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Published in: Annals of Surgical Oncology 12/2009

01-12-2009 | Breast Oncology

Ratio Between Positive Lymph Nodes and Total Excised Axillary Lymph Nodes as an Independent Prognostic Factor for Overall Survival in Patients with Nonmetastatic Lymph Node-Positive Breast Cancer

Authors: Hassan A. Hatoum, MD, Faek R. Jamali, MD, Nagi S. El-Saghir, MD, Khaled M. Musallam, MD, Muhieddine Seoud, MD, Hani Dimassi, PhD, Jaber Abbas, MD, Mohamad Khalife, MD, Fouad I. Boulos, MD, Ayman N. Tawil, MD, Fadi B. Geara, MD, Ziad Salem, MD, Achraf A. Shamseddine, BSc, Karine Al-Feghali, BSc, Ali I. Shamseddine, MD

Published in: Annals of Surgical Oncology | Issue 12/2009

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Abstract

Background

The status of the axillary lymph nodes in nonmetastatic lymph node-positive breast cancer (BC) patients remains the single most important determinant of overall survival (OS). Although the absolute number of nodes involved with cancer is important for prognosis, the role of the total number of excised nodes has received less emphasis. Thus, several studies have focused on the utility of the axillary lymph node ratio (ALNR) as an independent prognostic indicator of OS. However, most studies suffered from shortcomings, such as including patients who received neoadjuvant therapy or failing to consider the use of adjuvant therapy and tumor receptor status in their analysis.

Methods

We conducted a single-center retrospective review of 669 patients with nonmetastatic lymph node-positive BC. Data collected included patient demographics; breast cancer risk factors; tumor size, histopathological, receptor, and lymph node status; and treatment modalities used. Patients were subdivided into four groups according to ALNR value (<.25, .25–.49, .50–.74, .75–1.00). Study parameters were compared at the univariate and multivariate levels for their effect on OS.

Results

On univariate analysis, both the absolute number of positive lymph nodes and the ALNR were significant predictors of OS. On multivariate analysis, only the ALNR remained an independent predictor of OS, with a 2.5-fold increased risk of dying at an ALNR of ≥.25.

Conclusions

Our study demonstrates that ALNR is a stronger factor in predicting OS than the absolute number of positive axillary lymph nodes.
Literature
1.
2.
go back to reference Morton DL. Intra-operative lymphatic mapping and sentinel lymphadenectomy: community standard care or clinical investigation? Cancer J Sci Am. 1997;3:328–30.PubMed Morton DL. Intra-operative lymphatic mapping and sentinel lymphadenectomy: community standard care or clinical investigation? Cancer J Sci Am. 1997;3:328–30.PubMed
3.
go back to reference Kutiyanawala MA, Sayed M, Stotter A, et al. Staging the axilla in breast cancer: an audit of lymph-node retrieval in one UK regional centre. Eur J Surg Oncol. 1998;24:280–5.CrossRefPubMed Kutiyanawala MA, Sayed M, Stotter A, et al. Staging the axilla in breast cancer: an audit of lymph-node retrieval in one UK regional centre. Eur J Surg Oncol. 1998;24:280–5.CrossRefPubMed
4.
go back to reference Smeets A, Christiaens MR. Implications of the sentinel lymph node procedure for local and systemic adjuvant treatment. Curr Opin Oncol. 2005;17:539–44.CrossRefPubMed Smeets A, Christiaens MR. Implications of the sentinel lymph node procedure for local and systemic adjuvant treatment. Curr Opin Oncol. 2005;17:539–44.CrossRefPubMed
5.
go back to reference Schulze T, Mucke J, Markwardt J, et al. Long-term morbidity of patients with early breast cancer after sentinel lymph node biopsy compared to axillary lymph node dissection. J Surg Oncol. 2006;93:109–19.CrossRefPubMed Schulze T, Mucke J, Markwardt J, et al. Long-term morbidity of patients with early breast cancer after sentinel lymph node biopsy compared to axillary lymph node dissection. J Surg Oncol. 2006;93:109–19.CrossRefPubMed
6.
go back to reference Woodward WA, Strom EA, Tucker SL, et al. Changes in the 2003 American Joint Committee on Cancer staging for breast cancer dramatically affect stage-specific survival. J Clin Oncol. 2003;21:3244–8.CrossRefPubMed Woodward WA, Strom EA, Tucker SL, et al. Changes in the 2003 American Joint Committee on Cancer staging for breast cancer dramatically affect stage-specific survival. J Clin Oncol. 2003;21:3244–8.CrossRefPubMed
7.
go back to reference Recht A, Gray R, Davidson NE, et al. Locoregional failure 10 years after mastectomy and adjuvant chemotherapy with or without tamoxifen without irradiation: experience of the Eastern Cooperative Oncology Group. J Clin Oncol. 1999;17:1689–700.PubMed Recht A, Gray R, Davidson NE, et al. Locoregional failure 10 years after mastectomy and adjuvant chemotherapy with or without tamoxifen without irradiation: experience of the Eastern Cooperative Oncology Group. J Clin Oncol. 1999;17:1689–700.PubMed
8.
go back to reference Taghian A, Jeong JH, Mamounas E, et al. Patterns of locoregional failure in patients with operable breast cancer treated by mastectomy and adjuvant chemotherapy with or without tamoxifen and without radiotherapy: results from five National Surgical Adjuvant Breast and Bowel Project randomized clinical trials. J Clin Oncol. 2004;22:4247–54.CrossRefPubMed Taghian A, Jeong JH, Mamounas E, et al. Patterns of locoregional failure in patients with operable breast cancer treated by mastectomy and adjuvant chemotherapy with or without tamoxifen and without radiotherapy: results from five National Surgical Adjuvant Breast and Bowel Project randomized clinical trials. J Clin Oncol. 2004;22:4247–54.CrossRefPubMed
9.
go back to reference Vinh-Hung V, Burzykowski T, Cserni G, et al. Functional form of the effect of the numbers of axillary nodes on survival in early breast cancer. Int J Oncol. 2003;22:697–704.PubMed Vinh-Hung V, Burzykowski T, Cserni G, et al. Functional form of the effect of the numbers of axillary nodes on survival in early breast cancer. Int J Oncol. 2003;22:697–704.PubMed
10.
go back to reference Vinh-Hung V, Cserni G, Burzykowski T, et al. Effect of the number of uninvolved nodes on survival in early breast cancer. Oncol Rep. 2003;10:363–8.PubMed Vinh-Hung V, Cserni G, Burzykowski T, et al. Effect of the number of uninvolved nodes on survival in early breast cancer. Oncol Rep. 2003;10:363–8.PubMed
11.
go back to reference Krag DN, Single RM. Breast cancer survival according to number of nodes removed. Ann Surg Oncol. 2003;10:1152–9.CrossRefPubMed Krag DN, Single RM. Breast cancer survival according to number of nodes removed. Ann Surg Oncol. 2003;10:1152–9.CrossRefPubMed
12.
go back to reference van der Wal BC, Butzelaar RM, van der Meij S, et al. Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol. 2002;28:481–9.CrossRefPubMed van der Wal BC, Butzelaar RM, van der Meij S, et al. Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol. 2002;28:481–9.CrossRefPubMed
13.
go back to reference Voordeckers M, Vinh-Hung V, Van de Steene J, et al. The lymph node ratio as prognostic factor in node-positive breast cancer. Radiother Oncol. 2004;70:225–30.CrossRefPubMed Voordeckers M, Vinh-Hung V, Van de Steene J, et al. The lymph node ratio as prognostic factor in node-positive breast cancer. Radiother Oncol. 2004;70:225–30.CrossRefPubMed
14.
go back to reference Vinh-Hung V, Verschraegen C, Promish DI, et al. Ratios of involved nodes in early breast cancer. Breast Cancer Res. 2004;6:R680–8.CrossRefPubMed Vinh-Hung V, Verschraegen C, Promish DI, et al. Ratios of involved nodes in early breast cancer. Breast Cancer Res. 2004;6:R680–8.CrossRefPubMed
15.
go back to reference Truong PT, Berthelet E, Lee J, et al. The prognostic significance of the percentage of positive/dissected axillary lymph nodes in breast cancer recurrence and survival in patients with one to three positive axillary lymph nodes. Cancer. 2005;103:2006–13.CrossRefPubMed Truong PT, Berthelet E, Lee J, et al. The prognostic significance of the percentage of positive/dissected axillary lymph nodes in breast cancer recurrence and survival in patients with one to three positive axillary lymph nodes. Cancer. 2005;103:2006–13.CrossRefPubMed
16.
go back to reference Kuru B. Prognostic significance of total number of nodes removed, negative nodes removed, and ratio of positive nodes to removed nodes in node positive breast carcinoma. Eur J Surg Oncol. 2006;32:1082–8.CrossRefPubMed Kuru B. Prognostic significance of total number of nodes removed, negative nodes removed, and ratio of positive nodes to removed nodes in node positive breast carcinoma. Eur J Surg Oncol. 2006;32:1082–8.CrossRefPubMed
17.
go back to reference Lale Atahan I, Yildiz F, Ozyigit G, et al. Percent positive axillary lymph node metastasis predicts survival in patients with non-metastatic breast cancer. Acta Oncol. 2008;47:232–8.CrossRefPubMed Lale Atahan I, Yildiz F, Ozyigit G, et al. Percent positive axillary lymph node metastasis predicts survival in patients with non-metastatic breast cancer. Acta Oncol. 2008;47:232–8.CrossRefPubMed
18.
go back to reference Vinh-Hung V, Verkooijen HM, Fioretta G, et al. Lymph node ratio as an alternative to pN staging in node-positive breast cancer. J Clin Oncol. 2009;27:1062–8.CrossRefPubMed Vinh-Hung V, Verkooijen HM, Fioretta G, et al. Lymph node ratio as an alternative to pN staging in node-positive breast cancer. J Clin Oncol. 2009;27:1062–8.CrossRefPubMed
19.
go back to reference Greene FL, Page DL, Fleming ID, et al. AJCC cancer staging manual. 6th ed. New York, NY: Springer; 2002. Greene FL, Page DL, Fleming ID, et al. AJCC cancer staging manual. 6th ed. New York, NY: Springer; 2002.
20.
go back to reference Atkinson EN, Brown BW, Montague ED. Tumor volume, nodal status, and metastasis in breast cancer in women. J Natl Cancer Inst. 1986;76:171–8.PubMed Atkinson EN, Brown BW, Montague ED. Tumor volume, nodal status, and metastasis in breast cancer in women. J Natl Cancer Inst. 1986;76:171–8.PubMed
21.
go back to reference Carter CL, Allen C, Henson DE. Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989;63:181–7.CrossRefPubMed Carter CL, Allen C, Henson DE. Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989;63:181–7.CrossRefPubMed
22.
go back to reference Gray RJ. Flexible methods for analyzing survival data using splines, with application to breast cancer prognosis. J Am Stat Assoc. 1992;87:942–51.CrossRef Gray RJ. Flexible methods for analyzing survival data using splines, with application to breast cancer prognosis. J Am Stat Assoc. 1992;87:942–51.CrossRef
23.
go back to reference Hilsenbeck SG, Ravdin PM, de Moor CA, et al. Time-dependence of hazard ratios for prognostic factors in primary breast cancer. Breast Cancer Res Treat. 1998;52:227–37.CrossRefPubMed Hilsenbeck SG, Ravdin PM, de Moor CA, et al. Time-dependence of hazard ratios for prognostic factors in primary breast cancer. Breast Cancer Res Treat. 1998;52:227–37.CrossRefPubMed
24.
go back to reference Sauerbrei W, Royston P, Bojar H, et al. Modelling the effects of standard prognostic factors in nodepositive breast cancer: German Breast Cancer Study Group (GBSG). Br J Cancer. 1999;79:1752–60.CrossRefPubMed Sauerbrei W, Royston P, Bojar H, et al. Modelling the effects of standard prognostic factors in nodepositive breast cancer: German Breast Cancer Study Group (GBSG). Br J Cancer. 1999;79:1752–60.CrossRefPubMed
25.
go back to reference McMasters KM. The eternally enigmatic axilla: further controversy about axillary lymph node in breast cancer. Ann Surg Oncol. 2003;10:1128–30.CrossRefPubMed McMasters KM. The eternally enigmatic axilla: further controversy about axillary lymph node in breast cancer. Ann Surg Oncol. 2003;10:1128–30.CrossRefPubMed
26.
go back to reference Early Breast Cancer Trialists Collaborative Group. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365:1687–17. Early Breast Cancer Trialists Collaborative Group. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365:1687–17.
27.
go back to reference Early Breast Cancer Trialists’ Collaborative Group. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15- year survival: an overview of the randomised trials. Lancet. 2005;366:2087–106. Early Breast Cancer Trialists’ Collaborative Group. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15- year survival: an overview of the randomised trials. Lancet. 2005;366:2087–106.
28.
go back to reference Baslaim MM, Al Malik OA, Al Sobhi SS, et al. Decreased axillary lymph node retrieval in patients after neoadjuvant chemotherapy. Am J Surg. 2002;184:299–301.CrossRefPubMed Baslaim MM, Al Malik OA, Al Sobhi SS, et al. Decreased axillary lymph node retrieval in patients after neoadjuvant chemotherapy. Am J Surg. 2002;184:299–301.CrossRefPubMed
29.
go back to reference Kyndi M, Sørensen FB, Knudsen H, et al. Danish Breast Cancer Cooperative Group. Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in high-risk breast cancer: the Danish Breast Cancer Cooperative Group. J Clin Oncol. 2008;26:1419–26.CrossRefPubMed Kyndi M, Sørensen FB, Knudsen H, et al. Danish Breast Cancer Cooperative Group. Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in high-risk breast cancer: the Danish Breast Cancer Cooperative Group. J Clin Oncol. 2008;26:1419–26.CrossRefPubMed
30.
go back to reference The Steering Committee on Clinical Practice. Guidelines for the care and treatment of breast cancer. CMAJ. 1998;158(Suppl 3):S1–2. The Steering Committee on Clinical Practice. Guidelines for the care and treatment of breast cancer. CMAJ. 1998;158(Suppl 3):S1–2.
31.
go back to reference Weir L, Speers C, D’Yachkova Y, et al. Prognostic significance of the number of axillary lymph nodes removed in patients with node-negative breast cancer. J Clin Oncol. 2002;20:1793–9.CrossRefPubMed Weir L, Speers C, D’Yachkova Y, et al. Prognostic significance of the number of axillary lymph nodes removed in patients with node-negative breast cancer. J Clin Oncol. 2002;20:1793–9.CrossRefPubMed
32.
go back to reference Fowble B, Solin LJ, Schultz DJ, et al. Frequency, sites of relapse, and outcome of regional node failures following conservative surgery and radiation for early breast cancer. Int J Radiat Oncol Biol Phys. 1989;17:703–10.PubMed Fowble B, Solin LJ, Schultz DJ, et al. Frequency, sites of relapse, and outcome of regional node failures following conservative surgery and radiation for early breast cancer. Int J Radiat Oncol Biol Phys. 1989;17:703–10.PubMed
33.
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;6:109–16.CrossRefPubMed Orr RK. The impact of prophylactic axillary node dissection on breast cancer survival—a Bayesian meta-analysis. Ann Surg Oncol. 1999;6:109–16.CrossRefPubMed
34.
go back to reference Chaudhry R, Goel V, Sawka C. Breast cancer survival by teaching status of the initial treating hospital. CMAJ. 2001;164:183–8.PubMed Chaudhry R, Goel V, Sawka C. Breast cancer survival by teaching status of the initial treating hospital. CMAJ. 2001;164:183–8.PubMed
35.
go back to reference Sosa JA, Diener-West M, Gusev Y, et al. Association between extent of axillary lymph node dissection and survival in patients with stage I breast cancer. Ann Surg Oncol. 1998;5:140–9.CrossRefPubMed Sosa JA, Diener-West M, Gusev Y, et al. Association between extent of axillary lymph node dissection and survival in patients with stage I breast cancer. Ann Surg Oncol. 1998;5:140–9.CrossRefPubMed
36.
go back to reference Gillanders WE, Mikhitarian K, Hebert R, et al. Molecular detection of micrometastatic breast cancer in histopathologynegative axillary lymph nodes correlates with traditional predictors of prognosis: an interim analysis of a prospective multi-institutional cohort study. Ann Surg. 2004;239:828–37.CrossRefPubMed Gillanders WE, Mikhitarian K, Hebert R, et al. Molecular detection of micrometastatic breast cancer in histopathologynegative axillary lymph nodes correlates with traditional predictors of prognosis: an interim analysis of a prospective multi-institutional cohort study. Ann Surg. 2004;239:828–37.CrossRefPubMed
37.
go back to reference Cserni G, Bianchi S, Boecker W, et al. Improving the reproducibility of diagnosing micrometastases and isolated tumor cells. Cancer. 2005;103:358–67.CrossRefPubMed Cserni G, Bianchi S, Boecker W, et al. Improving the reproducibility of diagnosing micrometastases and isolated tumor cells. Cancer. 2005;103:358–67.CrossRefPubMed
38.
go back to reference Turner RR, Weaver DL, Cserni G, et al. Nodal stage classification for breast carcinoma: improving interobserver reproducibility through standardized histologic criteria and image-based training. J Clin Oncol. 2008;26:258–63.CrossRefPubMed Turner RR, Weaver DL, Cserni G, et al. Nodal stage classification for breast carcinoma: improving interobserver reproducibility through standardized histologic criteria and image-based training. J Clin Oncol. 2008;26:258–63.CrossRefPubMed
39.
go back to reference Sakorafas GH, Tsiotou AG, Balsiger BM. Axillary lymph node dissection in breast cancer—current status and controversies, alternative strategies and future perspectives. Acta Oncol. 2000;39:455–66.CrossRefPubMed Sakorafas GH, Tsiotou AG, Balsiger BM. Axillary lymph node dissection in breast cancer—current status and controversies, alternative strategies and future perspectives. Acta Oncol. 2000;39:455–66.CrossRefPubMed
40.
go back to reference Bundred NJ, Morgan DA, Dixon JM. ABC of breast diseases. Management of regional nodes in breast cancer. Br Med J. 1994;309:1222–5. Bundred NJ, Morgan DA, Dixon JM. ABC of breast diseases. Management of regional nodes in breast cancer. Br Med J. 1994;309:1222–5.
Metadata
Title
Ratio Between Positive Lymph Nodes and Total Excised Axillary Lymph Nodes as an Independent Prognostic Factor for Overall Survival in Patients with Nonmetastatic Lymph Node-Positive Breast Cancer
Authors
Hassan A. Hatoum, MD
Faek R. Jamali, MD
Nagi S. El-Saghir, MD
Khaled M. Musallam, MD
Muhieddine Seoud, MD
Hani Dimassi, PhD
Jaber Abbas, MD
Mohamad Khalife, MD
Fouad I. Boulos, MD
Ayman N. Tawil, MD
Fadi B. Geara, MD
Ziad Salem, MD
Achraf A. Shamseddine, BSc
Karine Al-Feghali, BSc
Ali I. Shamseddine, MD
Publication date
01-12-2009
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 12/2009
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-009-0653-8

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