N-acetyl-L-cysteine decreases intra-abdominal adhesion formation through the upregulation of peritoneal fibrinolytic activity and antioxidant defenses

Surgery

Volumn 149, Issue 6, 2011, Pages 801-812

  Chu, Daniel I ^a   Lim, Rizal ^a   Heydrick, Stanley ^a   Gainsbury, Melanie L ^a   Abdou, Rami ^a   D'Addese, Laura ^a   Reed, Karen L ^a   Stucchi, Arthur F ^a   Becker, James M ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 ISOPROSTANE; ACETYLCYSTEINE; GLUTATHIONE; PLASMINOGEN ACTIVATOR INHIBITOR 1; TISSUE PLASMINOGEN ACTIVATOR;

ABDOMINAL ADHESION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; EXPERIMENTAL MODEL; FIBRINOLYSIS; HUMAN; HUMAN CELL; MALE; MESOTHELIUM CELL; NONHUMAN; PERITONEAL FLUID; PERITONEUM; PERITONEUM ADHESION; PRESSURE MEASUREMENT; PRIORITY JOURNAL; RAT; UPREGULATION; WISTAR RAT; WOUND HEALING;

ABDOMEN; ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; DINOPROST; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FIBRINOLYSIS; GLUTATHIONE; HUMANS; INJECTIONS, INTRAPERITONEAL; MALE; MODELS, ANIMAL; OXIDATIVE STRESS; PERITONEUM; PLASMINOGEN ACTIVATOR INHIBITOR 1; RATS; RATS, WISTAR; TISSUE ADHESIONS; TISSUE PLASMINOGEN ACTIVATOR; UP-REGULATION; WOUND HEALING;

EID: 79957745738     PISSN: 00396060     EISSN: 15327361     Source Type: Journal    
DOI: 10.1016/j.surg.2011.02.015     Document Type: Article

References (55)

1. Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL. Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Recent advances in prevention and management. Dig Surg 2001;18:260-73.
2. Becker JM, Dayton MT, Fazio VW, Beck DE, Stryker SJ, Wexner SD, et al. Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane: a prospective, randomized, double-blind multicenter study. J Am Coll Surg 1996;183:297-306.
3. Wiseman DM. Disorders of adhesions or adhesion-related disorder: monolithic entities or part of something bigger - CAPPS? Semin Reprod Med 2008;26:356-68.
4. ten Raa S, van den Tol MP, Sluiter W, Hofland LJ, van Eijck CH, Jeekel H. The role of neutrophils and oxygen free radicals in post-operative adhesions. J Surg Res 2006;136:45-52.
5. Reed KL, Heydrick SJ, Aarons CB, Prushik S, Gower AC, Stucchi AF, 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:G544-51.
6. Reed KL, Stucchi AF, Becker JM. Pharmacologic inhibition of adhesion formation and peritoneal tissue-type plasminogen activator activity. Semin Reprod Med 2008;26:331-40.
7. Gotloib L, Wajsbrot V, Cuperman Y, Shostak A. Acute oxidative stress induces peritoneal hyperpermeability, mesothelial loss, and fibrosis. J Lab Clin Med 2004;143:31-40. (Pubitemid 38156414)
8. Holmdahl L. The role of fibrinolysis in adhesion formation. Eur J Surg Suppl 1997;577:24-31. (Pubitemid 27115967)
9. 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;84:537-43.
10. Reed KL, Fruin AB, Gower AC, Stucchi AF, Leeman SE, Becker JM. A neurokinin 1 receptor antagonist decreases postoperative peritoneal adhesion formation and increases peritoneal fibrinolytic activity. Proc Natl Acad Sci USA 2004;101:9115-20. (Pubitemid 38781620)
11. Aarons CB, Cohen PA, Gower A, Reed KL, Leeman SE, Stucchi AF, et al. Statins (HMG-CoA reductase inhibitors) decrease postoperative adhesions by increasing peritoneal fibrinolytic activity. Ann Surg 2007;245:176-84. (Pubitemid 46148475)
12. Lim R, Morrill JM, Prushik SG, Reed KL, Gower AC, Leeman SE, et al. An FDA approved neurokinin-1 receptor antagonist is effective in reducing intraabdominal adhesions when administered intraperitoneally, but not orally. J Gastrointest Surg 2008;12:1754-61.
13. Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009;7:65-74.
14. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 2009;390:191-214.
15. Heydrick SJ, Reed KL, Cohen PA, Aarons CB, Gower AC, Becker JM, et al. Intraperitoneal administration of methylene blue attenuates oxidative stress, increases peritoneal fibrinolysis, and inhibits intraabdominal adhesion formation. J Surg Res 2007;143:311-9. (Pubitemid 350101560)
16. Rijhwani A, Sen S, Gunasekaran S, Ponnaiya J, Balasubramanian KA, Mammen KE. Allopurinol reduces the severity of peritoneal adhesions in mice. J Pediatr Surg 1995;30:533-7.
17. Hatipoǧlu A, Türkyilmaz Z, Mert S. The effects of melatonin on postoperative intraabdominal adhesion formation. Yonsei Med J 2007;48:659-64. (Pubitemid 47496729)
18. Wolf SJ, Heard K, Sloan EP, Jagoda AS, American College of Emergency Physicians Clinical Policies Subcommittee (Writing Committee) on Critical Issues in the Management of Patients Presenting to the Emergency Department with Acetaminophen Overdose. Clinical policy: critical issues in the management of patients presenting to the emergency department with acetaminophen overdose. J Emerg Nurs 2008;34:e1-18.
19. Nigwekar SU, Kandula P. N-acetylcysteine in cardiovascular-surgery- associated renal failure: a meta-analysis. Ann Thorac Surg 2009;87:139-47.
20. Lieberman J. The appropriate use of mucolytic agents. Am J Med 1970;49:1-4.
21. Ege T, Eskiocak S, Edis M, Duran E. The role of N-acetylcysteine in lower extremity ischemia/reperfusions. J Cardiovasc Surg (Torino) 2006;47:563-8. (Pubitemid 44696784)
22. Kabali B, Girgin S, Gedik E, Ozturk H, Kale E, Buyukbayram H. N-acetylcysteine prevents deleterious effects of ischemia/reperfusion injury on healing of colonic anastomosis in rats. Eur Surg Res 2009;43:8-12.
23. Balansky R, Ganchev G, Iltcheva M, Steele VE, De Flora S. Prenatal N-acetylcysteine prevents cigarette smoke-induced lung cancer in neonatal mice. Carcinogenesis 2009;30:1398-401.
24. De Flora S, Izzotti A, D'Agostini F, Balansky RM. Mechanisms of N-acetylcysteine in the prevention of DNA damage and cancer, with special reference to smoking-related endpoints. Carcinogenesis 2001;22:999-1013. (Pubitemid 32633597)
25. Pata O, Yazici G, Apa DD, Tok E, Oz U, Kaplanoglu M, et al. The effect of inducible nitric oxide synthase on postoperative adhesion formation in rats. Eur J Obstet Gynecol Reprod Biol 2004;117:64-9. (Pubitemid 39335865)
26. Reed KL, Fruin AB, Bishop-Bartolomei KK, Gower AC, Nicolaou M, Stucchi AF, et al. Neurokinin-1 receptor and substance P messenger RNA levels increase during intraabdominal adhesion formation. J Surg Res 2002;108:165-72. (Pubitemid 35373829)
27. Dickey DT, Muldoon LL, Doolittle ND, Peterson DR, Kraemer DF, Neuwelt EA. Effect of N-acetylcysteine route of administration on chemoprotection against cisplatin-induced toxicity in rat models. Cancer Chemother Pharmacol 2008;62:235-41. (Pubitemid 351692079)
28. Hadaegh A, Burns J, Burgess L, Rose R, Rowe E, LaMorte WW, et al. Effects of hyaluronic acid/carboxymethylcellulose gel on bowel anastomoses in the New Zealand white rabbit. J Gastrointest Surg 1997;1:569-75. (Pubitemid 127437052)
29. Prushik SG, Aarons CB, Matteotti R, Reed KL, Gower AC, Leeman SE, et al. A neurokinin 1 receptor antagonist decreases adhesion reformation after laparoscopic lysis of adhesions in a rat model of adhesion formation. Surg Endosc 2007;21:1790-5. (Pubitemid 47407728)
30. Menzies D, Ellis H. Intra-abdominal adhesions and their prevention by topical tissue plasminogen activator. J R Soc Med 1989;82:534-5. (Pubitemid 19211411)
31. Evans DM, McAree K, Guyton DP, Hawkins N, Stakleff K. Dose dependency and wound healing aspects of the use of tissue plasminogen activator in the prevention of intraabdominal adhesions. Am J Surg 1993;165:229-32. (Pubitemid 23281372)
32. Jaulmes A, Sansilvestri-Morel P, Rolland-Valognes G, Bernhardt F, Gaertner R, Lockhart BP, et al. Nox4 mediates the expression of plasminogen activator inhibitor-1 via p38 MAPK pathway in cultured human endothelial cells. Thromb Res 2009;124:439-46.
33. Whawell SA, Vipond MN, Scott-Coombes DM, Thompson JN. Plasminogen activator inhibitor 2 reduces peritoneal fibrinolytic activity in inflammation. Br J Surg 1993;80:107-9. (Pubitemid 23071492)
34. Ohan J, Gilbert MA, Brouland JP, Rougier JP, Trugnan G, Wassef M, et al. Phenotypic and functional characteristics of porcine peritoneal mesothelial cells. Vitro Cell Dev Biol Anim 1999;35:625-34. (Pubitemid 30007661)
35. El Midaoui A, Ismael MA, Lu H, Fantus IG, de Champlain J, Couture R. Comparative effects of N-acetyl-L-cysteine and ramipril on arterial hypertension, insulin resistance, and oxidative stress in chronically glucose-fed rats. Can J Physiol Pharmacol 2008;86:752-60.
36. Kumar S, Sitasawad SL. N-acetylcysteine prevents glucose/glucose oxidase-induced oxidative stress, mitochondrial damage and apoptosis in H9c2 cells. Life Sci 2009;84:328-36.
37. Allegra L, Dal Sasso M, Bovio C, Massoni C, Fonti E, Braga PC. Human neutrophil oxidative bursts and their in vitro modulation by different N-acetylcysteine concentrations. Arzneimittelforschung 2002;52:669-76.
38. Vasu VT, de Cruz SJ, Houghton JS, Hayakawa KA, Morrissey BM, Cross CE, et al. Evaluation of thiol-based antioxidant therapeutics in cystic fibrosis sputum: focus on myeloperoxidase. Free Radic Res 2011;45:165-76.
39. Moon C, Lee YJ, Park HJ, Chong YH, Kang JL. N-acetylcysteine inhibits RhoA and promotes apoptotic cell clearance during intense lung inflammation. Am J Respir Crit Care Med 2010;181:374-87.
40. Nielsen VG, Crow JP, Zhou F, Parks DA. Peroxynitrite inactivates tissue plasminogen activator. Anesth Analg 2004;98:1312-7; table of contents.
41. Feng YH, Hart G. In vitro oxidative damage to tissue-type plasminogen activator: a selective modification of the biological functions. Cardiovasc Res 1995;30:255-61.
42. Swiatkowska M, Szemraj J, Al-Nedawi KN, Pawlowska Z. Reactive oxygen species upregulate expression of PAI-1 in endothelial cells. Cell Mol Biol Lett 2002;7:1065-71. (Pubitemid 36119538)
43. Cheng JJ, Chao YJ, Wung BS, Wang DL. Cyclic strain-induced plasminogen activator inhibitor-1 (PAI-1) release from endothelial cells involves reactive oxygen species. Biochem Biophys Res Commun 1996;225:100-5. (Pubitemid 26285402)
44. Pascual I, Fernández de Miguel G, García Arranz M, García-Olmo D. Biosutures improve healing of experimental weak colonic anastomoses. Int J Colorectal Dis 2010;25:1447-51.
45. Dinc S, Ozaslan C, Kuru B, Karaca S, Ustun H, Alagol H, et al. Methylene blue prevents surgery-induced peritoneal adhesions but impairs the early phase of anastomotic wound healing. Can J Surg 2006;49:321-8. (Pubitemid 44870843)
46. Gehlbach DL, O'Hair KC, Parks AL, Rosa C. Combined effects of tissue plasminogen activator and carboxymethylcellulose on adhesion reformation in rabbits. Int J Fertil Menopausal Stud 1994;39:172-6. (Pubitemid 24204006)
47. Arfsten DP, Johnson EW, Wilfong ER, Jung AE, Bobb AJ. Distribution of radio-labeled N-Acetyl-L-Cysteine in Sprague-Dawley rats and its effect on glutathione metabolism following single and repeat dosing by oral gavage. Cutan Ocul Toxicol 2007;26:113-34. (Pubitemid 47027131)
48. Greene AK, Alwayn IP, Nose V, Flynn E, Sampson D, Zurakowski D, et al. Prevention of intra-abdominal adhesions using the antiangiogenic COX-2 inhibitor celecoxib. Ann Surg 2005;242:140-6. (Pubitemid 40917978)
49. Kim S, Lee S, Greene AK, Arsenault DA, Le H, Meisel J, et al. Inhibition of intra-abdominal adhesion formation with the angiogenesis inhibitor sunitinib. J Surg Res 2008;149:115-9.
50. Jackson EK. Intraperitoneal administration of adenosine inhibits formation of abdominal adhesions. Dis Colon Rectum 2004;47:1390-6. (Pubitemid 39180217)
51. Yeo Y, Adil M, Bellas E, Astashkina A, Chaudhary N, Kohane DS. Prevention of peritoneal adhesions with an in situ crosslinkable hyaluronan hydrogel delivering budesonide. J Control Release 2007;120:178-85. (Pubitemid 47064479)
52. Ayten R, Cetinkaya Z, Girgin M, Ozercan I, Ustundag B, Aygen E. The effects of intraperitoneal sildenafil administration on healing of left colonic anastomoses and intra-abdominal adhesion formation in the presence of intra-abdominal infection. Dis Colon Rectum 2008;51:1837-41.
53. Koc O, Duran B, Topcuoglu A, Bugdayci G, Yilmaz F, Dönmez M. Intraperitoneal administration of single dose type I collagen or low dose melatonin to prevent intraperitoneal adhesion formation: a comparative study. Eur J Obstet Gynecol Reprod Biol 2009;145:209-13.
54. Hill-West JL, Dunn RC, Hubbell JA. Local release of fibrinolytic agents for adhesion prevention. J Surg Res 1995;59:759-63. (Pubitemid 26013901)
55. Risberg B. Adhesions: preventive strategies. Eur J Surg Suppl 1997;577:32-9. (Pubitemid 27115968)