Bisphenol AF Caused Reproductive Toxicity in Rats and Cineole Co-Treatment Exhibited Protective Effect.

Endocrine disruptor Herbal medicine Infertility Natural antioxidant Oxidative stress

Journal

Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249

Informations de publication

Date de publication:
19 Aug 2024
Historique:
received: 15 05 2024
accepted: 08 08 2024
medline: 20 8 2024
pubmed: 20 8 2024
entrez: 19 8 2024
Statut: aheadofprint

Résumé

Bisphenol AF (BPAF) is increasingly used and now found in products intended for human consumption. The protective effect of 1,8-cineole (CIN) against BPAF-induced reproductive toxicity was investigated. Four groups were created, with each group consisting of eight rats: control, BPAF (200 mg/kg), CIN (200 mg/kg), and BPAF + CIN groups. The results demonstrated that the BPAF group exhibited a decline in testosterone levels and a decrease in sperm parameters compared with the control. Additionally, higher levels of MDA were observed, along with lower levels of GSH and GPx activity. CAT activity also decreased slightly. Tnf-α, Nf-κB levels were significantly higher, and caspase-3 expression was elevated, while PCNA expression decreased. BPAF significantly increased tissue degeneration compared with the control. However, the BPAF + CIN group showed statistically significant improvements in sperm parameters, except for concentration. They also exhibited an increase in testosterone levels and an improvement in MDA and GSH levels compared with the BPAF group. However, GPx activity partially enhanced. Tnf-α and Nf-κB levels were significantly reduced, and caspase-3 levels declined while PCNA and Bcl-2 levels increased. The Johnsen Testicular Biopsy score showed a substantial increase. Overall, these results suggest that CIN co-treatment in rats enhanced reproductive health and exhibited antioxidant, antiapoptotic, and anti-inflammatory properties against BPAF-induced testicular damage.

Identifiants

pubmed: 39160422
doi: 10.1007/s43032-024-01677-7
pii: 10.1007/s43032-024-01677-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Mustafa Kemal Üniversitesi
ID : 22.GAP.006

Informations de copyright

© 2024. The Author(s), under exclusive licence to Society for Reproductive Investigation.

Références

Madore MP, Sakaki JR, Chun OK. Protective effects of polyphenols against endocrine disrupting chemicals. Food Sci Biotechnol. 2022;31(8):905–34. https://doi.org/10.1007/s10068-022-01105-z .
doi: 10.1007/s10068-022-01105-z pubmed: 35873371 pmcid: 9300791
Tvrdý V, Dias P, Nejmanová I, Carazo A, Jirkovský E, Pourová J, Fadraersada J, Moravcová M, Peterlin Mašič L, Sollner Dolenc M, Mladěnka P. The effects of bisphenols on the cardiovascular system ex vivo and in vivo. Chemosphere. 2023;2023(313):137565. https://doi.org/10.1016/j.chemosphere.2022.137565 .
doi: 10.1016/j.chemosphere.2022.137565
Meng Z, Tian S, Yan J, Jia M, Yan S, Li R, Zhang R, Zhu W, Zhou Z. Effects of perinatal exposure to BPA, BPF and BPAF on liver function in male mouse offspring involving in oxidative damage and metabolic disorder. Environ Pollut. 2019;2019(247):935–43. https://doi.org/10.1016/j.envpol.2019.01.116 .
doi: 10.1016/j.envpol.2019.01.116
Lei B, Sun S, Xu J, Feng C, Yu Y, Xu G, Wu M, Peng W. Low-concentration BPAF- and BPF-induced cell biological effects are mediated by ROS in MCF-7 breast cancer cells. Environ Sci Pollut Res. 2018;25:3200–8. https://doi.org/10.1007/s11356-017-9709-7 .
doi: 10.1007/s11356-017-9709-7
Feng Y, Yin J, Jiao Z, Shi J, Li M, Shao B. Bisphenol AF may cause testosterone reduction by directly affecting testis function in adult male rats. Toxicol Lett. 2012;211(2):201–9. https://doi.org/10.1016/j.toxlet.2012.03.802 .
doi: 10.1016/j.toxlet.2012.03.802 pubmed: 22504055
Chen S, Li X, Li H, Yuan S, Li J, Liu C. Greater toxic potency of bisphenol AF than bisphenol A in growth, reproduction, and transcription of genes in Daphnia magna. Environ Sci Pollut Res. 2021;28:25218–27. https://doi.org/10.1007/s11356-020-12153-5 .
doi: 10.1007/s11356-020-12153-5
Shi J, Jiao Z, Zheng S, Li M, Zhang J, Feng Y, Yin J, Shao B. Long-term effects of Bisphenol AF (BPAF) on hormonal balance and genes of hypothalamus-pituitary-gonad axis and liver of zebrafish (Danio rerio), and the impact on offspring. Chemosphere. 2015;2015(128):252–7. https://doi.org/10.1016/j.chemosphere.2015.01.060 .
doi: 10.1016/j.chemosphere.2015.01.060
Song M, Liang D, Liang Y, Chen M, Wang F, Wang H, Jiang G. Assessing developmental toxicity and estrogenic activity of halogenated bisphenol a on zebrafish (Danio rerio). Chemosphere. 2014;2014(112):275–81. https://doi.org/10.1016/j.chemosphere.2014.04.084 .
doi: 10.1016/j.chemosphere.2014.04.084
Li Y, Burns KA, Arao Y, Luh CJ, Korach KS. Differential estrogenic actions of endocrine-disrupting chemicals bisphenol a, bisphenol af, and zearalenone through estrogen receptor α and β in vitro. Environ Health Perspect. 2012;120(7):1029–35. https://doi.org/10.1289/ehp.1104689 .
doi: 10.1289/ehp.1104689 pubmed: 22494775 pmcid: 3404668
Mentor A, Wann M, Brunström B, Jönsson M, Mattsson A. Bisphenol AF and bisphenol f induce similar feminizing effects in chicken embryo testis as bisphenol a. Toxicol Sci. 2020;178(2):239–50. https://doi.org/10.1093/toxsci/kfaa152 .
doi: 10.1093/toxsci/kfaa152 pubmed: 33010167 pmcid: 7706397
Skledar DG, Carino A, Trontelj J, Troberg J, Distrutti E, Marchianò S, Tomašič T, Zega A, Finel M, Fiorucci S, Mašič LP. Endocrine activities and adipogenic effects of bisphenol AF and its main metabolite. Chemosphere. 2019;2019(215):870–80. https://doi.org/10.1016/j.chemosphere.2018.10.129 .
doi: 10.1016/j.chemosphere.2018.10.129
Li Y, Xiong Y, Lv L, Li X, Qin Z. Effects of low-dose bisphenol AF on mammal testis development via complex mechanisms: alterations are detectable in both infancy and adulthood. Arch Toxicol. 2022;96:3373–83. https://doi.org/10.1007/s00204-022-03377-0 .
doi: 10.1007/s00204-022-03377-0 pubmed: 36098747
Barratt CLR, Björndahl L, De Jonge CJ, Lamb DJ, Martini FO, McLachlan R, Oates RD, van der Poel S, John BS, Sigman M, Sokol R, Tournaye H. The diagnosis of male infertility: an analysis of the evidence to support the development of global WHO guidance—challenges and future research opportunities. Hum Reprod Update. 2017;23(6):660–80. https://doi.org/10.1093/humupd/dmx021 .
doi: 10.1093/humupd/dmx021 pubmed: 28981651 pmcid: 5850791
Taskin T, Kahvecioglu D, Turkoglu A, Dogan A, Kuzu M, Turkoğlu A. In vitro biological activities of different extracts from alcea dissecta. Clin Exp Health Sci. 2022;12(1):53–60. https://doi.org/10.33808/clinexphealthsci.787845 .
doi: 10.33808/clinexphealthsci.787845
Dorostghoal M, Seyyednejad SM, Nejad MNT. Beneficial effects of Cichorium intybus L. extract on oxidative status and reproductive parameters in male Wistar rats: an experimental study. Int J Reprod Biomed. 2019;17(6):425–34. https://doi.org/10.18502/ijrm.v17i6.4814 .
doi: 10.18502/ijrm.v17i6.4814 pubmed: 31508567 pmcid: 6719518
Salehi B, Sharifi-Rad J, Quispe C, Llaique H, Villalobos M, Smeriglio A, Trombetta D, Ezzat SM, Salem MA, Zayed A, Salgado Castillo CM, Yazdi SE, Sen S, Acharya K, Sharopov F, Martins N. Insights into Eucalyptus genus chemical constituents, biological activities and health-promoting effects. Trends Food Sci Technol. 2019;2019(91):609–24. https://doi.org/10.1016/j.tifs.2019.08.003 .
doi: 10.1016/j.tifs.2019.08.003
Dey B, Mitra A. Chemo-profiling of eucalyptus and study of its hypoglycemic potential. World J Diabetes. 2013;4(5):170–6. https://doi.org/10.4239/wjd.v4.i5.170 .
doi: 10.4239/wjd.v4.i5.170 pubmed: 24147201 pmcid: 3797882
Silva SM, Abe SY, Murakami FS, Frensch G, Marques FA, Nakashima T. Essential oils from different plant parts of eucalyptus cinerea F. Muell. ex Benth. (Myrtaceae) as a source of 1,8-cineole and their bioactivities. Pharmaceuticals. 2011;4(12):1535–50.
doi: 10.3390/ph4121535 pubmed: 26791641 pmcid: 4060100
Bhowal M, Gopal M. Eucalyptol: Safety and pharmacological profile. J Pharm Sci. 2015;5(4):125–31. https://doi.org/10.5530/rjps.2015.4.2 .
doi: 10.5530/rjps.2015.4.2
Widjaja G, Ibrahim NJ, Hadi SJ, Cababat F, Jalil AT, Al-Charak AGH, Yasin G, Sultan MQ, Fakri Mustafa Y. The effect of eucalyptus globulus hydroalcoholic extract on LH, FSH and testosterone concentrations and sperm morphology. Arch Razi Inst. 2023;78(1):115–23. https://doi.org/10.22092/ARI.2022.359470.2426 .
doi: 10.22092/ARI.2022.359470.2426 pubmed: 37312694 pmcid: 10258301
Lima PR, De Melo TS, Carvalho KMMB, De Oliveira ÍB, Arruda BR, De Castro Brito GA, Rao VS, Santos FA. 1,8-cineole (eucalyptol) ameliorates cerulein-induced acute pancreatitis via modulation of cytokines, oxidative stress and NF-κB activity in mice. Life Sci. 2013;92(24–26):1195–201. https://doi.org/10.1016/j.lfs.2013.05.009 .
doi: 10.1016/j.lfs.2013.05.009 pubmed: 23702424
Karnam SS, Ghosh RC, Mondal S, Mondal M. Evaluation of subacute bisphenol – A toxicity on male reproductive system. Vet World. 2015;8(6):738–44.
doi: 10.14202/vetworld.2015.738-744 pubmed: 27065640 pmcid: 4825275
Türk G, Ateşşahin A, Sönmez M, Yüce A, Çeribaşi AO. Lycopene protects against cyclosporine a-induced testicular toxicity in rats. Theriogenology. 2007;67(4):778–85. https://doi.org/10.1016/j.theriogenology.2006.10.013 .
doi: 10.1016/j.theriogenology.2006.10.013 pubmed: 17123593
Cellat M, Kuzu M, İşler CT, Etyemez M, Dikmen N, Uyar A, Gökçek İ, Türk E, Güvenç M. Tyrosol improves ovalbumin (OVA)-induced asthma in rat model through prevention of airway inflammation. Naunyn Schmiedebergs Arch Pharmacol. 2021;394:2061–75. https://doi.org/10.1007/s00210-021-02117-y .
doi: 10.1007/s00210-021-02117-y pubmed: 34287677
Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–8. https://doi.org/10.1016/0003-2697(79)90738-3 .
doi: 10.1016/0003-2697(79)90738-3 pubmed: 36810
Beutler E, Dubon O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882–8.
pubmed: 13967893
Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–6. https://doi.org/10.1016/S0076-6879(84)05016-3 .
doi: 10.1016/S0076-6879(84)05016-3 pubmed: 6727660
Beutler E (1975) Red cell metabolism: a manual of biochemical methods. Newyork: Grune Strottan
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurument with the folin phenol geagent. J Biol Chem. 1951;193(1):265–75.
doi: 10.1016/S0021-9258(19)52451-6 pubmed: 14907713
Türk E, Tekeli IO, Özkan H, Uyar A, Cellat M, Kuzu M, Yavas I, Yegani AA, Yaman T, Güvenç M. The protective effect of esculetin against aluminium chloride-induced reproductive toxicity in rats. Andrologia. 2021;53:e13930. https://doi.org/10.1111/and.13930 .
doi: 10.1111/and.13930 pubmed: 33368464
Luna L. Manual of histologic staining methods of the Armed Forces Institute of Pathology. New York: McGraw-Hill Book Co.; 1968.
Johnsen SG. Testicular biopsy score count – a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Horm Res Paediatr. 1970;1(1):2–25. https://doi.org/10.1159/000178170 .
doi: 10.1159/000178170
Uyar A, Cellat M, Kanat Ö, Etyemez M, Kutlu T, Deveci MYZ, Yavaş İ, Kuzu M. Carvacrol showed a curative effect on reproductive toxicity caused by Bisphenol AF via antioxidant, anti-inflammatory and anti-apoptotic properties. Reprod Toxicol. 2023;121:108456. https://doi.org/10.1016/j.reprotox.2023.108456 .
doi: 10.1016/j.reprotox.2023.108456 pubmed: 37586593
Biggs SN, Kennedy J, Lewis SL, Hearps S, O’Bryan MK, McLachlan R, von Saldern S, Chambers G, Halliday J. Lifestyle and environmental risk factors for unexplained male infertility: study protocol for Australian Male Infertility Exposure (AMIE), a case-control study. Reprod Health. 2023;20(32):1–9. https://doi.org/10.1186/s12978-023-01578-z .
doi: 10.1186/s12978-023-01578-z
Mima M, Greenwald D, Ohlander S. Environmental toxins and male fertility. Curr Urol Rep. 2018;19(50):1–8. https://doi.org/10.1007/s11934-018-0804-1 .
doi: 10.1007/s11934-018-0804-1
Nallella KP, Sharma RK, Aziz N, Agarwal A. Significance of sperm characteristics in the evaluation of male infertility. Fertil Steril. 2006;85(3):629–34. https://doi.org/10.1016/j.fertnstert.2005.08.024 .
doi: 10.1016/j.fertnstert.2005.08.024 pubmed: 16500330
Li Y, Xiong Y, Lv L, Li X, Qin Z. Effects of low-dose bisphenol AF on mammal testis development via complex mechanisms: alterations are detectable in both infancy and adulthood. Arch Toxicol. 2022;96(12):3373–83. https://doi.org/10.1007/s00204-022-03377-0 .
doi: 10.1007/s00204-022-03377-0 pubmed: 36098747
Wu D, Huang CJ, Jiao XF, Ding ZM, Zhang SX, Miao YL, Huo LJ. Bisphenol AF compromises blood-testis barrier integrity and sperm quality in mice. Chemosphere. 2019;237:124410. https://doi.org/10.1016/j.chemosphere.2019.124410 .
doi: 10.1016/j.chemosphere.2019.124410 pubmed: 31362132
Čmiková N, Galovičová L, Schwarzová M, Vukic MD, Vukovic NL, Kowalczewski PŁ, Bakay L, Kluz MI, Puchalski C, Kačániová M. Chemical composition and biological activities of eucalyptus globulus essential oil. Plants. 2023;12(5):1–18. https://doi.org/10.3390/plants12051076 .
doi: 10.3390/plants12051076
Mousa AA, Elweza AE, Elbaz HT. Tahoun EAE aziz, Shoghy KM, Elsayed I, Hassan EB. Eucalyptus Globulus protects against diclofenac sodium induced hepatorenal and testicular toxicity in male rats. J Tradit Complement Med. 2020;10(6):521–8. https://doi.org/10.1016/j.jtcme.2019.11.002 .
doi: 10.1016/j.jtcme.2019.11.002 pubmed: 33134128
Cellat M, İşler CT, Uyar A, Kuzu M, Aydın T, Etyemez M, Türk E, Yavas I, Güvenç M. Protective effect of Smilax excelsa L pretreatment via antioxidant, anti-inflammatory effects, and activation of Nrf-2/HO-1 pathway in testicular torsion model. J Food Biochem. 2022;46:e14161. https://doi.org/10.1111/jfbc.14161 .
doi: 10.1111/jfbc.14161 pubmed: 35347733
Yan B, Lu G, Wang R, Kang S, Huang C, Wu H, Yong Q. Protective effects of lignin fractions obtained from grape seeds against bisphenol AF neurotoxicity via antioxidative effects mediated by the Nrf2 pathway. Front Chem Sci Eng. 2023;7(7):976–89. https://doi.org/10.1007/s11705-022-2237-0 .
doi: 10.1007/s11705-022-2237-0
Gao C, He H, Qiu W, Zheng Y, Chen Y, Hu S, Zhao X. Oxidative stress, endocrine disturbance, and immune interference in humans showed relationships to serum bisphenol concentrations in a dense industrial area. Environ Sci Technol. 2021;55(3):1953–63. https://doi.org/10.1021/acs.est.0c07587 .
doi: 10.1021/acs.est.0c07587 pubmed: 33496180
Taheri Mirghaed A, Hoseini SM, Ghelichpour M. Effects of dietary 1,8-cineole supplementation on physiological, immunological and antioxidant responses to crowding stress in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2018;81:182–8. https://doi.org/10.1016/j.fsi.2018.07.027 .
doi: 10.1016/j.fsi.2018.07.027 pubmed: 30010015
Ciftci O, Ozdemir I, Tanyildizi S, Yildiz S, Oguzturk H. Antioxidative effects of curcumin, β-myrcene and 1,8-cineole against 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced oxidative stress in rats liver. Toxicol Ind Health. 2011;27(5):447–53. https://doi.org/10.1177/0748233710388452 .
doi: 10.1177/0748233710388452 pubmed: 21245202
Taheri Mirghaed A, Fayaz S, Hoseini SM. Effects of dietary 1,8-cineole supplementation on serum stress and antioxidant markers of common carp (Cyprinus carpio) acutely exposed to ambient ammonia. Aquaculture. 2019;509:8–15. https://doi.org/10.1016/j.aquaculture.2019.04.071 .
doi: 10.1016/j.aquaculture.2019.04.071
Bhattacharya I, Sen Sharma S, Majumdar SS. Etiology of Male Infertility: an Update. Reprod Sci. 2024;31:942–65.
doi: 10.1007/s43032-023-01401-x pubmed: 38036863
Walke G, Gaurkar SS, Prasad R, Lohakare T, Wanjari M. The Impact of Oxidative Stress on Male Reproductive Function: Exploring the Role of Antioxidant Supplementation. Cureus. 2023;15(7):e42583. https://doi.org/10.7759/cureus.42583 .
doi: 10.7759/cureus.42583 pubmed: 37641770 pmcid: 10460465
Meli R, Monnolo A, Annunziata C, Pirozzi C, Ferrante MC. Oxidative Stress and BPA Toxicity: An Antioxidant Approach for Male and Female Reproductive Dysfunction. Antioxidants. 2020;9:405. https://doi.org/10.3390/antiox9050405 .
doi: 10.3390/antiox9050405 pubmed: 32397641 pmcid: 7278868
Kuzu M, Kandemir FM, Yıldırım S, Çağlayan C, Küçükler S. Attenuation of sodium arsenite-induced cardiotoxicity and neurotoxicity with the antioxidant, anti-inflammatory, and antiapoptotic effects of hesperidin. Environ Sci Pollut Res. 2020;28:10818–31. https://doi.org/10.1007/s11356-020-11327-5 .
doi: 10.1007/s11356-020-11327-5
Çibuk S, Yılmaz HC, Mert H, Mis L, Yörük M, Mert N. Effect of Bisphenol-A on Oxidative Status and Certain Inflammatory Markers in Rats: Experimental Study. Turkiye Klinikleri J Vet Sci. 2023;14(2):39–46. https://doi.org/10.5336/vetsci.2023-98134 .
doi: 10.5336/vetsci.2023-98134
Wang K, Huang D, Zhou P, Su X, Yang R, Shao C, Ma A, Wu J. Individual and Combined Effect of Bisphenol A and Bisphenol AF on Prostate Cell Proliferation through NF-κB Signaling Pathway. Int J Mol Sci. 2022;23(20):12283. https://doi.org/10.3390/ijms232012283 .
doi: 10.3390/ijms232012283 pubmed: 36293141 pmcid: 9602908
Asadi M, Rahmani M, Samadi A, Hesari AK. Protective Effect of Low-Volume High-Intensity Interval Training on Aspirin-Induced Reproductive Impairments in Adult Male Wistar Rats. Reprod Sci. 2024;31:393–403. https://doi.org/10.1007/s43032-023-01369-8 .
doi: 10.1007/s43032-023-01369-8 pubmed: 37794199
Liu XX, Wang ZX, Liu FJ. Chronic exposure of BPA impairs male germ cell proliferation and induces lower sperm quality in male mice. Chemosphere. 2021;262:127880. https://doi.org/10.1016/j.chemosphere.2020.127880 .
doi: 10.1016/j.chemosphere.2020.127880 pubmed: 32777607
Kuzu M, Kandemir FM, Yildirim S, Kucukler S, Caglayan C, Turk E. Morin attenuates doxorubicin-induced heart and brain damage by reducing oxidative stress, inflammation and apoptosis. Biomed Pharmacother. 2018;106:443–53. https://doi.org/10.1016/j.biopha.2018.06.161 .
doi: 10.1016/j.biopha.2018.06.161 pubmed: 29990832
Duan S, Jiang X, Li J, Fu M, Li Z, Cheng Y, Zhuang Y, Yang M, Xiao W, Ping H, Xie Y, Xie X, Zhang X. The RXFP2-PLC/PKC signaling pathway mediates INSL3-induced regulation of the proliferation, migration and apoptosis of mouse gubernacular cells. Cell Mol Biol Lett. 2023;28(16):1–14. https://doi.org/10.1186/s11658-023-00433-0 .
doi: 10.1186/s11658-023-00433-0
Gyimah E, Zhu X, Zhang Z, Guo M, Xu H, Mensah JK, Dong X, Zhang Z, Gyimah GNW. Oxidative Stress and Apoptosis in Bisphenol AF–Induced Neurotoxicity in Zebrafish Embryos. Environ Toxicol Chem. 2022;41(9):2273–84. https://doi.org/10.1002/etc.5412 .
doi: 10.1002/etc.5412 pubmed: 35723417
Chen L, Tao D, Yu F, Wang T, Qi M, Xu S. Cineole regulates Wnt/β-catenin pathway through Nrf2/keap1/ROS to inhibit bisphenol A-induced apoptosis, autophagy inhibition and immunosuppression of grass carp hepatocytes. Fish Shellfish Immunol. 2022;131:30–41. https://doi.org/10.1016/j.fsi.2022.09.067 .
doi: 10.1016/j.fsi.2022.09.067 pubmed: 36195267
Rocha Caldas GF, Oliveira ARDS, Araújo AV, Lafayette SSL, Albuquerque GS, Silva-Neto JDC, Costa-Silva JH, Ferreira F, Da Costa JGM, Wanderley AG. Gastroprotective Mechanisms of the Monoterpene 1,8-Cineole (Eucalyptol). PLoS ONE. 2015;10:e0134558. https://doi.org/10.1371/journal.pone.0134558 .
doi: 10.1371/journal.pone.0134558 pubmed: 26244547 pmcid: 4526535

Auteurs

Ahmet Uyar (A)

Department of Pathology, Faculty of Veterinary Medicine, Hatay Mustafa Kemal University, 31060, Hatay, Türkiye. ahmetuyar@mku.edu.tr.

Mustafa Cellat (M)

Department of Physiology, Hatay Mustafa Kemal University, Hatay, Türkiye.

Özgür Kanat (Ö)

Department of Pathology, Necmettin Erbakan University, Konya, Türkiye.

Muhammed Etyemez (M)

Department of Physiology, Hatay Mustafa Kemal University, Hatay, Türkiye.

Tuncer Kutlu (T)

Department of Pathology, Faculty of Veterinary Medicine, Hatay Mustafa Kemal University, 31060, Hatay, Türkiye.

Mehmet Zeki Yılmaz Deveci (MZY)

Department of Surgery, Hatay Mustafa Kemal University, Hatay, Türkiye.

İlker Yavaş (İ)

Department of Reproduction and Artificial Insemination, Mustafa Kemal University, Hatay, Türkiye.

Müslüm Kuzu (M)

Department of Nutrition and Dietetics, Karabuk University, Karabuk, Türkiye.

Classifications MeSH