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Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme

Year 2021, Volume: 16 Issue: 3, 320 - 329, 30.12.2021

Tuba Parlak Ak , Mine Yaman , Pınar Tatlı Seven , Burcu Gül Baykalır Seda İflazoğlu Mutlu , Aslıhan Sur Arslan , İsmail Seven

https://doi.org/10.17094/ataunivbd.985666
Cited By: 1

Abstract

Bu çalışmanın amacı, ratlarda karbon tetraklorür (CCl4) ile indüklenen testis hasarı üzerine krisinin etkisini değerlendirmektir. Yirmi dört adet erkek Spraque-Dawley rat; kontrol grubu, Krisin grubu, CCl4 grubu ve Krisin+CCl4 grubu olmak üzere dört gruba ayrıldı. Krisin (100 mg/kg/vücut ağırlığı/gün) ve CCl4 (mısır yağı (1:1) içerisinde 0.5 ml/kg/vücut ağırlığı/gün) gavaj yoluyla 14 gün boyunca uygulandı. Kontrol grubu ile karşılaştırıldığında, CCl4 grubunda; malondialdehit (MDA) düzeyinin arttığı, redükte glutatyon (GSH) düzeyi ile süperoksit dismutaz (SOD) ve katalaz (KAT) aktivitelerinin ise azaldığı belirlendi. Bu grupta ayrıca birçok testiküler lezyonun indüklendiği, Johnsen’s Ortalama Testiküler Biyopsi Skoru (JMTBS)’nun azaldığı, kaspaz-3 immünoreaktivitesinin ise arttığı belirlendi. CCl4 grubu ile karşılaştırıldığında, Krisin+CCl4 grubunda; GSH düzeyi ile SOD ve KAT aktivitelerinin arttığı, MDA düzeyinin ise azaldığı tespit edildi. Bu grupta ayrıca testiküler lezyonların hafiflediği, JMTBS’nun arttığı ve kaspaz-3 immünoreaktivitesinin ise azaldığı gözlendi. Sonuç olarak; krisinin sahip olduğu antioksidan ve anti-apoptotik özellikler neticesinde, CCl4 kaynaklı testis toksisitesinin tedavisinde faydalı etkiler gösterebileceği kanaatine varılmıştır.

Keywords

Apoptozis Karbon tetraklorür Krisin Oksidatif stres Testis

Supporting Institution

yok

References

  • 1. Rahmouni F., Daoud S., Rebai T., 2019. Teucrium polium attenuates carbon tetrachloride-induced toxicity in the male reproductive system of rats. Andrologia, 51, e13182.
  • 2. Yüce A., Türk G., Çeribaşı S., Güvenç M., Çiftçi M., Sönmez M., Özer Kaya Ş., Çay M., Aksakal M., 2013. Effectiveness of cinnamon (Cinnamomum zeylanicum) bark oil in the prevention of carbon tetrachloride-induced damages on male reproductive system. Andrologia, 46, 263-272.
  • 3. EPA, IRIS, 2010. Toxicological review of carbon tetrachloride (External Review Draft). U.S. Environmental Protection Agency, Washington, DC, EPA/635/R-08/005A.
  • 4. Elgawish RAR., Rahman HGA., Abdelrazek HMA., 2015. Green tea extract attenuates CCl4-induced hepatic injury in male hamsters via inhibition of lipid peroxidation and p53-mediated apoptosis. Toxicol Rep, 2, 1149-1156.
  • 5. Safhi MM., 2018. Nephroprotective effect of zingerone against CCl4-induced renal toxicity in Swiss albino mice: Molecular mechanism. Oxid Med Cell Longev, 2474831, 1-8.
  • 6. Abdel Moneim AE., 2016. Prevention of carbon tetrachloride (CCl4)-induced toxicity in testes of rats treated with Physalis peruviana L. fruit. Toxicol Ind Health, 32, 1064-1073.
  • 7. Ritesh KR., Suganya A., Dileepkumar HV., Rajashekar Y., Shivanandappa T., 2015. A single acute hepatotoxic dose of CCl4 causes oxidative stress in the rat brain. Toxicol Rep, 2, 891-895.
  • 8. Abdou HS., Salah SH., Hoda FB., 2012. Effect of pomegranate pretreatment on genotoxicity and hepatotoxicity induced by carbon tetrachloride (CCl4) in male rats. J Med Plant Res, 6, 3370-3380.
  • 9. Küçükler S., Benzer F., Yıldırım S., Gür C., Kandemir FM., Bengü AS., Ayna A., Çağlayan C., Dörtbudak MB., 2021. Protective effects of chrysin against oxidative stress and inflammation induced by lead acetate in rat kidneys: a biochemical and histopathological approach. Biol Trace Elem Res, 199, 1501-1514.
  • 10. Aksu EH., Kandemir FM., Küçükler S., Mahamadu A., 2018. Improvement in colistin-induced reproductive damage, apoptosis and autophagy in testes via reducing oxidative stress by chrysin. J Biochem Mol Toxicol, 32, 11, e22201.
  • 11. Eldutar E., Kandemir FM., Küçükler S., Çağlayan C., 2017. Restorative effects of chrysin pretreatment on oxidant-antioxidant status, inflammatory cytokine production, and apoptotic and autophagic markers in acute paracetamol-induced hepatotoxicity in rats: An experimental and biochemical study. J Biochem Mol Toxicol, 31, e21960.
  • 12. Del Fabbro L., Jesse CR., de Gomes MG., Borges Filho C., Donato F., Souza LC., Goes AR., Furian AF., Boeira SP., 2019. The flavonoid chrysin protects against zearalenone induced reproductive toxicity in male mice. Toxicon, 165, 13-21.
  • 13. Çiftçi O., Özdemir İ., Aydın M., Beytur A., 2012. Beneficial effects of chrysin on the reproductive system of adult male rats. Andrologia, 44, 181-186.
  • 14. Sönmez M., Türk G., Çeribaşı S., Çiftçi M., Yüce A., Güvenç M., Özer Kaya Ş., Çay M., Aksakal M., 2014. Quercetin attenuates carbon tetrachloride-induced testicular damage in rats. Andrologia, 46, 848-858.
  • 15. Ohkawa H., Ohishi N., Yagi K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 95, 351-358.
  • 16. Ellman GL., 1959. Tissue sulfhydryl groups. Arch Biochem Biophys, 82, 70-77.
  • 17. Lowry OH., Rosebrough NJ., Farr AL., Randall RJ., 1951. Protein measurement with the Folin phenol reagent. J Biol Chem, 193, 265-275.
  • 18. Sun Y., Oberley LW., Li Y., 1988. A simple method for clinical assay of superoxide dismutase. Clin Chem, 34, 497-500.
  • 19. Aebi H., 1984. Catalase in vitro methods in enzymology. In: Willam BJ, editor. Methods in Enzymology. New York, NY, USA: Academic Press, pp. 121-126.
  • 20. Johnsen SG., 1970. Testicular biopsy score count-a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones, 1, 2-25.
  • 21. Seven İ., Tatlı Seven P., Gül Baykalır B., Parlak Ak T., Özer Kaya Ş., Yaman M., 2020. Bee glue (propolis) improves reproductive organs, sperm quality and histological changes and antioxidant parameters of testis tissues in rats exposed to excess copper. Andrologia, 52, e13540.
  • 22. Ojo OA., Ojo AB., Ajiboye B., Fadaka A., Imiere OB., Adeyonu O., Olayid I., 2016. Protective influence of Ficus asperifolia Miq leaf extract on carbon tetrachloride (CCl4)-induced testicular toxicity in rats. J Appl Pharm Sci, 6, 6, 37-41.
  • 23. Sahreen S., Khan MR., Khan RA., 2013. Ameliorating effect of various fractions of Rumex hastatus roots against hepato- and testicular toxicity caused by CCl4. Oxid Med Cell Longev, 325406.
  • 24. Okolo KO., Orisakwe OE., Siminialay IM., 2017. Pleurotus tuber-regium mushrooms in the diet of rats ameliorates reproductive and testicular injury caused by carbon tetrachloride. Clin Phytoscience, 3, 14-24.
  • 25. Mazani M., Ojarudi M., Banaei S., Salimnejad R., LatifiM., Azizi H., Rezagholizadeh L., 2020. The protective effect of cinnamon and ginger hydro-alcoholic extract on carbon tetrachloride-induced testicular damage in rats. Andrologia, 52, e13651.
  • 26. Keshtmand Z., Akbaribazm M., Bagheri Y., Oliaei R., 2021. The ameliorative effects of Lactobacillus coagulans and Lactobacillus casei probiotics on CCl4-induced testicular toxicity based on biochemical, histological and molecular analyses in rat. Andrologia, 53, e13908.
  • 27. Joshi D., Mittal DK., Shukla S., Srivastav SK., Dixit VA., 2017. Curcuma longa Linn. extract and curcumin protect CYP 2E1 enzymatic activity against mercuric chloride-induced hepatotoxicity and oxidative stress: A protective approach. Exp Toxicol Pathol, 69, 6, 373-382.
  • 28. Mazani M., Banaei S., Rezagholizadeh L., 2020. Feverfew attenuates carbon tetrachloride-induced testicular damage in rats. J Herbmed Pharmacol, 9, 42-47.
  • 29. Belhan S., Özkaraca M., Özdek U., Kömüroğlu, AU., 2020. Protective role of chrysin on doxorubicin-induced oxidative stress and DNA damage in rat testes. Andrologia, 52, 9, e13747.
  • 30. Mladenovic JM., Paunovic MG., Matic MM., Knezevic VS., Ognjanovic BI., Stajn AS., Saicic ZS., 2014. Copper-induced changes of lipid peroxidation and hemato-biochemical parameters in rat blood: Protective role of flavonoids. Arch Biol Sci, 66, 1271-1279.
  • 31. Szymonik-Lesiuk S., Czechowska G., Stryjecka-Zimmer M., Slomka M., Madro A., Celinski K., Wielosz M., 2003. Catalase, superoxide dismutase, and glutathione peroxidase activities in various rat tissues after carbon tetrachloride intoxication. J Hepatobiliary Pancreat Surg, 10, 309-315.
  • 32. Emek H., Dönmez DB., Bayçu C., Musmul A., 2017. Erişkin erkek sıçanlarda karbon tetraklorür ile oluşturulan testis hasarı üzerine kuersetinin etkisi. Osmangazi Tıp Derg, 39, 65-73.
  • 33. Türk G., Çeribaşı S., Sönmez M., Çiftçi M., Yüce A., Güvenç M., Özer Kaya Ş., Çay M., Aksakal M., 2016. Ameliorating effect of pomegranate juice consumption on carbon tetrachloride-induced sperm damages, lipid peroxidation, and testicular apoptosis. Toxicol Ind Health, 32, 126-137.
  • 34. Hassan MH., Ghobara M., Abd-Allah GM., 2014. Modulator effects of meloxicam against doxorubicin-induced nephrotoxicity in mice. J Biochem Mol Toxicol, 28, 337-346. 35. Kumar S., Pandey AK., 2013. Chemistry and biological activities of flavonoids: An overview. Sci World J, 162750.
  • 36. Shah NA., Khan MR., 2017. Increase of glutathione, testosterone and antioxidant effects of Jurenia dolomiaea on CCl4 induced testicular toxicity in rat. BMC Complement Altern Med, 17, 206.
  • 37. El-Sisi AE., El-Sayad ME., Abdelsalam NM., 2017. Protective effects of mirtazapine and chrysin on experimentally induced testicular damage in rats. Biomed Pharmacother, 95, 1059-10

Effects of Chrysin on Carbon Tetrachloride-Induced Testicular Damage in Rats: Biochemical, Histopathological and Immunohistochemical Evaluation

Year 2021, Volume: 16 Issue: 3, 320 - 329, 30.12.2021

Tuba Parlak Ak , Mine Yaman , Pınar Tatlı Seven , Burcu Gül Baykalır Seda İflazoğlu Mutlu , Aslıhan Sur Arslan , İsmail Seven

https://doi.org/10.17094/ataunivbd.985666
Cited By: 1

Abstract

The aim of this study was to evaluate the effect of chrysin on testicular damage induced by carbon tetrachloride (CCl4) in rats. Twenty-four male Spraque-Dawley rats were divided into four groups as the control group, Chrysin group, CCl4 group, and Chrysin+CCl4 group. Chrysin (100 mg/kg/body weight/day) and CCl4 (0.5 ml/kg/body weight/day in corn oil (1:1)) were administered by gavage for 14 days. Compared to the control group, it was determined that malondialdehyde (MDA) level increased, reduced glutathione (GSH) level, and superoxide dismutase (SOD) and catalase (KAT) activities decreased in the CCl4 group. It was also determined that many testicular lesions were induced, Johnsen’s Mean Testicular Biopsy Score (JMTBS) decreased, and caspase-3 immunoreactivity increased in this group. Compared to the CCl4 group, it was determined that GSH level and SOD and CAT activities increased, MDA level decreased in the Chrysin+CCl4 group. It was also observed that testicular lesions were alleviated, JMTBS increased, and caspase-3 immunoreactivity was decreased in this group. As a result, it was concluded that chrysin might have beneficial effects in the treatment of CCl4-induced testicular toxicity as a result of its antioxidant and anti-apoptotic properties.

Keywords

Apoptosis Carbon tetrachloride Chrysin Oxidative stress Testis

References

  • 1. Rahmouni F., Daoud S., Rebai T., 2019. Teucrium polium attenuates carbon tetrachloride-induced toxicity in the male reproductive system of rats. Andrologia, 51, e13182.
  • 2. Yüce A., Türk G., Çeribaşı S., Güvenç M., Çiftçi M., Sönmez M., Özer Kaya Ş., Çay M., Aksakal M., 2013. Effectiveness of cinnamon (Cinnamomum zeylanicum) bark oil in the prevention of carbon tetrachloride-induced damages on male reproductive system. Andrologia, 46, 263-272.
  • 3. EPA, IRIS, 2010. Toxicological review of carbon tetrachloride (External Review Draft). U.S. Environmental Protection Agency, Washington, DC, EPA/635/R-08/005A.
  • 4. Elgawish RAR., Rahman HGA., Abdelrazek HMA., 2015. Green tea extract attenuates CCl4-induced hepatic injury in male hamsters via inhibition of lipid peroxidation and p53-mediated apoptosis. Toxicol Rep, 2, 1149-1156.
  • 5. Safhi MM., 2018. Nephroprotective effect of zingerone against CCl4-induced renal toxicity in Swiss albino mice: Molecular mechanism. Oxid Med Cell Longev, 2474831, 1-8.
  • 6. Abdel Moneim AE., 2016. Prevention of carbon tetrachloride (CCl4)-induced toxicity in testes of rats treated with Physalis peruviana L. fruit. Toxicol Ind Health, 32, 1064-1073.
  • 7. Ritesh KR., Suganya A., Dileepkumar HV., Rajashekar Y., Shivanandappa T., 2015. A single acute hepatotoxic dose of CCl4 causes oxidative stress in the rat brain. Toxicol Rep, 2, 891-895.
  • 8. Abdou HS., Salah SH., Hoda FB., 2012. Effect of pomegranate pretreatment on genotoxicity and hepatotoxicity induced by carbon tetrachloride (CCl4) in male rats. J Med Plant Res, 6, 3370-3380.
  • 9. Küçükler S., Benzer F., Yıldırım S., Gür C., Kandemir FM., Bengü AS., Ayna A., Çağlayan C., Dörtbudak MB., 2021. Protective effects of chrysin against oxidative stress and inflammation induced by lead acetate in rat kidneys: a biochemical and histopathological approach. Biol Trace Elem Res, 199, 1501-1514.
  • 10. Aksu EH., Kandemir FM., Küçükler S., Mahamadu A., 2018. Improvement in colistin-induced reproductive damage, apoptosis and autophagy in testes via reducing oxidative stress by chrysin. J Biochem Mol Toxicol, 32, 11, e22201.
  • 11. Eldutar E., Kandemir FM., Küçükler S., Çağlayan C., 2017. Restorative effects of chrysin pretreatment on oxidant-antioxidant status, inflammatory cytokine production, and apoptotic and autophagic markers in acute paracetamol-induced hepatotoxicity in rats: An experimental and biochemical study. J Biochem Mol Toxicol, 31, e21960.
  • 12. Del Fabbro L., Jesse CR., de Gomes MG., Borges Filho C., Donato F., Souza LC., Goes AR., Furian AF., Boeira SP., 2019. The flavonoid chrysin protects against zearalenone induced reproductive toxicity in male mice. Toxicon, 165, 13-21.
  • 13. Çiftçi O., Özdemir İ., Aydın M., Beytur A., 2012. Beneficial effects of chrysin on the reproductive system of adult male rats. Andrologia, 44, 181-186.
  • 14. Sönmez M., Türk G., Çeribaşı S., Çiftçi M., Yüce A., Güvenç M., Özer Kaya Ş., Çay M., Aksakal M., 2014. Quercetin attenuates carbon tetrachloride-induced testicular damage in rats. Andrologia, 46, 848-858.
  • 15. Ohkawa H., Ohishi N., Yagi K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 95, 351-358.
  • 16. Ellman GL., 1959. Tissue sulfhydryl groups. Arch Biochem Biophys, 82, 70-77.
  • 17. Lowry OH., Rosebrough NJ., Farr AL., Randall RJ., 1951. Protein measurement with the Folin phenol reagent. J Biol Chem, 193, 265-275.
  • 18. Sun Y., Oberley LW., Li Y., 1988. A simple method for clinical assay of superoxide dismutase. Clin Chem, 34, 497-500.
  • 19. Aebi H., 1984. Catalase in vitro methods in enzymology. In: Willam BJ, editor. Methods in Enzymology. New York, NY, USA: Academic Press, pp. 121-126.
  • 20. Johnsen SG., 1970. Testicular biopsy score count-a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones, 1, 2-25.
  • 21. Seven İ., Tatlı Seven P., Gül Baykalır B., Parlak Ak T., Özer Kaya Ş., Yaman M., 2020. Bee glue (propolis) improves reproductive organs, sperm quality and histological changes and antioxidant parameters of testis tissues in rats exposed to excess copper. Andrologia, 52, e13540.
  • 22. Ojo OA., Ojo AB., Ajiboye B., Fadaka A., Imiere OB., Adeyonu O., Olayid I., 2016. Protective influence of Ficus asperifolia Miq leaf extract on carbon tetrachloride (CCl4)-induced testicular toxicity in rats. J Appl Pharm Sci, 6, 6, 37-41.
  • 23. Sahreen S., Khan MR., Khan RA., 2013. Ameliorating effect of various fractions of Rumex hastatus roots against hepato- and testicular toxicity caused by CCl4. Oxid Med Cell Longev, 325406.
  • 24. Okolo KO., Orisakwe OE., Siminialay IM., 2017. Pleurotus tuber-regium mushrooms in the diet of rats ameliorates reproductive and testicular injury caused by carbon tetrachloride. Clin Phytoscience, 3, 14-24.
  • 25. Mazani M., Ojarudi M., Banaei S., Salimnejad R., LatifiM., Azizi H., Rezagholizadeh L., 2020. The protective effect of cinnamon and ginger hydro-alcoholic extract on carbon tetrachloride-induced testicular damage in rats. Andrologia, 52, e13651.
  • 26. Keshtmand Z., Akbaribazm M., Bagheri Y., Oliaei R., 2021. The ameliorative effects of Lactobacillus coagulans and Lactobacillus casei probiotics on CCl4-induced testicular toxicity based on biochemical, histological and molecular analyses in rat. Andrologia, 53, e13908.
  • 27. Joshi D., Mittal DK., Shukla S., Srivastav SK., Dixit VA., 2017. Curcuma longa Linn. extract and curcumin protect CYP 2E1 enzymatic activity against mercuric chloride-induced hepatotoxicity and oxidative stress: A protective approach. Exp Toxicol Pathol, 69, 6, 373-382.
  • 28. Mazani M., Banaei S., Rezagholizadeh L., 2020. Feverfew attenuates carbon tetrachloride-induced testicular damage in rats. J Herbmed Pharmacol, 9, 42-47.
  • 29. Belhan S., Özkaraca M., Özdek U., Kömüroğlu, AU., 2020. Protective role of chrysin on doxorubicin-induced oxidative stress and DNA damage in rat testes. Andrologia, 52, 9, e13747.
  • 30. Mladenovic JM., Paunovic MG., Matic MM., Knezevic VS., Ognjanovic BI., Stajn AS., Saicic ZS., 2014. Copper-induced changes of lipid peroxidation and hemato-biochemical parameters in rat blood: Protective role of flavonoids. Arch Biol Sci, 66, 1271-1279.
  • 31. Szymonik-Lesiuk S., Czechowska G., Stryjecka-Zimmer M., Slomka M., Madro A., Celinski K., Wielosz M., 2003. Catalase, superoxide dismutase, and glutathione peroxidase activities in various rat tissues after carbon tetrachloride intoxication. J Hepatobiliary Pancreat Surg, 10, 309-315.
  • 32. Emek H., Dönmez DB., Bayçu C., Musmul A., 2017. Erişkin erkek sıçanlarda karbon tetraklorür ile oluşturulan testis hasarı üzerine kuersetinin etkisi. Osmangazi Tıp Derg, 39, 65-73.
  • 33. Türk G., Çeribaşı S., Sönmez M., Çiftçi M., Yüce A., Güvenç M., Özer Kaya Ş., Çay M., Aksakal M., 2016. Ameliorating effect of pomegranate juice consumption on carbon tetrachloride-induced sperm damages, lipid peroxidation, and testicular apoptosis. Toxicol Ind Health, 32, 126-137.
  • 34. Hassan MH., Ghobara M., Abd-Allah GM., 2014. Modulator effects of meloxicam against doxorubicin-induced nephrotoxicity in mice. J Biochem Mol Toxicol, 28, 337-346. 35. Kumar S., Pandey AK., 2013. Chemistry and biological activities of flavonoids: An overview. Sci World J, 162750.
  • 36. Shah NA., Khan MR., 2017. Increase of glutathione, testosterone and antioxidant effects of Jurenia dolomiaea on CCl4 induced testicular toxicity in rat. BMC Complement Altern Med, 17, 206.
  • 37. El-Sisi AE., El-Sayad ME., Abdelsalam NM., 2017. Protective effects of mirtazapine and chrysin on experimentally induced testicular damage in rats. Biomed Pharmacother, 95, 1059-10
There are 36 citations in total.

Details

Primary Language Turkish
Subjects Health Care Administration
Journal Section Araştırma Makaleleri
Authors

Tuba Parlak Ak 0000-0002-8318-7995

Mine Yaman 0000-0001-9427-9150

Pınar Tatlı Seven 0000-0002-0067-4190

Burcu Gül Baykalır This is me 0000-0002-9122-8953

Seda İflazoğlu Mutlu 0000-0002-6835-2171

Aslıhan Sur Arslan 0000-0002-3692-5510

İsmail Seven 0000-0001-9489-8074

Publication Date December 30, 2021
Published in Issue Year 2021 Volume: 16 Issue: 3

Cite

APA Parlak Ak, T., Yaman, M., Tatlı Seven, P., Gül Baykalır, B., et al. (2021). Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 16(3), 320-329. https://doi.org/10.17094/ataunivbd.985666
AMA Parlak Ak T, Yaman M, Tatlı Seven P, Gül Baykalır B, İflazoğlu Mutlu S, Sur Arslan A, Seven İ. Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. December 2021;16(3):320-329. doi:10.17094/ataunivbd.985666
Chicago Parlak Ak, Tuba, Mine Yaman, Pınar Tatlı Seven, Burcu Gül Baykalır, Seda İflazoğlu Mutlu, Aslıhan Sur Arslan, and İsmail Seven. “Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik Ve İmmunohistokimyasal Değerlendirme”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16, no. 3 (December 2021): 320-29. https://doi.org/10.17094/ataunivbd.985666.
EndNote Parlak Ak T, Yaman M, Tatlı Seven P, Gül Baykalır B, İflazoğlu Mutlu S, Sur Arslan A, Seven İ (December 1, 2021) Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16 3 320–329.
IEEE T. Parlak Ak, M. Yaman, P. Tatlı Seven, B. Gül Baykalır, S. İflazoğlu Mutlu, A. Sur Arslan, and İ. Seven, “Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 16, no. 3, pp. 320–329, 2021, doi: 10.17094/ataunivbd.985666.
ISNAD Parlak Ak, Tuba et al. “Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik Ve İmmunohistokimyasal Değerlendirme”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16/3 (December 2021), 320-329. https://doi.org/10.17094/ataunivbd.985666.
JAMA Parlak Ak T, Yaman M, Tatlı Seven P, Gül Baykalır B, İflazoğlu Mutlu S, Sur Arslan A, Seven İ. Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021;16:320–329.
MLA Parlak Ak, Tuba et al. “Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik Ve İmmunohistokimyasal Değerlendirme”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 16, no. 3, 2021, pp. 320-9, doi:10.17094/ataunivbd.985666.
Vancouver Parlak Ak T, Yaman M, Tatlı Seven P, Gül Baykalır B, İflazoğlu Mutlu S, Sur Arslan A, Seven İ. Ratlarda Karbon Tetraklorür Kaynaklı Testis Hasarı Üzerine Krisinin Etkileri: Biyokimyasal, Histopatolojik ve İmmunohistokimyasal Değerlendirme. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021;16(3):320-9.

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