微创化直肠癌保肛术患者围手术期的免疫学变化
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摘要
目的 研究微创化直肠癌全直肠系膜切除保肛术患者围手术期免疫学变化；比较经腹腔镜和开腹两种途径行直肠癌全直肠系膜切除保肛术对患者免疫功能的影响。
方法 45例行直肠癌全直肠系膜切除保肛术患者，分为开腹组(n=25)和腹腔镜组(n=20)，并选取30例同期健康献血者作为术前正常对照，于术前1天、术后第1天、术后第5天检测血清IL-2、IL-6、TNF_α值；术前1天和术后第5天检测全血CD_3~+CD_(56)~+T细胞和CD_3~-CD_(56)~+NK细胞的百分比，血清免疫球蛋白IgG、IgM、IgA值。IL-2、IL-6、TNF_α值的检测用酶联免疫吸附法(ELISA)，Ig的测定用免疫散射比浊法，CD_3~+CD_(56)~+T细胞和CD_3~-CD_(56)~+NK细胞用流式细胞仪进行检测。
结果 直肠癌患者CD_3~-CD_(56)~+NK细胞百分比(23.50±15.56)％，血清IL-6水平(62.86±160.21)pg／ml，IgA水平(2597.54±1492.93)mg/L，均高于正常对照组(p＜0.05)。开腹组术后第5天CD_3~-CD_(56)~+NK细胞和IgG明显下降(p＜0.05)，腹腔镜组术后第5天IgG明显下降(p＜0.05)，其余免疫学指标围手术期无明显变化(p＞0.05)。两组手术对CD_3~+CD_(56)~+T细胞、CD_3~-CD_(56)~+NK细胞、IL-2、IL-6、TNF_α和免疫球蛋白的影响差异无显著性。
结论直肠癌患者免疫功能受到一定程度的抑制;在国内外首次报道:开
腹和腹腔镜直肠癌全直肠系膜切除保肛术对患者机体免疫功能有一定影
响;腹腔镜和开腹直肠癌全直肠系膜切除保肛术对患者免疫学功能的影响
差异无显著性。
Immune response after total mesorectal excision & anal sphincter preservation for rectal cancer with minimal invasive surgery
AIM This study was designed to compare immune function after laparoscopic and open total mesorectal excision & anal sphincter preservation for rectal cancer, and to assess the immune response in patients undergoing total mesorectal excision for rectal cancer with minimal invasive surgery.
METHODS This study involved 45 patients undergoing laparoscopic(n=20) and open(n=25) total mesorectal excision & anal sphincter preservation for rectal cancer, and 30 healthy individuals for normal control. Interleukin-2(IL-2), Interleukin-6(IL-6), and tumor necrosis factor a (TNFa) were assayed preoperatively and on the 1st and 5th postoperative day. CD3+ CD56+ T lymphocyte count, CD3 CD56+ natural killer cell (NK) count and immunoglobulin (IgG/IgM/IgA) were assayed preoperatively and at 5 day postoperatively. The numbers of CD3+ CD56+ T lymphocyte and CD3- CD56+ NK cell were counted using flowcytometry. An enzyme-linked
immunosorbent assay was used for IL-2, IL-6 and TNF determination. Immunoglobulin was tested with Immage analyzer by immuno-scattering turbidimetry.
RESULTS The levels of CD3- CD56+ NK cell, IL-6 and IgA were demonstrated higher in patients with rectal cancer than those in healthy control. Significant decreases in NK and IgG were revealed within 5 day postoperatively in open group (p<0.05) . IgG was decreased within 5 day postoperatively in laparoscopic group (p<0.05 ) . The other parameters had no significant change (p>0.05) perioperatively. No significant difference of immune response between the open and laparoscopic groups was seen
CONCLUSION Patients with rectal cancer reveal immune depression, and exhibit significant perioperative immune disturbance with laparoscopic and open surgery. There is no difference in immune responses in patients having laparoscopic total mesorectal excision & anal sphincter preservation compared with those undergoing open surgery for rectal cancer.
方法 45例行直肠癌全直肠系膜切除保肛术患者，分为开腹组(n=25)和腹腔镜组(n=20)，并选取30例同期健康献血者作为术前正常对照，于术前1天、术后第1天、术后第5天检测血清IL-2、IL-6、TNF_α值；术前1天和术后第5天检测全血CD_3~+CD_(56)~+T细胞和CD_3~-CD_(56)~+NK细胞的百分比，血清免疫球蛋白IgG、IgM、IgA值。IL-2、IL-6、TNF_α值的检测用酶联免疫吸附法(ELISA)，Ig的测定用免疫散射比浊法，CD_3~+CD_(56)~+T细胞和CD_3~-CD_(56)~+NK细胞用流式细胞仪进行检测。
结果 直肠癌患者CD_3~-CD_(56)~+NK细胞百分比(23.50±15.56)％，血清IL-6水平(62.86±160.21)pg／ml，IgA水平(2597.54±1492.93)mg/L，均高于正常对照组(p＜0.05)。开腹组术后第5天CD_3~-CD_(56)~+NK细胞和IgG明显下降(p＜0.05)，腹腔镜组术后第5天IgG明显下降(p＜0.05)，其余免疫学指标围手术期无明显变化(p＞0.05)。两组手术对CD_3~+CD_(56)~+T细胞、CD_3~-CD_(56)~+NK细胞、IL-2、IL-6、TNF_α和免疫球蛋白的影响差异无显著性。
结论直肠癌患者免疫功能受到一定程度的抑制;在国内外首次报道:开
腹和腹腔镜直肠癌全直肠系膜切除保肛术对患者机体免疫功能有一定影
响;腹腔镜和开腹直肠癌全直肠系膜切除保肛术对患者免疫学功能的影响
差异无显著性。
Immune response after total mesorectal excision & anal sphincter preservation for rectal cancer with minimal invasive surgery
AIM This study was designed to compare immune function after laparoscopic and open total mesorectal excision & anal sphincter preservation for rectal cancer, and to assess the immune response in patients undergoing total mesorectal excision for rectal cancer with minimal invasive surgery.
METHODS This study involved 45 patients undergoing laparoscopic(n=20) and open(n=25) total mesorectal excision & anal sphincter preservation for rectal cancer, and 30 healthy individuals for normal control. Interleukin-2(IL-2), Interleukin-6(IL-6), and tumor necrosis factor a (TNFa) were assayed preoperatively and on the 1st and 5th postoperative day. CD3+ CD56+ T lymphocyte count, CD3 CD56+ natural killer cell (NK) count and immunoglobulin (IgG/IgM/IgA) were assayed preoperatively and at 5 day postoperatively. The numbers of CD3+ CD56+ T lymphocyte and CD3- CD56+ NK cell were counted using flowcytometry. An enzyme-linked
immunosorbent assay was used for IL-2, IL-6 and TNF determination. Immunoglobulin was tested with Immage analyzer by immuno-scattering turbidimetry.
RESULTS The levels of CD3- CD56+ NK cell, IL-6 and IgA were demonstrated higher in patients with rectal cancer than those in healthy control. Significant decreases in NK and IgG were revealed within 5 day postoperatively in open group (p<0.05) . IgG was decreased within 5 day postoperatively in laparoscopic group (p<0.05 ) . The other parameters had no significant change (p>0.05) perioperatively. No significant difference of immune response between the open and laparoscopic groups was seen
CONCLUSION Patients with rectal cancer reveal immune depression, and exhibit significant perioperative immune disturbance with laparoscopic and open surgery. There is no difference in immune responses in patients having laparoscopic total mesorectal excision & anal sphincter preservation compared with those undergoing open surgery for rectal cancer.
引文
1. Law WL, Chu KW. Impact of total mesorectal excision on the results of surgery of distal rectal cancer[J]. Br J Surg, 2001; 88(12): 1607-1612
2. Dahlberg M, Pahlman L, Bergstrom R, et al. Improved survival in patients with rectal cancer: a population-based register study[J]. Br J Surg, 1998; 85(4): 515-520
3. Dahlberg M, Glimelius B, Pahlman L. Changing strategy for rectal cancer is associated with improved outcome[J]. Br J Surg, 1999; 86(3): 379-384
4. Arenas RB, Fichera A, Mhoon D, et al. Total mesenteric excision in the surgical treatment of rectal cancer[J]. Arch Surg, 1998; 133(6): 608-612
5. Heald R J, Moran B J, Ryall RDH, et al. Rectal cancer: the Basingstoke experience of total mesorectal excision, 1978-1997[J]. Arch Surg, 1998; 133(8): 894-899
6. Hartley JE, Mehigan BJ, Qureshi AE, et al. Total mesorectal excision: assessment of the laparoscopic approach[J]. Dis Colon Rectum, 2001; 44(3): 315-321
7. Maxwell ACA, Robinson MH, Scholefield JH. Laparoscopic colorectal cancer surgery[J]. Am J Surg,2000; 179(6):500-7
8．周总光，李立，舒晔，等．腹腔镜 DST、低位／超低位／结-肛吻合术治疗低位直肠癌[J]．华西医科大学学报，2002；33(1)：5-7
9. Bellon JM, Manzano L, Larrad A, et al. Endocrine and immune response to injury after open and laparoscopic cholecystectomy[J]. Int Surg, 1998; 83(1): 24-7
10. Kristinansson M, Saraste L, Soop M, et al. Diminished interleukin-6 and C-reactive protein responses to laparoscopic versus open cholecystectomy[J]. Acta Anaesthesiol Scand, 1999; 43(2): 146-52
11. Karayiannakis AJ, Makri GG, Mantzioka A, et al. Systemic stress
response after laparoscopic or open cholecystectomy: a randomized trial[J]. Br J Surg, 1997; 84(4): 467-71
12. Nishiguchi K, Okuda J, Toyoda M, et al. Comparative evaluation of surgical of laparoscopic and open surgeries for colorectal carcinoma[J]. Dis Colon Rectum, 2001; 44(2):223-30
13. Kuntz C, Wunsch A, Bay F, et al. Prospective randomized study of stress and immune response after laparoscopic vs conventional colonic resection[J]. Surg Endosc, 1998; 12(7):963-7
14. Heald RJ, Karanjia ND. Results of radical surgery for rectal cancer[J]. World J Surg, 1992;16(5):848-857
15．周总光，李立，舒晔．微创外科结、直肠肿瘤规范化手术标准(草案)[J]．中国普外基础与临床杂志，2002；9(1)：51-52
16．张家骅，冉江华，张捷，等．结直肠癌围手术期T细胞亚群、肿瘤坏死因子-a和可溶性白细胞介素-2受体的表达[J]．中华普通外科杂志，1998：13(4)：207～209
17. Espi A, Arenas J, Granero EG, et al. Relationship of curative surgery on natural killer cell activity in colorectal cancer[J]. Dis Colon Rectum, 1996; 39(4): 429-434
18. Coca S, Piqueras JP, Martinez D, et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma[J]. Cancer, 1997;79(12):2320-2328
19. Nichols PH, Ramsden CW, Ward U, et al. Peri-operative modulation of cellular immunity in patients with colorectal cancer[J]. Clin Exp Immunol, 1993; 94(1):4-10
20. Kinoshita T, Ito H, Miki C. Serum interleukin-6 level reflects the tumor
proliferative activity in patients with colorectal carcinoma[J]. Cancer, 1999; 85(12): 2526-2531
21. Komoda H, Tanaka Y, Honda M, et al. Interleukin-6 levels in colorectal cancer tissues[J]. World J Surg, 1998;22(8):895-898
22. Heriot AG, Marriott JB, Cookson S, et al. Reduction in cytokine production in colorectal cancer patients: association with stage and reversal by resection[J]. Br J Cancer, 2000;82(5): 1009-1012
23. Lahm H, Schindel M, Frikart L, et al. Selective suppression of cytokines of patients with colorectal cancer[J]. Br J Cancer, 1998;78(8): 1018-1023
24. Walker CBJ, Bruce DM, Heys SD, et al. Minimal modulation of lymphocyte and natural killer cell subsets following minimal access surgery[J]. Am J Surg,1999;177(1):48-54
25. Braga M, Vignali A, Zuliani W, et al. Metabolic and functional results after.laparoscopic colorectal surgery: a randomized, controlled tri(?) [J]. Dis Colon Rectum,2002;45(8): 1070-1077
26. Schwenk W, Jacobi C, Mansmann U, et al. Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial[J]. Langenbecks Arch Surg,2000;385(1):2-9
27. Delgado S, Lacy AM, Filella X, et al. Acute phase response in laparoscopic and open colectomy in colon cancer: randomized study[J]. Dis Colon Rectum,2001 ;44(5):638-646
28. Leung KL, Lai PB, Ho RL, et al. Systemic cytokine response after laparoscopic-assisted resection of rectosigrnoid carcinoma: a prospective randomized trial[J]. Ann Surg,2000;231(4):506-511
29. Ordemann J, Jacobi CA, Schwenk W, et al. Cellular and humoral
inflammatory response after laparoscopic and conventional colorectal resections[J]. Surg Endosc, 2001; 15(6):600-608
30. Mehigan BJ, Hartley JE, Drew PJ, et al. Changes in T cell subsets, interleukin-6 and C-reactive protein after laparoscopic and open colorectal resection for malignancy[J]. Surg Endosc, 2001; 15(11):1289-1293
31. Sandoval BA, Robinson AV, Sulaiman TT, et al. Open versus laparoscopic surgery: a comparison of natural antitumoral cellular immunity in a small animal model[J]. Am Surg, 1996;62(8):625-630
32. 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[J]. Br J Surg,2001 ;88(6):801-807
33. Fukushima R, Kawamura YJ, Saito H, et al. Interleukin-6 and stress hormone responses after uncoplicated gasless laparoscopic-assisted and open sigmoid colectomy[J]. Dis Colon Rectum, 1996;39(10s) :s29-s34
34. Jacobi CA, Wenger F, Sabat R, et al. The impact of laparoscopy with carbon dioxide versus helium on immunologic function and tumor growth in a rat model[J]. Dis Surg, 1998; 15(2): 110-116
35. Chekan EG, Nataraj C, Clary EM, et al. Intraperitoneal immunity and pneumoperitoneum [J]. Surg Endosc, 1999; 13 (11): 1135-1138
36. Kamei H, Yoshida S, Yamasaki K, et al. Carbon dioxide pneumoperitoneum reduces levels of TNF- a mRNA in the brain, liver, and peritoneum in mice[J]. Surg Endosc,2001; 15(6):609-613
37. Chapman AE, Levitt MD, Hewett P, et al. Laparoscopic-assisted resection of colorectal malignancies: a systematic review[J]. Ann.Surg,
2001; 234(5): 590-606
38. Feliciotti F, Paganini AM, Guerrieri M, et al. Results of laparoscopic vs open resections for colon cancer in patients with a minimum follow-up of 3 years[J]. Surg Endosc,2002; 16(8): 1158-1161
39. Hong D, Tabet J, Anvari M. Laparoscopic vs open resection for colorectal adenocarcinoma[J]. Dis Colon Rectum,2001 ;44(1): 10-18
40. Lezoche E, Feliciotti F, Paganini AM, et al. Laparoscopic vs open hemicolectomy for colon cancer[J]. Surg Endosc,2002; 16(4):596-602
41. Paolucci V, Schaeff B, Schneider M, et al. Tumor seeding following laparoscopy: international survey[J]. World J Surg,2001 ;25(3):387
42. Wu JS, Brasfield EB, Guo LW, et al. Implantation of colon cancer at trocar sites is increased by low pressure pneumoperitoneum[J]. Surgery, 1997; 122(1):1-7
43. Lee SW, Gleason N, Blanco I, et al. Higher colon cancer turnor proliferative index and lower tumor cell death rate in mice undergoing laparotomy versus insuffiation[J]. Surg Endosc,2002; 16(1):36-39
44. Tomita H, Marcello PW, Milsom JW, et al. CO_2 pneumoperitoneum does not enhance tumor growth and metastasis: study of a rat cecal wall inoculation model[J]. Dis Colon Rectum,2001 ;44(9): 1297-1301
45. Jacobi CA, Wenger FA, Ordemann J, et al. Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumor growth and port site metastasis[J]. Br J Surg, 1998;85(10): 1419-1422
46. Jacobi CA, Ordemann J, Bohm B, et al. Inhibition of peritoneal tumor cell growth and implantation in laparoscopic surgery in a rat model[J]. Am J Surg,1997; 174(3):359-363
47. Moreno EF, Nelson H, Carugno F, et al. Effects of laparoscopy on tumor growth[J]. Surg Laparosc Endosc Percutan Tech,2000; 10(5):296-301
48. Ridgway PF, Smith A, Ziprin P, et al. Pneumoperitoneum augmented tumor invasiveness is abolished by matrix metalloproteinase blockade[J]. Surg Endosc,2002; 16(3):533-536
49. Ishida H, Murata N, Yokoyama M, et al. The influence of different insufflation pressures during carbon dioxide pneumoperitoneum on the development of pulmonary metastasis in a mouse model[J]. Surg Endosc, 2000; 14(6): 578-581
50. Gutt CN, Kim ZG, Schmandra T, et al. Carbon dioxide pneumoperitoneum is associated with increased liver metastases in a rat model[J]. Surgery,2000; 127(5):566-570
51. Pross M, Lippert H, Mantke R, et al. A proteinase inhibitor decreases tumor growth in a laparoscopic rat model[J]. Surg Endosc, 2001; 15(8):882-885
2. Dahlberg M, Pahlman L, Bergstrom R, et al. Improved survival in patients with rectal cancer: a population-based register study[J]. Br J Surg, 1998; 85(4): 515-520
3. Dahlberg M, Glimelius B, Pahlman L. Changing strategy for rectal cancer is associated with improved outcome[J]. Br J Surg, 1999; 86(3): 379-384
4. Arenas RB, Fichera A, Mhoon D, et al. Total mesenteric excision in the surgical treatment of rectal cancer[J]. Arch Surg, 1998; 133(6): 608-612
5. Heald R J, Moran B J, Ryall RDH, et al. Rectal cancer: the Basingstoke experience of total mesorectal excision, 1978-1997[J]. Arch Surg, 1998; 133(8): 894-899
6. Hartley JE, Mehigan BJ, Qureshi AE, et al. Total mesorectal excision: assessment of the laparoscopic approach[J]. Dis Colon Rectum, 2001; 44(3): 315-321
7. Maxwell ACA, Robinson MH, Scholefield JH. Laparoscopic colorectal cancer surgery[J]. Am J Surg,2000; 179(6):500-7
8．周总光，李立，舒晔，等．腹腔镜 DST、低位／超低位／结-肛吻合术治疗低位直肠癌[J]．华西医科大学学报，2002；33(1)：5-7
9. Bellon JM, Manzano L, Larrad A, et al. Endocrine and immune response to injury after open and laparoscopic cholecystectomy[J]. Int Surg, 1998; 83(1): 24-7
10. Kristinansson M, Saraste L, Soop M, et al. Diminished interleukin-6 and C-reactive protein responses to laparoscopic versus open cholecystectomy[J]. Acta Anaesthesiol Scand, 1999; 43(2): 146-52
11. Karayiannakis AJ, Makri GG, Mantzioka A, et al. Systemic stress
response after laparoscopic or open cholecystectomy: a randomized trial[J]. Br J Surg, 1997; 84(4): 467-71
12. Nishiguchi K, Okuda J, Toyoda M, et al. Comparative evaluation of surgical of laparoscopic and open surgeries for colorectal carcinoma[J]. Dis Colon Rectum, 2001; 44(2):223-30
13. Kuntz C, Wunsch A, Bay F, et al. Prospective randomized study of stress and immune response after laparoscopic vs conventional colonic resection[J]. Surg Endosc, 1998; 12(7):963-7
14. Heald RJ, Karanjia ND. Results of radical surgery for rectal cancer[J]. World J Surg, 1992;16(5):848-857
15．周总光，李立，舒晔．微创外科结、直肠肿瘤规范化手术标准(草案)[J]．中国普外基础与临床杂志，2002；9(1)：51-52
16．张家骅，冉江华，张捷，等．结直肠癌围手术期T细胞亚群、肿瘤坏死因子-a和可溶性白细胞介素-2受体的表达[J]．中华普通外科杂志，1998：13(4)：207～209
17. Espi A, Arenas J, Granero EG, et al. Relationship of curative surgery on natural killer cell activity in colorectal cancer[J]. Dis Colon Rectum, 1996; 39(4): 429-434
18. Coca S, Piqueras JP, Martinez D, et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma[J]. Cancer, 1997;79(12):2320-2328
19. Nichols PH, Ramsden CW, Ward U, et al. Peri-operative modulation of cellular immunity in patients with colorectal cancer[J]. Clin Exp Immunol, 1993; 94(1):4-10
20. Kinoshita T, Ito H, Miki C. Serum interleukin-6 level reflects the tumor
proliferative activity in patients with colorectal carcinoma[J]. Cancer, 1999; 85(12): 2526-2531
21. Komoda H, Tanaka Y, Honda M, et al. Interleukin-6 levels in colorectal cancer tissues[J]. World J Surg, 1998;22(8):895-898
22. Heriot AG, Marriott JB, Cookson S, et al. Reduction in cytokine production in colorectal cancer patients: association with stage and reversal by resection[J]. Br J Cancer, 2000;82(5): 1009-1012
23. Lahm H, Schindel M, Frikart L, et al. Selective suppression of cytokines of patients with colorectal cancer[J]. Br J Cancer, 1998;78(8): 1018-1023
24. Walker CBJ, Bruce DM, Heys SD, et al. Minimal modulation of lymphocyte and natural killer cell subsets following minimal access surgery[J]. Am J Surg,1999;177(1):48-54
25. Braga M, Vignali A, Zuliani W, et al. Metabolic and functional results after.laparoscopic colorectal surgery: a randomized, controlled tri(?) [J]. Dis Colon Rectum,2002;45(8): 1070-1077
26. Schwenk W, Jacobi C, Mansmann U, et al. Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial[J]. Langenbecks Arch Surg,2000;385(1):2-9
27. Delgado S, Lacy AM, Filella X, et al. Acute phase response in laparoscopic and open colectomy in colon cancer: randomized study[J]. Dis Colon Rectum,2001 ;44(5):638-646
28. Leung KL, Lai PB, Ho RL, et al. Systemic cytokine response after laparoscopic-assisted resection of rectosigrnoid carcinoma: a prospective randomized trial[J]. Ann Surg,2000;231(4):506-511
29. Ordemann J, Jacobi CA, Schwenk W, et al. Cellular and humoral
inflammatory response after laparoscopic and conventional colorectal resections[J]. Surg Endosc, 2001; 15(6):600-608
30. Mehigan BJ, Hartley JE, Drew PJ, et al. Changes in T cell subsets, interleukin-6 and C-reactive protein after laparoscopic and open colorectal resection for malignancy[J]. Surg Endosc, 2001; 15(11):1289-1293
31. Sandoval BA, Robinson AV, Sulaiman TT, et al. Open versus laparoscopic surgery: a comparison of natural antitumoral cellular immunity in a small animal model[J]. Am Surg, 1996;62(8):625-630
32. 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[J]. Br J Surg,2001 ;88(6):801-807
33. Fukushima R, Kawamura YJ, Saito H, et al. Interleukin-6 and stress hormone responses after uncoplicated gasless laparoscopic-assisted and open sigmoid colectomy[J]. Dis Colon Rectum, 1996;39(10s) :s29-s34
34. Jacobi CA, Wenger F, Sabat R, et al. The impact of laparoscopy with carbon dioxide versus helium on immunologic function and tumor growth in a rat model[J]. Dis Surg, 1998; 15(2): 110-116
35. Chekan EG, Nataraj C, Clary EM, et al. Intraperitoneal immunity and pneumoperitoneum [J]. Surg Endosc, 1999; 13 (11): 1135-1138
36. Kamei H, Yoshida S, Yamasaki K, et al. Carbon dioxide pneumoperitoneum reduces levels of TNF- a mRNA in the brain, liver, and peritoneum in mice[J]. Surg Endosc,2001; 15(6):609-613
37. Chapman AE, Levitt MD, Hewett P, et al. Laparoscopic-assisted resection of colorectal malignancies: a systematic review[J]. Ann.Surg,
2001; 234(5): 590-606
38. Feliciotti F, Paganini AM, Guerrieri M, et al. Results of laparoscopic vs open resections for colon cancer in patients with a minimum follow-up of 3 years[J]. Surg Endosc,2002; 16(8): 1158-1161
39. Hong D, Tabet J, Anvari M. Laparoscopic vs open resection for colorectal adenocarcinoma[J]. Dis Colon Rectum,2001 ;44(1): 10-18
40. Lezoche E, Feliciotti F, Paganini AM, et al. Laparoscopic vs open hemicolectomy for colon cancer[J]. Surg Endosc,2002; 16(4):596-602
41. Paolucci V, Schaeff B, Schneider M, et al. Tumor seeding following laparoscopy: international survey[J]. World J Surg,2001 ;25(3):387
42. Wu JS, Brasfield EB, Guo LW, et al. Implantation of colon cancer at trocar sites is increased by low pressure pneumoperitoneum[J]. Surgery, 1997; 122(1):1-7
43. Lee SW, Gleason N, Blanco I, et al. Higher colon cancer turnor proliferative index and lower tumor cell death rate in mice undergoing laparotomy versus insuffiation[J]. Surg Endosc,2002; 16(1):36-39
44. Tomita H, Marcello PW, Milsom JW, et al. CO_2 pneumoperitoneum does not enhance tumor growth and metastasis: study of a rat cecal wall inoculation model[J]. Dis Colon Rectum,2001 ;44(9): 1297-1301
45. Jacobi CA, Wenger FA, Ordemann J, et al. Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumor growth and port site metastasis[J]. Br J Surg, 1998;85(10): 1419-1422
46. Jacobi CA, Ordemann J, Bohm B, et al. Inhibition of peritoneal tumor cell growth and implantation in laparoscopic surgery in a rat model[J]. Am J Surg,1997; 174(3):359-363
47. Moreno EF, Nelson H, Carugno F, et al. Effects of laparoscopy on tumor growth[J]. Surg Laparosc Endosc Percutan Tech,2000; 10(5):296-301
48. Ridgway PF, Smith A, Ziprin P, et al. Pneumoperitoneum augmented tumor invasiveness is abolished by matrix metalloproteinase blockade[J]. Surg Endosc,2002; 16(3):533-536
49. Ishida H, Murata N, Yokoyama M, et al. The influence of different insufflation pressures during carbon dioxide pneumoperitoneum on the development of pulmonary metastasis in a mouse model[J]. Surg Endosc, 2000; 14(6): 578-581
50. Gutt CN, Kim ZG, Schmandra T, et al. Carbon dioxide pneumoperitoneum is associated with increased liver metastases in a rat model[J]. Surgery,2000; 127(5):566-570
51. Pross M, Lippert H, Mantke R, et al. A proteinase inhibitor decreases tumor growth in a laparoscopic rat model[J]. Surg Endosc, 2001; 15(8):882-885