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Fetal programming in pregnant cows and epigenetic changes: The impact of nutrition and heat stress

Yıl 2025, Cilt: 96 Sayı: 1, 76 - 87, 15.01.2025
https://doi.org/10.33188/vetheder.1440226

Öz

The vital functions of an adult animal are shaped by environmental influences encountered postnatally. However, recent research has shown that the prenatal period can also significantly determine an animal's future performance. This concept, referred to variously as fetal programming, developmental programming, or the developmental origins of health and disease, suggests that environmental factors during the prenatal period can have long-term effects on an individual’s postnatal growth, health, and physiological functions. This crucial concept emphasizes the ability to program the measurable genetic structures that shape the offspring’s postnatal characteristics in various ways. Initial fetal programming studies in pregnant cows focused on calf birth weight, later revealing that environmental factors such as maternal nutrient deficiency and heat stress can have diverse impacts on the fetus. It has been understood that prenatal environmental factors can negatively affect vital traits such as milk production, carcass yield, feed efficiency, and reproductive function throughout the animal's life. Epigenetic changes, which involve permanent modifications in gene expression without altering the DNA sequence, play a key role in this process. Maternal nutrition and heat stress can alter the fetus's gene expression profiles through epigenetic mechanisms such as DNA methylation and histone modifications. These changes can result in permanent phenotypic traits that affect the calf's health and productivity in the postnatal period. Therefore, proper management of the prenatal period and provision of appropriate environmental conditions are crucial for animal welfare and sectoral productivity. This review addresses the mechanisms affecting fetal programming processes in pregnant cows and the long-term effects of such programming.

Kaynakça

  • Barker DJP. In utero programming of chronic disease. Clinical Science 1998;95:115–128.
  • Godfrey KM, Costell PM, Lillycrop KA. The developmental environment, epigenetic biomarkers and long-term health. Journal of Developmental Origins of Health and Disease 2015;6(5): 399–406.
  • Lemley CO. Managing The Pregnant Female – Fetal Programming Proceedings. Applied Reproductive Strategies in Beef Cattle 2019;20-21.
  • Jaenisch R , Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33: 245-254.
  • Stevenson K, Lillycrop KA, Silver MJ. Fetal programming and epigenetics. Current Opinion in Endocrine and Metabolic Research 2020; 13:1-6.
  • Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Buchanan DS, Hafez SA, Grazul-Bilska AT, Redmer DA. Uteroplacental vascular development and placental function: an update. Int. J.Dev.Biol. 2010;(2–3): 355– 366.
  • Funston RN, Summers AF. Epigenetics: Setting Up Lifetime Production of Beef Cows by Managing Nutrition. Annu. Rev. Anim. Biosci. 2013;1:339–363.
  • Palmer P, Velazquez MA, Jammes H, Duranthov N. Review: Epigenetics, developmental programming and nutrition in herbivores. Animal 2018; 12-2: 363–371.
  • Thompson RP, Nilsson E, Skinner MK. Environmental epigenetics and epigenetic inheritance in domestic farm animals. Animal Reproduction Science 2020;220 .
  • Khalil CA. The emerging role of epigenetics in cardiovascular disease. Ther Adv Chronic Dis.2014;5(4): 178-187.
  • Rogers JM, Ellis-Hutchings RG, Lau C. Epigenetics and the Developmental Origins of Health and Disease Comprehensive. Toxicology 2010; 12: 69–88.
  • Wu C, Sirard MA. Parental Effects on Epigenetic Programming in Gametes and Embryos of Dairy Cows Front. Genet. 2020;11:557846.
  • Gardner KE, Allis CD, Strahl BD. Operating on chromatin, a colorful language where context matters. Journal of Molecular Biology 2011;409:36–46.
  • Nolte-‘T Hoen EN, Van Rooij E, Bushell M, Zhang CY, Dashwood RH, James WP, Harris C, Baltimore D. The role of microRNA in nutritional control. Journal of Internal Medicin 2020; 278:99–109.
  • Chen K, Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics 2007;8:93–103.
  • Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nature Reviews Genetics 2012;13: 271–282.
  • Wathes DC. Developmental Programming of Fertility in Cattle—Is It a Cause for Concern? Animals, 2022;12:2654.
  • Hales CN, Barker DJ. The thrifty phenotype hypothesis. British Medical Bulletin 2001;60, 5–20.
  • Micke GC, Sullivan TM, Gatford KL, Owens JA, Perry VE. Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits. Anim Reprod Sci. 2010;121(3-4): 208-17.
  • Long JM, Trubenbach LA, Pryor JH, Long CR, Wickersham TA, Sawyer JE, Satterfield MC. Maternal nutrient restriction alters endocrine pancreas development in fetal heifers Domest Anim Endocrinol. 2021;74:106580.
  • Polizel GHG, Fantinato-Neto P, Rangel RB, Grigoletto L, Bussiman FDO, Cracco RC, Garcia NP, Ruy IM, Ferraz JBS, Santana MHDA. Evaluation of reproductive traits and the effect of nutrigenetics on bulls submitted to fetal programming. Livestock Science 2021;247: 104487.
  • Yao S, Lopez-Tello J, Sferruzzi-Perri AN. Developmental programming of the female reproductive system—a review. Biology of Reproduction 2021;104(4):745–770 .
  • Greenwood P, Cafe L. Prenatal and pre-weaning growth and nutrition of cattle: Long-term consequences for beef production. Animal 2007;1:(9) 1283-1296.
  • Zago D, Canozzİ M, Barcellos J. Pregnant cow nutrition and its effects on foetal weight –a meta-analysis. The Journal of Agricultural Science 2019;157(1):83-95.
  • Gonzalez JM, Camacho LE, Ebarb SM, Swanson KC, Vonnahme KA, Stelzleni AM, Johnson SE. Realimentation of nutrient restricted pregnant beef cows supports compensatory fetal muscle growth. J. Anim. Sci. 2013;91:4797–4806.
  • Du M, Ford SP, Zhu M-J. Optimizing livestock production efficiency through maternal nutritional management and fetal developmental programming. Animal Frontiers 2017; 7(3): 5–11.
  • Posont RJ, Yates D. Postnatal Nutrient Repartitioning due to Adaptive Developmental Programming. Vet Clin North Am Food Anim Pract. 2019;35(2):277-288.
  • Khanal P, Nielsen MO. Impacts of prenatal nutrition on animal production and performance: A focus on growth and metabolic and endocrine function in sheep. J.Anim. Sci. Biotechnol. 2017;8:75.
  • Rutkowskaa K, Stachowiakb M, Oprzadeka J, Bauersachsc S, Flisikowski K. Altered miRNA-4321 expression in maternal and foetal placenta of intrauterine growth restricted bovine foetuses. Placenta 2018;70:50–52.
  • Vonnahme KA. Nutrition During Gestation and Fetal Programming Proceedings. The Range Beef Cow Symposium 2007;11-13 Colorado: Fort Collins.
  • Zhang H, Sun W, Wang ZY, Deng MT, Zhang GM, Guo RH, Ma TW, Wang F. Dietary N-carbamylglutamate and rumen-protected L-arginine supplementation ameliorate fetal growth restriction in undernourished ewes. J. Anim. Sci. 2016; 94:2072-2085.
  • Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two-thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biology and Reproduction 2007;76:259-267.
  • Van Eetvelde M, Verdru K, De Jong G, Van Pelt ML, Meesters M, Opsomer G. Researching 100 t cows: An innovative approach to identify intrinsic cow factors associated with a high lifetime milk production. Prev. Vet. Med. 2021;193, 105392.
  • Caton JS, Crouse MS, Reynolds LP, Neville TL, Dahlen CR, Ward AK, Swanson KC. Maternal nutrition and programming of offspring energy requirements. Translational Animal Science 2019;3(3): 976–990.
  • Sullivan TM, Micke GC, Perkins N, Martin GB, Wallace CR, Gatford KL, Owens JA, Perry VE. Dietary protein during gestation affects maternal insulin-like growth factor, insulin-like growth factor binding protein, leptin concentrations, and fetal growth in heifers. J. Anim. Sci.2009; 87: 3304–3316.
  • Mossa F, Walsh SW, Butler ST, Berry DP, Carter F, Lonergan P, Smith GW, Ireland JJ, Evans AC. Low numbers of ovarian follicles ≥3 mm in diameter are associated with low fertility in dairy cows. J. Dairy Sci. 2012;95: 2355–2361.
  • Hurlbert JL, Baumgaertner F, Menezes ACB, Bochantin KA, Diniz WJS, Underdahl SR, Dorsam ST, Kirsch JD, Sedivec KK, Dahlen CR. Supplementing vitamins and minerals to beef heifers during gestation: impacts on mineral status in the dam and offspring, and growth and physiological responses of female offspring from birth to puberty. J Anim Sci 2024 ;102.
  • Thomson EE, Beltman ME, Crowe MA, McAloon CG, Furlong JG, Duane MM, Brennan JPN, McDonald MM, Kelly ET. Association between maternal growth in the pre-conception and early gestational period of nulliparous dairy heifers with anti-Müllerian hormone in their female offspring. Reprod Domest Anim 2024;59(1).
  • Cushman RA, Akbarinejad V, Perry GA, Lents CA. Developmental programming of the ovarian reserve in livestock. Anim Reprod Sci 2024;264.
  • Aiken CE, Tarry-Adkins JL, Penfold NC, Dearden L, Ozanne SE. Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet. FASEB J Off Publ Fed Am Soc Exp Biol 2016;30:1548–1556.
  • Laporta J, Dado-Senn B, Skibiel AL. Late gestation hyperthermia:epigenetic programming of daughter's mammary development and function. Domest Anim Endocrinol. 2022;78,106681.
  • Dahl GE, Skibiel AL, Laporta J. In Utero Heat Stress Programs Reduced Performance and Health in Calves. Vet Clin North Am Food Anim Pract. 2019;35(2):343-353.
  • Geiger AJ, Parsons CLM, Akers RM. Feeding a higher plane of nutrition and providing exogenous estrogen increases mammary gland development in Holstein heifer calves. J Dairy Sci 2016;99:7642–53.
  • Polsky L, Keyserlingk MA. Invited review: Effects of heat stress on dairy cattle welfare. J. Dairy Sci. 2017;100:8645–8657.
  • Vural R. Sıcak Stresinin Reprodüksiyon Üzerine Etkisi. Sürü Sağlığı ve Yönetimi E- Kongresi; 88-97; 2021.
  • Herbut P, Angrecka S, Walczak J. Environmental parameters to assessing of heat stress in dairy cattle—a review. Int J Biometeorol 2018;62:2089–2097.
  • Dado-Senn B, Laporta J, Dahl GE. Carry over effects of late-gestational heat stress on dairy cattle progeny. Theriogenology 2020;154:17-23.
  • Nickles KR, Relling AE, Garcia-Guerra A, Fluharty FL, Kieffer J, Parker AJ. Beef cows housed in mud during late gestation have greater net energy requirements compared with cows housed on wood chip bedding. Transl. Anim. Sci 2022;6(2).
  • Monteiro APA, Guo JR, Weng XS, Ahmed BM, Hayen MJ, Dahl GE, Bernard JK, Tao S. Effect of maternal heat stress during the dry period on growth and metabolism of calves. J. Dairy Sci. 2016;99(5): 3896-3907.
  • Dahl GE, Tao S, Laporta J. Heat Stress Impacts Immune Status in Cows Across the Life Cycle. Front. Vet. Sci 2020;7:116.
  • Tao S, Monteiro APA, Thompson IM, Hayen MJ, Dahl GE. Effect of late-gestation maternal heat stress on growth and immune function of dairy calves. J. Dairy Sci 2012;95 :7128–7136.
  • Ahmed BMS., Younas U, Asar TO, Monteiro APA, Hayen J, Tao S. Maternal heat stress reduces body and organ growth in calves: relationship to immune tissue development. J Anim Sci 2016;94:617.
  • Ghaffari MH. Developmental programming: prenatal and postnatal consequences of hyperthermia in dairy cows and calves. Domest Anim Endocrinol. 2020;80.
  • Lemley CO, Littlejohn BP, Burnett DD. Fetal Programming. In: Hopper RM, editor. Bovine Reproduction, Second Edition. John Wiley & Sons; 2021. p. 339-346.

Gebe ineklerde fetal programlama ve epigenetik değişimler: Beslenme ve ısı stresinin etkisi

Yıl 2025, Cilt: 96 Sayı: 1, 76 - 87, 15.01.2025
https://doi.org/10.33188/vetheder.1440226

Öz

Yetişkin bir hayvanın yaşamsal işlevleri, doğum sonrasında maruz kaldığı çevresel etkilerle şekillenirken, son yıllarda yapılan araştırmalar, doğumdan önceki dönemin de hayvanın gelecekteki performansını belirleyebileceğini göstermektedir. Fetal programlama, gelişimsel programlama ya da sağlık ve hastalığın gelişimsel kökenleri olarak çeşitli şekillerde adlandırılan bu kavram, doğum öncesi dönemdeki çevresel faktörlerin bireyin doğum sonrası büyüme, sağlık ve fizyolojik işlevleri üzerinde uzun vadeli etkiler yaratabileceğini ortaya koymaktadır. Bu önemli konsept, yavrunun doğum sonrası özelliklerini şekillendiren ölçülebilir genetik yapıları farklı şekillerde programlayabilme yeteneğine vurgu yapar. Özellikle gebe ineklerde yavru doğum ağırlığına odaklanan ilk fetal programlama çalışmaları, daha sonra annenin yaşadığı besin eksikliği, ısı stresi gibi çevresel etkilerin de fetüs üzerinde farklı sonuçlar yaratabileceğini göstermiştir. Doğum öncesi dönemdeki çevresel faktörlerin, hayvanın yaşamının geri kalanında süt üretimi, karkas verimi, yemden yararlanma verimliliği ve/veya üreme işlevi gibi hayati özellikler üzerinde olumsuz sonuçlar doğurabileceği anlaşılmaktadır. Epigenetik değişimler ise, DNA diziliminde bir değişiklik olmaksızın gen ekspresyonunda meydana gelen kalıcı değişikliklerdir. Anne inekteki beslenme ve ısı stresi, DNA metilasyonu ve histon modifikasyonları gibi epigenetik mekanizmalar üzerinden fetusun gen ekspresyon profillerini değiştirebilir. Bu değişimler, buzağıların doğum sonrası dönemde sağlık ve verimliliklerini etkileyen kalıcı fenotipik özellikler oluşturabilir. Bu nedenle, doğum öncesi dönemin doğru yönetimi ve hayvanın ihtiyaç duyduğu uygun çevresel koşulların sağlanması, hem hayvan refahı hem de sektörel verimlilik açısından kritik öneme sahiptir. Bu derleme, gebe ineklerdeki fetal programlama süreçlerini etkileyen mekanizmaları ve bu programlamanın doğurduğu uzun vadeli etkileri ele almaktadır.

Kaynakça

  • Barker DJP. In utero programming of chronic disease. Clinical Science 1998;95:115–128.
  • Godfrey KM, Costell PM, Lillycrop KA. The developmental environment, epigenetic biomarkers and long-term health. Journal of Developmental Origins of Health and Disease 2015;6(5): 399–406.
  • Lemley CO. Managing The Pregnant Female – Fetal Programming Proceedings. Applied Reproductive Strategies in Beef Cattle 2019;20-21.
  • Jaenisch R , Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33: 245-254.
  • Stevenson K, Lillycrop KA, Silver MJ. Fetal programming and epigenetics. Current Opinion in Endocrine and Metabolic Research 2020; 13:1-6.
  • Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Buchanan DS, Hafez SA, Grazul-Bilska AT, Redmer DA. Uteroplacental vascular development and placental function: an update. Int. J.Dev.Biol. 2010;(2–3): 355– 366.
  • Funston RN, Summers AF. Epigenetics: Setting Up Lifetime Production of Beef Cows by Managing Nutrition. Annu. Rev. Anim. Biosci. 2013;1:339–363.
  • Palmer P, Velazquez MA, Jammes H, Duranthov N. Review: Epigenetics, developmental programming and nutrition in herbivores. Animal 2018; 12-2: 363–371.
  • Thompson RP, Nilsson E, Skinner MK. Environmental epigenetics and epigenetic inheritance in domestic farm animals. Animal Reproduction Science 2020;220 .
  • Khalil CA. The emerging role of epigenetics in cardiovascular disease. Ther Adv Chronic Dis.2014;5(4): 178-187.
  • Rogers JM, Ellis-Hutchings RG, Lau C. Epigenetics and the Developmental Origins of Health and Disease Comprehensive. Toxicology 2010; 12: 69–88.
  • Wu C, Sirard MA. Parental Effects on Epigenetic Programming in Gametes and Embryos of Dairy Cows Front. Genet. 2020;11:557846.
  • Gardner KE, Allis CD, Strahl BD. Operating on chromatin, a colorful language where context matters. Journal of Molecular Biology 2011;409:36–46.
  • Nolte-‘T Hoen EN, Van Rooij E, Bushell M, Zhang CY, Dashwood RH, James WP, Harris C, Baltimore D. The role of microRNA in nutritional control. Journal of Internal Medicin 2020; 278:99–109.
  • Chen K, Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics 2007;8:93–103.
  • Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nature Reviews Genetics 2012;13: 271–282.
  • Wathes DC. Developmental Programming of Fertility in Cattle—Is It a Cause for Concern? Animals, 2022;12:2654.
  • Hales CN, Barker DJ. The thrifty phenotype hypothesis. British Medical Bulletin 2001;60, 5–20.
  • Micke GC, Sullivan TM, Gatford KL, Owens JA, Perry VE. Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits. Anim Reprod Sci. 2010;121(3-4): 208-17.
  • Long JM, Trubenbach LA, Pryor JH, Long CR, Wickersham TA, Sawyer JE, Satterfield MC. Maternal nutrient restriction alters endocrine pancreas development in fetal heifers Domest Anim Endocrinol. 2021;74:106580.
  • Polizel GHG, Fantinato-Neto P, Rangel RB, Grigoletto L, Bussiman FDO, Cracco RC, Garcia NP, Ruy IM, Ferraz JBS, Santana MHDA. Evaluation of reproductive traits and the effect of nutrigenetics on bulls submitted to fetal programming. Livestock Science 2021;247: 104487.
  • Yao S, Lopez-Tello J, Sferruzzi-Perri AN. Developmental programming of the female reproductive system—a review. Biology of Reproduction 2021;104(4):745–770 .
  • Greenwood P, Cafe L. Prenatal and pre-weaning growth and nutrition of cattle: Long-term consequences for beef production. Animal 2007;1:(9) 1283-1296.
  • Zago D, Canozzİ M, Barcellos J. Pregnant cow nutrition and its effects on foetal weight –a meta-analysis. The Journal of Agricultural Science 2019;157(1):83-95.
  • Gonzalez JM, Camacho LE, Ebarb SM, Swanson KC, Vonnahme KA, Stelzleni AM, Johnson SE. Realimentation of nutrient restricted pregnant beef cows supports compensatory fetal muscle growth. J. Anim. Sci. 2013;91:4797–4806.
  • Du M, Ford SP, Zhu M-J. Optimizing livestock production efficiency through maternal nutritional management and fetal developmental programming. Animal Frontiers 2017; 7(3): 5–11.
  • Posont RJ, Yates D. Postnatal Nutrient Repartitioning due to Adaptive Developmental Programming. Vet Clin North Am Food Anim Pract. 2019;35(2):277-288.
  • Khanal P, Nielsen MO. Impacts of prenatal nutrition on animal production and performance: A focus on growth and metabolic and endocrine function in sheep. J.Anim. Sci. Biotechnol. 2017;8:75.
  • Rutkowskaa K, Stachowiakb M, Oprzadeka J, Bauersachsc S, Flisikowski K. Altered miRNA-4321 expression in maternal and foetal placenta of intrauterine growth restricted bovine foetuses. Placenta 2018;70:50–52.
  • Vonnahme KA. Nutrition During Gestation and Fetal Programming Proceedings. The Range Beef Cow Symposium 2007;11-13 Colorado: Fort Collins.
  • Zhang H, Sun W, Wang ZY, Deng MT, Zhang GM, Guo RH, Ma TW, Wang F. Dietary N-carbamylglutamate and rumen-protected L-arginine supplementation ameliorate fetal growth restriction in undernourished ewes. J. Anim. Sci. 2016; 94:2072-2085.
  • Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two-thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biology and Reproduction 2007;76:259-267.
  • Van Eetvelde M, Verdru K, De Jong G, Van Pelt ML, Meesters M, Opsomer G. Researching 100 t cows: An innovative approach to identify intrinsic cow factors associated with a high lifetime milk production. Prev. Vet. Med. 2021;193, 105392.
  • Caton JS, Crouse MS, Reynolds LP, Neville TL, Dahlen CR, Ward AK, Swanson KC. Maternal nutrition and programming of offspring energy requirements. Translational Animal Science 2019;3(3): 976–990.
  • Sullivan TM, Micke GC, Perkins N, Martin GB, Wallace CR, Gatford KL, Owens JA, Perry VE. Dietary protein during gestation affects maternal insulin-like growth factor, insulin-like growth factor binding protein, leptin concentrations, and fetal growth in heifers. J. Anim. Sci.2009; 87: 3304–3316.
  • Mossa F, Walsh SW, Butler ST, Berry DP, Carter F, Lonergan P, Smith GW, Ireland JJ, Evans AC. Low numbers of ovarian follicles ≥3 mm in diameter are associated with low fertility in dairy cows. J. Dairy Sci. 2012;95: 2355–2361.
  • Hurlbert JL, Baumgaertner F, Menezes ACB, Bochantin KA, Diniz WJS, Underdahl SR, Dorsam ST, Kirsch JD, Sedivec KK, Dahlen CR. Supplementing vitamins and minerals to beef heifers during gestation: impacts on mineral status in the dam and offspring, and growth and physiological responses of female offspring from birth to puberty. J Anim Sci 2024 ;102.
  • Thomson EE, Beltman ME, Crowe MA, McAloon CG, Furlong JG, Duane MM, Brennan JPN, McDonald MM, Kelly ET. Association between maternal growth in the pre-conception and early gestational period of nulliparous dairy heifers with anti-Müllerian hormone in their female offspring. Reprod Domest Anim 2024;59(1).
  • Cushman RA, Akbarinejad V, Perry GA, Lents CA. Developmental programming of the ovarian reserve in livestock. Anim Reprod Sci 2024;264.
  • Aiken CE, Tarry-Adkins JL, Penfold NC, Dearden L, Ozanne SE. Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet. FASEB J Off Publ Fed Am Soc Exp Biol 2016;30:1548–1556.
  • Laporta J, Dado-Senn B, Skibiel AL. Late gestation hyperthermia:epigenetic programming of daughter's mammary development and function. Domest Anim Endocrinol. 2022;78,106681.
  • Dahl GE, Skibiel AL, Laporta J. In Utero Heat Stress Programs Reduced Performance and Health in Calves. Vet Clin North Am Food Anim Pract. 2019;35(2):343-353.
  • Geiger AJ, Parsons CLM, Akers RM. Feeding a higher plane of nutrition and providing exogenous estrogen increases mammary gland development in Holstein heifer calves. J Dairy Sci 2016;99:7642–53.
  • Polsky L, Keyserlingk MA. Invited review: Effects of heat stress on dairy cattle welfare. J. Dairy Sci. 2017;100:8645–8657.
  • Vural R. Sıcak Stresinin Reprodüksiyon Üzerine Etkisi. Sürü Sağlığı ve Yönetimi E- Kongresi; 88-97; 2021.
  • Herbut P, Angrecka S, Walczak J. Environmental parameters to assessing of heat stress in dairy cattle—a review. Int J Biometeorol 2018;62:2089–2097.
  • Dado-Senn B, Laporta J, Dahl GE. Carry over effects of late-gestational heat stress on dairy cattle progeny. Theriogenology 2020;154:17-23.
  • Nickles KR, Relling AE, Garcia-Guerra A, Fluharty FL, Kieffer J, Parker AJ. Beef cows housed in mud during late gestation have greater net energy requirements compared with cows housed on wood chip bedding. Transl. Anim. Sci 2022;6(2).
  • Monteiro APA, Guo JR, Weng XS, Ahmed BM, Hayen MJ, Dahl GE, Bernard JK, Tao S. Effect of maternal heat stress during the dry period on growth and metabolism of calves. J. Dairy Sci. 2016;99(5): 3896-3907.
  • Dahl GE, Tao S, Laporta J. Heat Stress Impacts Immune Status in Cows Across the Life Cycle. Front. Vet. Sci 2020;7:116.
  • Tao S, Monteiro APA, Thompson IM, Hayen MJ, Dahl GE. Effect of late-gestation maternal heat stress on growth and immune function of dairy calves. J. Dairy Sci 2012;95 :7128–7136.
  • Ahmed BMS., Younas U, Asar TO, Monteiro APA, Hayen J, Tao S. Maternal heat stress reduces body and organ growth in calves: relationship to immune tissue development. J Anim Sci 2016;94:617.
  • Ghaffari MH. Developmental programming: prenatal and postnatal consequences of hyperthermia in dairy cows and calves. Domest Anim Endocrinol. 2020;80.
  • Lemley CO, Littlejohn BP, Burnett DD. Fetal Programming. In: Hopper RM, editor. Bovine Reproduction, Second Edition. John Wiley & Sons; 2021. p. 339-346.
Toplam 54 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Veteriner Doğum ve Jinekoloji
Bölüm ÇAĞRILI MAKALE / DERLEME
Yazarlar

Nazlı Senem Cam 0009-0006-7345-4574

Mehmet Rıfat Vural 0000-0001-7252-7977

Erken Görünüm Tarihi 13 Ocak 2025
Yayımlanma Tarihi 15 Ocak 2025
Gönderilme Tarihi 20 Şubat 2024
Kabul Tarihi 1 Ağustos 2024
Yayımlandığı Sayı Yıl 2025 Cilt: 96 Sayı: 1

Kaynak Göster

Vancouver Cam NS, Vural MR. Gebe ineklerde fetal programlama ve epigenetik değişimler: Beslenme ve ısı stresinin etkisi. Vet Hekim Der Derg. 2025;96(1):76-87.

Veteriner Hekimler Derneği Dergisi açık erişimli bir dergi olup, derginin yayın modeli Budapeşte Erişim Girişimi (BOAI) bildirisine dayanmaktadır. Yayınlanan tüm içerik, çevrimiçi ve ücretsiz olarak sunulan Creative Commons CC BY-NC 4.0 lisansı altında lisanslanmıştır. Yazarlar, Veteriner Hekimler Derneği Dergisi'nde yayınlanan eserlerinin telif haklarını saklı tutarlar.


Veteriner Hekimler Derneği / Turkish Veterinary Medical Society