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Journal of Clinical Pathology logoLink to Journal of Clinical Pathology
. 2000 Oct;53(10):733–741. doi: 10.1136/jcp.53.10.733

Axillary staging of breast cancer and the sentinel node

G Cserni 1
PMCID: PMC1731094  PMID: 11064665

Abstract

Pathological aspects of axillary nodal staging of breast cancer and in particular sentinel lymph node (SLN) biopsy are reviewed. SLN biopsy seems an almost ideal staging procedure because it has both high accuracy and a low false negative rate. It may also allow a cost effective use of more sensitive methods of metastasis detection. However, the biological relevance of metastases detected only by modern tools remains to be elucidated. This review focuses on standard axillary staging and the histopathological investigation of SLNs, with emphasis on the intraoperative setting. Future trends including ancillary studies, quality control issues, prediction of non-SLN involvement, and suggestions concerning the minimum requirements for the histology of axillary SLNs are also discussed.

Key Words: axillary staging • breast cancer • sentinel lymph node

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Selected References

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  1. Albertini J. J., Lyman G. H., Cox C., Yeatman T., Balducci L., Ku N., Shivers S., Berman C., Wells K., Rapaport D. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA. 1996 Dec 11;276(22):1818–1822. [PubMed] [Google Scholar]
  2. Allred D. C., Elledge R. M. Caution concerning micrometastatic breast carcinoma in sentinel lymph nodes. Cancer. 1999 Sep 15;86(6):905–907. [PubMed] [Google Scholar]
  3. Anderson T. J. The challenge of sentinel lymph node biopsy. Histopathology. 1999 Jul;35(1):82–84. doi: 10.1046/j.1365-2559.1999.00737.x. [DOI] [PubMed] [Google Scholar]
  4. Apostolikas N., Petraki C., Agnantis N. J. The reliability of histologically negative axillary lymph nodes in breast cancer. Preliminary report. Pathol Res Pract. 1988 Dec;184(1):35–38. doi: 10.1016/S0344-0338(88)80188-2. [DOI] [PubMed] [Google Scholar]
  5. Avril N., Dose J., Jänicke F., Ziegler S., Römer 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 Sep 4;88(17):1204–1209. doi: 10.1093/jnci/88.17.1204. [DOI] [PubMed] [Google Scholar]
  6. Axelsson C. K., Mouridsen H. T., Zedeler K. 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. 1992;28A(8-9):1415–1418. doi: 10.1016/0959-8049(92)90534-9. [DOI] [PubMed] [Google Scholar]
  7. Barnwell J. M., Arredondo M. A., Kollmorgen D., Gibbs J. F., Lamonica D., Carson W., Zhang P., Winston J., Edge S. B. Sentinel node biopsy in breast cancer. Ann Surg Oncol. 1998 Mar;5(2):126–130. doi: 10.1007/BF02303845. [DOI] [PubMed] [Google Scholar]
  8. Bass S. S., Cox C. E., Ku N. N., Berman C., Reintgen D. S. The role of sentinel lymph node biopsy in breast cancer. J Am Coll Surg. 1999 Aug;189(2):183–194. doi: 10.1016/s1072-7515(99)00130-1. [DOI] [PubMed] [Google Scholar]
  9. Beechey-Newman N. Sentinel node biopsy: a revolution in the surgical management of breast cancer? Cancer Treat Rev. 1998 Jun;24(3):185–203. doi: 10.1016/s0305-7372(98)90049-4. [DOI] [PubMed] [Google Scholar]
  10. Bilchik A. J., Giuliano A., Essner R., Bostick P., Kelemen P., Foshag L. J., Sostrin S., Turner R. R., Morton D. L. Universal application of intraoperative lymphatic mapping and sentinel lymphadenectomy in solid neoplasms. Cancer J Sci Am. 1998 Nov-Dec;4(6):351–358. [PubMed] [Google Scholar]
  11. Bland K. I. Microstaging of sentinel lymph nodes. Ann Surg Oncol. 1999 Jan-Feb;6(1):15–16. doi: 10.1007/s10434-999-0015-6. [DOI] [PubMed] [Google Scholar]
  12. Blichert-Toft M., Smola M. G., Cataliotti L., O'Higgins N. Principles and guidelines for surgeons--management of symptomatic breast cancer. European Society of Surgical Oncology. Eur J Surg Oncol. 1997 Apr;23(2):101–109. doi: 10.1016/s0748-7983(97)80001-7. [DOI] [PubMed] [Google Scholar]
  13. Boova R. S., Bonanni R., Rosato F. E. Patterns of axillary nodal involvement in breast cancer. Predictability of level one dissection. Ann Surg. 1982 Dec;196(6):642–644. doi: 10.1097/00000658-198212001-00004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Borgstein P. J., Meijer S., Pijpers R. Intradermal blue dye to identify sentinel lymph-node in breast cancer. Lancet. 1997 Jun 7;349(9066):1668–1669. doi: 10.1016/s0140-6736(05)62634-7. [DOI] [PubMed] [Google Scholar]
  15. Borgstein P. J., Pijpers R., Comans E. F., van Diest P. J., Boom R. P., Meijer S. Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998 Mar;186(3):275–283. doi: 10.1016/s1072-7515(98)00011-8. [DOI] [PubMed] [Google Scholar]
  16. Bostick P. J., Chatterjee S., Chi D. D., Huynh K. T., Giuliano A. E., Cote R., Hoon D. S. Limitations of specific reverse-transcriptase polymerase chain reaction markers in the detection of metastases in the lymph nodes and blood of breast cancer patients. J Clin Oncol. 1998 Aug;16(8):2632–2640. doi: 10.1200/JCO.1998.16.8.2632. [DOI] [PubMed] [Google Scholar]
  17. Bostick P. J., Huynh K. T., Sarantou T., Turner R. R., Qi K., Giuliano A. E., Hoon D. S. Detection of metastases in sentinel lymph nodes of breast cancer patients by multiple-marker RT-PCR. Int J Cancer. 1998 Dec 18;79(6):645–651. doi: 10.1002/(sici)1097-0215(19981218)79:6<645::aid-ijc16>3.0.co;2-r. [DOI] [PubMed] [Google Scholar]
  18. Cabanas R. M. An approach for the treatment of penile carcinoma. Cancer. 1977 Feb;39(2):456–466. doi: 10.1002/1097-0142(197702)39:2<456::aid-cncr2820390214>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  19. Cady B., Stone M. D., Schuler J. G., Thakur R., Wanner M. A., Lavin P. T. The new era in breast cancer. Invasion, size, and nodal involvement dramatically decreasing as a result of mammographic screening. Arch Surg. 1996 Mar;131(3):301–308. doi: 10.1001/archsurg.1996.01430150079015. [DOI] [PubMed] [Google Scholar]
  20. Cady B. Total mastectomy and partial axillary dissection. Surg Clin North Am. 1973 Apr;53(2):313–318. doi: 10.1016/s0039-6109(16)39983-2. [DOI] [PubMed] [Google Scholar]
  21. Canavese G., Gipponi M., Catturich A., Di Somma C., Vecchio C., Rosato F., Tomei D., Cafiero F., Moresco L., Nicolò G. Sentinel lymph node mapping opens a new perspective in the surgical management of early-stage breast cancer: a combined approach with vital blue dye lymphatic mapping and radioguided surgery. Semin Surg Oncol. 1998 Dec;15(4):272–277. doi: 10.1002/(sici)1098-2388(199812)15:4<272::aid-ssu17>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  22. Chu K. U., Turner R. R., Hansen N. M., Brennan M. B., Bilchik A., Giuliano A. E. Do all patients with sentinel node metastasis from breast carcinoma need complete axillary node dissection? Ann Surg. 1999 Apr;229(4):536–541. doi: 10.1097/00000658-199904000-00013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Chu K. U., Turner R. R., Hansen N. M., Brennan M. B., Giuliano A. E. Sentinel node metastasis in patients with breast carcinoma accurately predicts immunohistochemically detectable nonsentinel node metastasis. Ann Surg Oncol. 1999 Dec;6(8):756–761. doi: 10.1007/s10434-999-0756-2. [DOI] [PubMed] [Google Scholar]
  24. Cibull M. L. Handling sentinel lymph node biopsy specimens.A work in progress. Arch Pathol Lab Med. 1999 Jul;123(7):620–621. doi: 10.5858/1999-123-0620-HSLNBS. [DOI] [PubMed] [Google Scholar]
  25. Cote R. J., Peterson H. F., Chaiwun B., Gelber R. D., Goldhirsch A., Castiglione-Gertsch M., Gusterson B., Neville A. M. Role of immunohistochemical detection of lymph-node metastases in management of breast cancer. International Breast Cancer Study Group. Lancet. 1999 Sep 11;354(9182):896–900. doi: 10.1016/s0140-6736(98)11104-2. [DOI] [PubMed] [Google Scholar]
  26. Cox C. E. Clinical relevance of serial sectioning of sentinel nodes and the detection of micrometastatic nodal disease in breast cancer. Ann Surg Oncol. 1998 Jun;5(4):297–298. doi: 10.1007/BF02303490. [DOI] [PubMed] [Google Scholar]
  27. Cox C. E., Pendas S., Cox J. M., Joseph E., Shons A. R., Yeatman T., Ku N. N., Lyman G. H., Berman C., Haddad F. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998 May;227(5):645–653. doi: 10.1097/00000658-199805000-00005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Crowe J. P., Jr, Adler L. P., Shenk R. R., Sunshine J. Positron emission tomography and breast masses: comparison with clinical, mammographic, and pathological findings. Ann Surg Oncol. 1994 Mar;1(2):132–140. doi: 10.1007/BF02303557. [DOI] [PubMed] [Google Scholar]
  29. Cserni G., Boross G., Baltás B. Value of axillary sentinel nodal status in breast cancer. World J Surg. 2000 Mar;24(3):341–344. doi: 10.1007/s002689910054. [DOI] [PubMed] [Google Scholar]
  30. Cserni G. How to improve low lymph node recovery rates from axillary clearance specimens of breast cancer. A short-term audit. J Clin Pathol. 1998 Nov;51(11):846–849. doi: 10.1136/jcp.51.11.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Cserni G. Mapping metastases in sentinel lymph nodes of breast cancer. Am J Clin Pathol. 2000 Mar;113(3):351–354. doi: 10.1309/V0VC-25AF-09VY-T6Q1. [DOI] [PubMed] [Google Scholar]
  32. Cserni G. Metastases in axillary sentinel lymph nodes in breast cancer as detected by intensive histopathological work up. J Clin Pathol. 1999 Dec;52(12):922–924. doi: 10.1136/jcp.52.12.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Cserni G. Misidentification of an axillary sentinel lymph node due to anthracosis. Eur J Surg Oncol. 1998 Jun;24(3):168–168. doi: 10.1016/s0748-7983(98)92844-x. [DOI] [PubMed] [Google Scholar]
  34. Cserni G. The reliability of sampling three to six nodes for staging breast cancer. J Clin Pathol. 1999 Sep;52(9):681–683. doi: 10.1136/jcp.52.9.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Czerniecki B. J., Scheff A. M., Callans L. S., Spitz F. R., Bedrosian I., Conant E. F., Orel S. G., Berlin J., Helsabeck C., Fraker D. L. Immunohistochemistry with pancytokeratins improves the sensitivity of sentinel lymph node biopsy in patients with breast carcinoma. Cancer. 1999 Mar 1;85(5):1098–1103. [PubMed] [Google Scholar]
  36. Dale P. S., Williams J. T., 4th Axillary staging utilizing selective sentinel lymphadenectomy for patients with invasive breast carcinoma. Am Surg. 1998 Jan;64(1):28–32. [PubMed] [Google Scholar]
  37. Danforth D. N., Jr, Findlay P. A., McDonald H. D., Lippman M. E., Reichert C. M., d'Angelo T., Gorrell C. R., Gerber N. L., Lichter A. S., Rosenberg S. A. Complete axillary lymph node dissection for stage I-II carcinoma of the breast. J Clin Oncol. 1986 May;4(5):655–662. doi: 10.1200/JCO.1986.4.5.655. [DOI] [PubMed] [Google Scholar]
  38. Davidson T. How should the axilla be treated in breast cancer? Why I favour axillary node clearance in the management of breast cancer. Eur J Surg Oncol. 1995 Feb;21(1):5–7. doi: 10.1016/s0748-7983(05)80057-5. [DOI] [PubMed] [Google Scholar]
  39. Davies G. C., Millis R. R., Hayward J. L. Assessment of axillary lymph node status. Ann Surg. 1980 Aug;192(2):148–151. doi: 10.1097/00000658-198008000-00002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Dixon M. Sentinel node biopsy in breast cancer. A promising technique, but it should not be introduced without proper trials. BMJ. 1998 Aug 1;317(7154):295–296. doi: 10.1136/bmj.317.7154.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Dowlatshahi K., Fan M., Bloom K. J., Spitz D. J., Patel S., Snider H. C., Jr Occult metastases in the sentinel lymph nodes of patients with early stage breast carcinoma: A preliminary study. Cancer. 1999 Sep 15;86(6):990–996. [PubMed] [Google Scholar]
  42. Dowlatshahi K., Fan M., Snider H. C., Habib F. A. Lymph node micrometastases from breast carcinoma: reviewing the dilemma. Cancer. 1997 Oct 1;80(7):1188–1197. doi: 10.1002/(sici)1097-0142(19971001)80:7<1188::aid-cncr2>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  43. Fechner R. E. Frozen section examination of breast biopsies. Practice parameter. Am J Clin Pathol. 1995 Jan;103(1):6–7. doi: 10.1093/ajcp/103.1.6. [DOI] [PubMed] [Google Scholar]
  44. Feldman S. M., Krag D. N., McNally R. K., Moor B. B., Weaver D. L., Klein P. Limitation in gamma probe localization of the sentinel node in breast cancer patients with large excisional biopsy. J Am Coll Surg. 1999 Mar;188(3):248–254. doi: 10.1016/s1072-7515(98)00306-8. [DOI] [PubMed] [Google Scholar]
  45. Fisher B., Bauer M., Wickerham D. L., Redmond C. K., Fisher E. R., Cruz A. B., Foster R., Gardner B., Lerner H., Margolese R. Relation of number of positive axillary nodes to the prognosis of patients with primary breast cancer. An NSABP update. Cancer. 1983 Nov 1;52(9):1551–1557. doi: 10.1002/1097-0142(19831101)52:9<1551::aid-cncr2820520902>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
  46. Fisher B., Slack N. H. Number of lymph nodes examined and the prognosis of breast carcinoma. Surg Gynecol Obstet. 1970 Jul;131(1):79–88. [PubMed] [Google Scholar]
  47. 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 Jun;152(6):765–772. [PubMed] [Google Scholar]
  48. Fisher E. R., Palekar A., Rockette H., Redmond C., Fisher B. Pathologic findings from the National Surgical Adjuvant Breast Project (Protocol No. 4). V. Significance of axillary nodal micro- and macrometastases. Cancer. 1978 Oct;42(4):2032–2038. doi: 10.1002/1097-0142(197810)42:4<2032::aid-cncr2820420453>3.0.co;2-o. [DOI] [PubMed] [Google Scholar]
  49. Fisher E. R., Swamidoss S., Lee C. H., Rockette H., Redmond C., Fisher B. Detection and significance of occult axillary node metastases in patients with invasive breast cancer. Cancer. 1978 Oct;42(4):2025–2031. doi: 10.1002/1097-0142(197810)42:4<2025::aid-cncr2820420452>3.0.co;2-j. [DOI] [PubMed] [Google Scholar]
  50. Flett M. M., Going J. J., Stanton P. D., Cooke T. G. Sentinel node localization in patients with breast cancer. Br J Surg. 1998 Jul;85(7):991–993. doi: 10.1046/j.1365-2168.1998.00746.x. [DOI] [PubMed] [Google Scholar]
  51. Forrest A. P., Roberts M. M., Cant E., Shivas A. Simple mastectomy and pectoral node biopsy. Br J Surg. 1976 Aug;63(8):569–575. doi: 10.1002/bjs.1800630802. [DOI] [PubMed] [Google Scholar]
  52. Galea M. H., Athanassiou E., Bell J., Dilks B., Robertson J. F., Elston C. W., Blamey R. W., Ellis I. O. Occult regional lymph node metastases from breast carcinoma: immunohistological detection with antibodies CAM 5.2 and NCRC-11. J Pathol. 1991 Nov;165(3):221–227. doi: 10.1002/path.1711650305. [DOI] [PubMed] [Google Scholar]
  53. Giuliano A. E., Jones R. C., Brennan M., Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol. 1997 Jun;15(6):2345–2350. doi: 10.1200/JCO.1997.15.6.2345. [DOI] [PubMed] [Google Scholar]
  54. Giuliano A. E., Kirgan D. M., Guenther J. M., Morton D. L. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994 Sep;220(3):391–401. doi: 10.1097/00000658-199409000-00015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Giuliano A. E. Mapping a pathway for axillary staging: a personal perspective on the current status of sentinel lymph node dissection for breast cancer. Arch Surg. 1999 Feb;134(2):195–199. doi: 10.1001/archsurg.134.2.195. [DOI] [PubMed] [Google Scholar]
  56. Glass E. C., Basinski J. E., Krasne D. L., Giuliano A. E. Radiation safety considerations for sentinel node techniques. Ann Surg Oncol. 1999 Jan-Feb;6(1):10–11. doi: 10.1007/s10434-999-0010-y. [DOI] [PubMed] [Google Scholar]
  57. Greenall M. J. How should the axilla be treated in breast cancer? Why I favour axillary node sampling in the management of breast cancer. Eur J Surg Oncol. 1995 Feb;21(1):2–5. doi: 10.1016/s0748-7983(05)80056-3. [DOI] [PubMed] [Google Scholar]
  58. Guenther J. M., Krishnamoorthy M., Tan L. R. Sentinel lymphadenectomy for breast cancer in a community managed care setting. Cancer J Sci Am. 1997 Nov-Dec;3(6):336–340. [PubMed] [Google Scholar]
  59. Henson D. E., Fielding L. P., Grignon D. J., Page D. L., Hammond M. E., Nash G., Pettigrew N. M., Gorstein F., Hutter R. V. College of American Pathologists Conference XXVI on clinical relevance of prognostic markers in solid tumors. Summary. Members of the Cancer Committee. Arch Pathol Lab Med. 1995 Dec;119(12):1109–1112. [PubMed] [Google Scholar]
  60. Hsueh E. C., Turner R. R., Glass E. C., Brenner R. J., Brennan M. B., Giuliano A. E. Sentinel node biopsy in breast cancer. J Am Coll Surg. 1999 Aug;189(2):207–213. doi: 10.1016/s1072-7515(99)00110-6. [DOI] [PubMed] [Google Scholar]
  61. Ivens D., Hoe A. L., Podd T. J., Hamilton C. R., Taylor I., Royle G. T. Assessment of morbidity from complete axillary dissection. Br J Cancer. 1992 Jul;66(1):136–138. doi: 10.1038/bjc.1992.230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Jannink I., Fan M., Nagy S., Rayudu G., Dowlatshahi K. Serial sectioning of sentinel nodes in patients with breast cancer: a pilot study. Ann Surg Oncol. 1998 Jun;5(4):310–314. doi: 10.1007/BF02303493. [DOI] [PubMed] [Google Scholar]
  63. Kelley S. W., Komorowski R. A., Dayer A. M. Axillary sentinel lymph node examination in breast carcinoma. Arch Pathol Lab Med. 1999 Jun;123(6):533–535. doi: 10.5858/1999-123-0533-ASLNEI. [DOI] [PubMed] [Google Scholar]
  64. Kingsley W. B., Peters G. N., Cheek J. H. What constitutes adequate study of axillary lymph nodes in breast cancer? Ann Surg. 1985 Mar;201(3):311–314. doi: 10.1097/00000658-198503000-00009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Kinne D. W. Controversies in primary breast cancer management. Am J Surg. 1993 Nov;166(5):502–508. doi: 10.1016/s0002-9610(05)81144-4. [DOI] [PubMed] [Google Scholar]
  66. Kiricuta C. I., Tausch J. A mathematical model of axillary lymph node involvement based on 1446 complete axillary dissections in patients with breast carcinoma. Cancer. 1992 May 15;69(10):2496–2501. doi: 10.1002/1097-0142(19920515)69:10<2496::aid-cncr2820691018>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
  67. Kissin M. W., Querci della Rovere G., Easton D., Westbury G. Risk of lymphoedema following the treatment of breast cancer. Br J Surg. 1986 Jul;73(7):580–584. doi: 10.1002/bjs.1800730723. [DOI] [PubMed] [Google Scholar]
  68. Kjaergaard J., Blichert-Toft M., Andersen J. A., Rank F., Pedersen B. V. Probability of false negative nodal staging in conjunction with partial axillary dissection in breast cancer. Br J Surg. 1985 May;72(5):365–367. doi: 10.1002/bjs.1800720511. [DOI] [PubMed] [Google Scholar]
  69. Klimberg V. S., Rubio I. T., Henry R., Cowan C., Colvert M., Korourian S. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg. 1999 Jun;229(6):860–865. doi: 10.1097/00000658-199906000-00013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Koller M., Barsuk D., Zippel D., Engelberg S., Ben-Ari G., Papa M. Z. Sentinel lymph node involvement--a predictor for axillary node status with breast cancer--has the time come? Eur J Surg Oncol. 1998 Jun;24(3):166–168. doi: 10.1016/s0748-7983(98)92827-x. [DOI] [PubMed] [Google Scholar]
  71. Krag D. N., Weaver D. L., Alex J. C., Fairbank J. T. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993 Dec;2(6):335–340. doi: 10.1016/0960-7404(93)90064-6. [DOI] [PubMed] [Google Scholar]
  72. Krag D., Weaver D., Ashikaga T., Moffat F., Klimberg V. S., Shriver C., Feldman S., Kusminsky R., Gadd M., Kuhn J. The sentinel node in breast cancer--a multicenter validation study. N Engl J Med. 1998 Oct 1;339(14):941–946. doi: 10.1056/NEJM199810013391401. [DOI] [PubMed] [Google Scholar]
  73. Ku N. N. Pathologic examination of sentinel lymph nodes in breast cancer. Surg Oncol Clin N Am. 1999 Jul;8(3):469–479. [PubMed] [Google Scholar]
  74. Larson D., Weinstein M., Goldberg I., Silver B., Recht A., Cady B., Silen W., Harris J. R. Edema of the arm as a function of the extent of axillary surgery in patients with stage I-II carcinoma of the breast treated with primary radiotherapy. Int J Radiat Oncol Biol Phys. 1986 Sep;12(9):1575–1582. doi: 10.1016/0360-3016(86)90280-4. [DOI] [PubMed] [Google Scholar]
  75. Linehan D. C., Hill A. D., Akhurst T., Yeung H., Yeh S. D., Tran K. N., Borgen P. I., Cody H. S., 3rd Intradermal radiocolloid and intraparenchymal blue dye injection optimize sentinel node identification in breast cancer patients. Ann Surg Oncol. 1999 Jul-Aug;6(5):450–454. doi: 10.1007/s10434-999-0450-4. [DOI] [PubMed] [Google Scholar]
  76. March D. E., Wechsler R. J., Kurtz A. B., Rosenberg A. L., Needleman L. CT-pathologic correlation of axillary lymph nodes in breast carcinoma. J Comput Assist Tomogr. 1991 May-Jun;15(3):440–444. doi: 10.1097/00004728-199105000-00017. [DOI] [PubMed] [Google Scholar]
  77. Mathiesen O., Carl J., Bonderup O., Panduro J. Axillary sampling and the risk of erroneous staging of breast cancer. An analysis of 960 consecutive patients. Acta Oncol. 1990;29(6):721–725. doi: 10.3109/02841869009092990. [DOI] [PubMed] [Google Scholar]
  78. McIntosh S. A., Going J. J., Soukop M., Purushotham A. D., Cooke T. G. Therapeutic implications of the sentinel lymph node in breast cancer. Lancet. 1999 Aug 14;354(9178):570–570. doi: 10.1016/s0140-6736(99)02155-8. [DOI] [PubMed] [Google Scholar]
  79. McLean R. G., Ege G. N. Prognostic value of axillary lymphoscintigraphy in breast carcinoma patients. J Nucl Med. 1986 Jul;27(7):1116–1124. [PubMed] [Google Scholar]
  80. McNeil C. Sentinel node biopsy: studies should bring needed data. J Natl Cancer Inst. 1998 May 20;90(10):728–730. doi: 10.1093/jnci/90.10.728. [DOI] [PubMed] [Google Scholar]
  81. Meyer J. S. Sentinel lymph node biopsy: strategies for pathologic examination of the specimen. J Surg Oncol. 1998 Dec;69(4):212–218. doi: 10.1002/(sici)1096-9098(199812)69:4<212::aid-jso4>3.0.co;2-v. [DOI] [PubMed] [Google Scholar]
  82. Miltenburg D. M., Miller C., Karamlou T. B., Brunicardi F. C. Meta-analysis of sentinel lymph node biopsy in breast cancer. J Surg Res. 1999 Jun 15;84(2):138–142. doi: 10.1006/jsre.1999.5629. [DOI] [PubMed] [Google Scholar]
  83. Min C. J., Tafra L., Verbanac K. M. Identification of superior markers for polymerase chain reaction detection of breast cancer metastases in sentinel lymph nodes. Cancer Res. 1998 Oct 15;58(20):4581–4584. [PubMed] [Google Scholar]
  84. Miner T. J., Shriver C. D., Flicek P. R., Miner F. C., Jaques D. P., Maniscalco-Theberge M. E., Krag D. N. Guidelines for the safe use of radioactive materials during localization and resection of the sentinel lymph node. Ann Surg Oncol. 1999 Jan-Feb;6(1):75–82. doi: 10.1007/s10434-999-0075-7. [DOI] [PubMed] [Google Scholar]
  85. Moffat F. L., Jr, Senofsky G. M., Davis K., Clark K. C., Robinson D. S., Ketcham A. S. Axillary node dissection for early breast cancer: some is good, but all is better. J Surg Oncol. 1992 Sep;51(1):8–13. doi: 10.1002/jso.2930510105. [DOI] [PubMed] [Google Scholar]
  86. Mori M., Mimori K., Ueo H., Tsuji K., Shiraishi T., Barnard G. F., Sugimachi K., Akiyoshi T. Clinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription-polymerase chain reaction in patients with gastrointestinal or breast carcinomas. J Clin Oncol. 1998 Jan;16(1):128–132. doi: 10.1200/JCO.1998.16.1.128. [DOI] [PubMed] [Google Scholar]
  87. Morrow M., Evans J., Rosen P. P., Kinne D. W. Does clearing of axillary lymph nodes contribute to accurate staging of breast carcinoma? Cancer. 1984 Mar 15;53(6):1329–1332. doi: 10.1002/1097-0142(19840315)53:6<1329::aid-cncr2820530618>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
  88. Morton D. L., Wen D. R., Wong J. H., Economou J. S., Cagle L. A., Storm F. K., Foshag L. J., Cochran A. J. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. 1992 Apr;127(4):392–399. doi: 10.1001/archsurg.1992.01420040034005. [DOI] [PubMed] [Google Scholar]
  89. Mussurakis S., Buckley D. L., Horsman A. Prediction of axillary lymph node status in invasive breast cancer with dynamic contrast-enhanced MR imaging. Radiology. 1997 May;203(2):317–321. doi: 10.1148/radiology.203.2.9114081. [DOI] [PubMed] [Google Scholar]
  90. Noguchi M., Bando E., Tsugawa K., Miwa K., Yokoyama K., Nakajima K., Michigishi T., Tonami N., Minato H., Nonomura A. Staging efficacy of breast cancer with sentinel lymphadenectomy. Breast Cancer Res Treat. 1999 Sep;57(2):221–229. doi: 10.1023/a:1006268426526. [DOI] [PubMed] [Google Scholar]
  91. Noguchi M., Katev N., Miyazaki I. Diagnosis of axillary lymph node metastases in patients with breast cancer. Breast Cancer Res Treat. 1996;40(3):283–293. doi: 10.1007/BF01806817. [DOI] [PubMed] [Google Scholar]
  92. Noguchi S., Aihara T., Motomura K., Inaji H., Imaoka S., Koyama H. Detection of breast cancer micrometastases in axillary lymph nodes by means of reverse transcriptase-polymerase chain reaction. Comparison between MUC1 mRNA and keratin 19 mRNA amplification. Am J Pathol. 1996 Feb;148(2):649–656. [PMC free article] [PubMed] [Google Scholar]
  93. O'Hea B. J., Hill A. D., El-Shirbiny A. M., Yeh S. D., Rosen P. P., Coit D. G., Borgen P. I., Cody H. S., 3rd Sentinel lymph node biopsy in breast cancer: initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg. 1998 Apr;186(4):423–427. doi: 10.1016/s1072-7515(98)00060-x. [DOI] [PubMed] [Google Scholar]
  94. Ollila D. W., Brennan M. B., Giuliano A. E. Therapeutic effect of sentinel lymphadenectomy in T1 breast cancer. Arch Surg. 1998 Jun;133(6):647–651. doi: 10.1001/archsurg.133.6.647. [DOI] [PubMed] [Google Scholar]
  95. PICKREN J. W. Significance of occult metastases. A study of breast cancer. Cancer. 1961 Nov-Dec;14:1266–1271. doi: 10.1002/1097-0142(196111/12)14:6<1266::aid-cncr2820140617>3.0.co;2-9. [DOI] [PubMed] [Google Scholar]
  96. Pendas S., Dauway E., Cox C. E., Giuliano R., Ku N. N., Schreiber R. H., Reintgen D. S. Sentinel node biopsy and cytokeratin staining for the accurate staging of 478 breast cancer patients. Am Surg. 1999 Jun;65(6):500–506. [PubMed] [Google Scholar]
  97. Pijpers R., Meijer S., Hoekstra O. S., Collet G. J., Comans E. F., Boom R. P., van Diest P. J., Teule G. J. Impact of lymphoscintigraphy on sentinel node identification with technetium-99m-colloidal albumin in breast cancer. J Nucl Med. 1997 Mar;38(3):366–368. [PubMed] [Google Scholar]
  98. Rahusen F. D., Meijer S., van Diest P. J. Re: Chu et al "Do all patients with sentinel node metastasis from breast carcinoma need complete axillary node dissection?". Ann Surg. 2000 Apr;231(4):615–616. doi: 10.1097/00000658-200004000-00029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Ratanawichitrasin A., Biscotti C. V., Levy L., Crowe J. P. Touch imprint cytological analysis of sentinel lymph nodes for detecting axillary metastases in patients with breast cancer. Br J Surg. 1999 Oct;86(10):1346–1348. doi: 10.1046/j.1365-2168.1999.01212.x. [DOI] [PubMed] [Google Scholar]
  100. Reuhl T., Kaisers H., Markwardt J., Haensch W., Hohenberger P., Schlag P. M. Axillaausräumung bei klinisch nodal-negativem Mammakarzinom. Kann die Indikation durch "sentinel node"-Nachweis individualisiert werden? Dtsch Med Wochenschr. 1998 May 8;123(19):583–587. doi: 10.1055/s-2007-1024023. [DOI] [PubMed] [Google Scholar]
  101. Reynolds C., Mick R., Donohue J. H., Grant C. S., Farley D. R., Callans L. S., Orel S. G., Keeney G. L., Lawton T. J., Czerniecki B. J. Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol. 1999 Jun;17(6):1720–1726. doi: 10.1200/JCO.1999.17.6.1720. [DOI] [PubMed] [Google Scholar]
  102. Reynolds J. V., Mercer P., McDermott E. W., Cross S., Stokes M., Murphy D., O'Higgins N. J. Audit of complete axillary dissection in early breast cancer. Eur J Cancer. 1994;30A(2):148–149. doi: 10.1016/0959-8049(94)90075-2. [DOI] [PubMed] [Google Scholar]
  103. Richter T., Nährig J., Komminoth P., Kowolik J., Werner M. Protocol for ultrarapid immunostaining of frozen sections. J Clin Pathol. 1999 Jun;52(6):461–463. doi: 10.1136/jcp.52.6.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Rosen P. P., Saigo P. E., Braun D. W., Weathers E., Fracchia A. A., Kinne D. W. Axillary micro- and macrometastases in breast cancer: prognostic significance of tumor size. Ann Surg. 1981 Nov;194(5):585–591. doi: 10.1097/00000658-198111000-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Roumen R. M., Geuskens L. M., Valkenburg J. G. In search of the true sentinel node by different injection techniques in breast cancer patients. Eur J Surg Oncol. 1999 Aug;25(4):347–351. doi: 10.1053/ejso.1999.0655. [DOI] [PubMed] [Google Scholar]
  106. Roumen R. M., Valkenburg J. G., Geuskens L. M. Lymphoscintigraphy and feasibility of sentinel node biopsy in 83 patients with primary breast cancer. Eur J Surg Oncol. 1997 Dec;23(6):495–502. doi: 10.1016/s0748-7983(97)92885-7. [DOI] [PubMed] [Google Scholar]
  107. Rubio I. T., Korourian S., Cowan C., Krag D. N., Colvert M., Klimberg V. S. Use of touch preps for intraoperative diagnosis of sentinel lymph node metastases in breast cancer. Ann Surg Oncol. 1998 Dec;5(8):689–694. doi: 10.1007/BF02303478. [DOI] [PubMed] [Google Scholar]
  108. Sacre R. A. Clinical evaluation of axillar lymph nodes compared to surgical and pathological findings. Eur J Surg Oncol. 1986 Jun;12(2):169–173. [PubMed] [Google Scholar]
  109. Schneebaum S., Stadler J., Cohen M., Yaniv D., Baron J., Skornick Y. Gamma probe-guided sentinel node biopsy--optimal timing for injection. Eur J Surg Oncol. 1998 Dec;24(6):515–519. doi: 10.1016/s0748-7983(98)93392-3. [DOI] [PubMed] [Google Scholar]
  110. Schoenfeld A., Luqmani Y., Smith D., O'Reilly S., Shousha S., Sinnett H. D., Coombes R. C. Detection of breast cancer micrometastases in axillary lymph nodes by using polymerase chain reaction. Cancer Res. 1994 Jun 1;54(11):2986–2990. [PubMed] [Google Scholar]
  111. Senofsky G. M., Moffat F. L., Jr, Davis K., Masri M. M., Clark K. C., Robinson D. S., Sabates B., Ketcham A. S. Total axillary lymphadenectomy in the management of breast cancer. Arch Surg. 1991 Nov;126(11):1336–1342. doi: 10.1001/archsurg.1991.01410350026004. [DOI] [PubMed] [Google Scholar]
  112. Sinzinger H. Scientific poster presentation at the EANM-meeting: a penalty system would solve the problem immediately. Eur J Nucl Med. 1999 May;26(5):556–556. [PubMed] [Google Scholar]
  113. Sinzinger H. Scientific poster presentation at the EANM-meeting: a penalty system would solve the problem immediately. Eur J Nucl Med. 1999 May;26(5):556–556. [PubMed] [Google Scholar]
  114. Sinzinger H. Scientific poster presentation at the EANM-meeting: a penalty system would solve the problem immediately. Eur J Nucl Med. 1999 May;26(5):556–556. [PubMed] [Google Scholar]
  115. Smith P. A., Harlow S. P., Krag D. N., Weaver D. L. Submission of lymph node tissue for ancillary studies decreases the accuracy of conventional breast cancer axillary node staging. Mod Pathol. 1999 Aug;12(8):781–785. [PubMed] [Google Scholar]
  116. Steele R. J., Forrest A. P., Gibson T., Stewart H. J., Chetty U. The efficacy of lower axillary sampling in obtaining lymph node status in breast cancer: a controlled randomized trial. Br J Surg. 1985 May;72(5):368–369. doi: 10.1002/bjs.1800720512. [DOI] [PubMed] [Google Scholar]
  117. Tate J. J., Lewis V., Archer T., Guyer P. G., Royle G. T., Taylor I. Ultrasound detection of axillary lymph node metastases in breast cancer. Eur J Surg Oncol. 1989 Apr;15(2):139–141. [PubMed] [Google Scholar]
  118. Torrenga H., Rahusen F. D., Borgstein P. J., Meijer S., van Diest P. Immunohistochemical detection of lymph-node metastases. Lancet. 2000 Jan 8;355(9198):144–144. doi: 10.1016/s0140-6736(05)72057-2. [DOI] [PubMed] [Google Scholar]
  119. Trojani M., de Mascarel I., Bonichon F., Coindre J. M., Delsol G. Micrometastases to axillary lymph nodes from carcinoma of breast: detection by immunohistochemistry and prognostic significance. Br J Cancer. 1987 Mar;55(3):303–306. doi: 10.1038/bjc.1987.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Turnbull A. R., Turner D. T., Chant A. D., Shepherd J. M., Buchanan R. B., Fraser J. D. Treatment of early breast cancer. Lancet. 1978 Jul 1;2(8079):7–9. doi: 10.1016/s0140-6736(78)91320-x. [DOI] [PubMed] [Google Scholar]
  121. Turner R. R., Giuliano A. E. Intraoperative pathologic examination of the sentinel lymph node. Ann Surg Oncol. 1998 Dec;5(8):670–672. doi: 10.1007/BF02303475. [DOI] [PubMed] [Google Scholar]
  122. Turner R. R., Hansen N. M., Stern S. L., Giuliano A. E. Intraoperative examination of the sentinel lymph node for breast carcinoma staging. Am J Clin Pathol. 1999 Nov;112(5):627–634. doi: 10.1093/ajcp/112.5.627. [DOI] [PubMed] [Google Scholar]
  123. 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 Sep;226(3):271–278. doi: 10.1097/00000658-199709000-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Turner R. R., Ollila D. W., Stern S., Giuliano A. E. Optimal histopathologic examination of the sentinel lymph node for breast carcinoma staging. Am J Surg Pathol. 1999 Mar;23(3):263–267. doi: 10.1097/00000478-199903000-00003. [DOI] [PubMed] [Google Scholar]
  125. Uren R. F., Howman-Giles R. B., Thompson J. F., Malouf D., Ramsey-Stewart G., Niesche F. W., Renwick S. B. Mammary lymphoscintigraphy in breast cancer. J Nucl Med. 1995 Oct;36(10):1775–1780. [PubMed] [Google Scholar]
  126. Valagussa P., Bonadonna G., Veronesi U. Patterns of relapse and survival following radical mastectomy. Analysis of 716 consecutive patients. Cancer. 1978 Mar;41(3):1170–1178. doi: 10.1002/1097-0142(197803)41:3<1170::aid-cncr2820410355>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  127. Van Diest P. J., Torrenga H., Borgstein P. J., Pijpers R., Bleichrodt R. P., Rahusen F. D., Meijer S. Reliability of intraoperative frozen section and imprint cytological investigation of sentinel lymph nodes in breast cancer. Histopathology. 1999 Jul;35(1):14–18. doi: 10.1046/j.1365-2559.1999.00667.x. [DOI] [PubMed] [Google Scholar]
  128. Vassallo P., Wernecke K., Roos N., Peters P. E. Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology. 1992 Apr;183(1):215–220. doi: 10.1148/radiology.183.1.1549675. [DOI] [PubMed] [Google Scholar]
  129. Veronesi U., Paganelli G., Galimberti V., Viale G., Zurrida S., Bedoni M., Costa A., de Cicco C., Geraghty J. G., Luini A. Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet. 1997 Jun 28;349(9069):1864–1867. doi: 10.1016/S0140-6736(97)01004-0. [DOI] [PubMed] [Google Scholar]
  130. Veronesi U., Paganelli G., Viale G., Galimberti V., Luini A., Zurrida S., Robertson C., Sacchini V., Veronesi P., Orvieto E. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst. 1999 Feb 17;91(4):368–373. doi: 10.1093/jnci/91.4.368. [DOI] [PubMed] [Google Scholar]
  131. Veronesi U., Zurrida S., Galimberti V. Consequences of sentinel node in clinical decision making in breast cancer and prospects for future studies. Eur J Surg Oncol. 1998 Apr;24(2):93–95. doi: 10.1016/s0748-7983(98)91303-8. [DOI] [PubMed] [Google Scholar]
  132. Viale G., Bosari S., Mazzarol G., Galimberti V., Luini A., Veronesi P., Paganelli G., Bedoni M., Orvieto E. Intraoperative examination of axillary sentinel lymph nodes in breast carcinoma patients. Cancer. 1999 Jun 1;85(11):2433–2438. [PubMed] [Google Scholar]
  133. Wells C. A., Heryet A., Brochier J., Gatter K. C., Mason D. Y. The immunocytochemical detection of axillary micrometastases in breast cancer. Br J Cancer. 1984 Aug;50(2):193–197. doi: 10.1038/bjc.1984.162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Wilking N., Rutqvist L. E., Carstensen J., Mattsson A., Skoog L. Prognostic significance of axillary nodal status in primary breast cancer in relation to the number of resected nodes. Stockholm Breast Cancer Study Group. Acta Oncol. 1992;31(1):29–35. doi: 10.3109/02841869209088261. [DOI] [PubMed] [Google Scholar]
  135. Zhang P. J., Reisner R. M., Nangia R., Edge S. B., Brooks J. J. Effectiveness of multiple-level sectioning in detecting axillary nodal micrometastasis in breast cancer: a retrospective study with immunohistochemical analysis. Arch Pathol Lab Med. 1998 Aug;122(8):687–690. [PubMed] [Google Scholar]
  136. de Freitas R., Jr, Costa M. V., Schneider S. V., Nicolau M. A., Marussi E. Accuracy of ultrasound and clinical examination in the diagnosis of axillary lymph node metastases in breast cancer. Eur J Surg Oncol. 1991 Jun;17(3):240–244. [PubMed] [Google Scholar]
  137. van Diest P. J. Histopathological workup of sentinel lymph nodes: how much is enough? J Clin Pathol. 1999 Dec;52(12):871–873. doi: 10.1136/jcp.52.12.871. [DOI] [PMC free article] [PubMed] [Google Scholar]

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