THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION

Gizem Deynez; Ece Miser Salihoğlu; İpek Süntar

doi:10.23902/trkjnat.1309119

TR EN

THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION

Abstract

Peritoneal adhesion occurs as a result of surgery, peritoneal injury, peritonitis, hypoxia, and ischemia. Surgical trauma causes many pathophysiological processes which include inflammation, oxidation, coagulation, fibrinolysis, cell proliferation, and apoptosis. After intra-abdominal operations, the adhesion tissue may occur on the peritoneal surface due to low fibrinolytic activity. This may result in permanent excessive adhesion tissue bands instead of properly formed fibrin structures. Therefore, anticoagulant, thrombolytic, and fibrinolytic activities have a key role in preventing peritoneal adhesion. Indeed, several studies have been conducted to find out new and effective agents against intra-abdominal adhesion. Thus, revealing the causes, development processes, and investigation techniques are highly important for designing and conducting such scientific studies. In this context, this study aims to summarize the pathophysiological processes of above-mentioned activities and to emphasize their importance in the peritoneal adhesion model as well as to explain the evaluation methods, particularly in terms of the investigation of natural products.

Keywords

References

1. Ablat, N., Ablimit, M., Abudoukadier, A., Kadeer, B. & Yang, L. 2021. Investigating the hemostatic effect of medicinal plant Arnebia euchroma (Royle) I.M.Johnst extract in a mouse model. Journal of Ethnopharmacology, 278: 114306. https://doi.org/10.1016/j.jep.2021.114306
2. Ahmed, A., Tariq, M., Hussain, M., Andleeb, A., Masoud, M.S., Ali, I., Mraiche, F. & Hasan, A. 2019. Phenolic contents-based assessment of therapeutic potential of Syzygium cumini leaves extract. Plos one, 14(8): e0221318. https://doi.org/10.1371/journal.pone.0221318
3. Ahmed, F. & Rahman, M.S. 2016. Preliminary assessment of free radical scavenging, thrombolytic and membrane stabilizing capabilities of organic fractions of Callistemon citrinus (Curtis.) skeels leaves. BMC Complementary and Alternative Medicine, 16: 247. https://doi.org/10.1186/s12906-016-1239-1
4. Akter, S., Jahan, I., Khatun, R., Khan, M.F., Arshad, L., Jakaria, & Haque, A. 2021. Pharmacological insights into Merremia vitifolia (Burm.f.) Hallier f. leaf for its antioxidant, thrombolytic, anti-arthritic and anti-nociceptive potential. Bioscience Reports, 41(1): BSR20203022. https://doi.org/10.1042/BSR20203022
5. Alam, N., Banu, N., Aziz, A.I., Barua, N., Ruman, U., Jahan, I., Chy, F.J., Denath, S., Paul, A., Chy, N.U., Sayeed, M.A., Emran, T.B. & Gandara, J.S. 2021. Chemical profiling, pharmacological insights and in silico studies of methanol seed extract of Sterculia foetida. Plants, 10(6): 1135. https://doi.org/10.3390/plants10061135
6. Alam, S., Emon, N.U., Shahriar, S., Richi, F.T., Haque, M.R., Islam, M.N., Sakib, S.A. & Ganguly, A. 2020. Pharmacological and computer-aided studies provide new insights into Millettia peguensis Ali (Fabaceae). Saudi Pharmaceutical Journal, 28(12): 1777-1790. https://doi.org/10.1016/j.jsps.2020.11.004
7. Alamgeer, Tarar, M., Hasan, U.H. & Saleem, M. 2018. Evaluation of anticoagulant and thrombolytic activity of Berberis orthobotrys in animal model. Bangladesh Journal of Pharmacology, 13(2): 196-202. https://doi.org/10.3329/bjp.v13i2.36201
8. Ali, S., Sayem, S.A.J., Quah, H.Y., Lee, E.B., Birhanu, B.T., Suk, K. & Park, S.C. 2021. Investigation of potential antioxidant, thrombolytic and neuropharmacological activities of Homalomena aromatica leaves using experimental and in silico approaches. Molecules, 26(4): 975. https://doi.org/10.3390/molecules26040975

9. Almarshad, F.M. 2019. Evaluation of fibrinolytic efficacy of Averrhoa Bilimbi Linn. by using euglobulin lysis time method. International Journal of Medical Research & Health Sciences, 8(9): 21-24.
10. Altaf, F., Wu, S. & Kasim, V. 2021. Role of Fibrinolytic Enzymes in Anti-Thrombosis Therapy. Frontiers in Molecular Biosciences, 8: 680397. https://doi.org/10.3389/fmolb.2021.680397
11. Ambler, D.R., Fletcher, N.M., Diamond, M.P. & Saed, G.M. 2012. Effects of hypoxia on the expression of inflammatory markers IL-6 and TNF-a in human normal peritoneal and adhesion fibroblasts. Systems Biology İn Reproductive Medicine, 58(6): 324-329. https://doi.org/10.3109/19396368.2012.713439
12. Amer, A.A., Elgohary, R., Ibrahim, F.M. & Taha, H.S. 2023. Anticoagulant effect of Feijoa sellowiana extracts generated by different biotechnological techniques. Heliyon, 9(4): e15444. https://doi.org/10.1016/j.heliyon.2023.e15444
13. Ansari, F., Soltan Mohammadi, N., Naderi, G., Sadegh Sabet, M. & Karimi, A. 2011. Study of garlic effect on fibrinolytic activity of the blood clot in vitro. Iranian Journal of Pediatric Hematology Oncology. 1(2): 48-52.
14. Ar’Rajab, A., Dawidson, I., Sentementes, J., Sikes, P., Harris, R. & Mileski, W. 1995. Enhancement of peritoneal macrophages reduces postoperative peritoneal adhesion formation. Journal of Surgical Research, 58(3): 307-312. https://doi.org/10.1006/jsre.1995.1048
15. Arung, W., Meurisse, M. & Detry, O. 2011. Pathophysiology and prevention of postoperative peritoneal adhesions. World Journal of Gastroenterology, 17(41): 4545-4553. https://doi.org/10.3748/wjg.v17.i41.4545
16. Asghar, M.A., Yousuf, R.I., Shoaib, M.H. & Asghar, M.A. 2020. Antibacterial, anticoagulant and cytotoxic evaluation of biocompatible nanocomposite of chitosan loaded green synthesized bioinspired silver nanoparticles. International Journal of Biological Macromolecules, 160: 934-943. https://doi.org/10.1016/j.ijbiomac.2020.05.197
17. Astrup, T. & Mullertz, S. 1952. The fibrin plate method for estimating fibrinolytic activity. Archives of Biochemistry and Biophysics, 40(2): 346-351. https://doi.org/10.1016/0003-9861(52)90121-5
18. Banerjee, A., Chisti, Y. & Banerjee, U.C. 2004. Streptokinase-a clinically useful thrombolytic agent. Biotechnology Advances, 22(4): 287-307. https://doi.org/10.1016/j.biotechadv.2003.09.004
19. Bijak, M., Ziewiecki, R., Saluk, J., Ponczek, M., Pawlaczyk, I., Krotkiewski, H., Wachowicz, B., Nowak, P. 2014. Thrombin inhibitory activity of some polyphenolic compounds. Medicinal Chemistry Research, 23(5): 2324-2337. https://doi.org/10.1007/s00044-013-0829-4
20. Boron, W.F. & Boulpaep, E.L. 2005. Medical physiology (Updated ed.), Philadelphia: Elsevier.
21. Chaity, F.R., Khatun, M. & Rahman, M.S. 2016. In vitro membrane stabilizing, thrombolytic and antioxidant potentials of Drynaria quercifolia L., a remedial plant of the Garo tribal people of Bangladesh. BMC Complementary and Alternative Medicine, 16: 184. https://doi.org/10.1186/s12906-016-1170-5
22. Cheong, Y.C., Laird, S.M., Li, T.C., Shelton, J.B., Ledger, W.L. & Cooke, I.D. 2001. Peritoneal healing and adhesion formation/reformation. Human Reproduction Update, 7(6): 556-566. https://doi.org/10.1093/humupd/7.6.556
23. Choi, H.S. & Sa, Y.S. 2001. Fibrinolytic and antithrombotic protease from Spirodela polyrhiza. Bioscience, Biotechnology, and Biochemistry, 65(4): 781-786. https://doi.org/10.1271/bbb.65.781
24. Choi, J.H., Kim, D.W., Park, S.E., Lee, H.J., Kim, K.M., Kim, K.J., Kim, M.K., Kim, S.J. & Kim, S. 2015. Anti-thrombotic effect of rutin isolated from Dendropanax morbifera Leveille. Journal of Bioscience and Bioengineering, 120(2): 181-186. https://doi.org/10.1016/j.jbiosc.2014.12.012
25. Chourasia, S.R., Kashyap, R.S., Purohit, H.J., Deopujari, J.Y., Taori, G.M. & Daginawala, H.F. 2011. In-vitro clot lytic potential of Fagonia arabica: a comparative study of two methods. Blood Coagulation and Fibrinolysis, 22(4): 288-294. https://doi.org/10.1097/MBC.0b013e32834512d8
26. Chowdhury, R., Chowdhury, K.H., Hanif, N.B., Sayeed, M.A., Mouah, J., Mahmud, I., Kamal, M., Chy, N.U. & Adnan. 2020. An integrated exploration of pharmacological potencies of Bischofia javanica (Blume) leaves through experimental and computational modeling. Heliyon, 6: e04895. https://doi.org/10.1016/j.heliyon.2020.e04895
27. Chowdhury, S., Ghosh, S. & Gond, S.K. 2022. Anti-MRSA and clot lysis activities of Pestalotiopsis microspora isolated from Dillenia pentagyna Roxb. Journal of Basic Microbiology, 63(3-4): 340-358. https://doi.org/10.1002/jobm.202200294
28. Clercq, K.D., Schelfhout, C., Bracke, M., Wever, O.D., Bockstal, M.V., Ceelen, W., Remon, J.P. & Vervaet, C. 2016. Genipin-crosslinked gelatin microspheres as a strategy to prevent postsurgical peritoneal adhesions: In vitro and in vivo characterization. Biomaterials, 96: 33-46. https://doi.org/10.1016/j.biomaterials.2016.04.012
29. Colucci, M., Paramo, J.A. & Collen, D. 1985. Generation in plasma of a fast-acting inhibitor of plasminogen activator in response to endotoxin stimulation. Journal of Clinical Investigation, 75(3): 818-824. https://doi.org/10.1172/JCI111777
30. da Costa e Silva, P.E., de Barros, R.C., Albuquerque W.W.C., Brandão, R.M.P., Bezerra, R.P. & Porto, A.L.F. 2018. In vitro thrombolytic activity of a purified fibrinolytic enzyme from Chlorella vulgaris. Journal of Chromatography B, 1092: 524-52. https://doi.org/10.1016/j.jchromb.2018.04.040
31. Diamond, M.P. & Decherney, A.H. 1987. Pathogenesis of adhesion formation/reformation: Application to reproductive pelvic surgery. Microsurgery, 8(2): 103-107. https://doi.org/10.1002/micr.1920080215
32. DiZerega, G.S. & Rodgers K.E. 1992. Peritoneal surgery, New York: Springer-Verlag Inc, 1-25.
33. Duarte da Luz, J.R., Silva do Nascimento, T.E., Araujo-Silva, G., de Rezende, A.A., Brandaoneto, J., Galvão Ururahy, M.A., Luchessi, A.D., López, J.A., Oliveira Rocha, H.A. & das Graças Almeida, M. 2021. Licania rigida Benth leaf extracts: Assessment of toxicity and potential anticoagulant effect. South African Journal of Botany, 139(6): 217-225. https://doi.org/10.1016/j.sajb.2021.02.016
34. Duarte da Luz, J.R., Silva do Nascimento, T.E., Fernandes de Morais, L.V., Menezes da Cruz, A.K., de Rezende, A.A., Neto, J.B., Galvão Ururahy, M.A., Luchessi, A.D., López, J.A., Oliveira Rocha, H.A. & das Graças Almeida, M. 2019. Thrombin inhibition: Preliminary assessment of the anticoagulant potential Turnera subulata (Passifloraceae). Journal of Medicinal Food, 22(4): 384-392. https://doi.org/10.1089/jmf.2018.0141
35. Dubey, R., Kumar, J., Agrawala, D., Char, T. & Pusp, P. 2011. Isolation, production, purification, assay and characterization of fibrinolytic enzymes (Nattokinase, Streptokinase and Urokinase) from bacterial sources. African Journal of Biotechnology, 10(8): 1408-1420. https://doi.org/10.5897/AJB10.1268
36. Duron, J.J. 2007. Postoperative intraperitoneal adhesion pathophysiology. Colorectal Disease, 9(2): 14-24. https://doi.org/10.1111/j.1463-1318.2007.01343.x
37. Edziri, H., Guerrab, M., Anthonissen, R., Mastouri, M. & Verschave, L. 2020. Phytochemical screening, antioxidant, anticoagulant and in vitro toxic and genotoxic properties of aerial parts extracts of Fumaria officinalis L. growing in Tunisia. South African Journal of Botany, 130: 268-273. https://doi.org/10.1016/j.sajb.2020.01.014
38. Eskeland, G. 1966. Regeneration of parietal peritoneum in rats. A light microscopical study. Acta Pathologica et Microbiologica Scandinavica, 68(3): 355-378. https://doi.org/10.1111/apm.1966.68.3.355
39. Fakruddin, Mannan, K.S.B., Mazumdar, R.M. & Afroz, H. 2012. Antibacterial, antifungal and antioxidant activities of the ethanol extract of the stem bark of Clausena heptaphylla. BMC Complementary and Alternative Medicine. 12: 232. https://doi.org/10.1186/1472-6882-12-232
40. Fatehi Hassanabad, A., Zarzycki, A.N., Jeon, K., Dundas, J.A., Vasanthan, V., Deniset, J.F. & Fedak, P.W.M. 2021. Prevention of post-operative adhesions: A comprehensive review of present and emerging strategies. Biomolecules, 11(7): 1027. https://doi.org/10.3390/biom11071027
41. Félix-Silva, J., Souza, T., Camara, R.B.G., Cabral, B., Silva-Júnior, A.A., Rebecchi, I.V.M., Zucolotto, S.M., Rocha, H.A.O. & Fernandes-Pedrosa, M.F. 2014. In vitro anticoagulant and antioxidant activities of Jatropha gossypiifolia L. (Euphorbiaceae) leaves aiming therapeutical applications. BMC Complementary and Alternative Medicine, 14(405): 2-13. https://doi.org/10.1186/1472-6882-14-405
42. Flutur, I.M., Păduraru, D.N., Bolocan, A., Palcău, A.C., Ion, D., Andronic, O. 2023. Postsurgical adhesions: Is there any prophylactic strategy really working? Journal of Clinical Medicine, 12: 3931. https://doi.org/10.3390/jcm12123931
43. Fometescu, S.G., Costache, M., Coveney, A., Oprescu, S.M., Serban, D. & Savlovschi, C. 2013. Peritoneal fibrinolytic activity and adhesiogenesis, Chirurgia, 108(3): 331-40.
44. Fukuda, K., Murata, K., Itoh, K., Taniguchi, M., Shibano, M., Baba, K., Shiratori, M., Tani, T. & Matsuda, H. 2009. Fibrinolytic activity of ligustilide and pharmaceutical comparison of Angelica acutiloba roots before and after processing in hot water. Journal of Traditional Medicines, 26: 210-218. https://doi.org/10.11339/jtm.26.210
45. Genevieve, M.B. & Weigel, R.J. 2006. Formation and prevention of postoperative abdominal adhesions. Journal of Surgical Research, 132(1): 3-12. https://doi.org/10.1016/j.jss.2005.12.002
46. Gul, H., Jamshed, A. & Jabeen, Q. 2022. Pharmacological investigation of Asphodelus tenuifolius Cav. for its potential against thrombosis in experimental models. Dose Response, 20(3): 155932582211275. https://doi.org/10.1177/15593258221127566
47. Guo, Q., Li, Q.F., Liu, H.J., Li, R., Wu, C.T., Wang, L.S. 2007. Sphingosine kinase 1 gene transfer reduces postoperative peritoneal adhesion in an experimental model. British Journal of Surgery, 95: 252-258. https://doi.org/10.1002/bjs.5890
48. Gürbüz, İ., Gençler-Özkan, A.M., Akaydın, G., Salihoğlu, E., Günbatan, T., Demirci, F. & Yeşilada, E. 2019. Folk medicine in Düzce province (Turkey). Turkish Journal of Botany, 43: 769-784. https://doi.org/10.3906/bot-1905-13
49. Harmening, D.M. 2002. Clinical hematology and fundamentalsof hemostasis, 4th Edition, Philadelphia: F. A. Davis.
50. Harris, E.S., Morgan, R.F. & Rodeheaver, G.T. 1995. Analysis of the kinetics of peritoneal adhesion formation in the rat and evaluation of potential antiadhesive agents. Surgery; 117(6): 663-669. https://doi.org/10.1016/s0039-6060(95)80010-7
51. Hau, T., Payne, W. & Simmons, R. 1979. Fibrinolytic activity of the peritoneum during experimental peritonitis. Surgery, Gynecology and Obstetrics, 148(3): 415-418.
52. Hellebrekers, B.W.J. & Kooistra, T. 2011. Pathogenesis of postoperative adhesion formation. British Journal of Surgery, 98(11): 1503-1516. https://doi.org/10.1002/bjs.7657
53. Hellebrekers, B.W.J., Trimbos-Kemper T.C.M., Trimbos J.B.M.Z., Emeis, J.J. & Kooistra T. 2000. Use of fibrinolytic agents in the prevention of postoperative adhesion formation. Fertility and Sterility, 74(2): 203-212. https://doi.org/10.1016/s0015-0282(00)00656-7
54. Hoffman, R., Benz, E.J., Shattil, S.J., Furie, B., Cohen, H.J., Silberstein, L.E. & McGlave, P. (2005). Hematology: Basic principles and practice, 4th Edition, Philadelphia: Elsevier, 2821 pp.
55. Holmdahl, L. & Ivarsson, M.L. 1999. The role of cytokines, coagulation, and fibrinolysis in peritoneal tissue repair. European Journal of Surgery, 165(11): 1012-1019. https://doi.org/10.1080/110241599750007810
56. Holmdahl, L., Eriksson, E., al-Jabreen, M. & Risberg, B. 1996. Fibrinolysis in human peritoneum during operation. Surgery. 119(6): 701-705. https://doi.org/10.1016/s0039-6060(96)80196-6
57. Holmdahl, L., Falkenberg, M., Ivarsson, M. & Risberg, B. 1997. Plasminogen activators and inhibitors in peritoneal tissue. Acta Pathologica, Microbiologica, Et İmmunologica Scandinavica. 105(1): 25-30. https://doi.org/10.1111/j.1699-0463.1997.tb00535.x
58. Hu, Q., Xia, X., Kang, X., Song, P., Liu, Z., Wang, M., Lu, X., Guan, W. & Liu, S. 2021. A review of physiological and cellular mechanisms underlying fibrotic postoperative adhesion. International Journal of Biological Sciences, 17(1): 298-306. https://doi.org/10.7150/ijbs.54403
59. Hussain, F., Islam, A., Bulbul, L., Moghal, M.R. & Hossain, M.S. 2014. In vitro thrombolytic potential of root extracts of four medicinal plants available in Bangladesh. Ancient Science of Life, 33(3): 162-164. https://doi.org/10.4103/0257-7941.144620
60. Ilich, A., Bokarev, I. & Key, N.S. 2017. Global assays of fibrinolysis. International Journal of Laboratory Hematology, 39(5): 441-447. https://doi.org/10.1111/ijlh.12688
61. Ivarsson, M.L., Holmdahl, L., Falk, P., Mölne, J. & Risberg, B. 1998. Characterisation and fibrinolytic properties of mesothelial cells isolated from peritoneal lavage. Scandinavian Journal of Clinical and Laboratory Investigation, 58(3): 195-203. https://doi.org/10.1080/00365519850186580
62. Jedinák, A., Maliar, T., Grancai, D., Nagy, M. 2006. Inhibition activities of natural products on serine proteases. Phytotherapy Research, 20(3): 214-217. https://doi.org/10.1002/ptr.1836
63. Jiang, M., Zhou, Y., Chen, J., Zhang, W., Sun, Z., Qin, M., Liu, Y. & Liu, G. 2021. Effects of Herba Erigerontis injection on pharmacodynamics and pharmacokinetics of warfarin in rats in vivo. Basic & Clinical Pharmacology & Toxicology, 128: 386-393. https://doi.org/10.1111/bcpt.13531
64. Jung, K.A., Song, T.C., Han, D., Kım, I.H., Kim, Y.E. & Lee, C.H. 2005. Cardiovascular protective properties of kiwifruit extracts in vitro. Biological and Pharmaceutical Bulletin, 28(9): 1782-1785. https://doi.org/10.1248/bpb.28.1782
65. Jung, Y.S., Kim, M.H., Lee, S.H., Baik, E.J., Park, S.W. & Moon, C.H. 2002. Antithrombotic effect of onion in streptozotocin-induced diabetic rat. Prostaglandins, Leukotrienes and Essential Fatty Acids, 66(4): 453-458. https://doi.org/10.1054/plef.2002.0373
66. Kamal, S., Bibi, I., Rehman, K., Zahoor, A.F., Kamal, A., Aslam, F., Alasmary, F.A., Almutairi, T.M., Alhajri, H.M., Alissa, S.A. & Iqbal, H.M.N. 2021. Biological activities of in-house developed Haloxylon griffithii plant extract formulations. Plants, 10(7): 1427. https://doi.org/10.3390/plants10071427
67. Kamruzzaman, S.M., Endale, M., Jun Oh, W., Park, S.C., Kim, K.S., Heon Hong, J., Kwak, Y.S., Yun, B.S., Rhee, M.H. 2010. Inhibitory effects of Bulnesia sarmienti aqueous extract on agonist-induced platelet activation and thrombus formation involves mitogen-activated protein kinases. Journal of Ethnopharmacology, 130(3): 614-620. https://doi.org/10.1016/j.jep.2010.05.049
68. Kement, M., Censur, Z., Oncel, M., Buyukkokuroglu, M.E. & Gezen, F.C. 2011. Heparin for adhesion prevention: Comparison of three different dosages with Seprafilm in a murine model. International Journal of Surgery, 9(3): 225-228. https://doi.org/10.1016/j.ijsu.2010.11.016
69. Khan, M.F., Kader, F.B., Arman, M., Ahmed, S., Lyzu, C., Sakib, A., Tanzil, M., Zim, I.U., Imran, A.S., Venneri, T., Romano, B., Haque, A. & Capasso, R. 2020. Pharmacological insights and prediction of lead bioactive isolates of Dita bark through experimental and computer-aided mechanism. Biomedicine & Pharmacotherapy, 131: 110774. https://doi.org/10.1016/j.biopha.2020.110774
70. Khouya, T., Ramchoun, M., Amrani, S., Harnafi, H., Rouis, M., Couchie, D., Simmet, T. & Alem, C. 2020. Anti-inflammatory and anticoagulant effects of polyphenol-rich extracts from Thymus atlanticus: An in vitro and in vivo study. Journal of Ethnopharmacology. 252: 112475. https://doi.org/10.1016/j.jep.2019.112475
71. Kiflemariam, F.K., Tewelde, A.G., Hamid, A.M., Beshir, B.M., Solomon, S.N., Eman, T.G., Abraha, D.M., Kahsu, R., Issac, J. & Kaushik, J.J. 2022. Meriandra dianthera aqueous extract and its fraction prevents blood coagulation by specifically inhibiting the intrinsic coagulation pathway: An in vitro study. Journal of Experimental Pharmacology, 14: 205-212. https://doi.org/10.2147/JEP.S362258
72. Kim, K.J., Kim, M.S., Seok, P.R., Shin, J.H. & Kim, J.Y. 2019. Antithrombotic effect of Artemisia princeps Pampanini extracts in vitro and in FeCl3-Induced thrombosis rats. Journal of Food Science. 84(10): 3037-3044. https://doi.org/10.1111/1750-3841.14786
73. Kolodziejczyk-Czepas, J., Sieradzka, M., Moniuszko-Szajwaj, B., Pecio, Ł., Ponczek, M.B., Nowak, P., Stochmal, A. 2017. Bufadienolides from Kalanchoe daigremontiana as thrombin inhibitors-In vitro and in silico study. Int. International Journal of Biological Macromolecules, 99: 141-150. https://doi.org/10.1016/j.ijbiomac.2017.02.051
74. Koninckx, P.R., Gomel, V., Ussia, A. & Adamyan, L. 2016. Role of the peritoneal cavity in the prevention of postoperative adhesions, pain, and fatigue. Fertility and Sterility, 106(5): 998-1010. https://doi.org/10.1016/j.fertnstert.2016.08.012
75. Kosaka, H., Yoshimoto, T., Yoshimoto, T., Fujimoto, J. & Nakanishi, K. 2008. Interferon-gamma is a therapeutic target molecule for prevention of postoperative adhesion formation. Nature Medicine, 14(4): 437-441. https://doi.org/10.1038/nm1733
76. Kotb, E. 2012. Fibrinolytic bacterial enzymes with thrombolytic activity, Springer Briefs in Microbiology, 2012th Edition, 1-74.
77. Kowarzyk, H. & Buluk, K. 1950. Progress of the studies on blood coagulation. Postepy Higieny i Medycyny Doswiadczalnej, 2(1): 76.
78. Lauder, C.I.W., Garcea, G., Strickland, A. & Maddern, G.J. 2010. Abdominal adhesion prevention: still a sticky subject?. Digestive Surgery, 27(5): 347-58. https://doi.org/10.1159/000314805
79. Le, H.L., Nguyen, T.M.H., Vu, T.T., Nguyen, T.T.O., Ly, H.D.T., Le, N.T., Nguyen, V.H. & Nguyen, T.V.A. 2022. Potent antiplatelet aggregation, anticoagulant and antioxidant activity of aerial Canna x generalis L.H Bailey & E.Z Bailey and its phytoconstituents. South African Journal of Botany, 147: 882-893. https://doi.org/10.1016/j.sajb.2022.03.035
80. Legrand, E.K., Rodgers, K.E., Girgis, W., Campeau, J.D. & Dizerega, G.S. 1995. Comparative efficacy of nonsteroidal anti-inflammatory drugs and anti-thromboxane agents in a rabbit adhesion-prevention model. Journal of Investigative Surgery, 8(3): 187-194. https://doi.org/10.3109/08941939509023141
81. Li, C., Tu, C., Che, Y., Zhang, M., Dong, B., Zhou, X., Shi, Y., Li, G. & Wang, J. 2019. Bioassay based screening for the antiplatelet aggregation quality markers of Polygonum multiflorum with UPLC and chemometrics. Journal of Pharmaceutical and Biomedical Analysis. 166: 264-272. https://doi.org/10.1016/j.jpba.2019.01.005
82. Liu, B., Zhang, T., Xie, Z., Hong, Z., Lu, Y., Long, Y., Ji, C., Liu, Y., Yang, Y. & Wu, Z. 2022. Effective components and mechanism analysis of anti-platelet aggregation effect of Justicia procumbens L. Journal of Ethnopharmacology, 294: 115392. https://doi.org/10.1016/j.jep.2022.115392
83. Liu, H.J., Wu, C.T., Duan, H.F., Wu, B., Lu, Z.Z. & Wang, L. 2006. Adenoviral-mediated gene expression of hepatocyte growth factor prevents postoperative peritoneal adhesion in a rat model. Surgery, 140(3): 441-447. https://doi.org/10.1016/j.surg.2005.12.014
84. Liu, J., Xu, D., Xia, N., Hou, K., Chen, S., Wang, Y. & Li, Y. 2018. Anticoagulant Activities of activities of indobufen, an antiplatelet drug. Molecules, 23(6): 1452. https://doi.org/10.3390/molecules23061452
85. Liu, X.I., Zheng, X.Q., Qian, P.Z., Kopparapu, N.K., Deng, Y.P., Nonaka, M. & Harada, N. 2014. Purification and Characterization of a Novel Fibrinolytic Enzyme from Culture Supernatant of Pleurotus ostreatus. Journal of Microbiology and Biotechnology, 24(2): 245-253. https://doi.org/10.4014/jmb.1307.07063
86. Luchtman-Jones, L. & Broze, G.J. 1995. The current status of coagulation. Annals of Medicine, 27(1): 47-52. https://doi.org/10.3109/07853899509031935
87. Matsuda, H., Samukawa, K., Fukuda, S., Shiomoto, H., Chun-ning, T. & Kubo, M. 1989. Studies of Panax japonicus Fibrinolysis. Planta Medica, 55(1): 18-21. https://doi.org/10.1055/s-2006-961767
88. Menzies, D. & Ellis, H. 1990. Intestinal obstruction from adhesions -how big is the problem?. Annals of The Royal College of Surgeons of England, 72(1): 60-63.
89. Miser-Salihoğlu, E., Akaydin, G., Caliskan-Can, E. & Yardim-Akaydin, S. 2013. Evalution of Antioxidant Activity of Various Herbal Folk Medicines. Journal of Nutrition & Food Sciences, 3: 5. https://doi.org/10.4172/2155-9600.1000222
90. Monroe, D.M., Hoffman, M. & Roberts, H.R. 2002. Platelets and thrombin generation. Arteriosclerosis Thrombosis and Vascular Biology, 22(9): 1381-1389. https://doi.org/10.1161/01.atv.0000031340.68494.34
91. Moris, D., Chakedis, J., Rahnemai-Azar, A.A., Wilson, A., Hennessy, M.M., Athanasiou, A., Beal, E.W., Argyrou, C., Felekouras, E. & Pawlik, T.M. 2017. Postoperative abdominal adhesions: Clinical significance and advances in prevention and management. Journal of Gastrointestinal Surgery, 21(10): 1713-1722. https://doi.org/10.1007/s11605-017-3488-9
92. Mozzicafreddo, M., Cuccioloni, M., Eleuteri, A.M., Fioretti, E., Angeletti, M. 2006. Flavonoids inhibit the amidolytic activity of human thrombin. Biochimie, 88(9): 1297-1306. https://doi.org/10.1016/j.biochi.2006.04.007
93. Mozzicafreddo, M., Cuccioloni, M., Bonfili, L., Eleuteri, A.M., Fioretti, E., Angeletti, M. 2008. Antiplasmin activity of natural occurring polyphenols. Biochimica et Biophysica Acta, 1784, 995-1001. https://doi.org/10.1016/j.bbapap.2008.03.016
94. Mukherjee, A.K., Rai, S.K., Thakur, R., Chattopadhyay, P. & Kar, S.K. 2012. Bafibrinase: A non-toxic, non-hemorrhagic, direct-acting fibrinolytic serine protease from Bacillus sp. strain AS-S20-I exhibits in vivo anticoagulant activity and thrombolytic potency. Biochimie, 94(6): 1300-1308. https://doi.org/10.1016/j.biochi.2012.02.027
95. Murata, K., Abe, Y., Futamura-Masuda, M., Uwaya, A., Isami, F., Deng, S. & Matsuda, H. 2014. Effect of Morinda citrifolia fruit extract and its iridoid glycosides on blood fluidity. Journal of Natural Medicines. 68(3): 498–504. https://doi.org/10.1007/s11418-014-0826-z
96. Nachman, R.L., Hajjar, K.A., Silverstein, R.L. & Dinarello, C.A. 1986. Interleukin 1 induces endothelial cell synthesis of plasminogen activator inhibitor. Journal of Experimental Medicine, 163(6): 1595-600. https://doi.org/10.1084/jem.163.6.1595
97. Naderi, G.A., Asgary, S., Jafarian, A., Askari, N., Behagh, A. & Aghdam, R.H. 2005. Fibrinolytic effects of Ginkgo biloba extract. Experimental and Clinical Cardiology. 10(2): 85-87.
98. Nair, S., Saed, G., Atta, H., Rajaratnam, V., Diamond, M., Curiel, D., Al-Hendy, A. 2013. Towards gene therapy of postoperative adhesions: Fiber and transcriptional modifications enhance adenovirus targeting towards human adhesion cells. Gynecologic and Obstetric Investigation, 76: 119-124. https://doi.org/10.1159/000353426
99. Nguyen, T.M.H., Le, H.L., Ha, T.T., Bui, B.H., Le, N.T., Nguyen, V.H. & Nguyen, T.V.A. 2020. Inhibitory effect on human platelet aggregation and coagulation and antioxidant activity of C. edulis Ker Gawl rhizome and its secondary metabolites. Journal of Ethnopharmacology, 263: 113136. https://doi.org/10.1016/j.jep.2020.113136
100. Nguyen, T.M.H., Nguyen, T.T.O., Le, N.T., Spyridovich, E.V., Nguyen, V.H. & Chau, V.M. 2021. Preliminary observation on the fibrinolytic activity of Dimocarpus longan seed. Chemistry of Natural Compounds, 57(5): 945-948. https://doi.org/10.1007/s10600-021-03519-3
101. Ohashi, K., Yoshimoto, T., Kosaka, H., Hirano, T., Iimuro, Y., Nakanishi, K. & Fujimoto, J. 2014. Interferon gamma and plasminogen activator inhibitor 1 regulate adhesion formation after partial hepatectomy. The British Journal Of Surgery, 101(4): 398-407. https://doi.org/10.1002/bjs.9405
102. Orkin, S., Nathan, D., Ginsburg, D., Look, T.A., Fisher, D. & Lux, S. 2014. Nathan and Oski’s hematology of infancy and childhood, 8th Edition, Philadelphia: Saunders.
103. Park, S.E., Li, M.H., Kim, J.S., Sapkota, K., Kim, J.E., Choi, B.S., Yoon, Y.H., Lee, J.C., Lee, H.H., Kim, C.S. & Kim, S.J. 2007. Purification and characterization of a fibrinolytic protease from a culture supernatant of Flammulina velutipes mycelia. Bioscience, Biotechnology, and Biochemistry, 71(9): 2214-2222. https://doi.org/10.1271/bbb.70193
104. Petraglia, T., Latronico, T., Liuzzi, G.M., Fanigliulo, A., Crescenzi, A. & Rossano, R. 2022. Edible mushrooms as source of fibrin(ogen)olytic enzymes: Comparison between four cultivated species. Molecules, 27(23): 8145. https://doi.org/10.3390/molecules27238145
105. Porter, J.M., McGregor, F.M., Mullen, D.C. & Silver, D. 1969. Fibrinolytic activity of the mesothelial surfaces. Surgical Forum, 20: 80-82.
106. Prasad, S., Kashyap, R.S., Deopujari, J.Y., Purohit, H.J., Taori, G.M. & Daginawala, H.F. 2006. Development of an in vitro model to study clot lysis activity of thrombolytic drugs. Thrombosis Journal, 4(14): 1-4. https://doi.org/10.1186/1477-9560-4-14
107. Qi, X., Mao, W., Gao, Y., Chen, Y., Chen, Y., Zhao, C., Li, N., Wang, C., Yan, M., Lin, C. & Shan, C. 2012. Chemical characteristic of an anticoagulant-active sulfated polysaccharide from Enteromorpha clathrata. Carbohydrate Polymers, 90(4): 1804-1810. https://doi.org/10.1016/j.carbpol.2012.07.077
108. Raftery, A.T. 1979. Regeneration of peritoneum: a fibrinolytic study. Journal of Anatomy, 129(3): 659-664.
109. Raftery, A.T. 1981. Method of measuring fibrinolytic activity in a single layer of cells. Journal of Clinical Pathology, 34(6): 625-629. https://doi.org/10.1136/jcp.34.6.625
110. Rajput, M.A., Khan, R.A., Zafar, S., Riaz, A. & Ikram, R. 2019. Assessment of anti-coagulant activity of Nelumbo nucifera fruit. Pakistan Journal of Pharmaceutical Sciences, 32(6): 2561-2564.
111. Rasche, H. 2001. Haemostasis and thrombosis: an overview. European Heart Journal Supplements, 3(Q): 3-72. https://doi.org/10.1016/S1520-765X(01)90034-3
112. Rehman, A.A., Riaz, A., Asghar, M.A., Raza, M.L., Ahmed, S. & Khan, K. 2019. In vivo assessment of anticoagulant and antiplatelet effects of Syzygium cumini leaves extract in rabbits. BMC Complementary and Alternative Medicine. 19(1): 236. https://doi.org/10.1186/s12906-019-2661-y
113. Rendu, F. & Brohard-Bohn, B. 2001. The platelet release reaction: grannules’ constituents, secretion and functions. Platelets, 12(5): 61-73. https://doi.org/10.1080/09537100120068170
114. Riddel, J.P., Aouizerat, B.E., Miaskowski, C. & Lilicrap, D.P. 2007. Theories of blood coagulation. Journal of Pediatric Oncology Nursing, 24(3): 123-131. https://doi.org/10.1177/1043454206298693
115. Ripa, F.A., Hossain, J., Nesa, L., Zahan, M.S., Mitra, S., Rashid, M.A., Roy, A., Alghamdi, S., Almehmadi, M. & Abdulaziz, O. 2022. Phytochemical and pharmacological profiling of Heritiera fomes Buch. Ham. deciphered thrombolytic, antiarthritic, anthelmintic, and insecticidal potentialities via in vitro approach. Evidence-based Complementary and Alternative Medicine, 2594127. https://doi.org/10.1155/2022/2594127
116. Sartor, L., Pezzato, E., Dell’Aica, I., Caniato, R., Biggin, S., Garbisa, S. 2002. Inhibition of matrix-proteases by polyphenols: Chemical insights for anti-inflammatory and anti-invasion drug design. Biochemical Pharmacology, 64(2): 229-237. https://doi.org/10.1016/s0006-2952(02)01069-9
117. Schnüriger, B., Barmparas, G., Branco, B.C., Lustenberger, T., Inaba, K. & Demetriades, D. 2011. Prevention of postoperative peritoneal adhesions: a review of the literature. The American Journal of Surgery, 201(1): 111-121. https://doi.org/10.1016/j.amjsurg.2010.02.008
118. Seo, E.J., Ngoc, T.M., Lee, S.M., Kim, Y.S. & Jung, Y.S. 2012. Chrysophanol-8-O-glucoside, an anthraquinone derivative in rhubarb, has antiplatelet and anticoagulant activities. Journal of Pharmacological Sciences, 118(2): 245-254. https://doi.org/10.1254/jphs.11123fp
119. Shanti, N., Arumugam, P., Murugan, M., Sudhakar, M.P. & Arunkumar, K. 2021. Extraction of of fucoidan from Turbinaria decurrens and the synthesis of fucoidan-coated AgNPs for anticoagulant application. ACS Omega, 6(46): 30998-31008. https://doi.org/10.1021/acsomega.1c03776
120. Sharifi, S., Derakhshanfar, A., Pourjafar, M., Mohamadnia, A. & Charlang, K. 2007. Effect of heparin in prevention of experimental abdominal adhesions in rat. Iranian Journal of Veterınary Surgery, 2(3): 24-31.
121. Sharmin, T., Rahman, S. & Mohammadi, H. 2018. Investigation of biological activities of the flowers of Lagerstroemia speciosa, the Jarul flower of Bangladesh. BMC Complementary and Alternative Medicine, 18: 231. https://doi.org/10.1186/s12906-018-2286-6
122. Silence, K., Collen, D. & Lijnen, H.R. 1993. Interaction between staphylokinase, plasmin(ogen), and alpha 2-antiplasmin. Recycling of staphylokinase after neutralization of the plasmin-staphylokinase complex by alpha 2-antiplasmin. The Journal of Biological Chemistry, 268(13): 9811-9816.
123. Sitter, T., Spannagl, M., Schiffl, H., Held, E., van Hinsbergh, V.W.M. & Kooistra, T. 1995. Imbalance between intraperitoneal coagulation and fibrinolysis during peritonitis of CAPD patients: the role of mesothelial cells. Nephrology Dialysis Transplantation, 10(5): 677-683. https://doi.org/10.1093/ndt/10.5.677
124. Suzuki, Y., Kondo, K., Ichise, H., Tsukamoto, Y., Urano, T. & Umemura, K. 2003. Dietary supplementation with fermented soybeans suppresses intimal thickening. Nutrition, 19(3): 261-264. https://doi.org/10.1016/s0899-9007(02)00853-5
125. Süntar, I., Demirel, M.A., Ceribasi, A.O., Ergin, I. & Gökbulut, A. 2021. Preventive effect of Rumex crispus L. on surgically induced intra-abdominal adhesion model in rats. DARU Journal of Pharmaceutical Sciences, 29(1): 101-115. https://doi.org/10.1007/s40199-021-00387-8
126. Süntar, İ. 2014. The medicinal value of Asteraceae family plants in terms of wound healing activity. FABAD Journal of Pharmaceutical Sciences, 39: 21-31.
127. Süntar, İ. 2020. Importance of ethnopharmacological studies in drug discovery: role of medicinal plants. Phytochemistry Reviews, 19: 1199-1209. https://doi.org/10.1007/s11101-019-09629-9
128. Süntar, İ. Çetinkaya, S., Panieri, E., Saha, S., Buttari, B., Profumo, E. & Saso, L. 2021. Regulatory role of Nrf2 signaling pathway in wound healing process. Molecules, 26(9): 2424. https://doi.org/10.3390/molecules26092424
129. Süntar, İ., Küpeli Akkol, E., Keles, H., Yesilada, E., Sarker, S. & Baykal, T. 2014. Daphne oleoides Schreber ssp. oleoides exhibits potent wound healing effect: Isolation of the active components and elucidation of the activity mechanism. ACG Publications, 8(2): 93-109.
130. Tang, J., Xiang, Z., Bernards, M.T. & Chen, S. 2020. Peritoneal adhesions: Occurrence, prevention and experimental models. Acta Biomaterialia, 116(3): 84-104. https://doi.org/10.1016/j.actbio.2020.08.036
131. Thompson, J.N., Paterson-Brown, S., Harbourne, T., Whawell, S.A., Kalodiki, E. & Dudley H.A. 1989. Reduced human peritoneal plasminogen activating activity: a possible mechanism of adhesion formation. British Journal of Surgery, 76(4): 382-384. https://doi.org/10.1002/bjs.1800760422
132. Uddin, M.M.N., Kabir, M.S.H., Hasan, M., Mahmud, Z.A., Bhuiya, N.M.M.A., Ahmed, F., Hasan, R., Hosenİ M.T. & Alam, M.S. 2018. Assessment of the antioxidant, thrombolytic, analgesic, anti-inflammatory, antidepressant and anxiolytic activities of leaf extracts and fractions of Tetracera sarmentosa (L.) Vahl. Journal of Basic and Clinical Physiology and Pharmacology, 29(1): 81-93. https://doi.org/10.1515/jbcpp-2016-0173
133. Urano, T., Sakakibara, K., Rydzewski, A., Urano, S., Takada, Y. & Takada, A. 1990. Relationships between euglobulin clot lysis time and the plasma levels of tissue plasminogen activator and plasminogen activator inhibitor 1. Thrombosis and Haemostasis, 63(1): 82-86. https://doi.org/10.1055/s-0038-1645691 135. Uyama, N., Tsutsui, H., Wu, S., Yasuda, K., Hatano, E., Qin, X.Y., Kojima, S. & Fujimoto, J. 2019. Anti-interleukin-6 receptor antibody treatment ameliorates postoperative adhesion formation. Scientific Reports, 9(1): 17558. https://doi.org/10.1038/s41598-019-54175-1
136. van Hinsbergh, V., Kooistra, T., Scheffer, M.A., van Bockel, J.H. & van Muijen, G.N.P. 1990. Characterisation and fibrinolytic properties of human omental tissue mesothelial cells. Comparison with endothelial cells. Blood, 75: 1490-1497. https://doi.org/10.1182/blood.V75.7.1490.1490
137. van Hinsbergh, V., Kooistra, T., van den Berg, E., Princen, H., Fiers, W. & Emeis, J. 1988. Tumor necrosis factor increases the production of plasminogen activator inhibitor in human endothelial cells in vitro and in rats in vivo. Blood, 72(5): 1467-1473. https://doi.org/10.1182/blood.V72.5.1467.1467
138. Vipond, M.N., Whawell, S.A., Thompson, J.N. & Dudley, H.A. 1990. Peritoneal fibrinolytic activity and intra-abdominal adhesions. Lancet, 335(8698): 1120-1122. https://doi.org/10.1016/0140-6736(90)91125-t
139. Vipond, M.N., Whawell, S.A., Thompson, J.N. & Dudley, H.A. 1994. Effect of experimental peritonitis and ischaemia on peritoneal fibrinolytic activity. European Journal of Surgery, 160(9): 471-477.
140. Viskupicova, J., Danihelova, M., Majekova, M., Liptaj, T., Sturdik, E. 2011. Polyphenol fatty acid esters as serine protease inhibitors: A quantum-chemical QSAR analysis. Journal of Enzyme Inhibition and Medicinal Chemistry, 27(6): 800-809. https://doi.org/10.3109/14756366.2010.616860
141. Vrijland, W.W., Jeekel, J., van Geldorp, H.J., Swank, D.J. & Bonjer, H.J. 2003. Abdominal adhesions: intestinal obstruction, pain, and infertility. Surgical Endoscopy, 17(7): 1017-1022. https://doi.org/10.1007/s00464-002-9208-9
142. Wang, G., Wu, K., Li, W., Zhao, E., Shi, L., Wang, J., Shuai, X., Cai, K., Lu, X., Tao, K. & Wang, G. 2014. Role of IL-17 and TGF-beta in peritoneal adhesion formation after surgical trauma. Wound Repair And Regeneration. 22(5): 631-639. https://doi.org/10.1111/wrr.12203
143. Whawell, S.A. & Thompson, J.N. 1995. Cytokine-induced release of plasminogen activator inhibitor-1 by human mesothelial cells. European Journal of Surgery, 161(5): 315-318.
144. Wu, F., Liu, W., Feng, H., Long, L., Hou, L. & Hou, C. 2020. Application of Traditional Chinese Medicines in postoperative abdominal adhesion. Evidence-based Complementary and Alternative Medicine, 8073467. https://doi.org/10.1155/2020/8073467
145. Yang, L., Xie, G.L., Ma, J.L., Huang, X.O., Gu, Y., Huang, L., Chen, H.Y. & Ouyang, X.L. 2022. Phytochemical constituents of Camellia osmantha fruit cores with antithrombotic activity. Food Science&Nutrition, 10(5): 1510-1519. https://doi.org/10.1002/fsn3.2769
146. Zhou, C., Jia, P., Jiang, Z., Chen, K., Wang, G., Wang, K., Wei, G. & Li, X. 2016. Preventive effects of the intestine function recovery decoction, a Traditional Chinese Medicine, on postoperative intra-abdominal adhesion formation in a rat model. Evidence-based Complementary and Alternative Medicine, 1621894. https://doi.org/10.1155/2016/1621894
147. Zhou, J., Zhai, J., Zheng, W., Han, N., Liu, Z., Lv, G. & Zheng, X. 2019. The antithrombotic activity of the active fractions from the fruits of Celastrus orbiculatus Thunb through the anti-coagulation, anti-platelet activation and anti-fibrinolysis pathways. Journal of Ethnopharmacology, 241: 111974. https://doi.org/10.1016/j.jep.2019.111974
148. Zhou, W., Abdurahman, A., Umar, A., Iskander, G., Abdusalam, E., Berké, B., Bégaud, B. & Moore, N. 2014. Effects of Cydonia oblonga Miller extracts on blood hemostasis, coagulation and fibrinolysis in mice, and experimental thrombosis in rats. Journal of Ethnopharmacology, 154(1): 163-169. https://doi.org/10.1016/j.jep.2014.03.056

Details

Primary Language

English

Subjects

Pharmacognosy

Journal Section

Review

Authors

Gizem Deynez
0000-0003-0324-0192
Türkiye

Ece Miser Salihoğlu
0000-0003-0681-3566
Türkiye

İpek Süntar ^*
0000-0003-4201-1325
Türkiye

Publication Date

October 15, 2023

Submission Date

June 2, 2023

Acceptance Date

September 25, 2023

Published in Issue

Year 2023 Volume: 24 Number: 2

DOI

https://doi.org/10.23902/trkjnat.1309119

IZ

https://izlik.org/JA23WF26KX

Cite

RIS / Bibtex

APA

Deynez, G., Miser Salihoğlu, E., & Süntar, İ. (2023). THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION. Trakya University Journal of Natural Sciences, 24(2), 101-116. https://doi.org/10.23902/trkjnat.1309119

AMA

1.Deynez G, Miser Salihoğlu E, Süntar İ. THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION. Trakya Univ J Nat Sci. 2023;24(2):101-116. doi:10.23902/trkjnat.1309119

Chicago

Deynez, Gizem, Ece Miser Salihoğlu, and İpek Süntar. 2023. “THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION”. Trakya University Journal of Natural Sciences 24 (2): 101-16. https://doi.org/10.23902/trkjnat.1309119.

EndNote

Deynez G, Miser Salihoğlu E, Süntar İ (October 1, 2023) THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION. Trakya University Journal of Natural Sciences 24 2 101–116.

IEEE

[1]G. Deynez, E. Miser Salihoğlu, and İ. Süntar, “THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION”, Trakya Univ J Nat Sci, vol. 24, no. 2, pp. 101–116, Oct. 2023, doi: 10.23902/trkjnat.1309119.

ISNAD

Deynez, Gizem - Miser Salihoğlu, Ece - Süntar, İpek. “THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION”. Trakya University Journal of Natural Sciences 24/2 (October 1, 2023): 101-116. https://doi.org/10.23902/trkjnat.1309119.

JAMA

1.Deynez G, Miser Salihoğlu E, Süntar İ. THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION. Trakya Univ J Nat Sci. 2023;24:101–116.

MLA

Deynez, Gizem, et al. “THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION”. Trakya University Journal of Natural Sciences, vol. 24, no. 2, Oct. 2023, pp. 101-16, doi:10.23902/trkjnat.1309119.

Vancouver

1.Gizem Deynez, Ece Miser Salihoğlu, İpek Süntar. THE ROLE OF ANTICOAGULANT, THROMBOLYTIC, AND FIBRINOLYTIC ACTIVITIES IN THE PREVENTION OF PERITONEAL ADHESION. Trakya Univ J Nat Sci. 2023 Oct. 1;24(2):101-16. doi:10.23902/trkjnat.1309119