Comparison of Laparoscopic Versus Open Radical Surgery for Colorectal Cancer in Stress Response: A Meta-Analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 MAOZi-han ,  ZHANGHong , CONGJin-chun , LINGYun-zhi , LIUDing-sheng , CUIMing-ming , CHENChun-sheng

Department of Colorectal Tumor Surgery, Shengjing Hospital of China Medical University, Shenyang 110004, Liaoning Province, China;

Corresponding author：

ZHANGHong, Email: haojiubujian1203@sina.cn

Keywords：

Laparoscopy; Open surgery; Colorectal cancer; Stress

DOI：

10.7507/1007-9424.20160276

Video：

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Objective To systematically evaluate the stress response of laparoscopic surgery (LS) and conventional open surgery (OS) in patients with colorectal cancer. Methods The literatures about the immune stress response of LS and OS for colorectal cancer were collected from PubMed, Springer, OVID, Cochrane library, CNKI, VIP Database, and Wanfang Database from May 2001 to September 2014. RevMan 5.3 software was used for data analysis. Results Fifteen randomized controlled trials including 881 patients were brought into this Meta analysis, of 881 patients, 424 patients were treated with LS and 457 patients were treated with OS. The results of Meta-analysis showed that:①At 24, 72, and 120 hours after surgery, the levels of interleukin (IL-6) in LS group were all lower than those of OS group at same time point[24 h (WMD=-27.78, 95% CI:-43.24--12.32, P < 0.01), 72 h (WMD=-13.23, 95% CI:-19.89--6.57, P < 0.01), 120 h (WMD=-16.51, 95% CI:-30.13--2.89, P=0.02)]. ②At 24, 72, and 120 hours after surgery, the levels of C reactive protein (CRP) in LS group were all lower than those of OS group at same time point[24 h (WMD=-31.11, 95% CI:-47.49--14.73, P < 0.01), 72 h (WMD=-29.81, 95% CI:-49.99--9.64, P < 0.01), 120 h (WMD=-32.03, 95% CI:-45.34--18.71, P < 0.01)]. ③There was no significant difference between the 2 groups in WBC level at 24 hours after surgery (WMD=-0.63, 95% CI:-1.80-0.54, P=0.29), but the WBC levels of LS group at 72 hours and 120 hours after surgery were lower than those of OS group[72 h (WMD=-0.21, 95% CI:-0.41--0.01, P=0.04), 120 h (WMD=-0.86, 95% CI:-1.66--0.06, P=0.03). ④There was no significant difference between the 2 groups in cortisol level at 24 hours and 72 hours after surgery[24 h (WMD=-60.19, 95% CI:-194.77-74.39, P=0.38), 72 h (WMD=-13.83, 95% CI:-43.94-16.28, P=0.37). ⑤There was no significant difference between the 2 groups in blood glucose level at 24 hours and 72 hours after surgery[24 h (WMD=-0.95, 95% CI:-2.74-0.84, P=0.30), 72 h (WMD=-0.69, 95% CI:-2.05-0.66, P=0.32)]. ⑥There was no significant difference between the 2 groups in insulin level (WMD=-0.52, 95% CI:-1.87-0.82, P=0.45) at 24 hours after surgery. ⑦There was no significant difference between the 2 groups in tumor necrosis factor (TNF) level at 24 hours after surgery (WMD=-4.18, 95% CI:-9.39-1.04, P=0.12). Conclusion Compared with open radical surgery, laparoscopic radical surgery for colorectal cancer causes less stress and less effect on the immune function, it also can reduce postoperative complications and can be propitious to faster body recovery.

Citation： MAO Zi-han, ZHANG Hong, CONG Jin-chun, LING Yun-zhi, LIU Ding-sheng, CUI Ming-ming, CHEN Chun-sheng. Comparison of Laparoscopic Versus Open Radical Surgery for Colorectal Cancer in Stress Response: A Meta-Analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2016, 23(9): 1073-1083. doi: 10.7507/1007-9424.20160276 Copy

1.	Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc, 1991, 1(3):144-150.
2.	Luo K, Li JS, Li LT, et al. Operative stress response and energy metabolism after laparoscopic cholecystectomy compared to open surgery. World J Gastroenterol, 2003, 9(4):847-850.
3.	Haque Z, Rahman M, Siddique MA, et al. Metabolic and stress responses of the body to trauma:produced by the laparoscopic and open cholecystectomy. Mymensingh Med J, 2004, 13(1):48-52.
4.	Nakamura T, Mitomi H, Ohtani Y, et al. Comparison of long-term outcome of laparoscopic and conventional surgery for advanced colon and rectosigmoid cancer. Hepatogastroenterology, 2006, 53(69):351-353.
5.	张淼, 张云, 鱼海峰, 等.腹腔镜与传统开腹结直肠癌根治手术疗效比较.中国现代普通外科进展, 2012, 15(5):410-411.
6.	Braga M, Frasson M, Vignali A, et al. Laparoscopic resection in rectal cancer patients:outcome and cost-benefit analysis. Dis Colon Rectum, 2007, 50(4):464-471.
7.	王玉林, 陈元, 汪翼, 等. 《中华儿科杂志》发表的治疗性研究文献质量评价.中华儿科杂志, 2013, 51(1):29-33.
8.	叶乾礼, 林建荣, 林世强.腹腔镜辅助结直肠癌根治术对机体应激反应的影响分析.中国医学工程, 2014, 22(9):68-69.
9.	周保军, 张国建, 段国强, 等.腹腔镜和开腹直肠癌保肛手术对机体应激反应的影响.世界华人消化杂志, 2007, 15(26):2856-2859.
10.	赵波, 吴卫, 徐艳松, 等.腹腔镜结直肠癌与开腹手术对应激相关因子的对比研究.结直肠肛门外科, 2013, 19(2):73-76.
11.	李炳辉, 张彩坤, 齐湘杰.腹腔镜手术对腹型肥胖直肠癌患者术后代谢影响的研究.中国临床实用医学, 2008, 2(6):29-30.
12.	陈一伟, 吴庆华, 夏兆立.腹腔镜与开腹结直肠癌根治术对机体应激反应的影响.临床合理用药杂志, 2013, 6(25):131.
13.	潘书鸿, 张从雨, 潘绪科, 等.腹腔镜与开腹结直肠癌手术对机体应激反应及细胞免疫功能影响的比较.中国现代普通外科进展, 2014, 17(5):408-411.
14.	陈欣, 吕振晔.腹腔镜与开腹直肠癌根治术对机体应激及内脏蛋白的影响.河北医科大学学报, 2012, 33(4):399-401.
15.	曹传培, 汪峰.腹腔镜与开腹直肠癌根治术对老年患者机体应激的影响.中国当代医药, 2014, 21(26):171-173.
16.	江秀丽, 王倩, 张建立, 等.腹腔镜与开腹直肠癌术后应激反应期ghrelin的动态变化及意义.医学研究生学报, 2013, 26(8):823-828.
17.	Wu FP, Hoekman K, Sietses C, et al, Systemic and peritoneal angiogenic response after laparoscopic or conventional colon resection in cancer patients:a prospective, randomized trial. Dis Colon Rectum, 2004, 47(10):1670-1674.
18.	Veenhof AA, Vlug MS, van der Pas MH, et al. Surgical stress response and postoperative immune function after laparoscopy or open surgery with fast track or standard perioperative care:a randomized trial. Ann Surg, 2012, 255(2):216-221.
19.	Delgado S, Lacy AM, Filella X, et al. Acute phase response in laparoscopic and open colectomy in colon cancer. Dis Colon Rectum, 2001, 44(5):638-646.
20.	Kvarnström A, Swartling T, Kurlberg G, et al. Pro-inflammatory cytokine release in rectal surgery:comparison between laparoscopic and open surgical techniques. Arch Immunol Ther Exp (Warsz), 2013, 61(5):407-411.
21.	Veenhof AA, Sietses C, von Blomberg BM, et al. The surgical stress response and postoperative immune function after laparoscopic or conventional total mesorectal excision in rectal cancer:a randomized trial. Int J Colorectal Dis, 2011, 26(1):53-59.
22.	Tsimogiannis KE, Tellis CC, Tselepis AD, et al. Toll-like receptors in the inflammatory response during open and laparoscopic colectomy for colorectal cancer. Surg Endosc, 2012, 26(2):330-336.
23.	Haga Y, Beppu T, DoiK, et al. Systemic inflammatory response syndrome and organ dysfunction following gastrointestinal surgery. Crit Care Med, 1997, 25(12):1994-2000.
24.	Cunliffe RN, Kamal M, Rose FR, et al. Expression of antimicrobial neutrophil defensins in epithelial cells of active inflammatory bowel disease mucosa. J Clin Pathol, 2002, 55(4):298-304.
25.	Lenz A, Franklin GA, Cheadle WG. Systemic inflammation after trauma. Injury, 2007, 38(12):1336-1345.
26.	Kehlet H. The surgical stress response:should it be prevented?. Can J Surg, 1991, 34(6):565-567.
27.	Tang CL, Eu KW, Tai BC, et al. Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancer. Br J Surg, 2001, 88(6):801-807.
28.	Wigmore SJ, MacMahon AJ, Sturgeon CM, et al. Acute-phase protein response, survival and tumour recurrence in patients with colorectal cancer. Br J Surg, 2001, 37(88):255-260.
29.	杨硕, 张建立.腹腔镜与开腹结直肠癌根治术对机体免疫系统影响的比较研究.腹腔镜外科杂志, 2008, 13(1):22-24.
30.	Allendorf JD, Bessler M, Horvath KD, et al. Increased tumor establishment and growth after open vs laparoscopic surgery in mice may be related to differences in postoperative T-cell function. Surg Endosc, 1999, 13(3):233-235.
31.	Lennard TW, Shenton BK, Borzotta A, et al. The influence of surgical operations on components of the human immune system. Br J Surg, 1985, 72(10):771-776.
32.	赵刚, 肖刚, 黄美雄, 等.腹腔镜结直肠癌根治对机体免疫状态的影响.中华胃肠外科杂志, 2005, 8(5):407-409.
33.	Wakefield CH, Carey PD, Foulds S, et al. Changes in major histocompatibility complex class Ⅱ expression in monocytes and T cells of patients developing infection after surgery. Br J Surg, 1993, 80(2):205-209.
34.	叶平江, 郭贵龙, 应晓江, 等.腹腔镜与开腹结直肠癌根治术对机体免疫系统影响的比较研究.中国内镜杂志, 2011, 17(5):478-480.
35.	周志涛, 李俊, 毛常青, 等.腹腔镜直肠癌根治术对患者免疫功能影响的研究.实用预防医学, 2011, 18(5):895-897.
36.	Jakeways MS, Mitchell V, Hashim IA, et al. Metabolic and inflammatory responses after open or laparoscopic cholecystectomy. Br J Surg, 1994, 81(1):127-131.
37.	Ordemann J, Jacobi CA, Schwenk W, et al. Cellular and humoral inflammatory response after laparoscopic and conventional colorectal resections. Surg Endosc, 2001, 15(6):600-608.
38.	Whelan RL, Franklin M, Holubar SD, et al. Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. Surg Endosc, 2003, 17(6):972-978.
39.	Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med, 1999, 340(6):448-454.
40.	Watt DG, Horgan PG, McMillan DC. Routine clinical markers of the magnitude of the systemic inflammatory response after elective operation:a systematic review. Surgery, 2015, 157(2):362-380.
41.	田玉科, 罗爱林, 金士翱.重度创伤后血清肿瘤坏死因子α及白细胞介素6水平变化与感染性并发症的关系.中华实验外科杂志, 1999, 16(1):38-39.
42.	Ogawa K, Hirai M, Katsube T, et al. Suppression of cellular immunity by surgical stress. Surgery, 2000, 127(3):329-336.
43.	Leung KL, Kwok SP, Lam SC, et al. Laparoscopic resection of rectosigmoid carcinoma:prospective randomised trial. Lancet, 2004, 363(9416):1187-1192.
44.	Nash GF. Randomized clinical trial comparing inflammatory and angiogenic response after open versus laparoscopic curative resection for colonic cancer. Br J Surg, 2011, 98(5):745-746.
45.	Heinrich PC, Castell JV, Andus T. Interleukin-6 and the acute phase response. Biochem J, 1990, 265(3):282-291.
46.	Tsamis D, Theodoropoulos G, Stamopoulos P, et al. Systemic inflammatory response after laparoscopic and conventional colectomy for cancer:a matched case-control study. Surg Endosc, 2012, 26(5):1436-1443.
47.	Wichmann MW, Hüttl TP, Winter H, et al. Immunological effects of laparoscopic vs open colorectal surgery:a prospective clinical study. Arch Surg, 2005, 140(7):692-697.
48.	Sammour T, Kahokehr A, Chan S, et al. The humoral response after laparoscopic versus open colorectal surgery:a meta-analysis. J Surg Res, 2010, 164(1):28-37.
49.	李豫江, 李志刚, 孙旭凌, 等.腹腔镜与开腹直肠癌根治术对机体C反应蛋白及细胞免疫影响的比较.临床和实验医学杂志, 2012, 11(13):1031-1033.
50.	Schwenk W, Jacobi C, Mansmann U, et al. Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial. Langenbecks Arch Surg, 2000, 385(1):2-9.
51.	Ramanathan ML, MacKay G, Platt J, et al. The impact of open versus laparoscopic resection for colon cancer on C-reactive protein concentrations as a predictor of postoperative infective complications. Ann Surg Oncol, 2015, 22(3):938-943.
52.	Liu C, Liu J, Zhang S. Laparoscopic versus conventional open surgery for immune function in patients with colorectal cancer. Int J Colorectal Dis, 2011, 26(11):1375-1385.

1. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc, 1991, 1(3):144-150.
2. Luo K, Li JS, Li LT, et al. Operative stress response and energy metabolism after laparoscopic cholecystectomy compared to open surgery. World J Gastroenterol, 2003, 9(4):847-850.
3. Haque Z, Rahman M, Siddique MA, et al. Metabolic and stress responses of the body to trauma:produced by the laparoscopic and open cholecystectomy. Mymensingh Med J, 2004, 13(1):48-52.
4. Nakamura T, Mitomi H, Ohtani Y, et al. Comparison of long-term outcome of laparoscopic and conventional surgery for advanced colon and rectosigmoid cancer. Hepatogastroenterology, 2006, 53(69):351-353.
5. 张淼, 张云, 鱼海峰, 等.腹腔镜与传统开腹结直肠癌根治手术疗效比较.中国现代普通外科进展, 2012, 15(5):410-411.
6. Braga M, Frasson M, Vignali A, et al. Laparoscopic resection in rectal cancer patients:outcome and cost-benefit analysis. Dis Colon Rectum, 2007, 50(4):464-471.
7. 王玉林, 陈元, 汪翼, 等. 《中华儿科杂志》发表的治疗性研究文献质量评价.中华儿科杂志, 2013, 51(1):29-33.
8. 叶乾礼, 林建荣, 林世强.腹腔镜辅助结直肠癌根治术对机体应激反应的影响分析.中国医学工程, 2014, 22(9):68-69.
9. 周保军, 张国建, 段国强, 等.腹腔镜和开腹直肠癌保肛手术对机体应激反应的影响.世界华人消化杂志, 2007, 15(26):2856-2859.
10. 赵波, 吴卫, 徐艳松, 等.腹腔镜结直肠癌与开腹手术对应激相关因子的对比研究.结直肠肛门外科, 2013, 19(2):73-76.
11. 李炳辉, 张彩坤, 齐湘杰.腹腔镜手术对腹型肥胖直肠癌患者术后代谢影响的研究.中国临床实用医学, 2008, 2(6):29-30.
12. 陈一伟, 吴庆华, 夏兆立.腹腔镜与开腹结直肠癌根治术对机体应激反应的影响.临床合理用药杂志, 2013, 6(25):131.
13. 潘书鸿, 张从雨, 潘绪科, 等.腹腔镜与开腹结直肠癌手术对机体应激反应及细胞免疫功能影响的比较.中国现代普通外科进展, 2014, 17(5):408-411.
14. 陈欣, 吕振晔.腹腔镜与开腹直肠癌根治术对机体应激及内脏蛋白的影响.河北医科大学学报, 2012, 33(4):399-401.
15. 曹传培, 汪峰.腹腔镜与开腹直肠癌根治术对老年患者机体应激的影响.中国当代医药, 2014, 21(26):171-173.
16. 江秀丽, 王倩, 张建立, 等.腹腔镜与开腹直肠癌术后应激反应期ghrelin的动态变化及意义.医学研究生学报, 2013, 26(8):823-828.
17. Wu FP, Hoekman K, Sietses C, et al, Systemic and peritoneal angiogenic response after laparoscopic or conventional colon resection in cancer patients:a prospective, randomized trial. Dis Colon Rectum, 2004, 47(10):1670-1674.
18. Veenhof AA, Vlug MS, van der Pas MH, et al. Surgical stress response and postoperative immune function after laparoscopy or open surgery with fast track or standard perioperative care:a randomized trial. Ann Surg, 2012, 255(2):216-221.
19. Delgado S, Lacy AM, Filella X, et al. Acute phase response in laparoscopic and open colectomy in colon cancer. Dis Colon Rectum, 2001, 44(5):638-646.
20. Kvarnström A, Swartling T, Kurlberg G, et al. Pro-inflammatory cytokine release in rectal surgery:comparison between laparoscopic and open surgical techniques. Arch Immunol Ther Exp (Warsz), 2013, 61(5):407-411.
21. Veenhof AA, Sietses C, von Blomberg BM, et al. The surgical stress response and postoperative immune function after laparoscopic or conventional total mesorectal excision in rectal cancer:a randomized trial. Int J Colorectal Dis, 2011, 26(1):53-59.
22. Tsimogiannis KE, Tellis CC, Tselepis AD, et al. Toll-like receptors in the inflammatory response during open and laparoscopic colectomy for colorectal cancer. Surg Endosc, 2012, 26(2):330-336.
23. Haga Y, Beppu T, DoiK, et al. Systemic inflammatory response syndrome and organ dysfunction following gastrointestinal surgery. Crit Care Med, 1997, 25(12):1994-2000.
24. Cunliffe RN, Kamal M, Rose FR, et al. Expression of antimicrobial neutrophil defensins in epithelial cells of active inflammatory bowel disease mucosa. J Clin Pathol, 2002, 55(4):298-304.
25. Lenz A, Franklin GA, Cheadle WG. Systemic inflammation after trauma. Injury, 2007, 38(12):1336-1345.
26. Kehlet H. The surgical stress response:should it be prevented?. Can J Surg, 1991, 34(6):565-567.
27. Tang CL, Eu KW, Tai BC, et al. Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancer. Br J Surg, 2001, 88(6):801-807.
28. Wigmore SJ, MacMahon AJ, Sturgeon CM, et al. Acute-phase protein response, survival and tumour recurrence in patients with colorectal cancer. Br J Surg, 2001, 37(88):255-260.
29. 杨硕, 张建立.腹腔镜与开腹结直肠癌根治术对机体免疫系统影响的比较研究.腹腔镜外科杂志, 2008, 13(1):22-24.
30. Allendorf JD, Bessler M, Horvath KD, et al. Increased tumor establishment and growth after open vs laparoscopic surgery in mice may be related to differences in postoperative T-cell function. Surg Endosc, 1999, 13(3):233-235.
31. Lennard TW, Shenton BK, Borzotta A, et al. The influence of surgical operations on components of the human immune system. Br J Surg, 1985, 72(10):771-776.
32. 赵刚, 肖刚, 黄美雄, 等.腹腔镜结直肠癌根治对机体免疫状态的影响.中华胃肠外科杂志, 2005, 8(5):407-409.
33. Wakefield CH, Carey PD, Foulds S, et al. Changes in major histocompatibility complex class Ⅱ expression in monocytes and T cells of patients developing infection after surgery. Br J Surg, 1993, 80(2):205-209.
34. 叶平江, 郭贵龙, 应晓江, 等.腹腔镜与开腹结直肠癌根治术对机体免疫系统影响的比较研究.中国内镜杂志, 2011, 17(5):478-480.
35. 周志涛, 李俊, 毛常青, 等.腹腔镜直肠癌根治术对患者免疫功能影响的研究.实用预防医学, 2011, 18(5):895-897.
36. Jakeways MS, Mitchell V, Hashim IA, et al. Metabolic and inflammatory responses after open or laparoscopic cholecystectomy. Br J Surg, 1994, 81(1):127-131.
37. Ordemann J, Jacobi CA, Schwenk W, et al. Cellular and humoral inflammatory response after laparoscopic and conventional colorectal resections. Surg Endosc, 2001, 15(6):600-608.
38. Whelan RL, Franklin M, Holubar SD, et al. Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. Surg Endosc, 2003, 17(6):972-978.
39. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med, 1999, 340(6):448-454.
40. Watt DG, Horgan PG, McMillan DC. Routine clinical markers of the magnitude of the systemic inflammatory response after elective operation:a systematic review. Surgery, 2015, 157(2):362-380.
41. 田玉科, 罗爱林, 金士翱.重度创伤后血清肿瘤坏死因子α及白细胞介素6水平变化与感染性并发症的关系.中华实验外科杂志, 1999, 16(1):38-39.
42. Ogawa K, Hirai M, Katsube T, et al. Suppression of cellular immunity by surgical stress. Surgery, 2000, 127(3):329-336.
43. Leung KL, Kwok SP, Lam SC, et al. Laparoscopic resection of rectosigmoid carcinoma:prospective randomised trial. Lancet, 2004, 363(9416):1187-1192.
44. Nash GF. Randomized clinical trial comparing inflammatory and angiogenic response after open versus laparoscopic curative resection for colonic cancer. Br J Surg, 2011, 98(5):745-746.
45. Heinrich PC, Castell JV, Andus T. Interleukin-6 and the acute phase response. Biochem J, 1990, 265(3):282-291.
46. Tsamis D, Theodoropoulos G, Stamopoulos P, et al. Systemic inflammatory response after laparoscopic and conventional colectomy for cancer:a matched case-control study. Surg Endosc, 2012, 26(5):1436-1443.
47. Wichmann MW, Hüttl TP, Winter H, et al. Immunological effects of laparoscopic vs open colorectal surgery:a prospective clinical study. Arch Surg, 2005, 140(7):692-697.
48. Sammour T, Kahokehr A, Chan S, et al. The humoral response after laparoscopic versus open colorectal surgery:a meta-analysis. J Surg Res, 2010, 164(1):28-37.
49. 李豫江, 李志刚, 孙旭凌, 等.腹腔镜与开腹直肠癌根治术对机体C反应蛋白及细胞免疫影响的比较.临床和实验医学杂志, 2012, 11(13):1031-1033.
50. Schwenk W, Jacobi C, Mansmann U, et al. Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial. Langenbecks Arch Surg, 2000, 385(1):2-9.
51. Ramanathan ML, MacKay G, Platt J, et al. The impact of open versus laparoscopic resection for colon cancer on C-reactive protein concentrations as a predictor of postoperative infective complications. Ann Surg Oncol, 2015, 22(3):938-943.
52. Liu C, Liu J, Zhang S. Laparoscopic versus conventional open surgery for immune function in patients with colorectal cancer. Int J Colorectal Dis, 2011, 26(11):1375-1385.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Comparison of Laparoscopic Versus Open Radical Surgery for Colorectal Cancer in Stress Response: A Meta-Analysis

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