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Factors Influencing Non-sentinel Node Involvement in Sentinel Node Positive Patients and Validation of MSKCC Nomogram in Indian Breast Cancer Population

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Abstract

Current guidelines recommend completion axillary lymphnode dissection (ALND) when sentinel lymphnode (SLN) contains metastatic tumor deposit. In consequent ALND sentinel node is the only node involved by tumor in 40–70 % of cases. Recent studies demonstrate the oncologic safety of omitting completion ALND in low risk patients. Several nomograms (MSKCC, Stanford, MD Anderson score, Tenon score) had been developed in predicting the likelihood of additional nodes metastatic involvement. We evaluated accuracy of MSKCC nomogram and other clinicopathologic variables associated with additional lymph node metastasis in our patients. A total of 334 patients with primary breast cancer patients underwent SLN biopsy during the period Jan 2007 to June 2014. Clinicopathologic variables were prospectively collected. Completion ALND was done in 64 patients who had tumor deposit in SLN. The discriminatory accuracy of nomogram was analyzed using Area under Receiver operating characteristic curve (ROC). SLN was the only node involved with tumor in 69 % (44/64) of our patients. Additional lymph node metastasis was seen in 31 % (20/64). On univariate analysis, extracapsular infiltration in sentinel node and multiple sentinel nodes positivity were significantly associated (p < 0.05) with additional lymph node metastasis in the axilla. Area under ROC curve for nomogram was 0.58 suggesting poor performance of the nomogram in predicting NSLN involvement. Sentinel nodes are the only nodes to be involved by tumor in 70 % of the patients. Our findings indicate that multiple sentinel node positivity and extra-capsular invasion in sentinel node significantly predicted the likelihood of additional nodal metastasis. MSKCC nomogram did not reliably predict the involvement of additional nodal metastasis in our study population.

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References

  1. Petrek JA, Heelan MC (1998) Incidence of breast carcinoma-related lymphedema. Cancer 83:2776–2781

    Article  CAS  PubMed  Google Scholar 

  2. Veronesi U, Paganelli G, Galimberti V et al (1997) Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 349:1864–1867

    Article  CAS  PubMed  Google Scholar 

  3. Scomersi S, Torelli L, Zanconati F et al (2012) Evaluation of a breast cancer nomogram for predicting the likelihood of additional nodal metastases in patients with a positive sentinel node biopsy. Ann Ital Chir 83:461–468

    PubMed  Google Scholar 

  4. Van Zee KJ, Manasseh DM, Bevilacqua JL et al (2003) A nomogram for predicting the likelihood of additional nodal metastases in breast cancer patients with a positive sentinel node biopsy. Ann Surg Oncol 10:1140–1151

    Article  PubMed  Google Scholar 

  5. Pal A, Provenzano E, Duffy SW, Pinder SE, Purushotham AD (2008) A model for predicting non-sentinel lymph node metastatic disease when the sentinel lymph node is positive. Br J Surg 95:302–309

    Article  CAS  PubMed  Google Scholar 

  6. Kohrt HE, Olshen RA, Bermas HR et al (2008) New models and online calculator for predicting non-sentinel lymph node status in sentinel lymph node positive breast cancer patients. BMC Cancer 8:66

    Article  PubMed  PubMed Central  Google Scholar 

  7. Barranger E, Coutant C, Flahault A et al (2005) An axilla scoring system to predict non-sentinel lymph node status in breast cancer patients with sentinel lymph node involvement. Breast Cancer Res Treat 91:113–119

    Article  PubMed  Google Scholar 

  8. Hwang RF, Krishnamurthy S, Hunt KK et al. (2003) Clinicopathologic factors predicting involvement of nonsentinel axillary nodes in women with breast cancer. Ann Surg Oncol 10:248–254

    Article  PubMed  Google Scholar 

  9. Soni N, Carmalt H, Gillett D et al (2005) Evaluation of a breast cancer nomogram for prediction of non-sentinel lymph node positivity. Eur J Surg Oncol 31:958–964

    Article  CAS  PubMed  Google Scholar 

  10. Lambert L, Ayers G, Hwang R, Hunt K, Ross M, Kuerer H et al (2006) Validation of a breast cancer nomogram for predicting nonsentinel lymph node metastases after a positive sentinel node biopsy. Ann Surg Oncol 13:310–320

    Article  PubMed  Google Scholar 

  11. Cripe M, Beran L, Liang W, Sickle-Santanello B (2006) The likelihood of additional nodal disease following a positive sentinel lymph node biopsy in breast cancer patients: validation of a nomogram. Am J Surg 192:484–487

    Article  PubMed  Google Scholar 

  12. Alran S, de Rycke Y, Fourchotte V et al (2007) Validation and limitations of use of a breast cancer nomogram predicting the likelihood of non-sentinel node involvement after positive sentinel node biopsy. Ann Surg Oncol 14:2195–2201

    Article  PubMed  Google Scholar 

  13. Ponzone R, Maggiorotto F, Mariani L et al (2007) Comparison of two models for the prediction of nonsentinel node metastases in breast cancer. Am J Surg 193:686–692

    Article  PubMed  Google Scholar 

  14. Van la Parra RF, Francissen CM, Peer PG, Ernst MF et al (2013) Assessment of the Memorial Sloan-Kettering Cancer Center nomogram to predict sentinel lymph node metastases in a Dutch breast cancer population. Eur J Cancer 49(3):564–571

    Article  Google Scholar 

  15. Klar M, Jochmann A, Foeldi M et al (2008) The MSKCC nomogram for prediction the likelihood of non-sentinel node involvement in a German breast cancer population. Breast Cancer Res Treat 112(3):523–531

    Article  CAS  PubMed  Google Scholar 

  16. Hidara S, Harrabia I, Benregaya L et al (2011) Validation of nomograms to predict the risk of non-sentinel lymph node metastases in North African Tunisian breast cancer patients with sentinel node involvement. Breast 20:26–30

    Article  Google Scholar 

  17. Tryggvadóttir L, Gislum M, Bray F et al (2010) Trends in the survival of patients diagnosed with breast cancer in the Nordic countries 1964–2003 followed up to the end of 2006. Acta Oncol 49(5):624–631

    Article  PubMed  Google Scholar 

  18. Sant M, Allemani C, Santaquilani M et al (2009) EUROCARE-4. Survival of cancer patients diagnosed in 1995–1999. Results and commentary. Eur J Cancer 45(6):931–991

    Article  PubMed  Google Scholar 

  19. Giuliano A, Linda McCall L, Beitsch P et al (2010) Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases. The American College of Surgeons Oncology Group Z0011 Randomized Trial. Ann Surg 252:426–433

    PubMed  Google Scholar 

  20. Gatzemeier W, Mann GB (2013) Which sentinel lymph-node (SLN) positive breast cancer patient needs an axillary lymph-node dissection (ALND)–ACOSOG Z0011 Results and beyond. Breast 22(3):211–216

    Article  PubMed  Google Scholar 

  21. Noguchi M (2008) Avoidance of axillary lymph node dissection in selected patients with node-positive breast cancer. EJSO 34:129–134

    Article  CAS  PubMed  Google Scholar 

  22. Langer I, Guller U, Viehl CT et al. (2009) Axillary lymph node dissection for sentinel lymph node micrometastases may be safely omitted in early-stage breast cancer patients: long-term outcomes of a prospective study. Ann Surg Oncol 16(12):3366–3374

    Article  PubMed  Google Scholar 

  23. Ponzone R, Biglia N, Maggiorotto F et al (2003) Performance of sentinel node dissection as definitive treatment for node negative breast cancer patients. Eur J Surg Oncol 29:703–706

    Article  CAS  PubMed  Google Scholar 

  24. Giuliano AE, Morrow M, Duggal S, Julian TB (2012) Should ACOSOG Z0011 change practice with respect to axillary lymph node dissection for a positive sentinel lymph node biopsy in breast cancer? Clin Exp Metastasis 29:687–692

    Article  PubMed  Google Scholar 

  25. D’Angelo-Donovan DD, Dickson-Witmer D, Petrelli NJ (2012) Sentinel lymph node biopsy in breast cancer: a history and current clinical recommendations. Surg Oncol 21:196–200

    Article  PubMed  Google Scholar 

  26. Wong SL, Edwards MJ, Chao C et al (2001) Predicting the status of the nonsentinel axillary nodes. Arch Surg 136:563–568

    Article  CAS  PubMed  Google Scholar 

  27. Joseph KA, El-Tamer M, Komenaka I, Troxel A et al (2004) Predictors of nonsentinel node metastasis in patients with breast cancer after sentinel node metastasis. Arch Surg 139:648–651

    Article  PubMed  Google Scholar 

  28. Hwang RF, Krishnamurthy S, Hunt KK, et al (2003) Clinicopathologic factors predicting involvement of nonsentinel axillary nodes in women with breast cancer. Ann Surg Oncol 10:248–253

    Article  PubMed  Google Scholar 

  29. Boler DE, Uras C, Ince U et al (2012) Factors predicting the non-sentinel lymph node involvement in breast cancer patients with sentinel lymph node metastases. Breast 21:518–523

    Article  CAS  PubMed  Google Scholar 

  30. Turner RR, Chu K, Qi K, Hansen NM, Glass EC, Giuliano AE (2000) Pathologic features associated with nonsentinel lymph node metastases in patients with metastatic breast carcinoma in a sentinel lymph node. Cancer 89:574–581

    Article  CAS  PubMed  Google Scholar 

  31. Kohrt HE, Olshen RA, Bermas HR, Goodson WH, Wood DJ et al. (2008) New models and online calculator for predicting non-sentinel lymph node status in sentinel lymph node positive breast cancer patients. BMC Cancer 8:66. doi:10.1186/1471-2407-8-66

    Article  PubMed  PubMed Central  Google Scholar 

  32. Weiser MR, Montgomery LL, Tan LK et al (2001) (2001) Lymphovascular invasion enhances the prediction of non-sentinel node metastases in breast cancer patients with positive sentinel nodes. Ann Surg Oncol 8:145–149

    Article  CAS  PubMed  Google Scholar 

  33. Degnim AC, Griffith KA, Sabel MS et al (2003) Clinicopathologic features of metastasis in nonsentinel lymph nodes of breast carcinoma patients: a metaanalysis. Cancer 98:2307–2315

    Article  PubMed  Google Scholar 

  34. Reynolds C, Mick R, Donohue JH et al (1999) Sentinel lymph node biopsy with metastasis: can axillary dissection be avoided in some patients with breast cancer? J Clin Oncol 17:1720–1726

    CAS  PubMed  Google Scholar 

  35. Chu KU, Turner RR, Hansen NM et al (1999) Do all patients with sentinel node metastasis from breast carcinoma need complete axillary node dissection? Ann Surg 229:536–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Krag DN, Anderson SJ, Julian TB et al (2010) Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 11:927–933

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hunt KK, Ballman KV, McCall LM, Boughey JC, Mittendorf EA et al. (2012) Factors associated with local-regional recurrence after a negative sentinel node dissection: results of the ACOSOG Z0010 trial. Ann Surg 256:428–436

    Article  PubMed  Google Scholar 

  38. Goldstein NS, Mani A, Vicini F, Ingold J (1999) Prognostic features in patients with stage T1 breast carcinoma and a 0.5 cm or less lymph node metastasis. Am J Clin Pathol 111:21–28

    Article  CAS  PubMed  Google Scholar 

  39. Eldweny H, Alkhaldy K, Alsaleh N et al (2012) Predictors of non-sentinel lymph node metastasis in breast cancer patients with positive sentinel lymph node pilot study. J Egypt Natl Cancer Inst 24(1):23–30

    Article  Google Scholar 

  40. Meretoja TJ, Leidenius MHK, Heikkilä PS et al (2012) International multicenter tool to predict the risk of nonsentinel node metastasis in breast cancer. J Natl Cancer Inst 104(24):1888–1896

    Article  PubMed  Google Scholar 

  41. Stitzenberg KB, Meyer AA, Stern SL et al (2003) Extracapsular extension of the sentinel lymph node metastasis: a predictor of nonsentinel node tumor burden. Ann Surg 237:607–612

    PubMed  PubMed Central  Google Scholar 

  42. Moosavi SA, Abdirad A, Omranipour R et al (2014) Clinicopathological Factors Predicting Non-Sentinel Lymph Node Metastasis of Breast Cancer in Iran. Asian Pac J Cancer Prev 15:7049–7054

    Article  PubMed  Google Scholar 

  43. Ozmen V, Karanlik H, Cabioglu N et al (2006) Factors predicting the sentinel and nonsentinel lymph node metastases in breast cancer. Breast Cancer Res Treat 95:1–6

    Article  CAS  PubMed  Google Scholar 

  44. Coutant C, Olivier C, Lambaudie E, Fondrinier E, Marchal F, Guillemin F et al. (2009) Comparison of models to predict nonsentinel lymph node status in breast cancer patients with metastatic sentinel lymph nodes: a prospective multicenter study. J Clin Oncol 27:2800–2808

    Article  PubMed  Google Scholar 

  45. Smidt ML, Kuster DM, van der Wilt GJ et al (2005) 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 12:1066–1072

    Article  PubMed  Google Scholar 

  46. Lombardi A, Maggi S, Lo Russo M, Scopinaro F, Di Stefano D, Pittau MG et al (2011) Non-sentinel lymph node metastases in breast cancer patients with a positive sentinel lymph node: validation of five nomograms and development of a new predictive model. Tumori 97:749–755

    PubMed  Google Scholar 

  47. Soni NK, Carmalt HL, Gillett DJ, Spillane AJ et al (2005) Evaluation of a breast cancer nomogram for prediction of non-sentinel lymph node positivity. Eur J Surg Oncol 31:958–964

    Article  CAS  PubMed  Google Scholar 

  48. Kuo YL, Chen WC, Yao WJ et al (2013) Validation of Memorial Sloan-Kettering Cancer Center nomogram for prediction of non-sentinel lymph node metastasis in sentinel lymph node positive breast cancer patients an international comparison. Int J Surg 11(7):538–543

    Article  PubMed  Google Scholar 

  49. Hidar S, Harrabi I, Benregaya L, Fatnassi R, Khelifi A, Benabdelkader A et al. (2011) Validation of nomograms to predict the risk of non-sentinels lymph node metastases in North African Tunisian breast cancer patients with sentinel node involvement. Breast 20:26–30

    Article  PubMed  Google Scholar 

  50. Sasada T, Murakami S, Kataoka T, Ohara M, Ozaki S, Okada M et al (2012) Memorial SloaneKettering Cancer Center nomogram to predict the risk of non-sentinel lymph node metastasis in japanese breast cancer patients. Surg Today 42:245–249

    Article  PubMed  Google Scholar 

  51. Amanti C, Lombardi A, Maggi S, Moscaroli A, Lo Russo M, Maglio R et al (2009) Is complete axillary dissection necessary for all patients with positive findings on sentinel lymph node biopsy? Validation of a breast cancer nomogram for predicting the likelihood of a non-sentinel lymph node. Tumori 95:153–155

    PubMed  Google Scholar 

  52. Van la Parra RF, Ernst MF, Bevilacqua JL, Mol SJ, Van Zee KJ, Broekman JM et al. (2009) Validation of a nomogram to predict the risk of nonsentinel lymph node metastases in breast cancer patients with a positive sentinel node biopsy: validation of the MSKCC breast nomogram. Ann Surg Oncol 16:1128–1135

    Article  Google Scholar 

  53. Gur AS, Unal B, Ozbek U, Ozmen V, Aydogan F, Gokgoz S et al (2010) Validation of breast cancer nomograms for predicting the non-sentinel lymph node metastases after a positive sentinel lymph node biopsy in a multi-center study. Eur J Surg Oncol 36:30–35

    Article  CAS  PubMed  Google Scholar 

  54. Poirier E, Sideris L, Dube P, Drolet P, Meterissian SH (2008) Analysis of clinical applicability of the breast cancer nomogram for positive sentinel lymph node: the Canadian experience. Ann Surg Oncol 15:2562–2567

    Article  PubMed  Google Scholar 

  55. Pinero A, Canteras M, Moreno A, Vicente F, Gimenez J, Tocino A et al (2013) Multicenter validation of two nomograms to predict non-sentinel node involvement in breast cancer. Clin Transl Oncol 15:117–123

    Article  PubMed  Google Scholar 

  56. Coufal O, Pavlik T, Fabian P, Bori R, Boross G, Sejben I et al (2009) Predicting nonsentinel lymph node status after positive sentinel biopsy in breast cancer: what model performs the best in a Czech population? Pathol Oncol Res 15:733–740

    Article  PubMed  Google Scholar 

  57. van den Hoven I, Kuijt GP, Voogd AC et al (2010) Value of Memorial Sloan Kettering Cancer Center nomogram in clinical decision making for sentinel lymph node-positive breast cancer. Br J Surg 97:1653–1658

    Article  PubMed  Google Scholar 

  58. Sanjuan A, Escaramis G, Vidal-Sicart S, Illa M, Zanon G, Pahisa J et al (2010) Predicting non-sentinel lymph node status in breast cancer patients with sentinel lymph node involvement: evaluation of two scoring systems. Breast J 16:134–140

    Article  PubMed  Google Scholar 

  59. Moghaddam Y, Falzon M, Fulford L, Williams NR, Keshtgar MR (2010) Comparison of three mathematical models for predicting the risk of additional axillary nodal metastases after positive sentinel lymph node biopsy in early breast cancer. Br J Surg 97:1646–1652

    Article  CAS  PubMed  Google Scholar 

  60. Fougo JL, Senra FS, Araujo C, Dias T, Afonso M, Leal C et al (2011) Validating the MSKCC nomogram and a clinical decision rule in the prediction of non-sentinel node metastases in a Portuguese population of breast cancer patients. Breast 20:134–140

    Article  PubMed  Google Scholar 

  61. Forza Operativa sul Carcinoma Mammario. Linee guida sulla diagnosi,il trattamento e la riabilitazione. Aggiornamento 2005 (2005) Attualità Senologia 46:33–106

  62. Woznick A, Franco M, Bendick P, Benitez PR (2006) Sentinel lymph node dissection for breast cancer: how many nodes are enough and which technique is optimal? Am J Surg 191:330–333

    Article  PubMed  Google Scholar 

  63. Cserni G (2007) Comparison of different validation studies on the use of the Memorial-Sloan Kettering Cancer Center nomogram predicting nonsentinel node involvement in sentinel node–positive breast cancer patients. Letters to the Editor. Am J Surg 194:699–700

    Article  PubMed  Google Scholar 

  64. Kocsis L, Svebis M, Boross G et al (2004) Use and limitations of a nomogram predicting the likelihood of non-sentinel node involvement after a positive sentinel node biopsy in breast cancer patients. Am Surg 70:1019–1024

    PubMed  Google Scholar 

  65. Soni NK, Carmalt HL, Gillett DJ, Spillane AJ (2005) Evaluation of a breast cancer nomogram for prediction of non-sentinel lymph node positivity. Eur J Surg Oncol 31:958–964

    Article  CAS  PubMed  Google Scholar 

  66. Degnim AC, Reynolds C, Pantvaidya G et al (2005) Nonsentinel node metastasis in breast cancer patients: assessment of an existing and a new predictive nomogram. Am J Surg 190:543–550

    Article  PubMed  Google Scholar 

  67. Gur AS, Unal B, Johnson R, Ahrendt G, Bonaventura M, Gordon P et al (2009) Predictive probability of four different breast cancer nomograms for nonsentinel axillary lymph node metastasis in positive sentinel node biopsy. J Am Coll Surg 208:229–235

    Article  PubMed  Google Scholar 

  68. D’Eredità G, Troilo VL, Giardina C et al (2010) Sentinel lymph node micrometastasis and risk of non-sentinel lymph node metastasis: validation of two breast cancer nomograms. Clin Breast Cancer 10(6):445–451

    Article  PubMed  Google Scholar 

  69. Kamath VJ, Giuliano R, Dauway EL et al (2001) Characteristics of the sentinel lymph node in breast cancer predict further involvement of higher-Echelon nodes in the axilla. Arch Surg 136:688–692

    Article  CAS  PubMed  Google Scholar 

  70. Rahusen FD, Torrenga H, van Diest PJ, et al (2001) Predictive factors for metastatic involvement of nonsentinel nodes in patients with breast cancer. Arch Surg 136:1059–1063

    Article  CAS  PubMed  Google Scholar 

  71. Donker M, van Tienhoven G, Straver ME et al. (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet 15:1303–1310

    Article  PubMed  PubMed Central  Google Scholar 

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Padmanabhan, N., Ayub, M.F., Hussain, K. et al. Factors Influencing Non-sentinel Node Involvement in Sentinel Node Positive Patients and Validation of MSKCC Nomogram in Indian Breast Cancer Population. Indian J Surg Oncol 6, 337–345 (2015). https://doi.org/10.1007/s13193-015-0431-y

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