Advances in the pathogenesis of adhesion development: The role of oxidative stress

Reproductive Sciences

Volumn 21, Issue 7, 2014, Pages 823-836

  Awonuga, Awoniyi O ^a,b   Belotte, Jimmy ^a   Abuanzeh, Suleiman ^a   Fletcher, Nicole M ^a   Diamond, Michael P ^c   Saed, Ghassan M ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

adhesion markers; hypoxia; oxidative stress; postoperative adhesions

Indexed keywords

ANTIOXIDANT; CATALASE; ENZYME; FREE RADICAL; GLUTATHIONE PEROXIDASE; NITROGEN DERIVATIVE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR;

HUMAN; HYPOXEMIA; INFLAMMATION; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TISSUE ADHESION;

EID: 84904625770     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719114522550     Document Type: Review

References (141)

1. Agarwal A, Allamaneni SS. Role of free radicals in female reproductive diseases and assisted reproduction. Reprod Biomed Online. 2004 ; 9 (3). 338-347
2. Halliwell BG, John Gutteridge Free Radicals in Biology and Medicine. Oxford: Clarendon ; 1989: 1-20.
3. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007 ; 39 (1). 44-84
4. Yung LM, Leung FP, Yao X, Chen ZY, Huang Y. Reactive oxygen species in vascular wall. Cardiovasc Hematol Disord Drug Targets. 2006 ; 6 (1). 1-19
5. Crimi E, Ignarro LJ, Napoli C. Microcirculation and oxidative stress. Free Radic Res. 2007 ; 41 (12). 1364-1375
6. Agarwal A, Gupta S, Sharma R. Oxidative stress and its implications in female infertility - a clinician's perspective. Reprod Biomed Online. 2005 ; 11 (5). 641-650
7. Fissore RA, Kurokawa M, Knott J, Zhang M, Smyth J. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction. 2002 ; 124 (6). 745-754
8. Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med. 2008 ; 44 (7). 1295-1304
9. Goud AP, Goud PT, Diamond MP, Abu-Soud HM. Nitric oxide delays oocyte aging. Biochemistry. 2005 ; 44 (34). 11361-11368
10. Rizzo A, Roscino M, Binetti F, Sciorsci R. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim. 2012 ; 47 (2). 344-352
11. Clerici G, Slavescu C, Fiengo S, et al. Oxidative stress in pathological pregnancies. J Obstet Gynaecol. 2012 ; 32 (2). 124-127
12. Yildirim G, Attar R, Ozkan F, Kumbak B, Ficicioglu C, Yesildaglar N. The effects of letrozole and melatonin on surgically induced endometriosis in a rat model: a preliminary study. Fertil Steril. 2010 ; 93 (6). 1787-1792
13. Taddei ML, Giannoni E, Raugei G, et al. Mitochondrial oxidative stress due to complex I dysfunction promotes fibroblast activation and melanoma cell invasiveness. J Signal Transduct. 2012 ; 2012: 684592
14. Diamond MP Gynecology and Obstetrics. Sciarra JW, ed. Philadelphia: Harper & Row ; 1988: 1-23.
15. Diamond MP. Reduction of adhesions after uterine myomectomy by Seprafilm membrane (HAL-F): a blinded, prospective, randomized, multicenter clinical study. seprafilm adhesion study group. Fertil Steril. 1996 ; 66 (6). 904-910
16. Diamond MP Peritoneal Surgery. GS d diZerega, ed. New York: Spriger-Verlag ; 2000: 217-220.
17. Awonuga AO, Fletcher NM, Saed GM, Diamond MP. Postoperative adhesion development following cesarean and open intra-abdominal gynecological operations: a review. Reprod Sci. 2011 ; 18 (12). 1166-1185
18. Vrijland WW JJ, van Geldorp HJ, Swank DJ, Bonjer HJ. Abdominal adhesions: intestinal obstruction, pain, and infertility. Surg Endosc. 2003 ; 17 (7). 1017-1022
19. Marana R, Catalano GF, Muzii L. Salpingoscopy. Curr Opin Obstet Gynecol. 2003 ; 15 (4). 333-336
20. Barmparas G, Branco BC, Schnuriger B, Lam L, Inaba K, Demetriades D. The incidence and risk factors of post-laparotomy adhesive small bowel obstruction. J Gastrointest Surg. 2010 ; 14 (10). 1619-1628
21. Duffy DM, diZerega GS. Adhesion controversies: pelvic pain as a cause of adhesions, crystalloids in preventing them. J Reprod Med. 1996 ; 41 (1). 19-26
22. Holmdahl L, Risberg B. Adhesions: prevention and complications in general surgery. Eur J Surg. 1997 ; 163 (3). 169-174
23. Murdoch C, Lewis CE. Macrophage migration and gene expression in response to tumor hypoxia. Int J Cancer. 2005 ; 117 (5). 701-708
24. Terada LS, Guidot DM, Leff JA, et al. Hypoxia injures endothelial cells by increasing endogenous xanthine oxidase activity. Proc Natl Acad Sci U S A. 1992 ; 89 (8). 3362-3366
25. Fridovich I. The biology of oxygen radicals. Science. 1978 ; 201 (4359). 875-880
26. Yamamoto Y, Konig P, Henrich M, Dedio J, Kummer W. Hypoxia induces production of nitric oxide and reactive oxygen species in glomus cells of rat carotid body. Cell Tissue Res. 2006 ; 325 (1). 3-11
27. Zhu H, Bunn HF. Oxygen sensing and signaling: impact on the regulation of physiologically important genes. Respir Physiol. 1999 ; 115 (2). 239-247
28. McNally JS, Davis ME, Giddens DP, et al. Role of xanthine oxidoreductase and NAD(P)H oxidase in endothelial superoxide production in response to oscillatory shear stress. Am J Physiol Heart Circ Physiol. 2003 ; 285 (6). H2290 - H2297
29. Stuehr DJ, Cho HJ, Kwon NS, Weise MF, Nathan CF. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein. Proc Natl Acad Sci U S A. 1991 ; 88 (17). 7773-7777
30. Yui Y, Hattori R, Kosuga K, Eizawa H, Hiki K, Kawai C. Purification of nitric oxide synthase from rat macrophages. J Biol Chem. 1991 ; 266 (19). 12544-12547
31. Stuehr DJ. Structure-function aspects in the nitric oxide synthases. Annu Rev Pharmacol Toxicol. 1997 ; 37: 339-359
32. Chinje EC, Stratford IJ. Role of nitric oxide in growth of solid tumours: a balancing act. Essays Biochem. 1997 ; 32: 61-72
33. MacMicking JD, Nathan C, Hom G, et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 1995 ; 81 (4). 641-650
34. Kettle AJ, van Dalen CJ, Winterbourn CC. Peroxynitrite and myeloperoxidase leave the same footprint in protein nitration. Redox Rep. 1997 ; 3 (5-6). 257-258
35. Weiss SJ, Klein R, Slivka A, Wei M. Chlorination of taurine by human neutrophils. evidence for hypochlorous acid generation. J Clin Invest. 1982 ; 70 (3). 598-607
36. Tahboub YR, Galijasevic S, Diamond MP, Abu-Soud HM. Thiocyanate modulates the catalytic activity of mammalian peroxidases. J Biol Chem. 2005 ; 280 (28). 26129-26136
37. Pullar JM, Vissers MC, Winterbourn CC. Living with a killer: the effects of hypochlorous acid on mammalian cells. IUBMB Life. 2000 ; 50 (4-5). 259-266
38. Pascoe GA, Fariss MW, Olafsdottir K, Reed DJ. A. role of vitamin E in protection against cell injury. Maintenance of intracellular glutathione precursors and biosynthesis. Eur J Biochem. 1987 ; 166 (1). 241-247
39. Harrison FE, Meredith ME, Dawes SM, Saskowski JL, May JM. Low ascorbic acid and increased oxidative stress in gulo(-/-) mice during development. Brain Res. 2010 ; 1349: 143-152
40. Beckman JS, Chen J, Ischiropoulos H, Crow JP. Oxidative chemistry of peroxynitrite. Methods Enzymol. 1994 ; 233: 229-240
41. Akaike T, Suga M, Maeda H. Free radicals in viral pathogenesis: molecular mechanisms involving superoxide and NO. Proc Soc Exp Biol Med. 1998 ; 217 (1). 64-73
42. Turko IV, Murad F. Protein nitration in cardiovascular diseases. Pharmacol Rev. 2002 ; 54 (4). 619-634
43. Fletcher NM, Jiang ZL, Diamond MP, Abu Soud HM, Saed GM. Hypoxia-generated superoxide induces the development of the adhesion phenotype. Free Radic Biol Med. 2008 ; 45 (4). 530-536
44. Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril. 2003 ; 79 (6). 1288-1293
45. Van Langendonckt A, Casanas Roux F, Donnez J. Oxidative stress and peritoneal endometriosis. Fertil Steril. 2002 ; 77 (5). 861-870
46. El Mouatassim S, Guerin P, Menezo Y. Mammalian oviduct and protection against free oxygen radicals: expression of genes encoding antioxidant enzymes in human and mouse. Eur J Obstet Gynecol Reprod Biol. 2000 ; 89 (1). 1-6
47. Saed GM, Diamond MP. Molecular characterization of postoperative adhesions: the adhesion phenotype. J Am Assoc Gynecol Laparosc. 2004 ; 11 (3). 307-314
48. Li YQ BJ, Nordal RA, Su ZF, Wong CS. Hypoxia in radiation-induced blood spinal cord barrier breakdown. Cancer Res Treat. 2000 ; 61 (8). 3348-3354
49. Reed KL, Heydrick SJ, Aarons CB, et al. A neurokinin-1 receptor antagonist that reduces intra-abdominal adhesion formation decreases oxidative stress in the peritoneum. Am J Physiol Gastrointest Liver Physiol. 2007 ; 293 (3). G544 - G551
50. Heydrick SJ, Reed KL, Cohen PA, et al. Intraperitoneal administration of methylene blue attenuates oxidative stress, increases peritoneal fibrinolysis, and inhibits intraabdominal adhesion formation. J Surg Res. 2007 ; 143 (2). 311-319
51. Dunn RC, Buttram VC. Tissue-type plasminogen activator as an adjuvant for post surgical adhesions. Prog Clin Biol Res. 1990 ; 358: 113-118
52. Desmouliere A, Redard M, Darby I, Gabbiani G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol. 1995 ; 146 (1). 56-66
53. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB. Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am J Physiol. 1999 ; 277 (2 pt 1). C183 - C201
54. Sogawa K. Overview: hypoxia [in Japanese]. Tanpakushitsu Kakusan Koso. 1999 ; 44 (15 suppl). 2470-2471
55. Saed GM, Diamond MP. Hypoxia-induced irreversible up-regulation of type I collagen and transforming growth factor-beta1 in human peritoneal fibroblasts. Fertil Steril. 2002 ; 78 (1). 144-147
56. Alpay Z, Ozgonenel M, Savasan S, Buck S, Saed GM, Diamond MP. Altered in vitro immune response to hypoxia-treated normal peritoneal fibroblasts. Fertil Steril. 2007 ; 87 (2). 426-429
57. Falanga V. Wound healing. an overview. J Dermatol Surg Oncol. 1993 ; 19 (8). 689-690
58. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol. 1993 ; 122 (1). 103-111
59. Saed GM, Diamond MP. Differential expression of alpha smooth muscle cell actin in human fibroblasts isolated from intraperitoneal adhesions and normal peritoneal tissues. Fertil Steril. 2004 ; 82 (suppl 3). 1188-1192
60. Saed GM, Abu-Soud HM, Diamond MP. Role of nitric oxide in apoptosis of human peritoneal and adhesion fibroblasts after hypoxia. Fertil Steril. 2004 ; 82 (suppl 3). 1198-1205
61. Shavell VI, Saed GM, Diamond MP. Review: cellular metabolism: contribution to postoperative adhesion development. Reprod Sci. 2009 ; 16 (7). 627-634
62. Cookson VJ, Chapman NR. NF-kappaB function in the human myometrium during pregnancy and parturition. Histol Histopathol. 2010 ; 25 (7). 945-956
63. Saed GM, Diamond MP. Apoptosis and proliferation of human peritoneal fibroblasts in response to hypoxia. Fertil Steril. 2002 ; 78 (1). 137-143
64. Chegini N. The role of growth factors in peritoneal healing: transforming growth factor beta (TGF-beta). Eur J Surg Suppl. 1997 ; (577). 17-23
65. Idell S, Zwieb C, Boggaram J, Holiday D, Johnson AR, Raghu G. Mechanisms of fibrin formation and lysis by human lung fibroblasts: influence of TGF-beta and TNF-alpha. Am J Physiol. 1992 ; 263 (4 pt 1). L487 - L494
66. Saed GM, Zhang W, Diamond MP. Molecular characterization of fibroblasts isolated from human peritoneum and adhesions. Fertil Steril. 2001 ; 75 (4). 763-768
67. Ivarsson ML, 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 (3). 195-203
68. Diamond MP, El-Hammady E, Munkarah A, Bieber EJ, Saed G. Modulation of the expression of vascular endothelial growth factor in human fibroblasts. Fertil Steril. 2005 ; 83 (2). 405-409
69. Saed GM, Zhang W, Chegini N, Holmdahl L, Diamond MP. Alteration of type I and III collagen expression in human peritoneal mesothelial cells in response to hypoxia and transforming growth factor-beta1. Wound Repair Regen. 1999 ; 7 (6). 504-510
70. Saed GM, Munkarah AR, Abu-Soud HM, Diamond MP. Hypoxia upregulates cyclooxygenase-2 and prostaglandin E(2) levels in human peritoneal fibroblasts. Fertil Steril. 2005 ; 83 (suppl 1). 1216-1219
71. Saed GM, Diamond MP. Modulation of the expression of tissue plasminogen activator and its inhibitor by hypoxia in human peritoneal and adhesion fibroblasts. Fertil Steril. 2003 ; 79 (1). 164-168
72. Lu Y, Wahl LM. Oxidative stress augments the production of matrix metalloproteinase-1, cyclooxygenase-2, and prostaglandin E2 through enhancement of NF-kappa B activity in lipopolysaccharide-activated human primary monocytes. J Immunol. 2005 ; 175 (8). 5423-5429
73. Saed GM, Zhao M, Diamond MP, Abu-Soud HM. Regulation of inducible nitric oxide synthase in post-operative adhesions. Hum Reprod. 2006 ; 21 (6). 1605-1611
74. Abu-Soud HM, Stuehr DJ. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc Natl Acad Sci U S A. 1993 ; 90 (22). 10769-10772
75. Rosen GM, Tsai P, Weaver J, et al. The role of tetrahydrobiopterin in the regulation of neuronal nitric-oxide synthase-generated superoxide. J Biol Chem. 2002 ; 277 (43). 40275-40280
76. Jiang ZL, Fletcher NM, Diamond MP, Abu-Soud HM, Saed GM. S-nitrosylation of caspase-3 is the mechanism by which adhesion fibroblasts manifest lower apoptosis. Wound Repair Regen. 2009 ; 17 (2). 224-229
77. Kowaltowski AJ, Vercesi AE. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med. 1999 ; 26 (3-4). 463-471
78. Yang HW, Hwang KJ, Kwon HC, Kim HS, Choi KW, Oh KS. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod. 1998 ; 13 (4). 998-1002
79. Tarin JJ, Gomez-Piquer V, Pertusa JF, Hermenegildo C, Cano A. Association of female aging with decreased parthenogenetic activation, raised MPF, and MAPKs activities and reduced levels of glutathione S-transferases activity and thiols in mouse oocytes. Mol Reprod Dev. 2004 ; 69 (4). 402-410
80. Gardiner CS, Salmen JJ, Brandt CJ, Stover SK. Glutathione is present in reproductive tract secretions and improves development of mouse embryos after chemically induced glutathione depletion. Biol Reprod. 1998 ; 59 (2). 431-436
81. Shukla A, Rasik AM, Shankar R. Nitric oxide inhibits wounds collagen synthesis. Mol Cell Biochem. 1999 ; 200 (1-2). 27-33
82. Ferrini MG, Vernet D, Magee TR, et al. Antifibrotic role of inducible nitric oxide synthase. Nitric Oxide. 2002 ; 6 (3). 283-294
83. Jiang ZL, Zhu X, Diamond MP, Abu-Soud HM, Saed GM. Nitric oxide synthase isoforms expression in fibroblasts isolated from human normal peritoneum and adhesion tissues. Fertil Steril. 2008 ; 90 (3). 769-774
84. Cudd A, Fridovich I. Electrostatic interactions in the reaction mechanism of bovine erythrocyte superoxide dismutase. J Biol Chem. 1982 ; 257 (19). 11443-11447
85. van der Vliet A, Eiserich JP, Halliwell B, Cross CE. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J Biol Chem. 1997 ; 272 (12). 7617-7625
86. Hazen SL, Zhang R, Shen Z, et al. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation In vivo. Circ Res. 1999 ; 85 (10). 950-958
87. Jong EC, Klebanoff SJ. Eosinophil-mediated mammalian tumor cell cytotoxicity: role of the peroxidase system. J Immunol. 1980 ; 124 (4). 1949-1953
88. Mayeno AN, Curran AJ, Roberts RL, Foote CS. Eosinophils preferentially use bromide to generate halogenating agents. J Biol Chem. 1989 ; 264 (10). 5660-5668
89. Klebanoff SJ, Waltersdorph AM, Rosen H. Antimicrobial activity of myeloperoxidase. Methods Enzymol. 1984 ; 105: 399-403
90. Stocker R, Keaney JF. Role of oxidative modification in atherosclerosis. Physiol Rev. 2004 ; 84 (4). 1381-1478
91. Abu-Soud HM, Hazen SL. Nitric oxide is a physiological substrate for mammalian peroxidases. J Biol Chem. 2000 ; 275 (48). 37524-37532
92. Abu-Soud HM, Hazen SL. Nitric oxide modulates the catalytic activity of myeloperoxidase. J Biol Chem. 2000 ; 275 (8). 5425-5430
93. Abu-Soud HM, Hazen SL. Interrogation of heme pocket environment of mammalian peroxidases with diatomic ligands. Biochemistry. 2001 ; 40 (36). 10747-10755
94. Galijasevic S, Saed GM, Diamond MP, Abu-Soud HM. Myeloperoxidase up-regulates the catalytic activity of inducible nitric oxide synthase by preventing nitric oxide feedback inhibition. Proc Natl Acad Sci U S A. 2003 ; 100 (25). 14766-14771
95. Abu-Soud HM, Khassawneh MY, Sohn JT, Murray P, Haxhiu MA, Hazen SL. Peroxidases inhibit nitric oxide (NO) dependent bronchodilation: development of a model describing NO-peroxidase interactions. Biochemistry. 2001 ; 40 (39). 11866-11875
96. Kettle AJ, Winterbourn CC. Myeloperoxidase: a key regulator of neutrophil oxidant production. Redox Rep. 1997 ; 3 (3). 3-15
97. Abu-Soud HM, Raushel FM, Hazen SL. A novel multistep mechanism for oxygen binding to ferrous hemoproteins: rapid kinetic analysis of ferrous-dioxy myeloperoxidase (compound III) formation. Biochemistry. 2004 ; 43 (36). 11589-11595
98. Shao B, Oda MN, Vaisar T, Oram JF, Heinecke JW. Pathways for oxidation of high-density lipoprotein in human cardiovascular disease. Curr Opin Mol Ther. 2006 ; 8 (3). 198-205
99. Xu W, Zheng S, Dweik RA, Erzurum SC. Role of epithelial nitric oxide in airway viral infection. Free Radic Biol Med. 2006 ; 41 (1). 19-28
100. Westman E, Lundberg K, Erlandsson Harris H. Arthritogenicity of collagen type II is increased by chlorination. Clin Exp Immunol. 2006 ; 145 (2). 339-345
101. Midwinter RG, Vissers MC, Winterbourn CC. Hypochlorous acid stimulation of the mitogen-activated protein kinase pathway enhances cell survival. Arch Biochem Biophys. 2001 ; 394 (1). 13-20
102. McCord JM, Fridovich I. Superoxide dismutase. an enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969 ; 244 (22). 6049-6055
103. Schallreuter KU, Moore J, Wood JM, et al. In vivo and in vitro evidence for hydrogen peroxide (H2O2) accumulation in the epidermis of patients with vitiligo and its successful removal by a UVB-activated pseudocatalase. J Investig Dermatol Symp Proc. 1999 ; 4 (1). 91-96
104. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979 ; 59 (3). 527-605
105. Halliwell B.. Oxygen and nitrogen are pro-carcinogens. Damage to DNA by reactive oxygen, chlorine and nitrogen species: measurement, mechanism and the effects of nutrition. Mutat Res. 1999 ; 443 (1-2). 37-52
106. Balasubramanian B, Pogozelski WK, Tullius TD. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc Natl Acad Sci U S A. 1998 ; 95 (17). 9738-9743
107. Diamond MP, 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 (4). 926-934
108. Gomel V. The impact of microsurgery in gynecology. Clin Obstet Gynecol. 1980 ; 23 (4). 1301-1310
109. Winston RM. Microsurgery of the fallopian tube: from fantasy to reality. Fertil Steril. 1980 ; 34 (6). 521-530
110. Awonuga AO, Saed GM, Diamond MP. Laparoscopy in gynecologic surgery: adhesion development, prevention, and use of adjunctive therapies. Clin Obstet Gynecol. 2009 ; 52 (3). 412-422
111. Lundorff P, Hahlin M, Kallfelt B, Thorburn J, Lindblom B. Adhesion formation after laparoscopic surgery in tubal pregnancy: a randomized trial versus laparotomy. Fertil Steril. 1991 ; 55 (5). 911-915
112. Milingos S, Kallipolitis G, Loutradis D, et al. Adhesions: laparoscopic surgery versus laparotomy. Ann N Y Acad Sci. 2000 ; 900: 272-285
113. operative laparoscopy study group. Fertil Steril. 1991 ; 55 (4). 700-704
114. Ott DE. Desertification of the peritoneum by thin-film evaporation during laparoscopy. JSLS. 2003 ; 7 (3). 189-195
115. Yesildaglar N, Ordonez JL, Laermans I, Koninckx PR. The mouse as a model to study adhesion formation following endoscopic surgery: a preliminary report. Hum Reprod. 1999 ; 14 (1). 55-59
116. Michelson AM, Puget K. [Medical aspects of superoxide dismutases]. C R Seances Soc Biol Fil. 1979 ; 173 (2). 380-393
117. Lefaix JL, Delanian S, Leplat JJ, et al. Successful treatment of radiation-induced fibrosis using Cu/Zn-SOD and Mn-SOD: an experimental study. Int J Radiat Oncol Biol Phys. 1996 ; 35 (2). 305-312
118. Martin M, Lefaix J, Delanian S. TGF-beta1 and radiation fibrosis: a master switch and a specific therapeutic target?. Int J Radiat Oncol Biol Phys. 2000 ; 47 (2). 277-290
119. Batinic-Haberle I, Spasojevic I, Stevens RD, et al. New PEG-ylated Mn(III) porphyrins approaching catalytic activity of SOD enzyme. Dalton Trans. 2006 ; (4). 617-624
120. Ferrer-Sueta G, Hannibal L, Batinic-Haberle I, Radi R. Reduction of manganese porphyrins by flavoenzymes and submitochondrial particles: a catalytic cycle for the reduction of peroxynitrite. Free Radic Biol Med. 2006 ; 41 (3). 503-512
121. Vujaskovic Z, Batinic-Haberle I, Rabbani ZN, et al. A small molecular weight catalytic metalloporphyrin antioxidant with superoxide dismutase (SOD) mimetic properties protects lungs from radiation-induced injury. Free Radic Biol Med. 2002 ; 33 (6). 857-863
122. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002 ; 82 (1). 47-95
123. Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol. 1993 ; 21 (4). 433-441
124. Victory R, Saed GM, Diamond MP. Antiadhesion effects of docosahexaenoic acid on normal human peritoneal and adhesion fibroblasts. Fertil Steril. 2007 ; 88 (6). 1657-1662
125. Stadtman ER. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem. 1993 ; 62: 797-821
126. Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med. 2011 ; 51 (5). 1000-1013
127. Sies H, Stahl W, Sundquist AR. Antioxidant functions of vitamins. Vitamins E and C, beta-carotene, and other carotenoids. Ann N Y Acad Sci. 1992 ; 669: 7-20
128. Fletcher NM, Awonuga AO, Saed MG, Abu-Soud HM, Diamond MP, Saed GM. Lycopene, a powerful antioxidant, significantly reduces the development of the adhesion phenotype. Syst Biol Reprod Med. 2014 ; 60 (1). 14-20
129. Pennathur S, Maitra D, Byun J, et al. Potent antioxidative activity of lycopene: A potential role in scavenging hypochlorous acid. Free Radic Biol Med. 2010 ; 49 (2). 205-213
130. Reed KL, Stucchi AF, Leeman SE, Becker JM. Inhibitory effects of a neurokinin-1 receptor antagonist on postoperative peritoneal adhesion formation. Ann N Y Acad Sci. 2008 ; 1144: 116-126
131. Kluger Y, Weinbroum A, Ben-Avraham R, Galili Y, Klausner J, Rabau M. Reduction in formation of peritoneal adhesions by methylene blue in rats: a dose response study. Eur J Surg. 2000 ; 166 (7). 568-571
132. Gul A, Kotan C, Dilek I, Gul T, Tas A, Berktas M. Effects of methylene blue, indigo carmine solution and autologous erythrocyte suspension on formation of adhesions after injection into rats. J Reprod Fertil. 2000 ; 120 (2). 225-229
133. Mendes JB, Campos PP, Rocha MA, Andrade SP. Cilostazol and pentoxifylline decrease angiogenesis, inflammation, and fibrosis in sponge-induced intraperitoneal adhesion in mice. Life Sci. 2009 ; 84 (15-16). 537-543
134. Chegini N, Rong H, Bennett B, Stone IK. Peritoneal fluid cytokine and eicosanoid levels and their relation to the incidence of peritoneal adhesion. J Soc Gynecol Investig. 1999 ; 6 (3). 153-157
135. Saed GM, Jiang Z, Fletcher NM, Diamond MP. Modulation of the BCL-2/BAX ratio by interferon-gamma and hypoxia in human peritoneal and adhesion fibroblasts. Fertil Steril. 2008 ; 90 (5). 1925-1930
136. Saed GM, Diamond MP. Effects of interferon-gamma reverse hypoxia-stimulated extracellular matrix expression in human peritoneal and adhesion fibroblasts. Fertil Steril. 2006 ; 85 (suppl 1). 1300-1305
137. Yamanaka O, Saika S, Okada Y, Ooshima A, Ohnishi Y. Effects of interferon-gamma on human subconjunctival fibroblasts in the presence of TGFbeta1: reversal of TGFbeta-stimulated collagen production. Graefes Arch Clin Exp Ophthalmol. 2003 ; 241 (2). 116-124
138. Galijasevic S, Abdulhamid I, Abu-Soud HM. Melatonin is a potent inhibitor for myeloperoxidase. Biochemistry. 2008 ; 47 (8). 2668-2677
139. Proteasa G, Tahboub YR, Galijasevic S, Raushel FM, Abu-Soud HM. Kinetic evidence supports the existence of two halide binding sites that have a distinct impact on the heme iron microenvironment in myeloperoxidase. Biochemistry. 2007 ; 46 (2). 398-405
140. Saed GM, Al-Hendy A, Salama SA, Diamond MP. Adenovirus-mediated expression of cyclooxygenase-2 antisense reverse abnormal genetic profile of human adhesion fibroblasts. Fertil Steril. 2008 ; 89 (5 suppl). 1455-1460
141. Ahmad G, Duffy JM, Farquhar C, et al. Barrier agents for adhesion prevention after gynaecological surgery. Cochrane Database Syst Rev. 2008 ; (2). CD000475