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Published in: Annals of Surgical Oncology 4/2006

01-04-2006

The Prognostic Effect of the Number of Histologically Examined Axillary Lymph Nodes in Breast Cancer: Stage Migration or Age Association?

Authors: Michael Schaapveld, PhD, Elisabeth G. E. de Vries, MD, PhD, Winette T. A. van der Graaf, MD, PhD, Renée Otter, MD, PhD, Jakob de Vries, MD, PhD, Pax H. B. Willemse, MD, PhD

Published in: Annals of Surgical Oncology | Issue 4/2006

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Abstract

Background

The number of pathologically examined axillary nodes has been associated with breast cancer survival, and examination of ≥10 nodes has been advocated for reliable axillary staging. The considerable variation observed in axillary staging prompted this population-based study, which evaluated the prognostic effect of a variable number of pathologically examined nodes.

Methods

In total, 5314 consecutive breast cancer patients who underwent mastectomy or breast-conserving surgery and axillary dissection between 1994 and 1999 were included. The prognostic effect of the examined number of nodes was assessed with crude and relative survival analysis.

Results

A median number of 12 (range, 1–43) nodes were histologically examined, and 59% of the patients had no nodal tumor involvement. The number of examined nodes decreased with age (P < .001) and increased with tumor size (P < .001). Stratified for the number of tumor-positive nodes, overall survival seemed to be worse for patients with <10 compared with patients with ≥10 examined nodes (P < .001), whereas the relative survival did not differ. After adjusting for age, tumor size, number of positive nodes, and detection by screening in a multivariate analysis, the number of examined nodes was not associated with relative survival.

Conclusions

This study shows that the association between the number of pathologically examined axillary nodes and overall survival in node-negative and node-positive patients results from stage migration. The absence of an association between the number of examined nodes and relative survival further indicates that the association between the number of examined nodes and crude survival is confounded by age.
Literature
1.
go back to reference National Comprehensive Cancer Network: update of the NCCN guidelines for treatment of breast cancer. Oncology 1997;11:199–222 National Comprehensive Cancer Network: update of the NCCN guidelines for treatment of breast cancer. Oncology 1997;11:199–222
2.
go back to reference Link BK, Budd GT, Scott S, et al. Oncology Practice Pattern Study Working Group. Delivering adjuvant chemotherapy to women with early-stage breast carcinoma. Current patterns of care. Cancer 2001;92:1354–67PubMed Link BK, Budd GT, Scott S, et al. Oncology Practice Pattern Study Working Group. Delivering adjuvant chemotherapy to women with early-stage breast carcinoma. Current patterns of care. Cancer 2001;92:1354–67PubMed
3.
go back to reference Olivotto IA, Jackson JS, Mates D, et al. Prediction of axillary lymph node involvement of women with invasive breast carcinoma: a multivariate analysis. Cancer 1998;83:948–55CrossRefPubMed Olivotto IA, Jackson JS, Mates D, et al. Prediction of axillary lymph node involvement of women with invasive breast carcinoma: a multivariate analysis. Cancer 1998;83:948–55CrossRefPubMed
4.
go back to reference Voogd AC, Coebergh JW, Repelaer van Driel OJ, 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;62:63–9CrossRefPubMed Voogd AC, Coebergh JW, Repelaer van Driel OJ, 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;62:63–9CrossRefPubMed
5.
go back to reference Veronesi U, Paganelli G, Galimberti V, et al. Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 1997;349:1864–7CrossRefPubMed Veronesi U, Paganelli G, Galimberti V, et al. Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 1997;349:1864–7CrossRefPubMed
6.
go back to reference McMasters KM, Giuliano AE, Ross MI, et al. Sentinel-lymph-node biopsy for breast cancer—not yet the standard of care. N Engl J Med 1998;339:990–5CrossRefPubMed McMasters KM, Giuliano AE, Ross MI, et al. Sentinel-lymph-node biopsy for breast cancer—not yet the standard of care. N Engl J Med 1998;339:990–5CrossRefPubMed
7.
go back to reference Reynolds C, Mick R, Donohue JH, et al. Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol 1999;17:1720–6PubMed Reynolds C, Mick R, Donohue JH, et al. Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol 1999;17:1720–6PubMed
8.
go back to reference 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;18:2553–9PubMed 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;18:2553–9PubMed
9.
go back to reference Krag D, Ashikaga T, Abrams J. Sentinel nodes: clinical trial data needed. J Clin Oncol 2000;18:3873–4PubMed Krag D, Ashikaga T, Abrams J. Sentinel nodes: clinical trial data needed. J Clin Oncol 2000;18:3873–4PubMed
10.
go back to reference Edge SB, Niland JC, Bookman MA, et al. Emergence of sentinel node biopsy in breast cancer as standard-of-care in academic comprehensive cancer centers. J Natl Cancer Inst 2003;95:1514–21PubMed Edge SB, Niland JC, Bookman MA, et al. Emergence of sentinel node biopsy in breast cancer as standard-of-care in academic comprehensive cancer centers. J Natl Cancer Inst 2003;95:1514–21PubMed
11.
go back to reference 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;152:765–22PubMed 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;152:765–22PubMed
12.
go back to reference Rosen PP, Lesser ML, Kinne DW, Beattie EJ. Discontinuous or “skip” metastases in breast carcinoma: analysis of 1228 axillary dissections. Ann Surg 1983;4:655–62 Rosen PP, Lesser ML, Kinne DW, Beattie EJ. Discontinuous or “skip” metastases in breast carcinoma: analysis of 1228 axillary dissections. Ann Surg 1983;4:655–62
13.
go back to reference Schaapveld M, Otter R, de Vries EG, et al. Variability in axillary lymph node dissection for breast cancer. J Surg Oncol 2004;87:4–12CrossRefPubMed Schaapveld M, Otter R, de Vries EG, et al. Variability in axillary lymph node dissection for breast cancer. J Surg Oncol 2004;87:4–12CrossRefPubMed
14.
go back to reference Wilking N, Rutqvist LE, Carstensen J, Mattsson A, Skoog L. Prognostic significance of axillary nodal status in primary breast cancer in relation to the number of resected nodes. Acta Oncol 1992;31:29–35PubMed Wilking N, Rutqvist LE, Carstensen J, Mattsson A, Skoog L. Prognostic significance of axillary nodal status in primary breast cancer in relation to the number of resected nodes. Acta Oncol 1992;31:29–35PubMed
15.
go back to reference Fisher B, Slack NH. Number of lymph nodes examined and the prognosis of breast carcinoma. Surg Gynecol Obstet 1970;131:79–88PubMed Fisher B, Slack NH. Number of lymph nodes examined and the prognosis of breast carcinoma. Surg Gynecol Obstet 1970;131:79–88PubMed
16.
go back to reference Kjaergaard J, Blichert-Toft M, Andersen JA, Rank F, Pedersen BV. Probability of false negative nodal staging in conjunction with partial axillary dissection in breast cancer. Br J Surg 1985;72:365–7PubMed Kjaergaard J, Blichert-Toft M, Andersen JA, Rank F, Pedersen BV. Probability of false negative nodal staging in conjunction with partial axillary dissection in breast cancer. Br J Surg 1985;72:365–7PubMed
17.
go back to reference Jatoi I, Hilsenbeck SG, Clarck GM, Osborne CK. Significance of axillary lymph nodes metastasis in primary breast cancer. J Clin Oncol 1999;17:2334–40PubMed Jatoi I, Hilsenbeck SG, Clarck GM, Osborne CK. Significance of axillary lymph nodes metastasis in primary breast cancer. J Clin Oncol 1999;17:2334–40PubMed
18.
go back to reference Camp RL, Rimm EB, Rimm DL. A high number of tumor free axillary lymph nodes from patients with lymph node negative breast carcinoma is associated with poor outcome. Cancer 2000;88:108–13CrossRefPubMed Camp RL, Rimm EB, Rimm DL. A high number of tumor free axillary lymph nodes from patients with lymph node negative breast carcinoma is associated with poor outcome. Cancer 2000;88:108–13CrossRefPubMed
19.
go back to reference Moorman PG, Hamza A, Marks JR, Olson JA. Prognostic significance of the number of lymph nodes examined in patients with lymph node-negative breast carcinoma. Cancer 2001;91:2258–62CrossRefPubMed Moorman PG, Hamza A, Marks JR, Olson JA. Prognostic significance of the number of lymph nodes examined in patients with lymph node-negative breast carcinoma. Cancer 2001;91:2258–62CrossRefPubMed
20.
go back to reference Weir L, Speers C, D’yachkova Y, Olivotto IA. Prognostic significance of the number of axillary lymph nodes removed in patients with node negative breast cancer. J Clin Oncol 2002;20:1793–9CrossRefPubMed Weir L, Speers C, D’yachkova Y, Olivotto IA. Prognostic significance of the number of axillary lymph nodes removed in patients with node negative breast cancer. J Clin Oncol 2002;20:1793–9CrossRefPubMed
21.
go back to reference Krag DN, Single RM. Breast cancer survival according to number of nodes removed. Ann Surg Oncol 2003;10:1152–9CrossRefPubMed Krag DN, Single RM. Breast cancer survival according to number of nodes removed. Ann Surg Oncol 2003;10:1152–9CrossRefPubMed
22.
go back to reference Polednak AP. Survival of lymph node-negative breast cancer in relation to number of lymph nodes examined. Ann Surg 2003;237:163–7CrossRefPubMed Polednak AP. Survival of lymph node-negative breast cancer in relation to number of lymph nodes examined. Ann Surg 2003;237:163–7CrossRefPubMed
23.
go back to reference Du X, Freeman JL, Goodwin JS. The declining use of axillary dissection in patients with early stage breast cancer. Breast Cancer Res Treat 1999;53:137–44CrossRefPubMed Du X, Freeman JL, Goodwin JS. The declining use of axillary dissection in patients with early stage breast cancer. Breast Cancer Res Treat 1999;53:137–44CrossRefPubMed
24.
go back to reference Hermanek P, Sobin LH (eds). International Union Against Cancer (UICC): TNM Classification of Malignant Tumors. 4th ed, 2nd rev. Berlin: Springer-Verlag, 1992 Hermanek P, Sobin LH (eds). International Union Against Cancer (UICC): TNM Classification of Malignant Tumors. 4th ed, 2nd rev. Berlin: Springer-Verlag, 1992
25.
go back to reference Sobin LH, Wittekind C (eds). International Union Against Cancer (UICC): TNM Classification of Malignant Tumors. 5th ed. New York: Wiley-Liss, 1997 Sobin LH, Wittekind C (eds). International Union Against Cancer (UICC): TNM Classification of Malignant Tumors. 5th ed. New York: Wiley-Liss, 1997
27.
go back to reference Ederer F, Heise H. Instructions to IBM 650 Programmers in Processing Survival Computations. Methodological Note No. 10, End Results Evaluation Section. Bethesda, MD: National Cancer Institute, 1959 Ederer F, Heise H. Instructions to IBM 650 Programmers in Processing Survival Computations. Methodological Note No. 10, End Results Evaluation Section. Bethesda, MD: National Cancer Institute, 1959
28.
go back to reference Dickman PW, Sloggett A, Hills M, Hakulinen T. Regression models for relative survival and the estimation of net survival. Stat Med 2004;23:51–64CrossRefPubMed Dickman PW, Sloggett A, Hills M, Hakulinen T. Regression models for relative survival and the estimation of net survival. Stat Med 2004;23:51–64CrossRefPubMed
29.
go back to reference McCullagh P, Nelder JA. Generalized Linear Models. 2nd ed. London: Chapman & Hall, 1989 McCullagh P, Nelder JA. Generalized Linear Models. 2nd ed. London: Chapman & Hall, 1989
30.
go back to reference Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon: stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 1985;312:1604–8PubMed Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon: stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 1985;312:1604–8PubMed
31.
go back to reference Orr RK. The impact of prophylactic axillary node dissection on breast cancer survival—a Bayesian meta-analysis. Ann Surg Oncol 1999;6:109–16CrossRefPubMed Orr RK. The impact of prophylactic axillary node dissection on breast cancer survival—a Bayesian meta-analysis. Ann Surg Oncol 1999;6:109–16CrossRefPubMed
32.
go back to reference Early Breast Cancer Trialists’ Collaborative Group. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 1998;351:1451–67 Early Breast Cancer Trialists’ Collaborative Group. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 1998;351:1451–67
33.
go back to reference Early Breast Cancer Trialists’ Collaborative Group. Polychemotherapy for early breast cancer: an overview of the randomised trials. Lancet 1998;352:930–45 Early Breast Cancer Trialists’ Collaborative Group. Polychemotherapy for early breast cancer: an overview of the randomised trials. Lancet 1998;352:930–45
34.
go back to reference Whelan TJ, Julian J, Wright J, Jadad AR, Levine ML. Does locoregional radiation therapy improve survival in breast cancer? A meta-analysis. J Clin Oncol 2000;18:1220–9.PubMed Whelan TJ, Julian J, Wright J, Jadad AR, Levine ML. Does locoregional radiation therapy improve survival in breast cancer? A meta-analysis. J Clin Oncol 2000;18:1220–9.PubMed
35.
go back to reference Haffty BG, Lee C, Philpotts L, et al. Prognostic significance of mammographic detection in a cohort of conservatively treated breast cancer patients. Cancer J Sci Am 1998;4:35–40PubMed Haffty BG, Lee C, Philpotts L, et al. Prognostic significance of mammographic detection in a cohort of conservatively treated breast cancer patients. Cancer J Sci Am 1998;4:35–40PubMed
36.
go back to reference Gill PG, Farshid G, Luke CG, Roder DM. Detection by screening mammography is a powerful independent predictor of survival in women diagnosed with breast cancer. Breast 2004;13:15–22CrossRefPubMed Gill PG, Farshid G, Luke CG, Roder DM. Detection by screening mammography is a powerful independent predictor of survival in women diagnosed with breast cancer. Breast 2004;13:15–22CrossRefPubMed
37.
go back to reference Ernst MF, Voogd AC, Coebergh JW, Roukema JA. Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer 2004;100:1337–44CrossRefPubMed Ernst MF, Voogd AC, Coebergh JW, Roukema JA. Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer 2004;100:1337–44CrossRefPubMed
Metadata
Title
The Prognostic Effect of the Number of Histologically Examined Axillary Lymph Nodes in Breast Cancer: Stage Migration or Age Association?
Authors
Michael Schaapveld, PhD
Elisabeth G. E. de Vries, MD, PhD
Winette T. A. van der Graaf, MD, PhD
Renée Otter, MD, PhD
Jakob de Vries, MD, PhD
Pax H. B. Willemse, MD, PhD
Publication date
01-04-2006
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 4/2006
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/ASO.2006.02.020

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