Research progress about resection of primary tumor in breast cancer of stage Ⅳ_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHEN Ying , ZHANG Yan , DU Tonghua , ZHANG Jinxiang , WANG Jiaqi ,  JIANG Yi

Department of Breast Surgery, The Second Hospital of Jilin University, Changchun 130022, P. R. China;

Corresponding author：

JIANG Yi, Email: jiangyi1025@yahoo.com

Keywords：

breast cancer of stage Ⅳ; primary tumor resection; prognosis; review

DOI：

10.7507/1007-9424.201903113

Video：

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Objective To discuss the role of primary tumor resection in breast cancer of stage Ⅳ.Methods To search and review retrospective and prospective clinical trials about primary tumor resection in breast cancer of stage Ⅳ in recent years at home and abroad.Results The results of most retrospective clinical trials were that primary tumor resection in breast cancer of stage Ⅳ was beneficial. But there were some obvious bias: younger patients, smaller tumors, non-randomized design, and so on. The results of several prospective studies abroad were inconsistent. In the MF07-01, hazard of death was lower in the surgery group and subgroup analysis showed that the risk of death was lower in the surgery group with respect to positive-hormone receptor, negative-human epidermal growth factor 2, patients younger than 55 years, and patients with solitary bone-only metastases when other prospective studies come to the different conclusions. Several Chinese retrospective studies also had similar results that primary tumor resection was beneficial.Conclusion Primary tumor resection in breast cancer of stage Ⅳ can benefit some patients, whom need more prospective studies to choose.

Citation： CHEN Ying, ZHANG Yan, DU Tonghua, ZHANG Jinxiang, WANG Jiaqi, JIANG Yi. Research progress about resection of primary tumor in breast cancer of stage Ⅳ. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(8): 1016-1020. doi: 10.7507/1007-9424.201903113 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. 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.
2.	Li J, Zhang BN, Fan JH, et al. A nation-wide multicenter 10-year (1999-2008) retrospective clinical epidemiological study of female breast cancer in China. BMC Cancer, 2011, 11: 364.
3.	Fan L, Strasser-Weippl K, Li JJ, et al. Breast cancer in China. Lancet Oncol, 2014, 15(7): e279-e289.
4.	Ruiterkamp J, Ernst MF, de Munck L, et al. Improved survival of patients with primary distant metastatic breast cancer in the period of 1995-2008. A nationwide population-based study in the Netherlands. Breast Cancer Res Treat, 2011, 128(2): 495-503.
5.	Shien T, Nakamura K, Shibata T, et al. A randomized controlled trial comparing primary tumour resection plus systemic therapy with systemic therapy alone in metastatic breast cancer (PRIM-BC): Japan Clinical Oncology Group Study JCOG1017. Jpn J Clin Oncol, 2012, 42(10): 970-973.
6.	Miller JW, Smith JL, Ryerson AB, et al. Disparities in breast cancer survival in the United States (2001-2009): findings from the CONCORD-2 study. Cancer, 2017, 123(Suppl 24): 5100-5118.
7.	Xiong Z, Deng G, Huang X, et al. Score for the survival probability in metastasis breast cancer: a nomogram-based risk assessment model. Cancer Res Treat, 2018, 50(4): 1260-1269.
8.	Danna EA, Sinha P, Gilbert M, et al. Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res, 2004, 64(6): 2205-2211.
9.	Norton L, Massagué J. Is cancer a disease of self-seeding? Nat Med, 2006, 12(8): 875-878.
10.	Folkman J. New perspectives in clinical oncology from angiogenesis research. Eur J Cancer, 1996, 32A(14): 2534-2539.
11.	Cady B, Nathan NR, Michaelson JS, et al. Matched pair analyses of stage Ⅳ breast cancer with or without resection of primary breast site. Ann Surg Oncol, 2008, 15(12): 3384-3395.
12.	Rapiti E, Verkooijen HM, Vlastos G, et al. Complete excision of primary breast tumor improves survival of patients with metastatic breast cancer at diagnosis. J Clin Oncol, 2006, 24(18): 2743-2749.
13.	Babiera GV, Rao R, Feng L, et al. Effect of primary tumor extirpation in breast cancer patients who present with stage Ⅳ disease and an intact primary tumor. Ann Surg Oncol, 2006, 13(6): 776-782.
14.	Fields RC, Jeffe DB, Trinkaus K, et al. Surgical resection of the primary tumor is associated with increased long-term survival in patients with stage Ⅳ breast cancer after controlling for site of metastasis. Ann Surg Oncol, 2007, 14(12): 3345-3351.
15.	McGuire KP, Eisen S, Rodriguez A, et al. Factors associated with improved outcome after surgery in metastatic breast cancer patients. Am J Surg, 2009, 198(4): 511-515.
16.	Shien T, Kinoshita T, Shimizu C, et al. Primary tumor resection improves the survival of younger patients with metastatic breast cancer. Oncol Rep, 2009, 21(3): 827-832.
17.	Ruiterkamp J, Ernst MF, van de Poll-Franse LV, et al. Surgical resection of the primary tumour is associated with improved survival in patients with distant metastatic breast cancer at diagnosis. Eur J Surg Oncol, 2009, 35(11): 1146-1151.
18.	Neuman HB, Morrogh M, Gonen M, et al. Stage Ⅳ breast cancer in the era of targeted therapy: does surgery of the primary tumor matter? Cancer, 2010, 116(5): 1226-1233.
19.	Nguyen DH, Truong PT, Alexander C, et al. Can locoregional treatment of the primary tumor improve outcomes for women with stage Ⅳ breast cancer at diagnosis? Int J Radiat Oncol Biol Phys, 2012, 84(1): 39-45.
20.	Nguyen DH, Truong PT, Walter CV, et al. Limited M1 disease: a significant prognostic factor for stage Ⅳ breast cancer. Ann Surg Oncol, 2012, 19(9): 3028-3034.
21.	Rashaan ZM, Bastiaannet E, Portielje JE, et al. Surgery in metastatic breast cancer: patients with a favorable profile seem to have the most benefit from surgery. Eur J Surg Oncol, 2012, 38(1): 52-56.
22.	Thomas A, Khan SA, Chrischilles EA, et al. Initial surgery and survival in stage Ⅳ breast cancer in the United States, 1988-2011. JAMA Surg, 2016, 151(5): 424-431.
23.	Blanchard DK, Shetty PB, Hilsenbeck SG, et al. Association of surgery with improved survival in stage Ⅳ breast cancer patients. Ann Surg, 2008, 247(5): 732-738.
24.	Harano K, Lei X, Gonzalez-Angulo AM, et al. Clinicopathological and surgical factors associated with long-term survival in patients with HER2-positive metastatic breast cancer. Breast Cancer Res Treat, 2016, 159(2): 367-374.
25.	Wong Y, Raghavendra AS, Hatzis C, et al. Long-term survival of de novo stage Ⅳ human epidermal growth receptor 2 (HER2) positive breast cancers treated with HER2-targeted therapy. Oncologist, 2019, 24(3): 313-318.
26.	AlJohani B, AlMalik O, Anwar E, et al. Impact of surgery on survival in stage Ⅳ breast cancer. Breast J, 2016, 22(6): 678-682.
27.	Kim HJ, Kang E, Kim JH, et al. Survival benefit of surgical removal of primary tumor in patients with stage Ⅳ breast cancer. Clin Breast Cancer, 2018, 18(5): e1037-e1044.
28.	Badwe R, Hawaldar R, Nair N, et al. Locoregional treatment versus no treatment of the primary tumour in metastatic breast cancer: an open-label randomised controlled trial. Lancet Oncol, 2015, 16(13): 1380-1388.
29.	King TA, Lyman JP, Gonen M, et al. A prospective analysis of surgery and survival in stage Ⅳ breast cancer (TBCRC 013). J Clin Oncol, 2016, 34(15): 1006.
30.	Fitzal F, Bjelic-Radisic V, Knauer M, et al. Impact of breast surgery in primary metastasized breast cancer: outcomes of the prospective randomized phase Ⅲ ABCSG-28 POSYTIVE trial. Ann Surg, 2019, 269(6): 1163-1169.
31.	Soran A, Ozmen V, Ozbas S, et al. Randomized trial comparing resection of primary tumor with no surgery in stage Ⅳ breast cancer at presentation: protocol MF07-01. Ann Surg Oncol, 2018, 25(11): 3141-3149.
32.	Petrelli F, Barni S. Surgery of primary tumors in stage Ⅳ breast cancer: an updated meta-analysis of published studies with meta-regression. Med Oncol, 2012, 29(5): 3282-3290.
33.	Harris E, Barry M, Kell MR. Meta-analysis to determine if surgical resection of the primary tumour in the setting of stage Ⅳ breast cancer impacts on survival. Ann Surg Oncol, 2013, 20(9): 2828-2834.
34.	Lu S, Wu J, Fang Y, et al. The impact of surgical excision of the primary tumor in stage Ⅳ breast cancer on survival: a meta-analysis. Oncotarget, 2017, 9(14): 11816-11823.
35.	Ruiterkamp J, Voogd AC, Tjan-Heijnen VC, et al. SUBMIT: systemic therapy with or without up front surgery of the primary tumor in breast cancer patients with distant metastases at initial presentation. BMC Surg, 2012, 12: 5.
36.	National Cancer Institute. Early surgery or standard palliative therapy in treating patients with stage Ⅳ breast cancer. https: //www.cancer.gov/about-cancer/treatment/clinical-trials/search/v?id=NCT01242800&r=1.
37.	Xie Y, Lv X, Luo C, et al. Surgery of the primary tumor improves survival in women with stage Ⅳ breast cancer in Southwest China: a retrospective analysis. Medicine (Baltimore), 2017, 96(22): e7048.
38.	Wang W, Liu J, Wang J, et al. Impact of locoregional treatment on prognosis of de novo stage Ⅳ breast cancer: a retrospective long-term study of Chinese population. Gynecol Obstet Invest, 2019, 84(3): 248-258.
39.	Xiong Z, Deng G, Wang J, et al. Could local surgery improve survival in de novo stage Ⅳ breast cancer? BMC Cancer, 2018, 18(1): 885.
40.	Co M, Ng J, Kwong A. De-novo metastatic breast cancers with or without primary tumor resection-a 10-year study. Cancer Treat Res Commun, 2019, 19: 100118.
41.	Han MR, Zheng W, Cai Q, et al. Evaluating genetic variants associated with breast cancer risk in high and moderate-penetrance genes in Asians. Carcinogenesis, 2017, 38(5): 511-518.
42.	Pons-Tostivint E, Kirova Y, Lusque A, et al. Survival impact of locoregional treatment of the primary tumor in de novo metastatic breast cancers in a large multicentric cohort study: a propensity score-matched analysis. Ann Surg Oncol, 2019, 26(2): 356-365.
43.	Peng Z, Wei J, Lu X, et al. Diagnosis and treatment pattern among rural and urban breast cancer patients in Southwest China from 2005 to 2009. Oncotarget, 2016, 7(47): 78168-78179.
44.	Jackisch C, Leinweber M, Küchenmeister U, et al. Psychosocial acceptance of surgical interventions of the breast in oncological gynecology. Zentralbl Gynakol, 1997, 119(5): 218-224.

1. Bray F, Ferlay J, Soerjomataram I, et al. 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.
2. Li J, Zhang BN, Fan JH, et al. A nation-wide multicenter 10-year (1999-2008) retrospective clinical epidemiological study of female breast cancer in China. BMC Cancer, 2011, 11: 364.
3. Fan L, Strasser-Weippl K, Li JJ, et al. Breast cancer in China. Lancet Oncol, 2014, 15(7): e279-e289.
4. Ruiterkamp J, Ernst MF, de Munck L, et al. Improved survival of patients with primary distant metastatic breast cancer in the period of 1995-2008. A nationwide population-based study in the Netherlands. Breast Cancer Res Treat, 2011, 128(2): 495-503.
5. Shien T, Nakamura K, Shibata T, et al. A randomized controlled trial comparing primary tumour resection plus systemic therapy with systemic therapy alone in metastatic breast cancer (PRIM-BC): Japan Clinical Oncology Group Study JCOG1017. Jpn J Clin Oncol, 2012, 42(10): 970-973.
6. Miller JW, Smith JL, Ryerson AB, et al. Disparities in breast cancer survival in the United States (2001-2009): findings from the CONCORD-2 study. Cancer, 2017, 123(Suppl 24): 5100-5118.
7. Xiong Z, Deng G, Huang X, et al. Score for the survival probability in metastasis breast cancer: a nomogram-based risk assessment model. Cancer Res Treat, 2018, 50(4): 1260-1269.
8. Danna EA, Sinha P, Gilbert M, et al. Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res, 2004, 64(6): 2205-2211.
9. Norton L, Massagué J. Is cancer a disease of self-seeding? Nat Med, 2006, 12(8): 875-878.
10. Folkman J. New perspectives in clinical oncology from angiogenesis research. Eur J Cancer, 1996, 32A(14): 2534-2539.
11. Cady B, Nathan NR, Michaelson JS, et al. Matched pair analyses of stage Ⅳ breast cancer with or without resection of primary breast site. Ann Surg Oncol, 2008, 15(12): 3384-3395.
12. Rapiti E, Verkooijen HM, Vlastos G, et al. Complete excision of primary breast tumor improves survival of patients with metastatic breast cancer at diagnosis. J Clin Oncol, 2006, 24(18): 2743-2749.
13. Babiera GV, Rao R, Feng L, et al. Effect of primary tumor extirpation in breast cancer patients who present with stage Ⅳ disease and an intact primary tumor. Ann Surg Oncol, 2006, 13(6): 776-782.
14. Fields RC, Jeffe DB, Trinkaus K, et al. Surgical resection of the primary tumor is associated with increased long-term survival in patients with stage Ⅳ breast cancer after controlling for site of metastasis. Ann Surg Oncol, 2007, 14(12): 3345-3351.
15. McGuire KP, Eisen S, Rodriguez A, et al. Factors associated with improved outcome after surgery in metastatic breast cancer patients. Am J Surg, 2009, 198(4): 511-515.
16. Shien T, Kinoshita T, Shimizu C, et al. Primary tumor resection improves the survival of younger patients with metastatic breast cancer. Oncol Rep, 2009, 21(3): 827-832.
17. Ruiterkamp J, Ernst MF, van de Poll-Franse LV, et al. Surgical resection of the primary tumour is associated with improved survival in patients with distant metastatic breast cancer at diagnosis. Eur J Surg Oncol, 2009, 35(11): 1146-1151.
18. Neuman HB, Morrogh M, Gonen M, et al. Stage Ⅳ breast cancer in the era of targeted therapy: does surgery of the primary tumor matter? Cancer, 2010, 116(5): 1226-1233.
19. Nguyen DH, Truong PT, Alexander C, et al. Can locoregional treatment of the primary tumor improve outcomes for women with stage Ⅳ breast cancer at diagnosis? Int J Radiat Oncol Biol Phys, 2012, 84(1): 39-45.
20. Nguyen DH, Truong PT, Walter CV, et al. Limited M1 disease: a significant prognostic factor for stage Ⅳ breast cancer. Ann Surg Oncol, 2012, 19(9): 3028-3034.
21. Rashaan ZM, Bastiaannet E, Portielje JE, et al. Surgery in metastatic breast cancer: patients with a favorable profile seem to have the most benefit from surgery. Eur J Surg Oncol, 2012, 38(1): 52-56.
22. Thomas A, Khan SA, Chrischilles EA, et al. Initial surgery and survival in stage Ⅳ breast cancer in the United States, 1988-2011. JAMA Surg, 2016, 151(5): 424-431.
23. Blanchard DK, Shetty PB, Hilsenbeck SG, et al. Association of surgery with improved survival in stage Ⅳ breast cancer patients. Ann Surg, 2008, 247(5): 732-738.
24. Harano K, Lei X, Gonzalez-Angulo AM, et al. Clinicopathological and surgical factors associated with long-term survival in patients with HER2-positive metastatic breast cancer. Breast Cancer Res Treat, 2016, 159(2): 367-374.
25. Wong Y, Raghavendra AS, Hatzis C, et al. Long-term survival of de novo stage Ⅳ human epidermal growth receptor 2 (HER2) positive breast cancers treated with HER2-targeted therapy. Oncologist, 2019, 24(3): 313-318.
26. AlJohani B, AlMalik O, Anwar E, et al. Impact of surgery on survival in stage Ⅳ breast cancer. Breast J, 2016, 22(6): 678-682.
27. Kim HJ, Kang E, Kim JH, et al. Survival benefit of surgical removal of primary tumor in patients with stage Ⅳ breast cancer. Clin Breast Cancer, 2018, 18(5): e1037-e1044.
28. Badwe R, Hawaldar R, Nair N, et al. Locoregional treatment versus no treatment of the primary tumour in metastatic breast cancer: an open-label randomised controlled trial. Lancet Oncol, 2015, 16(13): 1380-1388.
29. King TA, Lyman JP, Gonen M, et al. A prospective analysis of surgery and survival in stage Ⅳ breast cancer (TBCRC 013). J Clin Oncol, 2016, 34(15): 1006.
30. Fitzal F, Bjelic-Radisic V, Knauer M, et al. Impact of breast surgery in primary metastasized breast cancer: outcomes of the prospective randomized phase Ⅲ ABCSG-28 POSYTIVE trial. Ann Surg, 2019, 269(6): 1163-1169.
31. Soran A, Ozmen V, Ozbas S, et al. Randomized trial comparing resection of primary tumor with no surgery in stage Ⅳ breast cancer at presentation: protocol MF07-01. Ann Surg Oncol, 2018, 25(11): 3141-3149.
32. Petrelli F, Barni S. Surgery of primary tumors in stage Ⅳ breast cancer: an updated meta-analysis of published studies with meta-regression. Med Oncol, 2012, 29(5): 3282-3290.
33. Harris E, Barry M, Kell MR. Meta-analysis to determine if surgical resection of the primary tumour in the setting of stage Ⅳ breast cancer impacts on survival. Ann Surg Oncol, 2013, 20(9): 2828-2834.
34. Lu S, Wu J, Fang Y, et al. The impact of surgical excision of the primary tumor in stage Ⅳ breast cancer on survival: a meta-analysis. Oncotarget, 2017, 9(14): 11816-11823.
35. Ruiterkamp J, Voogd AC, Tjan-Heijnen VC, et al. SUBMIT: systemic therapy with or without up front surgery of the primary tumor in breast cancer patients with distant metastases at initial presentation. BMC Surg, 2012, 12: 5.
36. National Cancer Institute. Early surgery or standard palliative therapy in treating patients with stage Ⅳ breast cancer. https: //www.cancer.gov/about-cancer/treatment/clinical-trials/search/v?id=NCT01242800&r=1.
37. Xie Y, Lv X, Luo C, et al. Surgery of the primary tumor improves survival in women with stage Ⅳ breast cancer in Southwest China: a retrospective analysis. Medicine (Baltimore), 2017, 96(22): e7048.
38. Wang W, Liu J, Wang J, et al. Impact of locoregional treatment on prognosis of de novo stage Ⅳ breast cancer: a retrospective long-term study of Chinese population. Gynecol Obstet Invest, 2019, 84(3): 248-258.
39. Xiong Z, Deng G, Wang J, et al. Could local surgery improve survival in de novo stage Ⅳ breast cancer? BMC Cancer, 2018, 18(1): 885.
40. Co M, Ng J, Kwong A. De-novo metastatic breast cancers with or without primary tumor resection-a 10-year study. Cancer Treat Res Commun, 2019, 19: 100118.
41. Han MR, Zheng W, Cai Q, et al. Evaluating genetic variants associated with breast cancer risk in high and moderate-penetrance genes in Asians. Carcinogenesis, 2017, 38(5): 511-518.
42. Pons-Tostivint E, Kirova Y, Lusque A, et al. Survival impact of locoregional treatment of the primary tumor in de novo metastatic breast cancers in a large multicentric cohort study: a propensity score-matched analysis. Ann Surg Oncol, 2019, 26(2): 356-365.
43. Peng Z, Wei J, Lu X, et al. Diagnosis and treatment pattern among rural and urban breast cancer patients in Southwest China from 2005 to 2009. Oncotarget, 2016, 7(47): 78168-78179.
44. Jackisch C, Leinweber M, Küchenmeister U, et al. Psychosocial acceptance of surgical interventions of the breast in oncological gynecology. Zentralbl Gynakol, 1997, 119(5): 218-224.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress about resection of primary tumor in breast cancer of stage Ⅳ

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