lymph nodes after neoadjuvant chemotherapy. Am J Surg. 2006;191:225–9.

    Article  PubMed  Google Scholar 

  76. Fernandez A, Cortes M, Benito E, et al. Gamma probe sentinel node localization and biopsy in breast cancer patients treated with a neoadjuvant chemotherapy scheme. Nucl Med Commun. 2001;22:361–6.

    Article  PubMed  CAS  Google Scholar 

  77. Nason KS, Anderson BO, Byrd DR, et al. Increased false negative sentinel node biopsy rates after preoperative chemotherapy for invasive breast carcinoma. Cancer. 2000;89:2187–94.

    Article  PubMed  CAS  Google Scholar 

  78. Cox CE, Cox JM, White LB, et al. Sentinel node biopsy before neoadjuvant chemotherapy for determining axillary status and treatment prognosis in locally advanced breast cancer. Ann Surg Oncol. 2006;13:483–90.

    Article  PubMed  Google Scholar 

  79. van Rijk MC, Nieweg OE, Rutgers EJ, et al. Sentinel node biopsy before neoadjuvant chemotherapy spares breast cancer patients axillary lymph node dissection. Ann Surg Oncol. 2006;13:475–9.

    Article  PubMed  Google Scholar 

  80. Schrenk P, Tausch C, Wolfl S, et al. Sentinel node mapping performed before preoperative chemotherapy may avoid axillary dissection in breast cancer patients with negative or micrometastatic sentinel nodes. Am J Surg. 2008;196:176–83.

    Article  PubMed  Google Scholar 

  81. Menard JP, Extra JM, Jacquemier J, et al. Sentinel lymphadenectomy for the staging of clinical axillary node-negative breast cancer before neoadjuvant chemotherapy. Eur J Surg Oncol. 2009;35:916–20.

    PubMed  Google Scholar 

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  1. Department of Surgical Oncology, John Wayne Cancer Institute at Saint John’s Health Center, 2200 Santa Monica Blvd., Santa Monica, CA, USA

    Alice Chung MD & Armando Giuliano MD

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  1. Alice Chung MD
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  2. Armando Giuliano MD
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Correspondence to Alice Chung MD.

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Chung, A., Giuliano, A. Axillary Staging in the Neoadjuvant Setting. Ann Surg Oncol 17, 2401–2410 (2010). https://doi.org/10.1245/s10434-010-1001-8

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