Prognostic effects of breast conservation therapy and mastectomy on different luminal subtypes of early breast cancer: a meta-analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

OUYANG Chibin ^1,2 ,  DU Zhenggui ¹

1. Department of Breast Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Department of Breast, Sichuan Jinxin Women and Children’s Hospital, Chengdu 610066, P. R. China;

Corresponding author：

DU Zhenggui, Email: docduzg@163.com

Keywords：

　luminal breast cancer; breast conservation therapy; mastectomy; molecular subtype; prognosis

DOI：

10.7507/1007-9424.201909067

Video：

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Objective To investigate the effect of breast conservation therapy (BCT) and mastectomy (Mast) on the prognosis of early luminal breast cancer (ELBC).Methods By retrieving the PubMed, Embase, Web of Science, CNKI, Wanfang data, and VIP databases, the meta-analysis was performed on the documents that met the inclusion criteria. The Review Manager 5.3 and Stata 12.0 were used for statistical analysis.Results A total of 25 articles were included, involving 13 032 patients with ELBC, of which 8 419 underwent the BCT and 4 613 underwent the Mast. The results of meta-analysis showed that there was no significant difference in the postoperative local regional relapse (LRR) between the BCT and the Mast in the treatment of all patients with ELBC [OR=0.84, 95% CI (0.43, 1.64), P=0.61]. For treating with BCT, the local relapse (LR), distant metastasis rate (DMR), disease-free survival (DFS), and overall survival (OS) in the patients with luminal A ELBC were better than those in the patients with luminal B ELBC (P<0.05); Using the same method, the DMR and DFS in the patients with luminal A/B ELBC were better than those in the patients with luminal-HER2 ELBC (P<0.05). For treating with Mast, the LRR, LR, DMR, and OS in the patients with luminal A ELBC were better than those in the patients with luminal B ELBC (P<0.05); Using the same method, the LRR in the patients with luminal A/B ELBC was better than that in the patients with luminal-HER2 ELBC (P<0.05).Conclusions For patients with ELBC, similar LRR can be obtained by BCT and Mast treatment. Regardless of the surgical strategy, patients with luminal A ELBC are more likely to obtain relatively ideal clinical prognosis. Luminal-HER2 ELBC has the worst prognosis after BCT treatment.

Citation： OUYANG Chibin, DU Zhenggui. Prognostic effects of breast conservation therapy and mastectomy on different luminal subtypes of early breast cancer: a meta-analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(3): 326-336. doi: 10.7507/1007-9424.201909067 Copy

1.	Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med, 2002, 347(16): 1233-1241.
2.	Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med, 2002, 347(16): 1227-1232.
3.	Fodor J, Major T, Polgár C, et al. Prognosis of patients with local recurrence after mastectomy or conservative surgery for early-stage invasive breast cancer. Breast, 2008, 17(3): 302-308.
4.	Fodor J, Polgár C, Major T, et al. The time-course of metastases from breast cancer after mastectomy and breast-conserving surgery with and without isolated local-regional recurrence. Breast, 2002, 11(1): 53-57.
5.	van Dongen JA, Voogd AC, Fentiman IS, et al. Long-term results of a randomized trial comparing breast-conserving therapy with mastectomy: European Organization for Research and Treatment of Cancer 10801 trial. J Natl Cancer Inst, 2000, 92(14): 1143-1150.
6.	Holland R, Veling SH, Mravunac M, et al. Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer, 1985, 56(5): 979-990.
7.	Clarke M, Collins R, Darby S, et al. 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(9503): 2087-2106.
8.	Buchholz TA, Wazer DE. Molecular biology and genetics of breast cancer development: a clinical perspective. Semin Radiat Oncol, 2002, 12(4): 285-295.
9.	van’t Veer LJ, Dai H, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature, 2002, 415(6871): 530-536.
10.	Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA, 2003, 100(14): 8418-8423.
11.	Tang P, Skinner KA, Hicks DG. Molecular classification of breast carcinomas by immunohistochemical analysis: are we ready? Diagn Mol Pathol, 2009, 18(3): 125-132.
12.	Nguyen PL, Taghian AG, Katz MS, et al. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol, 2008, 26(14): 2373-2378.
13.	Voduc KD, Cheang MC, Tyldesley S, et al. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol, 2010, 28(10): 1684-1691.
14.	Lowery AJ, Kell MR, Glynn RW, et al. Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat, 2012, 133(3): 831-841.
15.	Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials, 1996, 17(1): 1-12.
16.	Song F, Sheldon TA, Sutton AJ, et al. Methods for exploring heterogeneity in meta-analysis. Eval Health Prof, 2001, 24(2): 126-151.
17.	Bane AL, Whelan TJ, Pond GR, et al. Tumor factors predictive of response to hypofractionated radiotherapy in a randomized trial following breast conserving therapy. Ann Oncol, 2014, 25(5): 992-998.
18.	Braunstein LZ, Taghian AG, Niemierko A, et al. Breast-cancer subtype, age, and lymph node status as predictors of local recurrence following breast-conserving therapy. Breast Cancer Res Treat, 2017, 161(1): 173-179.
19.	Braunstein LZ, Niemierko A, Shenouda MN, et al. Outcome following local-regional recurrence in women with early-stage breast cancer: impact of biologic subtype. Breast J, 2015, 21(2): 161-167.
20.	Jwa E, Shin KH, Kim JY, et al. Locoregional recurrence by tumor biology in breast cancer patients after preoperative chemotherapy and breast conservation treatment. Cancer Res Treat, 2016, 48(4): 1363-1372.
21.	Demirci S, Broadwater G, Marks LB, et al. Breast conservation therapy: the influence of molecular subtype and margins. Int J Radiat Oncol Biol Phys, 2012, 83(3): 814-820.
22.	Gabos Z, Thoms J, Ghosh S, et al. The association between biological subtype and locoregional recurrence in newly diagnosed breast cancer. Breast Cancer Res Treat, 2010, 124(1): 187-194.
23.	Gangi A, Chung A, Mirocha J, et al. Breast-conserving therapy for triple-negative breast cancer. JAMA Surg, 2014, 149(3): 252-258.
24.	Ihemelandu CU, Naab TJ, Mezghebe HM, et al. Treatment and survival outcome for molecular breast cancer subtypes in black women. Ann Surg, 2008, 247(3): 463-469.
25.	Wen G, Zhang JS, Zhang YJ, et al. Predictive value of molecular subtyping for locoregional recurrence in early-stage breast cancer with N1 without postmastectomy radiotherapy. J Breast Cancer, 2016, 19(2): 176-184.
26.	Kaiser J, Kronberger C, Moder A, et al. Intraoperative tumor bed boost with electrons in breast cancer of clinical stages Ⅰ through Ⅲ: updated 10-year results. Int J Radiat Oncol Biol Phys, 2018, 102(1): 92-101.
27.	Ragaz J, Jackson SM, Le N, et al. Adjuvant radiotherapy and chemotherapy in node-positive premenopausal women with breast cancer. N Engl J Med, 1997, 337(14): 956-962.
28.	Overgaard M, Hansen PS, Overgaard J, et al. Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. Danish Breast Cancer Cooperative Group 82b Trial. N Engl J Med, 1997, 337(14): 949-955.
29.	Mazouni C, Rimareix F, Mathieu MC, et al. Outcome in breast molecular subtypes according to nodal status and surgical procedures. Am J Surg, 2013, 205(6): 662-667.
30.	Mersin H, Gülben K, Berberoğlu U, et al. Prognostic factors affecting postmastectomy locoregional recurrence in patients with early breast cancer: are intrinsic subtypes effective? World J Surg, 2011, 35(10): 2196-2202.
31.	Meyers MO, Klauber-Demore N, Ollila DW, et al. Impact of breast cancer molecular subtypes on locoregional recurrence in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. Ann Surg Oncol, 2011, 18(10): 2851-2857.
32.	Moo TA, McMillan R, Lee M, et al. Impact of molecular subtype on locoregional recurrence in mastectomy patients with T1-T2 breast cancer and 1-3 positive lymph nodes. Ann Surg Oncol, 2014, 21(5): 1569-1574.
33.	Jia WJ, Jia HX, Feng HY, et al. HER2-enriched tumors have the highest risk of local recurrence in Chinese patients treated with breast conservation therapy. Asian Pac J Cancer Prev, 2014, 15(1): 315-320.
34.	Millar EK, Graham PH, O'Toole SA, et al. Prediction of local recurrence, distant metastases, and death after breast-conserving therapy in early-stage invasive breast cancer using a five-biomarker panel. J Clin Oncol, 2009, 27(28): 4701-4708.
35.	Sanpaolo P, Barbieri V, Genovesi D. Prognostic value of breast cancer subtypes on breast cancer specific survival, distant metastases and local relapse rates in conservatively managed early stage breast cancer: a retrospective clinical study. Eur J Surg Oncol, 2011, 37(10): 876-882.
36.	Straver ME, Rutgers EJ, Rodenhuis S, et al. The relevance of breast cancer subtypes in the outcome of neoadjuvant chemotherapy. Ann Surg Oncol, 2010, 17(9): 2411-2418.
37.	Wong FY, Chin FK, Lee KA, et al. Hormone receptors and HER-2 status as surrogates for breast cancer molecular subtypes prognosticate for disease control in node negative Asian patients treated with breast conservation therapy. Ann Acad Med Singapore, 2011, 40(2): 90-96.
38.	Yamazaki N, Wada N, Yamauchi C, et al. High expression of post-treatment Ki-67 status is a risk factor for locoregional recurrence following breast-conserving surgery after neoadjuvant chemotherapy. Eur J Surg Oncol, 2015, 41(5): 617-624.
39.	Wu SG, He ZY, Li Q, et al. Predictive value of breast cancer molecular subtypes in Chinese patients with four or more positive nodes after postmastectomy radiotherapy. Breast, 2012, 21(5): 657-661.
40.	Nakamura N, Arahira S, Zenda S, et al. Post-mastectomy radiation therapy without usage of a bolus may be a reasonable option. J Radiat Res, 2017, 58(1): 66-70.
41.	Sørlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A, 2001, 98(19): 10869-10874.
42.	Rouzier R, Perou CM, Symmans WF, et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res, 2005, 11(16): 5678-5685.
43.	Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol, 2009, 27(8): 1160-1167.
44.	Haffty BG, Yang Q, Reiss M, et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol, 2006, 24(36): 5652-5657.
45.	Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res, 2007, 13(15 Pt 1): 4429-4434.

1. Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med, 2002, 347(16): 1233-1241.
2. Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med, 2002, 347(16): 1227-1232.
3. Fodor J, Major T, Polgár C, et al. Prognosis of patients with local recurrence after mastectomy or conservative surgery for early-stage invasive breast cancer. Breast, 2008, 17(3): 302-308.
4. Fodor J, Polgár C, Major T, et al. The time-course of metastases from breast cancer after mastectomy and breast-conserving surgery with and without isolated local-regional recurrence. Breast, 2002, 11(1): 53-57.
5. van Dongen JA, Voogd AC, Fentiman IS, et al. Long-term results of a randomized trial comparing breast-conserving therapy with mastectomy: European Organization for Research and Treatment of Cancer 10801 trial. J Natl Cancer Inst, 2000, 92(14): 1143-1150.
6. Holland R, Veling SH, Mravunac M, et al. Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer, 1985, 56(5): 979-990.
7. Clarke M, Collins R, Darby S, et al. 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(9503): 2087-2106.
8. Buchholz TA, Wazer DE. Molecular biology and genetics of breast cancer development: a clinical perspective. Semin Radiat Oncol, 2002, 12(4): 285-295.
9. van’t Veer LJ, Dai H, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature, 2002, 415(6871): 530-536.
10. Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA, 2003, 100(14): 8418-8423.
11. Tang P, Skinner KA, Hicks DG. Molecular classification of breast carcinomas by immunohistochemical analysis: are we ready? Diagn Mol Pathol, 2009, 18(3): 125-132.
12. Nguyen PL, Taghian AG, Katz MS, et al. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol, 2008, 26(14): 2373-2378.
13. Voduc KD, Cheang MC, Tyldesley S, et al. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol, 2010, 28(10): 1684-1691.
14. Lowery AJ, Kell MR, Glynn RW, et al. Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat, 2012, 133(3): 831-841.
15. Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials, 1996, 17(1): 1-12.
16. Song F, Sheldon TA, Sutton AJ, et al. Methods for exploring heterogeneity in meta-analysis. Eval Health Prof, 2001, 24(2): 126-151.
17. Bane AL, Whelan TJ, Pond GR, et al. Tumor factors predictive of response to hypofractionated radiotherapy in a randomized trial following breast conserving therapy. Ann Oncol, 2014, 25(5): 992-998.
18. Braunstein LZ, Taghian AG, Niemierko A, et al. Breast-cancer subtype, age, and lymph node status as predictors of local recurrence following breast-conserving therapy. Breast Cancer Res Treat, 2017, 161(1): 173-179.
19. Braunstein LZ, Niemierko A, Shenouda MN, et al. Outcome following local-regional recurrence in women with early-stage breast cancer: impact of biologic subtype. Breast J, 2015, 21(2): 161-167.
20. Jwa E, Shin KH, Kim JY, et al. Locoregional recurrence by tumor biology in breast cancer patients after preoperative chemotherapy and breast conservation treatment. Cancer Res Treat, 2016, 48(4): 1363-1372.
21. Demirci S, Broadwater G, Marks LB, et al. Breast conservation therapy: the influence of molecular subtype and margins. Int J Radiat Oncol Biol Phys, 2012, 83(3): 814-820.
22. Gabos Z, Thoms J, Ghosh S, et al. The association between biological subtype and locoregional recurrence in newly diagnosed breast cancer. Breast Cancer Res Treat, 2010, 124(1): 187-194.
23. Gangi A, Chung A, Mirocha J, et al. Breast-conserving therapy for triple-negative breast cancer. JAMA Surg, 2014, 149(3): 252-258.
24. Ihemelandu CU, Naab TJ, Mezghebe HM, et al. Treatment and survival outcome for molecular breast cancer subtypes in black women. Ann Surg, 2008, 247(3): 463-469.
25. Wen G, Zhang JS, Zhang YJ, et al. Predictive value of molecular subtyping for locoregional recurrence in early-stage breast cancer with N1 without postmastectomy radiotherapy. J Breast Cancer, 2016, 19(2): 176-184.
26. Kaiser J, Kronberger C, Moder A, et al. Intraoperative tumor bed boost with electrons in breast cancer of clinical stages Ⅰ through Ⅲ: updated 10-year results. Int J Radiat Oncol Biol Phys, 2018, 102(1): 92-101.
27. Ragaz J, Jackson SM, Le N, et al. Adjuvant radiotherapy and chemotherapy in node-positive premenopausal women with breast cancer. N Engl J Med, 1997, 337(14): 956-962.
28. Overgaard M, Hansen PS, Overgaard J, et al. Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. Danish Breast Cancer Cooperative Group 82b Trial. N Engl J Med, 1997, 337(14): 949-955.
29. Mazouni C, Rimareix F, Mathieu MC, et al. Outcome in breast molecular subtypes according to nodal status and surgical procedures. Am J Surg, 2013, 205(6): 662-667.
30. Mersin H, Gülben K, Berberoğlu U, et al. Prognostic factors affecting postmastectomy locoregional recurrence in patients with early breast cancer: are intrinsic subtypes effective? World J Surg, 2011, 35(10): 2196-2202.
31. Meyers MO, Klauber-Demore N, Ollila DW, et al. Impact of breast cancer molecular subtypes on locoregional recurrence in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. Ann Surg Oncol, 2011, 18(10): 2851-2857.
32. Moo TA, McMillan R, Lee M, et al. Impact of molecular subtype on locoregional recurrence in mastectomy patients with T1-T2 breast cancer and 1-3 positive lymph nodes. Ann Surg Oncol, 2014, 21(5): 1569-1574.
33. Jia WJ, Jia HX, Feng HY, et al. HER2-enriched tumors have the highest risk of local recurrence in Chinese patients treated with breast conservation therapy. Asian Pac J Cancer Prev, 2014, 15(1): 315-320.
34. Millar EK, Graham PH, O'Toole SA, et al. Prediction of local recurrence, distant metastases, and death after breast-conserving therapy in early-stage invasive breast cancer using a five-biomarker panel. J Clin Oncol, 2009, 27(28): 4701-4708.
35. Sanpaolo P, Barbieri V, Genovesi D. Prognostic value of breast cancer subtypes on breast cancer specific survival, distant metastases and local relapse rates in conservatively managed early stage breast cancer: a retrospective clinical study. Eur J Surg Oncol, 2011, 37(10): 876-882.
36. Straver ME, Rutgers EJ, Rodenhuis S, et al. The relevance of breast cancer subtypes in the outcome of neoadjuvant chemotherapy. Ann Surg Oncol, 2010, 17(9): 2411-2418.
37. Wong FY, Chin FK, Lee KA, et al. Hormone receptors and HER-2 status as surrogates for breast cancer molecular subtypes prognosticate for disease control in node negative Asian patients treated with breast conservation therapy. Ann Acad Med Singapore, 2011, 40(2): 90-96.
38. Yamazaki N, Wada N, Yamauchi C, et al. High expression of post-treatment Ki-67 status is a risk factor for locoregional recurrence following breast-conserving surgery after neoadjuvant chemotherapy. Eur J Surg Oncol, 2015, 41(5): 617-624.
39. Wu SG, He ZY, Li Q, et al. Predictive value of breast cancer molecular subtypes in Chinese patients with four or more positive nodes after postmastectomy radiotherapy. Breast, 2012, 21(5): 657-661.
40. Nakamura N, Arahira S, Zenda S, et al. Post-mastectomy radiation therapy without usage of a bolus may be a reasonable option. J Radiat Res, 2017, 58(1): 66-70.
41. Sørlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A, 2001, 98(19): 10869-10874.
42. Rouzier R, Perou CM, Symmans WF, et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res, 2005, 11(16): 5678-5685.
43. Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol, 2009, 27(8): 1160-1167.
44. Haffty BG, Yang Q, Reiss M, et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol, 2006, 24(36): 5652-5657.
45. Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res, 2007, 13(15 Pt 1): 4429-4434.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Prognostic effects of breast conservation therapy and mastectomy on different luminal subtypes of early breast cancer: a meta-analysis

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