Skip to main content
Top
Published in: Surgical Endoscopy 10/2004

01-10-2004 | Review

The net immunologic advantage of laparoscopic surgery

Authors: Y. W. Novitsky, D. E. M. Litwin, M. P. Callery

Published in: Surgical Endoscopy | Issue 10/2004

Login to get access

Abstract

The trauma of surgery evokes a variety of physiologic and immunologic alterations that should contribute to host defense. However, an exaggerated response to injury may result in immunosuppression and lead to significant postoperative morbidity and mortality. Laparoscopic surgery may result in less induced surgical trauma than conventional open surgery. Decreased postoperative pain and speedy functional recovery of laparoscopic patients may be attributable to the reduced inflammatory response and minimal immunosuppression. Inflammation, an early protective homeostatic immune response to injury, is characterized by the production of proinflammatory cytokines and by activation of cellular and humoral immune mechanisms. Postoperative levels of the inflammatory cytokines have been consistently lower after laparoscopic procedures, indicating a smaller degree of surgical insult and acute inflammatory reaction. Surgical stress derails the functions of both polymorphonuclear and mononuclear cells, which may lead to an increased risk of postoperative infection. Comparative studies of cellular immunity after laparoscopic and conventional surgery demonstrate immunologic advantage conferred by laparoscopy. Exaggerated activation of peritoneal immunity may lead to a relative local immunosuppression, resulting in ineffective intraperitoneal bacterial clearance and serious postoperative infections. Functions of the peritoneal macrophages are better preserved when laparotomy is avoided. Decreased perioperative stress may be particularly important for oncologic patients. Laparoscopic approaches may result in diminished perioperative tumor dissemination and better cancer outcomes. Although laparoscopy is “minimally invasive,” systemic immune responses still are undeniably activated. However, laparoscopic surgery appears to induce a smaller injury, resulting in proportionally decreased immunologic changes. In addition to improved cosmesis and faster functional recovery, a patient undergoing laparoscopic surgery may benefit most from a net immunologic advantage.
Literature
1.
go back to reference Allendorf, JDF, Bessler, M, Kayton, ML, Oesterling, SD, Treat, MR, Nowygrod, R, Whelan, RL 1995Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine modelArch Surg130649653PubMed Allendorf, JDF, Bessler, M, Kayton, ML, Oesterling, SD, Treat, MR, Nowygrod, R, Whelan, RL 1995Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine modelArch Surg130649653PubMed
2.
go back to reference Allendorf, JD, Bessler, M, Whelan, RL, Trokel, M, Laird, DA, Terry, MB, Treat, MR 1996Better preservation of immune function after laparoscopic-assisted versus open bowel resection in a murine modelDis Colon Rectum39S67S72PubMed Allendorf, JD, Bessler, M, Whelan, RL, Trokel, M, Laird, DA, Terry, MB, Treat, MR 1996Better preservation of immune function after laparoscopic-assisted versus open bowel resection in a murine modelDis Colon Rectum39S67S72PubMed
3.
4.
go back to reference Baigrie, RJ, Lamont, PM, Kwiatkowski, D, Dallman, MJ, Morris, PJ 1992Systemic cytokine response after major surgeryBr J Surg79757760PubMed Baigrie, RJ, Lamont, PM, Kwiatkowski, D, Dallman, MJ, Morris, PJ 1992Systemic cytokine response after major surgeryBr J Surg79757760PubMed
5.
go back to reference Balague, C, Targarona, EM, Pujol, M, Filella, X, Espert, JJ, Trias, M 1999Peritoneal response to a septic challenge: comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall-lift laparoscopySurg Endosc13792796CrossRefPubMed Balague, C, Targarona, EM, Pujol, M, Filella, X, Espert, JJ, Trias, M 1999Peritoneal response to a septic challenge: comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall-lift laparoscopySurg Endosc13792796CrossRefPubMed
7.
go back to reference Biffl, WL, Moore, EE, Moore, FA, Peterson, VM 1996Interleukin-6 in the injured patient: marker of injury or mediator of inflammation?Ann Surg224647664CrossRefPubMed Biffl, WL, Moore, EE, Moore, FA, Peterson, VM 1996Interleukin-6 in the injured patient: marker of injury or mediator of inflammation?Ann Surg224647664CrossRefPubMed
8.
go back to reference Bolufer, JM, Delgado, F, Blanes, F, Martinez-Abad, M, Canos, JI, Martin, J, Oliver, MJ 1995Injury in laparoscopic surgerySurg Laparosc Endosc5318323PubMed Bolufer, JM, Delgado, F, Blanes, F, Martinez-Abad, M, Canos, JI, Martin, J, Oliver, MJ 1995Injury in laparoscopic surgerySurg Laparosc Endosc5318323PubMed
9.
go back to reference Brune, IB, Wilke, W, Hensler, T, Holzmann, B, Siewert, JR 1999Downregulation of T-helper type 1 immune response and altered proinflammatory and antiinflammatory T-cell cytokine balance following conventional but not laparoscopic surgeryAm J Surg1775560CrossRefPubMed Brune, IB, Wilke, W, Hensler, T, Holzmann, B, Siewert, JR 1999Downregulation of T-helper type 1 immune response and altered proinflammatory and antiinflammatory T-cell cytokine balance following conventional but not laparoscopic surgeryAm J Surg1775560CrossRefPubMed
10.
go back to reference Carey, PD, Wakefield, CH, Thayeb, A, Monson, JR, Darzi, A, Guillou, PJ 1994Effects of minimally invasive surgery on hypochlorous acid production by neutrophilsBr J Surg81557560PubMed Carey, PD, Wakefield, CH, Thayeb, A, Monson, JR, Darzi, A, Guillou, PJ 1994Effects of minimally invasive surgery on hypochlorous acid production by neutrophilsBr J Surg81557560PubMed
11.
go back to reference Carter, JJ, Whelan, RL 2001The immunologic consequences of laparoscopy in oncologySurg Oncol Clin North Am10655677 Carter, JJ, Whelan, RL 2001The immunologic consequences of laparoscopy in oncologySurg Oncol Clin North Am10655677
12.
go back to reference Cava, A, Roman, J, Gonzalez, QA, Martin, F, Aramburo, P 1990Subcutaneous metastasis following laparoscopy in gastric adenocarcinomaEur J Surg Oncol166376PubMed Cava, A, Roman, J, Gonzalez, QA, Martin, F, Aramburo, P 1990Subcutaneous metastasis following laparoscopy in gastric adenocarcinomaEur J Surg Oncol166376PubMed
13.
go back to reference Chapman, AE, Levitt, MD, Hewett, P, Woods, R, Sheiner, H, Madden, GJ 2001Laparoscopic-assisted resection of colorectal malignancies: a systematic reviewAnn Surg234590606CrossRefPubMed Chapman, AE, Levitt, MD, Hewett, P, Woods, R, Sheiner, H, Madden, GJ 2001Laparoscopic-assisted resection of colorectal malignancies: a systematic reviewAnn Surg234590606CrossRefPubMed
14.
go back to reference Cheadle, WG, Hershman, MJ, Wellhausen, SR, Polk, HC,Jr 1991HLA-DR antigen expression on peripheral blood monocytes correlates with surgical infectionAm J Surg161639645CrossRefPubMed Cheadle, WG, Hershman, MJ, Wellhausen, SR, Polk, HC,Jr 1991HLA-DR antigen expression on peripheral blood monocytes correlates with surgical infectionAm J Surg161639645CrossRefPubMed
15.
go back to reference Chekan, EG, Nataraj, C, Clary, EM, Hayward, TZ, Brody, FJ, Stamat, JC, Fina, MC, Eubanks, WS, Westcott, CJ 1999Intraperitoneal immunity and pneumoperitoneumSurg Endosc1311351138CrossRefPubMed Chekan, EG, Nataraj, C, Clary, EM, Hayward, TZ, Brody, FJ, Stamat, JC, Fina, MC, Eubanks, WS, Westcott, CJ 1999Intraperitoneal immunity and pneumoperitoneumSurg Endosc1311351138CrossRefPubMed
16.
go back to reference Cho, JM, LaPorta, AJ, Clark, JR, Schofield, MJ, Hammond, SL, Mallory, PL 1994Response of serum cytokines in patients undergoing laparoscopic cholecystectomySurg Endosc813801384CrossRefPubMed Cho, JM, LaPorta, AJ, Clark, JR, Schofield, MJ, Hammond, SL, Mallory, PL 1994Response of serum cytokines in patients undergoing laparoscopic cholecystectomySurg Endosc813801384CrossRefPubMed
17.
go back to reference Clair, DG, Lautz, DB, Brooks, DC 1993Rapid development of umbilical metastases after laparoscopic cholecystectomy for unsuspected gallbladder carcinomaSurgery113355358PubMed Clair, DG, Lautz, DB, Brooks, DC 1993Rapid development of umbilical metastases after laparoscopic cholecystectomy for unsuspected gallbladder carcinomaSurgery113355358PubMed
18.
go back to reference Collet, D, Vitale, GC, Reynolds, M, Klar, E, Cheadle, WG 1995Peritoneal host defenses are less impaired by laparoscopy than by open operationSurg Endosc910591064PubMed Collet, D, Vitale, GC, Reynolds, M, Klar, E, Cheadle, WG 1995Peritoneal host defenses are less impaired by laparoscopy than by open operationSurg Endosc910591064PubMed
19.
go back to reference DaCosta, ML, Redmond, HP, Finnegan, N, Flynn, M, Bouchie-Hayes, D 1998Laparotomy and laparoscopy differentially accelerate experimental flank tumour growthBr J Surg8514391442CrossRefPubMed DaCosta, ML, Redmond, HP, Finnegan, N, Flynn, M, Bouchie-Hayes, D 1998Laparotomy and laparoscopy differentially accelerate experimental flank tumour growthBr J Surg8514391442CrossRefPubMed
20.
21.
go back to reference Decker, D, Schondorf, M, Bidlingmaier, F, Hirner, A, Ruecker, AA 1996Surgical stress induces a shift in the type-1/type-2 T-helper cell balance, suggesting downregulation of cell-mediated and upregulation of antibody-mediated immunity commensurate to the traumaSurgery119316325PubMed Decker, D, Schondorf, M, Bidlingmaier, F, Hirner, A, Ruecker, AA 1996Surgical stress induces a shift in the type-1/type-2 T-helper cell balance, suggesting downregulation of cell-mediated and upregulation of antibody-mediated immunity commensurate to the traumaSurgery119316325PubMed
22.
go back to reference Delgado, S, Lacy, AM, Filella, X, Castells, A, Garcia-Valdecasas, JC, Pique, JM, Momblan, D, Visa, J 2001Acute-phase response in laparoscopic and conventional colectomy in colon cancer: a randomized studyDis Colon Rectum44638646PubMed Delgado, S, Lacy, AM, Filella, X, Castells, A, Garcia-Valdecasas, JC, Pique, JM, Momblan, D, Visa, J 2001Acute-phase response in laparoscopic and conventional colectomy in colon cancer: a randomized studyDis Colon Rectum44638646PubMed
23.
go back to reference Drouard, F, Delamarre, J, Capron, J 1991Cutaneous seeding of gallbladder cancer after laparoscopic cholecystectomyN Engl J Med3251316 Drouard, F, Delamarre, J, Capron, J 1991Cutaneous seeding of gallbladder cancer after laparoscopic cholecystectomyN Engl J Med3251316
24.
go back to reference Eggermont, AM, Steller, EP, Marquet, RL, Jeekel, J, Sugarbaker, PH 1988Local regional promotion of tumor growth after abdominal surgery is dominant over immunotherapy with interleukin-2 and lymphokine activated killer cellsCancer Detect Prev12421429PubMed Eggermont, AM, Steller, EP, Marquet, RL, Jeekel, J, Sugarbaker, PH 1988Local regional promotion of tumor growth after abdominal surgery is dominant over immunotherapy with interleukin-2 and lymphokine activated killer cellsCancer Detect Prev12421429PubMed
25.
go back to reference Franklin, ME, Kazantsev, B, Abrego, D, Diaz, EJ, Balli, J, Glass, L 2000Laparoscopic surgery for stage III colon cancer: long-term follow upSurg Endosc14612616CrossRefPubMed Franklin, ME, Kazantsev, B, Abrego, D, Diaz, EJ, Balli, J, Glass, L 2000Laparoscopic surgery for stage III colon cancer: long-term follow upSurg Endosc14612616CrossRefPubMed
26.
go back to reference Fusco, MA, Paluzi, MW 1993Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon: report of a caseDis Colon Rectum356858861 Fusco, MA, Paluzi, MW 1993Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon: report of a caseDis Colon Rectum356858861
27.
go back to reference Gitzelmann, CA, Mendoza-Sagaon, M, Talamini, MA, Ahmal, SA, Pegoli, W, Paidas, CN 1999Cell-mediated immune response is better preserved by laparoscopy than laparotomySurgery1266571 Gitzelmann, CA, Mendoza-Sagaon, M, Talamini, MA, Ahmal, SA, Pegoli, W, Paidas, CN 1999Cell-mediated immune response is better preserved by laparoscopy than laparotomySurgery1266571
28.
go back to reference Glaser, F, Sannwald, GA, Buhr, HJ, Kuntz, C, Mayer, H, Klee, F, Herfarth, C 1995General stress response to conventional and laparoscopic cholecystectomyAnn Surg221372380PubMed Glaser, F, Sannwald, GA, Buhr, HJ, Kuntz, C, Mayer, H, Klee, F, Herfarth, C 1995General stress response to conventional and laparoscopic cholecystectomyAnn Surg221372380PubMed
29.
go back to reference Goshima, H, Saji, S, Furuta, T, Taneumura, H, Takao, H, Kida, H, Takahashi, H 1989Experimental study on preventive effects of lung metastases using LAK cells induced from various lymphocytes: special references to enhancement of lung metastasis after laparotomy stressJpn J Surg Soc9012451250 Goshima, H, Saji, S, Furuta, T, Taneumura, H, Takao, H, Kida, H, Takahashi, H 1989Experimental study on preventive effects of lung metastases using LAK cells induced from various lymphocytes: special references to enhancement of lung metastasis after laparotomy stressJpn J Surg Soc9012451250
30.
go back to reference Hackam, DJ, Rotstein, OD 1998Host response to laparoscopic surgery: mechanisms and clinical correlatesCan J Surg41103110 Hackam, DJ, Rotstein, OD 1998Host response to laparoscopic surgery: mechanisms and clinical correlatesCan J Surg41103110
31.
go back to reference Halevy, A, Lin, G, Gold-Deutsch, R, Lavi, R, Negri, M, Evans, S, Cotariu, D, Sackier, JM 1995Comparison of serum C-reactive protein concentration for laparoscopic versus open cholecystectomySurg Endosc9280282CrossRefPubMed Halevy, A, Lin, G, Gold-Deutsch, R, Lavi, R, Negri, M, Evans, S, Cotariu, D, Sackier, JM 1995Comparison of serum C-reactive protein concentration for laparoscopic versus open cholecystectomySurg Endosc9280282CrossRefPubMed
32.
go back to reference Harmon, GD, Senagore, AJ, Kilbride, MJ, Warzynski, MJ 1994Interleukin-6 response to laparoscopic and open colectomyDis Colon Rectum37754759PubMed Harmon, GD, Senagore, AJ, Kilbride, MJ, Warzynski, MJ 1994Interleukin-6 response to laparoscopic and open colectomyDis Colon Rectum37754759PubMed
33.
go back to reference Hartley, JE, Mehigan, BJ, MacDonald, AW, Lee, PW, Monson, JR 2000Patterns of recurrence and survival after laparoscopic and conventional resections for colorectal carcinomaAnn Surg232181186CrossRefPubMed Hartley, JE, Mehigan, BJ, MacDonald, AW, Lee, PW, Monson, JR 2000Patterns of recurrence and survival after laparoscopic and conventional resections for colorectal carcinomaAnn Surg232181186CrossRefPubMed
34.
go back to reference Hewitt, PM, Ip, SM, Kwok, SP, Somers, SS, Li, K, Leung, KL, Lau, WY, Li, AK 1998Laparoscopic-assisted vs open surgery for colorectal cancers: comparative study of immune effectsDis Colon Rectum41901909PubMed Hewitt, PM, Ip, SM, Kwok, SP, Somers, SS, Li, K, Leung, KL, Lau, WY, Li, AK 1998Laparoscopic-assisted vs open surgery for colorectal cancers: comparative study of immune effectsDis Colon Rectum41901909PubMed
35.
go back to reference Hildebrandt, U, Kessler, K, Pistorius, G, Lindemann, W, Ecker, KW, Feifel, G, Menger, MD 1999Granulocyte elastase and systemic cytokine response after laparoscopic assisted and open resections in Crohn’s diseaseDis Colon Rectum4214801486PubMed Hildebrandt, U, Kessler, K, Pistorius, G, Lindemann, W, Ecker, KW, Feifel, G, Menger, MD 1999Granulocyte elastase and systemic cytokine response after laparoscopic assisted and open resections in Crohn’s diseaseDis Colon Rectum4214801486PubMed
36.
go back to reference Hill, AD, Banwell, PE, Darzi, A, Menzies-Gow, N, Monson, JR, Guillou, PJ 1995Inflammatory markers following laparoscopic and open hernia repairSurg Endosc9695698CrossRefPubMed Hill, AD, Banwell, PE, Darzi, A, Menzies-Gow, N, Monson, JR, Guillou, PJ 1995Inflammatory markers following laparoscopic and open hernia repairSurg Endosc9695698CrossRefPubMed
37.
go back to reference Horgan, PG, Fitzpatrick, M, Couse, NF 1992Laparoscopy is less immunotraumatic than laparotomyMinim Invasive Ther1241244 Horgan, PG, Fitzpatrick, M, Couse, NF 1992Laparoscopy is less immunotraumatic than laparotomyMinim Invasive Ther1241244
38.
go back to reference Iwanaka, T, Arkovitz, MS, Arya, G, Ziegler, MM 1997Evaluation of operative stress and peritoneal macrophage function in minimally invasive operationsJ Am Coll Surg184357363PubMed Iwanaka, T, Arkovitz, MS, Arya, G, Ziegler, MM 1997Evaluation of operative stress and peritoneal macrophage function in minimally invasive operationsJ Am Coll Surg184357363PubMed
39.
go back to reference Jackson, PG, Evans, SR 2000Intraperitoneal macrophages and tumor immunity: previewJ Surg Oncol75146154CrossRefPubMed Jackson, PG, Evans, SR 2000Intraperitoneal macrophages and tumor immunity: previewJ Surg Oncol75146154CrossRefPubMed
40.
go back to reference Jacobi, CA, Ordemann, J, Zieren, HU, Volk, HD, Bauhofer, A, Halle, E, Muller, JM 1998Increased systemic inflammation after laparotomy vs laparoscopy in an animal model of peritonitisArch Surg133258262CrossRefPubMed Jacobi, CA, Ordemann, J, Zieren, HU, Volk, HD, Bauhofer, A, Halle, E, Muller, JM 1998Increased systemic inflammation after laparotomy vs laparoscopy in an animal model of peritonitisArch Surg133258262CrossRefPubMed
41.
go back to reference Jakeways, MS, Mitchell, V, Hashim, IA, Chadwick, SJ, Shenkin, A, Green, CJ, Carli, F 1994Metabolic and inflammatory responses after open or laparoscopic cholecystectomyBr J Surg81127131PubMed Jakeways, MS, Mitchell, V, Hashim, IA, Chadwick, SJ, Shenkin, A, Green, CJ, Carli, F 1994Metabolic and inflammatory responses after open or laparoscopic cholecystectomyBr J Surg81127131PubMed
42.
go back to reference Joris, J, Cigarini, I, Legrand, M, Jacquet, N, Groote, D, Franchimont, P, Lamy, M 1992Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopyBr J Anaesth69341345PubMed Joris, J, Cigarini, I, Legrand, M, Jacquet, N, Groote, D, Franchimont, P, Lamy, M 1992Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopyBr J Anaesth69341345PubMed
43.
go back to reference Kirman, I, Poltoratskaia, N, Herlyn, D, Whelan, RL 2003Addition of interleukin-12 to GA 733 tumor protein vaccine lead to development of tumor protective immunity despite surgical stressSurg Endosc1711351139CrossRefPubMed Kirman, I, Poltoratskaia, N, Herlyn, D, Whelan, RL 2003Addition of interleukin-12 to GA 733 tumor protein vaccine lead to development of tumor protective immunity despite surgical stressSurg Endosc1711351139CrossRefPubMed
44.
go back to reference Kloosterman, T, Blomberg, BM, Borgstein, P, Cuesta, MA, Scheper, RJ, Meijer, S 1994Unimpaired immune function after laparoscopic cholecystectomySurgery115424428PubMed Kloosterman, T, Blomberg, BM, Borgstein, P, Cuesta, MA, Scheper, RJ, Meijer, S 1994Unimpaired immune function after laparoscopic cholecystectomySurgery115424428PubMed
45.
go back to reference Kopernik, G, Avinoach, E, Grossman, Y, Levy, R, Yulzari, R, Rogachev, B, Douvdevani, A 1998The effect of a high partial pressure of carbon dioxide environment on metabolism and immune functions of human peritoneal cells-relevance to carbon dioxide pneumoperitoneumAm J Obstet Gynecol17915031510PubMed Kopernik, G, Avinoach, E, Grossman, Y, Levy, R, Yulzari, R, Rogachev, B, Douvdevani, A 1998The effect of a high partial pressure of carbon dioxide environment on metabolism and immune functions of human peritoneal cells-relevance to carbon dioxide pneumoperitoneumAm J Obstet Gynecol17915031510PubMed
46.
go back to reference Kuntz, C, Wunsch, A, Bay, F, Windeler, J, Glaser, F, Herfarth, C 1996Laparoscopic colon resection in the rat: less immune and stress reaction and improved postoperative recoverySurg Endosc10568 Kuntz, C, Wunsch, A, Bay, F, Windeler, J, Glaser, F, Herfarth, C 1996Laparoscopic colon resection in the rat: less immune and stress reaction and improved postoperative recoverySurg Endosc10568
47.
go back to reference Lacy, AM, Garcia-Valdecasas, JC, Delgado, S, Castells, A, Taura, P, Pique, JM, Visa, J 2002Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trialLancet35922242229CrossRefPubMed Lacy, AM, Garcia-Valdecasas, JC, Delgado, S, Castells, A, Taura, P, Pique, JM, Visa, J 2002Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trialLancet35922242229CrossRefPubMed
48.
go back to reference Lee, SW, Feingold, DL, Carter, JJ, Zhai, C, Stapleton, G, Gleason, N, Whelan, RL 2003Peritoneal macrophage and blood monocyte functions after open and laparoscopic-assisted cecectomy in ratsSurg Endosc1719962002CrossRefPubMed Lee, SW, Feingold, DL, Carter, JJ, Zhai, C, Stapleton, G, Gleason, N, Whelan, RL 2003Peritoneal macrophage and blood monocyte functions after open and laparoscopic-assisted cecectomy in ratsSurg Endosc1719962002CrossRefPubMed
49.
go back to reference Leung, KL, Meng, WCS, Lee, JFY, Thung, KH, Lai, PBS, Lau, WY 1999Laparoscopic-assisted resection of colonic carcinoma: a case-control studyJ Surg Oncol7197100CrossRefPubMed Leung, KL, Meng, WCS, Lee, JFY, Thung, KH, Lai, PBS, Lau, WY 1999Laparoscopic-assisted resection of colonic carcinoma: a case-control studyJ Surg Oncol7197100CrossRefPubMed
50.
go back to reference Little, D, Regan, M, Keane, RM, Bouchier-Hayes, D 1993Perioperative immune modulationSurgery1148791PubMed Little, D, Regan, M, Keane, RM, Bouchier-Hayes, D 1993Perioperative immune modulationSurgery1148791PubMed
51.
go back to reference Malik, E, Buchweitz, O, Muller-Steinhardt, M, Kressin, P, Meyhofer-Malik, A, Diedrich, K 2001Prospective evaluation of the systemic immune response following abdominal, vaginal, and laparoscopically assisted vaginal hysterectomySurg Endosc15463466CrossRefPubMed Malik, E, Buchweitz, O, Muller-Steinhardt, M, Kressin, P, Meyhofer-Malik, A, Diedrich, K 2001Prospective evaluation of the systemic immune response following abdominal, vaginal, and laparoscopically assisted vaginal hysterectomySurg Endosc15463466CrossRefPubMed
52.
go back to reference Maruszynski, M, Pojda, Z 1995Interleukin-6 (IL-6) levels in the monitoring of surgical traumaSurg Endosc9882885PubMed Maruszynski, M, Pojda, Z 1995Interleukin-6 (IL-6) levels in the monitoring of surgical traumaSurg Endosc9882885PubMed
53.
go back to reference Mathew, G, Watson, DI, Ellis, TS, Jamieson, GG, Rofe, AM 1999The role of peritoneal immunity and the tumour-bearing state on the development of wound and peritoneal metastases after laparoscopyAust N Z J Surg691418CrossRefPubMed Mathew, G, Watson, DI, Ellis, TS, Jamieson, GG, Rofe, AM 1999The role of peritoneal immunity and the tumour-bearing state on the development of wound and peritoneal metastases after laparoscopyAust N Z J Surg691418CrossRefPubMed
54.
go back to reference McMahon, AJ, O’Dwyer, PJ, Cruikshank, AM, McMillan, DC, O’Reilly, DS, Lowe, GD, Rumley, A, Logan, RW, Baxter, JN 1993Comparison of metabolic responses to laparoscopic and minilaparotomy cholecystectomyBr J Surg8012551258PubMed McMahon, AJ, O’Dwyer, PJ, Cruikshank, AM, McMillan, DC, O’Reilly, DS, Lowe, GD, Rumley, A, Logan, RW, Baxter, JN 1993Comparison of metabolic responses to laparoscopic and minilaparotomy cholecystectomyBr J Surg8012551258PubMed
55.
go back to reference McMasters, KM, Cheadle, WG 1993Regulation of macrophage TNF alpha, IL-1 beta, and Ia (I-A alpha) mRNA expression during peritonitis is site dependentJ Surg Res54426430CrossRefPubMed McMasters, KM, Cheadle, WG 1993Regulation of macrophage TNF alpha, IL-1 beta, and Ia (I-A alpha) mRNA expression during peritonitis is site dependentJ Surg Res54426430CrossRefPubMed
56.
go back to reference Mealy, K, Gallagher, H, Barry, M, Lennon, F, Traynor, O, Hyland, J 1992Physiological and metabolic responses to open and laparoscopic cholecystectomyBr J Surg7910611064PubMed Mealy, K, Gallagher, H, Barry, M, Lennon, F, Traynor, O, Hyland, J 1992Physiological and metabolic responses to open and laparoscopic cholecystectomyBr J Surg7910611064PubMed
57.
go back to reference Milsom, JW, Bohm, B, Hammerhofer, KA, Fazio, V, Steiger, E, Elson, P 1998A prospective randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: a preliminary reportJ Am Coll Surg1874654CrossRefPubMed Milsom, JW, Bohm, B, Hammerhofer, KA, Fazio, V, Steiger, E, Elson, P 1998A prospective randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: a preliminary reportJ Am Coll Surg1874654CrossRefPubMed
58.
go back to reference Okamoto, T, Tsuburaya, A, Yanoma, S, Yoshikawa, T, Cho, H, Takanashi, Y, Noguchi, Y 2003Inhibition of peritoneal metastasis in an animal gastric cancer model by interferon-gamma and interleukin-2Anticancer Res23149153PubMed Okamoto, T, Tsuburaya, A, Yanoma, S, Yoshikawa, T, Cho, H, Takanashi, Y, Noguchi, Y 2003Inhibition of peritoneal metastasis in an animal gastric cancer model by interferon-gamma and interleukin-2Anticancer Res23149153PubMed
59.
go back to reference Ordemann, J, Jacobi, CA, Schwenk, W, Stosslein, R, Muller, JM 2001Cellular and humoral inflammatory response after laparoscopic colorectal resectionsSurg Endosc15600608CrossRefPubMed Ordemann, J, Jacobi, CA, Schwenk, W, Stosslein, R, Muller, JM 2001Cellular and humoral inflammatory response after laparoscopic colorectal resectionsSurg Endosc15600608CrossRefPubMed
60.
go back to reference Pearlstone, DB, Mansfield, PF, Curley, SA, Kumparatana, M, Cook, P, Feig, BW 1999Laparoscopy in 533 patients with abdominal malignancySurgery1256772CrossRefPubMed Pearlstone, DB, Mansfield, PF, Curley, SA, Kumparatana, M, Cook, P, Feig, BW 1999Laparoscopy in 533 patients with abdominal malignancySurgery1256772CrossRefPubMed
61.
go back to reference Perttila, J, Salo, M, Ovaska, J, Gronroos, J, Lavonius, M, Katila, A, Lahteenmaki, M, Pulkki, K 1999Immune response after laparoscopic and conventional Nissen fundoplicationEur J Surg1652128CrossRefPubMed Perttila, J, Salo, M, Ovaska, J, Gronroos, J, Lavonius, M, Katila, A, Lahteenmaki, M, Pulkki, K 1999Immune response after laparoscopic and conventional Nissen fundoplicationEur J Surg1652128CrossRefPubMed
62.
go back to reference Polk, HC,Jr, George, CD, Hershman, MJ, Wellhausen, SR, Cheadle, WG 1988The capacity of serum to support neutrophil phagocytosis is a vital host defense mechanism in severely injured patientsAnn Surg207686692PubMed Polk, HC,Jr, George, CD, Hershman, MJ, Wellhausen, SR, Cheadle, WG 1988The capacity of serum to support neutrophil phagocytosis is a vital host defense mechanism in severely injured patientsAnn Surg207686692PubMed
63.
go back to reference Redmond, HP, Watson, RW, Houghton, T, Condron, C, Watson, RG, Bouchier-Hayes, D 1994Immune function in patients undergoing open vs laparoscopic cholecystectomyArch Surg12912401246PubMed Redmond, HP, Watson, RW, Houghton, T, Condron, C, Watson, RG, Bouchier-Hayes, D 1994Immune function in patients undergoing open vs laparoscopic cholecystectomyArch Surg12912401246PubMed
64.
go back to reference Reilly, WT, Nelson, H, Schroeder, G, Weiand, HS, Bolton, J, O’Connell, MJ 1996Wound recurrence following conventional treatment of colorectal cancerDis Colon Rectum39200207PubMed Reilly, WT, Nelson, H, Schroeder, G, Weiand, HS, Bolton, J, O’Connell, MJ 1996Wound recurrence following conventional treatment of colorectal cancerDis Colon Rectum39200207PubMed
65.
go back to reference Riboli, E, Terrizzi, A, Arnulfo, G, Bertoglio, S 1984Immunosuppressive effect of surgery evaluated by the multitest cell-mediated immunity systemCan J Surg276063 Riboli, E, Terrizzi, A, Arnulfo, G, Bertoglio, S 1984Immunosuppressive effect of surgery evaluated by the multitest cell-mediated immunity systemCan J Surg276063
66.
go back to reference Rixen, D, Siegel, JH, Abu-Salih, A, Bertolini, M, Panagakos, F, Espina, N 1995Physiologic state severity classification as an indicator of posttrauma cytokine responseShock42738PubMed Rixen, D, Siegel, JH, Abu-Salih, A, Bertolini, M, Panagakos, F, Espina, N 1995Physiologic state severity classification as an indicator of posttrauma cytokine responseShock42738PubMed
67.
go back to reference Romeo, C, Impellizzeri, P, Antonuccio, P, Turiaco, N, Cifala, S, Gentile, C, Passaniti, M, Marini, H, Squadrito, F, Altavilla, D 2003Peritoneal macrophage activity after laparoscopy or laparotomyJ Pediatr Surg3897101CrossRefPubMed Romeo, C, Impellizzeri, P, Antonuccio, P, Turiaco, N, Cifala, S, Gentile, C, Passaniti, M, Marini, H, Squadrito, F, Altavilla, D 2003Peritoneal macrophage activity after laparoscopy or laparotomyJ Pediatr Surg3897101CrossRefPubMed
68.
go back to reference Rotstein, OD 2001Peritoneal host defenses: modulation by carbon dioxide insufflationSurg Infect2163168CrossRef Rotstein, OD 2001Peritoneal host defenses: modulation by carbon dioxide insufflationSurg Infect2163168CrossRef
69.
go back to reference Roumen, RM, Meurs, PA, Kuypers, HH, Kraak, WA, Sauerwein, RW 1992Serum interleukin-6 and C-reactive protein responses in patients after laparoscopic or conventional cholecystectomyEur J Surg158541544PubMed Roumen, RM, Meurs, PA, Kuypers, HH, Kraak, WA, Sauerwein, RW 1992Serum interleukin-6 and C-reactive protein responses in patients after laparoscopic or conventional cholecystectomyEur J Surg158541544PubMed
70.
go back to reference Sampson, LE, Chaplin, DJ 1996The influence of oxygen and carbon dioxide tension on the production of TNF alpha by activated macrophagesBr J Cancer27S133S135 Sampson, LE, Chaplin, DJ 1996The influence of oxygen and carbon dioxide tension on the production of TNF alpha by activated macrophagesBr J Cancer27S133S135
71.
go back to reference Scheidbach, H, Schneider, C, Hugel, O, Scheuerlein, H, Barlehner, E, Konradt, J, Wittekind, C, Kockerling, F 2003Oncological quality and preliminary long-term results in laparoscopic colorectal surgerySurg Endosc17903910CrossRefPubMed Scheidbach, H, Schneider, C, Hugel, O, Scheuerlein, H, Barlehner, E, Konradt, J, Wittekind, C, Kockerling, F 2003Oncological quality and preliminary long-term results in laparoscopic colorectal surgerySurg Endosc17903910CrossRefPubMed
72.
go back to reference Schwenk, W, Jacobi, C, Mansmann, U, Bohm, B, Muller, JM 2000Inflammatory response after laparoscopic and conventional colorectal resections: results of a prospective randomized trialLangenbeck’s Arch Surg38529CrossRef Schwenk, W, Jacobi, C, Mansmann, U, Bohm, B, Muller, JM 2000Inflammatory response after laparoscopic and conventional colorectal resections: results of a prospective randomized trialLangenbeck’s Arch Surg38529CrossRef
73.
go back to reference Sietses, C, Beelen, RH, Meijer, S, Cuesta, MA 1999Immunologic consequences of laparoscopic surgery: speculation on the causes and clinical implicationsLangenbeck’s Arch Surg384250258CrossRef Sietses, C, Beelen, RH, Meijer, S, Cuesta, MA 1999Immunologic consequences of laparoscopic surgery: speculation on the causes and clinical implicationsLangenbeck’s Arch Surg384250258CrossRef
74.
go back to reference Sietses, C, Havenith, CE, Eijsbouts, QA, Leeuwen, PA, Meijer, S, Beelen, RH, Cuesta, MA 2000Laparoscopic surgery preserves monocyte-mediated tumor cell killing in contrast to the conventional approachSurg Endosc14456460 Sietses, C, Havenith, CE, Eijsbouts, QA, Leeuwen, PA, Meijer, S, Beelen, RH, Cuesta, MA 2000Laparoscopic surgery preserves monocyte-mediated tumor cell killing in contrast to the conventional approachSurg Endosc14456460
75.
go back to reference Sietses, C, Wiezer, MJ, Eijsbouts, QA, Beelen, RH, Leeuwen, PA, Blomberg, BM, Meijer, S, Cuesta, MA 1999A prospective randomized study of the systemic immune response after laparoscopic and conventional Nissen fundoplicationSurgery12659CrossRefPubMed Sietses, C, Wiezer, MJ, Eijsbouts, QA, Beelen, RH, Leeuwen, PA, Blomberg, BM, Meijer, S, Cuesta, MA 1999A prospective randomized study of the systemic immune response after laparoscopic and conventional Nissen fundoplicationSurgery12659CrossRefPubMed
76.
go back to reference Smit, MJ, Beelen, RH, Eijsbouts, QA, Meijer, S, Cuesta, MA 1996Immunological response in laparoscopic surgeryActa Gastroenterol Belg59245247PubMed Smit, MJ, Beelen, RH, Eijsbouts, QA, Meijer, S, Cuesta, MA 1996Immunological response in laparoscopic surgeryActa Gastroenterol Belg59245247PubMed
77.
go back to reference Stage, JG, Schulze, S, Moller, P, Overgaard, H, Andersen, M, Rebsdorf-Pedersen, VB, Nielsen, HJ 1997Prospective randomized study of laparoscopic versus open colonic resection for adenocarcinomaBr J Surg83391396CrossRef Stage, JG, Schulze, S, Moller, P, Overgaard, H, Andersen, M, Rebsdorf-Pedersen, VB, Nielsen, HJ 1997Prospective randomized study of laparoscopic versus open colonic resection for adenocarcinomaBr J Surg83391396CrossRef
78.
go back to reference Tang, CL, Eu, KW, Tai, BC, Soh, JGS, Machin, D, Seow-Choen, F 2001Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancerBr J Surg88801807CrossRefPubMed Tang, CL, Eu, KW, Tai, BC, Soh, JGS, Machin, D, Seow-Choen, F 2001Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancerBr J Surg88801807CrossRefPubMed
79.
go back to reference Travis, J 1988Structure, function, and control of neutrophil proteinasesAm J Med843742CrossRef Travis, J 1988Structure, function, and control of neutrophil proteinasesAm J Med843742CrossRef
80.
go back to reference Tung, PHM, Smith, CD 1999Laparoscopic insufflation with room air exaggerated interleukin-6 responseSurg Endosc13473475CrossRefPubMed Tung, PHM, Smith, CD 1999Laparoscopic insufflation with room air exaggerated interleukin-6 responseSurg Endosc13473475CrossRefPubMed
81.
go back to reference Ure, BM, Niewold, TA, Bax, NM, Ham, M, Zee, DC, Essen, GJ 2002Peritoneal, systemic, and distant organ inflammatory responses are reduced by a laparoscopic approach and carbon dioxide versus airSurg Endosc16836842CrossRefPubMed Ure, BM, Niewold, TA, Bax, NM, Ham, M, Zee, DC, Essen, GJ 2002Peritoneal, systemic, and distant organ inflammatory responses are reduced by a laparoscopic approach and carbon dioxide versus airSurg Endosc16836842CrossRefPubMed
82.
go back to reference Valina, VL, Velasco, JM 1996The influence of laparoscopy on lymphocyte subpopulations in the surgical patientSurg Endosc10481484CrossRefPubMed Valina, VL, Velasco, JM 1996The influence of laparoscopy on lymphocyte subpopulations in the surgical patientSurg Endosc10481484CrossRefPubMed
83.
go back to reference Varga, G, Gal, I, Roth, E, Lantos, J, Jaberansari, MT 1997Inflammatory mediators and surgical trauma regarding laparoscopic access: neutrophil functionActa Chir Hung36368369PubMed Varga, G, Gal, I, Roth, E, Lantos, J, Jaberansari, MT 1997Inflammatory mediators and surgical trauma regarding laparoscopic access: neutrophil functionActa Chir Hung36368369PubMed
84.
go back to reference Vittimberga, FJ,Jr, Foley, DP, Meyers, WC, Callery, MP 1998Laparoscopic surgery and the systemic immune responseAnn Surg227326334CrossRefPubMed Vittimberga, FJ,Jr, Foley, DP, Meyers, WC, Callery, MP 1998Laparoscopic surgery and the systemic immune responseAnn Surg227326334CrossRefPubMed
85.
go back to reference Wakefield, CH, Carey, PD, Foulds, S, Monson, JRT, Guillou, PJ 1993Polymorphonuclear leukocyte activation; an early marker of the postsurgical sepsis responseArch Surg128390395PubMed Wakefield, CH, Carey, PD, Foulds, S, Monson, JRT, Guillou, PJ 1993Polymorphonuclear leukocyte activation; an early marker of the postsurgical sepsis responseArch Surg128390395PubMed
86.
go back to reference Watson, RW, Redmond, HP, McCarthy, J, Burke, PE, Bouchier-Hayes, D 1995Exposure of the peritoneal cavity to air regulates early inflammatory responses to surgery in a murine modelBr J Surg8210601065PubMed Watson, RW, Redmond, HP, McCarthy, J, Burke, PE, Bouchier-Hayes, D 1995Exposure of the peritoneal cavity to air regulates early inflammatory responses to surgery in a murine modelBr J Surg8210601065PubMed
87.
go back to reference West, MA, Hackam, DJ, Baker, J, Rodriguez, JL, Bellingham, J, Rotstein, OD 1997Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgeryAnn Surg226179190CrossRefPubMed West, MA, Hackam, DJ, Baker, J, Rodriguez, JL, Bellingham, J, Rotstein, OD 1997Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgeryAnn Surg226179190CrossRefPubMed
88.
go back to reference Wexner, SD, Cohen, SM 1995Portesite metastasis after laparoscopic colorectal surgery for cure of malignancyBr J Surg82295298PubMed Wexner, SD, Cohen, SM 1995Portesite metastasis after laparoscopic colorectal surgery for cure of malignancyBr J Surg82295298PubMed
90.
go back to reference Whelan, RL, Franklin, M, Holubar, SD, Donahue, J, Fowler, R, Munger, C, Doorman, J, Balli, JE, Glass, J, Gonzalez, JJ, Bessler, M, Xie, H, Treat, M 2003Postoperative cell-mediated immune response is better preserved after laparoscopic vs open colorectal resection in humansSurg Endosc17972978CrossRefPubMed Whelan, RL, Franklin, M, Holubar, SD, Donahue, J, Fowler, R, Munger, C, Doorman, J, Balli, JE, Glass, J, Gonzalez, JJ, Bessler, M, Xie, H, Treat, M 2003Postoperative cell-mediated immune response is better preserved after laparoscopic vs open colorectal resection in humansSurg Endosc17972978CrossRefPubMed
91.
go back to reference Wollenberg, GK, DeForge, LE, Bolgos, G, Remick, DG 1993Differential expression of tumor necrosis factor and interleukin-6 by peritoneal macrophages in vivo and in cultureAm J Pathol14311211130PubMed Wollenberg, GK, DeForge, LE, Bolgos, G, Remick, DG 1993Differential expression of tumor necrosis factor and interleukin-6 by peritoneal macrophages in vivo and in cultureAm J Pathol14311211130PubMed
Metadata
Title
The net immunologic advantage of laparoscopic surgery
Authors
Y. W. Novitsky
D. E. M. Litwin
M. P. Callery
Publication date
01-10-2004
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 10/2004
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-003-8275-x

Other articles of this Issue 10/2004

Surgical Endoscopy 10/2004 Go to the issue