The effect of carbon monoxide releasing molecule-2 (CORM-2) on healing of ischemic colon anastomosis in rats

The effect of carbon monoxide releasing molecule-2 (CORM-2) on healing of ischemic colon anastomosis in rats

Background/aim: Ischemia on the colon wall negatively affects healing of anastomosis. We were aimed to evaluate the effects of carbon monoxide releasing molecule-2 (CORM-2) on the healing of anastomosis in a rat model of the ischemic colon. Materials and methods: In this prospective study a total of 60 rats were randomly divided into three groups as colon transection and end-to-end anastomosis (Group I), colon transection, and end-to-end anastomosis following the induction of ischemia (Group II), and colon transection and end-to-end anastomosis following the induction of ischemia and treated with daily intraperitoneal administration of CORM-2 (Group III). Each group was also divided into two equal subgroups as postoperative 3rd and 7th day. Postoperative healing of anastomoses was evaluated by anastomosis burst pressure (ABP), tissue biomarkers including hydroxyproline (HP), malondialdehyde (MDA), glutathione (GSH), and histopathological findings. Results: In the ischemic group treated with CORM-2, lower MDA and higher HP levels were observed in comparison to the untreated ischemic group on the 3rd day. GSH and HP levels were higher and MDA levels was lower in the ischemic rats treated with CORM-2 than in the ischemic untreated rats on the 7th day. In the ischemic group treated with CORM-2, the mucosal epithelial score decreased and the neoangiogenesis score increased compared to the untreated rats on the 7th day. Conclusion: In ischemic colon anastomosis, reduces cell destruction by suppressing the oxidative reaction, and strengthening the antioxidative mechanisms of the cells. It also increases collagen formation, epithelial development, and neoangiogenesis.Key words: Anastomotic leak, angiogenesis, necrosis, ischemia, carbon monoxide releasing molecule-2 (CORM-2)

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  • 1. Murrell ZA, Stamos MJ. Reoperation for anastomotic failure. Clinics in Colon and Rectal Surgery 2006; 19 (4): 213- 216. doi: 10.1055/s-2006-956442
  • 2. Shaban F, Carney K, McGarry K, Holtham S. Perforated diverticulitis: to anastomose or not to anastomose? A systematic review and meta-analysis. International Journal of Surgery 2018; 58: 11-21. doi: 10.1016/j.ijsu.2018.08.009
  • 3. Parra-Membrives P, Ruiz-Luque V, Escudero-Severín C, Aguilar-Luque J, Méndez-García V. Effect of pentoxifylline on the healing of ıschemic colorectal anastomoses. Diseases of the Colon & Rectum 2007; 50 (3): 369-375. doi: 10.1007/s10350- 006-0803-z
  • 4. Tseng J, Loper B, Jain M, Lewis AV, Margulies DR et al. Predictive factors of mortality after colectomy in ischemic colitis: an ACSNSQIP database study. Trauma Surgery & Acute Care Open 2017; 2 (1): e000126. doi: 10.1136/tsaco-2017-000126
  • 5. Pehlivanlı F, Aydin O, Karaca G, Aydin G, Devrim T et al. Healing of ischemic colon anastomosis in rats could be provided by administering dexpanthenol or coenzyme Q10. Journal of Clinical Medicine 2018; 7 (7): 161. doi: 10.3390/jcm7070161
  • 6. Monnet E, Smeak DD. Gastrointestinal Healing. In: Monnet E, Smeak DD (editors). Gastrointestinal Surgical Techniques in Small Animals. 1st ed. Hoboken, NJ, USA: Wiley-Blackwell; 2020. pp. 1-8. doi: 10.1002/9781119369257.ch1
  • 7. Thompson SK, Chang EY, Jobe BA. Clinical review: healing in gastrointestinal anastomoses. Part I. Microsurgery 2006; 26 (3): 131-136. doi: 10.1002/micr.20197
  • 8. Enestvedt CK, Thompson SK, Chang EY, Jobe BA. Clinical review: healing in gastrointestinal anastomoses. Part II. Microsurgery 2006; 26 (3): 137-143. doi: 10.1002/micr.20198
  • 9. De Oliveira THC, Souza DG, Teixeira MM, Amaral FA. Tissue dependent role of ptx3 during ischemia-reperfusion injury. Frontiers in Immunology 2019; 10: 1461. doi: 10.3389/ fimmu.2019.01461
  • 10. Reischl S, Wilhelm D, Friess H, Neumann P. Innovative approaches for induction of gastrointestinal anastomotic healing: an update on experimental and clinical aspects. Langenbeck’s Archives of Surgery 2020; 1-10. doi: 10.1007/ s00423-020-01957-1
  • 11. Motterlini R. Carbon monoxide-releasing molecules (CORMs): vasodilatory, anti-ischaemic and anti-inflammatory activities: Figure 1. Biochemical Society Transactions 2007; 35 (5): 1142-1146. doi: 10.1042/bst0351142
  • 12. Katada K, Bihari A, Mizuguchi S, Yoshida N, Yoshikawa T et al. carbon monoxide liberated from CO-releasing molecule (CORM-2) attenuates ischemia/reperfusion (I/R)-induced inflammation in the small intestine. Inflammation 2009; 33 (2): 92-100. doi: 10.1007/s10753-009-9162-y
  • 13. Ahanger AA, Prawez S, Kumar D, Prasad R, Amarpal SK et al. Wound healing activity of carbon monoxide liberated from CO-releasing molecule (CO-RM). Naunyn-Schmiedeberg’s Archives of Pharmacology 2011; 384 (1): 93-102. doi: 10.1007/ s00210-011-0653-7
  • 14. Jamall IS, Finelli VN, Que Hee SQ. A simple method determines nanogram levels of 4- hydroxyproline in biological tissues. Analytical Biochemistry 1981; 112 (1): 70-75. doi: 10.1016/0003-2697(81)90261-X
  • 15. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry 1978; 86 (1): 271-278. doi: 10.1016/0003-2697 (78)90342-1
  • 16. Ellman GL. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 1959; 82 (1): 70-77. doi: 10.1016/0003- 9861(59)90090-6
  • 17. Verhofstadt MH, Lange WP, Van Der Laak JA, Verhofstad AAJ, Hendriks T. Microscopic analysis of anastomotic healing in the intestine of normal and diabetic rats. Diseases of the Colon & Rectum 2001; 44 (3): 423-431. doi:10.1007/bf02234744
  • 18. Ehrlich HP, Hunt TK. The effects of cortisone and anabolic steroids on the tensile strength of healing wounds. Annals of Surgery 1969; 170 (2): 203-206. doi: 10.1097/00000658-196908000-00007
  • 19. Phillips JD, Kim CS, Fonkalsrud EW, Zeng H, Dindar H. Effect of chronic corticosteroid and vitamin A on the healing of intestinal anastomoses. The American Journal of Surgery 1992; 163 (1): 71-77. doi: 10.1016/0002-9610(92)90255-P
  • 20. Irkorucu O, Ucan BH, Cakmak GK, Emre AU, Tascilar O et al. Does sildenafil reverse the adverse effects of ischemia on ischemic colon anastomosis: yes, “no.” International Journal of Surgery 2009; 7 (1): 39-43. doi: 10.1016/j.ijsu.2008.10.003
  • 21. İnan A, Sürgit O, Şen M, Akpınar A, Bozer M. Etofenamate and anastomoses of the colon in rats. Turkish Journal of Medical Sciences 2009; 39 (5): 713-718. doi: 10.3906/sag-0901-32
  • 22. Sarıbeyoğlu K, Baca B, Hamzaoğlu İ, Pekmezci S, Karahasanoğlu T et al. does becaplermin (platelet-derived growth factor-BB) reverse detrimental effects of ıschemia on colonic anastomosis? Diseases of the Colon & Rectum 2003; 46 (4): 516-520. doi:10.1007/s10350-004-6592-3
  • 23. Tsikas D. Assessment of lipid peroxidation by measuring malondialdehyde and relatives in biological samples: analytical and biological challenges. Analytical Biochemistry 2017; 524: 13-30. doi: 10.1016/j.ab.2016.10.021
  • 24. Guan LY, Fu PY, Li PD, Li ZN, Liu HY et al. Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide. World Journal of Gastrointestinal Surgery 2014; 6 (7): 122-128. doi: 10.4240/wjgs.v6.i7.122
  • 25. Liu Y, Wang X, Xu X, Qin W, Sun B. Carbon monoxide releasing molecule-2 (CORM-2)-liberated CO ameliorates acute pancreatitis. Molecular Medicine Reports 2019; 19: 5142- 5152. doi: 10.3892/mmr.2019.10173
  • 26. Adach W, Olas B. The role of CORM-2 as a modulator of oxidative stress and hemostatic parameters of human plasma in vitro. PLoS One 2017; 12 (9): e0184787. doi: 10.1371/journal. pone.0184787
  • 27. Meng X, Fei D, Liu M, Yang S, Song N et al. Carbon monoxide-releasing molecule-2 suppresses thrombomodulin and endothelial protein C receptor expression of human umbilical vein endothelial cells induced by lipopolysaccharide in vitro. Medicine 2017; 96 (21): e6978. doi: 10.1097/ md.0000000000006978
  • 28. Magierowska K, Wojcik D, Chmura A, Bakalarz D, Wierdak M et al. Alterations in gastric mucosal expression of calcitonin gene-related peptides, vanilloid receptors, and heme oxygenase-1 mediate gastroprotective action of carbon monoxide against ethanol-ınduced gastric mucosal lesions. International Journal of Molecular Sciences 2018; 19 (10): 2960. doi: 10.3390/ijms19102960
  • 29. Ikeda H, Suzuki Y, Suzuki M, Koike M, Tamura J et al. Apoptosis is a major mode of cell death caused by ischaemia and ischaemia/reperfusion injury to the rat intestinal epithelium. Gut 1998; 42 (4): 530-537. doi: 10.1136/gut.42.4.530
  • 30. Němeček D, Dvořáková M, Heroutová I, Chmelíková E, Sedmíková M. Anti apoptotic properties of carbon monoxide in porcine oocyte during in vitro aging. Peerj 2017; 5: e3876. doi: 10.7717/peerj.3876
  • 31. Takagi T, Naito Y, Uchiyama K, Suzuki T, Hirata I et al. Carbon monoxide liberated from carbon monoxide-releasing molecule exerts an anti-inflammatory effect on dextran sulfate sodiumınduced colitis in mice. Digestive Diseases and Sciences 2011; 56: 1663-1671. doi: 10.1007/s10620-010-1484-y
  • 32. Ault JG, Lawrance DA. Glutathione distribution in normal and oxidatively stressed cells. Experimental Cell Research 2003; 285 (1): 9-14. doi: 10.1016/S0014- 4827(03)00012-0
  • 33. Aktop S, Çevreli B, Genç D, Kaşikçi ES, Üstündağ NÇ et al. Effects of ankaferd blood stopper on dermal healing in diabetic rats. Turkish Journal of Medical Sciences 2017; 47: 675-680. doi: 10.3906/sag-1604-145
  • 34. Sawle P, Foresti R, Mann BE, Johnson TR, Green CJ et al. Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages. British Journal of Pharmacology 2005; 145 (6): 800-810. doi: 10.1038/ sj.bjp.0706241
  • 35. Adas G, Arikan S, Karatepe O, Kemik O, Ayhan S. Mesenchymal stem cells improve the healing of ischemic colonic anastomoses (experimental study). Langenbeck’s Archives of Surgery 2010; 396 (1): 115-126. doi: 10.1007/s00423-010-0717-z
  • 36. Çekiç SG, Çekiç EG, Baydar D, Tuncer M, Soydan G. Vascular responses of aortic, renal, and uterine arteries in suramininduced preeclampsia-like syndrome in rats. Turkish Journal of Medical Sciences 2018; 48 (6): 1328-1339. doi: 10.3906/sag1807-254
  • 37. Yadav V, Matsakas A, Lorca S, Narkar VA. PGC1β activates an antiangiogenic program to repress neoangiogenesis in muscle ischemia. Cell Reports 2014; 8 (3): 783-797. doi: 10.1016/j. celrep. 2014.06.040
  • 38. Choi YK, Kim CK, Lee H, Jeoung D, Ha KS et al. Carbonmonoxide promotes VEGF expression by increasing HIF-1α protein level via two distinct mechanisms, translation activation and stabilization of HIF-1α protein. Journal of Biological Chemistry 2010; 285 (42): 32116-32125. doi: 10.1074/jbc.M110.131284
  • 39. Zhang S, Zheng S, Wang X, Shi Q, Wang X et al. Carbon monoxide-releasing molecule-2 reduces ıntestinal epithelial tight-junction damage and mortality in septic rats. PLoS One 2015; 10 (12): e0145988. doi:10.1371/journal.pone.0145988
  • 40. Uchiyama K, Naito Y, Takagi T, Mizushima K, Hayashi N et al. Carbon monoxide enhances colonic epithelial restitution via FGF15 derived from colonic myofibroblasts. Biochemical and Biophysical Research Communications 2010; 391 (1): 1122- 1126. doi: 10.1016/j.bbrc.2009.12.035
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