Peritoneal changes due to laparoscopic surgery

W J A Brokelman, M Lensvelt, I H M Borel Rinkes, J H G Klinkenbijl, M M P J Reijnen, W J A Brokelman, M Lensvelt, I H M Borel Rinkes, J H G Klinkenbijl, M M P J Reijnen

Abstract

Background: Laparoscopic surgery has been incorporated into common surgical practice. The peritoneum is an organ with various biologic functions that may be affected in different ways by laparoscopic and open techniques. Clinically, these alterations may be important in issues such as peritoneal metastasis and adhesion formation.

Methods: A literature search using the Pubmed and Cochrane databases identified articles focusing on the key issues of laparoscopy, peritoneum, inflammation, morphology, immunology, and fibrinolysis.

Results: Laparoscopic surgery induces alterations in the peritoneal integrity and causes local acidosis, probably due to peritoneal hypoxia. The local immune system and inflammation are modulated by a pneumoperitoneum. Additionally, the peritoneal plasmin system is inhibited, leading to peritoneal hypofibrinolysis.

Conclusion: Similar to open surgery, laparoscopic surgery affects both the integrity and biology of the peritoneum. These observations may have implications for various clinical conditions.

Figures

Fig. 1
Fig. 1

References

    1. Berggren U, Gordt T, Grama D, Haglund U, Rastad J, Arvidsson D. Laparoscopic versus open cholecystectomy: hospitalization, sick leave, analgesia, and trauma responses. Br J Surg. 1994;81:1362–1365. doi: 10.1002/bjs.1800810936.
    1. Berrevoet E, Biglari M, Sinove Y, De Baardemaeker L, Troise R, de Hemptinne B. Outpatient laparoscopic cholecystectomy in Belgium: what are we waiting for? Acta Chir Belg. 2006;106:537–540.
    1. Gutt CN, Oniu T, Schemmer P, Mehrabi A, Buchler MW. Fewer adhesions induced by laparoscopic surgery? Surg Endosc. 2004;18:898–906. doi: 10.1007/s00464-004-0056-7.
    1. Yung S, Chan TM. Mesothelial cells. Perit Dial Int. 2007;27(Suppl 2):S110–S115.
    1. Nachtsheim R, Dudley B, McNeil PL, Howdieshell TR. The peritoneal cavity is a distinct compartment of angiogenic molecular mediators. J Surg Res. 2006;134:28–35. doi: 10.1016/j.jss.2006.03.008.
    1. Chegini N. Peritoneal molecular environment, adhesion formation, and clinical implication. Front Biosci. 2002;7:e91–e115. doi: 10.2741/chegini.
    1. diZerega GS. Biochemical events in peritoneal tissue repair. Eur J Surg Suppl. 1997;577:10–16.
    1. Holmdahl L, Ivarsson ML. The role of cytokines, coagulation, and fibrinolysis in peritoneal tissue repair. Eur J Surg. 1999;165:1012–1019. doi: 10.1080/110241599750007810.
    1. van der Wal JB, Jeekel J. Biology of the peritoneum in normal homeostasis and after surgical trauma. Colorectal Dis. 2007;9(Suppl 2):9–13.
    1. Michailova K, Wassilev W, Wedel T. Scanning and transmission electron microscopic study of visceral and parietal peritoneal regions in the rat. Ann Anat. 1999;181:253–260. doi: 10.1016/S0940-9602(99)80040-5.
    1. Suematsu T, Hirabayashi Y, Shiraishi N, Adachi Y, Kitamura H, Kitano S. Morphology of the murine peritoneum after pneumoperitoneum vs. laparotomy. Surg Endosc. 2001;15:954–958. doi: 10.1007/s004640090100.
    1. Volz J, Koster S, Spacek Z, Paweletz N. Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc. 1999;13:611–614. doi: 10.1007/s004649901052.
    1. Bertram P, Tietze L, Hoopmann M, Treutner KH, Mittermayer C, Schumpelick V. Intraperitoneal transplantation of isologous mesothelial cells for prevention of adhesions. Eur J Surg. 1999;165:705–709. doi: 10.1080/11024159950189780.
    1. Lucas PA, Warejcka DJ, Zhang LM, Newman WH, Young HE. Effect of rat mesenchymal stem cells on development of abdominal adhesions after surgery. J Surg Res. 1996;62:229–232. doi: 10.1006/jsre.1996.0200.
    1. Papparella A, Noviello C, Romano M, Parmeggiani P, Paciello O, Papparella S. Local and systemic impact of pneumoperitoneum on prepuberal rats. Pediatr Surg Int. 2007;23:453–457. doi: 10.1007/s00383-006-1860-z.
    1. Rosario MT, Ribeiro U, Jr, Corbett CE, Ozaki AC, Bresciani CC, Zilberstein B, Gama-Rodriques JJ. Does CO2 pneumoperitoneum alter the ultra-structure of the mesothelium? J Surg Res. 2006;133:84–88. doi: 10.1016/j.jss.2005.09.032.
    1. Hazebroek EJ, Schreve MA, Visser P, De Bruin RW, Marquet RL, Bonjer HJ. Impact of temperature and humidity of carbon dioxide pneumoperitoneum on body temperature and peritoneal morphology. J Laparoendosc Adv Surg Tech A. 2002;12:355–364. doi: 10.1089/109264202320884108.
    1. Erikoglu M, Yol S, Avunduk MC, Erdemli E, Can A. Electron-microscopic alterations of the peritoneum after both cold and heated carbon dioxide pneumoperitoneum. J Surg Res. 2005;125:73–77. doi: 10.1016/j.jss.2004.11.029.
    1. Liu Y, Hou QX. Effect of carbon dioxide pneumoperitoneum during laparoscopic surgery on morphology of peritoneum. Zhonghua Yi Xue Za Zhi. 2006;86:164–166.
    1. Wildbrett P, Oh A, Naundorf D, Volk T, Jacobi CA. Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function. Surg Endosc. 2003;17:78–82. doi: 10.1007/s00464-002-9015-3.
    1. Bourdel N, Matsuzaki S, Bazin JE, Pouly JL, Mage G, Canis M. Peritoneal tissue–oxygen tension during a carbon dioxide pneumoperitoneum in a mouse laparoscopic model with controlled respiratory support. Hum Reprod. 2007;22:1149–1155. doi: 10.1093/humrep/del482.
    1. Molinas CR, Koninckx PR. Hypoxaemia induced by CO2 or helium pneumoperitoneum is a cofactor in adhesion formation in rabbits. Hum Reprod. 2000;15:1758–1763. doi: 10.1093/humrep/15.8.1758.
    1. Molinas CR, Mynbaev O, Pauwels A, Novak P, Koninckx PR. Peritoneal mesothelial hypoxia during pneumoperitoneum is a cofactor in adhesion formation in a laparoscopic mouse model. Fertil Steril. 2001;76:560–567. doi: 10.1016/S0015-0282(01)01964-1.
    1. Elkelani OA, Binda MM, Molinas CR, Koninckx PR. Effect of adding more than 3% oxygen to carbon dioxide pneumoperitoneum on adhesion formation in a laparoscopic mouse model. Fertil Steril. 2004;82:1616–1622. doi: 10.1016/j.fertnstert.2004.07.933.
    1. Molinas CR, Campo R, Elkelani OA, Binda MM, Carmeliet P, Koninckx PR. Role of hypoxia-inducible factors 1alpha and 2alpha in basal adhesion formation and in carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in transgenic mice. Fertil Steril. 2003;80(Suppl 2):795–802. doi: 10.1016/S0015-0282(03)00779-9.
    1. Binda MM, Molinas CR, Bastidas A, Koninckx PR. Effect of reactive oxygen species scavengers, antiinflammatory drugs, and calcium-channel blockers on carbon dioxide pneumoperitoneum-enhanced adhesions in a laparoscopic mouse model. Surg Endosc. 2007;21:1826–1834. doi: 10.1007/s00464-007-9296-7.
    1. Bergstrom M, Falk P, Park PO, Holmdahl L. Peritoneal and systemic pH during pneumoperitoneum with CO2 and helium in a pig model. Surg Endosc. 2008;22:359–364. doi: 10.1007/s00464-007-9409-3.
    1. Hanly EJ, Aurora AR, Fuentes JM, Shih SP, Marohn MR, De Maio A, Talamini MA. Abdominal insufflation with CO2 causes peritoneal acidosis independent of systemic pH. J Gastrointest Surg. 2005;9:1245–1251. doi: 10.1016/j.gassur.2005.09.007.
    1. Wong YT, Shah PC, Birkett DH, Brams DM. Carbon dioxide pneumoperitoneum causes severe peritoneal acidosis, unaltered by heating, humidification, or bicarbonate in a porcine model. Surg Endosc. 2004;18:1498–1503. doi: 10.1007/s00464-003-9290-7.
    1. Hanly EJ, Aurora AA, Shih SP, Fuentes JM, Marohn MR, De Maio A, Talamini MA. Peritoneal acidosis mediates immunoprotection in laparoscopic surgery. Surgery. 2007;142:357–364. doi: 10.1016/j.surg.2007.02.017.
    1. Heel KA, Hall JC. Peritoneal defences and peritoneum-associated lymphoid tissue. Br J Surg. 1996;83:1031–1036. doi: 10.1002/bjs.1800830804.
    1. Allendorf JD, Bessler M, Horvath KD, Marvin MR, Laird DA, Whelan RL. 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;13:233–235. doi: 10.1007/s004649900952.
    1. Whelan RL, Franklin M, Holubar SD, Donahue J, Fowler R, Munger C, Doorman J, Balli JE, Glass J, Gonzalez JJ, Bessler M, Wie H, Treat M. Postoperative cell-mediated immune response is better preserved after laparoscopic vs. open colorectal resection in humans. Surg Endosc. 2003;17:972–978. doi: 10.1007/s00464-001-8263-y.
    1. Gitzelmann CA, Mendoza-Sagaon M, Talamini MA, Ahmad SA, Pegoli W, Jr, Paidas CN. Cell-mediated immune response is better preserved by laparoscopy than laparotomy. Surgery. 2000;127:65–71. doi: 10.1067/msy.2000.101152.
    1. Wichmann MW, Huttl TP, Winter H, Spelsberg F, Angele MK, Heiss MM, Jauch KW. Immunological effects of laparoscopic vs. open colorectal surgery: a prospective clinical study. Arch Surg. 2005;140:692–697. doi: 10.1001/archsurg.140.7.692.
    1. Glaser F, Sannwald GA, Buhr HJ, Kuntz C, Mayer H, Klee F, Herfarth C. General stress response to conventional and laparoscopic cholecystectomy. Ann Surg. 1995;221:372–380. doi: 10.1097/00000658-199504000-00007.
    1. Cho JM, LaPorta AJ, Clark JR, Schofield MJ, Hammond SL, Mallory PL. Response of serum cytokines in patients undergoing laparoscopic cholecystectomy. Surg Endosc. 1994;8:1380–1383. doi: 10.1007/BF00187340.
    1. Menger MD, Vollmar B. Surgical trauma: hyperinflammation versus immunosuppression? Langenbecks Arch Surg. 2004;389:475–484. doi: 10.1007/s00423-004-0472-0.
    1. Kuntz C, Wunsch A, Bay F, Windeler J, Glaser F, Herfarth C. Prospective randomized study of stress and immune response after laparoscopic vs. conventional colonic resection. Surg Endosc. 1998;12:963–967. doi: 10.1007/s004649900757.
    1. Redmond HP, Watson RW, Houghton T, Condron C, Watson RG, Bouchier-Hayes D. Immune function in patients undergoing open vs. laparoscopic cholecystectomy. Arch Surg. 1994;129:1240–1246.
    1. Moehrlen U, Ziegler U, Boneberg E, Reichmann E, Gitzelmann CA, Meuli M, Hamacher J. Impact of carbon dioxide versus air pneumoperitoneum on peritoneal cell migration and cell fate. Surg Endosc. 2006;20:1607–1613. doi: 10.1007/s00464-005-0775-4.
    1. Moehrlen U, Schwoebel F, Reichmann E, Stauffer U, Gitzelmann CA, Hamacher J. Early peritoneal macrophage function after laparoscopic surgery compared with laparotomy in a mouse mode. Surg Endosc. 2005;19:958–963. doi: 10.1007/s00464-004-2118-2.
    1. West MA, Hackam DJ, Baker J, Rodriquez JL, Bellingham J, Rotstein OD. Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgery. Ann Surg. 1997;226:179–190. doi: 10.1097/00000658-199708000-00010.
    1. Mathew G, Watson DI, Ellis TS, Jamieson GG, Rofe AM. The role of peritoneal immunity and the tumour-bearing state on the development of wound and peritoneal metastases after laparoscopy. Aust N Z J Surg. 1999;69:14–18. doi: 10.1046/j.1440-1622.1999.01484.x.
    1. Volz J, Koster S, Spacek Z, Paweletz N. The influence of pneumoperitoneum used in laparoscopic surgery on an intraabdominal tumor growth. Cancer. 1999;86:770–774. doi: 10.1002/(SICI)1097-0142(19990901)86:5<770::AID-CNCR11>;2-3.
    1. Neuhaus SJ, Watson DI, Ellies T, Rowland R, Rofe AM, Pike GK, Mathew G, Jamieson GG. Wound metastasis after laparoscopy with different insufflation gases. Surgery. 1998;123:579–583. doi: 10.1067/msy.1998.88089.
    1. West MA, Baker J, Bellingham J. Kinetics of decreased LPS-stimulated cytokine release by macrophages exposed to CO2. J Surg Res. 1996;63:269–274. doi: 10.1006/jsre.1996.0259.
    1. Jacobs VR, Morrison JE, Jr, Mundhenke C, Golombeck K, Jonat W. Intraoperative evaluation of laparoscopic insufflation technique for quality control in the OR. JSLS. 2000;4:189–195.
    1. Bessell JR, Ludbrook G, Miljard SH, Baxter PS, Ubhi SS, Maddern GJ. Humidified gas prevents hypothermia induced by laparoscopic insufflation: a randomized controlled study in a pig model. Surg Endosc. 1999;13:101–105. doi: 10.1007/s004649900914.
    1. Puttick MI, Scott-Coombes DM, Dye J, Nduka CC, Menzies-Gow NM, Mansfield AO, Darzi A. Comparison of immunologic and physiologic effects of CO2 pneumoperitoneum at room and body temperatures. Surg Endosc. 1999;13:572–575. doi: 10.1007/s004649901043.
    1. Ohzato H, Yoshizaki K, Nishimoto N, Ogata A, Tagoh H, Monden M, Gotoh M, Kishimoto T, Mori T. Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery. 1992;111:201–209.
    1. Yao V, Platell C, Hall JC. Peritoneal mesothelial cells produce inflammatory related cytokines. ANZ J Surg. 2004;74:997–1002. doi: 10.1111/j.1445-1433.2004.03220.x.
    1. Liberek T, Topley N, Luttmann W, Williams JD. Adherence of neutrophils to human peritoneal mesothelial cells: role of intercellular adhesion molecule-1. J Am Soc Nephrol. 1996;7:208–217.
    1. Brokelman WJ, Holmdahl L, Berstrom M, Falk P, Klinkenbijl JH, Reijnen MM. Peritoneal transforming growth factor beta-1 expression during laparoscopic surgery: a clinical trial. Surg Endosc. 2007;21:1537–1541. doi: 10.1007/s00464-006-9164-x.
    1. Kagami S, Kuhara T, Yasutomo K, Okada K, Loster K, Reutte W, Kuroda Y. Transforming growth factor-beta (TGF-beta) stimulates the expression of beta1 integrins and adhesion by rat mesangial cells. Exp Cell Res. 1996;229:1–6. doi: 10.1006/excr.1996.0336.
    1. Ignotz RA, Massague J. Cell adhesion protein receptors as targets for transforming growth factor-beta action. Cell. 1987;51:189–197. doi: 10.1016/0092-8674(87)90146-2.
    1. Duron JJ. Postoperative intraperitoneal adhesion pathophysiology. Colorectal Dis. 2007;9(Suppl 2):14–24. doi: 10.1111/j.1463-1318.2007.01343.x.
    1. Hobson KG, DeWing M, Ho HS, Wolfe BM, Cho K, Greenhalgh DG. Expression of transforming growth factor beta1 in patients with and without previous abdominal surgery. Arch Surg. 2003;138:1249–1252. doi: 10.1001/archsurg.138.11.1249.
    1. Holmdahl L, Kotseos K, Bergström M, Falk P, Ivarsson ML, Chegini N. Overproduction of transforming growth factor-beta1 (TGF-beta1) is associated with adhesion formation and peritoneal fibrinolytic impairment. Surgery. 2001;129:626–632. doi: 10.1067/msy.2001.113039.
    1. Freeman ML, Saed GM, Elhammady EF, Diamond MP. Expression of transforming growth factor beta isoform mRNA in injured peritoneum that healed with adhesions and without adhesions and in uninjured peritoneum. Fertil Steril. 2003;80(Suppl 2):708–713. doi: 10.1016/S0015-0282(03)00770-2.
    1. Sendt W, Amberg R, Schöffel U, Hassan A, von Specht BU, Farthmann EH. Local inflammatory peritoneal response to operative trauma: studies on cell activity, cytokine expression, and adhesion molecules. Eur J Surg. 1999;165:1024–1030. doi: 10.1080/110241599750007838.
    1. Molinas CR, Binda MM, Carmeliet P, Koninckx PR. Role of vascular endothelial growth factor receptor 1 in basal adhesion formation and in carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in mice. Fertil Steril. 2004;82(Suppl 3):1149–1153. doi: 10.1016/j.fertnstert.2004.04.032.
    1. Holmdahl L, Eriksson E, al Jabreen M, Risberg B. Fibrinolysis in human peritoneum during operation. Surgery. 1996;119:701–705. doi: 10.1016/S0039-6060(96)80196-6.
    1. Scott-Coombes DM, Whawell SA, Thompson JN. The operative peritoneal fibrinolytic response to abdominal operation. Eur J Surg. 1995;161:395–399.
    1. Ivarsson ML, Falk P, Holmdahl L. Response of visceral peritoneum to abdominal surgery. Br J Surg. 2001;88:148–151. doi: 10.1046/j.1365-2168.2001.01630.x.
    1. Ziprin P, Ridgway PF, Peck DH, Darzi AW. Laparoscopic-type environment enhances mesothelial cell fibrinolytic activity in vitro via a downregulation of plasminogen activator inhibitor-1 activity. Surgery. 2003;134:758–765. doi: 10.1016/S0039-6060(03)00293-9.
    1. Bergström M, Falk P, Holmdahl L. CO2 promotes plasminogen activator inhibitor type 1 expression in human mesothelial cells. Surg Endosc. 2003;17:1818–1822. doi: 10.1007/s00464-002-9113-2.
    1. Molinas CR, Elkelani O, Campo R, Luttun A, Carmeliet P, Koninckx PR. Role of the plasminogen system in basal adhesion formation and carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in transgenic mice. Fertil Steril. 2003;80:184–192. doi: 10.1016/S0015-0282(03)00496-5.
    1. Nagelschmidt M, Gerbecks D, Minor T. The impact of gas laparoscopy on abdominal plasminogen activator activity. Surg Endosc. 2001;15:585–588. doi: 10.1007/s004640010282.
    1. Tarhan OR, Barut I, Akdeniz Y, Sutcu R, Cerci C, Bulbul M. Fibrinolytic responses of human peritoneal fluid in laparoscopic cholecystectomy: a prospective clinical study. Surg Endosc. 2008;22:1008–1013. doi: 10.1007/s00464-007-9566-4.
    1. Brokelman WJ, Holmdahl L, Bergström M, Falk P, Klinkenbijl JH, Reijnen MM. Peritoneal fibrinolytic response to various aspects of laparoscopic surgery: a randomized trial. J Surg Res. 2006;136:309–313. doi: 10.1016/j.jss.2006.07.044.
    1. Brokelman WJ, Holmdahl L, Janssen IM, Falk P, Bergström M, Klinkenbijl JH, Reijnen MM. Decreased peritoneal tissue plasminogen activator during prolonged laparoscopic surgery. J Surg Res. 2008;151:89–93. doi: 10.1016/j.jss.2008.01.005.
    1. Brokelman WJ, Holmdahl L, Bergström M, Falk P, Klinkenbijl JH, Reijnen MM. Heating of carbon dioxide during insufflation alters the peritoneal fibrinolytic response to laparoscopic surgery: a clinical trial. Surg Endosc. 2007;5:1232–1236.
    1. Bergström M, Ivarsson ML, Holmdahl L. Peritoneal response to pneumoperitoneum and laparoscopic surgery. Br J Surg. 2002;89:1465–1469. doi: 10.1046/j.1365-2168.2002.02228.x.
    1. Neudecker J, Junghans T, Ziemer S, Raue W, Schwenk W. Effect of laparoscopic and conventional colorectal resection on peritoneal fibrinolytic capacity: a prospective randomized clinical trial. Int J Colorectal Dis. 2002;17:426–429. doi: 10.1007/s00384-002-0391-x.
    1. Brokelman W, Holmdahl L, Falk P, Klinkenbijl J, Reijnen M (2009) The peritoneal fibrinolytic response to conventional and laparoscopic colonic surgery. J Laparoendosc Adv Surg Tech A 19:489–93
    1. Strobel T, Cannistra SA. Beta1-integrins partly mediate binding of ovarian cancer cells to peritoneal mesothelium in vitro. Gynecol Oncol. 1999;73:362–367. doi: 10.1006/gyno.1999.5388.
    1. Wilson MS. Practicalities and costs of adhesions. Colorectal Dis. 2007;9(Suppl 2):60–65. doi: 10.1111/j.1463-1318.2007.01360.x.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever