Long-term survival of primary tumor resection <i>versus</i> chemotherapy alone for asymptomatic stage Ⅳ colorectal cancer patients with unresectable synchronous metastasis: a pooled-analysis and trial sequential analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHENG Bobo ¹ , YUE Yumin ¹ , WANG Xin ² , WANG Quan ³ ,  WANG Guorong ¹

1. Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an 710068, P. R. China;
2. Department of Gastroenterology, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an 710068, P. R. China;
3. Day Surgery Center, Xijing Hospital, Air Force Medical University, Xi’an 710068, P. R. China;

Corresponding author：

WANG Guorong, Email: 13227701303@qq.com

Keywords：

primary tumor resection; chemotherapy; unresectable; asymptomatic; metastatic colorectal cancer

DOI：

10.7507/1007-9424.202202001

Video：

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Objective To systematically evaluate whether primary tumor resection (PTR) has a statistical survival benefit as compared with chemotherapy alone (CTA) for asymptomatic stage Ⅳ colorectal cancer patients with unresectable synchronous metastasis (ACRCUSR). Methods The PubMed, Embase, Web of Science, Cochrane Central, CNKI, Wanfang, and the other databases were searched systematically and the prospective or retrospective controlled studies of PTR versus CTA in treatment of ACRCUSR were collected. The outcomes included overall survival (OS) and overall 1–5-year survival rates. The Stata 12.0 and RevMan 5.3 softwares were used for the pooled-analysis of relative risk (RR) and hazard ratio (HR). The trial sequential analysis (TSA) software was used to analyze overall 5-year survival rate and calculate the sample size required to achieve stable results. Results A total of 35 studies involving 258 478 patients were included. The results of pooled-analysis showed that the OS of ACRCUSR with PTR was statistically better than that with CTA [HR=0.57, 95%CI (0.52, 0.61), P<0.001]; Meanwhile, it was found that the overall survival rates at 1-, 2-, 3-, 4-, and 5-year of ACRCUSR with PTR were statistically better than those with CTA [1-year: RR=1.30, 95%CI (1.21, 1.40), P<0.001; 2-year: RR=1.78, 95%CI (1.64, 1.93), P<0.001; 3-year: RR=2.10, 95%CI (1.65, 2.68), P<0.001; 4-year: RR=3.05, 95%CI (2.07, 3.44), P<0.001; 5-year: RR=3.43, 95%CI (3.00, 3.92), P<0.001]. The TSA showed the reliable outcome at overall 5-year survival rate and the sample size required to achieve stable result was 96 662 cases. Conclusion From analysis results of this study, for ACRCUSR with PTR can benefit survival as compared with CTA, which still needs to be verified by more randomized controlled trials.

Citation： ZHENG Bobo, YUE Yumin, WANG Xin, WANG Quan, WANG Guorong. Long-term survival of primary tumor resection versus chemotherapy alone for asymptomatic stage Ⅳ colorectal cancer patients with unresectable synchronous metastasis: a pooled-analysis and trial sequential analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(10): 1318-1325. doi: 10.7507/1007-9424.202202001 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.	Cook AD, Single R, McCahill LE. Surgical resection of primary tumors in patients who present with stage Ⅳ colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000. Ann Surg Oncol, 2005, 12(8): 637-645.
3.	Zhao J, Zhu J, Huang C, et al. Impact of primary tumor resection on the survival of patients with unresectable colon cancer liver metastasis at different colonic subsites: a propensity score matching analysis. Acta Chir Belg, 2021: 1-16. doi: 10.1080/00015458.2021.1956799.
4.	Kawamura H, Ogawa Y, Yamazaki H, et al. Impact of primary tumor resection on mortality in patients with stage Ⅳ colorectal cancer with unresectable metastases: a multicenter retrospective cohort study. World J Surg, 2021, 45(10): 3230-3239.
5.	Fujita Y, Hida K, Hoshino N, et al. Impact of postoperative complications after primary tumor resection on survival in patients with incurable stage Ⅳ colorectal cancer: a multicenter retrospective cohort study. Ann Gastroenterol Surg, 2021, 5(3): 354-362.
6.	Doah KY, Shin US, Jeon BH, et al. The impact of primary tumor resection on survival in asymptomatic colorectal cancer patients with unresectable metastases. Ann Coloproctol, 2021, 37(2): 94-100.
7.	Chen JN, Shoucair S, Wang Z, et al. Primary tumor resection for rectal cancer with unresectable liver metastases: a chance to cut is a chance for improved survival. Front Oncol, 2021, 11: 628715. doi: 10.3389/fonc.2021.628715.
8.	Simillis C, Kalakouti E, Afxentiou T, et al. Primary tumor resection in patients with incurable localized or metastatic colorectal cancer: a systematic review and meta-analysis. World J Surg, 2019, 43(7): 1829-1840.
9.	Kanemitsu Y, Shitara K, Mizusawa J, et al. Primary tumor resection plus chemotherapy versus chemotherapy alone for colorectal cancer patients with asymptomatic, synchronous unresectable metastases (JCOG1007; iPACS): a randomized clinical trial. J Clin Oncol, 2021, 39(10): 1098-1107.
10.	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.
11.	Wells G, SBO’Connell D, Peterson J, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ott. Hosp. Res. Inst. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
12.	周支瑞, 张天嵩, 李博, 等. 生存曲线中Meta分析适宜数据的提取与转换. 中国循证心血管医学杂志, 2014, 6(3): 243-247.
13.	Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
14.	Thorlund KEJ, Wetterslev J, Brok J, et al. (2011) User manual for trial sequential analysis (TSA), copenhagen trial unit, centre for clinical intervention research. http://www.ctu.dk/tsa.
15.	Park EJ, Baek JH, Choi GS, et al. The role of primary tumor resection in colorectal cancer patients with asymptomatic, synchronous, unresectable metastasis: a multicenter randomized controlled trial. Cancers (Basel) , 2020, 12 (8): 2306. doi: 10.3390/cancers12082306.
16.	Wang Z, Liang L, Yu Y, et al. Primary tumour resection could improve the survival of unresectable metastatic colorectal cancer patients receiving bevacizumab-containing chemotherapy. Cell Physiol Biochem, 2016, 39(3): 1239-1246.
17.	Yun JA, Huh JW, Park YA, et al. The role of palliative resection for asymptomatic primary tumor in patients with unresectable stage Ⅳ colorectal cancer. Dis Colon Rectum, 2014, 57(9): 1049-1058.
18.	Faron M, Pignon JP, Malka D, et al. Is primary tumour resection associated with survival improvement in patients with colorectal cancer and unresectable synchronous metastases? A pooled analysis of individual data from four randomised trials. Eur J Cancer, 2015, 51(2): 166-176.
19.	Huang Y, Ge K, Fu G, et al. Efficacy of primary tumor resection in metastatic colorectal cancer. Med Sci Monit, 2020, 26: e923501. doi: 10.12659/MSM.923501.
20.	Ergun Y, Bal O, Dogan M, et al. Does primary tumor resection contribute to overall survival in unresectable synchronous metastatic colorectal cancer? J Res Med Sci, 2020, 25: 14. doi: 10.4103/jrms.JRMS_1056_18.
21.	Shida D, Boku N, Tanabe T, et al. Primary tumor resection for stage Ⅳ colorectal cancer in the era of targeted chemotherapy. J Gastrointest Surg, 2019, 23(11): 2144-2150.
22.	Ahmed S, Fields A, Pahwa P, et al. Surgical resection of primary tumor in asymptomatic or minimally symptomatic patients with stage Ⅳ colorectal cancer: a canadian province experience. Clin Colorectal Cancer, 2015, 14(4): e41-e47. doi: 10.1016/j.clcc.2015.05.008.
23.	Cao G, Zhou W, Chen E, et al. A novel scoring system predicting survival benefits of palliative primary tumor resection for patients with unresectable metastatic colorectal cancer: a retrospective cohort study protocol. Medicine (Baltimore), 2019, 98(37): e17178. doi: 10.1097/MD.0000000000017178.
24.	Tsang WY, Ziogas A, Lin BS, et al. Role of primary tumor resection among chemotherapy-treated patients with synchronous stage Ⅳ colorectal cancer: a survival analysis. J Gastrointest Surg, 2014, 18(3): 592-598.
25.	Alawadi Z, Phatak UR, Hu CY, et al. Comparative effectiveness of primary tumor resection in patients with stage Ⅳ colon cancer. Cancer, 2017, 123(7): 1124-1133.
26.	Yang Y, Lu Y, Jiang W, et al. Individualized prediction of survival benefit from primary tumor resection for patients with unresectable metastatic colorectal cancer. World J Surg Oncol, 2020, 18(1): 193. doi: 10.1186/s12957-020-01972-y.
27.	Xu H, Xia Z, Jia X, et al. Primary tumor resection is associated with improved survival in stage Ⅳ colorectal cancer: an instrumental variable analysis. Sci Rep, 2015, 5: 16516. doi: 10.1038/srep16516.
28.	Tarantino I, Warschkow R, Worni M, et al. Prognostic relevance of palliative primary tumor removal in 37 793 metastatic colorectal cancer patients: a population-based, propensity score-adjusted trend analysis. Ann Surg, 2015, 262(1): 112-120.
29.	Gulack BC, Nussbaum DP, Keenan JE, et al. Surgical resection of the primary tumor in stage Ⅳ colorectal cancer without metastasectomy is associated with improved overall survival compared with chemotherapy/radiation therapy alone. Dis Colon Rectum, 2016, 59(4): 299-305.
30.	Mehta HB, Vargas GM, Adhikari D, et al. Comparative effectiveness of chemotherapy vs resection of the primary tumour as the initial treatment in older patients with stage Ⅳ colorectal cancer. Colorectal Dis, 2017, 19(6): O210-O218. doi: 10.1111/codi.13659.
31.	Maroney S, de Paz CC, Reeves ME, et al. Benefit of surgical resection of the primary tumor in patients undergoing chemotherapy for stage Ⅳ colorectal cancer with unresected metastasis. J Gastrointest Surg, 2018, 22(3): 460-466.
32.	’t Lam-Boer J, Van der Geest LG, Verhoef C, et al. Palliative resection of the primary tumor is associated with improved overall survival in incurable stage Ⅳ colorectal cancer: a nationwide population-based propensity-score adjusted study in the Netherlands. Int J Cancer, 2016, 139(9): 2082-2094.
33.	Hosseinali Khani M, Påhlman L, Smedh K. Treatment strategies for patients with stage Ⅳ rectal cancer: a report from the Swedish Rectal Cancer Registry. Eur J Cancer, 2012, 48(11): 1616-1623.
34.	Gresham G, Renouf DJ, Chan M, et al. Association between palliative resection of the primary tumor and overall survival in a population-based cohort of metastatic colorectal cancer patients. Ann Surg Oncol, 2014, 21(12): 3917-3923.
35.	Ferrand F, Malka D, Bourredjem A, et al. Impact of primary tumour resection on survival of patients with colorectal cancer and synchronous metastases treated by chemotherapy: results from the multicenter, randomised trial Fédération Francophone de Cancérologie Digestive 9601. Eur J Cancer, 2013, 49(1): 90-97.
36.	Ishihara S, Nishikawa T, Tanaka T, et al. Benefit of primary tumor resection in stage Ⅳ colorectal cancer with unresectable metastasis: a multicenter retrospective study using a propensity score analysis. Int J Colorectal Dis, 2015, 30(6): 807-812.
37.	van Rooijen KL, Shi Q, Goey KKH, et al. Prognostic value of primary tumour resection in synchronous metastatic colorectal cancer: Individual patient data analysis of first-line randomised trials from the ARCAD database. Eur J Cancer, 2018, 91: 99-106.
38.	Boselli C, Renzi C, Gemini A, et al. Surgery in asymptomatic patients with colorectal cancer and unresectable liver metastases: the authors’ experience. Onco Targets Ther, 2013, 6: 267-272.
39.	Kim SK, Lee CH, Lee MR, et al. Multivariate analysis of the survival rate for treatment modalities in incurable stage Ⅳ colorectal cancer. J Korean Soc Coloproctol, 2012, 28(1): 35-41.
40.	Yoon YS, Kim CW, Lim SB, et al. Palliative surgery in patients with unresectable colorectal liver metastases: a propensity score matching analysis. J Surg Oncol, 2014, 109(3): 239-244.
41.	Matsumoto T, Hasegawa S, Matsumoto S, et al. Overcoming the challenges of primary tumor management in patients with metastatic colorectal cancer unresectable for cure and an asymptomatic primary tumor. Dis Colon Rectum, 2014, 57(6): 679-686.
42.	Park JH, Kim TY, Lee KH, et al. The beneficial effect of palliative resection in metastatic colorectal cancer. Br J Cancer, 2013, 108(7): 1425-1431.
43.	Kim MS, Chung M, Ahn JB, et al. Clinical significance of primary tumor resection in colorectal cancer patients with synchronous unresectable metastasis. J Surg Oncol, 2014, 110(2): 214-221.
44.	Watanabe A, Yamazaki K, Kinugasa Y, et al. Influence of primary tumor resection on survival in asymptomatic patients with incurable stage Ⅳ colorectal cancer. Int J Clin Oncol, 2014, 19(6): 1037-1042.
45.	Niitsu H, Hinoi T, Shimomura M, et al. Up-front systemic chemotherapy is a feasible option compared to primary tumor resection followed by chemotherapy for colorectal cancer with unresectable synchronous metastases. World J Surg Oncol, 2015, 13: 162. doi: 10.1186/s12957-015-0570-1.

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. Cook AD, Single R, McCahill LE. Surgical resection of primary tumors in patients who present with stage Ⅳ colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000. Ann Surg Oncol, 2005, 12(8): 637-645.
3. Zhao J, Zhu J, Huang C, et al. Impact of primary tumor resection on the survival of patients with unresectable colon cancer liver metastasis at different colonic subsites: a propensity score matching analysis. Acta Chir Belg, 2021: 1-16. doi: 10.1080/00015458.2021.1956799.
4. Kawamura H, Ogawa Y, Yamazaki H, et al. Impact of primary tumor resection on mortality in patients with stage Ⅳ colorectal cancer with unresectable metastases: a multicenter retrospective cohort study. World J Surg, 2021, 45(10): 3230-3239.
5. Fujita Y, Hida K, Hoshino N, et al. Impact of postoperative complications after primary tumor resection on survival in patients with incurable stage Ⅳ colorectal cancer: a multicenter retrospective cohort study. Ann Gastroenterol Surg, 2021, 5(3): 354-362.
6. Doah KY, Shin US, Jeon BH, et al. The impact of primary tumor resection on survival in asymptomatic colorectal cancer patients with unresectable metastases. Ann Coloproctol, 2021, 37(2): 94-100.
7. Chen JN, Shoucair S, Wang Z, et al. Primary tumor resection for rectal cancer with unresectable liver metastases: a chance to cut is a chance for improved survival. Front Oncol, 2021, 11: 628715. doi: 10.3389/fonc.2021.628715.
8. Simillis C, Kalakouti E, Afxentiou T, et al. Primary tumor resection in patients with incurable localized or metastatic colorectal cancer: a systematic review and meta-analysis. World J Surg, 2019, 43(7): 1829-1840.
9. Kanemitsu Y, Shitara K, Mizusawa J, et al. Primary tumor resection plus chemotherapy versus chemotherapy alone for colorectal cancer patients with asymptomatic, synchronous unresectable metastases (JCOG1007; iPACS): a randomized clinical trial. J Clin Oncol, 2021, 39(10): 1098-1107.
10. 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.
11. Wells G, SBO’Connell D, Peterson J, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ott. Hosp. Res. Inst. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
12. 周支瑞, 张天嵩, 李博, 等. 生存曲线中Meta分析适宜数据的提取与转换. 中国循证心血管医学杂志, 2014, 6(3): 243-247.
13. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
14. Thorlund KEJ, Wetterslev J, Brok J, et al. (2011) User manual for trial sequential analysis (TSA), copenhagen trial unit, centre for clinical intervention research. http://www.ctu.dk/tsa.
15. Park EJ, Baek JH, Choi GS, et al. The role of primary tumor resection in colorectal cancer patients with asymptomatic, synchronous, unresectable metastasis: a multicenter randomized controlled trial. Cancers (Basel) , 2020, 12 (8): 2306. doi: 10.3390/cancers12082306.
16. Wang Z, Liang L, Yu Y, et al. Primary tumour resection could improve the survival of unresectable metastatic colorectal cancer patients receiving bevacizumab-containing chemotherapy. Cell Physiol Biochem, 2016, 39(3): 1239-1246.
17. Yun JA, Huh JW, Park YA, et al. The role of palliative resection for asymptomatic primary tumor in patients with unresectable stage Ⅳ colorectal cancer. Dis Colon Rectum, 2014, 57(9): 1049-1058.
18. Faron M, Pignon JP, Malka D, et al. Is primary tumour resection associated with survival improvement in patients with colorectal cancer and unresectable synchronous metastases? A pooled analysis of individual data from four randomised trials. Eur J Cancer, 2015, 51(2): 166-176.
19. Huang Y, Ge K, Fu G, et al. Efficacy of primary tumor resection in metastatic colorectal cancer. Med Sci Monit, 2020, 26: e923501. doi: 10.12659/MSM.923501.
20. Ergun Y, Bal O, Dogan M, et al. Does primary tumor resection contribute to overall survival in unresectable synchronous metastatic colorectal cancer? J Res Med Sci, 2020, 25: 14. doi: 10.4103/jrms.JRMS_1056_18.
21. Shida D, Boku N, Tanabe T, et al. Primary tumor resection for stage Ⅳ colorectal cancer in the era of targeted chemotherapy. J Gastrointest Surg, 2019, 23(11): 2144-2150.
22. Ahmed S, Fields A, Pahwa P, et al. Surgical resection of primary tumor in asymptomatic or minimally symptomatic patients with stage Ⅳ colorectal cancer: a canadian province experience. Clin Colorectal Cancer, 2015, 14(4): e41-e47. doi: 10.1016/j.clcc.2015.05.008.
23. Cao G, Zhou W, Chen E, et al. A novel scoring system predicting survival benefits of palliative primary tumor resection for patients with unresectable metastatic colorectal cancer: a retrospective cohort study protocol. Medicine (Baltimore), 2019, 98(37): e17178. doi: 10.1097/MD.0000000000017178.
24. Tsang WY, Ziogas A, Lin BS, et al. Role of primary tumor resection among chemotherapy-treated patients with synchronous stage Ⅳ colorectal cancer: a survival analysis. J Gastrointest Surg, 2014, 18(3): 592-598.
25. Alawadi Z, Phatak UR, Hu CY, et al. Comparative effectiveness of primary tumor resection in patients with stage Ⅳ colon cancer. Cancer, 2017, 123(7): 1124-1133.
26. Yang Y, Lu Y, Jiang W, et al. Individualized prediction of survival benefit from primary tumor resection for patients with unresectable metastatic colorectal cancer. World J Surg Oncol, 2020, 18(1): 193. doi: 10.1186/s12957-020-01972-y.
27. Xu H, Xia Z, Jia X, et al. Primary tumor resection is associated with improved survival in stage Ⅳ colorectal cancer: an instrumental variable analysis. Sci Rep, 2015, 5: 16516. doi: 10.1038/srep16516.
28. Tarantino I, Warschkow R, Worni M, et al. Prognostic relevance of palliative primary tumor removal in 37 793 metastatic colorectal cancer patients: a population-based, propensity score-adjusted trend analysis. Ann Surg, 2015, 262(1): 112-120.
29. Gulack BC, Nussbaum DP, Keenan JE, et al. Surgical resection of the primary tumor in stage Ⅳ colorectal cancer without metastasectomy is associated with improved overall survival compared with chemotherapy/radiation therapy alone. Dis Colon Rectum, 2016, 59(4): 299-305.
30. Mehta HB, Vargas GM, Adhikari D, et al. Comparative effectiveness of chemotherapy vs resection of the primary tumour as the initial treatment in older patients with stage Ⅳ colorectal cancer. Colorectal Dis, 2017, 19(6): O210-O218. doi: 10.1111/codi.13659.
31. Maroney S, de Paz CC, Reeves ME, et al. Benefit of surgical resection of the primary tumor in patients undergoing chemotherapy for stage Ⅳ colorectal cancer with unresected metastasis. J Gastrointest Surg, 2018, 22(3): 460-466.
32. ’t Lam-Boer J, Van der Geest LG, Verhoef C, et al. Palliative resection of the primary tumor is associated with improved overall survival in incurable stage Ⅳ colorectal cancer: a nationwide population-based propensity-score adjusted study in the Netherlands. Int J Cancer, 2016, 139(9): 2082-2094.
33. Hosseinali Khani M, Påhlman L, Smedh K. Treatment strategies for patients with stage Ⅳ rectal cancer: a report from the Swedish Rectal Cancer Registry. Eur J Cancer, 2012, 48(11): 1616-1623.
34. Gresham G, Renouf DJ, Chan M, et al. Association between palliative resection of the primary tumor and overall survival in a population-based cohort of metastatic colorectal cancer patients. Ann Surg Oncol, 2014, 21(12): 3917-3923.
35. Ferrand F, Malka D, Bourredjem A, et al. Impact of primary tumour resection on survival of patients with colorectal cancer and synchronous metastases treated by chemotherapy: results from the multicenter, randomised trial Fédération Francophone de Cancérologie Digestive 9601. Eur J Cancer, 2013, 49(1): 90-97.
36. Ishihara S, Nishikawa T, Tanaka T, et al. Benefit of primary tumor resection in stage Ⅳ colorectal cancer with unresectable metastasis: a multicenter retrospective study using a propensity score analysis. Int J Colorectal Dis, 2015, 30(6): 807-812.
37. van Rooijen KL, Shi Q, Goey KKH, et al. Prognostic value of primary tumour resection in synchronous metastatic colorectal cancer: Individual patient data analysis of first-line randomised trials from the ARCAD database. Eur J Cancer, 2018, 91: 99-106.
38. Boselli C, Renzi C, Gemini A, et al. Surgery in asymptomatic patients with colorectal cancer and unresectable liver metastases: the authors’ experience. Onco Targets Ther, 2013, 6: 267-272.
39. Kim SK, Lee CH, Lee MR, et al. Multivariate analysis of the survival rate for treatment modalities in incurable stage Ⅳ colorectal cancer. J Korean Soc Coloproctol, 2012, 28(1): 35-41.
40. Yoon YS, Kim CW, Lim SB, et al. Palliative surgery in patients with unresectable colorectal liver metastases: a propensity score matching analysis. J Surg Oncol, 2014, 109(3): 239-244.
41. Matsumoto T, Hasegawa S, Matsumoto S, et al. Overcoming the challenges of primary tumor management in patients with metastatic colorectal cancer unresectable for cure and an asymptomatic primary tumor. Dis Colon Rectum, 2014, 57(6): 679-686.
42. Park JH, Kim TY, Lee KH, et al. The beneficial effect of palliative resection in metastatic colorectal cancer. Br J Cancer, 2013, 108(7): 1425-1431.
43. Kim MS, Chung M, Ahn JB, et al. Clinical significance of primary tumor resection in colorectal cancer patients with synchronous unresectable metastasis. J Surg Oncol, 2014, 110(2): 214-221.
44. Watanabe A, Yamazaki K, Kinugasa Y, et al. Influence of primary tumor resection on survival in asymptomatic patients with incurable stage Ⅳ colorectal cancer. Int J Clin Oncol, 2014, 19(6): 1037-1042.
45. Niitsu H, Hinoi T, Shimomura M, et al. Up-front systemic chemotherapy is a feasible option compared to primary tumor resection followed by chemotherapy for colorectal cancer with unresectable synchronous metastases. World J Surg Oncol, 2015, 13: 162. doi: 10.1186/s12957-015-0570-1.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Long-term survival of primary tumor resection versus chemotherapy alone for asymptomatic stage Ⅳ colorectal cancer patients with unresectable synchronous metastasis: a pooled-analysis and trial sequential analysis

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