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The Effect of Melatonin Supplementation During In Vitro Maturation of Sheep Oocytes on Heat Stress and Embryo Development

Year 2025, Volume: 44 Issue: 1, 42 - 48, 29.07.2025

Ahmet Aktar , Selim Alçay

Abstract

The aim of this study was to investigate the effect of melatonin administration during in vitro oocyte maturation in sheep on heat stress, with a focus on its impact at the level of embryonic development.
One of the most critical stages in in vitro embryo (IVF) production is the oocyte maturation phase, during which the maturation rate of oocytes plays a key role. Stress factors encountered during this stage lead to an increase in reactive oxygen species, causing cellular damage. This study evaluated the embryonic development of sheep oocytes exposed to heat stress and treated with the hormone melatonin. A concentration of 10⁻⁷ M melatonin was added to the maturation medium under different temperature conditions. Oocytes were collected from the ovaries of sheep slaughtered at a local abattoir. Incubation procedures were carried out using specially prepared solutions under appropriate laboratory conditions. Embryonic development was assessed through cleavage, morula, and blastocyst stages. When cleavage rates were compared, the highest rate was observed in group G39M, and the lowest in group G41, with a statistically significant difference (P<0.05). Similarly, the highest morula rate was found in G39M, while the lowest was in G41 (P<0.05). The best blastocyst rates were also observed in G39M. Accordingly, melatonin showed a positive effect on cleavage and morula stages under heat stress; however, a significant reduction was observed at the blastocyst stage (P<0.05).

Keywords

IVF Melatonin Heat Stress Embryonic Development

Project Number

TAO-2022-670

References

  • Bergstein–Galan TG, Busato E, Abreu ACMR, Bertol MAF, Pereire JFS, Hartmann W, Bertol MAF. Reproduction Biotechnology in Farm Animals, (pp. 181-200). Avid Science, 2018.
  • Orland B. The invention of artificial fertilization in the eighteenth and nineteenth century. Hist Philos Life Sci, 39(2), 2017. https://doi.org/10.1007/s40656–017–0136–3
  • Betteridge KJ. A history of farm animal embryo transfer and some associated techniques. Anim Reprod Sci, 79(3–4), 203–244, 2003. https://doi.org/10.1016/s0378-4320(03)00166–0
  • Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. Effects of Controlled Heat Stress on Ovarian Function of Dairy Cattle. 1. Lactating Cows. J Dairy Sci, 81(8), 2124–2131, 1998. https://doi.org/10.3168/jds.s0022–0302(98)75788–1
  • Agarwal A, Gupta S, Sharma, R. Oxidative stress and its implications in female infertility – a clinican’s perspective. Reprod Biomed Online, 11(5), 641-650, 2005. https://doi.org/10.1016/s1472-6483(10)61174-1
  • Takahashi M. Heat stress on reproductive function and fertility in mammals. Reprod Med Biol, 11(1), 37–47, 2011. https://doi.org/10.1007/s12522–011–0105–6
  • Ozdaş OB, Baran A, TAŞ M, Cirit U, Demir K, Bacınoğlu S, Pabuccuoğlu S, Ak K. Effect of different transport temperatures on in vitro maturation of oocytes collected from frozen–thawed sheep ovaries. Turkish Journal of Veterinary and Animal Sciences, 37(1),15–19, 2013. https://doi.org/10.3906/vet-1104-24
  • Cipolla-Neto J. Do Amaral FG. Melatonin as a Hormone: New Physiological and Clinical Insights. Endocr Rev, 39, 990–1028, 2018. https://doi.org/ 10.1210/er.2018-00084
  • Hardeland R. Taxon- and Site-Specific Melatonin Catabolism. Molecules, 21-22(11), 2015, 2017. https://doi.org/10.3390/molecules22112015
  • Tamura H, Tanabe M, Jozaki M, Taketani T, Sugino N. Antioxidative Action of Melatonin and Reproduction. Glycative Stress Research, 6, 192–197. (2019). https://doi.org/10.24659/gsr.6.3_192
  • Lord T, Nixon B, Jones KT, Aitken RJ. Melatonin Prevents Postovulatory Oocyte Aging in the Mouse and Extends the Window for Optimal Fertilization in Vitro. Biol Reprod, 88, 1–9, 2013. https://doi.org/ 10.1095/biolreprod.112.106450
  • Lin T, Lee JE, Kang JW, Oqani RK, Cho ES, Kim SB, Il Jin D. Melatonin Supplementation during Prolonged in Vitro Maturation Improves the Quality and Development of Poor-Quality Porcine Oocytes via Anti-Oxidative and Anti-Apoptotic Effects. Mol Reprod Dev, 85, 665–68, 2018. https://doi.org/10.1002/mrd.23052
  • Marques TC, da Silva Santos EC, Diesel TO, Leme LO, Martins CF, Dode MAN, Alves, BG, Costa, F, de Oliveira, EB, Gambarini ML. Melatonin Reduces Apoptotic Cells, SOD2 and HSPB1 and Improves the in Vitro Production and Quality of Bovine Blastocysts. Reprod Domest Anim, 53, 226–236, 2018. https://doi.org/10.1111/rda.13097
  • Kaymakçı M. Sönmez R. Koyun yetiştiriciliği, Hasad Yayıncılık, İstanbul, 1992.
  • Stroud B. IETS 2011 Statistics and Data Retrieval Committee Report. The year 2010 worldwide statistics of embryo transfer in domestic farm animals. Embryo Transfer Newsletter, IETS Publications, 29, 14–23, 2011.
  • Agarwal A, Said TM, Bedaiwy, MA, Banerjee J, Alvarez JG. Oxidative stress in an assisted reproductive techniques setting. Fertil Steril, 86, 503–512, 2006. https://doi.org/10.1016/j.fertnstert.2006.02.088
  • Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Theriogenology, 30, 195–209, 1988. https://doi.org/10.1016/0093-691x(88)90169-0
  • Rodrigues-Cunha MC, Mesquita LG, Bressan F, Collado MD, Balieiro JC, Schwarz KR, de Castro F, Watanabe, OY, Watanabe YF, Coelho LA, Leal CL. Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology, 86, 1685-1694, 2016. https://doi.org/10.1016/j.theriogenology.2016.05.026
  • Payton RR, Rispol, LA, Nagle KA, Gondro C, Saxton AM, Voy BH, Edwards JL. Mitochondrial-related consequences of heat stress exposure during bovine oocyte maturation persist in early embryo development. J Reprod Dev, 64, 243–51, 2018. https://doi.org/10.1262/jrd.2017-160
  • de Castro e Paula LA, Hansen PJ. Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology, 68, 763–770, 2007. https://doi.org/10.1016/j.theriogenology.2007.06.005
  • Meiyu Q, Liu D, Roth Z. IGF-I slightly improves nuclear maturation and cleavage rate of bovine oocytes exposed to acute heat shock in vitro. Zygote, 23, 514–24, 2015. https://doi.org/10.1017/S096719941400015X
  • Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod, 71, 1898–906, 2004. https://doi.org/10.1095/biolreprod.104.031690
  • Roth Z, Hansen PJ. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reprod, 129, 235–44, 2005. https://doi.org/10.1530/rep.1.00394
  • Nabenishi H, Ohta H, Nishimoto T, Morita T, Ashizawa K, Tsuzuki Y. The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote, 20, 249–59, 2012. https://doi.org/10.1017/S0967199411000220
  • Li Y, Zhang Z, He C, Zhu K, Xu Z, Ma T, Tao J, Liu, G. Melatonin protects porcine oocyte in vitro maturation from heat stress. J Pineal Res, 59, 365-375, 2015. https://doi.org/10.1111/jpi.12268
  • 26Hansen PJ. Effects of heat stress on mammalian reproduction. Philos Trans R Soc B Biol Sci, 364, 3341–3350, 2009. https://doi.org/10.1098/rstb.2009.0131
  • He C, Wang J, Zhang Z, Yang M, Li Y, Tian X, Ma T, Tao J, Zhu K, Song Y, Ji P, Liu G. Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions. Int J Mol Sci, 17, 939, 2016. https://doi.org/10.3390/ijms17060939
  • Roth Z. Heat stress, the follicle, and its enclosed oocyte: mechanisms and potential strategies to improve fertility in dairy cows. Reprod Domest Anim, 43(2), 238–244, 2008. https://doi.org/10.1111/j.1439-0531.2008.01168.x
  • Perreault SD, Barbee RR, Slott VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol, 125(1), 181-186, 1988. https://doi.org/10.1016/0012-1606(88)90070-x
  • Yoshida M, Ishigaki K, Pursel VG. Effect of maturation media on male pronucleus formation in pig oocytes matured in-vitro. Mol Reprod Dev, 31, 68–71, 1992. https://doi.org/10.1002/mrd.1080310112
  • Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod, 49, 89–94, 1993. https://doi.org/10.1095/biolreprod49.1.89
  • Poleszczuk O, Papis kwenta-Muchalska E. An effect of melatonin on development of bovine embryos cultured in vitro under optimal or enhanced oxygen tensions. Reprod Fertil Dev, 17, 224, 2005.
  • Ishizuka B, Kuribayashi Y, Murai K, Amemiya A, Itoh MT. The effect of melatonin on in vitro fertilization and embryo development in mice. J Pineal Res, 28, 48–51, 2000. https://doi.org/ 10.1034/j.1600-079x.2000.280107.x
  • Iwata H, Ohota M, Hashimoto Snagai Y. Free oxygen radicals are generated at the time of aspiration of oocytes from ovaries that have been stored for a long time. Zygote, 11, 1–5, 2003. https://doi.org/10.1017/s0967199403001011
  • Rodriguez-Osorio N, Kim IJ, Wang H, Kaya A. Memili E. Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. Journal of Pineal Research, 43, 283-288, 2007. https://doi.org/10.1111/j.1600-079X.2007.00475.x

Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi

Year 2025, Volume: 44 Issue: 1, 42 - 48, 29.07.2025

Ahmet Aktar , Selim Alçay

Abstract

Çalışmada koyunlarda in vitro maturasyon sırasında uygulanan melatonin hormonunun sıcaklık stresi üzerine etkisinin embriyonik gelişim düzeyinde araştırılması amaçlanmıştır.
In vitro embriyo (IVF) üretim aşamlarından en kritik noktalardan birisi de in vitro maturasyon aşamasında oositlerin mature olma oranlarıdır. Bu aşamada meydana gelen streslere bağlı olarak reaktif oksijenlerin artması hücrelerde hasarlara sebep olmaktadır. Melatonin hormonunun sıcaklık stresine karşı koyun oositlerinde meydana gelen embriyonik gelişim değerlendirildi. Maturasyon medyumu içerisine farklı sıcaklıklarda 10-7 M melatonin hormunu ilave edildi. Mezbahada kesilen koyunların ovaryumlarından oositler elde edildi. Uygun şartlar altında laboratuvar ortamında hazırlanan solüsyonlar ile inkübasyon işlemleri gerçekleştirildi. Embriyonik gelişim aşamaları bölünme, marula, blastosit aşamaları olarak değerlendirildi. Bölünme oranları kıyaslandığında en yüksek oran G39M, en düşük değer G41 elde edildi ve istatiksel olarak anlamlı bir fark vardır (P<0,05). Morula oranlarında ise en yüksek değer G39M gözlenirken en düşük değer G41 elde edildi (P<0,05). Elde edilen blastosist oranları en iyi G39M de elde edildi. Buna göre melatonin sıcaklık stresinde bölünme ve marula aşamasında etki gösterirken blastosit aşamasında anlamlı ölçüde azalma oldu. (P<0,05)

Keywords

IVF Melatonin Sıcaklık Stresi Embriyonik Gelişim

Project Number

TAO-2022-670

Thanks

Bu makale Dr. Ahmet AKTAR’ın " Koyunlarda In Vitro Oosit Maturasyonu Sırasında Uygulanan Melatonin Hormonunun Sıcaklık Stresi Üzerine Etkisinin Tüm Genom Ekspresyonu Düzeyinde Araştırılması " başlıklı doktora tezinden türetilmiştir.

References

  • Bergstein–Galan TG, Busato E, Abreu ACMR, Bertol MAF, Pereire JFS, Hartmann W, Bertol MAF. Reproduction Biotechnology in Farm Animals, (pp. 181-200). Avid Science, 2018.
  • Orland B. The invention of artificial fertilization in the eighteenth and nineteenth century. Hist Philos Life Sci, 39(2), 2017. https://doi.org/10.1007/s40656–017–0136–3
  • Betteridge KJ. A history of farm animal embryo transfer and some associated techniques. Anim Reprod Sci, 79(3–4), 203–244, 2003. https://doi.org/10.1016/s0378-4320(03)00166–0
  • Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. Effects of Controlled Heat Stress on Ovarian Function of Dairy Cattle. 1. Lactating Cows. J Dairy Sci, 81(8), 2124–2131, 1998. https://doi.org/10.3168/jds.s0022–0302(98)75788–1
  • Agarwal A, Gupta S, Sharma, R. Oxidative stress and its implications in female infertility – a clinican’s perspective. Reprod Biomed Online, 11(5), 641-650, 2005. https://doi.org/10.1016/s1472-6483(10)61174-1
  • Takahashi M. Heat stress on reproductive function and fertility in mammals. Reprod Med Biol, 11(1), 37–47, 2011. https://doi.org/10.1007/s12522–011–0105–6
  • Ozdaş OB, Baran A, TAŞ M, Cirit U, Demir K, Bacınoğlu S, Pabuccuoğlu S, Ak K. Effect of different transport temperatures on in vitro maturation of oocytes collected from frozen–thawed sheep ovaries. Turkish Journal of Veterinary and Animal Sciences, 37(1),15–19, 2013. https://doi.org/10.3906/vet-1104-24
  • Cipolla-Neto J. Do Amaral FG. Melatonin as a Hormone: New Physiological and Clinical Insights. Endocr Rev, 39, 990–1028, 2018. https://doi.org/ 10.1210/er.2018-00084
  • Hardeland R. Taxon- and Site-Specific Melatonin Catabolism. Molecules, 21-22(11), 2015, 2017. https://doi.org/10.3390/molecules22112015
  • Tamura H, Tanabe M, Jozaki M, Taketani T, Sugino N. Antioxidative Action of Melatonin and Reproduction. Glycative Stress Research, 6, 192–197. (2019). https://doi.org/10.24659/gsr.6.3_192
  • Lord T, Nixon B, Jones KT, Aitken RJ. Melatonin Prevents Postovulatory Oocyte Aging in the Mouse and Extends the Window for Optimal Fertilization in Vitro. Biol Reprod, 88, 1–9, 2013. https://doi.org/ 10.1095/biolreprod.112.106450
  • Lin T, Lee JE, Kang JW, Oqani RK, Cho ES, Kim SB, Il Jin D. Melatonin Supplementation during Prolonged in Vitro Maturation Improves the Quality and Development of Poor-Quality Porcine Oocytes via Anti-Oxidative and Anti-Apoptotic Effects. Mol Reprod Dev, 85, 665–68, 2018. https://doi.org/10.1002/mrd.23052
  • Marques TC, da Silva Santos EC, Diesel TO, Leme LO, Martins CF, Dode MAN, Alves, BG, Costa, F, de Oliveira, EB, Gambarini ML. Melatonin Reduces Apoptotic Cells, SOD2 and HSPB1 and Improves the in Vitro Production and Quality of Bovine Blastocysts. Reprod Domest Anim, 53, 226–236, 2018. https://doi.org/10.1111/rda.13097
  • Kaymakçı M. Sönmez R. Koyun yetiştiriciliği, Hasad Yayıncılık, İstanbul, 1992.
  • Stroud B. IETS 2011 Statistics and Data Retrieval Committee Report. The year 2010 worldwide statistics of embryo transfer in domestic farm animals. Embryo Transfer Newsletter, IETS Publications, 29, 14–23, 2011.
  • Agarwal A, Said TM, Bedaiwy, MA, Banerjee J, Alvarez JG. Oxidative stress in an assisted reproductive techniques setting. Fertil Steril, 86, 503–512, 2006. https://doi.org/10.1016/j.fertnstert.2006.02.088
  • Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Theriogenology, 30, 195–209, 1988. https://doi.org/10.1016/0093-691x(88)90169-0
  • Rodrigues-Cunha MC, Mesquita LG, Bressan F, Collado MD, Balieiro JC, Schwarz KR, de Castro F, Watanabe, OY, Watanabe YF, Coelho LA, Leal CL. Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology, 86, 1685-1694, 2016. https://doi.org/10.1016/j.theriogenology.2016.05.026
  • Payton RR, Rispol, LA, Nagle KA, Gondro C, Saxton AM, Voy BH, Edwards JL. Mitochondrial-related consequences of heat stress exposure during bovine oocyte maturation persist in early embryo development. J Reprod Dev, 64, 243–51, 2018. https://doi.org/10.1262/jrd.2017-160
  • de Castro e Paula LA, Hansen PJ. Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology, 68, 763–770, 2007. https://doi.org/10.1016/j.theriogenology.2007.06.005
  • Meiyu Q, Liu D, Roth Z. IGF-I slightly improves nuclear maturation and cleavage rate of bovine oocytes exposed to acute heat shock in vitro. Zygote, 23, 514–24, 2015. https://doi.org/10.1017/S096719941400015X
  • Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod, 71, 1898–906, 2004. https://doi.org/10.1095/biolreprod.104.031690
  • Roth Z, Hansen PJ. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reprod, 129, 235–44, 2005. https://doi.org/10.1530/rep.1.00394
  • Nabenishi H, Ohta H, Nishimoto T, Morita T, Ashizawa K, Tsuzuki Y. The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote, 20, 249–59, 2012. https://doi.org/10.1017/S0967199411000220
  • Li Y, Zhang Z, He C, Zhu K, Xu Z, Ma T, Tao J, Liu, G. Melatonin protects porcine oocyte in vitro maturation from heat stress. J Pineal Res, 59, 365-375, 2015. https://doi.org/10.1111/jpi.12268
  • 26Hansen PJ. Effects of heat stress on mammalian reproduction. Philos Trans R Soc B Biol Sci, 364, 3341–3350, 2009. https://doi.org/10.1098/rstb.2009.0131
  • He C, Wang J, Zhang Z, Yang M, Li Y, Tian X, Ma T, Tao J, Zhu K, Song Y, Ji P, Liu G. Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions. Int J Mol Sci, 17, 939, 2016. https://doi.org/10.3390/ijms17060939
  • Roth Z. Heat stress, the follicle, and its enclosed oocyte: mechanisms and potential strategies to improve fertility in dairy cows. Reprod Domest Anim, 43(2), 238–244, 2008. https://doi.org/10.1111/j.1439-0531.2008.01168.x
  • Perreault SD, Barbee RR, Slott VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol, 125(1), 181-186, 1988. https://doi.org/10.1016/0012-1606(88)90070-x
  • Yoshida M, Ishigaki K, Pursel VG. Effect of maturation media on male pronucleus formation in pig oocytes matured in-vitro. Mol Reprod Dev, 31, 68–71, 1992. https://doi.org/10.1002/mrd.1080310112
  • Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod, 49, 89–94, 1993. https://doi.org/10.1095/biolreprod49.1.89
  • Poleszczuk O, Papis kwenta-Muchalska E. An effect of melatonin on development of bovine embryos cultured in vitro under optimal or enhanced oxygen tensions. Reprod Fertil Dev, 17, 224, 2005.
  • Ishizuka B, Kuribayashi Y, Murai K, Amemiya A, Itoh MT. The effect of melatonin on in vitro fertilization and embryo development in mice. J Pineal Res, 28, 48–51, 2000. https://doi.org/ 10.1034/j.1600-079x.2000.280107.x
  • Iwata H, Ohota M, Hashimoto Snagai Y. Free oxygen radicals are generated at the time of aspiration of oocytes from ovaries that have been stored for a long time. Zygote, 11, 1–5, 2003. https://doi.org/10.1017/s0967199403001011
  • Rodriguez-Osorio N, Kim IJ, Wang H, Kaya A. Memili E. Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. Journal of Pineal Research, 43, 283-288, 2007. https://doi.org/10.1111/j.1600-079X.2007.00475.x
There are 35 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Sciences (Other)
Journal Section Research Articles
Authors

Ahmet Aktar 0000-0002-2975-2594

Selim Alçay 0000-0002-2472-8157

Project Number TAO-2022-670
Publication Date July 29, 2025
Submission Date May 22, 2025
Acceptance Date June 3, 2025
Published in Issue Year 2025 Volume: 44 Issue: 1

Cite

APA Aktar, A., & Alçay, S. (2025). Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi. Journal of Research in Veterinary Medicine, 44(1), 42-48.
AMA Aktar A, Alçay S. Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi. J Res Vet Med. July 2025;44(1):42-48.
Chicago Aktar, Ahmet, and Selim Alçay. “Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi Ve Embriyo Gelişimi Üzerine Etkisi”. Journal of Research in Veterinary Medicine 44, no. 1 (July 2025): 42-48.
EndNote Aktar A, Alçay S (July 1, 2025) Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi. Journal of Research in Veterinary Medicine 44 1 42–48.
IEEE A. Aktar and S. Alçay, “Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi”, J Res Vet Med, vol. 44, no. 1, pp. 42–48, 2025.
ISNAD Aktar, Ahmet - Alçay, Selim. “Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi Ve Embriyo Gelişimi Üzerine Etkisi”. Journal of Research in Veterinary Medicine 44/1 (July 2025), 42-48.
JAMA Aktar A, Alçay S. Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi. J Res Vet Med. 2025;44:42–48.
MLA Aktar, Ahmet and Selim Alçay. “Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi Ve Embriyo Gelişimi Üzerine Etkisi”. Journal of Research in Veterinary Medicine, vol. 44, no. 1, 2025, pp. 42-48.
Vancouver Aktar A, Alçay S. Koyun Oositlerinin In Vitro Maturasyonu Sırasında Melatonin İlavesinin Sıcaklık Stresi ve Embriyo Gelişimi Üzerine Etkisi. J Res Vet Med. 2025;44(1):42-8.
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