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Farklı Stres Uygulamalarının Bazı Üreme Hormonları, Sperm Parametreleri, Lipid Profili, İmmünohistokimyasal ve İmmünofloresan Belirteçler Üzerine Etkileri

Year 2023, Volume: 34 Issue: 3, 263 - 270, 27.11.2023
https://doi.org/10.36483/vanvetj.1326578

Abstract

Mevcut çalışma, uygulanan 5 stres protokolünün sperm parametrelerini, lipid profilini ve bazı üreme hormonlarını nasıl etkilediğini değerlendirdi. Çalışmanın canlı materyalini 50 sıçan oluşturdu. Gruplardaki sıçan sayısı eşitti ve rastgele dağıtıldılar. Her grup 10 sıçandan oluşuyordu. Kontrol grubuna herhangi bir stres uygulaması yapılmadı. Psikolojik stres grubundaki sıçanlar günde 4 saat aydınlık, 20 saat karanlık döngüsüne tabi tutuldu. Fiziksel stres grubundaki sıçanlar günde 2 saat yem ve sudan mahrum bırakıldı. Psikolojik stres + fiziksel stres grubunda psikolojik ve fiziksel stres protokolü uygulandı. İlk 4 grupta tüm uygulamalar 14 gün süreyle yapılmıştır. Depresyon grubundaki sıçanlara her gün farklı bir stres uygulama uygulandı. Anormal sperm oranının stres ve depresyon gruplarında yüksek olduğu ancak en yüksek oranın depresyon grubunda olduğu belirlendi. Ayrıca sperm motilitesi ve yoğunluğu depresyon grubunda en düşüktü. Stres ve depresyon gruplarında serum trigliserit ve HDL düzeyleri ile LH ve FSH düzeyleri anlamlı olarak düşük bulunurken, kolesterol ve LDL değerleri anlamlı olarak yüksekti. Bax ekspresyonu ve 8 OHdG ekspresyonu psikolojik stress + fiziksel stres grubu ve depresyon grubunda şiddetli düzeydeydi. Bulgular toplu olarak değerlendirildiğinde; stresin sperm parametrelerini, lipid profilini, üreme hormonlarını, immünofloresan ve immünohistokimyasal parametreleri olumsuz etkilediği belirlendi.

References

  • Aksu EH, Akman O, Ozkaraca M, Omur AD, Ucar, O (2015). Effect of Maclura pomifera extract against cisplatin‐induced damage in reproductive system of male rats. Kafkas Univ Vet Fak Derg, 21 (3), 397-403.
  • Arun S, Burawat J, Sukhorum W et al. (2016). Chronic restraint stress induces sperm acrosome reaction and changes in testicular tyrosine phosphorylated proteins in rats. Int J Reprod Biomed, 14 (7), 443-452.
  • Awadalla NJ, El-Helaly M, Gouida M, Mandour R, Mansour M (2011). Sperm chromatin structure, semen quality and lead in blood and seminal fluid of infertile men. Int J Occup Environ Med, 2 (1), 27-36.
  • Bagheri Y, Fathi E, Maghoul A et al. (2021). Effects of Achillea tenuifolia Lam. hydro-alcoholic extract on anxiety-like behavior and reproductive parameters in rat model of chronic restraint stress. Hum Exp Toxicol, 40 (11), 1852-1866.
  • Baldwin DS (2001). Depression and sexual function. Br Med Bull, 57 (1), 81-99.
  • Basar K, Ertugrul A (2005). Depresyon Araştırmalarında kullanılan Hayvan Modelleri. Klinik Psikiyatri, 8 (3), 123-134.
  • Belhan S, Ozkaraca M, Kandemir FM et al. (2017). Effectiveness of hesperidin on methotrexate induced testicular toxicity in rats. Kafkas Univ Vet Fak Derg, 23 (5), 779-786.
  • Belhan S, Yildirim S, Huyut Z et al. (2020). Effects of curcumin on sperm quality, lipid profile, antioxidant activity and histopathological changes in streptozotocin-induced diabetes in rats. Andrologia, 52, e13584.
  • Bower JE, Sergerstrom SC (2001). Stress management; finding benefit and immune function: positive effects on physiology. J Psychosom Res, 56 (1), 9-11.
  • Bulmus O (2018). Stres ve egzersize bağlı olarak beyinde ve davranışlarda meydana gelen fizyopatolojik değişikliklerin araştırılması. Doktora tezi, Fırat Üniversitesi, Sağlık Bilimleri Enstitüsü, Elazığ, Türkiye.
  • Damber JE, Janson PO (1978). The influence of scrotal warming on testicular blood flow and endocrine function in the rat. Acta Physiol Scand, 104 (1), 61-67.
  • Devaki M, Nirupama R, Yajurvedi HN (2013). Chronic stress-induced oxidative damage and hyperlipidemia are accompanied by atherosclerotic development in rats. Stress, 16 (2), 233-243.
  • Fahim AT, Abd El-Fattah AA, Sadik NAH, Ali BM (2019). Resveratrol and Dimethyl Fumarate Ameliorate Testicular Dysfunction Caused by Chronic Unpredictable Mild Stress-Induced Depression in Rats. Arch Biochem Biophys, 665, 152-165.
  • García-Díaz EC, Gómez-Quiroz LE, Arenas-Ríos E et al. (2015). Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat. Syst Biol Reprod Med, 61 (3), 150-160.
  • Kennedy SH, Dickens SE, Eisfeld BS, Bagby RM (1999). Sexual dysfunction before antidepressant therapy in major depression. J Affect Disord, 56 (2-3), 201-208.
  • Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D (2009). Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci U S A, 106 (27), 11324-11329.
  • Koolhaas JM, Bartolomucci A, Buwalda B et al. (2011). Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev, 35 (5), 1291-1301.
  • Kopalli SR, Cha KM, Hwang SY, Jeong MS, Kim SK (2019). Korean Red Ginseng (Panax ginseng Meyer) with enriched Rg3 ameliorates chronic intermittent heat stresseinduced testicular damage in rats via multifunctional approach. J Ginseng Res, 2019 (43), 135-142.
  • Lee DY, Kim E, Choi MH (2015). Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Rep, 48 (4), 209-216.
  • Lee S-H, Choi K-H, Cha K-M et al. (2019). Protective effects of Korean Red Ginseng against sub-acute immobilization stress-induced testicular damage in experimental rats. J Ginseng Res, 43 (1), 125-134.
  • Liu B, Zhao L, Yue C, Qian M, Xie M (2019). Changes in gonadal function at different stages of chronic restraint stress-induced depression animals. Physiol Behav, 210, 112656.
  • Mehta K, Balaraman R, Amin AH, Bafna PA, Gulati OD (2003). Effect of fruits of Moringa oleifera on the lipid profile of normal and hypercholesterolaemic rabbits. J Ethnopharmacol, 86 (2-3), 191-195.
  • Mohamadpour M, Noorafshan A, Karbalay-Doust S, Talaei-Khozani T, Aliabadi E (2017). Protective effects of curcumin co-treatment in rats with establishing chronic variable stress on testis and reproductive hormones. Int J Reprod Biomed, 15 (7), 447-452.
  • Moustafa A (2021). Changes in nitric oxide, carbon monoxide, hydrogen sulfide and male reproductive hormones in response to chronic restraint stress in rats. Free Radic Biol Med, 162, 353-366.
  • Neves VJ, Moura MJ, Tamascia ML et al. (2009). Proatherosclerotic effects of chronic stress in male rats: altered phenylephrine sensitivity and nitric oxide synthase activity of arota and circulating lipids. Stress, 12 (4), 320-327.
  • Pan Q, Wu J, Liu Y, Li X, Chen J (2019). Involvement of Hepatic SHIP2 and PI3K/ Akt signalling in the regulation of plasma insulin by Xiaoyaosan in chronic immobilization-stressed rats. Molecules, 24 (3), 480.
  • Roboon J, Nudmamud-Thanoi S, Thanoi S (2016). Recovery effect of pre-germinated brown rice on the alteration of sperm quality, testicular structure and androgen receptor expression in rat model of depression. Andrologia, 49 (1), e12596.
  • Rosmond R, Bjorntorp P (2000). The hypothalamic‑pituitary‑adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. J Intern Med, 247 (2), 188-197.
  • Salami SA, Salahdeen HM, Moronkola OT, Murtala BA, Raji Y (2020). Vitamin C supplementation during chronic variable stress exposure modulates contractile functions of testicular artery and sperm parameters in male Wistar rats. Middle East Fertil Soc J, 25 (8), 1-10.
  • Shalet SM (2009). Normal testicular function and spermatogenesis. Pediatr Blood Cancer, 53 (2), 285-288.
  • Stepanichev M, Dygalo NN, Grigoryan G, Shishkina GT, Gulyaeva N (2014). Rodent models of depression: neurotrophic and neuroinflammatory biomarkers. Biomed Res Int, 2014, 932757.
  • Stephens MAC, Wand G (2012). Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res, 34 (4), 468-483.
  • Temel Y, Kucukler S, Yıldırım S, Caglayan C, Kandemir FM (2020). Protective effect of chrysin on cyclophosphamide induced hepatotoxicity and nephrotoxicity via the inhibition of oxidative stress, inflammation, and apoptosis. Naunyn Schmiedebergs Arch Pharmacol, 393 (3), 325-337.
  • Turk G, Atessahin A, Sonmez M, Ceribasi AO, Yuce A (2008). Improvement of cisplatin‐induced injuries to sperm quality, the oxidant–antioxidant system, and the histologic structure of the rat testis by ellagic acid. Fertil Steril, 89 (5 Suppl), 1474-1481.
  • Uchihara Y, Tanaka K, Asano T, Tamura F, Mizushima T (2016). Superoxide dismutase overexpression protects against glucocorticoid-induced depressive-like behavioral phenotypes in mice. Biochem Biophys Res Commun, 469 (4), 873-877.
  • Wang X, Xie Y, Zhang T et al. (2016). Resveratrol reverses chronic restraint stress-induced depressionlike behaviour: involvement of BDNF level, ERK phosphorylation and expression of Bcl-2 and Bax in rats. Brain Res Bull, 125, 134-143.
  • Whirledge S, Cidlowski JA (2010). Glucocorticoids, stress, and fertility. Minerva Endocrinol, 35 (2), 109-125. Yazawa H, Sasagawa I, Ishigooka M, Nakada T (1999). Effect of immobilization stress on testicular germ cell apoptosis in rats. Hum Reprod, 14 (7), 1806-1810.
  • Zeeni N, Daher C, Fromentin G et al. (2013). A cafeteria diet modifies the response to chronic variable stress in rats. Stress, 16 (2), 211-219.
  • Zou P, Wang X, Yang W et al. (2019). Mechanisms of Stress-Induced Spermatogenesis Impairment in Male Rats Following Unpredictable Chronic Mild Stress (uCMS). Int J Mol Sci, 20 (18), 4470.

Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers

Year 2023, Volume: 34 Issue: 3, 263 - 270, 27.11.2023
https://doi.org/10.36483/vanvetj.1326578

Abstract

The current study assessed how 5 stress protocols applied affected sperm parameters, lipid profile, and some reproductive hormones. Live materials of the study consisted of 50 rats. The number of rats in the groups was equal and they were randomly assigned. Each group consisted of 10 rats. No stress application was conducted in the control group. The rats in the psychological stress group were subjected to a cycle of 4-hour light and 20-hour dark per day. The rats in the physical stress group were deprived of feed and water for two hours per day. In the psychological stress + physical stress group, the psychological and physical stress protocol was conducted. In the first 4 groups, all the applications were conducted for 14 days. A different stress application was applied to the rats in the depression group every day. It was determined that the abnormal sperm rate was high in the stress and depression groups, but the highest rate was in the depression group. In addition, sperm motility and sperm concentration were the lowest in the depression group. While the stress and depression groups had significantly lower serum triglyceride and HDL levels and LH and FSH levels, cholesterol and LDL values were significantly higher. Bax expression and 8 OHdG expression were severe in psychological stress+physical stress group and depression group. When the findings are evaluated collectively; it was determined that stress negatively affected sperm parameters, lipid profile, reproductive hormones, immunofluorescence and immunohistochemical parameters.

References

  • Aksu EH, Akman O, Ozkaraca M, Omur AD, Ucar, O (2015). Effect of Maclura pomifera extract against cisplatin‐induced damage in reproductive system of male rats. Kafkas Univ Vet Fak Derg, 21 (3), 397-403.
  • Arun S, Burawat J, Sukhorum W et al. (2016). Chronic restraint stress induces sperm acrosome reaction and changes in testicular tyrosine phosphorylated proteins in rats. Int J Reprod Biomed, 14 (7), 443-452.
  • Awadalla NJ, El-Helaly M, Gouida M, Mandour R, Mansour M (2011). Sperm chromatin structure, semen quality and lead in blood and seminal fluid of infertile men. Int J Occup Environ Med, 2 (1), 27-36.
  • Bagheri Y, Fathi E, Maghoul A et al. (2021). Effects of Achillea tenuifolia Lam. hydro-alcoholic extract on anxiety-like behavior and reproductive parameters in rat model of chronic restraint stress. Hum Exp Toxicol, 40 (11), 1852-1866.
  • Baldwin DS (2001). Depression and sexual function. Br Med Bull, 57 (1), 81-99.
  • Basar K, Ertugrul A (2005). Depresyon Araştırmalarında kullanılan Hayvan Modelleri. Klinik Psikiyatri, 8 (3), 123-134.
  • Belhan S, Ozkaraca M, Kandemir FM et al. (2017). Effectiveness of hesperidin on methotrexate induced testicular toxicity in rats. Kafkas Univ Vet Fak Derg, 23 (5), 779-786.
  • Belhan S, Yildirim S, Huyut Z et al. (2020). Effects of curcumin on sperm quality, lipid profile, antioxidant activity and histopathological changes in streptozotocin-induced diabetes in rats. Andrologia, 52, e13584.
  • Bower JE, Sergerstrom SC (2001). Stress management; finding benefit and immune function: positive effects on physiology. J Psychosom Res, 56 (1), 9-11.
  • Bulmus O (2018). Stres ve egzersize bağlı olarak beyinde ve davranışlarda meydana gelen fizyopatolojik değişikliklerin araştırılması. Doktora tezi, Fırat Üniversitesi, Sağlık Bilimleri Enstitüsü, Elazığ, Türkiye.
  • Damber JE, Janson PO (1978). The influence of scrotal warming on testicular blood flow and endocrine function in the rat. Acta Physiol Scand, 104 (1), 61-67.
  • Devaki M, Nirupama R, Yajurvedi HN (2013). Chronic stress-induced oxidative damage and hyperlipidemia are accompanied by atherosclerotic development in rats. Stress, 16 (2), 233-243.
  • Fahim AT, Abd El-Fattah AA, Sadik NAH, Ali BM (2019). Resveratrol and Dimethyl Fumarate Ameliorate Testicular Dysfunction Caused by Chronic Unpredictable Mild Stress-Induced Depression in Rats. Arch Biochem Biophys, 665, 152-165.
  • García-Díaz EC, Gómez-Quiroz LE, Arenas-Ríos E et al. (2015). Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat. Syst Biol Reprod Med, 61 (3), 150-160.
  • Kennedy SH, Dickens SE, Eisfeld BS, Bagby RM (1999). Sexual dysfunction before antidepressant therapy in major depression. J Affect Disord, 56 (2-3), 201-208.
  • Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D (2009). Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci U S A, 106 (27), 11324-11329.
  • Koolhaas JM, Bartolomucci A, Buwalda B et al. (2011). Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev, 35 (5), 1291-1301.
  • Kopalli SR, Cha KM, Hwang SY, Jeong MS, Kim SK (2019). Korean Red Ginseng (Panax ginseng Meyer) with enriched Rg3 ameliorates chronic intermittent heat stresseinduced testicular damage in rats via multifunctional approach. J Ginseng Res, 2019 (43), 135-142.
  • Lee DY, Kim E, Choi MH (2015). Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Rep, 48 (4), 209-216.
  • Lee S-H, Choi K-H, Cha K-M et al. (2019). Protective effects of Korean Red Ginseng against sub-acute immobilization stress-induced testicular damage in experimental rats. J Ginseng Res, 43 (1), 125-134.
  • Liu B, Zhao L, Yue C, Qian M, Xie M (2019). Changes in gonadal function at different stages of chronic restraint stress-induced depression animals. Physiol Behav, 210, 112656.
  • Mehta K, Balaraman R, Amin AH, Bafna PA, Gulati OD (2003). Effect of fruits of Moringa oleifera on the lipid profile of normal and hypercholesterolaemic rabbits. J Ethnopharmacol, 86 (2-3), 191-195.
  • Mohamadpour M, Noorafshan A, Karbalay-Doust S, Talaei-Khozani T, Aliabadi E (2017). Protective effects of curcumin co-treatment in rats with establishing chronic variable stress on testis and reproductive hormones. Int J Reprod Biomed, 15 (7), 447-452.
  • Moustafa A (2021). Changes in nitric oxide, carbon monoxide, hydrogen sulfide and male reproductive hormones in response to chronic restraint stress in rats. Free Radic Biol Med, 162, 353-366.
  • Neves VJ, Moura MJ, Tamascia ML et al. (2009). Proatherosclerotic effects of chronic stress in male rats: altered phenylephrine sensitivity and nitric oxide synthase activity of arota and circulating lipids. Stress, 12 (4), 320-327.
  • Pan Q, Wu J, Liu Y, Li X, Chen J (2019). Involvement of Hepatic SHIP2 and PI3K/ Akt signalling in the regulation of plasma insulin by Xiaoyaosan in chronic immobilization-stressed rats. Molecules, 24 (3), 480.
  • Roboon J, Nudmamud-Thanoi S, Thanoi S (2016). Recovery effect of pre-germinated brown rice on the alteration of sperm quality, testicular structure and androgen receptor expression in rat model of depression. Andrologia, 49 (1), e12596.
  • Rosmond R, Bjorntorp P (2000). The hypothalamic‑pituitary‑adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. J Intern Med, 247 (2), 188-197.
  • Salami SA, Salahdeen HM, Moronkola OT, Murtala BA, Raji Y (2020). Vitamin C supplementation during chronic variable stress exposure modulates contractile functions of testicular artery and sperm parameters in male Wistar rats. Middle East Fertil Soc J, 25 (8), 1-10.
  • Shalet SM (2009). Normal testicular function and spermatogenesis. Pediatr Blood Cancer, 53 (2), 285-288.
  • Stepanichev M, Dygalo NN, Grigoryan G, Shishkina GT, Gulyaeva N (2014). Rodent models of depression: neurotrophic and neuroinflammatory biomarkers. Biomed Res Int, 2014, 932757.
  • Stephens MAC, Wand G (2012). Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res, 34 (4), 468-483.
  • Temel Y, Kucukler S, Yıldırım S, Caglayan C, Kandemir FM (2020). Protective effect of chrysin on cyclophosphamide induced hepatotoxicity and nephrotoxicity via the inhibition of oxidative stress, inflammation, and apoptosis. Naunyn Schmiedebergs Arch Pharmacol, 393 (3), 325-337.
  • Turk G, Atessahin A, Sonmez M, Ceribasi AO, Yuce A (2008). Improvement of cisplatin‐induced injuries to sperm quality, the oxidant–antioxidant system, and the histologic structure of the rat testis by ellagic acid. Fertil Steril, 89 (5 Suppl), 1474-1481.
  • Uchihara Y, Tanaka K, Asano T, Tamura F, Mizushima T (2016). Superoxide dismutase overexpression protects against glucocorticoid-induced depressive-like behavioral phenotypes in mice. Biochem Biophys Res Commun, 469 (4), 873-877.
  • Wang X, Xie Y, Zhang T et al. (2016). Resveratrol reverses chronic restraint stress-induced depressionlike behaviour: involvement of BDNF level, ERK phosphorylation and expression of Bcl-2 and Bax in rats. Brain Res Bull, 125, 134-143.
  • Whirledge S, Cidlowski JA (2010). Glucocorticoids, stress, and fertility. Minerva Endocrinol, 35 (2), 109-125. Yazawa H, Sasagawa I, Ishigooka M, Nakada T (1999). Effect of immobilization stress on testicular germ cell apoptosis in rats. Hum Reprod, 14 (7), 1806-1810.
  • Zeeni N, Daher C, Fromentin G et al. (2013). A cafeteria diet modifies the response to chronic variable stress in rats. Stress, 16 (2), 211-219.
  • Zou P, Wang X, Yang W et al. (2019). Mechanisms of Stress-Induced Spermatogenesis Impairment in Male Rats Following Unpredictable Chronic Mild Stress (uCMS). Int J Mol Sci, 20 (18), 4470.
There are 39 citations in total.

Details

Primary Language English
Subjects Reproduction and Artificial Insemination
Journal Section Araştırma Makaleleri
Authors

Saadet Belhan 0000-0002-8115-2051

Zübeyir Huyut 0000-0002-7623-1492

Serkan Yildirim 0000-0003-2457-3367

Sermin Algül 0000-0003-2489-3619

Early Pub Date November 27, 2023
Publication Date November 27, 2023
Submission Date July 12, 2023
Acceptance Date October 23, 2023
Published in Issue Year 2023 Volume: 34 Issue: 3

Cite

APA Belhan, S., Huyut, Z., Yildirim, S., Algül, S. (2023). Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers. Van Veterinary Journal, 34(3), 263-270. https://doi.org/10.36483/vanvetj.1326578
AMA Belhan S, Huyut Z, Yildirim S, Algül S. Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers. Van Vet J. November 2023;34(3):263-270. doi:10.36483/vanvetj.1326578
Chicago Belhan, Saadet, Zübeyir Huyut, Serkan Yildirim, and Sermin Algül. “Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers”. Van Veterinary Journal 34, no. 3 (November 2023): 263-70. https://doi.org/10.36483/vanvetj.1326578.
EndNote Belhan S, Huyut Z, Yildirim S, Algül S (November 1, 2023) Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers. Van Veterinary Journal 34 3 263–270.
IEEE S. Belhan, Z. Huyut, S. Yildirim, and S. Algül, “Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers”, Van Vet J, vol. 34, no. 3, pp. 263–270, 2023, doi: 10.36483/vanvetj.1326578.
ISNAD Belhan, Saadet et al. “Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers”. Van Veterinary Journal 34/3 (November 2023), 263-270. https://doi.org/10.36483/vanvetj.1326578.
JAMA Belhan S, Huyut Z, Yildirim S, Algül S. Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers. Van Vet J. 2023;34:263–270.
MLA Belhan, Saadet et al. “Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers”. Van Veterinary Journal, vol. 34, no. 3, 2023, pp. 263-70, doi:10.36483/vanvetj.1326578.
Vancouver Belhan S, Huyut Z, Yildirim S, Algül S. Effects of Different Stress Applications on Some Reproductive Hormones, Sperm Parameters, Lipid Profile, Immunohistochemical and Immunofluorescent Markers. Van Vet J. 2023;34(3):263-70.

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