Abstract
Background
Cytokines are the main mediators of the inflammation and the response to trauma. The purpose of the present study was the comparative assessment in sera of patients with benign adnexal masses treated by laparoscopy or laparotomy of the following proinflammatory and anti-inflammatory cytokines: interleukin (IL)-1β, IL-6, IL-8, tumor necrosis factor-alpha (TNF-α), and IL-10 in the early postoperative period.
Methods
A total of 40 patients with benign adnexal masses were studied; 25 of whom underwent laparoscopy and 15, laparotomy. Blood serum concentration of IL-1β, IL-6, IL-8, TNF-α, and IL-10 were measured by commercially available ELISA assays before and 4 h, 24 h, and 48 h after the operation.
Results
Concentrations of IL-6 were significantly increased in both groups at 4 h, 24 h, and 48 h after the surgery; levels of IL-10 showed a significant increase 4 h and 24 h after the operation; an increase in IL-1β levels was observed only after laparotomy; no significant variations were observed in serum levels of IL-8; the postoperative increase of IL-1β, IL-6, and IL-10 levels was more pronounced in patients undergoing laparotomy than in those treated laparoscopically; length of the surgical procedure, amount of CO2 used, tumor diameter, age, and body mass index (BMI) of the patients did not influence the postoperative patterns of the studied cytokines.
Conclusions
Systemic cytokine response after operations for benign adnexal masses depends on the degree of the surgical trauma, and is less pronounced in patients undergoing laparoscopy.
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Abu-Eshy SA, Moosa RA, Al-Rofaidi AA, Al-Faki AS, Sadik AA, Salati MI, Ghalib HW (2002) Proinflammatory cytokines in open versus laparoscopic cholecystectomy. Saudi Med J 23: 436–440
Aubert JM, Rombaut C, Argacha P, Romero F, Leira J, Gomez-Bolea F (1998) Simple adnexal cysts in postmenopausal women: conservative management. Maturitas 30: 51–54
Back MR, Sarac TP, Moldawer LL, Welborn MB 3rd, Seeger JM, Huber TS (2000) Laparotomy prevents lethal endotoxemia in a murine sequential insult model by an IL-10-dependent mechanism. Shock 14: 157–162
Badia JM, Whawell SA, Scott-Coombes DM, Abel PD, Williamson RC, Thompson JN(1996) Peritoneal and systemic cytokine response to laparotomy. Br J Surg 83: 347–348
Baigrie RJ, Lamont PM, Kwiatkowski D, Dallman MJ, Morris PJ (1992) Systemic cytokine response after major surgery. Br J Surg 79: 757–760
Bar-Hava I, Orvieto R, Vardimon D, Manor J, Weissman A, Nelinger R, Ben-Rafael Z (1997) Ovarian cyst and cyclic hormone replacement therapy: is there an association? Acta Obstet Gynecol Scand 76: 563–566
Beal AL, Cerra FB (1994) Multiple organ failure syndrome in the 1990s. Systemic inflammatory response and organ dysfunction. JAMA 271: 226–233
Berguer R, Bravo N, Bowyer M, Ferrick D (2000) Measurement of intracellular gamma-interferon, interleukin-4, and interleukin-10 levels in patients following laparoscopic cholecystectomy. J Invest Surg 13: 161–167
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
Buunen M, Gholghesaei M, Veldkamp R, Meijer DW, Bonjer HJ, Bouvy ND (2004) Stress response to laparoscopic surgery: a review. Surg Endosc 18: 1022–1028
Campbell S, Bhan V, Royston P, Whitehead MI, Collins WP (1989) Transabdominal ultrasound screening for early ovarian cancer. BMJ 29: 1363–1367
Conway C, Zalud I, Dilena M, Maulik D, Schulman H, Haley J, Simonelli K (1998) Simple cyst in the postmenopausal patient: detection and management. J Ultrasound Med 17: 369–372
Decker D, Tolba R, Springer W, Lauschke H, Hirner A, von Ruecker A (2005) Abdominal surgical interventions: local and systemic consequences for the immune system—a prospective study on elective gastrointestinal surgery. J Surg Res 126: 12–18
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: 638–646
Dinarello CA, Gelfand JA, Wolff SM (1993) Anticytokine strategies in the treatment of the systemic inflammatory response syndrome. JAMA 269: 1829–1835
Dorum A, Blom GP, Ekerhovd E, Granberg S (2005) Prevalence and histologic diagnosis of adnexal cysts in postmenopausal women: an autopsy study. Am J Obstet Gynecol 192: 48–54
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: 1238–1244
Ellstrom M, Bengtsson A, Tylman M, Haeger M, Olsson JH, Hahlin M (1996) Evaluation of tissue trauma after laparoscopic and abdominal hysterectomy: measurements of neutrophil activation and release of interleukin-6, cortisol, and C-reactive protein. J Am Coll Surg 182: 423–430
Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O’Garra A (1991) IL-10 inhibits cytokine production by activated macrophages. J Immunol 147: 3815–3822
Fornara P, Doehn C, Seyfarth M, Jocham D (2000) Why is urological laparoscopy minimally invasive? Eur Urol 37: 241–250
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
Gupta A, Watson DI (2001) Effect of laparoscopy on immune function. Br J Surg 88: 1296–1306
Hajri A, Mutter D, Wack S, Bastien C, Gury JF, Marescaux J, Aprahamian M (2000) Dual effect of laparoscopy on cell-mediated immunity. Eur Surg Res 32: 261–266
Haq Z, Rahman M, Siddique MA, Roy RK, Rahman AM, Khatun M (2004) Interleukin-6 (IL-6) and tumour necrosis factor-alpha in open and laparoscopic cholecystectomy. Mymensingh Med J 13: 153–156
Harkki-Siren P, Sjoberg J, Toivonen J, Tiitinen A. (2000) Clinical outcome and tissue trauma after laparoscopic and abdominal hysterectomy: a randomized controlled study Acta Obstet Gynecol Scand 79: 866–871
Helmy SA, Wahby MA, El-Nawaway M (1999) The effect of anaesthesia and surgery on plasma cytokine production. Anaesthesia 54: 733–738
Hildebrandt U, Kessler K, Plusczyk T, Pistorius G, Vollmar B, Menger MD (2003) Comparison of surgical stress between laparoscopic and open colonic resections. Surg Endosc 17: 242–246
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: 2690–2694
Igarashi T, Takahashi H, Tanaka M, Murakami S. (1996) Serum interleukin-6 levels after urologic operations Int J Urol 3: 340–342
Jaberansari MT, Roth E, Gal I, Lantos J, Varga G (1997) Inflammatory mediators and surgical trauma regarding laparoscopic access: acute phase response. Acta Chir Hung 36:138–140
Jansson K, Redler Britt, Truedsson L, Magnuson A, Matthiessen P, Andersson M, Norgren L (2004) Intraperitoneal cytokine response after major surgery: higher postoperative intraperitoneal versus systemic cytokine levels suggest the gastrointestinal tract as the major source of the postoperative inflammatory reaction. Am J Surg 187: 372–377
Jess P, Schultz K, Bendtzen K, Nielsen OH (2000) Systemic inflammatory responses during laparoscopic and open inguinal hernia repair: a randomised prospective study. Eur J Surg 166: 540–544
Karayiannakis AJ, Makri GG, Mantzioka A, Karousos D, Karatzas G (1997) Systemic stress response after laparoscopic or open cholecystectomy: a randomized trial. Br J Surg 84: 467–471
Kato M, Honda I, Suzuki H, Murakami M, Matsukawa S, Hashimoto Y (1998) Interleukin-10 production during and after upper abdominal surgery. J Clin Anesth 10: 184–188
Kato M, Suzuki H, Murakami M, Akama M, Matsukawa S, Hashimoto Y (1997) Elevated plasma levels of interleukin-6, interleukin-8, and granulocyte colony-stimulating factor during and after major abdominal surgery. J Clin Anesth 9: 293–298
Kuhry E, Jeekel J, Bonjer HJ. (2004) Effect of laparoscopy on the immune system Semin Laparosc Surg 11: 37–44
Labib M, Palfrey S, Paniagua E, Callender R (1997) The postoperative inflammatory response to injury following laparoscopic assisted vaginal hysterectomy versus abdominal hysterectomy. Ann Clin Biochem 34: 543–545
Lee JW, Kim CJ, Lee JE, Lee SJ, Kim BG, Lee JH, Bae DS, Park CS (2005) Selected adnexal cystic masses in postmenopausal women can be safely managed by laparoscopy. J Korean Med Sci 20: 468–472
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: 506–511
Lin E, Calvano SE, Lowry SF (2000) Inflammatory cytokines and cell response in surgery. Surgery 127: 117–126
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
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: 1289–1293
Miyake H, Kawabata G, Gotoh A, Fujisawa M, Okada H, Arakawa S, Kamidono S, Hara I (2002) Comparison of surgical stress between laparoscopy and open surgery in the field of urology by measurement of humoral mediators. Int J Urol 9: 329–333
Nanashima A, Yamaguchi H, Tsuji T, Yamaguchi E, Sawai T, Yasutake T, Nakagoe T, Ayabe H (1998) Physiologic stress responses to laparoscopic cholecystectomy (1998) A comparison of the gasless and pneumoperitoneal procedures. Surg Endosc 12: 1381–1385
Nguyen NT, Goldman CD, Ho HS, Gosselin RC, Singh A, Wolfe BM (2002) Systemic stress response after laparoscopic and open gastric bypass. J Am Coll Surg 194: 557–566
Ni Choileain N, Redmond HP (2006) Cell response to surgery. Arch Surg 141: 1132–1140
Novitsky YW, Czerniach DR, Kaban GK, Bergner A, Gallagher KA, Perugini RA, Litwin DE (2006) Immunologic effects of hand-assisted surgery on peritoneal macrophages: comparison to open and standard laparoscopic approaches. Surgery 139: 39–45
O’Sullivan ST, Lederer JA, Horgan AF, Chin DH, Mannick JA, Rodrick ML (1995) Major injury leads to predominance of the T helper-2 lymphocyte phenotype and diminished interleukin-12 production associated with decreased resistance to infection. Ann Surg 222: 482–490
Ribeiro SC, Ribeiro RM, Santos NC, Pinotti JA (2003) A randomized study of total abdominal, vaginal and laparoscopic hysterectomy. Int J Gynaecol Obstet 83: 37–43
Riese J, Schoolmann S, Beyer A, Denzel C, Hohenberger W, Haupt W (2000) Production of IL-6 and MCP-1 by the human peritoneum in vivo during major abdominal surgery. Shock 14: 91–94
Rongione AJ, Kusske AM, Kwan K, Ashley SW, Reber HA, McFadden DW (2000) Interleukin-10 protects against lethality of intra-abdominal infection and sepsis. J Gastrointest Surg 4: 70–76
Rorarius MG, Kujansuu E, Baer GA, Suominen P, Teisala K, Miettinen A, Ylitalo P, Laippala P (2001) Laparoscopically assisted vaginal and abdominal hysterectomy: comparison of postoperative pain, fatigue and systemic response. A case-control study. Eur J Anaesthesiol 18: 530–539
Sari R, Sevinc A (2004) The effects of laparascopic cholecystectomy operation on C-reactive protein, hormones, and cytokines. J Endocrinol Invest 27: 106–110
Schietroma M, Carlei F, Franchi L, Mazzotta C, Sozio A, Lygidakis NJ, Amicucci G (2004) A comparison of serum interleukin-6 concentrations in patients treated by cholecystectomy via laparotomy or laparoscopy. Hepatogastroenterology 51: 1595–1599
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: 2–9
Sido B, Teklote J, Hartel M, Friess H, Büchler MW (2004) Inflammatory response after abdominal surgery. Best Pract Res Clin Anaesthesiol 18: 439–454
Suter M, Martinet O, Spertini F (2002) Reduced acute phase response after laparoscopic total extraperitoneal bilateral hernia repair compared to open repair with the Stoppa procedure. Surg Endosc 16: 1214–1219
Targarona EM, Rodriguez TM, Camacho M, Balague C, Gich I, Vila L, Trias M (2006) Immediate peritoneal response to bacterial contamination during laparoscopic surgery. Surg Endosc 20: 316–321
Ure BM, Niewold TA, Bax NM, Ham M, van der Zee DC, Essen GJ (2002) Peritoneal, systemic, and distant organ inflammatory responses are reduced by a laparoscopic approach and carbon dioxide versus air. Surg Endosc 16: 836–842
van Berge Henegouwen MI, van der Poll T, van Deventer SJ, Gouma DJ (1998) Peritoneal cytokine release after elective gastrointestinal surgery and postoperative complications. Am J Surg 175: 311–316
Wu FP, Sietses C, von Blomberg BM, van Leeuwen PA, Meijer S, Cuesta MA (2003) Systemic and peritoneal inflammatory response after laparoscopic or conventional colon resection in cancer patients: a prospective, randomized trial. Dis Colon Rectum 46: 147–155
Yuen PM, Yu KM, Yip SK, Lau WC, Rogers MS, Chang A (1997) A randomized prospective study of laparoscopy and laparotomy in the management of benign ovarian masses. Am J Obstet Gynecol 177: 109–114
Zengin K, Taskin M, Sakoglu N, Salihoglu Z, Demiroluk S, Uzun H (2002) Systemic inflammatory response after laparoscopic and open application of adjustable banding for morbidly obese patients. Obes Surg 12: 276–279
Zieren J, Jacobi CA, Wenger FA, Volk HD, Muller JM (2000) Fundoplication: a model for immunologic aspects of laparoscopic and conventional surgery. J Laparoendosc Adv Surg Tech A 10: 35–40
Acknowledgments
The authors thank Professor Tomasz Rechberger, MD, PhD, Chief, II Department of Gynecology, Medical University of Lublin, Poland, for invaluable help and cooperation during the course of this study.
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Torres, A., Torres, K., Paszkowski, T. et al. Cytokine response in the postoperative period after surgical treatment of benign adnexal masses: comparison between laparoscopy and laparotomy. Surg Endosc 21, 1841–1848 (2007). https://doi.org/10.1007/s00464-007-9260-6
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DOI: https://doi.org/10.1007/s00464-007-9260-6