Association between axillary lymph node involvement and clinicopathological features of breast cancer among Indonesian women

  • Dody Novrial Department of Anatomical Pathology, Faculty of Medicine, Universitas Jenderal Soedirman, Margono Soekarjo Hospital, Purwokerto, Indonesia
  • Gita Nawangtantrini Department of Anatomical Pathology, Faculty of Medicine, Universitas Jenderal Soedirman, Margono Soekarjo Hospital, Purwokerto, Indonesia
  • Hidayat Sulistyo Department of Anatomical Pathology, Faculty of Medicine, Universitas Jenderal Soedirman, Margono Soekarjo Hospital, Purwokerto, Indonesia
  • Henida Dwi Sari Faculty of Medicine, Universitas Jenderal Soedirman, Purwokerto, Indonesia
  • Wahyu Djatmiko Department of Internal Medicine, Faculty of Medicine, Universitas Jenderal Soedirman, Margono Soekarjo Hospital, Purwokerto, Indonesia
Keywords: breast cancer, lymph node metastases, lymphovascular space invasion, tumor stage
Abstract viewed: 880 times
PDF downloaded: 663 times
HTML downloaded: 158 times
EPUB downloaded: 304 times


BACKGROUND Some clinicopathological features play roles in the spread of breast cancer to axillary lymph node (ALN). However, their roles as predictive factors are not well-established. This study was conducted to determine the correlation between the clinicopathological features of breast cancer and the risk of ALN involvement in Indonesian women.

METHODS This cross-sectional study was conducted in Margono Soekarjo Hospital using archival data from January 2017 to June 2018. All subjects with breast cancer who had undergone modified radical mastectomies without any evidence of distant metastasis were included. Chi-square and Fisher’s exact tests were performed to assess the relationship between ALN involvement and age, menopausal status, laterality, tumor size, tumor stage, histological type, tumor grade, lymphovascular space invasion (LVSI), skin or nipple infiltration, perineural invasion, estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 status. The odds ratio of each variable was evaluated using ordinal regression analysis.

RESULTS Stage 3 breast cancer had the worst status of ALN involvement compared with stage 1 (OR = 3.49; 95% CI = 1.51–8.08) and stage 2 (OR = 3.04; 95% CI = 1.32–6.98). Likewise, positive LVSI also had the worst status of ALN involvement compared with negative LVSI (OR = 8.68; 95% CI = 4.23–17.81).

CONCLUSIONS Tumor stage and LVSI could be considered as independent predictive factors of ALN involvement in patients with breast cancer, especially among Indonesian women.


Download data is not yet available.


  1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359-86.

  2. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394-424.

  3. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, et al. GLOBOCAN 2012 estimated cancer incidence, mortality and prevalence worldwide in 2012 v1.0: IARC Cancer Base No. 11 [Internet]. Lyon: International Agency for Research on Cancer; 2013 [cited 2016 Mar 7]. Available from:

  4. Ng CJ, Teo CH, Abdullah N, Tan WP, Tan HM. Relationships between cancer pattern, country income and geographical region in Asia. BMC Cancer. 2015;15:613.

  5. Karatas F, Sahin S, Erdem GU, Ates O, Babacan T, Akin S, et al. Left laterality is an independent prognostic factor for metastasis in N3 stage breast cancer. J BUON. 2016;21(4):851-8.

  6. Nouh MA, Ismail H, El-Din NH, El-Bolkainy MN. Lymph node metastasis in breast carcinoma: clinicopathological correlations in 3747 patients. J Egypt Natl Canc Inst. 2004;16(1):50-6.

  7. Gabriel N, James L, Carl J, Stephen B, Elizabeth A, Hope S, et al. Breast. In: Mahul B, editor. American Joint Committee on Cancer (AJCC) cancer staging manual. 8th ed. New York: Springer; 2017. p. 589-628.

  8. Tavassoli FA, Devilee P. Pathology and genetics: tumours of the breast and female genital organs. WHO Classification of Tumours series - volume IV. Lyon: IARC Press; 2003. p. 18-9.

  9. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, et al. American Society of Clinical Oncology/College of American Pathologists Guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol. 2010;28(16):2784-95.

  10. Ali EM, Ahmed AR, Ali AM. Correlation of breast cancer subtypes based on ER, PR and HER2 expression with axillary lymph node status. Cancer Oncol Res. 2014;2(4):51-7.

  11. Smith TJ, McKenna CM. An examination of ordinal regression goodness-of-fit indices under varied sample conditions and link functions. Multiple Linear Regression Viewpoints. 2012;38(1):1-7.

  12. Lale Atahan I, Yildiz F, Ozyigit G, Sari S, Gurkaynak M, Selek U, et al. Percent positive axillary lymph node metastasis predicts survival in patients with non-metastatic breast cancer. Acta Oncol. 2008;47(2):232-8.

  13. Wallgren A, Bonetti M, Gelber RD, Goldhirsch A, Castiglione- Gertsch M, Holmberg SB, et al. Risk factors for locoregional recurrence among breast cancer patients: results from International Breast Cancer Study Group Trials I through VII. J Clin Oncol. 2003;21(7):1205-13.

  14. Hadi NI, Jamal Q. Comparison of clinicopathological characteristics of lymph node positive and lymph node negative breast cancer. Pak J Med Sci. 2016;32(4):863-8.

  15. Oliveira Filho HR, Dória MT, Piato JR, Soares Junior JM, Filassi JR, Baracat EC, et al. Criteria for prediction of metastatic axillary lymph nodes in early-stage breast cancer. Rev Bras Ginecol Obstet. 2015;37(7):308-13.

  16. Ding J, Jiang L, Wu W. Predictive value of clinicopathological characteristics for sentinel lymph node metastasis in early breast cancer. Med Sci Monit. 2017;23:4102-8.

  17. Blackburn HL, Ellsworth DL, Shriver CD, Ellsworth RE. Breast cancer metastasis to the axillary lymph nodes: are changes to the lymph node "soil" localized or systemic? Breast Cancer. 2017:11:1178223417691246.

  18. Gismalla M, Elhassan M, Abass M. Clinical and pathological factors predicting axillary nodal metastasis in breast cancer patients of central Sudan: a single institution experience. Saudi J Health Sci. 2019;8(3):146-50.

  19. Chandrashekar S, Ajith VL, Ashwin Raghavendra A. Axillary lymph node status, age at presentation and menopausal status in female breast cancer patients attending a government tertiary care teaching hospital in Mysore, Karnataka, India. Int Surg J. 2017;4(5):1566-8.

  20. Chollet-Hinton L, Anders CK, Tse CK, Bell MB, Yang YC, Carey LA, et al. Breast cancer biologic and etiologic heterogeneity by young age and menopausal status in the Carolina Breast Cancer Study: a case-control study. Breast Cancer Res. 2016;18(79).

  21. Roychoudhuri R, Putcha V, Møller H. Cancer and laterality: a study of the five major paired organs (UK). Cancer Causes Control. 2006;17(5):655-62.

  22. Amer MH. Genetic factors and breast cancer laterality. Cancer Manag Res. 2014;6:191-203.

  23. Melnik Y, Slater P, Steinitz R, Davies A. Breast cancer in Israel: laterality and survival. J Cancer Res Clin Oncol. 1979;95(3):291-3.

  24. Ing R, Petrakis NL, Ho JH. Unilateral breast-feeding and breast cancer. Lancet. 1977;2(8029):124-7.

  25. Anstey EH, Shoemaker ML, Barrera CM, O'Neil ME, Verma AB, Holman DM. Breastfeeding and breast cancer risk reduction: implications for black mothers. Am J Prev Med. 2017;53(3S1):S40-6.

  26. Lee SY, Kim MT, Kim SW, Song MS, Yoon SJ. Effect of lifetime lactation on breast cancer risk: a Korean women's cohort study. Int J Cancer. 2003;105(3):390-3.

  27. Moosavi SA, Abdirad A, Omranipour R, Hadji M, Razavi AE, Najafi M. Clinicopathologic features predicting involvement of non-sentinel axillary lymph nodes in Iranian women with breast cancer. Asian Pac J Cancer Prev. 2014;15(17):7049-54.

  28. Friedman D, Gipponi M, Murelli F, Meszaros P, Solari N, Massa M, et al. Predictive factors of non-sentinel lymph node involvement in patients with invasive breast cancer and sentinel node micrometastases. Anticancer Res. 2013;33(10):4509-14.

  29. Dong G, Wang D, Liang X, Gao H, Wang L, Yu X, et al. Factors related to survival rates for breast cancer patients. Int J Clin Exp Med. 2014;7(10):3719-24.

  30. Camacho-Rivera M, Ragin C, Roach V, Kalwar T, Taioli E. Breast cancer clinical characteristics and outcomes in Trinidad and Tobago. J Immigrant Minority Health. 2015;17:765-72.

  31. Song YJ, Shin SH, Cho JS, Park MH, Yoon JH, Jegal YJ. The role of lymphovascular invasion as a prognostic factor in patients with lymph node-positive operable Invasive breast cancer. J Breast Cancer. 2011;14(3):198-203.

  32. Ryu YJ, Kang SJ, Cho JS, Yoon JH, Park MH. Lymphovascular invasion can be better than pathologic complete response to predict prognosis in breast cancer treated with neoadjuvant chemotherapy. Medicine. 2018;97(30):e11647.

How to Cite
Novrial D, Nawangtantrini G, Sulistyo H, Sari HD, Djatmiko W. Association between axillary lymph node involvement and clinicopathological features of breast cancer among Indonesian women. Med J Indones [Internet]. 2020Mar.26 [cited 2024Jul.16];29(1):32-7. Available from:
Clinical Research