Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Surgical Endoscopy
Published in: Surgical Endoscopy 1/2011

Open Access 01-01-2011 | Review

Peritoneal changes due to laparoscopic surgery

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

Published in: Surgical Endoscopy | Issue 1/2011

Login to get access

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.
Literature
1.
Berggren U, Gordt T, Grama D, Haglund U, Rastad J, Arvidsson D (1994) Laparoscopic versus open cholecystectomy: hospitalization, sick leave, analgesia, and trauma responses. Br J Surg 81:1362–1365CrossRefPubMed
2.
Berrevoet E, Biglari M, Sinove Y, De Baardemaeker L, Troise R, de Hemptinne B (2006) Outpatient laparoscopic cholecystectomy in Belgium: what are we waiting for? Acta Chir Belg 106:537–540PubMed
3.
Gutt CN, Oniu T, Schemmer P, Mehrabi A, Buchler MW (2004) Fewer adhesions induced by laparoscopic surgery? Surg Endosc 18:898–906CrossRefPubMed
4.
Yung S, Chan TM (2007) Mesothelial cells. Perit Dial Int 27(Suppl 2):S110–S115PubMed
5.
Nachtsheim R, Dudley B, McNeil PL, Howdieshell TR (2006) The peritoneal cavity is a distinct compartment of angiogenic molecular mediators. J Surg Res 134:28–35CrossRefPubMed
6.
Chegini N (2002) Peritoneal molecular environment, adhesion formation, and clinical implication. Front Biosci 7:e91–e115CrossRefPubMed
7.
diZerega GS (1997) Biochemical events in peritoneal tissue repair. Eur J Surg Suppl 577:10–16PubMed
8.
Holmdahl L, Ivarsson ML (1999) The role of cytokines, coagulation, and fibrinolysis in peritoneal tissue repair. Eur J Surg 165:1012–1019CrossRefPubMed
9.
van der Wal JB, Jeekel J (2007) Biology of the peritoneum in normal homeostasis and after surgical trauma. Colorectal Dis 9(Suppl 2):9–13PubMed
10.
Michailova K, Wassilev W, Wedel T (1999) Scanning and transmission electron microscopic study of visceral and parietal peritoneal regions in the rat. Ann Anat 181:253–260CrossRefPubMed
11.
Suematsu T, Hirabayashi Y, Shiraishi N, Adachi Y, Kitamura H, Kitano S (2001) Morphology of the murine peritoneum after pneumoperitoneum vs. laparotomy. Surg Endosc 15:954–958CrossRefPubMed
12.
Volz J, Koster S, Spacek Z, Paweletz N (1999) Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc 13:611–614CrossRefPubMed
13.
Bertram P, Tietze L, Hoopmann M, Treutner KH, Mittermayer C, Schumpelick V (1999) Intraperitoneal transplantation of isologous mesothelial cells for prevention of adhesions. Eur J Surg 165:705–709CrossRefPubMed
14.
Lucas PA, Warejcka DJ, Zhang LM, Newman WH, Young HE (1996) Effect of rat mesenchymal stem cells on development of abdominal adhesions after surgery. J Surg Res 62:229–232CrossRefPubMed
15.
Papparella A, Noviello C, Romano M, Parmeggiani P, Paciello O, Papparella S (2007) Local and systemic impact of pneumoperitoneum on prepuberal rats. Pediatr Surg Int 23:453–457CrossRefPubMed
16.
Rosario MT, Ribeiro U Jr, Corbett CE, Ozaki AC, Bresciani CC, Zilberstein B, Gama-Rodriques JJ (2006) Does CO2 pneumoperitoneum alter the ultra-structure of the mesothelium? J Surg Res 133:84–88CrossRefPubMed
17.
Hazebroek EJ, Schreve MA, Visser P, De Bruin RW, Marquet RL, Bonjer HJ (2002) Impact of temperature and humidity of carbon dioxide pneumoperitoneum on body temperature and peritoneal morphology. J Laparoendosc Adv Surg Tech A 12:355–364CrossRefPubMed
18.
Erikoglu M, Yol S, Avunduk MC, Erdemli E, Can A (2005) Electron-microscopic alterations of the peritoneum after both cold and heated carbon dioxide pneumoperitoneum. J Surg Res 125:73–77CrossRefPubMed
19.
Liu Y, Hou QX (2006) Effect of carbon dioxide pneumoperitoneum during laparoscopic surgery on morphology of peritoneum. Zhonghua Yi Xue Za Zhi 86:164–166PubMed
20.
Wildbrett P, Oh A, Naundorf D, Volk T, Jacobi CA (2003) Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function. Surg Endosc 17:78–82CrossRefPubMed
21.
Bourdel N, Matsuzaki S, Bazin JE, Pouly JL, Mage G, Canis M (2007) Peritoneal tissue–oxygen tension during a carbon dioxide pneumoperitoneum in a mouse laparoscopic model with controlled respiratory support. Hum Reprod 22:1149–1155CrossRefPubMed
22.
Molinas CR, Koninckx PR (2000) Hypoxaemia induced by CO2 or helium pneumoperitoneum is a cofactor in adhesion formation in rabbits. Hum Reprod 15:1758–1763CrossRefPubMed
23.
Molinas CR, Mynbaev O, Pauwels A, Novak P, Koninckx PR (2001) Peritoneal mesothelial hypoxia during pneumoperitoneum is a cofactor in adhesion formation in a laparoscopic mouse model. Fertil Steril 76:560–567CrossRefPubMed
24.
Elkelani OA, Binda MM, Molinas CR, Koninckx PR (2004) Effect of adding more than 3% oxygen to carbon dioxide pneumoperitoneum on adhesion formation in a laparoscopic mouse model. Fertil Steril 82:1616–1622CrossRefPubMed
25.
Molinas CR, Campo R, Elkelani OA, Binda MM, Carmeliet P, Koninckx PR (2003) 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 80(Suppl 2):795–802CrossRefPubMed
26.
Binda MM, Molinas CR, Bastidas A, Koninckx PR (2007) 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 21:1826–1834CrossRefPubMed
27.
Bergstrom M, Falk P, Park PO, Holmdahl L (2008) Peritoneal and systemic pH during pneumoperitoneum with CO2 and helium in a pig model. Surg Endosc 22:359–364CrossRefPubMed
28.
Hanly EJ, Aurora AR, Fuentes JM, Shih SP, Marohn MR, De Maio A, Talamini MA (2005) Abdominal insufflation with CO2 causes peritoneal acidosis independent of systemic pH. J Gastrointest Surg 9:1245–1251CrossRefPubMed
29.
Wong YT, Shah PC, Birkett DH, Brams DM (2004) Carbon dioxide pneumoperitoneum causes severe peritoneal acidosis, unaltered by heating, humidification, or bicarbonate in a porcine model. Surg Endosc 18:1498–1503CrossRefPubMed
30.
Hanly EJ, Aurora AA, Shih SP, Fuentes JM, Marohn MR, De Maio A, Talamini MA (2007) Peritoneal acidosis mediates immunoprotection in laparoscopic surgery. Surgery 142:357–364CrossRefPubMed
31.
Heel KA, Hall JC (1996) Peritoneal defences and peritoneum-associated lymphoid tissue. Br J Surg 83:1031–1036CrossRefPubMed
32.
Allendorf JD, Bessler M, Horvath KD, Marvin MR, Laird DA, Whelan RL (1999) Increased tumor establishment and growth after open vs. laparoscopic surgery in mice may be related to differences in postoperative T-cell function. Surg Endosc 13:233–235CrossRefPubMed
33.
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 (2003) Postoperative cell-mediated immune response is better preserved after laparoscopic vs. open colorectal resection in humans. Surg Endosc 17:972–978CrossRefPubMed
34.
Gitzelmann CA, Mendoza-Sagaon M, Talamini MA, Ahmad SA, Pegoli W Jr, Paidas CN (2000) Cell-mediated immune response is better preserved by laparoscopy than laparotomy. Surgery 127:65–71CrossRefPubMed
35.
Wichmann MW, Huttl TP, Winter H, Spelsberg F, Angele MK, Heiss MM, Jauch KW (2005) Immunological effects of laparoscopic vs. open colorectal surgery: a prospective clinical study. Arch Surg 140:692–697CrossRefPubMed
36.
Glaser F, Sannwald GA, Buhr HJ, Kuntz C, Mayer H, Klee F, Herfarth C (1995) General stress response to conventional and laparoscopic cholecystectomy. Ann Surg 221:372–380CrossRefPubMed
37.
Cho JM, LaPorta AJ, Clark JR, Schofield MJ, Hammond SL, Mallory PL (1994) Response of serum cytokines in patients undergoing laparoscopic cholecystectomy. Surg Endosc 8:1380–1383CrossRefPubMed
38.
Menger MD, Vollmar B (2004) Surgical trauma: hyperinflammation versus immunosuppression? Langenbecks Arch Surg 389:475–484CrossRefPubMed
39.
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 12:963–967CrossRefPubMed
40.
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 129:1240–1246PubMed
41.
Moehrlen U, Ziegler U, Boneberg E, Reichmann E, Gitzelmann CA, Meuli M, Hamacher J (2006) Impact of carbon dioxide versus air pneumoperitoneum on peritoneal cell migration and cell fate. Surg Endosc 20:1607–1613CrossRefPubMed
42.
Moehrlen U, Schwoebel F, Reichmann E, Stauffer U, Gitzelmann CA, Hamacher J (2005) Early peritoneal macrophage function after laparoscopic surgery compared with laparotomy in a mouse mode. Surg Endosc 19:958–963CrossRefPubMed
43.
West MA, Hackam DJ, Baker J, Rodriquez JL, Bellingham J, Rotstein OD (1997) Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgery. Ann Surg 226:179–190CrossRefPubMed
44.
Mathew G, Watson DI, Ellis TS, Jamieson GG, Rofe AM (1999) 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 69:14–18CrossRefPubMed
45.
Volz J, Koster S, Spacek Z, Paweletz N (1999) The influence of pneumoperitoneum used in laparoscopic surgery on an intraabdominal tumor growth. Cancer 86:770–774CrossRefPubMed
46.
Neuhaus SJ, Watson DI, Ellies T, Rowland R, Rofe AM, Pike GK, Mathew G, Jamieson GG (1998) Wound metastasis after laparoscopy with different insufflation gases. Surgery 123:579–583CrossRefPubMed
47.
West MA, Baker J, Bellingham J (1996) Kinetics of decreased LPS-stimulated cytokine release by macrophages exposed to CO2. J Surg Res 63:269–274CrossRefPubMed
48.
Jacobs VR, Morrison JE Jr, Mundhenke C, Golombeck K, Jonat W (2000) Intraoperative evaluation of laparoscopic insufflation technique for quality control in the OR. JSLS 4:189–195PubMed
49.
Bessell JR, Ludbrook G, Miljard SH, Baxter PS, Ubhi SS, Maddern GJ (1999) Humidified gas prevents hypothermia induced by laparoscopic insufflation: a randomized controlled study in a pig model. Surg Endosc 13:101–105CrossRefPubMed
50.
Puttick MI, Scott-Coombes DM, Dye J, Nduka CC, Menzies-Gow NM, Mansfield AO, Darzi A (1999) Comparison of immunologic and physiologic effects of CO2 pneumoperitoneum at room and body temperatures. Surg Endosc 13:572–575CrossRefPubMed
51.
Ohzato H, Yoshizaki K, Nishimoto N, Ogata A, Tagoh H, Monden M, Gotoh M, Kishimoto T, Mori T (1992) Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery 111:201–209PubMed
52.
Yao V, Platell C, Hall JC (2004) Peritoneal mesothelial cells produce inflammatory related cytokines. ANZ J Surg 74:997–1002CrossRefPubMed
53.
Liberek T, Topley N, Luttmann W, Williams JD (1996) Adherence of neutrophils to human peritoneal mesothelial cells: role of intercellular adhesion molecule-1. J Am Soc Nephrol 7:208–217PubMed
54.
Brokelman WJ, Holmdahl L, Berstrom M, Falk P, Klinkenbijl JH, Reijnen MM (2007) Peritoneal transforming growth factor beta-1 expression during laparoscopic surgery: a clinical trial. Surg Endosc 21:1537–1541CrossRefPubMed
55.
Kagami S, Kuhara T, Yasutomo K, Okada K, Loster K, Reutte W, Kuroda Y (1996) Transforming growth factor-beta (TGF-beta) stimulates the expression of beta1 integrins and adhesion by rat mesangial cells. Exp Cell Res 229:1–6CrossRefPubMed
56.
Ignotz RA, Massague J (1987) Cell adhesion protein receptors as targets for transforming growth factor-beta action. Cell 51:189–197CrossRefPubMed
57.
Duron JJ (2007) Postoperative intraperitoneal adhesion pathophysiology. Colorectal Dis 9(Suppl 2):14–24CrossRefPubMed
58.
Hobson KG, DeWing M, Ho HS, Wolfe BM, Cho K, Greenhalgh DG (2003) Expression of transforming growth factor beta1 in patients with and without previous abdominal surgery. Arch Surg 138:1249–1252CrossRefPubMed
59.
Holmdahl L, Kotseos K, Bergström M, Falk P, Ivarsson ML, Chegini N (2001) Overproduction of transforming growth factor-beta1 (TGF-beta1) is associated with adhesion formation and peritoneal fibrinolytic impairment. Surgery 129:626–632CrossRefPubMed
60.
Freeman ML, Saed GM, Elhammady EF, Diamond MP (2003) Expression of transforming growth factor beta isoform mRNA in injured peritoneum that healed with adhesions and without adhesions and in uninjured peritoneum. Fertil Steril 80(Suppl 2):708–713CrossRefPubMed
61.
Sendt W, Amberg R, Schöffel U, Hassan A, von Specht BU, Farthmann EH (1999) Local inflammatory peritoneal response to operative trauma: studies on cell activity, cytokine expression, and adhesion molecules. Eur J Surg 165:1024–1030CrossRefPubMed
62.
Molinas CR, Binda MM, Carmeliet P, Koninckx PR (2004) 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 82(Suppl 3):1149–1153CrossRefPubMed
63.
Holmdahl L, Eriksson E, al Jabreen M, Risberg B (1996) Fibrinolysis in human peritoneum during operation. Surgery 119:701–705CrossRefPubMed
64.
Scott-Coombes DM, Whawell SA, Thompson JN (1995) The operative peritoneal fibrinolytic response to abdominal operation. Eur J Surg 161:395–399PubMed
65.
Ivarsson ML, Falk P, Holmdahl L (2001) Response of visceral peritoneum to abdominal surgery. Br J Surg 88:148–151CrossRefPubMed
66.
Ziprin P, Ridgway PF, Peck DH, Darzi AW (2003) Laparoscopic-type environment enhances mesothelial cell fibrinolytic activity in vitro via a downregulation of plasminogen activator inhibitor-1 activity. Surgery 134:758–765CrossRefPubMed
67.
Bergström M, Falk P, Holmdahl L (2003) CO2 promotes plasminogen activator inhibitor type 1 expression in human mesothelial cells. Surg Endosc 17:1818–1822CrossRefPubMed
68.
Molinas CR, Elkelani O, Campo R, Luttun A, Carmeliet P, Koninckx PR (2003) Role of the plasminogen system in basal adhesion formation and carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in transgenic mice. Fertil Steril 80:184–192CrossRefPubMed
69.
Nagelschmidt M, Gerbecks D, Minor T (2001) The impact of gas laparoscopy on abdominal plasminogen activator activity. Surg Endosc 15:585–588CrossRefPubMed
70.
Tarhan OR, Barut I, Akdeniz Y, Sutcu R, Cerci C, Bulbul M (2008) Fibrinolytic responses of human peritoneal fluid in laparoscopic cholecystectomy: a prospective clinical study. Surg Endosc 22:1008–1013CrossRefPubMed
71.
Brokelman WJ, Holmdahl L, Bergström M, Falk P, Klinkenbijl JH, Reijnen MM (2006) Peritoneal fibrinolytic response to various aspects of laparoscopic surgery: a randomized trial. J Surg Res 136:309–313CrossRefPubMed
72.
Brokelman WJ, Holmdahl L, Janssen IM, Falk P, Bergström M, Klinkenbijl JH, Reijnen MM (2008) Decreased peritoneal tissue plasminogen activator during prolonged laparoscopic surgery. J Surg Res 151:89–93CrossRefPubMed
73.
Brokelman WJ, Holmdahl L, Bergström M, Falk P, Klinkenbijl JH, Reijnen MM (2007) Heating of carbon dioxide during insufflation alters the peritoneal fibrinolytic response to laparoscopic surgery: a clinical trial. Surg Endosc 5:1232–1236
74.
Bergström M, Ivarsson ML, Holmdahl L (2002) Peritoneal response to pneumoperitoneum and laparoscopic surgery. Br J Surg 89:1465–1469CrossRefPubMed
75.
Neudecker J, Junghans T, Ziemer S, Raue W, Schwenk W (2002) Effect of laparoscopic and conventional colorectal resection on peritoneal fibrinolytic capacity: a prospective randomized clinical trial. Int J Colorectal Dis 17:426–429CrossRefPubMed
76.
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
77.
Strobel T, Cannistra SA (1999) Beta1-integrins partly mediate binding of ovarian cancer cells to peritoneal mesothelium in vitro. Gynecol Oncol 73:362–367CrossRefPubMed
78.
Metadata
Title
Peritoneal changes due to laparoscopic surgery
Authors
W. J. A. Brokelman
M. Lensvelt
I. H. M. Borel Rinkes
J. H. G. Klinkenbijl
M. M. P. J. Reijnen
Publication date
01-01-2011
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 1/2011
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-010-1139-2

Other articles of this Issue 1/2011

Surgical Endoscopy 1/2011 Go to the issue

OriginalPaper

Maximizing coupling strength of magnetically anchored surgical instruments: how thick can we go?

OriginalPaper

A collaborative approach reduces the learning curve and improves outcomes in laparoscopic nephrectomy

OriginalPaper

Laparoscopic treatment of intestinal malrotation in neonates and infants: retrospective study

OriginalPaper

Dexterous miniature robot for advanced minimally invasive surgery

OriginalPaper

Laparoscopic resection for rectal cancer: a case-matched study

OriginalPaper

Effects of preemptive analgesia in laparoscopic cholecystectomy: a double-blind randomized controlled trial