Abstract
Surgeons have routinely removed ipsilateral axillary lymph nodes from women with breast cancer for over 100 years. The procedure provides important staging information, enhances regional control of the malignancy and may improve survival. As screening of breast cancer has increased, the mean size of newly diagnosed primary invasive breast cancers has steadily decreased and so has the number of women with lymph node metastases. Recognising that the therapeutic benefit of removing normal nodes may be low, alternatives to the routine level I/II axillary lymph node dissection have been sought. A decade ago sentinel lymph node biopsy (SLNB) was introduced. Because of its high accuracy and relatively low morbidity, this technique is now widely used to identify women with histologically involved nodes prior to the formal axillary node dissection. Specifically, SLNB has allowed surgeons to avoid a formal axillary lymph node biopsy in women with histologically uninvolved sentinel nodes, while identifying women with involved sentinel nodes who derive the most benefit from a completion axillary node dissection. Despite the increasing use of SLNB for initial management of the axilla in women with breast cancer, important questions remain regarding patient selection criteria and optimal surgical methods for performing the biopsy. This article discusses the evolution of axillary node surgery for women with breast cancer.
Similar content being viewed by others
References
Halsted WS (1898) A clinical and histological study of certain adenocarcinoma of the breast and a brief consideration of the supraclavicular operation and of the results of operation for cancer of the breast from 1989 to 1898 at the Johns Hopkins Hospital. Ann Surg 28:557–576
Halsted WS (1894) The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June 1889 to January 1894. Ann Surg 20:497–555
Bonnadonna G, Valagussa P (1988) The contribution of medicine to the primary treatment of breast cancer. Cancer Res 48:2314–2324
Lacour J, Bucalossi P, Cacers E et al (1976) Radical mastectomy versus radical mastectomy plus internal mammary dissection. Cancer 37:206–214
Urban JA, Marjoni MA (1971) Significance of internal mammary lymph node metastases in breast cancer. AJR Am J Roentgenol 111:130–136
Veronesi U, Cascinelli N, Mariani L et al (2002) Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 347:1227–1232
Mena A, Garcia A, Moreno L et al (2005) Conservative treatment for infiltrating breast cancer. Ten years follow-up experience. Clin Transl Oncol 8:672–675
Monteiro-Grillo I, Marques-Vidal P, Jorge M (2005) Psychosocial effect of mastectomy versus conservative surgery in patients with early breast cancer. Clin Transl Oncol 7:499–503
Fisher B, Redmond C, Fisher E et al (1985) Ten year results of a randomized clinical trial comparing radical mastectomy and total mastectomy with or without radiation. N Engl J Med 312:674–681
Cancer Research Campaign Working Party (1980) Cancer Research Campaign (King’s/ Cambridge) trial for early breast cancer. Lancet 2:55–60
Mittra I (1993) Axillary lymph node metastasis in breast cancer: prognostic indicator or leadtime bias? Eur J Cancer 29:300–302
Giuliano AE, Kigram DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–401
Krag DN, Weaver DL, Alex JC, Fairbank JT (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335
Uhm JH, Dooley NP, Athanassios P (1999) Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells form apoptotic death. Clin Cancer Res 5:1587–1594
Cassella M, Skobe M (2002) Lymphatic vessel activation in cancer. Ann NY Acad Sci 979:120–130
Achen MG, Mann GB, Stacker SA (2006) Targeting lymphangiogenesis to prevent tumour metastasis. Br J Cancer 94:1355–1360
Carr I, Watson P, Petigrew NM (1989) Mechanisms of invasion and lymphatic penetration in human colorectal cancer. Clin Exp Metastasis 7:507–516
Gervasoni JE, Taneja C, Chung MD, Cady B (2000) Biologic and clinical significance of lymphadenectomy. Surg Clin North Am 80:1631
Hoon DSB, Korn EL, Cochran AJ (1987) Variations in functional immunocompetence of individual tumor-draining lymph nodes in humans. Cancer Res 47:1740–1744
Leong SP (2004) Paradigm of metastasis for melanoma and breast cancer based on the sentinel lymph node experience. Ann Surg Oncol 11:192S–197S
Jatoi I (2001) Surgery for primary invasive breast cancer. In: Jatoi I (ed.) Manual of breast diseases. Lippincott, Williams and Wilkins, Philadelphia, pp 289–307
Schnitt SJ (2001) Traditional and newer pathologic factors. J Natl Cancer Inst Monogr 30:22–26
Heimann R, Hellman S (2000) Clinical progression of breast cancer malignant behavior: what to expect and when to expect it. J Clin Oncol 18:591
Cady B (1997) Case against axillary lymphadenectomy for most patients with infiltrating breast cancer. J Surg Oncol 66:7–10
Mincey BA, Palmieri FM, Perez EA (2002) Adjuvant therapy for breast cancer: recommendations for management based on consensus review and recent clinical trials. Oncologist 7:246–250
Morrow M (1996) Axillary dissection: when and how radical? Semin Surg Oncol 12:321–327
Fitzgibbons PL, Page DL, Weaver D et al (2000) Prognostic factors in breast cancer. College of American Pathologists consensus statement 1999. Arch Path Lab Med 124:966–978
Liberman L (2000) Pathologic analysis of sentinel lymph nodes in breast carcinoma. Cancer 88:971–977
Giuliano AE, Dale PS, Turner RR et al (1995) Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 222:394–399
Braun S, Cevatli BS, Assemi C et al (2001) Comparative analysis of micrometastasis to the bone marrow and lymph nodes of node-negative breast cancer patients receiving. J Clin Oncol 19:1468–1475
Singletary SE, Allred C, Ashley P et al (2002) Part VII. Breast. In: Greene FL, Page DL, Fleming ID (eds) American Joint Committee on Cancer Manual (6th Edn). Springer-Verlag, New York, pp 221–240
Jatoi I, Hilsenbeck SG, Clark GM, Osborne CK (1999) Significance of axillary lymph node metastasis in primary breast cancer. J Clin Oncol 17:2334–2340
Early Breast Cancer Trialists’ Collaborative Group (1998) Polychemotherapy for early breast cancer: an overview of the randomised trials. Lancet 352:930–942
Early Breast Cancer Collaborative Group (1998) Tamoxifen for early breast cancer: an overview of the randomized trials. Lancet 351:1451–1467
Bland KI, Menck HR, Scott-Conner CEH et al (1998) The National Cancer Data Base 10-year survey of breast cancer treatment at hospitals in the United States. Cancer 83:1262–1273
Wong JS, Recht A, Beard CJ et al (1997) Treatment outcome after tangential radiation therapy without axillary dissection in patients with early stage breast cancer and clinically negative axillary nodes. Int J Radiat Oncol Biol Phys 9:119–132
Greco M, Agresti R, Raselli R et al (1996) Axillary dissection can be avoided in selected breast cancer patients: analysis of 401 cases. Anticancer Res 16:3913–3917
Silverstein MJ, Gierson ED, Waisman JR et al (1995) Predicting axillary node positivity in patients with invasive carcinoma of the breast by using a combination of T category and palpability. J Am Coll Surg 180:700–704
Rosen PP, Groshen S, Saigo PE et al (1989) A long term follow-up study of survival in stage I (T1N0M0) and stage II (T1N1M0) breast carcinoma. J Clin Oncol 7:355–366
Carter CL, Allen C, Henson DE (1989) Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 63:181–187
Sacks NP, Baum M (1993) Primary management of carcinoma of the breast. Lancet 342:1402–1408
Graversen HP, Blichert-Toft M, Andersen J et al (1988) Breast cancer: risk of axillary recurrence in node-negative patients following partial dissection of the axilla. Eur J Surg Oncol 14:407–412
Veronesi U, Luini A, Galimberti V et al (1990) Extent of metastatic axillary involvement in 1446 cases of breast cancer. Eur J Surg Oncol 16:127–133
Ragaz J, Jackson SM, Le N et al (1997) Adjuvant radiotherapy and chemotherapy in nodepositive premenopausal women with breast cancer. N Engl J Med 337:956–962
Overgaard M, Hansen PS, Overgaard J et al (1997) Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. Danish Breast Cancer Cooperative Group 82b. N Engl J Med 337:949–955
Diab SG, Hilsenbeck SG, de Moor C (1998) Radiation therapy and survival in breast cancer patients with 10 or more positive axillary lymph nodes treated with mastectomy. J Clin Oncol 16:1655–1660
Axelsson C, Mouridsen H, Zedeler K (1992) Axillary dissection of level I and II lymph nodes is important in breast cancer classification. The Danish Breast Cancer Cooperative Group (DBCG). Eur J Cancer 28A:1415–1418
Recht A, Pierce SM, Abner A et al (1991) Regional nodal failure after conservative surgery and radiotherapy for early-stage breast carcinoma. J Clin Oncol 9:988–996
Graverson HP, Blichert-Toft M, Andersen J et al (1988) Breast cancer: risk of axillary recurrence in node-negative patients following partial dissection of the axilla. Eur J Surg Oncol 14:407–412
Steele RJ, Forrest AP, Gibson T et al (1985) The efficacy of lower axillary sampling in obtaining lymph node status in breast cancer: A controlled randomized trial. Br J Surg 72:368–369
Kissin MW, Thompson EM, Price AB et al (1982) The inadequacy of axillary sampling in breast cancer. Lancet 1:1210–1212
Alhlgren J, Holmberg L, Bergh J, Liljegren G (2002) Five-node biopsy of the axilla: an alternative to axillary dissection of levels I-II in operable breast cancer. Eur J Surg Oncol 28:97–102
Macmillan R, Barbera D, Hadjiminas DJ (2001) Sentinel node biopsy for breast cancer may have little to offer four-node-samplers: results of a prospective comparison study. Eur J Cancer 37:1076–1080
Du Toit RS, Locker AP, Ellis IO et al (1990) Evaluation of the prognostic value of triple node biopsy in early breast cancer. Br J Surg 77:163
Amalric R, Santamaria F, Robert F et al (1982) Radiation therapy with or without primary limited surgery for operable breast cancer. Cancer 49:30
Olsen NK, Pfeiffer P, Johannsen L et al (1993) Radiation-induced brachial plexopathy: neurological follow-up in 161recurrence-free breast cancer patients. Int J Radiat Oncol Biol 26:43
Bland KI, Coburn MC (1998) Wound care and complications of mastectomy. In: Bland KI, Copeland EM (eds) The breast. Comprehensive management of benign and malignant diseases. W.B. Saunders Company, Philadelphia, pp 995–1002
Liljegren G, Holmberg L, The Upsala-Oregro Breast Cancer Study Group (1997) Arm morbidity after sector resection and axillary dissection with or without postoperative radiotherapy in breast cancer stage I. Results from a randomised trial. Uppsala-Orebro Breast Cancer Study Group. Eur J Cancer 33:193–199
Hladiuk M, Huchcroft S, Temple W, Schnurr BE (1992) Arm function after axillary dissection for breast cancer. J Surg Oncol 50:47–52
Gonzalez EA, Saltzstein EC, Riedner CS, Nelson BK (2003) Seroma formation following breast cancer surgery. Breast J 9:385–388
Reintgen DS, Cox CE, Puleo CA (1998) Lymphedema in the postmastectomy patient: pathophysiology, prevention, and management. In: Bland KI, Copeland EM (eds) The breast. Comprehensive management of benignant and malignant diseases. W.C. Saunders Company, Philadelphia, pp 1003–1011
Soran A, D’Angelo G, Begovic M et al (2006) Risk factors and severity of lymphedema. Breast J 12:536–543
Golshan M, Martin WJ, Dowlatshahi K (2003) Sentinel lymph node biopsy lowers the rate of lymphedema when compared with standard axillary lymph node dissection. Am Surg 69:209–211
Chua B, Ung O, Taylor R, Boyages J (2003) Is information from axillary dissection relevant to patients with clinically node-negative breast cancer? Breast J 9:478
Cody HS (2003) Sentinel lymph node biopsy for breast cancer: does anybody not need one? Ann Surg Oncol 10:1131–1132
Goldhirsch A, Wood WC, Gelber RD et al (2003) Meeting highlights: updated international expert consensus on the primary therapy of early breast cancer. J Clin Oncol 21:3357–3365
Martelli G, Miceli R, De Palo G et al (2003) Is axillary lymph node dissection necessary in elderly patients with breast carcinoma who have a clinically uninvolved axilla? Cancer 97:1156–1163
Martelli G, Borachi P, De Palo M et al (2005) A randomized trial comparing axillary dissection to no axillary dissection in older patients with T1N0 breast cancer. Results after 5 years of follow-up. Ann Surg 242:1–6
Favret AM, Carlson RW, Goffinet DR et al (2001) Locally advanced breast cancer: is surgery necessary? Breast J 7:131–137
Veronesi U, Paganelli G, Viale G et al (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349:546–553
Schwartz GF, Giuliano AE, Veronesi U (2002) Proceedings of the Consensus Conference on the role of sentinel node biopsy in carcinoma of the breast, April 19–22, 2001, Pennsylvania. Cancer 94:2542–2551
Van Rijk MC, Tanis PJ, Nieweg OE et al (2006) Clinical implications of sentinel nodes outside the axilla and internal mammary chain in patients with breast cancer. J Surg Oncol 94:266–268
Senn HJ, Thurlimann B, Goldhirsch A et al (2003) Comments on the Saint Gallen consensus 2003 on the Primary Therapy of Early Breast Cancer. Breast 12:569–582
Recht A (1999) Should irradiation replace dissection for patients with breast cancer with clinically negative axillary lymph nodes? J Surg Oncol 72:184
Fraile M, Rull M, Julian FJ et al (2000) Sentinel node biopsy as a practical alternative to axillary lymph node dissection in breast cancer patients: an approach to its validity. Ann Oncol 11:701–05
McMasters KM (2003) The eternally enigmatic axilla: further controversy about axillary lymph nodes in breast cancer. Ann Surg Oncol 10:1128–1130
Hwang RF, Krishnamurthy S, Hunt KK et al (2003) Clinicopathologic factors predicting involvement of nonsentinel axillary nodes in women with breast cancer. Ann Surg Oncol 10:248–254
Callejo IP, Brito JA, Bivar JW et al (2005) Predictors of positive axillary lymph nodes in breast cancer patients with metastatic sentinel lymph node. Clin Transl Oncol 7:18–22
Cserni G, Gregori D, Merlleti F et al (2004) Meta-analysis of non-sentinel node metastases associated with micrometastatic sentinel nodes in breast cancer. Br J Surg 91:1245–1252
Viale G, Maiorano E, Pruneri G et al (2005) Predicting the risk for additional axillary metastases in patients with breast carcinoma and positive sentinel lymph node biopsy. Ann Surg 241:319–325
Houvenaeghel G, Nos C, Mignotte H et al (2006) Micrometastases in sentinel lymph node in a multicentric study: predictive factors of nonsentinel lymph node involvement — Groupe des Chirurgiens de la Federation des Centres de Lutte Contre le Cancer. J Clin Oncol 24:1814–1822
Van Rijk MC, Peterse JL, Nieweg OE et al (2006) Additional axillary metastases and stage migration in breast cancer patients with micrometastases or submicrometastases in sentinel lymph nodes. Cancer 107:467–471
Reynolds C, Mick R, Donohue JH et al (1999) Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol 17:1720–1726
Wong SL, Edwards MJ, Chao C et al (2001) Predicting the status of non-sentinel axillary nodes: a multicenter study. Arch Surg 136:563–568
Jakub JW, Pendas S, Reintgen DS (2003) Current status of sentinel lymph node mapping and biopsy: facts and controversies. Oncologist 8:59–68
Turner RR, Chu KU, Qi K et al (2000) Pathologic features associated with nonsentinel lymph node metastases in patients with metastatic breast carcinoma in a sentinel lymph node. Cancer 89:574–581
Louis-Sylvestre C, Clough K, Asselain B et al (2004) Axillary treatment in conservative management of operable breast cancer: dissection or radiotherapy? Results of a randomized study with 15 years of follow-up. J Clin Oncol 22:97–101
Goyal A, Mansel RE (2004) Current status of sentinel lymph node biopsy in solid malignancies. World J Surg Oncol 2(1):9
Buchholz TA, Strom EA, McNeese M et al (2003) Radiation therapy as an adjuvant treatment after sentinel lymph node surgery for breast cancer. Surg Clin North Am 83:911–930
Guenther JM, Hansen NM, DiFronzo LA et al (2003) Axillary dissection is not required for all patients with breast cancer and positive sentinel nodes. Arch Surg 138:52–56
Fant JS, Grant MD, Know SM et al (2003) Preliminary outcome analysis in patients with breast cancer and a positive sentinel lymph node who declined axillary dissection. Ann Surg Oncol 10:126–130
Langer I, Marti WR, Guller U et al (2005) Axillary recurrence rate in breast cancer patients with negative sentinel lymph node (SLN) or SLN micrometastases: prospective analysis of 150 patients after SLN biopsy. Ann Surg 241:152–158
Shimazu K, Tamaki Y, Taguchi T et al (2003) Lymphoscintigraphic visualization of internal mammary nodes with subtumoral injection of radiocolloid in patients with breast cancer. Ann Surg 237:390–398
Clarke D, Newcombe RG, Mansel RE. ALMANAC Trialists Group (2004) The learning curve in sentinel node biopsy: The ALMANAC experience. Ann Surg Oncol 11[2 Suppl]:2115–2155
Wong SL, Edwards MJ, Chao C et al (2002) The effect of prior breast axilla biopsy method and concurrent definitive breast procedure on success and accuracy of sentinel lymph node biopsy. Ann Surg Oncol 9:272–277
Luini A, Galimberti V, Gatti G et al (2005) The sentinel node biopsy after previous breast surgery: preliminary results on 543 patients treated at the European Institute of Oncology. Breast Cancer Res Treat 89:159–163
Haigh PI, Hansen NM, Qi K et al (2000) Biopsy method and excision volume do not affect success rate of subsequent sentinel lymph node dissection in breast cancer. Ann Surg Oncol 7:21–27
Tousimis E, Van Zee KJ, Fey JV et al (2003) The accuracy of sentinel lymph node biopsy in multicentric and multifocal breast cancers. J Am Coll Surg 197:529–535
Liberman L, Cody HIS (2001) Percutaneous biopsy and sentinel lymphadenectomy: minimally invasive diagnosis and treatment of nonpalpable breast cancer. AJR Am J Roentgenol 177:887–891
Dupont EL, Kuhn MA, McCann C et al (2000) The role of sentinel lymph node biopsy in women undergoing prophylactic mastectomy. Am J Surg 180:274–277
Port ER, Fey J, Gemignani ML et al (2002) Reoperative sentinel lymph node biopsy: a new option for patients with primary or locally recurrent breast carcinoma. J Am Coll Surg 195:167–172
Mamounas A, Brown A, Anderson S et al (2005) Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 23:2694–2702
Stearns V, Ewing CA, Slack R et al (2002) Sentinel lymphadenectomy after neoadjuvant chemotherapy for breast cancer may reliably represent the axilla except for inflammatory breast cancer. Ann Surg Oncol 9:235–242
Cox CE, Cox JM, White LB et al (2006) Sentinel node biopsy before neoadjuvant chemotherapy for determining axillary status and treatment prognosis in locally advanced breast cancer. Ann Surg Oncol 13:483–490
Waddington WA, Keshtgar MR, Taylor I et al (2000) Radiation safety of the sentinel lymph node technique in breast cancer. Eur J Nucl Med 27:377–391
Spetch MC, Fey JV, Borgen PI, Cody HS (2005) Is the clinically positive axilla in breast cancer really a contraindication to sentinel lymph node biopsy? J Am Coll Surg 200:100–104
Intra M, Veronesi P, Mazzarol G et al (2003) Axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. Arch Surg 138:309–313
González-Palacios Martínez JF (2004) Una nueva modificación en la clasificación TNM del cáncer mamario. Rev Esp Patol 37:247–251
Hermanek P, Hutter RVP, Sobin LH, Wittekind C (1999) Classification of isolated tumor cells and micrometastasis. Cancer 86:2668–2673
Veronesi U, Marubini E, Mariani L et al (1999) The dissection of internal mammary nodes does not improve the survival of breast cancer patients: 30-year results of a randomized trial. Eur J Cancer 35:1320–1325
Thor A (2004) A revised Staging System for Breast Cancer. Breast J 10[Suppl 1]:S15–S18
Hortobagyi G (2000) Adjuvant therapy for breast cancer. Annu Rev Med 51:377–392
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Millet, A., Fuster, C.A., Lluch, A. et al. Axillary surgery in breast cancer patients. Clin Transl Oncol 9, 513–520 (2007). https://doi.org/10.1007/s12094-007-0095-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12094-007-0095-3