Skip to main content
Top
Published in: BMC Surgery 1/2011

Open Access 01-12-2011 | Research article

Severe inflammatory reaction induced by peritoneal trauma is the key driving mechanism of postoperative adhesion formation

Authors: Sergei V Pismensky, Zhomart R Kalzhanov, Marina Yu Eliseeva, Ioannis P Kosmas, Ospan A Mynbaev

Published in: BMC Surgery | Issue 1/2011

Login to get access

Abstract

Background

Many factors have been put forward as a driving mechanism of surgery-triggered adhesion formation (AF). In this study, we underline the key role of specific surgical trauma related with open surgery (OS) and laparoscopic (LS) conditions in postoperative AF and we aimed to study peritoneal tissue inflammatory reaction (TIR), remodelling specific complications of open surgery (OS) versus LS and subsequently evaluating AF induced by these conditions.

Methods

A prospective randomized study was done in 80 anaesthetised female Wistar rats divided equally into 2 groups. Specific traumatic OS conditions were induced by midline incision line (MIL) extension and tissue drying and specific LS conditions were remodelled by intraperitoneal CO2 insufflation at the 10 cm of water. TIR was evaluated at the 24th, 72nd, 120th and 168th hour by scoring scale. Statistical analysis was performed by the non-parametric t test and two-way ANOVA using Bonferroni post-tests.

Results

More pronounced residual TIR was registered after OS than after LS. There were no significant TIR interactions though highly significant differences were observed between the OS and LS groups (p < 0.0001) with regard to surgical and time factors. The TIR change differences between the OS and LS groups were pronounced with postoperative time p < 0.05 at the 24th and 72nd; p < 0.01 - 120th and p < 0.001 - 168th hrs. Adhesion free wounds were observed in 20.0 and 31.0% of cases after creation of OS and LS conditions respectively; with no significant differences between these values (p > 0.05). However larger adhesion size (41.67 ± 33.63) was observed after OS in comparison with LS (20.31 ± 16.38). The upper-lower 95% confidential limits ranged from 60.29 to 23.04 and from 29.04 to 11.59 respectively after OS and LS groups with significant differences (p = 0.03). Analogous changes were observed in adhesion severity values. Subsequently, severe TIR parameters were followed by larger sizes of severe postoperative adhesions in the OS group than those observed in the LS group.

Conclusions

MIL extension and tissue drying seem to be the key factors in the pathogenesis of adhesion formation, triggering severe inflammatory reactions of the peritoneal tissue surrounding the MIL resulting in local and systemic consequences. CO2 insufflation however, led to moderate inflammation and less adhesion formation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Al-Jaroudi D, Tulandi T: Adhesion prevention in gynecologic surgery. Obstet Gynecol Surv. 2004, 59 (5): 360-367. 10.1097/00006254-200405000-00024.CrossRefPubMed Al-Jaroudi D, Tulandi T: Adhesion prevention in gynecologic surgery. Obstet Gynecol Surv. 2004, 59 (5): 360-367. 10.1097/00006254-200405000-00024.CrossRefPubMed
2.
go back to reference Baakdah H, Tulandi T: Adhesion in gynecology complication, cost, and prevention: a review. Surg Technol Int. 2005, 14: 185-90.PubMed Baakdah H, Tulandi T: Adhesion in gynecology complication, cost, and prevention: a review. Surg Technol Int. 2005, 14: 185-90.PubMed
3.
go back to reference Parker MC, Wilson MS, van Goor H, Moran BJ, Jeekel J, Duron JJ, Menzies D, Wexner SD, Ellis H: Adhesions and colorectal surgery - call for action. Colorectal Dis. 2007, 9 (Suppl 2): 66-72.CrossRefPubMed Parker MC, Wilson MS, van Goor H, Moran BJ, Jeekel J, Duron JJ, Menzies D, Wexner SD, Ellis H: Adhesions and colorectal surgery - call for action. Colorectal Dis. 2007, 9 (Suppl 2): 66-72.CrossRefPubMed
4.
go back to reference Sileri P, Sthory R, McVeigh E, Child T, Cunningham C, Mortensen NJ, Lindsey I: Adhesions are common and costly after open pouch surgery. J Gastrointest Surg. 2008, 12 (7): 1239-45. 10.1007/s11605-008-0481-3.CrossRefPubMed Sileri P, Sthory R, McVeigh E, Child T, Cunningham C, Mortensen NJ, Lindsey I: Adhesions are common and costly after open pouch surgery. J Gastrointest Surg. 2008, 12 (7): 1239-45. 10.1007/s11605-008-0481-3.CrossRefPubMed
5.
go back to reference van Goor H: Consequences and complications of peritoneal adhesions. Colorectal Dis. 2007, 9 (Suppl 2): 25-34.CrossRefPubMed van Goor H: Consequences and complications of peritoneal adhesions. Colorectal Dis. 2007, 9 (Suppl 2): 25-34.CrossRefPubMed
6.
go back to reference Ahmad G, Duffy JM, Farquhar C, Vail A, Vandekerckhove P, Watson A, Wiseman D: Barrier agents for adhesion prevention after gynaecological surgery. Cochrane Database Syst Rev. 2008, CD000475-2 Ahmad G, Duffy JM, Farquhar C, Vail A, Vandekerckhove P, Watson A, Wiseman D: Barrier agents for adhesion prevention after gynaecological surgery. Cochrane Database Syst Rev. 2008, CD000475-2
7.
go back to reference Robertson D, Lefebvre G, Leyland N, Wolfman W, Allaire C, Awadalla A, Best C, Contestabile E, Dunn S, Heywood M, Leroux N, Potestio F, Rittenberg D, Senikas V, Soucy R, Singh S, SOGC: SOGC clinical practice guidelines: Adhesion prevention in gynaecological surgery: no. 243, June 2010. Int J Gynaecol Obstet. 2010, 111 (2): 193-7. 10.1016/j.ijgo.2010.07.002.CrossRefPubMed Robertson D, Lefebvre G, Leyland N, Wolfman W, Allaire C, Awadalla A, Best C, Contestabile E, Dunn S, Heywood M, Leroux N, Potestio F, Rittenberg D, Senikas V, Soucy R, Singh S, SOGC: SOGC clinical practice guidelines: Adhesion prevention in gynaecological surgery: no. 243, June 2010. Int J Gynaecol Obstet. 2010, 111 (2): 193-7. 10.1016/j.ijgo.2010.07.002.CrossRefPubMed
8.
go back to reference Leroy J, Ananian P, Rubino F, Claudon B, Mutter D, Marescaux J: The Impact of Obesity on Technical Feasibility and Postoperative Outcomes of Laparoscopic Left Colectomy. Ann Surg. 2005, 241 (1): 69-76.PubMedPubMedCentral Leroy J, Ananian P, Rubino F, Claudon B, Mutter D, Marescaux J: The Impact of Obesity on Technical Feasibility and Postoperative Outcomes of Laparoscopic Left Colectomy. Ann Surg. 2005, 241 (1): 69-76.PubMedPubMedCentral
9.
go back to reference Lin F, Zhang QJ, Zheng FY, Zhao HQ, Zeng QQ, Zheng MH, Zhu HY: Laparoscopically assisted versus open surgery for endometrial cancer--a meta-analysis of randomized controlled trials. Int J Gynecol Cancer. 2008, 18 (6): 1315-25. 10.1111/j.1525-1438.2007.01180.x.CrossRefPubMed Lin F, Zhang QJ, Zheng FY, Zhao HQ, Zeng QQ, Zheng MH, Zhu HY: Laparoscopically assisted versus open surgery for endometrial cancer--a meta-analysis of randomized controlled trials. Int J Gynecol Cancer. 2008, 18 (6): 1315-25. 10.1111/j.1525-1438.2007.01180.x.CrossRefPubMed
10.
go back to reference Sica GS, Iaculli E, Benavoli D, Biancone L, Calabrese E, Onali S, Gaspari AL: Laparoscopic versus open ileo-colonic resection in Crohn's disease: short- and long-term results from a prospective longitudinal study. J Gastrointest Surg. 2008, 12 (6): 1094-102. 10.1007/s11605-007-0394-6.CrossRefPubMed Sica GS, Iaculli E, Benavoli D, Biancone L, Calabrese E, Onali S, Gaspari AL: Laparoscopic versus open ileo-colonic resection in Crohn's disease: short- and long-term results from a prospective longitudinal study. J Gastrointest Surg. 2008, 12 (6): 1094-102. 10.1007/s11605-007-0394-6.CrossRefPubMed
11.
go back to reference Stumpf M, Klinge U, Tittel A, Brücker C, Schupelick V: The surgical trauma of abdominal wall incision: A comparison of laparoscopic vs open surgery with three-dimensional stereography. Surg Endosc. 2001, 15 (10): 1147-1149. 10.1007/s004640090067.CrossRefPubMed Stumpf M, Klinge U, Tittel A, Brücker C, Schupelick V: The surgical trauma of abdominal wall incision: A comparison of laparoscopic vs open surgery with three-dimensional stereography. Surg Endosc. 2001, 15 (10): 1147-1149. 10.1007/s004640090067.CrossRefPubMed
12.
go back to reference Mynbaev OA, Corona R: Possible mechanisms of peritoneal tissue-oxygen tension changes during CO2-pneumoperitoneum: the role of design, methodology and animal models. Hum Reprod. 2009, 24 (6): 1242-1246. 10.1093/humrep/dep025.CrossRefPubMed Mynbaev OA, Corona R: Possible mechanisms of peritoneal tissue-oxygen tension changes during CO2-pneumoperitoneum: the role of design, methodology and animal models. Hum Reprod. 2009, 24 (6): 1242-1246. 10.1093/humrep/dep025.CrossRefPubMed
13.
go back to reference Hellebrekers BW, Emeis JJ, Kooistra T, Trimbos JB, Moore NR, Zwinderman KH, Trimbos-Kemper TC: A role for the fibrinolytic system in postsurgical adhesion formation. Fertil Steril. 2005, 83 (1): 122-9. 10.1016/j.fertnstert.2004.06.060.CrossRefPubMed Hellebrekers BW, Emeis JJ, Kooistra T, Trimbos JB, Moore NR, Zwinderman KH, Trimbos-Kemper TC: A role for the fibrinolytic system in postsurgical adhesion formation. Fertil Steril. 2005, 83 (1): 122-9. 10.1016/j.fertnstert.2004.06.060.CrossRefPubMed
14.
go back to reference Holmdahl L: The role of fibrinolysis in adhesion formation. Eur J Surg Suppl. 1997, 24-31. 577 Holmdahl L: The role of fibrinolysis in adhesion formation. Eur J Surg Suppl. 1997, 24-31. 577
15.
go back to reference Kece C, Ulas M, Ozer I, Ozel U, Bilgehan A, Aydog G, Dalgic T, Oymaci E, Bostanci B: Carbondioxide pneumoperitoneum prevents postoperative adhesion formation in a rat cecal abrasion model. J Laparoendosc Adv Surg Tech A. 2010, 20 (1): 25-30. 10.1089/lap.2009.0216.CrossRefPubMed Kece C, Ulas M, Ozer I, Ozel U, Bilgehan A, Aydog G, Dalgic T, Oymaci E, Bostanci B: Carbondioxide pneumoperitoneum prevents postoperative adhesion formation in a rat cecal abrasion model. J Laparoendosc Adv Surg Tech A. 2010, 20 (1): 25-30. 10.1089/lap.2009.0216.CrossRefPubMed
16.
go back to reference Ott DE: Laparoscopy and adhesion formation, adhesions and laparoscopy. Semin Reprod Med. 2008, 26 (4): 322-30. 10.1055/s-0028-1082390.CrossRefPubMed Ott DE: Laparoscopy and adhesion formation, adhesions and laparoscopy. Semin Reprod Med. 2008, 26 (4): 322-30. 10.1055/s-0028-1082390.CrossRefPubMed
17.
go back to reference 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 (3): 560-567. 10.1016/S0015-0282(01)01964-1.CrossRefPubMed 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 (3): 560-567. 10.1016/S0015-0282(01)01964-1.CrossRefPubMed
18.
go back to reference Nagelschmidt M, Gerbecks D, Minor T: The impact of gas laparoscopy on abdominal plasminogen activator activity. Surg Endosc. 2001, 15 (6): 585-8. 10.1007/s004640010282.CrossRefPubMed Nagelschmidt M, Gerbecks D, Minor T: The impact of gas laparoscopy on abdominal plasminogen activator activity. Surg Endosc. 2001, 15 (6): 585-8. 10.1007/s004640010282.CrossRefPubMed
19.
go back to reference Winslow ER, Brunt LM: Perioperative outcomes of laparoscopic versus open splenectomy: A meta-analysis with an emphasis on complications. Surgery. 2003, 134 (4): 647-653. 10.1016/S0039-6060(03)00312-X.CrossRefPubMed Winslow ER, Brunt LM: Perioperative outcomes of laparoscopic versus open splenectomy: A meta-analysis with an emphasis on complications. Surgery. 2003, 134 (4): 647-653. 10.1016/S0039-6060(03)00312-X.CrossRefPubMed
20.
go back to reference Chegini N: Peritoneal molecular environment, adhesion formation and clinical implication. Front Biosci. 2002, 7: e91-115. 10.2741/chegini.PubMed Chegini N: Peritoneal molecular environment, adhesion formation and clinical implication. Front Biosci. 2002, 7: e91-115. 10.2741/chegini.PubMed
21.
go back to reference Dijkstra FR, Nieuwenhuijzen M, Reijnen MM, van Goor H: Recent clinical developments in pathophysiology, epidemiology, diagnosis and treatment of intra-abdominal adhesions. Scand J Gastroenterol Suppl. 2000, 52-59. 232 Dijkstra FR, Nieuwenhuijzen M, Reijnen MM, van Goor H: Recent clinical developments in pathophysiology, epidemiology, diagnosis and treatment of intra-abdominal adhesions. Scand J Gastroenterol Suppl. 2000, 52-59. 232
22.
go back to reference Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL: Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Recent advances in prevention and management. Dig Surg. 2001, 18 (4): 260-73. 10.1159/000050149.CrossRefPubMed Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL: Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Recent advances in prevention and management. Dig Surg. 2001, 18 (4): 260-73. 10.1159/000050149.CrossRefPubMed
23.
go back to reference Munireddy S, Kavalukas SL, Barbul A: Intra-abdominal healing: gastrointestinal tract and adhesions. Surg Clin North Am. 2010, 90 (6): 1227-36. 10.1016/j.suc.2010.08.002.CrossRefPubMed Munireddy S, Kavalukas SL, Barbul A: Intra-abdominal healing: gastrointestinal tract and adhesions. Surg Clin North Am. 2010, 90 (6): 1227-36. 10.1016/j.suc.2010.08.002.CrossRefPubMed
24.
go back to reference Mynbaev OA, Adamyan LV, Mailova K, Vanacker B, Koninckx PR: Effects of adding small amounts of oxygen to a carbon dioxide-pneumoperitoneum of increasing pressure in rabbit ventilation models. Fertil Steril. 2009, 92 (2): 778-84. 10.1016/j.fertnstert.2008.07.019. Epub 2008 Sep 27CrossRefPubMed Mynbaev OA, Adamyan LV, Mailova K, Vanacker B, Koninckx PR: Effects of adding small amounts of oxygen to a carbon dioxide-pneumoperitoneum of increasing pressure in rabbit ventilation models. Fertil Steril. 2009, 92 (2): 778-84. 10.1016/j.fertnstert.2008.07.019. Epub 2008 Sep 27CrossRefPubMed
25.
go back to reference Mynbaev OA, Koninckx PR, Bracke M: A possible mechanism of peritoneal pH changes during carbon dioxide pneumoperitoneum. Surg Endosc. 2007, 21 (3): 489-491. 10.1007/s00464-006-9009-7.CrossRefPubMed Mynbaev OA, Koninckx PR, Bracke M: A possible mechanism of peritoneal pH changes during carbon dioxide pneumoperitoneum. Surg Endosc. 2007, 21 (3): 489-491. 10.1007/s00464-006-9009-7.CrossRefPubMed
26.
go back to reference Mynbaev OA, Molinas CR, Adamyan LV, Vanacker B, Koninckx PR: Pathogenesis of CO(2) pneumoperitoneum-induced metabolic hypoxemia in a rabbit model. J Am Assoc Gynecol Laparosc. 2002, 9 (3): 306-314. 10.1016/S1074-3804(05)60409-4.CrossRefPubMed Mynbaev OA, Molinas CR, Adamyan LV, Vanacker B, Koninckx PR: Pathogenesis of CO(2) pneumoperitoneum-induced metabolic hypoxemia in a rabbit model. J Am Assoc Gynecol Laparosc. 2002, 9 (3): 306-314. 10.1016/S1074-3804(05)60409-4.CrossRefPubMed
27.
go back to reference Mynbaev OA, Molinas CR, Adamyan LV, Vanacker B, Koninckx PR: Reduction of CO(2)-pneumoperitoneum-induced metabolic hypoxaemia by the addition of small amounts of O(2) to the CO(2) in a rabbit ventilated model. A preliminary study. Hum Reprod. 2002, 17 (6): 1623-1629. 10.1093/humrep/17.6.1623.CrossRefPubMed Mynbaev OA, Molinas CR, Adamyan LV, Vanacker B, Koninckx PR: Reduction of CO(2)-pneumoperitoneum-induced metabolic hypoxaemia by the addition of small amounts of O(2) to the CO(2) in a rabbit ventilated model. A preliminary study. Hum Reprod. 2002, 17 (6): 1623-1629. 10.1093/humrep/17.6.1623.CrossRefPubMed
28.
go back to reference Miyano G, Yamataka A, Doi T, Okawada M, Takano Y, Kobayashi H, Lane GJ, Miyano T: Carbon dioxide pneumoperitoneum prevents intraperitoneal adhesions after laparotomy in rats. J Pediatr Surg. 2006, 41 (5): 1025-8. 10.1016/j.jpedsurg.2005.12.048.CrossRefPubMed Miyano G, Yamataka A, Doi T, Okawada M, Takano Y, Kobayashi H, Lane GJ, Miyano T: Carbon dioxide pneumoperitoneum prevents intraperitoneal adhesions after laparotomy in rats. J Pediatr Surg. 2006, 41 (5): 1025-8. 10.1016/j.jpedsurg.2005.12.048.CrossRefPubMed
29.
go back to reference Ziprin P, Ridgway PF, Peck DH, Darzi AW: Laparoscopic-type environment enhances mesothelial cell fibrinolytic activity in vitro via a down-regulation of plasminogen activator inhibitor-1 activity. Surgery. 2003, 134 (5): 758-65. 10.1016/S0039-6060(03)00293-9.CrossRefPubMed Ziprin P, Ridgway PF, Peck DH, Darzi AW: Laparoscopic-type environment enhances mesothelial cell fibrinolytic activity in vitro via a down-regulation of plasminogen activator inhibitor-1 activity. Surgery. 2003, 134 (5): 758-65. 10.1016/S0039-6060(03)00293-9.CrossRefPubMed
30.
go back to reference Berretta R, Rolla M, Patrelli TS, Gramellini D, Fadda GM, Nardelli GB: Incidence of port-site metastasis after laparoscopic management of borderline ovarian tumors: a series of 22 patients. Eur J Gynaecol Oncol. 2009, 30 (3): 300-2.PubMed Berretta R, Rolla M, Patrelli TS, Gramellini D, Fadda GM, Nardelli GB: Incidence of port-site metastasis after laparoscopic management of borderline ovarian tumors: a series of 22 patients. Eur J Gynaecol Oncol. 2009, 30 (3): 300-2.PubMed
31.
go back to reference Lundberg O, Kristoffersson A: Pneumoperitoneum impairs blood flow and augments tumor growth in the abdominal wall. Surg Endosc. 2004, 18 (2): 293-6. 10.1007/s00464-003-9035-7.CrossRefPubMed Lundberg O, Kristoffersson A: Pneumoperitoneum impairs blood flow and augments tumor growth in the abdominal wall. Surg Endosc. 2004, 18 (2): 293-6. 10.1007/s00464-003-9035-7.CrossRefPubMed
32.
go back to reference Martínez A, Querleu D, Leblanc E, Narducci F, Ferron G: Low incidence of port-site metastases after laparoscopic staging of uterine cancer. Gynecol Oncol. 2010, 118 (2): 145-50. 10.1016/j.ygyno.2010.03.011.CrossRefPubMed Martínez A, Querleu D, Leblanc E, Narducci F, Ferron G: Low incidence of port-site metastases after laparoscopic staging of uterine cancer. Gynecol Oncol. 2010, 118 (2): 145-50. 10.1016/j.ygyno.2010.03.011.CrossRefPubMed
34.
go back to reference Vergote I, Marquette S, Amant F, Berteloot P, Neven P: Port-site metastases after open laparoscopy: a study in 173 patients with advanced ovarian carcinoma. Int J Gynecol Cancer. 2005, 15 (5): 776-9. 10.1111/j.1525-1438.2005.00135.x.CrossRefPubMed Vergote I, Marquette S, Amant F, Berteloot P, Neven P: Port-site metastases after open laparoscopy: a study in 173 patients with advanced ovarian carcinoma. Int J Gynecol Cancer. 2005, 15 (5): 776-9. 10.1111/j.1525-1438.2005.00135.x.CrossRefPubMed
35.
go back to reference Corona R, Verguts J, Schonman R, Binda MM, Mailova K, Koninckx PR: Postoperative inflammation in the abdominal cavity increases adhesion formation in a laparoscopic mouse model. Fertil Steril. 2011 Corona R, Verguts J, Schonman R, Binda MM, Mailova K, Koninckx PR: Postoperative inflammation in the abdominal cavity increases adhesion formation in a laparoscopic mouse model. Fertil Steril. 2011
Metadata
Title
Severe inflammatory reaction induced by peritoneal trauma is the key driving mechanism of postoperative adhesion formation
Authors
Sergei V Pismensky
Zhomart R Kalzhanov
Marina Yu Eliseeva
Ioannis P Kosmas
Ospan A Mynbaev
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2011
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/1471-2482-11-30

Other articles of this Issue 1/2011

BMC Surgery 1/2011 Go to the issue