Determination of the Effect of Fetal Sex on Placentome Size in Sheep
Year 2023,
Volume: 16 Issue: 2, 59 - 64, 31.12.2023
Ece Koldaş Ürer
,
Onur Bahan
,
Ayşe Merve Köse
,
Ahmet Gözer
Abstract
This study was carried out to reveal the effect of fetal gender on the size of placentomes, which have an essential role in fetal development, during mid and late pregnancy. The animal material of the study consisted of 11 pregnant Awassi sheep bearing a single fetus. Pregnant sheep were divided into two groups according to the sex of the fetus as those bearing male fetuses (Group E, n: 7) and those bearing female fetuses (Group D, n: 4). The mean diameter and thickness of the placentomes were determined by abdominal ultrasonography performed every ten days between 85-145 days pregnancy. On the days of ultra-sonographic examination, blood samples were also taken, and serum progesterone level was measured. As a result of the analyzes, it was observed that fetal sex did not effect on the mean diameter and thickness of the placentomes measured by ultrasonography, and also on the serum progesterone concentration in singleton pregnant ewes in the middle and late pregnancy (P>0.05). However, the change in the mentioned parameters during the examination days was statistically significant in both groups (P<0.001). It was concluded that fetal sex did not effect on placentome size in singleton pregnant ewes during a healthy progressing pregnancy. It was thought that the role of placentome thickness during pregnancy is a subject waiting to be clarified in future studies.
References
- Ocak S, Ogun S, Gunduz Z, Onder H. (2015). Goat Placental Efficiency Determination by Comparing Litter Weight to the Surface Area of the Cotyledons. Anim Reprod. 12: 920-926.
- Degrelle SA, Murthi P, Evain-Brion D, Fournier T, Hue I. (2011). Expression and Localization of DLX3, PPARG and SP1 in Bovine Trophoblast during Binucleated Cell Differentation. Placenta. 32: 917-920.
- Şen U, Sirin E, Kuran M. (2013). The Effect of Maternal Nutritional Status During Mid-gestation on Placental Characteristics in Ewes. Anim Reprod Sci. 137: 31-36.
- Karaca T, Yörük M. (2010). Ruminant Plasentalarının Yapı ve Fonksiyonu. Van Vet J. 21(3): 191-194.
- Sammin D, Markey B, Bassett H, Buxton D. (2009). The Ovine Placenta and Placentitis - A Review. Vet Microbiol. 135: 90-97.
- Kolosov YA, Klimenko AI, Vasilenko VN, et al. (2017). Some Biological Characteristics and Prediction of Sheep Productivity at Different Variants of Breed Selection. Online J Biol Sci. 17: 343-347.
- Mellor DJ, Stafford KJ. (2004). Animal Welfare Implications of Neonatal Mortality and Morbidity in Farm Animals. Vet J. 168: 118-133.
- Kaşıkçı G, Yılmaz Ö, Gündüz MC, Kırşan İ. (2011). Comparison of Placentome Diameters in Single and Twin-pregnant Sheep by Ultrasonographic Method. Turk J Vet Anim Sci. 35(3): 187-191.
- Waziri MA, Ikpe AB, Bukar MM, Ribadu AY. (2017). Determination of Gestational Age Through Trans-abdominal Scan of Placentome Diameter in Nigerian Breed of Sheep and Goats. Sokoto J Vet Sci. 15(2): 49-53.
- Carr DJ, Aitken RP, Milne JS, David AL, Wallace JM. (2011). Ultrasonographic Assessment of Growth and Estimation of Birthweight in Late Gestation Fetal Sheep. Ultrasound Med Biol. 37: 1588-1595.
- Tekin TC, Köse AM. (2022). The Effectiveness of Transabdominal Ultrasonography on the 35th Day of Pregnancy in Sheep for Determining Pregnancy and Number of Fetuses. J VetBio Sci Tech. 7(2): 143-152.
- Vannucchi CI, Veiga GAL, Silva LCG, Lúcio CF. (2019). Relationship Between Fetal Biometric Assessment by Ultrasonography and Neonatal Lamb Vitality, Birth Weight and Growth. Anim Reprod.16: 923-929.
- Brzozowska A, Wojtasiak N, Błaszczyk B, et al (2020). The Effects of Non-Genetic Factors on The Morphometric Parameters of Sheep Placenta and the Birth Weight of Lambs. Large Anim Rev. 26(3): 119-126.
- Vatnick I, Schoknecht PA, Darrigrand R, Bell AW. (1991). Growth and Metabolism of the Placenta After Unilateral Fetectomy in Twin Pregnant Ewes. J Dev Physiol. 15(6): 351-356.
- Meyer KM, Koch JM, Ramadoss J, Kling PJ, Magness RR. (2010). Ovine Surgical Model of Uterine Space Restriction: Interactive Effects of Uterine Anomalies and Multifetal Gestations on Fetal and Placental Growth. Biol Reprod. 83: 799-806.
- Vonnahme KA, Arndt WJ, Johnson ML, Borowicz PP, Reynolds LP. (2008). Effect of Morphology on Placentome Size, Vascularity, and Vasoreactivity in Late Pregnant Sheep. Biol Reprod. 79(5): 976-982.
- Redifer CA, Duncan NB, Meyer AM. (2021). Factors Affecting Placental Size in Beef Cattle: Maternal and Fetal Influences. Theriogenology. 15:174-149.
- Romo-Barron CB, Diaz D, Portillo-Loera JJ, et al. (2019). Impact of Heat Stress on the Reproductive Performance and Physiology of Ewes: A Systematic Review and Meta-Analyses. Int J Biometeorol. 63: 949-962.
- Van der Linden DS, Sciascia Q, Sales F, McCoard SA. (2013). Placental Nutrient Transport is Affected by Pregnancy Rank in Sheep. J Anim Sci. 91(2): 644-653.
- Ocak S, Emsen E, Köycegiz F, Kutluca M, Önder H. (2009). Comparison of Placental Traits and Their Relations to Litter Size and Parity Weight in Sheep. J Anim Sci. 87: 3196-3201.
- Alkass JE, Merkhan KY, Hamo RAH. (2013). Placental Traits and Their Relation with Birth Weight in Meriz and Black Goats. Sci J Anim Sci. 2(6): 168-172.
- Fernandes CE, Cigerza CF, Pinto GDS, et al. (2013). Parturition Characteristics and Uterine Involution in Native Sheep from Brazilian Pantanal. Ci Anim Bras Goiânia. 14(2): 245-252.
- Jawasreh KIZ, Awawdeh FT, Al-Khasawneh AZ, et al. (2009). The Effect of Some Placental Factors in Birth Weight of Awassi Lambs. Res J Anim Vet Sci. 4: 5-8.
- Gardner DS, Buttery PJ, Daniel Z, Symonds ME. (2007). Factors Affecting Birth Weight in Sheep: Maternal Environment. Reproduction. 133(1): 297-307.
- Steyn C, Hawkins P, Saito T, et al. (2001). Undernutrition during the First Half of Gestation Increases the Predominance of Fetal Tissue in Late-Gestation Ovine Placentomes. Eur J Obstet Gynecol Reprod Biol. 98(2): 165-170.
- Şen U. (2021). The Relationship between Placental Characteristics and Lamb Birth Weight in Akkaraman Turkish Native Sheep Breed. Large Anim Rev. 27(4): 223-232.
- Baneh H, Hafezian SH. (2009). Effects of Environmental Factors on Growth Traits in Ghezel Sheep. African J Biotech. 8(12): 2903-2907.
- Şen U, Onder H. (2016). Poor placental Traits Reduce Kid Birth Weight in Young Saanen Dams at the First Parity. Turk J Vet Anim Sci. 40: 554-561.
- Dombrowski MP, Wolfe HM, Saleh A, Evans MI, O’Brien J. (1992). The Sonographically Thick Placenta: A Predictor of Increased Perinatal Morbidity and Mortality. Ultrasound Obstet Gynecol. 2: 252-255.
- Elchalal U, Ezra Y, Levi Y, et al. (2000). Sonographically Thick Placenta: A Marker for Increased Perinatal Risk-A Prospective Cross-Sectional Study. Placenta. 21: 268-272.
- Doize F, Vaillancourt D, Carabin H, Belanger D. (1997). Determination of Gestational Age in Sheep and Goats Using Transrectal Ultrasonographic Measurement of Placentomes. Theriogenology. 48: 449-460.
- Enginler SÖ, Evkuran Dal G, Çetin AC, Sabuncu A, Baykal K. (2021). Can Gestational Age Be Determined by Placentome Diameter, Placentome Blood Flow Pixel Area and Progesterone Concentration During Pregnancy in Kivircik Ewes? Kafkas Univ Vet Fak Derg. 27 (6): 763-769.
- Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. (2004). Maternal Nutrition and Fetal Development. J Nutr. 134: 2169-2172.
- Sartori ED, Sessim AG, Brutti DD, et al. (2020). Fetal Programming in Sheep: Effects on Pre-and Postnatal Development in Lambs. J Anim Sci. 98(9): skaa294.
- Ithurralde J, Pérez-Clariget R, Corrales F, et al. (2019). Sex-Dependent Effects of Maternal Undernutrition on Growth Performance, Carcass Characteristics and Meat Quality of Lambs. Livest Sci. 221: 105-114.
- Kumar V, Singh SP, Farooqui MM, Kumar P, Prakash A. (2015). Gross and Biometrical Studies of Placentome in Goat (Capra hircus) during Different Stages of Pregnancy. J Anim Res. 5(2): 251-255.
- Penninga L, Longo LD. (1998). Ovine Placentome Morphology: Effect of High Altitude, Long-Term Hypoxia. Placenta. 19: 187-193.
- Ward JW, Forhead AJ, Wooding FBP, Fowden AL. (2006). Functional Significance and Cortisol Dependence of the Gross Morphology of Ovine Placentomes during Late Gestation. Biol Reprod. 74(1): 137-145.
- Alexander B, Coppola G, Mastromonaco GF, et al. (2008). Early Pregnancy Diagnosis by Serum Progesterone and Ultrasound in Sheep Carrying Somatic Cell Nuclear Transfer-Derived Pregnancies. Reprod Domest Anim. 43(2): 207-211.
- Wallace JM, Aitken RP, Cheyne MA, Humblot P. (1997). Pregnancy-Specific Protein B and Progesterone Concentrations in Relation to Nutritional Regimen, Placental Mass and Pregnancy Outcome in Growing Adolescent Ewes Carrying Singleton Fetuses. J Reprod Fertil. 109(1): 53-58.
- Ranilla MJ, Sulon J, Carro MD, Mantecon AR, Beckers JF. (1994). Plasmatic Profiles of Pregnancy-Associated Glycoprotein and Progesterone Levels during Gestation in Churra and Merino Sheep. Theriogenology. 42(3): 537-545.
- Uyanık F, Güvenç K, Gültekin M, Gürbulak K. (2007). Koyunlarda Gebeliğin Değişik Dönemlerinde Leptin ve Progesteron Düzeyleri. Erciyes Üniv Vet Fak Derg. 6(1): 31-36.
- Leaver HA, Howie A, Aitken ID, et al. (1989). Changes in Progesterone, Oestradiol-17 Beta, and Intrauterine Prostaglandin E2 During Late Gestation in Sheep Experimentally Infected with an Ovine Abortion Strain of Chlamydia Psittaci. Microbiology. 135: 565-573.
- Bekeova E, Elecko J, Krajnicakova M, Hendrichovsky V, Maracek I. (1991). Dynamics of Changes in the Concentrations of Cholesterol and Thyroid and Ovarian Hormones in Blood Serum in the Postpartum Period in Ewes. Vet Med (Praha). 36: 673-684.
- Köse AM, Koldaş Ürer E. (2022). İnvestigation of Maternal Blood Progesterone Hormone Levels in Middle and Late Pregnancy and After Parturition in Sheep and Goats, AGRO, İnternational Conference on Agrıculture, June 04-06,Online.
- Özpinar A, Fırat A. (2003). Metabolic Profile of Pre-pregnancy, Pregnancy and Early Lactation in Multiple Lambing Sakız Ewes. 2. Changes in Plasma Progesterone, Estradiol-17 Beta and Cholesterol Levels. Ann Nutr Metab. 47(3/4): 139-143.
- Miura H, Yamazaki T, Kikuchi M, Sakaguchi M. (2019). Plasma Steroid Hormone Concentrations and Their Relationships in Suffolk Ewes during Gestation and Parturition. Anim Sci J. 90(11): 1426-1431.
Koyunlarda Plasentom Boyutuna Fötal Cinsiyetin Etkisinin Belirlenmesi
Year 2023,
Volume: 16 Issue: 2, 59 - 64, 31.12.2023
Ece Koldaş Ürer
,
Onur Bahan
,
Ayşe Merve Köse
,
Ahmet Gözer
Abstract
Bu çalışma fötal gelişimde önemli rolü olan plasentomların, orta ve ileri gebelik sürecindeki boyutuna fötal cinsiyetin etkisini ortaya çıkarmak amacıyla yürütülmüştür. Çalışmanın hayvan materyalini tekiz gebe olan 11 adet İvesi ırkı koyun oluşturdu. Gebe koyunlar taşıdıkları fetüsün cinsiyetine göre; erkek fetüs taşıyanlar (Grup E, n:7) ve dişi fetüs taşıyanlar olarak (Grup D, n:4) olarak iki gruba ayrıldı. Gebeliğin 85-145. günleri arasında her 10 günde bir gerçekleştirilen abdominal ultrasonografi ile plasentom ortalama çap ve kalınlıkları belirlendi. Ultrasonografik muayene günlerinde ayrıca kan numuneleri alınarak serum progesteron düzeyi ölçüldü. Analizler sonucunda orta ve ileri dönemde olan tekiz gebe koyunlarda fötal cinsiyetin ultrasonografik olarak ölçülen plasentom ortalama çap ve kalınlığına, ayrıca serum progesteron düzeyine etkisi olmadığı görüldü (P>0.05). Ancak sözü geçen parametrelerin muayene günleri boyunca değişimi her iki grupta da istatistik olarak anlamlıydı (P<0.001). Sağlıklı ilerleyen gebelik sürecinde tekiz gebe koyunlarda fötal cinsiyetin plasentom boyutuna etkisinin olmadığı sonucuna varıldı. Gebelik sürecinde plasentom kalınlığının rolünün gelecekte yapılacak çalışmalarda aydınlatılmayı bekleyen bir konu olduğu düşünüldü.
References
- Ocak S, Ogun S, Gunduz Z, Onder H. (2015). Goat Placental Efficiency Determination by Comparing Litter Weight to the Surface Area of the Cotyledons. Anim Reprod. 12: 920-926.
- Degrelle SA, Murthi P, Evain-Brion D, Fournier T, Hue I. (2011). Expression and Localization of DLX3, PPARG and SP1 in Bovine Trophoblast during Binucleated Cell Differentation. Placenta. 32: 917-920.
- Şen U, Sirin E, Kuran M. (2013). The Effect of Maternal Nutritional Status During Mid-gestation on Placental Characteristics in Ewes. Anim Reprod Sci. 137: 31-36.
- Karaca T, Yörük M. (2010). Ruminant Plasentalarının Yapı ve Fonksiyonu. Van Vet J. 21(3): 191-194.
- Sammin D, Markey B, Bassett H, Buxton D. (2009). The Ovine Placenta and Placentitis - A Review. Vet Microbiol. 135: 90-97.
- Kolosov YA, Klimenko AI, Vasilenko VN, et al. (2017). Some Biological Characteristics and Prediction of Sheep Productivity at Different Variants of Breed Selection. Online J Biol Sci. 17: 343-347.
- Mellor DJ, Stafford KJ. (2004). Animal Welfare Implications of Neonatal Mortality and Morbidity in Farm Animals. Vet J. 168: 118-133.
- Kaşıkçı G, Yılmaz Ö, Gündüz MC, Kırşan İ. (2011). Comparison of Placentome Diameters in Single and Twin-pregnant Sheep by Ultrasonographic Method. Turk J Vet Anim Sci. 35(3): 187-191.
- Waziri MA, Ikpe AB, Bukar MM, Ribadu AY. (2017). Determination of Gestational Age Through Trans-abdominal Scan of Placentome Diameter in Nigerian Breed of Sheep and Goats. Sokoto J Vet Sci. 15(2): 49-53.
- Carr DJ, Aitken RP, Milne JS, David AL, Wallace JM. (2011). Ultrasonographic Assessment of Growth and Estimation of Birthweight in Late Gestation Fetal Sheep. Ultrasound Med Biol. 37: 1588-1595.
- Tekin TC, Köse AM. (2022). The Effectiveness of Transabdominal Ultrasonography on the 35th Day of Pregnancy in Sheep for Determining Pregnancy and Number of Fetuses. J VetBio Sci Tech. 7(2): 143-152.
- Vannucchi CI, Veiga GAL, Silva LCG, Lúcio CF. (2019). Relationship Between Fetal Biometric Assessment by Ultrasonography and Neonatal Lamb Vitality, Birth Weight and Growth. Anim Reprod.16: 923-929.
- Brzozowska A, Wojtasiak N, Błaszczyk B, et al (2020). The Effects of Non-Genetic Factors on The Morphometric Parameters of Sheep Placenta and the Birth Weight of Lambs. Large Anim Rev. 26(3): 119-126.
- Vatnick I, Schoknecht PA, Darrigrand R, Bell AW. (1991). Growth and Metabolism of the Placenta After Unilateral Fetectomy in Twin Pregnant Ewes. J Dev Physiol. 15(6): 351-356.
- Meyer KM, Koch JM, Ramadoss J, Kling PJ, Magness RR. (2010). Ovine Surgical Model of Uterine Space Restriction: Interactive Effects of Uterine Anomalies and Multifetal Gestations on Fetal and Placental Growth. Biol Reprod. 83: 799-806.
- Vonnahme KA, Arndt WJ, Johnson ML, Borowicz PP, Reynolds LP. (2008). Effect of Morphology on Placentome Size, Vascularity, and Vasoreactivity in Late Pregnant Sheep. Biol Reprod. 79(5): 976-982.
- Redifer CA, Duncan NB, Meyer AM. (2021). Factors Affecting Placental Size in Beef Cattle: Maternal and Fetal Influences. Theriogenology. 15:174-149.
- Romo-Barron CB, Diaz D, Portillo-Loera JJ, et al. (2019). Impact of Heat Stress on the Reproductive Performance and Physiology of Ewes: A Systematic Review and Meta-Analyses. Int J Biometeorol. 63: 949-962.
- Van der Linden DS, Sciascia Q, Sales F, McCoard SA. (2013). Placental Nutrient Transport is Affected by Pregnancy Rank in Sheep. J Anim Sci. 91(2): 644-653.
- Ocak S, Emsen E, Köycegiz F, Kutluca M, Önder H. (2009). Comparison of Placental Traits and Their Relations to Litter Size and Parity Weight in Sheep. J Anim Sci. 87: 3196-3201.
- Alkass JE, Merkhan KY, Hamo RAH. (2013). Placental Traits and Their Relation with Birth Weight in Meriz and Black Goats. Sci J Anim Sci. 2(6): 168-172.
- Fernandes CE, Cigerza CF, Pinto GDS, et al. (2013). Parturition Characteristics and Uterine Involution in Native Sheep from Brazilian Pantanal. Ci Anim Bras Goiânia. 14(2): 245-252.
- Jawasreh KIZ, Awawdeh FT, Al-Khasawneh AZ, et al. (2009). The Effect of Some Placental Factors in Birth Weight of Awassi Lambs. Res J Anim Vet Sci. 4: 5-8.
- Gardner DS, Buttery PJ, Daniel Z, Symonds ME. (2007). Factors Affecting Birth Weight in Sheep: Maternal Environment. Reproduction. 133(1): 297-307.
- Steyn C, Hawkins P, Saito T, et al. (2001). Undernutrition during the First Half of Gestation Increases the Predominance of Fetal Tissue in Late-Gestation Ovine Placentomes. Eur J Obstet Gynecol Reprod Biol. 98(2): 165-170.
- Şen U. (2021). The Relationship between Placental Characteristics and Lamb Birth Weight in Akkaraman Turkish Native Sheep Breed. Large Anim Rev. 27(4): 223-232.
- Baneh H, Hafezian SH. (2009). Effects of Environmental Factors on Growth Traits in Ghezel Sheep. African J Biotech. 8(12): 2903-2907.
- Şen U, Onder H. (2016). Poor placental Traits Reduce Kid Birth Weight in Young Saanen Dams at the First Parity. Turk J Vet Anim Sci. 40: 554-561.
- Dombrowski MP, Wolfe HM, Saleh A, Evans MI, O’Brien J. (1992). The Sonographically Thick Placenta: A Predictor of Increased Perinatal Morbidity and Mortality. Ultrasound Obstet Gynecol. 2: 252-255.
- Elchalal U, Ezra Y, Levi Y, et al. (2000). Sonographically Thick Placenta: A Marker for Increased Perinatal Risk-A Prospective Cross-Sectional Study. Placenta. 21: 268-272.
- Doize F, Vaillancourt D, Carabin H, Belanger D. (1997). Determination of Gestational Age in Sheep and Goats Using Transrectal Ultrasonographic Measurement of Placentomes. Theriogenology. 48: 449-460.
- Enginler SÖ, Evkuran Dal G, Çetin AC, Sabuncu A, Baykal K. (2021). Can Gestational Age Be Determined by Placentome Diameter, Placentome Blood Flow Pixel Area and Progesterone Concentration During Pregnancy in Kivircik Ewes? Kafkas Univ Vet Fak Derg. 27 (6): 763-769.
- Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. (2004). Maternal Nutrition and Fetal Development. J Nutr. 134: 2169-2172.
- Sartori ED, Sessim AG, Brutti DD, et al. (2020). Fetal Programming in Sheep: Effects on Pre-and Postnatal Development in Lambs. J Anim Sci. 98(9): skaa294.
- Ithurralde J, Pérez-Clariget R, Corrales F, et al. (2019). Sex-Dependent Effects of Maternal Undernutrition on Growth Performance, Carcass Characteristics and Meat Quality of Lambs. Livest Sci. 221: 105-114.
- Kumar V, Singh SP, Farooqui MM, Kumar P, Prakash A. (2015). Gross and Biometrical Studies of Placentome in Goat (Capra hircus) during Different Stages of Pregnancy. J Anim Res. 5(2): 251-255.
- Penninga L, Longo LD. (1998). Ovine Placentome Morphology: Effect of High Altitude, Long-Term Hypoxia. Placenta. 19: 187-193.
- Ward JW, Forhead AJ, Wooding FBP, Fowden AL. (2006). Functional Significance and Cortisol Dependence of the Gross Morphology of Ovine Placentomes during Late Gestation. Biol Reprod. 74(1): 137-145.
- Alexander B, Coppola G, Mastromonaco GF, et al. (2008). Early Pregnancy Diagnosis by Serum Progesterone and Ultrasound in Sheep Carrying Somatic Cell Nuclear Transfer-Derived Pregnancies. Reprod Domest Anim. 43(2): 207-211.
- Wallace JM, Aitken RP, Cheyne MA, Humblot P. (1997). Pregnancy-Specific Protein B and Progesterone Concentrations in Relation to Nutritional Regimen, Placental Mass and Pregnancy Outcome in Growing Adolescent Ewes Carrying Singleton Fetuses. J Reprod Fertil. 109(1): 53-58.
- Ranilla MJ, Sulon J, Carro MD, Mantecon AR, Beckers JF. (1994). Plasmatic Profiles of Pregnancy-Associated Glycoprotein and Progesterone Levels during Gestation in Churra and Merino Sheep. Theriogenology. 42(3): 537-545.
- Uyanık F, Güvenç K, Gültekin M, Gürbulak K. (2007). Koyunlarda Gebeliğin Değişik Dönemlerinde Leptin ve Progesteron Düzeyleri. Erciyes Üniv Vet Fak Derg. 6(1): 31-36.
- Leaver HA, Howie A, Aitken ID, et al. (1989). Changes in Progesterone, Oestradiol-17 Beta, and Intrauterine Prostaglandin E2 During Late Gestation in Sheep Experimentally Infected with an Ovine Abortion Strain of Chlamydia Psittaci. Microbiology. 135: 565-573.
- Bekeova E, Elecko J, Krajnicakova M, Hendrichovsky V, Maracek I. (1991). Dynamics of Changes in the Concentrations of Cholesterol and Thyroid and Ovarian Hormones in Blood Serum in the Postpartum Period in Ewes. Vet Med (Praha). 36: 673-684.
- Köse AM, Koldaş Ürer E. (2022). İnvestigation of Maternal Blood Progesterone Hormone Levels in Middle and Late Pregnancy and After Parturition in Sheep and Goats, AGRO, İnternational Conference on Agrıculture, June 04-06,Online.
- Özpinar A, Fırat A. (2003). Metabolic Profile of Pre-pregnancy, Pregnancy and Early Lactation in Multiple Lambing Sakız Ewes. 2. Changes in Plasma Progesterone, Estradiol-17 Beta and Cholesterol Levels. Ann Nutr Metab. 47(3/4): 139-143.
- Miura H, Yamazaki T, Kikuchi M, Sakaguchi M. (2019). Plasma Steroid Hormone Concentrations and Their Relationships in Suffolk Ewes during Gestation and Parturition. Anim Sci J. 90(11): 1426-1431.