Semin Reprod Med 2008; 26(4): 289-297
DOI: 10.1055/s-0028-1082387
© Thieme Medical Publishers

Pathogenesis of Intra-abdominal and Pelvic Adhesion Development

Anthony N. Imudia1 , Sanjeev Kumar1 , Ghassan M. Saed2 , Michael P. Diamond1 , 2
  • 1Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, Michigan
  • 2C.S. Mott Center for Human Growth and Development, Wayne State University School of Medicine, Detroit, Michigan
Further Information

Publication History

Publication Date:
28 August 2008 (online)

ABSTRACT

Abdominal and pelvic adhesions are a frequent occurrence and are responsible for significant morbidity resulting in abdominal and pelvic pain, infertility, and small bowel obstruction. The process of adhesion development begins when damage to peritoneal surfaces from any source (operative trauma, infection, foreign bodies, desiccation, irradiation, allergic reaction, or chemical injury) induces a series of biochemical/molecular biologic cascades involving different elements. These elements include peritoneal fluid, neutrophils, leukocytes, macrophages, cytokines, mesothelial cells, and tissue and coagulation factors, which teleologically have the intention of peritoneal repair; however, these processes also result in adhesion development. Major pathways that play significant roles in the healing process of peritoneal damage leading to adhesion development are the fibrinolytic system, extracellular matrix deposition, growth factor and cytokines, cell adhesion molecules, angiogenesis, apoptosis and proliferation, and remesothelialization. Greater understanding of the regulation and interaction of these processes provides the potential for reduction of postoperative adhesion development.

REFERENCES

  • 1 Diamond M P, Freeman M L. Clinical implications of postsurgical adhesions.  Hum Reprod Update. 2001;  7 567-576
  • 2 Davey A K, Maher P J. Surgical adhesions: a timely update, a great challenge for the future.  J Minim Invasive Gynecol. 2007;  14 15-22
  • 3 Imudia A N, Diamond M P. Endometriosis and adhesion. Available at: http://wes.endometriosis.org/WES%20e-Journal%202007%201Q.pdf Accessed October 20, 2007
  • 4 Douvdevani A, Rapoport J, Konforty A, Argov S, Ovnat A, Chaimovitz C. Human peritoneal mesothelial cells synthesize IL-1 alpha and beta.  Kidney Int. 1994;  46 993-1001
  • 5 Bachus K E, Doty E, Haney A F, Weinberg J B. Differential effects of interleukin-1 alpha, tumor necrosis factor-alpha, indomethacin, hydrocortisone, and macrophage co-culture on the proliferation of human fibroblasts and peritoneal mesothelial cells.  J Soc Gynecol Investig. 1995;  2 636-642
  • 6 Offner F A, Obrist P, Stadlmann S et al.. IL-6 secretion by human peritoneal mesothelial and ovarian cancer cells.  Cytokine. 1995;  7 542-547
  • 7 Arici A, Tazuke S I, Attar E, Kliman H J, Olive D L. Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells.  Mol Hum Reprod. 1996;  2 40-45
  • 8 Saed G M, Zhang W, Diamond M P. Molecular characterization of fibroblasts isolated from human peritoneum and adhesions.  Fertil Steril. 2001;  75 763-768
  • 9 Bachus K E, Doty E, Haney A F, Weinberg J B. Differential effects of interleukin-1 alpha, tumor necrosis factor-alpha, indomethacin, hydrocortisone, and macrophage co-culture on the proliferation of human fibroblasts and peritoneal mesothelial cells.  J Soc Gynecol Investig. 1995;  2 636-642
  • 10 Offner F A, Feichtinger H, Stadlmann S et al.. Transforming growth factor-beta synthesis by human peritoneal mesothelial cells. Induction by interleukin-1.  Am J Pathol. 1996;  148 1679-1688
  • 11 Chegini N. The role of growth factors in peritoneal healing: transforming growth factor beta (TGF-beta).  Eur J Surg Suppl. 1997;  579 17-23
  • 12 Saed G M, Zhang W, Chegini N, Holmdahl L, Diamond M P. Transforming growth factor beta isoforms production by human peritoneal mesothelial cells after exposure to hypoxia.  Am J Reprod Immunol. 2000;  43 285-291
  • 13 Freeman M L, Saed G M, Elhammady E F, Diamond M P. 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
  • 14 Breborowicz A, Rodela H, Karon J, Martis L, Oreopoulos D G. In vitro simulation of the effect of peritoneal dialysis solution on mesothelial cells.  Am J Kidney Dis. 1997;  29 404-409
  • 15 Van Hinsberg V, Kooistra T, Scheffer M A, Hajo van B J, van Muijen G N. Characterization and fibrinolytic properties of human omental tissue mesothelial cells. Comparison with endothelial cells.  Blood. 1990;  75 1490-1497
  • 16 Sitter T, Spannagl M, Schiffl H, Held E, Van Hinsberg V, Kooistra T. Imbalance between intraperitoneal coagulation and fibrinolysis during peritonitis of CAPD patients: the role of mesothelial cells.  Nephrol Dial Transplant. 1995;  10 677-683
  • 17 Diamond M P, El-Hammady E, Wang R, Kruger M, Saed G. Regulation of expression of tissue plasminogen activator and plasminogen activator inhibitor-1 by dichloroacetic acid in human fibroblasts from normal peritoneum and adhesions.  Am J Obstet Gynecol. 2004;  190 926-934
  • 18 Saed G M, Abu-Soud H M, Diamond M P. Role of nitric oxide in apoptosis of human peritoneal and adhesion fibroblasts after hypoxia.  Fertil Steril. 2004;  82(Suppl 3) 1198-1205
  • 19 Liberek T, Topley N, Luttmann W, Williams J D. Adherence of neutrophils to human peritoneal mesothelial cells: role of intercellular adhesion molecule-1.  J Am Soc Nephrol. 1996;  7 208-217
  • 20 Chegini N, Kotseos K, Ma C et al.. Differential expression of integrin alpha v and beta 3 in serosal tissue of human intraperitoneal organs and adhesion.  Fertil Steril. 2001;  75 791-796
  • 21 Yung S, Coles G A, Davies M. IL-1 beta, a major stimulator of hyaluronan synthesis in vitro of human peritoneal mesothelial cells: relevance to peritonitis in CAPD.  Kidney Int. 1996;  50 1337-1343
  • 22 Svinarich D M, Zaher F M, Holmdahl L, Chegini N, Gonik B, Diamond M P. Adhesion development and the expression of endothelial nitric oxide synthase.  Infect Dis Obstet Gynecol. 2001;  9 113-116
  • 23 Topley N, Petersen M M, Mackenzie R et al.. Human peritoneal mesothelial cell prostaglandin synthesis: induction of cyclooxygenase mRNA by peritoneal macrophage-derived cytokines.  Kidney Int. 1994;  46 900-909
  • 24 Syrop C H, Halme J. Cyclic changes of peritoneal fluid parameters in normal and infertile patients.  Obstet Gynecol. 1987;  69 416-418
  • 25 Olive D L, Haney A F, Weinberg J B. The nature of the intraperitoneal exudate associated with infertility: peritoneal fluid and serum lysozyme activity.  Fertil Steril. 1987;  48 802-806
  • 26 Ellis H. The aetiology of post-operative abdominal adhesions. An experimental study.  Br J Surg. 1962;  50 10-16
  • 27 Raftery A T. Regeneration of parietal and visceral peritoneum in the immature animal: a light and electron microscopical study.  Br J Surg. 1973;  60 969-975
  • 28 Haney A F, Doty E. The formation of coalescing peritoneal adhesions requires injury to both contacting peritoneal surfaces.  Fertil Steril. 1994;  61 767-775
  • 29 Milligan D W, Raftery A T. Observations on the pathogenesis of peritoneal adhesions: a light and electron microscopical study.  Br J Surg. 1974;  61 274-280
  • 30 Kligman I, Drachenberg C, Papadimitriou J, Katz E. Immunohistochemical demonstration of nerve fibers in pelvic adhesions.  Obstet Gynecol. 1993;  82 566-568
  • 31 Tulandi T, Chen M F, Al-Took S, Watkin K. A study of nerve fibers and histopathology of postsurgical, postinfectious, and endometriosis-related adhesions.  Obstet Gynecol. 1998;  92 766-768
  • 32 Saed G M, Diamond M P. Hypoxia-induced irreversible up-regulation of type I collagen and transforming growth factor-beta1 in human peritoneal fibroblasts.  Fertil Steril. 2002;  78 144-147
  • 33 Saed G M, Diamond M P. Apoptosis and proliferation of human peritoneal fibroblasts in response to hypoxia.  Fertil Steril. 2002;  78 137-143
  • 34 Jones P A, Werb Z. 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. 1980;  152 1527-1536
  • 35 van der Poll T, Levi M, Büller H R et al.. Fibrinolytic response to tumor necrosis factor in healthy subjects.  J Exp Med. 1991;  174 729-732
  • 36 Hau T, Payne W D, Simmons R L. Fibrinolytic activity of the peritoneum during experimental peritonitis.  Surg Gynecol Obstet. 1979;  148 415-418
  • 37 Holmdahl L, Falkenberg M, Ivarsson M L, Risberg B. Plasminogen activators and inhibitors in peritoneal tissue.  APMIS. 1997;  105 25-30
  • 38 Porter J M, McGregor Jr F H, Mullen D C, Silver D. Fibrinolytic activity of mesothelial surfaces.  Surg Forum. 1969;  20 80-82
  • 39 Raftery A T. Method for measuring fibrinolytic activity in a single layer of cells.  J Clin Pathol. 1981;  34 625-629
  • 40 Thompson J N, Paterson-Brown S, Harbourne T, Whawell S A, Kalodiki E, Dudley H A. Reduced human peritoneal plasminogen activating activity: possible mechanism of adhesion formation.  Br J Surg. 1989;  76 382-384
  • 41 Rout U K, Diamond M P. Role of plasminogen activators during healing after uterine serosal lesioning in the rat.  Fertil Steril. 2003;  79 138-145
  • 42 Vipond M N, Whawell S A, Thompson J N, Dudley H A. Effect of experimental peritonitis and ischaemia on peritoneal fibrinolytic activity.  Eur J Surg. 1994;  160 471-477
  • 43 Diamond M P, El-Hammady E, Wang R, Kruger M, Saed G. Regulation of expression of tissue plasminogen activator and plasminogen activator inhibitor-1 by dichloroacetic acid in human fibroblasts from normal peritoneum and adhesions.  Am J Obstet Gynecol. 2004;  190 926-934
  • 44 Holmdahl L E, Al-Jabreen M, Risberg B. Role of fibrinolysis in the formation of postoperative adhesions.  Wound Repair Regen. 1994;  2 171-176
  • 45 Ivarsson M L, Holmdahl L, Falk P, Molne J, Risberg B. Characterization and fibrinolytic properties of mesothelial cells isolated from peritoneal lavage.  Scand J Clin Lab Invest. 1998;  58 195-203
  • 46 Saed G M, Diamond M P. Modulation of the expression of tissue plasminogen activator and its inhibitor by hypoxia in human peritoneal and adhesion fibroblasts.  Fertil Steril. 2003;  79 164-168
  • 47 Koks C A, Groothuis P G, Slaats P, Dunselman G A, de Goeij A F, Evers J L. Matrix metalloproteinases and their tissue inhibitors in antegradely shed menstruum and peritoneal fluid.  Fertil Steril. 2000;  73 604-612
  • 48 Sharpe-Timms K L, Keisler L W, McIntush E W, Keisler D H. Tissue inhibitor of metalloproteinase-1 concentrations are attenuated in peritoneal fluid and sera of women with endometriosis and restored in sera by gonadotropin-releasing hormone agonist therapy.  Fertil Steril. 1998;  69 1128-1134
  • 49 Chegini N, Kotseos K, Bennett B, Diamond M P, Holmdahl L, Burns J. Matrix metalloproteinase (MMP-1) and tissue inhibitor of MMP in peritoneal fluids and sera and correlation with peritoneal adhesions.  Fertil Steril. 2001;  76 1207-1211
  • 50 Sharpe-Timms K L, Zimmer R L, Jolliff W J, Wright J A, Nothnick W B, Curry T E. Gonadotropin-releasing hormone agonist (GnRH-a) therapy alters activity of plasminogen activators, matrix metalloproteinases, and their inhibitors in rat models for adhesion formation and endometriosis: potential GnRH-a-regulated mechanisms reducing adhesion formation.  Fertil Steril. 1998;  69 916-923
  • 51 Saed G M, Diamond M P. Effects of interferon-gamma reverse hypoxia-stimulated extracellular matrix expression in human peritoneal and adhesion fibroblasts.  Fertil Steril. 2006;  85(Suppl 1) 1300-1305
  • 52 Saed G M, Zhang W, Diamond M P. Molecular characterization of fibroblasts isolated from human peritoneum and adhesions.  Fertil Steril. 2001;  75 763-768
  • 53 Ma C, Tarnuzzer R W, Chegini N. Expression of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases in mesothelial cells and their regulation by transforming growth factor-beta1.  Wound Repair Regen. 1999;  7 477-485
  • 54 Sharpe-Timms K L, Zimmer R L, Jolliff W J, Wright J A, Nothnick W B, Curry T E. Gonadotropin-releasing hormone agonist (GnRH-a) therapy alters activity of plasminogen activators, matrix metalloproteinases, and their inhibitors in rat models for adhesion formation and endometriosis: potential GnRH-a-regulated mechanisms reducing adhesion formation.  Fertil Steril. 1998;  69 916-923
  • 55 Diamond M P, El-Hammady E, Wang R, Saed G. 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. 2004;  81 185-190
  • 56 Sato Y, Rifkin D B. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture.  J Cell Biol. 1989;  109 309-315
  • 57 Parks W C. Matrix metalloproteinases in repair.  Wound Repair Regen. 1999;  7 423-432
  • 58 Roberts A B. Transforming growth factor-beta: activity and efficacy in animal models of wound healing.  Wound Repair Regen. 1995;  3 408-418
  • 59 Assoian R K, Komoriya A, Meyers C A, Miller D M, Sporn M B. Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization.  J Biol Chem. 1983;  258 7155-7160
  • 60 Assoian R K, Fleurdelys B E, Stevenson H C et al.. Expression and secretion of type beta transforming growth factor by activated human macrophages.  Proc Natl Acad Sci U S A. 1987;  84 6020-6024
  • 61 Cromack D T, Sporn M B, Roberts A B, Merino M J, Dart L L, Norton J A. Transforming growth factor beta levels in rat wound chambers.  J Surg Res. 1987;  42 622-628
  • 62 Saed G M, Zhang W, Chegini N, Holmdahl L, Diamond M P. Transforming growth factor beta isoforms production by human peritoneal mesothelial cells after exposure to hypoxia.  Am J Reprod Immunol. 2000;  43 285-291
  • 63 Ignotz R A, Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix.  J Biol Chem. 1986;  261 4337-4345
  • 64 Frank S, Madlener M, Werner S. Transforming growth factors beta1, beta2, and beta3 and their receptors are differentially regulated during normal and impaired wound healing.  J Biol Chem. 1996;  271 10188-10193
  • 65 O'Kane S, Ferguson M W. Transforming growth factor beta s and wound healing.  Int J Biochem Cell Biol. 1997;  29 63-78
  • 66 Shah M, Foreman D M, Ferguson M W. Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring.  J Cell Sci. 1995;  108(Pt 3) 985-1002
  • 67 Border W A, Noble N A. Transforming growth factor beta in tissue fibrosis.  N Engl J Med. 1994;  331 1286-1292
  • 68 Chegini N, Gold L I, Williams R S, Masterson B J. Localization of transforming growth factor beta isoforms TGF-beta 1, TGF-beta 2, and TGF-beta 3 in surgically induced pelvic adhesions in the rat.  Obstet Gynecol. 1994;  83 449-454
  • 69 Chegini N, Rong H, Bennett B, Stone I K. Peritoneal fluid cytokine and eicosanoid levels and their relation to the incidence of peritoneal adhesion.  J Soc Gynecol Investig. 1999;  6 153-157
  • 70 Williams R S, Rossi A M, Chegini N, Schultz G. Effect of transforming growth factor beta on postoperative adhesion formation and intact peritoneum.  J Surg Res. 1992;  52 65-70
  • 71 Diamond M P, Wirth J J, Saed G M. PCBs enhance collagen I expression from human peritoneal fibroblasts.  Fertil Steril. 2008;  , in press
  • 72 Rout U K, Saed G M, Diamond M P. Transforming growth factor-beta1 modulates expression of adhesion and cytoskeletal proteins in human peritoneal fibroblasts.  Fertil Steril. 2002;  78 154-161
  • 73 Cheong Y C, Laird S M, Li T C, Shelton J B, Ledger W L, Cooke I D. Peritoneal healing and adhesion formation/reformation.  Hum Reprod Update. 2001;  7 556-566
  • 74 Miyake S, Yagita H, Maruyama T, Hashimoto H, Miyasaka N, Okumura K. Beta 1 integrin-mediated interaction with extracellular matrix proteins regulates cytokine gene expression in synovial fluid cells of rheumatoid arthritis patients.  J Exp Med. 1993;  177 863-868
  • 75 Werb Z, Tremble P M, Behrendtsen O, Crowley E, Damsky C H. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression.  J Cell Biol. 1989;  109 877-889
  • 76 Gazvani M R, Christmas S, Quenby S, Kirwan J, Johnson P M, Kingsland C R. Peritoneal fluid concentrations of interleukin-8 in women with endometriosis: relationship to stage of disease.  Hum Reprod. 1998;  13 1957-1961
  • 77 Rout U K, Oommen K, Diamond M P. Altered expressions of VEGF mRNA splice variants during progression of uterine-peritoneal adhesions in the rat.  Am J Reprod Immunol. 2000;  43 299-304
  • 78 Molinas C R, Campo R, Dewerchin M, Eriksson U, Carmeliet P, Koninckx P R. Role of vascular endothelial growth factor and placental growth factor in basal adhesion formation and in carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in transgenic mice.  Fertil Steril. 2003;  80(Suppl 2) 803-811
  • 79 Wiczyk H P, Grow D R, Adams L A, O'Shea D L, Reece M T. Pelvic adhesions contain sex steroid receptors and produce angiogenesis growth factors.  Fertil Steril. 1998;  69 511-516
  • 80 Diamond M P, El-Hammady E, Munkarah A, Bieber E J, Saed G. Modulation of the expression of vascular endothelial growth factor in human fibroblasts.  Fertil Steril. 2005;  83 405-409
  • 81 Ferrara N, vis-Smyth T. The biology of vascular endothelial growth factor.  Endocr Rev. 1997;  18 4-25
  • 82 Goldsmith H S, Griffith A L, Kupferman A, Catsimpoolas N. Lipid angiogenic factor from omentum.  JAMA. 1984;  252 2034-2036
  • 83 Muschel R J, Bernhard E J, Garza L, McKenna W G, Koch C J. Induction of apoptosis at different oxygen tensions: evidence that oxygen radicals do not mediate apoptotic signaling.  Cancer Res. 1995;  55 995-998
  • 84 Ladin D A, Hou Z, Patel D et al.. p53 and apoptosis alterations in keloids and keloid fibroblasts.  Wound Repair Regen. 1998;  6 28-37
  • 85 Sogawa K. Overview: hypoxia.  Tanpakushitsu Kakusan Koso. 1999;  44 2470-2471
  • 86 Stempien-Otero A, Karsan A, Cornejo C J et al.. Mechanisms of hypoxia-induced endothelial cell death. Role of p53 in apoptosis.  J Biol Chem. 1999;  274 8039-8045
  • 87 DeCherney A H, diZerega G S. Clinical problem of intraperitoneal postsurgical adhesion formation following general surgery and the use of adhesion prevention barriers.  Surg Clin North Am. 1997;  77 671-688
  • 88 diZerega G S. Biochemical events in peritoneal tissue repair.  Eur J Surg Suppl. 1997;  579 10-16
  • 89 Brauner A, Hylander B, Wretlind B. Interleukin-6 and interleukin-8 in dialysate and serum from patients on continuous ambulatory peritoneal dialysis.  Am J Kidney Dis. 1993;  22 430-435
  • 90 Brauner A, Hylander B, Wretlind B. Tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-1 receptor antagonist in dialysate and serum from patients on continuous ambulatory peritoneal dialysis.  Am J Kidney Dis. 1996;  27 402-408
  • 91 Zemel D, Koomen G C, Hart A A, Ten Berge I, Struijk D G, Krediet R T. Relationship of TNF-alpha, interleukin-6, and prostaglandins to peritoneal permeability for macromolecules during longitudinal follow-up of peritonitis in continuous ambulatory peritoneal dialysis.  J Lab Clin Med. 1993;  122 686-696
  • 92 Halme J. Release of tumor necrosis factor-alpha by human peritoneal macrophages in vivo and in vitro.  Am J Obstet Gynecol. 1989;  161 1718-1725
  • 93 Lowry S F. Cytokine mediators of immunity and inflammation.  Arch Surg. 1993;  128 1235-1241
  • 94 Mori H, Sawairi M, Nakagawa M, Itoh N, Wada K, Tamaya T. Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease.  Am J Reprod Immunol. 1991;  26 62-67
  • 95 Bauer J, Ganter U, Geiger T et al.. Regulation of interleukin-6 expression in cultured human blood monocytes and monocyte-derived macrophages.  Blood. 1988;  72 1134-1140
  • 96 Hirano T. Interleukin 6 and its receptor: ten years later.  Int Rev Immunol. 1998;  16 249-284
  • 97 Ivarsson M L, Holmdahl L, Falk P, Molne J, Risberg B. Characterization and fibrinolytic properties of mesothelial cells isolated from peritoneal lavage.  Scand J Clin Lab Invest. 1998;  58 195-203
  • 98 Whawell S A, Scott-Coombes D M, Vipond M N, Tebbutt S J, Thompson J N. Tumour necrosis factor-mediated release of plasminogen activator inhibitor 1 by human peritoneal mesothelial cells.  Br J Surg. 1994;  81 214-216
  • 99 Saba A A, Godziachvili V, Mavani A K, Silva Y J. Serum levels of interleukin 1 and tumor necrosis factor alpha correlate with peritoneal adhesion grades in humans after major abdominal surgery.  Am Surg. 1998;  64 734-736
  • 100 Guerra-Infante F M, Flores-Medina S, Lopez-Hurtado M et al.. Tumor necrosis factor in peritoneal fluid from asymptomatic infertile women.  Arch Med Res. 1999;  30 138-143
  • 101 Chegini N, Rong H, Bennett B, Stone I K. Peritoneal fluid cytokine and eicosanoid levels and their relation to the incidence of peritoneal adhesion.  J Soc Gynecol Investig. 1999;  6 153-157
  • 102 Mori H, Sawairi M, Nakagawa M, Itoh N, Wada K, Tamaya T. Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease.  Am J Reprod Immunol. 1991;  26 62-67
  • 103 Saed G M, Kruger M, Diamond M P. Expression of transforming growth factor-beta and extracellular matrix by human peritoneal mesothelial cells and by fibroblasts from normal peritoneum and adhesions: effect of Tisseel.  Wound Repair Regen. 2004;  12 557-564
  • 104 Buyalos R P, Funari V A, Azziz R, Watson J M, Martinez-Maza O. Elevated interleukin-6 levels in peritoneal fluid of patients with pelvic pathology.  Fertil Steril. 1992;  58 302-306
  • 105 Holschneider C H, Cristoforoni P M, Ghosh K, Punyasavatsut M, Abed E, Montz F J. Endogenous versus exogenous IL-10 in postoperative intraperitoneal adhesion formation in a murine model.  J Surg Res. 1997;  70 138-143

Michael P DiamondM.D. 

Wayne State University–Detroit Medical Center

3750 Woodward Avenue, Suite 200-D, Detroit, MI 48201

Email: mdiamond@med.wayne.edu

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