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Indian Journal of Surgical Oncology logoLink to Indian Journal of Surgical Oncology
. 2010 Aug 7;1(1):27–36. doi: 10.1007/s13193-010-0008-8

Value of frozen section and primary tumor factors in determining sentinel lymph node spread in early breast carcinoma

Rajshekhar C Jaka 1,, Shabber S Zaveri 1, S P Somashekhar 1, Sureshchandra 1, R V Parameswaran 1
PMCID: PMC3420992  PMID: 22930615

Abstract

Introduction

Sentinel lymph node biopsy (SLNB) is the standard of care to assess the metastasis in breast carcinoma. Accuracy of intraoperative frozen section examination to evaluate SLN in detecting metastasis is important as it determines the further management of axilla. Primary tumor characteristics determining the metastasis to the lymph node will help in predicting the probability of spread and to determine the nature of disease. It also helps in refining selection of patients for SLNB. We evaluated all these criteria on Indian patients for the better management.

Materials and methods

Between January 2005 and April 2009, 114 consecutive patients of all age group of both sex, with cytology or biopsy proven carcinoma breast, clinical stage T1/T2 N0 M0 at Manipal Comprehensive Cancer Center, Manipal Hospital, Bangalore were subjected to SLNB and introperative frozen examination. First 75 cases had complete axillary clearance irrespective of SLNB result and subsequently, positive cases underwent axillary lymph node dissection (ALND). Age of the patient and primary tumor characteristics like size, grade, lymphovascular invasion (LVI), perineural invasion, ER/PR status, Her2-neu status and histological sub-types were evaluated for predicting the SLN metastasis. Feasibility of SLNB in previously treated patient is also evaluated.

Results

The age of the patient ranged from 23 to 87 years and its association with SLN spread is not significant. Frozen section examination had accuracy of 97.37% in determining metastatic sentinel node with sensitivity of 96.15% and specificity of 100% with value P < 0.001. SLN remained significant indicator of the status of rest of axilla with value P < 0.001. Primary tumor characteristics like histological subtypes, grade (P = 0.353), ER/PR status (P = 0.839), Her2-neu status (P =0.296) were not significantly associated with SLN metastasis. Size of the primary tumor (P = 0.002), LVI (P < 0.001), perineural invasion (P = 0.084+) were significant factors determining the SLN metastasis. SLNB evaluation had no false negative values in previously treated breast.

Conclusion

SLNB is a valuable method of determining the axillary nodal metastasis. Intraoperative frozen section examination is highly ac-curate in detecting nodal metastasis. Primary tumor characteristics like size, LVI and perineural invasion are significant in predicting SLN metastasis. SLNB remains an important method of predicting axillary metastasis even in previously treated breast carcinomas.

Keywords: Sentinel lymph node, Breast carcinoma, Metastasis

References

  • 1.Veronesi U., Paganelli G., Galimberti V., et al. Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymphnodes. Lancet. 1997;349(9069):1864–1867. doi: 10.1016/S0140-6736(97)01004-0. [DOI] [PubMed] [Google Scholar]
  • 2.Turner R.R., Ollila D.W., Krasne D.L., Giuliano A.E. Histopathologic validation of the sentinel lymph node hypothesis for breast carcinoma. Ann Surg. 1997;226(3):271–276. doi: 10.1097/00000658-199709000-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Giuliano A.E., Jones R.C., Brennan M., Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol. 1997;15(6):2345–2350. doi: 10.1200/JCO.1997.15.6.2345. [DOI] [PubMed] [Google Scholar]
  • 4.Yiangou C., Shousha S., Sinnett H.D. Primary tumour characteristics and axillary lymph node status in breast cancer. Br J Cancer. 1999;80:1974–1978. doi: 10.1038/sj.bjc.6690629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Rivadeneira D.E., Simmons R.M., Christos P.J., Hanna K., Daly J.M., Osborne M.P. Predictive factors associated with axillary lymph node metastases in T1a and T1b breast carcinomas. J Am Coll Surg. 2000;191:1–8. doi: 10.1016/S1072-7515(00)00310-0. [DOI] [PubMed] [Google Scholar]
  • 6.Gajdos C., Tartter P.I., Bleiweiss I.J. Lymphatic invasion, tumor size, and age are independent predictors of axillary lymph node metastases in women with T1 breast cancers. Ann Surg. 1999;230:692–696. doi: 10.1097/00000658-199911000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Shoup M., Malinzak L., Weisenberger J., Arahna G.V. Predictors of axillary lymph node metastasis in T1 breast carcinoma. Ann Surg. 1999;65:748–753. [PubMed] [Google Scholar]
  • 8.Olivotto I.A., Jackson J.S.H., Mates D., et al. Prediction of axillary lymph node involvement of women with invasive breast carcinoma. Cancer. 1998;83:948–955. doi: 10.1002/(SICI)1097-0142(19980901)83:5&#x0003c;948::AID-CNCR21&#x0003e;3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  • 9.Ravdin P.M., Laurentiis M., Vendely T., Clark G. Prediction of axillary lymph nodes status in breast cancer patients by use of prognostic factors. J Natl Cancer Inst. 1994;86:1771–1775. doi: 10.1093/jnci/86.23.1771. [DOI] [PubMed] [Google Scholar]
  • 10.Silverstein M.J., Gierson E.D., Waisman J.R., Senofsky G.M., Colburn W.J., Gamagami P. Axillary lymph node dissection for T1a breast carcinoma: is it indicated? Cancer. 1994;73:664–667. doi: 10.1002/1097-0142(19940201)73:3&#x0003c;664::AID-CNCR2820730326&#x0003e;3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  • 11.Chadha M., Chabon A.B., Friedmann P., Vikram B. Predictors of axillary lymph node metastases in patients with T1 breast cancer. Cancer. 1994;73:350–353. doi: 10.1002/1097-0142(19940115)73:2&#x0003c;350::AID-CNCR2820730219&#x0003e;3.0.CO;2-5. [DOI] [PubMed] [Google Scholar]
  • 12.Caywood J., Gray R.J., Hentz J., Pockaj B.A. Older Age Independently Predicts a Lower Risk of Sentinel Lymph Node Metastasis in Breast Cancer. Ann Surg Oncol. 2005;12(12):1061–1065. doi: 10.1245/ASO.2005.02.013. [DOI] [PubMed] [Google Scholar]
  • 13.Flett M.M., Going J.J., Stanton P.D., Cooke T.G. Sentinel node localization in patients with breast cancer. Br J Surg. 1998;85(7):991–993. doi: 10.1046/j.1365-2168.1998.00746.x. [DOI] [PubMed] [Google Scholar]
  • 14.Nagashima T., Suzuki M., Yagata H., et al. Intraoperative cytologic diagnosis of sentinel node metastases in breast cancer. Acta Cytol. 2003;47(6):1028–1032. doi: 10.1159/000326640. [DOI] [PubMed] [Google Scholar]
  • 15.Tanis P.J., Boom R.P., Koops H.S., et al. Frozen section investigation of the sentinel node in malignant melanoma and breast cancer. Ann Surg Oncol. 2001;8(3):222–226. doi: 10.1007/s10434-001-0222-2. [DOI] [PubMed] [Google Scholar]
  • 16.Diest P.J., Torrenga H., Borgstein P.J., et al. Reliability of intraoperative frozen section and imprint cytological investigation of sentinel lymph nodes in breast cancer. Histopathology. 1999;35(1):14–18. doi: 10.1046/j.1365-2559.1999.00667.x. [DOI] [PubMed] [Google Scholar]
  • 17.Motomura K., Inaji H., Komoike Y., et al. Intraoperative sentinel lymph node examination by imprint cytology and frozen sectioning during breast surgery. Br J Surg. 2000;87(5):597–601. doi: 10.1046/j.1365-2168.2000.01423.x. [DOI] [PubMed] [Google Scholar]
  • 18.Dixon J.M., Mamman U., Thomas J. Accuracy of intraoperative frozen section analysis of axillary nodes. Edinburgh Breast Unit team. Br J Surg. 1999;86(3):392–395. doi: 10.1046/j.1365-2168.1999.01054.x. [DOI] [PubMed] [Google Scholar]
  • 19.Hill A.D., Tran K.N., Akhurst T., et al. Lessons learned from 500 cases of lymphatic mapping for breast cancer. Ann Surg. 1999;229(4):528–535. doi: 10.1097/00000658-199904000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Celebioglu F., Sylvan M., Perbeck L., Bergkvist L., Frisell J. Intraoperative sentinel lymph node examination by frozen section, Immunohistochemistry and imprint cytology during breast surgery a prospective study. Eur J Cancer. 2006;42(5):617–620. doi: 10.1016/j.ejca.2005.12.003. [DOI] [PubMed] [Google Scholar]
  • 21.Wright F.C., Walker J., Law C.H., McCready D.R. Outcomes after localized axillary node recurrence in breast cancer. Ann Surg Oncol. 2003;10:1054–1058. doi: 10.1245/ASO.2003.01.017. [DOI] [PubMed] [Google Scholar]
  • 22.Zavagno G., Bianco P.D., Koussis H., et al. Clinical impact of false-negative sentinel lymph nodes in breast cancer. EJSO. 2008;34:620–625. doi: 10.1016/j.ejso.2007.07.003. [DOI] [PubMed] [Google Scholar]
  • 23.Greco M., Gennaro M., Valagussa P., et al. Impact of nodal status on indication for adjuvant treatment in clinically node negative breast cancer. Ann Oncol. 2000;11:1079–1080. doi: 10.1023/A:1008302607206. [DOI] [PubMed] [Google Scholar]
  • 24.Catzeddu T., Bertelli G., Mastro L., Venturini M. Sentinel lymph node biopsy in breast cancer patients: the medical oncology perspective. J Surg Oncol. 2004;85:129–132. doi: 10.1002/jso.20025. [DOI] [PubMed] [Google Scholar]
  • 25.Houvenaeghel G., Martino M., Jacquemier J., et al. Risk of stage underestimation of breast cancer by sentinel lymph node biopsy method. Bull. Cancer. 2003;90:467–473. [PubMed] [Google Scholar]
  • 26.Nano M.T., Kollias J., Farshid G., Gill P.G., Bochner M. Clinical impact of false-negative sentinel node biopsy in primary breast cancer. Br J Surg. 2002;89:1430–1434. doi: 10.1046/j.1365-2168.2002.02233.x. [DOI] [PubMed] [Google Scholar]
  • 27.Lyman G., Giuliano A.E., Somerfield M.R., et al. American society of clinical oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23(30):7703–7720. doi: 10.1200/JCO.2005.08.001. [DOI] [PubMed] [Google Scholar]
  • 28.Kuehn T., Bembenek A., Decker T., et al. A concept for the clinical implementation of sentinel lymph node biopsy in patients with breast carcinoma with special regard to quality assurance. Cancer. 2005;103(3):451–461. doi: 10.1002/cncr.20786. [DOI] [PubMed] [Google Scholar]
  • 29.Giuliano A.E., Kirgan D.M., Guenther J.M., Morton D.L. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391–401. doi: 10.1097/00000658-199409000-00015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Reynolds C., Rosemarie M., Donohue J.H., et al. Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol. 1999;17:1720–1726. doi: 10.1200/JCO.1999.17.6.1720. [DOI] [PubMed] [Google Scholar]
  • 31.Abdessalam S.F., Zervos E.E., Prasad M., et al. Predictors of positive axillary lymph nodes after sentinel lymph node biopsy in breast cancer. Am J Surg. 2001;182:316–320. doi: 10.1016/S0002-9610(01)00719-X. [DOI] [PubMed] [Google Scholar]
  • 32.Rahusen F.D., Torrenga H., Diest P.J., et al. Predictive factors for metastatic involvement of nonsentinel nodes in patients with breast cancer. Arch Surg. 2001;136:1059–1063. doi: 10.1001/archsurg.136.9.1059. [DOI] [PubMed] [Google Scholar]
  • 33.Zee K.J., Manasseh D.M., Bevilacqua J.L., et al. A nomogram for predicting the likelihood of additional nodal metastases in breast cancer patients with a positive sentinel node biopsy. Ann Surg Oncol. 2003;10:1140–1151. doi: 10.1245/ASO.2003.03.015. [DOI] [PubMed] [Google Scholar]
  • 34.Degnim A.C., Reynolds C., Pantvaidya G., et al. Nonsentinel node metastasis in breast cancer patients: assessment of an existing and a new predictive nomogram. Am J Surg. 2005;190:543–450. doi: 10.1016/j.amjsurg.2005.06.008. [DOI] [PubMed] [Google Scholar]
  • 35.Smidt M.L., Kuster D.M., Wilt G.J., Thunnissen F.B., Zee K.J., Strobbe L.J. Can the Memorial Sloan-Kettering Cancer Center nomogram predict the likelihood of nonsentinel lymph node metastases in breast cancer patients in the Netherlands? Ann Surg Oncol. 2005;12:1066–1072. doi: 10.1245/ASO.2005.07.022. [DOI] [PubMed] [Google Scholar]
  • 36.Soni N.K., Carmalt H.L., Gillett D.J., Spillane A.J. Evaluation of a breast cancer nomogram for prediction of non-sentinel lymph node positivity. Eur J Surg Oncol. 2005;31:958–964. doi: 10.1016/j.ejso.2005.04.011. [DOI] [PubMed] [Google Scholar]
  • 37.Specht M.C., Kattan M.W., Gonen M., Fey J., Zee K.J. Predicting nonsentinel node status after positive sentinel lymph biopsy for breast cancer: clinicians versus nomogram. Ann Surg Oncol. 2005;12:654–659. doi: 10.1245/ASO.2005.06.037. [DOI] [PubMed] [Google Scholar]
  • 38.Cripe M.H., Beran L.C., Liang W.C., Sickle-Santanello B.J. The likelihood of additional nodal disease following a positive sentinel lymph node biopsy in breast cancer patients: validation of a nomogram. Am J Surg. 2006;192:484–487. doi: 10.1016/j.amjsurg.2006.06.016. [DOI] [PubMed] [Google Scholar]
  • 39.Lambert L.A., Ayers G.D., Hwang R.F., et al. Validation of a breast cancer nomogram for predicting nonsentinel lymph node metastases after a positive sentinel node biopsy. Ann Surg Oncol. 2006;13:310–320. doi: 10.1245/ASO.2006.03.078. [DOI] [PubMed] [Google Scholar]
  • 40.Smidt M.L., Strobbe L.J., Groenewoud H.M., Wilt G.J., Zee K.J., Wobbes T. Can surgical oncologists reliably predict the likelihood for non-SLN metastases in breast cancer patients? Ann Surg Oncol. 2007;14:615–620. doi: 10.1245/s10434-006-9150-5. [DOI] [PubMed] [Google Scholar]
  • 41.Rivadeneira D.E., Simmons R.M., Christos P.J., Hanna K., Daly J.M., Osborne M.P. Predictive factors associated with axillary lymph node metastases in T1a and T1b breast carcinomas. J Am Coll Surg. 2000;191:1–8. doi: 10.1016/S1072-7515(00)00310-0. [DOI] [PubMed] [Google Scholar]
  • 42.Gajdos C., Tartter P.I., Bleiweiss I.J. Lymphatic invasion, tumor size, and age are independent predictors of axillary lymph node metastases in women with T1 breast cancers. Ann Surg. 1999;230:692–696. doi: 10.1097/00000658-199911000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Ravdin P.M., Laurentiis M., Vendely T., Clark G. Prediction of axillary lymph nodes status in breast cancer patients by use of prognostic factors. J Natl Cancer Inst. 1994;86:1771–1775. doi: 10.1093/jnci/86.23.1771. [DOI] [PubMed] [Google Scholar]
  • 44.Fein D.A., Fowble B.L., Hanlon A.L., et al. Identification of women with T1–T2 breast cancer at low risk of positive axillary nodes. J Surg Oncol. 1997;65:34–39. doi: 10.1002/(SICI)1096-9098(199705)65:1&#x0003c;34::AID-JSO7&#x0003e;3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  • 45.Yiangou C., Shousha S., Sinnett H.D. Primary tumour characteristics and axillary lymph nodestatus in breast cancer. Br J Cancer. 1999;80:1974–1978. doi: 10.1038/sj.bjc.6690629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Shoup M., Malinzak L., Weisenberger J., Arahna G.V. Predictors of axillary lymph node metastasis in T1 breast carcinoma. Ann Surg. 1999;65:748–753. [PubMed] [Google Scholar]
  • 47.Fein D.A., Fowble B.L., Hanlon A.L., et al. Identification of women with T1–T2 breast cancer at low risk of positive axillary nodes. J Surg Oncol. 1997;65:34–39. doi: 10.1002/(SICI)1096-9098(199705)65:1&#x0003c;34::AID-JSO7&#x0003e;3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  • 48.Olivotto I.A., Jackson J.S.H., Mates D., et al. Prediction of axillary lymph node involvement of women with invasive breast carcinoma. Cancer. 1998;83:948–955. doi: 10.1002/(SICI)1097-0142(19980901)83:5&#x0003c;948::AID-CNCR21&#x0003e;3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  • 49.Chadha M., Chabon A.B., Friedmann P., Vikram B. Predictors of axillary lymph node metastases in patients with T1 breast cancer. Cancer. 1994;73:350–353. doi: 10.1002/1097-0142(19940115)73:2&#x0003c;350::AID-CNCR2820730219&#x0003e;3.0.CO;2-5. [DOI] [PubMed] [Google Scholar]
  • 50.Port E.R., Tan L.K., Borgen P.I., Zee K.J. Incidence of axillary lymph node metastases in T1a and T1b breast carcinoma. Ann Surg Oncol. 1998;5:23–27. doi: 10.1007/BF02303759. [DOI] [PubMed] [Google Scholar]
  • 51.Silverstein M.J., Gierson E.D., Waisman J.R., Senofsky G.M., Colburn W.J., Gamagami P. Axillary lymph node dissection for T1a breast carcinoma: is it indicated? Cancer. 1994;73:664–667. doi: 10.1002/1097-0142(19940201)73:3&#x0003c;664::AID-CNCR2820730326&#x0003e;3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  • 52.Bevilacqua J., Cody H., III, MacDonald K.A., Tan L.K., Borgen P.I., Zee K.J. A prospective validated model for predicting axillary node metastases based on 2,000 sentinel node procedures: the role of tumour location. [Corrected] Eur J Surg Oncol. 2002;28(5):490–500. doi: 10.1053/ejso.2002.1268. [DOI] [PubMed] [Google Scholar]
  • 53.Chen M., Palleschi S., Khoynezhad A., Gecelter G., et al. Role of primary breast characteristics in predicting positive sentinel lymph node biopsy results. Arch Surg. 2003;137:606–610. doi: 10.1001/archsurg.137.5.606. [DOI] [PubMed] [Google Scholar]
  • 54.Rosen P.P., Groshen S., Kinne D.W., et al. Factors influencing prognosis in node-negative breast carcinoma: analysis of 767 T1N0M0/T2N0M0 patients with long-term follow-up. J Clin Oncol. 1993;11:2090–100. doi: 10.1200/JCO.1993.11.11.2090. [DOI] [PubMed] [Google Scholar]
  • 55.Page D.L. Special types of invasive breast cancer, with clinical implications. Am J Clin Pathol. 2003;27:832–835. doi: 10.1097/00000478-200306000-00016. [DOI] [PubMed] [Google Scholar]
  • 56.Simpson J.F., Page D.L. Prognostic value of histopathology in the breast. Semin Oncol. 1992;19:254–262. [PubMed] [Google Scholar]
  • 57.Wong S.L., Chao C., Edwards M.J., et al. Frequency of sentinel lymph node metastases in patients with favorable breast cancer histologic subtypes. Am J Surg. 2002;184:492–498. doi: 10.1016/S0002-9610(02)01057-7. [DOI] [PubMed] [Google Scholar]
  • 58.Mendez J.E., Fey J.V., Cody H., Borgen P.I., Sclafani L.M. Can Sentinel Lymph Node Biopsy Be Omitted in Patients With Favorable Breast Cancer Histology? Ann Surg Oncol. 2005;12(1):24–28. doi: 10.1007/s10434-004-1169-x. [DOI] [PubMed] [Google Scholar]
  • 59.Bevilacqua J., Kattan M.W., Fey J.V., Cody H., III, Borgen P.I., Zee K.J. Doctor, What Are My Chances of Having a Positive Sentinel Node? A Validated Nomogram for Risk Estimation. J Clin Oncol. 2007;25(24):3670–3679. doi: 10.1200/JCO.2006.08.8013. [DOI] [PubMed] [Google Scholar]
  • 60.Carmichael A.R., Aparanji K., Nightingale P., Boparai R., Stonelake P.S. A clinicopathological scoring system to select breast cancer patients for sentinel node biopsy. Eur J Surg Oncol. 2006;32:1170–1174. doi: 10.1016/j.ejso.2006.05.022. [DOI] [PubMed] [Google Scholar]
  • 61.Nathanson S.D., Slater R., Debruyn D., Kapke A., Linden M. Her-2/neu expression in primary breast cancer with sentinel lymph node metastasis. Ann Surg Oncol. 2006;13:205–213. doi: 10.1245/ASO.2006.03.032. [DOI] [PubMed] [Google Scholar]
  • 62.Carcoforo P., Bergossi L., Basaglia E., et al. Prognostic and therapeutic impact of sentinel node micrometastasis in patients with invasive breast cancer. Tumori. 2002;88:S4–S5. doi: 10.1177/030089160208800319. [DOI] [PubMed] [Google Scholar]
  • 63.Chen J.H., Agrawal G., Carpenter P., Mehta R.S., Nalcioglu O., Su M.Y. Pathological Axillary Lymph Node Status in HER-2 Receptor Positive and Negative Breast Cancers. Ann Surg Oncol. 2008;15(3):941–942. doi: 10.1245/s10434-007-9677-0. [DOI] [PubMed] [Google Scholar]
  • 64.Rivadeneira D.E., Simmons R.M., Christos P.J., et al. Predictive factors associated with axillary lymph node metastases in T 1a and T1b breast carcinomas: Analysis in more than 900 patients. J Am Coll Surg. 2000;191:1–6. doi: 10.1016/S1072-7515(00)00310-0. [DOI] [PubMed] [Google Scholar]
  • 65.Fehr M.K., Kochli O.R., Helfenstein U., et al. Multivariate analysis of clinico-pathologic predictors of axillary lymph node metastasis ininvasive breast carcinoma [German] Geburtshilfe Frauenheilkd. 1995;55:182–188. doi: 10.1055/s-2007-1023298. [DOI] [PubMed] [Google Scholar]
  • 66.Jackson J.S., Olivotto I.A., Wai M.D.E., et al. A decision analysis of the effect of avoiding axillary lymph node dissection in low risk women with invasive breast carcinoma. Cancer. 2000;88:1852–1862. doi: 10.1002/(SICI)1097-0142(20000415)88:8&#x0003c;1852::AID-CNCR14&#x0003e;3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  • 67.Maibenco D.C., Weiss L.K., Pawlish K.S., et al. Axillary lymph node metastases associated with small invasive breast carcinomas. Cancer. 1999;85:1530–1536. doi: 10.1002/(SICI)1097-0142(19990401)85:7&#x0003c;1530::AID-CNCR14&#x0003e;3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  • 68.Mustafa I.A., Cole B., Wanebo H.J., et al. The impact of histopathology on nodal metastases in minimal breast cancer. Arch Surg. 1997;132:384–390. doi: 10.1001/archsurg.1997.01430280058008. [DOI] [PubMed] [Google Scholar]
  • 69.Olivotto I.A., Jackson J.S., Mates D., et al. Prediction of axillary lymph node involvement of women with invasive breast carcinoma: A multivariate analysis. Cancer. 1998;83:948–955. doi: 10.1002/(SICI)1097-0142(19980901)83:5&#x0003c;948::AID-CNCR21&#x0003e;3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  • 70.Port E.R., Tan L.K., Borgen P.I., et al. Incidence of axillary lymph node metastases in T1a and T1b breast carcinoma. Ann Surg Oncol. 1998;5:23–27. doi: 10.1007/BF02303759. [DOI] [PubMed] [Google Scholar]
  • 71.Voogd A.C., Coebergh J.W., Repelaer van Driel O.J., et al. The risk of nodal metastases in breast cancer patients with clinically negative lymph nodes: A population-based analysis. Breast Cancer Res Treat. 2000;62:63–69. doi: 10.1023/A:1006447825160. [DOI] [PubMed] [Google Scholar]

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