Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism

Engin Kölükçü; Nihat Uluocak; Velid Unsal

doi:10.28982/josam.560609

Research Article

Kril yağının deneysel priapizm modelinde iskemik reperfüzyon hasarı üzerine koruyucu etkileri

Year 2019, Volume: 3 Issue: 5, 371 - 376, 28.05.2019

Engin Kölükçü , Nihat Uluocak , Velid Unsal

https://doi.org/10.28982/josam.560609

Abstract

Amaç: Mevcut çalışmanın amacı ratlara uyarlanmış priapizm modelinde krill yağının priapizm kaynaklı iskemi-reperfüzyon hasarı üzerindeki etkilerinin değerlendirilmesidir.

Yöntemler: Toplam 24 adet rat her bir grupta 8 rat bulunacak şekilde randomize edildi. Grup 1 kontrol grubu olarak belirlendi. Deneysel priapizm modeli Grup 2 ve 3'teki ratlara 1 saat süreyle uygulandı ve ardından iskemi-reperfüzyon hasarını değerlendirmek için priapizm 30 dakika süre ile sonlandırıldı. Grup 1 ve 2 deki ratlara standart yem ve musluk suyu verildi. Grup 3: Aynı beslenme prosedürü deney hayvanlarına uygulandı, ancak bir ay boyunca krill yağı ile takviye edildi. Deney sonunda süperoksit dismutaz (SOD), glutatyon peroksidaz (GSH-Px), malondialdehid (MDA), nitrik oksit (NO), protein karbonil (PC) düzeylerinin belirlenmesi amacı ile tüm ratlara penektomi uygulanarak vena kava inferiordan kan örneği alındı.

Bulgular: Penil dokuların biyokimyasal değerlendirmesinde Grup 3’teki MDA ve PC seviyeleri Grup 2’e göre anlamlı derecede düşük gözlemlenirken GSH-Px aktiviteleri anlamlı düzeyde yüksek olarak izlendi (sırasıyla P=0.001, P=0.005, P=0.003). Serum analiz sonuçları ise Grup 3’teki MDA ve NO seviyelerini Grup 2’e göre anlamlı derecede düşük olduğunu gösterirken SOD aktivitesini anlamlı düzeyde yüksek olduğunu ortaya koydu (sırasıyla P=0.011, P=0.001, P=0.009).

Sonuç: Bu çalışmada krill yağının; kavernosal dokuda gelişen priapizm ile indüklenen iskemi-reperfüzyon hasarına karşı koruyucu etkinliği biyokimyasal kanıtlara dayanılarak gözlenmiştir.

Keywords

Krill yağı, İskemi, Reperfüzyon, Priapizm

References

1. Broderick GA, Kadioglu A, Bivalacqua TJ, Ghanem H, Nehra A, Shamloul R. Priapism: pathogenesis, epidemiology, and management. J Sex Med. 2010;7:476-500.
2. Hodgson D. Of gods and leeches: treatment of priapism in the nineteenth century. J R Soc Med. 2003;96:562-5.
3. Callaway T. Unusual case of priapism. London Med Repository. 1824;1:286-7.
4. Tay YK, Spernat D, Rzetelski-West K, Appu S, Love C. Acute management of priapism in men. BJU Int. 2012;109:15-21.
5. Munnariz R, Park K, Huang YH, et al. Reperfusion of ischemic corporal tissue: physiologic and biochemical changes in an animal model of ischemic priapism. Urology. 2003;62:760-4.
6. Pryor J, Akkus E, Alter G, et al. Priapism. The Journal Of Sexual Medicine. 2004;1:116-20.
7. Ralph DJ, Garaffa G, Muneer A, et al. The immediate insertion of a penile prosthesis for acute ischaemic priapism. Eur Urol. 2009;56:1033-8.
8. Zimmerman BJ, Granger DN. Reperfusion injury. Surg Clin North Am. 1992;72:65-83.
9. Ozcan O, Erdal H, Yonden Z. Biochemical Aspect of Oxidative Stress Related to Ischemia-Reperfusion Damage. Mustafa Kemal Üniv Tıp Derg. 2015;6:27-33.
10. Burri L, Johnsen L. Krill Products: An Overview of Animal Studies. Nutrients. 2015;7:3300-21.
11. Kwantes JM, Grundmann O. A brief review of krill oil history, research, and the commercial market. Journal of dietary supplements. 2015;12:23-35.
12. Cicero AF, Collett A. Krill oil: evidence of a new source of polyunsaturated fatty acids with high bioavailability. Clin. Lipidol. 2015;10:1-4.
13. Sanli O, Armagan A, Kandirali E, et al. TGF-β 1 neutralizing antibodies decrease the fibrotic effects of ischemic priapism. Intertional Journal of Impotence Research. 2004;16:492-7.
14. Karaguzel E, Bayraktar C, Kutlu O, et al. The possible protective effects of dipyridamole on ischemic reperfusion injury of priapism. International Brazilian Journal Urology. 2016;42:146-53.
15. Zhu JJ, Shi JH, Qian WB, Cai ZZ, Li D. Effects of krill oil on serum lipids of hyperlipidemic rats and human SW480 cells. Lipids Health Dis. 2008;7:30.
16. Esterbauer H, Cheeseman KH. Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods in Enzymology. 1990;186:407-21.
17. Durak I, Canbolat O, Kavutçu M, et al. Activities of total, cytoplasmic, and mitochondrial superoxide dismutase enzymes in sera and pleural fluids from patients with lung cancer. Journal of clinical laboratory analysis. 1996;10:17-20.
18. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine. 1967;70:158-69.
19. Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-78.
20. Hassanipour M, Amini-Khoei H, Shafaroodi H, Shirzadiana A, Rahimi N, Imran-Khan M, et al. Atorvastatin attenuates the antinociceptive tolerance of morphine via nitric oxide dependent pathway in male mice. Brain Research Bulletin. 2016;125:173-80.
21. Mueller AR, Platz KP, Langrehr JM, et al. The effects of administration of nitric oxide inhibitors during small bowel preservation and reperfusion. Transplatation. 1994;58:1309-16.
22. Spycher MA, Hauri D. The ultrastructure of the erectile tissue in priapism. J Urol. 1986;135:142-7.
23. Vreugdenhil S, de Jong IJ, van Driel MF. [Priapism is an emergency]. Ned Tijdschr Geneeskd. 2018;162:2895.
24. Panwar VK, Mavuduru RS, Devana SK, Vaiphei K, Bora GS. Priapism with penile gangrene: An unusual presentation of multiple myeloma. Indian J Urol. 2017;33:251-2.
25. Michiels C.Physiological and pathological responses to hypoxia. Am J Pathol. 2004;164:1875-82.
26. Yılmaz Y, Taken K, Atar M, Ergün M, Söylemez H. Protective effect of curcumin on priapism and ischemia-reperfusion injury in rats. European Review for Medical and Pharmacological Sciences. 2015;19:4664-70.
27. Yapca OE, Borekci B, Suleyman H.Ischemia-Reperfusion Damage. Eurasian J Med. 2013;45:126-7.
28. Chatauret N, Badet L, Barrou B, Hauet T. Ischemia-reperfusion: From cell biology to acute kidney injury. Prog Urol. 2014;24:4-12.
29. Evliyaoglu Y, Kayrin L, Kaya B. Effect of allopurinol on lipid peroxidation induced in corporal tissue by veno-oclusive priapism in a rat model. British Journal of Urology. 1997;80:476-9.
30. Celik O, Turkoz Y, Hascalik S, et al. The protective effect of caffeic acid phenethyl ester on ischemia-reperfusion injury in rat ovary. Eur J Obstet Gynecol Reprod Biol. 2004;117:183-8.
31. Schanaider A, de Carvalho TP, de Oliveira Coelho S, et al. Ischemia-reperfusion rat model of acute pancreatitis: protein carbonyl as a putative early biomarker of pancreatic injury. Clin Exp Med. 2015;15:311-20.
32. Bauer V, Sotníková R. Nitric oxide-the endothelium-derived relaxing factor and its role in endothelial functions. Gen Physiol Biophys. 2010;29:319-40.
33. Ozkan OV, Yuzbasioglu MF, Ciralik H, et al. Resveratrol, a natural antioxidant, attenuates intestinal ischemia/reperfusion injury in rats. Tohoku J Exp Med. 2009;218:251-58.
34. Unsal V, Belge Kurutaş E. Experimental Hepatic Carcinogenesis: Oxidative Stress and Natural Antioxidants. Open Access Maced J Med Sci. 2017;12:5:686-91.
35. Savage GP, Foulds MJ. Chemical composition and nutritive value of antarctic krill (Euphausia superba) and southern blue whiting (Micromesistius austral is). New Zealand Journal of Marine and Freshwater Research. 1987;21:599-604.
36. Tou JC, Jaczynski J, Chen YC. Krill for human consumption: nutritional value and potential health benefits. Nutr Rev. 2007;65:63-77.
37. Schuchardt JP, Schneider I, Meyer H, Neubronner J, von Schacky C, Hahn A. Incorporation of EPA and DHA into plasma phospholipids in response to different omega-3 fatty acid formulations-a comparative bioavailability study of fish oil vs krill oil. Lipids Health Dis. 2011;10:145.
38. Winther B, Hoem N, Berge K, Reubsaet L. Elucidation of phosphatidylcholine composition in krill oil extracted from Euphausia superba. Lipids 2011;46:25-36.
39. Tanaka T, Morishita Y, Suzui M, Kojima T, Okumura A, Mori H.Chemoprevention of mouse urinary bladder carcinogenesis by the naturally occurring carotenoid astaxanthin. Carcinogenesis 1994;15:15-9.
40. Tanaka T, Kawamori T, Ohnishi M, et al. Suppression of azoxymethane-induced rat colon carcinogenesis by dietary administration of naturally occurring xanthophylls astaxanthin and canthaxanthin during the postinitiation phase. Carcinogenesis. 1995;16:2957-63.
41. Pashkow FJ, Watumull DG, Campbell CL. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol. 2008;22:101:58-68.
42. Tripathi DN, Jena GB. Astaxanthin intervention ameliorates cyclophosphamide-induced oxidative stress, DNA damage and early hepatocarcinogenesis in rat: role of Nrf2, p53, p38 and phase-II enzymes. Mutat Res. 2010;696:69-80.
43. Curek GD, Cort A, Yucel G, et al. Effect of astaxanthin on hepatocellular injury following ischemia/reperfusion. Toxicology. 2010:12;267:147-53.
44. Higuera-Ciapara I, Félix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr. 2006;46:185-96.
45. Bunea R, El Farrah K, Deutsch L. Evaluation of the effects of Neptune Krill Oil on the clinical course of hyperlipidemia. Altern Med Rev. 2004;9:420-8.
46. Ierna M, Kerr A, Scales H, Berge K, Griinari M. Supplementation of diet with krill oil protects against experimental rheumatoid arthritis. BMC Musculoskelet Disord. 2010;29:11:136.
47. Deutsch L. Evaluation of the effect of Neptune Krill Oil on chronic inflammation and arthritic symptoms. J Am Coll Nutr. 2007;26:39-48.
48. Çiftçi N, Gevrek F. Biochemical, Histopathological, Immunohistochemical Evaluation of Ischemic Preconditioning and Krill Oil Effects in Ischemia / Reperfusion Model. Fırat University Veterinary Journal of Health Sciences. 2017;31:159-67.
49. Gamoh S. Krill-derived phospholipids rich in n-3 fatty acid improve spatial memory in adult rats. Journal of Agricultural Science. 2011;3:3-12.
50. Mellouk Z, Agustina M, Ramirez M, Pena K, Arivalo J. [The therapeutic effects of dietary krill oil (Euphausia superba) supplementation on oxidative stress and DNA damages markers in cafeteria diet-overfed rats]. Ann Cardiol Angeiol (Paris). 2016;65:223-8.

Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism

Year 2019, Volume: 3 Issue: 5, 371 - 376, 28.05.2019

Engin Kölükçü , Nihat Uluocak , Velid Unsal

https://doi.org/10.28982/josam.560609

Abstract

Aim: The aim of the study is to evaluate the effects of krill oil on priapism induced ischemia-reperfusion injury in priapism rat model.

Methods: Total of 24 rats were randomly divided into three groups with eight rats in each group. Group 1 was determined as the control group. Experimental priapism model was constructed in rats in Groups 2 and 3 for 1 hour and then priapism was terminated for 30 minutes to evaluate ischemia-reperfusion injury. The rats in Groups 1 and 2 were given tap water and standard chow pellets. Group 3: The same feeding procedure was applied to the experimental animals but supplemented with krill oil for one month. At the end of the experiment penectomy were performed, and blood samples were withdrawn from inferior vena cava of the rats to determine the levels of protein carbonyl (PC), malondialdehyde (MDA), nitric oxide (NO), glutathione peroxidase (GSH-Px) and superoxide dismutase (SOD) in systemic circulation, and cavernosal tissues.

Results: Biochemical examination of penile tissues showed that MDA and PC levels in Group 3 were significantly lower than group 2, while GSH-Px activities were significantly increased (P=0.001, P=0.005, P=0.003 respectively). Serum analysis results showed that MDA and NO levels in Group 3 were significantly lower than Group 2 and SOD activities significantly increased (P=0.011, P=0.001, P=0.009, respectively).

Conclusion: In this study, protective effect of krill oil against priapism induced ischemia-reperfusion injury in cavernosal tissue was observed based on biochemical evidence.

Keywords

Krill oil, Ischemia, Reperfusion, Priapism

References

1. Broderick GA, Kadioglu A, Bivalacqua TJ, Ghanem H, Nehra A, Shamloul R. Priapism: pathogenesis, epidemiology, and management. J Sex Med. 2010;7:476-500.
2. Hodgson D. Of gods and leeches: treatment of priapism in the nineteenth century. J R Soc Med. 2003;96:562-5.
3. Callaway T. Unusual case of priapism. London Med Repository. 1824;1:286-7.
4. Tay YK, Spernat D, Rzetelski-West K, Appu S, Love C. Acute management of priapism in men. BJU Int. 2012;109:15-21.
5. Munnariz R, Park K, Huang YH, et al. Reperfusion of ischemic corporal tissue: physiologic and biochemical changes in an animal model of ischemic priapism. Urology. 2003;62:760-4.
6. Pryor J, Akkus E, Alter G, et al. Priapism. The Journal Of Sexual Medicine. 2004;1:116-20.
7. Ralph DJ, Garaffa G, Muneer A, et al. The immediate insertion of a penile prosthesis for acute ischaemic priapism. Eur Urol. 2009;56:1033-8.
8. Zimmerman BJ, Granger DN. Reperfusion injury. Surg Clin North Am. 1992;72:65-83.
9. Ozcan O, Erdal H, Yonden Z. Biochemical Aspect of Oxidative Stress Related to Ischemia-Reperfusion Damage. Mustafa Kemal Üniv Tıp Derg. 2015;6:27-33.
10. Burri L, Johnsen L. Krill Products: An Overview of Animal Studies. Nutrients. 2015;7:3300-21.
11. Kwantes JM, Grundmann O. A brief review of krill oil history, research, and the commercial market. Journal of dietary supplements. 2015;12:23-35.
12. Cicero AF, Collett A. Krill oil: evidence of a new source of polyunsaturated fatty acids with high bioavailability. Clin. Lipidol. 2015;10:1-4.
13. Sanli O, Armagan A, Kandirali E, et al. TGF-β 1 neutralizing antibodies decrease the fibrotic effects of ischemic priapism. Intertional Journal of Impotence Research. 2004;16:492-7.
14. Karaguzel E, Bayraktar C, Kutlu O, et al. The possible protective effects of dipyridamole on ischemic reperfusion injury of priapism. International Brazilian Journal Urology. 2016;42:146-53.
15. Zhu JJ, Shi JH, Qian WB, Cai ZZ, Li D. Effects of krill oil on serum lipids of hyperlipidemic rats and human SW480 cells. Lipids Health Dis. 2008;7:30.
16. Esterbauer H, Cheeseman KH. Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods in Enzymology. 1990;186:407-21.
17. Durak I, Canbolat O, Kavutçu M, et al. Activities of total, cytoplasmic, and mitochondrial superoxide dismutase enzymes in sera and pleural fluids from patients with lung cancer. Journal of clinical laboratory analysis. 1996;10:17-20.
18. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine. 1967;70:158-69.
19. Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-78.
20. Hassanipour M, Amini-Khoei H, Shafaroodi H, Shirzadiana A, Rahimi N, Imran-Khan M, et al. Atorvastatin attenuates the antinociceptive tolerance of morphine via nitric oxide dependent pathway in male mice. Brain Research Bulletin. 2016;125:173-80.
21. Mueller AR, Platz KP, Langrehr JM, et al. The effects of administration of nitric oxide inhibitors during small bowel preservation and reperfusion. Transplatation. 1994;58:1309-16.
22. Spycher MA, Hauri D. The ultrastructure of the erectile tissue in priapism. J Urol. 1986;135:142-7.
23. Vreugdenhil S, de Jong IJ, van Driel MF. [Priapism is an emergency]. Ned Tijdschr Geneeskd. 2018;162:2895.
24. Panwar VK, Mavuduru RS, Devana SK, Vaiphei K, Bora GS. Priapism with penile gangrene: An unusual presentation of multiple myeloma. Indian J Urol. 2017;33:251-2.
25. Michiels C.Physiological and pathological responses to hypoxia. Am J Pathol. 2004;164:1875-82.
26. Yılmaz Y, Taken K, Atar M, Ergün M, Söylemez H. Protective effect of curcumin on priapism and ischemia-reperfusion injury in rats. European Review for Medical and Pharmacological Sciences. 2015;19:4664-70.
27. Yapca OE, Borekci B, Suleyman H.Ischemia-Reperfusion Damage. Eurasian J Med. 2013;45:126-7.
28. Chatauret N, Badet L, Barrou B, Hauet T. Ischemia-reperfusion: From cell biology to acute kidney injury. Prog Urol. 2014;24:4-12.
29. Evliyaoglu Y, Kayrin L, Kaya B. Effect of allopurinol on lipid peroxidation induced in corporal tissue by veno-oclusive priapism in a rat model. British Journal of Urology. 1997;80:476-9.
30. Celik O, Turkoz Y, Hascalik S, et al. The protective effect of caffeic acid phenethyl ester on ischemia-reperfusion injury in rat ovary. Eur J Obstet Gynecol Reprod Biol. 2004;117:183-8.
31. Schanaider A, de Carvalho TP, de Oliveira Coelho S, et al. Ischemia-reperfusion rat model of acute pancreatitis: protein carbonyl as a putative early biomarker of pancreatic injury. Clin Exp Med. 2015;15:311-20.
32. Bauer V, Sotníková R. Nitric oxide-the endothelium-derived relaxing factor and its role in endothelial functions. Gen Physiol Biophys. 2010;29:319-40.
33. Ozkan OV, Yuzbasioglu MF, Ciralik H, et al. Resveratrol, a natural antioxidant, attenuates intestinal ischemia/reperfusion injury in rats. Tohoku J Exp Med. 2009;218:251-58.
34. Unsal V, Belge Kurutaş E. Experimental Hepatic Carcinogenesis: Oxidative Stress and Natural Antioxidants. Open Access Maced J Med Sci. 2017;12:5:686-91.
35. Savage GP, Foulds MJ. Chemical composition and nutritive value of antarctic krill (Euphausia superba) and southern blue whiting (Micromesistius austral is). New Zealand Journal of Marine and Freshwater Research. 1987;21:599-604.
36. Tou JC, Jaczynski J, Chen YC. Krill for human consumption: nutritional value and potential health benefits. Nutr Rev. 2007;65:63-77.
37. Schuchardt JP, Schneider I, Meyer H, Neubronner J, von Schacky C, Hahn A. Incorporation of EPA and DHA into plasma phospholipids in response to different omega-3 fatty acid formulations-a comparative bioavailability study of fish oil vs krill oil. Lipids Health Dis. 2011;10:145.
38. Winther B, Hoem N, Berge K, Reubsaet L. Elucidation of phosphatidylcholine composition in krill oil extracted from Euphausia superba. Lipids 2011;46:25-36.
39. Tanaka T, Morishita Y, Suzui M, Kojima T, Okumura A, Mori H.Chemoprevention of mouse urinary bladder carcinogenesis by the naturally occurring carotenoid astaxanthin. Carcinogenesis 1994;15:15-9.
40. Tanaka T, Kawamori T, Ohnishi M, et al. Suppression of azoxymethane-induced rat colon carcinogenesis by dietary administration of naturally occurring xanthophylls astaxanthin and canthaxanthin during the postinitiation phase. Carcinogenesis. 1995;16:2957-63.
41. Pashkow FJ, Watumull DG, Campbell CL. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol. 2008;22:101:58-68.
42. Tripathi DN, Jena GB. Astaxanthin intervention ameliorates cyclophosphamide-induced oxidative stress, DNA damage and early hepatocarcinogenesis in rat: role of Nrf2, p53, p38 and phase-II enzymes. Mutat Res. 2010;696:69-80.
43. Curek GD, Cort A, Yucel G, et al. Effect of astaxanthin on hepatocellular injury following ischemia/reperfusion. Toxicology. 2010:12;267:147-53.
44. Higuera-Ciapara I, Félix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr. 2006;46:185-96.
45. Bunea R, El Farrah K, Deutsch L. Evaluation of the effects of Neptune Krill Oil on the clinical course of hyperlipidemia. Altern Med Rev. 2004;9:420-8.
46. Ierna M, Kerr A, Scales H, Berge K, Griinari M. Supplementation of diet with krill oil protects against experimental rheumatoid arthritis. BMC Musculoskelet Disord. 2010;29:11:136.
47. Deutsch L. Evaluation of the effect of Neptune Krill Oil on chronic inflammation and arthritic symptoms. J Am Coll Nutr. 2007;26:39-48.
48. Çiftçi N, Gevrek F. Biochemical, Histopathological, Immunohistochemical Evaluation of Ischemic Preconditioning and Krill Oil Effects in Ischemia / Reperfusion Model. Fırat University Veterinary Journal of Health Sciences. 2017;31:159-67.
49. Gamoh S. Krill-derived phospholipids rich in n-3 fatty acid improve spatial memory in adult rats. Journal of Agricultural Science. 2011;3:3-12.
50. Mellouk Z, Agustina M, Ramirez M, Pena K, Arivalo J. [The therapeutic effects of dietary krill oil (Euphausia superba) supplementation on oxidative stress and DNA damages markers in cafeteria diet-overfed rats]. Ann Cardiol Angeiol (Paris). 2016;65:223-8.

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Details

Primary Language	English
Subjects	Health Care Administration
Journal Section	Research article
Authors	Engin Kölükçü 0000-0003-3387-4428 Nihat Uluocak 0000-0001-8315-466X Velid Unsal 0000-0003-1415-0563
Publication Date	May 28, 2019
Published in Issue	Year 2019 Volume: 3 Issue: 5

Cite

APA	Kölükçü, E., Uluocak, N., & Unsal, V. (2019). Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism. Journal of Surgery and Medicine, 3(5), 371-376. https://doi.org/10.28982/josam.560609
AMA	Kölükçü E, Uluocak N, Unsal V. Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism. J Surg Med. May 2019;3(5):371-376. doi:10.28982/josam.560609
Chicago	Kölükçü, Engin, Nihat Uluocak, and Velid Unsal. “Protective Effects of Krill Oil on Ischemic Reperfusion Injury in Experimental Model of Priapism”. Journal of Surgery and Medicine 3, no. 5 (May 2019): 371-76. https://doi.org/10.28982/josam.560609.
EndNote	Kölükçü E, Uluocak N, Unsal V (May 1, 2019) Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism. Journal of Surgery and Medicine 3 5 371–376.
IEEE	E. Kölükçü, N. Uluocak, and V. Unsal, “Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism”, J Surg Med, vol. 3, no. 5, pp. 371–376, 2019, doi: 10.28982/josam.560609.
ISNAD	Kölükçü, Engin et al. “Protective Effects of Krill Oil on Ischemic Reperfusion Injury in Experimental Model of Priapism”. Journal of Surgery and Medicine 3/5 (May 2019), 371-376. https://doi.org/10.28982/josam.560609.
JAMA	Kölükçü E, Uluocak N, Unsal V. Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism. J Surg Med. 2019;3:371–376.
MLA	Kölükçü, Engin et al. “Protective Effects of Krill Oil on Ischemic Reperfusion Injury in Experimental Model of Priapism”. Journal of Surgery and Medicine, vol. 3, no. 5, 2019, pp. 371-6, doi:10.28982/josam.560609.
Vancouver	Kölükçü E, Uluocak N, Unsal V. Protective effects of krill oil on ischemic reperfusion injury in experimental model of priapism. J Surg Med. 2019;3(5):371-6.

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