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Peritoneal Damage: The Inflammatory Response and Clinical Implications of the Neuro-Immuno-Humoral Axis

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Abstract

Background

The peritoneum is a bilayer serous membrane that lines the abdominal cavity. We present a review of peritoneal structure and physiology, with a focus on the peritoneal inflammatory response to surgical injury and its clinical implications.

Methods

We conducted a nonsystematic clinical review. A search of the Ovid MEDLINE database from 1950 through January 2009 was performed using the following search terms: peritoneum, adhesions, cytokine, inflammation, and surgery.

Results

The peritoneum is a metabolically active organ, responding to insult through a complex array of immunologic and inflammatory cascades. This response increases with the duration and extent of injury and is central to the concept of surgical stress, manifesting via a combination of systemic effects, and local neural pathways via the neuro-immuno-humoral axis. There may be a decreased systemic inflammatory response after minimally invasive surgery; however, it is unclear whether this is due to a reduced local peritoneal reaction.

Conclusions

Interventions that dampen the peritoneal response and/or block the neuro-immuno-humoral pathway should be further investigated as possible avenues of enhancing recovery after surgery, and reducing postoperative complications.

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References

  1. Michailova KN, Usunoff KG (2006) Serosal membranes (pleura, pericardium, peritoneum). Normal structure, development and experimental pathology. Adv Anat Embryol Cell Biol 183:1–144

    Google Scholar 

  2. McMinn R (1994) Last’s anatomy: regional and applied, 9th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  3. Hills B (1992) Graphite-like lubrication of mesothelium by oligolamellar pleural surfactant. J Appl Physiol 73:1034–1039

    CAS  PubMed  Google Scholar 

  4. di Zerega GS (1990) The peritoneum and its response to surgical injury. Prog Clin Biol Res 358:1–11

    CAS  Google Scholar 

  5. Michailova KN (2004) Mesothelial lamellar bodies in norm and experimental conditions. Transmission and scanning electron microscopic observations on the peritoneum, pleura and pericardium. Anat Embryol (Berl) 208:301–309

    CAS  Google Scholar 

  6. Hills BA, Burke JR, Thomas K (1998) Surfactant barrier lining peritoneal mesothelium: lubricant and release agent. Perit Dial Int 18:157–165

    CAS  PubMed  Google Scholar 

  7. Yao V, Platell C, Hall JC (2003) Role of peritoneal mesothelial cells in peritonitis. Br J Surg 90:1187–1194

    CAS  PubMed  Google Scholar 

  8. Heel KA, Hall JC (1996) Peritoneal defences and peritoneum-associated lymphoid tissue. Br J Surg 83:1031–1036

    CAS  PubMed  Google Scholar 

  9. Fujiwara H, Kubota T, Amaike H (2002) Functional analysis of peritoneal lymphoid tissues by GFP expression in mice—possible application for targeting gene therapy against peritoneal dissemination. Gan To Kagaku Ryoho 29:2322–2324

    CAS  PubMed  Google Scholar 

  10. Cruickshank A, Fraser W, Burns H (1990) Response of serum interleukin-6 in patients undergoing elective surgery of varying severity. Clin Sci 79:161–165

    CAS  PubMed  Google Scholar 

  11. van den Tol P, van Rossen E, van Eijck C, Bonthuis F, Marquet R, Jeekel H (1998) Reduction of peritoneal trauma by using nonsurgical gauze leads to less implantation metastasis of spilled tumor cells. Ann Surg 227:242–248

    PubMed  Google Scholar 

  12. Coffey J, Smith M, Wang J, Bouchier-Hayes D, Cotter T, Redmond H (2006) Cancer surgery: risks and opportunities. Bio Essays 28:433–437

    CAS  Google Scholar 

  13. 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

    CAS  PubMed  Google Scholar 

  14. Riese J, Schoolmann S, Denzel C, Herrmann O, Hohenberger W, Haupt W (2002) Effect of abdominal infections on peritoneal and systemic production of interleukin 6 and monocyte chemoattractant protein-1. Shock 17:361–364

    PubMed  Google Scholar 

  15. Goehler L, Gaykema R, Hammack S, Maier S, Watkins L (1998) Interleukin-1 induces c-fos immunoreactivity in primary afferent neurons of the vagus nerve. Brain Res 804:306–310

    CAS  PubMed  Google Scholar 

  16. Maier SF, Goehler LE, Fleshner M, Watkins LR (1998) The role of the vagus nerve in cytokine-to-brain communication. Ann N Y Acad Sci 840:289–300

    CAS  PubMed  Google Scholar 

  17. Grundy D, Al-Chaer ED, Aziz Q, Collins SM, Ke M, Tache Y et al (2006) Fundamentals of neurogastroenterology: basic science. Gastroenterology 130:1391–1411

    CAS  PubMed  Google Scholar 

  18. Sendt W, Amberg R, Schoffel 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 165:1024–1030

    CAS  PubMed  Google Scholar 

  19. Wieczorek M, Dunn AJ (2006) Effect of subdiaphragmatic vagotomy on the noradrenergic and HPA axis activation induced by intraperitoneal interleukin-1 administration in rats. Brain Res 1101:73–84

    CAS  PubMed  Google Scholar 

  20. Marquette C, Linard C, Galonnier M, Van Uye A, Mathieu J, Gourmelon P et al (2003) IL-1beta, TNFalpha and IL-6 induction in the rat brain after partial-body irradiation: role of vagal afferents. Int J Radiat Biol 79:777–785

    CAS  PubMed  Google Scholar 

  21. Fleshner M, Goehler L, Schwartz B (1998) Thermogenic and corticosterone responses (IL-1 beta and TNF-alpha) are attenuated by subdiaphragmatic vagotomy. J Neuroimmunol 86:134–141

    CAS  PubMed  Google Scholar 

  22. Wieczorek M, Swiergiel AH, Pournajafi-Nazarloo H, Dunn AJ (2005) Physiological and behavioral responses to interleukin-1beta and LPS in vagotomized mice. Physiol Behav 85:500–511

    CAS  PubMed  Google Scholar 

  23. Chuang D, Paddison J, Booth R, Hill A (2006) Differential production of cytokines following colorectal surgery. ANZ J Surg 76:821–824

    PubMed  Google Scholar 

  24. 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

    PubMed  Google Scholar 

  25. Bertram P, Junge K, Schachtrupp A, Gotze C, Kunz D, Schumpelick V (2003) Peritoneal release of TNFalpha and IL-6 after elective colorectal surgery and anastomotic leakage. J Invest Surg 16:65–69

    CAS  PubMed  Google Scholar 

  26. Paddison JS, Booth RJ, Fuchs D, Hill AG (2008) Peritoneal inflammation and fatigue experiences following colorectal surgery: a pilot study. Psychoneuroendocrinology 33:446–454

    PubMed  Google Scholar 

  27. Zargar-Shoshtari K, Sammour T, Kahokehr A, Connolly A, Hill A (2009) Double-blind randomised controlled trial of the influence of dexamethasone on post-operative recovery following colectomy. Br J Surg 96:1253–1261

    CAS  PubMed  Google Scholar 

  28. Lepner U, Goroshina J, Samarutel J (2003) Postoperative pain relief after laparoscopic cholecystectomy: a randomised prospective double-blind clinical trial. Scand J Surg 92:121–124

    CAS  PubMed  Google Scholar 

  29. Palmes D, Rottgermann S, Classen C, Haier J, Horstmann R (2007) Randomized clinical trial of the influence of intraperitoneal local anaesthesia on pain after laparoscopic surgery. Br J Surg 94:824–832

    CAS  PubMed  Google Scholar 

  30. Chundrigar T, Hedges AR, Morris R, Stamatakis JD (1993) Intraperitoneal bupivacaine for effective pain relief after laparoscopic cholecystectomy. Ann R Coll Surg Engl 75:437–439

    CAS  PubMed  Google Scholar 

  31. Labaille T, Mazoit JX, Paqueron X, Franco D, Benhamou D (2002) The clinical efficacy and pharmacokinetics of intraperitoneal ropivacaine for laparoscopic cholecystectomy. Anesth Analg 94:100–105

    CAS  PubMed  Google Scholar 

  32. Maestroni U, Sortini D, Devito C, Pour Morad Kohan Brunaldi F, Anania G, Pavanelli L et al (2002) A new method of preemptive analgesia in laparoscopic cholecystectomy. Surg Endosc 16:1336–1340

    CAS  PubMed  Google Scholar 

  33. Paulson J, Mellinger J, Baguley W (2003) The use of intraperitoneal bupivacaine to decrease the length of stay in elective laparoscopic cholecystectomy patients. Am Surg 69:275–279

    PubMed  Google Scholar 

  34. Marret E, Rolin M, Beaussier M, Bonnet F (2008) Meta-analysis of intravenous lidocaine and postoperative recovery after abdominal surgery. Br J Surg 95:1331–1338

    CAS  PubMed  Google Scholar 

  35. Boddy AP, Mehta S, Rhodes M (2006) The effect of intraperitoneal local anesthesia in laparoscopic cholecystectomy: a systematic review and meta-analysis. Anesth Analg 103:682–688

    CAS  PubMed  Google Scholar 

  36. Zhitniuk RI, Kataeva GA (1969) [Prevention of postoperative intestinal paralysis by injection of novocain into the abdominal cavity]. Vestn Khir Im I I Grek 103:50–53

    CAS  PubMed  Google Scholar 

  37. Rimback G, Cassuto J, Faxen A, Hogstrom S, Wallin G, Tollesson PO (1986) Effect of intra-abdominal bupivacaine instillation on postoperative colonic motility. Gut 27:170–175

    CAS  PubMed  Google Scholar 

  38. Pasqualucci A, Contardo R, Da Broi U, Colo F, Terrosu G, Donini A et al (1997) The effects of intraperitoneal local anesthetic on analgesic requirements and endocrine response after laparoscopic cholecystectomy: a randomized double-blind controlled study. J Laparoendosc Surg 4:405–412

    Google Scholar 

  39. Zhitniuk RI, Kataeva GA (1974) [Intraperitoneal infusions of novocaine after laparotomies for the prevention of intraperitoneal adhesions]. Khirurgiia (Mosk) 67–69

  40. Toropov ID (1977) [Intraperitoneal administration of fibrinolysin, hydrocortisone and novocaine for the prevention of recurrences of adhesive obstruction of the intestines]. Klin Khir 63–66

  41. Hau T, Hoffman R, Simmons RL (1978) Mechanisms of the adjuvant effect of hemoglobin in experimental peritonitis. I. In vivo inhibition of peritoneal leukocytosis. Surgery 83:223–229

    CAS  PubMed  Google Scholar 

  42. Allen L (1936) The peritoneal stomata. Anat Rec 67:89

    Google Scholar 

  43. Higgins J, Beaver M, Lemon W (1990) Phrenic neurectomy and peritoneal absorption. Am J Anat 45:137

    Google Scholar 

  44. Florey H (1927) Reactions of, and absorption by, lymphatics, with special reference to those of the diaphragm. Br J Ex Pathol 8:479

    Google Scholar 

  45. Fukatsu K, Saito H, Han I, Inoue T, Furukawa S, Matsuda T et al (1999) Concomitant increase in neutrophil adhesion to inflammatory peritoneum and remote organs during peritonitis. J Surg Res 81:156–163

    CAS  PubMed  Google Scholar 

  46. Mizgerd JP, Kubo H, Kutkoski GJ, Bhagwan SD, Scharffetter-Kochanek K, Beaudet AL et al (1997) Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice. J Exp Med 186:1357–1364

    CAS  PubMed  Google Scholar 

  47. Oghiso Y, Yamada Y, Shibata Y (1992) Exudation of proliferative macrophages in local inflammation in the peritoneum. J Leukoc Biol 52:421–424

    CAS  PubMed  Google Scholar 

  48. Robson RL, McLoughlin RM, Witowski J, Loetscher P, Wilkinson TS, Jones SA et al (2001) Differential regulation of chemokine production in human peritoneal mesothelial cells: IFN-gamma controls neutrophil migration across the mesothelium in vitro and in vivo. J Immunol 167:1028–1038

    CAS  PubMed  Google Scholar 

  49. Bosse R, Vestweber D (1994) Only simultaneous blocking of the L- and P-selectin completely inhibits neutrophil migration into mouse peritoneum. Eur J Immunol 24:3019–3024

    CAS  PubMed  Google Scholar 

  50. Jongstra-Bilen J, Misener VL, Wang C, Ginzberg H, Auerbach A, Joyner AL et al (2000) LSP1 modulates leukocyte populations in resting and inflamed peritoneum. Blood 96:1827–1835

    CAS  PubMed  Google Scholar 

  51. Borges E, Eytner R, Moll T, Steegmaier M, Campbell MA, Ley K et al (1997) The P-selectin glycoprotein ligand-1 is important for recruitment of neutrophils into inflamed mouse peritoneum. Blood 90:1934–1942

    CAS  PubMed  Google Scholar 

  52. Wickel DJ, Mercer-Jones M, Peyton JC, Shrotri MS, Cheadle WG (1998) Neutrophil migration into the peritoneum is P-selectin dependent, but sequestration in lungs is selectin independent during peritonitis. Shock 10:265–269

    CAS  PubMed  Google Scholar 

  53. Scott MJ, Cheadle WG, Hoth JJ, Peyton JC, Subbarao K, Shao WH et al (2004) Leukotriene B4 receptor (BLT-1) modulates neutrophil influx into the peritoneum but not the lung and liver during surgically induced bacterial peritonitis in mice. Clin Diagn Lab Immunol 11:936–941

    CAS  PubMed  Google Scholar 

  54. Sendt W, Wolff-Vorbeck G, Leipziger J, von Specht BU, Schoffel U (2000) In vitro peritonitis: basic inflammatory reactions in a two-chamber coculture model of human peritoneum. Int J Colorectal Dis 15:229–235

    CAS  PubMed  Google Scholar 

  55. Fukatsu K, Saito H, Han I (1996) The greater omentum is the primary site of neutrophil exudation in peritonitis. J Am Coll Surg 183:450

    CAS  PubMed  Google Scholar 

  56. Fukatsu K, Saito H, Han I (1997) Nitric oxide inhibition decreases neutrophil adhesion at the inflammatory site, while increasing adhesion in remote organs in peritonitis. J Surg Res 68:79

    CAS  PubMed  Google Scholar 

  57. Fukatsu K, Saito H, Han I, Furukawa S, Lin MT, Matsuda T et al (1998) Nitric oxide donor decreases neutrophil adhesion in both lung and peritoneum during peritonitis. J Surg Res 74:119–124

    CAS  PubMed  Google Scholar 

  58. Sasaki K (1999) Abdominal peritoneum as a defense organ: analysis of ICAM-1 expression in the LPS-stimulated rat. Clin Anat 12:20–26

    CAS  PubMed  Google Scholar 

  59. Mitra R, Dharajiya N, Kumari L, Varalakshmi C, Khar A (2004) Migration of antigen presenting cells from periphery to the peritoneum during an inflammatory response: role of chemokines and cytokines. FASEB J 18:1764–1766

    CAS  PubMed  Google Scholar 

  60. Valle MT, Degl’Innocenti ML, Bertelli R, Facchetti P, Perfumo F, Fenoglio D et al (1995) Antigen-presenting function of human peritoneum mesothelial cells. Clin Exp Immunol 101:172–176

    CAS  PubMed  Google Scholar 

  61. Brodsky JA, Brody FJ, Endlich B, Armstrong DA, Ponsky JL, Hamilton IA (2002) MCP-1 is highly expressed in peritoneum following midline laparotomy with peritoneal abrasion in a murine model. Surg Endosc 16:1079–1082

    CAS  PubMed  Google Scholar 

  62. 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

    CAS  PubMed  Google Scholar 

  63. Zeillemaker AM, Mul FP, Van Papendrecht AA, Leguit P, Verbrugh HA, Roos D (1996) Limited influence of the mesothelium on the influx of monocytes into the peritoneal cavity. Inflammation 20:87–95

    CAS  PubMed  Google Scholar 

  64. Glik A, Douvdevani A (2006) T lymphocytes: the “cellular” arm of acquired immunity in the peritoneum. Perit Dial Int 26:438–448

    CAS  PubMed  Google Scholar 

  65. Hartmann J, MaaBen V, Rieber P, Fricke H (1995) T lymphocytes from normal human peritoneum are phenotypically different from their counterparts in peripheral blood and CD3-lymphocyte subsets contain mRNA for the recombination activating gene RAG-1. Eur J Immunol 25:2626–2631

    CAS  Google Scholar 

  66. Cannistra SA, Ottensmeier C, Tidy J, DeFranzo B (1994) Vascular cell adhesion molecule-1 expressed by peritoneal mesothelium partly mediates the binding of activated human T lymphocytes. Exp Hematol 22:996–1002

    CAS  PubMed  Google Scholar 

  67. Birkhofer A, Rehbock J, Fricke H (1996) T lymphocytes from the normal human peritoneum contain high frequencies of Th2-type CD8+ T cells. Eur J Immunol 26:957–960

    CAS  PubMed  Google Scholar 

  68. Cong Y, Weaver C, Lazenby A (2002) Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J Immunol 169:6112–6119

    CAS  PubMed  Google Scholar 

  69. Watanabe T, Yamori M, Kita T (2005) CD4+CD25+ T cells regulate colonic localization of CD4 T cells reactive to microbial antigen. Inflamm Bowel Dis 11:541–550

    PubMed  Google Scholar 

  70. Zantl N, Uebe A, Neumann B (1998) Essential role of gamma interferon in survival of colon ascendens stent peritonitis, a novel murine model of abdominal sepsis. Infect Immun 66:2300–2309

    CAS  PubMed  Google Scholar 

  71. Xia M, Gasser J, Feige U (1999) Dexamethasone enhances CTLA-4 expression during T cell activation. Cell Mol Life Sci 55:1649–1656

    CAS  PubMed  Google Scholar 

  72. Busse M, Traeger T, Pötschke C (2008) Detrimental role for CD4+ T lymphocytes in murine diffuse peritonitis due to inhibition of local bacterial elimination. Gut 57:188–195

    CAS  PubMed  Google Scholar 

  73. Stoermann B, Kretschmer K, Duber S, Weiss S (2007) B-1a cells are imprinted by the microenvironment in spleen and peritoneum. Eur J Immunol 37:1613–1620

    CAS  PubMed  Google Scholar 

  74. Berberich S, Dahne S, Schippers A, Peters T, Muller W, Kremmer E et al (2008) Differential molecular and anatomical basis for B cell migration into the peritoneal cavity and omental milky spots. J Immunol 180:2196–2203

    CAS  PubMed  Google Scholar 

  75. Mercolino TJ, Arnold LW, Hawkins LA, Haughton G (1988) Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline. Relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J Exp Med 168:687–698

    CAS  PubMed  Google Scholar 

  76. Rabson A, Roitt I, Delves P (eds) (2004) Really essential medical immunology (essentials), 2nd edn. Wiley Blackwell, Oxford

    Google Scholar 

  77. Sayers T, Mason L, Wiltrout T (1990) Trafficking and activation of murine natural killer cells: differing roles for IFN-T and IL-2. Cell Immunol 127:311–316

    CAS  PubMed  Google Scholar 

  78. Lovik G, Vaage JT, Naper C, Benestad HB, Rolstad B (1995) Recruitment of alloreactive natural killer cells to the rat peritoneum by a transfected cell line secreting rat recombinant interleukin-2. J Immunol Methods 179:59–69

    CAS  PubMed  Google Scholar 

  79. Hau T (1990) Bacteria, toxins, and the peritoneum. World J Surg 14:167–175

    CAS  PubMed  Google Scholar 

  80. Baigrie R, Lamont P, Kwiatkowski D (1992) Systemic cytokine response after major surgery. Br J Surg 19:757–760

    Google Scholar 

  81. Alonso J, Miguel LSD, Monton M (1997) Endothelial cytosolic proteins bind to the 3-untranslated region of endothelial nitric oxide synthase mRNA: regulation by tumor necrosis factor alpha. Mol Cell Biol 17:5719–5726

    CAS  PubMed  Google Scholar 

  82. Arriero MM, Rodriguez-Feo JA, Celdran A, Sanchez de Miguel L, Gonzalez-Fernandez F, Fortes J et al (2000) Expression of endothelial nitric oxide synthase in human peritoneal tissue: regulation by Escherichia coli lipopolysaccharide. J Am Soc Nephrol 11:1848–1856

    CAS  PubMed  Google Scholar 

  83. Sido B, Teklote JR, Hartel M, Friess H, Buchler MW (2004) Inflammatory response after abdominal surgery. Best Pract Res Clin Anaesthesiol 18:439–454

    CAS  PubMed  Google Scholar 

  84. Itoh Y, Joh T, Tanida S (2005) IL-8 promotes cell proliferation and migration through metalloproteinase-cleavage proHB-EGF in human colon carcinoma cells. Cytokine 29:275–282

    CAS  PubMed  Google Scholar 

  85. Tsukada K, Katoh H, Shiojima M, Suzuki T, Takenoshita S, Nagamachi Y (1993) Concentrations of cytokines in peritoneal fluid after abdominal surgery. Eur J Surg 159:475–479

    CAS  PubMed  Google Scholar 

  86. Lin E, Calvano SE, Lowry SF (2000) Inflammatory cytokines and cell response in surgery. Surgery 127:117–126

    CAS  PubMed  Google Scholar 

  87. Tracey K, Fong Y, Hesse D (1987) Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature 330:662–664

    CAS  PubMed  Google Scholar 

  88. Hinshaw L, Tekamp-Olson P, Chang A (1990) Survival of primates in LD100 septic shock following therapy with antibody to tumor necrosis factor (TNF alpha). Circ Shock 30:279–292

    CAS  PubMed  Google Scholar 

  89. Eskandari M, Bolgos G, Miller C (1992) Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia. J Immunol 148:2724–2730

    CAS  PubMed  Google Scholar 

  90. Alexander H, Sheppard B, Jensen J (1991) Treatment with recombinant human tumor necrosis factor-alpha protects rats against the lethality, hypotension, and hypothermia of gram-negative sepsis. J Clin Invest 88:34–39

    CAS  PubMed  Google Scholar 

  91. Matthiessen P, Strand I, Jansson K, Tornquist C, Andersson M, Rutegard J et al (2007) Is early detection of anastomotic leakage possible by intraperitoneal microdialysis and intraperitoneal cytokines after anterior resection of the rectum for cancer? Dis Colon Rectum 50:1918–1927

    PubMed  Google Scholar 

  92. Margetts PJ, Kolb M, Yu L, Hoff CM, Holmes CJ, Anthony DC et al (2002) Inflammatory cytokines, angiogenesis, and fibrosis in the rat peritoneum. Am J Pathol 160:2285–2294

    CAS  PubMed  Google Scholar 

  93. Ladero Quesada JM (2004) Role of the peritoneum in the pathogenesis of acute pancreatitis-associated lung injury. Rev Esp Enferm Dig 96:521–526

    Article  CAS  PubMed  Google Scholar 

  94. Stadlmann S, Raffeiner R, Amberger A, Margreiter R, Zeimet AG, Abendstein B et al (2003) Disruption of the integrity of human peritoneal mesothelium by interleukin-1beta and tumor necrosis factor-alpha. Virchows Arch 443:678–685

    CAS  PubMed  Google Scholar 

  95. Stadlmann S, Pollheimer J, Renner K, Zeimet AG, Offner FA, Amberger A (2006) Response of human peritoneal mesothelial cells to inflammatory injury is regulated by interleukin-1beta and tumor necrosis factor-alpha. Wound Repair Regen 14:187–194

    PubMed  Google Scholar 

  96. Sakamoto K, Arakawa H, Mita S (1994) Elevation of circulating interleukin 6 after surgery: factors influencing the serum level. Cytokine 6:181–186

    CAS  PubMed  Google Scholar 

  97. Riese J, Niedobitek G, Lisner R, Jung A, Hohenberger W, Haupt W (2004) Expression of interleukin-6 and monocyte chemoattractant protein-1 by peritoneal sub-mesothelial cells during abdominal operations. J Pathol 202:34–40

    CAS  PubMed  Google Scholar 

  98. Greca FH, Souza Filho ZA, Giovanini A, Camargo Junior CA, Rubin MR, Silva RF (2007) Interleukin-6 (IL-6) influence on colonic anastomosis healing in rats. Acta Cir Bras 22:110–114

    PubMed  Google Scholar 

  99. van der Poll T, Marchant A, Buurman W (1995) Endogenous IL-10 protects mice from death during septic peritonitis. J Immunol 155:5397–5401

    PubMed  Google Scholar 

  100. Kato T, Murata A, Ishida H (1995) Interleukin-10 reduces mortality from severe peritonitis in mice. Antimicrob Agents Chemother 39:1336–1340

    CAS  PubMed  Google Scholar 

  101. Fegan KS, Rae MT, Critchley HO, Hillier SG (2008) Anti-inflammatory steroid signalling in the human peritoneum. J Endocrinol 196:369–376

    CAS  PubMed  Google Scholar 

  102. Holmdahl L, Kotseos K, Bergstrom 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 129:626–632

    CAS  PubMed  Google Scholar 

  103. van der Wal JB, Jeekel J (2007) Biology of the peritoneum in normal homeostasis and after surgical trauma. Colorectal Dis 9(Suppl 2):9–13

    PubMed  Google Scholar 

  104. Chegini N, Rossi MJ, Schultz GS, Dunn WA, Masterson BJ (1993) Cellular distribution of epidermal growth factor, transforming growth factor-alpha, and epidermal growth factor receptor in fascia and peritoneum during healing in the rat: an autoradiographic and immunohistochemical study. Wound Repair Regen 1:28–40

    CAS  PubMed  Google Scholar 

  105. Saed GM, Zhang W, Diamond MP (2001) Molecular characterization of fibroblasts isolated from human peritoneum and adhesions. Fertil Steril 75:763–768

    CAS  PubMed  Google Scholar 

  106. Rout UK, Saed GM, Diamond MP (2005) Expression pattern and regulation of genes differ between fibroblasts of adhesion and normal human peritoneum. Reprod Biol Endocrinol 3:1

    PubMed  Google Scholar 

  107. Fukasawa M, Yanagihara DL, Rodgers KE, DiZerega GS (1989) The mitogenic activity of peritoneal tissue repair cells: control by growth factors. J Surg Res 47:45–51

    CAS  PubMed  Google Scholar 

  108. Margetts PJ, Kolb M, Galt T, Hoff CM, Shockley TR, Gauldie J (2001) Gene transfer of transforming growth factor-beta1 to the rat peritoneum: effects on membrane function. J Am Soc Nephrol 12:2029–2039

    CAS  PubMed  Google Scholar 

  109. Wallwiener D, Meyer A, Bastert G (1998) Adhesion formation of the parietal and visceral peritoneum: an explanation for the controversy on the use of autologous and alloplastic barriers? Fertil Steril 69:132–137

    CAS  PubMed  Google Scholar 

  110. Wilkosz S, Epstein J, de Giorgio-Miller A, McLean W, Ireland G, Herrick S (2008) Remodelling of adipose tissue during experimental omental adhesion formation. Br J Surg 95:387–396

    CAS  PubMed  Google Scholar 

  111. Muller SA, Treutner KH, Tietze L, Anurov M, Titkova S, Polivoda M et al (2001) Influence of intraperitoneal phospholipid dosage on adhesion formation and wound healing at different intervals after surgery. Langenbecks Arch Surg 386:278–284

    CAS  PubMed  Google Scholar 

  112. Thompson J (1998) Pathogenesis and prevention of adhesion formation. Dig Surg 15:153–157

    CAS  PubMed  Google Scholar 

  113. Diamond MP, El-Hammady E, Wang R, Saed G (2002) Metabolic regulation of collagen I in fibroblasts isolated from normal peritoneum and adhesions by dichloroacetic acid. Am J Obstet Gynecol 187:1456–1461

    CAS  PubMed  Google Scholar 

  114. Diamond MP, El-Hammady E, Wang R, Saed G (2004) Regulation of matrix metalloproteinase-1 and tissue inhibitor of matrix metalloproteinase-1 by dichloroacetic acid in human fibroblasts from normal peritoneum and adhesions. Fertil Steril 81:185–190

    CAS  PubMed  Google Scholar 

  115. de Jonge W, van Den Wijngaard R, The F (2003) Postoperative ileus is maintained by intestinal immune infiltrates that activate inhibitory neural pathways in mice. Gastroenterology 125:1137–1147

    PubMed  Google Scholar 

  116. DeCherney AH, di Zerega GS (1997) Clinical problem of intraperitoneal postsurgical adhesion formation following general surgery and the use of adhesion prevention barriers. Surg Clin North Am 77:671–688

    CAS  PubMed  Google Scholar 

  117. Epstein JC, Wilson MS, Wilkosz S, Ireland G, O’Dwyer ST, Herrick SE (2006) Human peritoneal adhesions show evidence of tissue remodeling and markers of angiogenesis. Dis Colon Rectum 49:1885–1892

    PubMed  Google Scholar 

  118. Herrick SE, Mutsaers SE, Ozua P, Sulaiman H, Omer A, Boulos P et al (2000) Human peritoneal adhesions are highly cellular, innervated, and vascularized. J Pathol 192:67–72

    CAS  PubMed  Google Scholar 

  119. Thompson J (ed) (2000) Peritoneal fibrinolysis and adhesion formation. Springer, New York

    Google Scholar 

  120. Jones P, Werb Z (1980) Degradation of connective tissue matrices by macrophages. II. Influence of matrix composition on proteolysis of glycoproteins, elastin, and collagen by macrophages in culture. J Exp Med 152:1527–1536

    CAS  PubMed  Google Scholar 

  121. van der Poll T, Levi M, Buller H (1991) Fibrinolytic response to tumor necrosis factor in healthy subjects. J Exp Med 174:729–732

    PubMed  Google Scholar 

  122. Merlo G, Fausone G, Castagna B (1983) Fibrinolytic activity of mesothelial lining of the displaced peritoneum. Am J Med Sci 286:12–14

    CAS  PubMed  Google Scholar 

  123. Whitaker D, Papadimitriou JM, Walters M (1982) The mesothelium: its fibrinolytic properties. J Pathol 136:291–299

    CAS  PubMed  Google Scholar 

  124. Vipond MN, Whawell SA, Thompson JN, Dudley HA (1990) Peritoneal fibrinolytic activity and intra-abdominal adhesions. Lancet 335:1120–1122

    CAS  PubMed  Google Scholar 

  125. Whawell SA, Scott-Coombes DM, Vipond MN, Tebbutt SJ, Thompson JN (1994) Tumour necrosis factor-mediated release of plasminogen activator inhibitor 1 by human peritoneal mesothelial cells. Br J Surg 81:214–216

    CAS  PubMed  Google Scholar 

  126. Ivarsson ML, Falk P, Holmdahl L (2001) Response of visceral peritoneum to abdominal surgery. Br J Surg 88:148–151

    CAS  PubMed  Google Scholar 

  127. Cohen PA, Gower AC, Stucchi AF, Leeman SE, Becker JM, Reed KL (2007) A neurokinin-1 receptor antagonist that reduces intraabdominal adhesion formation increases peritoneal matrix metalloproteinase activity. Wound Repair Regen 15:800–808

    PubMed  Google Scholar 

  128. Bhardwaj R, Parker MC (2007) Impact of adhesions in colorectal surgery. Colorectal Dis 9(Suppl 2):45–53

    PubMed  Google Scholar 

  129. Harris DA, Topley N (2008) Peritoneal adhesions. Br J Surg 95:271–272

    CAS  PubMed  Google Scholar 

  130. Fukuda H, Tsuchida D, Koda K, Miyazaki M, Pappas TN, Takahashi T (2007) Inhibition of sympathetic pathways restores postoperative ileus in the upper and lower gastrointestinal tract. J Gastroenterol Hepatol 22:1293–1299

    PubMed  Google Scholar 

  131. Artinyan A, Nunoo-Mensah JW, Balasubramaniam S, Gauderman J, Essani R, Gonzalez-Ruiz C et al (2008) Prolonged postoperative ileus-definition, risk factors, and predictors after surgery. World J Surg 32:1495–1500

    PubMed  Google Scholar 

  132. Wolff BG, Viscusi ER, Delaney CP, Du W, Techner L (2007) Patterns of gastrointestinal recovery after bowel resection and total abdominal hysterectomy: pooled results from the placebo arms of alvimopan phase III North American clinical trials. J Am Coll Surg 205:43–51

    PubMed  Google Scholar 

  133. Maron DJ, Fry RD (2008) New therapies in the treatment of postoperative ileus after gastrointestinal surgery. Am J Ther 15:59–65

    PubMed  Google Scholar 

  134. The FO, Bennink RJ, Ankum WM, Buist MR, Busch OR, Gouma DJ et al (2008) Intestinal handling-induced mast cell activation and inflammation in human postoperative ileus. Gut 57:33–40 (see comment)

    CAS  PubMed  Google Scholar 

  135. Frasko R, Maruna P, Gurlich R, Trca S (2008) Transcutaneous electrogastrography in patients with ileus. Relations to interleukin-1beta, interleukin-6, procalcitonin and C-reactive protein. Eur Surg Res 41:197–202

    CAS  PubMed  Google Scholar 

  136. Moore BA, Albers KM, Davis BM, Grandis JR, Togel S, Bauer AJ (2007) Altered inflammatory gene expression underlies increased susceptibility to murine postoperative ileus with advancing age. Am J Physiol Gastrointest Liver Physiol 292:G1650–G1659

    CAS  PubMed  Google Scholar 

  137. Uemura K, Tatewaki M, Harris M (2004) Magnitude of abdominal incision affects the duration of postoperative ileus in rats. Surg Endosc 18:606–610

    CAS  PubMed  Google Scholar 

  138. Kehlet H (2000) Manipulation of the metabolic response in clinical practice. World J Surg 24:690–695

    CAS  PubMed  Google Scholar 

  139. Jorgensen H, Wetterslev J, Moiniche S, Dahl JB (2008) Epidural local anaesthetics versus opioid-based analgesic regimens for postoperative gastrointestinal paralysis, PONV and pain after abdominal surgery. Cochrane Database Syst Rev 4:CD001893

    Google Scholar 

  140. Schmidt J, Stoffels B, Moore BA, Chanthaphavong RS, Mazie AR, Buchholz BM et al (2008) Proinflammatory role of leukocyte-derived Egr-1 in the development of murine postoperative ileus. Gastroenterology 135:926–936

    CAS  PubMed  Google Scholar 

  141. Schmidt J, Stoffels B, Nazir A, Dehaven-Hudkins DL, Bauer AJ (2008) Alvimopan and COX-2 inhibition reverse opioid and inflammatory components of postoperative ileus. Neurogastroenterol Motil 20:689–699

    CAS  PubMed  Google Scholar 

  142. van Rossen M, Hofland L, van den Tol M, van Koetsveld P, Jeekel J, Marquet R et al (2001) Effect of inflammatory cytokines and growth factors on tumour cell adhesion to the peritoneum. J Pathol 193:530–537

    PubMed  Google Scholar 

  143. Varghese S, Burness M, Xu H, Beresnev T, Pingpank J, Alexander R (2008) Site-specific gene expression profiles and novel molecular prognostic factors in patients with lower gastrointestinal adenocarcinoma diffusely metastatic to liver or peritoneum. Ann Surg Oncol 14:3460–3471

    Google Scholar 

  144. Eggermont A, Steller E, Sugarbaker P (1987) Laparotomy enhances intraperitoneal tumor growth and abrogates the antitumor effects interleukin-2 and lymphokine-activated killer cells. Surgery 102:71–78

    CAS  PubMed  Google Scholar 

  145. Weese J, Ottery F, Emoto S (1986) Do operations facilitate tumor growth? An experimental model in rats. Surgery 100:273–277

    CAS  PubMed  Google Scholar 

  146. Sugarbaker P (1991) A perspective on clinical research strategies in carcinoma of the large bowel. World J Surg 15:609–616

    CAS  PubMed  Google Scholar 

  147. Fisher B, Fisher E, Fedustea N (1967) Trauma and localization of the tumor cells. Cancer 20:23–30

    CAS  PubMed  Google Scholar 

  148. Abramovitch R, Marikovsky M, Meir G, Neeman M (1999) Stimulation of tumour growth by wound-derived growth factors. Br J Cancer 79:1392–1398

    CAS  PubMed  Google Scholar 

  149. Sugarbaker P (2007) Peritoneum as the first-Line of defense in carcinomatosis. J Surg Oncol 95:93–96

    PubMed  Google Scholar 

  150. Choileain N, Redmond H (2006) Cell response to surgery. Arch Surg 141:1132–1140

    Google Scholar 

  151. Singer M, De Santis V, Vitale D, Jeffcoate W (2004) Multiorgan failure is an adaptive, endocrine-mediated, metabolic response to overwhelming systemic inflammation. Lancet 364:545–548

    PubMed  Google Scholar 

  152. Hill A, Hill G (1998) Metabolic response to severe injury. Br J Surg 85:884–890

    CAS  PubMed  Google Scholar 

  153. Kendall GP (1985) Visceral pain. Br J Surg 72(Suppl):S4–S5

    PubMed  Google Scholar 

  154. Cervero F, Laird JM (1999) Visceral pain. Lancet 353:2145–2148

    CAS  PubMed  Google Scholar 

  155. Zargar-Shoshtari K, Paddison J, Booth R, Hill A (2009) A prospective study on the influence of a fast-track program on postoperative fatigue and functional recovery after major colonic surgery. J Surg Res 154:330–335

    PubMed  Google Scholar 

  156. Rubin G, Hardy R, Hotopf M (2004) A systematic review and metaanalysis of the incidence and severity of postoperative fatigue. J Psychosom Res 57:317

    PubMed  Google Scholar 

  157. Salmon P, Hall G (1997) A theory of postoperative fatigue: an interaction of biological, psychological, and social processes. Pharmacol Biochem Behav 56:623

    CAS  PubMed  Google Scholar 

  158. Menzies D (1992) Peritoneal adhesions. Incidence, cause, and prevention. Surg Annu 24(Pt 1):27–45

    PubMed  Google Scholar 

  159. Ellis H (1971) The cause and pitveation of postoperative intra-peritoneal adhesions. Surg Gynecol Obstet 133:497

    CAS  PubMed  Google Scholar 

  160. Hockel M, Ott S, Siemann U, Kissel T (1987) Prevention of peritoneal adhesions in the rat with sustained intraperitoneal dexamethasone delivered by a novel therapeutic system. Ann Chir Gynaecol 76:306–313

    CAS  PubMed  Google Scholar 

  161. DeSimone JM, Meguid MM, Kurzer M, Westervelt J (1988) Indomethacin decreases carrageenan-induced peritoneal adhesions. Surgery 104:788–795

    CAS  PubMed  Google Scholar 

  162. Steinleitner A, Lambert H, Montoro L (1988) The use of calcium channel blockade for prevention of postoperative adhesion formation. Fertil Steril 50:818–821

    CAS  PubMed  Google Scholar 

  163. Menzies D, Ellis H (1991) Role of plasminogen activator in adhesion prevention. Surg Gynaecol Obstet 172:326–366

    Google Scholar 

  164. Chen Y, Hills BA (2000) Surgical adhesions: evidence for adsorption of surfactant to peritoneal mesothelium. Aust N Z J Surg 70:443–447

    CAS  PubMed  Google Scholar 

  165. Krause TJ, Zazanis GA, McKinnon RD (1996) Prevention of postoperative adhesions with the chitin derivative N-O-carboxymethylchitosan. Wound Repair Regen 4:53–57

    CAS  PubMed  Google Scholar 

  166. Best C, Rittenhouse D, Vasquez C (1992) Evaluation of intercede (TC7) for reduction of postoperative adhesions in rabbits. Fertil Steril 58:817–820

    CAS  PubMed  Google Scholar 

  167. Burns J, Colts M, Burgees L, Skinner K (1997) Pre-clinical evaluation of Seprafilm bioresorbable membrane. Eur J Surg 577:S40–S48

    Google Scholar 

  168. Goldberg EP, Sheets JW, Habal MB (1980) Peritoneal adhesions: prevention with the use of hydrophilic polymer coatings. Arch Surg 115:776–780

    CAS  PubMed  Google Scholar 

  169. Chegini N (2002) Peritoneal molecular environment, adhesion formation and clinical implication. Front Biosci 7:e91–e115

    CAS  PubMed  Google Scholar 

  170. Sahin M, Cakir M, Avsar FM, Tekin A, Kucukkartallar T, Akoz M (2007) The effects of anti-adhesion materials in preventing postoperative adhesion in abdominal cavity (anti-adhesion materials for postoperative adhesions). Inflammation 30:244–249

    CAS  PubMed  Google Scholar 

  171. Yeo Y, Kohane DS (2008) Polymers in the prevention of peritoneal adhesions. Eur J Pharm Biopharm 68:57–66

    CAS  PubMed  Google Scholar 

  172. Kosaka H, Yoshimoto T, Yoshimoto T, Fujimoto J, Nakanishi K (2008) Interferon-gamma is a therapeutic target molecule for prevention of postoperative adhesion formation. Nat Med 14:437–441

    CAS  PubMed  Google Scholar 

  173. Reed KL, Heydrick SJ, Aarons CB, Prushik S, Gower AC, Stucchi AF et al (2007) A neurokinin-1 receptor antagonist that reduces intra-abdominal adhesion formation decreases oxidative stress in the peritoneum. Am J Physiol Gastrointest Liver Physiol 293:G544–G551

    CAS  PubMed  Google Scholar 

  174. Cohen PA, Aarons CB, Gower AC, Stucchi AF, Leeman SE, Becker JM et al (2007) The effectiveness of a single intraperitoneal infusion of a neurokinin-1 receptor antagonist in reducing postoperative adhesion formation is time dependent. Surgery 141:368–375

    PubMed  Google Scholar 

  175. Reed KL, Fruin AB, Gower AC, Stucchi AF, Leeman SE, Becker JM (2004) A neurokinin 1 receptor antagonist decreases postoperative peritoneal adhesion formation and increases peritoneal fibrinolytic activity. Proc Natl Acad Sci USA 101:9115–9120

    CAS  PubMed  Google Scholar 

  176. Novitsky YW, Litwin DE, Callery MP (2004) The net immunologic advantage of laparoscopic surgery. Surg Endosc 18:1411–1419

    CAS  PubMed  Google Scholar 

  177. Gupta A, Watson DI (2001) Effect of laparoscopy on immune function. Br J Surg 88:1296–1306

    CAS  PubMed  Google Scholar 

  178. Vittimberga F, Foley D, Meyers W (1998) Laparoscopic surgery and the systemic immune response. Ann Surg 227:326–334

    PubMed  Google Scholar 

  179. Yoshida S, Ohta J, Yamasaki K (2000) Effect of surgical stress on endogenous morphine and cytokine levels in the plasma after laparoscopic or open cholecystectomy. Surg Endosc 14:137–140

    CAS  PubMed  Google Scholar 

  180. Joris J, Cigarini I, Legrand M (1992) Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopy. Br J Anaesth 69:341–345

    CAS  PubMed  Google Scholar 

  181. Cho J, LaPorta A, Clark J (1994) Response of serum cytokines in patients undergoing laparoscopic cholecystectomy. Surg Endosc 8:1380–1384

    CAS  PubMed  Google Scholar 

  182. Glaser F, Sannwald G, Buhr H (1995) General stress response to conventional and laparoscopic cholecystectomy. Ann Surg 221:372–380

    CAS  PubMed  Google Scholar 

  183. Maruszynski M, Pojda Z (1995) Interleukin-6 (IL-6) levels in the monitoring of surgical trauma. Surg Endosc 9:882–885

    CAS  PubMed  Google Scholar 

  184. Vander Velpen G, Penninckx F, Kerremans R (1994) Interleukin-6 and coagulation-fibrinolysis fluctuations after laparoscopic and conventional cholecystectomy. Surg Endosc 8:1216–1220

    CAS  PubMed  Google Scholar 

  185. Suzuki M, Oka M, Tangoku A (1994) Interleukin-6 and granulocytic elastase levels following laparoscopic cholecystectomy. Surg Endosc 8:447

    Google Scholar 

  186. Hill AG, Connolly AB (2006) Minimal access colonic surgery: is it truly minimally invasive? ANZ J Surg 76:282–284

    PubMed  Google Scholar 

  187. Hill AG, Connolly AB (2006) Minimal access colorectal surgery: is it truly minimally invasive? Dis Colon Rectum 49:144–145

    PubMed  Google Scholar 

  188. Wiik H, Karttunen R, Haukipuro K, Syrjala H (2001) Maximal local and minimal systemic cytokine response to colorectal surgery: the influence of perioperative filgrastim. Cytokine 14:188–192

    CAS  PubMed  Google Scholar 

  189. 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

    CAS  PubMed  Google Scholar 

  190. Vittimberga FJ, Nolan B, Perugini RA, Spector L, Callery MP (2000) Laparoscopic surgery and Kupffer cell activation. Surg Endosc 14:1171–1176

    CAS  PubMed  Google Scholar 

  191. Ott DE (2008) Laparoscopy and adhesion formation, adhesions and laparoscopy. Semin Reprod Med 26:322–330

    CAS  PubMed  Google Scholar 

  192. Gutt CN, Oniu T, Schemmer P, Mehrabi A, Buchler MW (2004) Fewer adhesions induced by laparoscopic surgery? Surg Endosc 18:898–906 (see comment)

    CAS  PubMed  Google Scholar 

  193. Lower AM, Hawthorn RJS, Clark D, Boyd JH, Finlayson AR, Knight AD et al (2004) Adhesion-related readmissions following gynaecological laparoscopy or laparotomy in Scotland: an epidemiological study of 24,046 patients. Hum Reprod 19:1877–1885

    CAS  PubMed  Google Scholar 

  194. Dowson HM, Bong JJ, Lovell DP, Worthington TR, Karanjia ND, Rockall TA (2008) Reduced adhesion formation following laparoscopic versus open colorectal surgery. Br J Surg 95:909–914

    CAS  PubMed  Google Scholar 

  195. Ansari B, Vaidya J (2008) Reduced adhesion formation following laparoscopic versus open colorectal surgery. Br J Surg 95:1541–1542 (comment)

    Google Scholar 

  196. Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008) Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev CD003432

  197. Taskin O, Buhur A, Birincioglu M, Burak F, Atmaca R, Yilmaz I et al (1998) The effects of duration of CO2 insufflation and irrigation on peritoneal microcirculation assessed by free radical scavengers and total glutathion levels during operative laparoscopy. J Am Assoc Gynecol Laparosc 5:129–133

    CAS  PubMed  Google Scholar 

  198. Taskin O, Sadik S, Onoglu A, Gokdeniz R, Yilmaz I, Burak F et al (1999) Adhesion formation after microlaparoscopic and laparoscopic ovarian coagulation for polycystic ovary disease. J Am Assoc Gynecol Laparosc 6:159–163

    CAS  PubMed  Google Scholar 

  199. Nickkholgh A, Barro-Bejarano M, Liang R, Zorn M, Mehrabi A, Gebhard MM et al (2008) Signs of reperfusion injury following CO2 pneumoperitoneum: an in vivo microscopy study. Surg Endosc 22:122–128

    PubMed  Google Scholar 

  200. Molinas C, Koninckx P (2000) Hypoxemia induced by CO2 or helium pneumoperitoneum is a co-factor in adhesion formation in rabbits. Hum Reprod 15:1758–1763

    CAS  PubMed  Google Scholar 

  201. Sammour T, Mittal A, Loveday B, Kahokehr A, Phillips A, Windsor J et al (2009) Systematic review of oxidative stress associated with pneumoperitoneum. Br J Surg 96:836–850

    CAS  PubMed  Google Scholar 

  202. Sahin DA, Haliloglu B, Sahin FK, Akbulut G, Fidan H, Koken G et al (2007) Stepwise rising CO2 insufflation as an ischemic preconditioning method. J Laparoendosc Adv Surg Tech (Part A) 17:723–729

    Google Scholar 

  203. Stipancic I, Zarkovic N, Servis D, Sabolovic S, Tatzber F, Busic Z (2005) Oxidative stress markers after laparoscopic and open cholecystectomy. J Laparoendosc Adv Surg Tech (Part A) 15:347–352

    Google Scholar 

  204. Hakan Bukan M, Bukan N, Kaymakciouglu N, Tufan T (2004) Effects of open vs laparoscopic cholecystectomy on oxidative stress. Tohoku J Exp Med 202:51–56

    PubMed  Google Scholar 

  205. Eisen A, Fisman EZ, Rubenfire M, Freimark D, McKechnie R, Tenenbaum A et al (2004) Ischemic preconditioning: nearly two decades of research. A comprehensive review. Atherosclerosis 172:201–210

    CAS  PubMed  Google Scholar 

  206. Polat C, Yilmaz S, Serteser M, Koken T, Kahraman A, Dilek ON (2003) The effect of different intraabdominal pressures on lipid peroxidation and protein oxidation status during laparoscopic cholecystectomy. Surg Endosc 17:1719–1722

    CAS  PubMed  Google Scholar 

  207. Talbot D, Miller IT, Miller IA (1995) Fatal intestinal ischaemia following laparoscopic cholecystectomy. Br J Surg 82:1143

    CAS  PubMed  Google Scholar 

  208. Dwerryhouse SJ, Melsom DS, Burton PA, Thompson MH (1995) Acute intestinal ischaemia after laparoscopic cholecystectomy. Br J Surg 82:1413

    CAS  PubMed  Google Scholar 

  209. 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 76:560–567

    CAS  PubMed  Google Scholar 

  210. West M, Hackam D, Baker J (1997) Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgery. Ann Surg 226:179–190

    CAS  PubMed  Google Scholar 

  211. Volz J, Koster S, Weiss M, Schmidt R, Urbaschek R, Melchert F et al (1996) Pathophysiologic features of a pneumoperitoneum at laparoscopy: a swine model. Am J Obstet Gynecol 174:132–140

    CAS  PubMed  Google Scholar 

  212. Volz J, Koster S, Leweling H (1997) Surgical trauma and metabolic changes induced by surgical laparoscopy versus laparotomy. Gynecol Endosc 6:1–6

    Google Scholar 

  213. Molinas CR, Tjwa M, Vanacker B, Binda MM, Elkelani O, Koninckx PR (2004) Role of CO(2) pneumoperitoneum-induced acidosis in CO(2) pneumoperitoneum-enhanced adhesion formation in mice. Fertil Steril 81:708–711

    PubMed  Google Scholar 

  214. Yilmaz S, Polat C, Kahraman A, Koken T, Arikan Y, Dilek ON et al (2004) The comparison of the oxidative stress effects of different gases and intra-abdominal pressures in an experimental rat model. J Laparoendosc Adv Surg Tech (Part A) 14:165–168

    Google Scholar 

  215. Sammour T, Kahokehr A, Hill A (2008) The effect of warmed, humidified insufflation on postoperative pain in laparoscopy: a meta-analysis of randomised controlled trials. Br J Surg 95:950–956

    CAS  PubMed  Google Scholar 

  216. Koster S, Spacek Z, Paweletz N, Volz J (1999) [A scanning microscopy study of the peritoneum in mice after application of a CO2-pneumoperitoneum]. Zentralbl Gynakol 121:244–247

    CAS  PubMed  Google Scholar 

  217. Neuhaus SJ, Gupta A, Watson DI (2001) Helium and other alternative insufflation gases for laparoscopy. Surg Endosc 15:553–560

    CAS  PubMed  Google Scholar 

  218. Neuhaus SJ, Watson DI (2004) Pneumoperitoneum and peritoneal surface changes: a review. Surg Endosc 18:1316–1322

    CAS  PubMed  Google Scholar 

  219. 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 125:73–77

    PubMed  Google Scholar 

  220. Binda MM, Molinas CR, Mailova K, Koninckx PR (2004) Effect of temperature upon adhesion formation in a laparoscopic mouse model. Hum Reprod 19:2626–2632

    CAS  PubMed  Google Scholar 

  221. Ryan GB, Grobety J, Majno G (1973) Mesothelial injury and recovery. Am J Pathol 71:93–112

    CAS  PubMed  Google Scholar 

  222. Binda MM, Molinas CR, Hansen P, Koninckx PR (2006) Effect of desiccation and temperature during laparoscopy on adhesion formation in mice. Fertil Steril 86:166–175

    PubMed  Google Scholar 

  223. Binda MM, Molinas CR, Bastidas A, Jansen M, Koninckx PR (2007) Efficacy of barriers and hypoxia-inducible factor inhibitors to prevent CO(2) pneumoperitoneum-enhanced adhesions in a laparoscopic mouse model. J Minim Invasive Gynecol 14:591–599

    PubMed  Google Scholar 

  224. Peng Y, Zheng M, Ye Q, Chen X, Yu B, Liu B (2009) Heated and humidified CO2 prevents hypothermia, peritoneal injury, and intra-abdominal adhesions during prolonged laparoscopic insufflations. J Surg Res 151:40–47

    CAS  PubMed  Google Scholar 

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Acknowledgments

Tarik Sammour is supported by the Surgeon Scientist Scholarship, administered through the Royal Australasian College of Surgeons. Arman Kahokeher is supported by the Ruth Spencer scholarship from the Auckland Medical Research Foundation.

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  1. Department of Surgery, South Auckland Clinical School, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

    Tarik Sammour, Arman Kahokehr & Andrew G. Hill

  2. Department of Surgery, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

    Mattias Soop

  3. South Auckland Clinical School, Middlemore Hospital, Private Bag 93311, Otahuhu, Auckland, New Zealand

    Tarik Sammour

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Correspondence to Tarik Sammour.

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Sammour, T., Kahokehr, A., Soop, M. et al. Peritoneal Damage: The Inflammatory Response and Clinical Implications of the Neuro-Immuno-Humoral Axis. World J Surg 34, 704–720 (2010). https://doi.org/10.1007/s00268-009-0382-y

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