Abstract
Background
Studies dealing with laparoscopic colectomy for cancer have reached conflicting results in regards to various inflammatory cytokines. Most of them have not examined potential differences with the open procedures at later postoperative days, when the immunologic advantage of laparoscopic surgery would be more demanding to demonstrate (for earlier administration of adjuvant treatment). The aim of this work is to detect differences of proinflammatory cytokines between conventional and laparoscopic colectomy for cancer.
Patients and methods
30 patients who underwent laparoscopic colectomy were age, sex, and preoperative stage-matched with 30 patients treated by open surgery. C-reactive protein (CRP), interleukin (IL)-1, -6, and -8, and interferon (IFN)-γ serum levels were measured preoperatively, at 24 h, and at the 7th postoperative day (POD).
Results
CRP and IL-6 postoperative values (24 h and 7th POD) were significantly higher than baseline for both groups (p = 0.001), but the respective values at the 7th POD were less than at 24 h (p = 0.001). IL-1 and -8 levels did not show any differences between assessment timepoints. A higher IFN-γ measurement was demonstrated at 24 h compared with baseline for the laparoscopic group only (p = 0.03). This difference was not maintained at the 7th POD. IFN-γ levels at 24 h and the 7th POD were significantly less for the open compared with the laparoscopic group of patients (p = 0.001). No correlation was revealed between measured serum values and age, sex, tumor location, or stage.
Conclusions
This matched case–control study verifies the already reported lack of differences regarding IL-1. Controversy still exists on likely IL-6 differences. The inadequately studied IL-8 does not seem to play an important role in immunologic differences. The immunologically beneficial IFN-γ, produced by the principal effectors of cell-mediated immunity Th1 cells, seems to have a more active presence following laparoscopic colectomy, potentially contributing to an immunologic “advantage” by counteracting “harmful” cytokines, such as IL-1.
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References
Barlehner E, Benhidjeb T, Anders S, Schicke B (2004) Laparoscopic surgery for colon and rectal cancer. Surg Technol Int 13:93–99
Colon Cancer Laparoscopic or Open Resection Study Group, Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, Pahlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ (2009) Survival after laparoscopic surgery versus open surgery for colon cancer: long term outcome of a randomized clinical trial. Lancet Oncol 10(1):44–52
Lujan HJ, Plasencia G, Jacobs M, Viamonte M 3rd, Hartmann RF (2002) Long term survival after laparoscopic colon resection for cancer: complete five-year follow up. Dis Colon Rectum 45(4):491–501
Jacob BP, Salky B (2005) Laparoscopic colectomy for colon adenocarcinoma: an 11-year retrospective review with 5-year survival rates. Surg Endosc 19(5):643–649
Barlehner E, Benhidjeb T, Anders S, Schicke B (2005) Laparoscopic resection for rectal cancer: outcomes in 194 patients and review of the literature. Surg Endosc 19(6):757–766
Gupta A, Watson DI (2001) Effect of laparoscopy on immune function. Br J Surg 88(10):1296–1306
Lee SW, Whelan RL (2006) Immunologic and oncologic implications of laparoscopic surgery: what is the latest? Clin Colon Rect Surg 19(1):5–12
Tsamis D, Theodoropoulos G, Michalopoulos NV, Delistathi T, Nikiteas N, Tsigris C, Leandros E (2010) Inflammatory response after laparoscopic versus open colonic resection: Review of the literature. Int J Medic Med Sci 2(4):106–110
Koerner P, Westerholt A, Kessler W, Traeger T, Maier S, Heidecke CD (2008) Surgical trauma and postoperative immunosuppression. Chirurg 79(4):290–294
Sammour T, Kahokehr A, Chan S, Booth RJ, Hill AG (2010) The humoral response after laparoscopic versus open colorectal surgery: a meta-analysis. J Surg Res 164(1):28–37
Brivio F, Perego M, Mauri E, Gramazio F, Brivio O, Gariboldi G, Urso G, Nespoli A (1998) Variations in interleukin-2 and interleukin-6 due to surgical trauma in cancer patients. G Chir 19(10):377–380
Buunen M, Gholghesaei M, Veldkamp R, Meijer DW, Bonjer HJ, Bouvy ND (2004) Stress response to laparoscopic surgery: a review. Surg Endosc 18(7):1022–1028
Hartley JE, Mehigan BJ, Monson JR (2001) Alterations in the immune system and tumor growth in laparoscopy. Surg Endosc 15(3):305–313
Carter JJ, Whelan RL (2001) The immunologic consequences of laparoscopy in oncology. Surg Oncol Clin North Am 10(3):655–677
Ishikawa M, Nishioka M, Hanaki N, Miyauchi T, Kashiwagi Y, Ioki H, Kagawa A, Nakamura Y (2009) Perioperative immune responses in cancer patients undergoing digestive surgeries. W J Surg Oncol 7:7–16
Kuntz C, Wunsch A, Bay F, Windeler J, Glaser F, Herfarth C (1998) Prospective randomized study of stress and immune response after laparoscopic vs conventional colonic resection. Surg Endosc 12(7):963–967
Grande M, Tucci GF, Adorisio O, Barini A, Rulli F, Neri A, Franchi F, Farinon AM (2002) Systemic acute-phase response after laparoscopic and open cholecystectomy. Surg Endosc 16:313–316
Redmond HP, Watson RW, Houghton T, Condron C, Watson RG, Bouchier-Hayes D (1994) Immune function in patients undergoing open vs laparoscopic cholecystectomy. Arch Surg 129:1240–1246
Holub Z (2002) Impact of laparoscopic surgery on immune function. Clin Exp Obstet Gynec 29:77–81
Malik E, Buchweitz O, Muller-Steinhardt M, Kressin P, Meyhofer-Malik A, Diedrich K (2001) Prospective evaluation of the systemic immune response following abdominal, vaginal and laparoscopically assisted vaginal hysterectomy. Surg Endosc 15:463–466
Yuen PM, Mak TW, Yim SF, Kee WD, Lam CW, Rogers MS, Chang AM (1998) Metabolic and inflammatory responses after laparoscopic and abdominal hysterectomy. Am J Obstet Gynecol 179:1–5
Perttila J, Salo M, Ovaska J, Gronroos J, Lavonius M, Katila A, Lahteenmaki M, Pullki K (1999) Immune response after laparoscopic and conventional Nissen fundoplication. Eur J Surg 165:21–28
Uzunkoy A, Coskum A, Akinci OF, Kocyigit A (2000) Systemic stress responses after laparoscopic or open hernia repair. Eur J Surg 166:467–471
Fukushima R, Kawamura YJ, Saito H, Saito Y, Hashiguchi Y, Sawada T, Muto T (1996) Interleukin-6 and stress hormone responses after uncomplicated gasless laparoscopic-assisted and open sigmoid colectomy. Dis Colon Rectum 39(10 Suppl):S29–S34
Mehigan BJ, Hartley JE, Drew PJ, Saleh A, Dore PC, Lee PW, Monson JR (2001) Changes in T cell subsets, interleukin-6 and C-reactive protein after laparoscopic and open colorectal resection for malignancy. Surg Endosc 15(11):1289–1293
Braga M, Vignali A, Zuliani W, Radaelli G, Gianotti L, Martani C, Toussoun G, Di Carlo V (2002) Metabolic and functional results after laparoscopic colorectal surgery: a randomized, controlled trial. Dis Colon Rectum 45(8):1070–1077
Dunker MS, Ten Hove T, Bemelman WA, Slors JF, Gouma DJ, Van Deventer SJ (2003) Interleukin-6, C-reactive protein and expression of human leukocyte antigen-DR on peripheral blood mononuclear cells in patients after laparoscopic vs. conventional bowel resection: a randomized study. Dis Colon Rectum 46(9):1238–1244
Wu FP, Sietses C, von Blomberg BM, van Leeuwen PA, Meijer S, Cuesta MA (2003) Systematic and peritoneal inflammatory response after laparoscopic or conventional colon resection in cancer patients: a prospective, randomized trial. Dis Colon Rectum 46(2):147–155
Ytting H, Christensen IJ, Basse L, Lykke J, Thiel S, Jensenius JC, Nielsen HJ (2006) Influence of major surgery on the mannan-binding lectin pathway of innate immunity. Clin Exp Immunol 144(2):239–246
Huang C, Huang R, Jiang T, Huang K, Cao J, Qiu Z (2010) Laparoscopic and open resection for colorectal cancer: an evaluation of cellular immunity. BMC Gastroenterol 28(10):127
Schwenk W, Jacobi C, Mansmann U, Bohm B, Muller JM (2000) Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial. Langenbecks Arch Surg 385(1):2–9
Nishiguchi K, Okuda J, Toyoda M, Tanaka K, Tanigawa N (2001) Comparative evaluation of surgical stress of laparoscopic and open surgeries for colorectal carcinoma. Dis Colon Rectum 44(2):223–230
Delgado S, Lacy AM, Filella X, Castells A, Garcia-Valdecasas JC, Pique JM, Momblan D, Visa J (2001) Acute phase response in laparoscopic and open colectomy in colon cancer: randomized study. Dis Colon Rectum 44(5):638–646
Hasegawa H, Kabeshima Y, Watanabe M, Yamamoto S, Kitajima M (2003) Randomized controlled trial of laparoscopic versus open colectomy for advanced colorectal cancer. Surg Endosc 17(4):636–640
Harmon GD, Senagore AJ, Kilbride MJ, Warzynski MJ (1994) Interleukin-6 response to laparoscopic and open colectomy. Dis Colon Rectum 37(8):754–759
Leung KL, Lai PB, Ho RL, Meng WC, Yiu RY, Lee JF, Lau WY (2000) Systemic cytokine response after laparoscopic-assisted resection of rectosigmoid carcinoma: A prospective randomized trial. Ann Surg 231(4):506–511
Koch AE, Polverini PJ, Kunkel SL, Harlow LA, DiPietro LA, Elner VM, Elner SG, Strieter RM (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 11 258(5089):1798–1801
Baigrie R, Lamont P, Kwiatkowski D (1992) Systemic cytokine response after major surgery. Br J Surg 19:757
Hu JK, Zhou ZG, Chen ZX, Wang LL, Yu YY, Liu J, Zhang B, Li L, Shu Y, Chen JP (2003) Comparative evaluation of immune response after laparoscopical and open total mesorectal excisions with anal sphincter preservation in patients with rectal cancer. World J Gastroenterol 9(12):2690–2694
Hewitt PM, Ip SM, Kwok SP, Somers SS, Li K, Leung KL, Lau WY, Li AK (1998) Laparoscopic-assisted vs. open surgery for colorectal cancer: comparative study of immune effects. Dis Colon Rectum 41(7):901–909
Pascual M, Alonso S, Parés D, Courtier R, Gil MJ, Grande L, Pera M (2011) Randomized clinical trial comparing inflammatory and angiogenic response after open versus laparoscopic curative resection for colonic cancer. Br J Surg 98(1):50–59
Ordemann J, Jacobi CA, Schwenk W, Stosslein R, Muller JM (2001) Cellular and humoral inflammatory response after laparoscopic and conventional colorectal resections. Surg Endosc 15(6):600–608
Ozawa A, Konishi F, Nagai H, Okada M, Kanazawa K (2000) Cytokine and hormonal responses in laparoscopic-assisted colectomy and conventional open colectomy. Surg Today 30(2):107–111
Stage JG, Schulze S, Moller P, Overgaard H, Andersen M, Rebsdorf-Pedersen VB, Nielsen HJ (1997) Prospective randomized study of laparoscopic versus open colonic resection for adenocarcinoma. Br J Surg 84:391
Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, Visa J (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 29 359(9325):2224–2229
Tang CL, Eu KW, Tai BC, Soh JG, MacHin D, Seow-Choen F (2001) Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancer. Br J Surg 88(6):801–807
Sietses C, Havenith CE, Eijsbouts QA, van Leeuwen PA, Meijer S, Beelen RH, Cuesta MA (2000) Laparoscopic surgery preserves monocyte-mediated tumor cell killing in contrast to the conventional approach. Surg Endosc 14(5):456–460
Bolla G, Tuzzato G (2003) Immunologic postoperative competence after laparoscopy versus laparotomy. Surg Endosc 17(8):1247–1250
Brune IB, Wilke W, Hensler T, Holzmann B, Siewert JR (1999) Downregulation of T helper type 1 immune response and altered pro-inflammatory and anti-inflammatory T cell cytokine balance following conventional but not laparoscopic surgery. AM J Surg 177:55–60
Fujii K, Sonoda K, Izumi K, Shiraishi N, Adachi Y, Kitano S (2003) T lymphocyte subsets and Th1/Th2 balance after laparoscopy-assisted distal gastrectomy. Surg Endosc 17:1440–1444
Disclosures
Authors Dimitrios Tsamis, George Theodoropoulos, Paraskevas Stamopoulos, Spyridon Siakavellas, Thalassini Delistathi, Nikolaos V. Michalopoulos, and George C. Zografos have no conflicts of interest or financial ties to disclose.
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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 26, 1436–1443 (2012). https://doi.org/10.1007/s00464-011-2052-z
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DOI: https://doi.org/10.1007/s00464-011-2052-z