Fetal programming and the consequences on progeny development - a review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i12.20766

Keywords:

Animal behavior; Fetal growth; Performance.

Abstract

The objective of this work was, through a literature review, to identify the main physiological and behavioral changes caused by fetal programming that affect the health and performance of the progeny in the postnatal life. Among the numerous factors that alter fetal formation, maternal nutrition during pregnancy has been strongly referenced in recent research. Maternal nutrition during pregnancy can alter fetal formation in numerous ways, so that the fetus adapts as quickly as possible to the uterine environment, and these changes are noticeable during the adult life of the progeny. In general, the literature suggests that maternal restriction during pregnancy can promote physiological and functional changes in fetal organs and tissues, preparing the organism to survive in challenging environments also in postnatal life. In addition, individuals who experienced restricted environments during fetal formation have a greater search for food and altered psychosocial behaviors, such as fear reactions, isolation and reactivity. Higher production efficiency and consequently lower age at slaughter of the progeny has been associated with better maternal nutrition during pregnancy, since these individuals have adequate fetal formation and, therefore, greater metabolic capacity of nutrients in intensive production systems that aim for maximum performance animal.

References

Barouei, J., Moussavi, M., & Hodgson, D. M. (2012). Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome, Plos One, 7(10), e46051.

Bauman, D. E., & Currie, B. (1980). Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis e homeorhesis. Journal of Dairy Science, 63(9), 1514-1529.

Blecha, F., Bull, R. C., Olson, D. P., Ross, R. H., & Curtis, S. (1981). Effects of prepartum protein restriction in the beef cow on immunoglobin content in blood and colostral whey and subsequente immunoglobin absorption by the neonatal calf. Journal of Animal Science, 53(1), 1174-1180.

Bohnert, D. W., Stalker, L. A., Mills, R. R., Nyman, A., Falck, S. J., & Cooke, R. F. (2013). Late gestation suplementation of beff cows differing in body condition score: Effects on cow and calf performance. Journal of Animal Science, 91(11), 5485-5491.

Bowman, C. E., Alpergin, E. S. S., Cavagnini, K., Smith, D. M., Scafidi, S., & Wolfgang, M. J. (2019). Maternal lipid metabolism directs fetal liver programming following nutrient stress. Cell Reports, 29(5), 1299-1310.

Broadhead, D., Mulliniks, J. T., & Funston, R. N. (2019). Development programming in a beef production system. Veterinary Clinics Food Animal, 35(1), 379-390.

Carlin, J., George, R., Reyes, & T. M. (2013) Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. Plos One, 8(5), e63549, 2013.

Castro-Rodríguez, D. C., Rodríguez-González, G. L., Menjivar, M., & Zambrano, H. (2020). Maternal interventions to prevent adverse fetal programming outcomes due to maternal malnutrition: Evidence in animal models. Placenta, 102(1), 49-54.

Cruz, W. F. G., Schoonmaker, J. P., Resende, F. D., Siqueira, G. R., Rodrigues, L. M., Zamudio, G. D. R., & Ladeira, M. M. (2019). Effects of maternal protein supplementation and inclusion of rumen-protected fat in the finishing diet on nutrient digestibility and expression. of intestinal genes in Nellore steers. Animal Science Journal, 90(1), 1200–1211.

Dearden, L., Buller, S., Furigo, I. C., Fernandez-Twinn, D. S., & Ozanne, S. E. (2020). Maternal obesity causes fetal hypothalamic insulin resistance and disrupts development of hypothalamic feeding pathways. Molecular Metabolism, 42(1), 101079.

DeCapo, M., Thompson, J. R., Dunn, G., & Sullivan, E. L. (2019). Perinatal nutrition and programmed risk for neuropsychiatric desorders: A focus on animal models. Biological Psychiatry, 85(2), 122-134.

Donovan, E. L. Hernandez, C. E., Matthews, L. R., Oliver, M. H., Jaquiery, A. L., Bloomfield, F. H., & Harding, J. E. (2013). Periconceptional undernutrition in sheep leads to decreased locomotor activity in a natural environment. Journal of Developmental. Origins of Health and Disease, 4(1), 296–299.

Du, M., Huang, Y., Das, A. K., Yang, Q., Duarte, M. S., Modson, M. V., & Zhu, M. J. (2013). Manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. Journal Animal Science, 91(3), 1419-1427.

Duarte, M. S., Gionbelli, M. P., Paulino, P. V. R., Serão, N. V. L., Martins, T. S., Tótaro, P. I. S., Neves, C. A., Valadares Filho, S. C., Dodson, M. V., Zhu, M., & Du, M. (2013). Effects of maternal nutrition on development of gastrointestinal tract of bovine fetus at different stages of gestation. Livestock Science, 153, 60-65.

George, L. A. Zhang, L., Tuersunjiang, N., Ma, Y., Long, N. M., Uthlaut, A. B., Smith, D. T., Nathanielsz, P. W., & Ford, S. P. (2012). Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring. American Journal of Physiology, 302(1), 795-804.

Keomanivong, F. E., Camacho, L. E., Lemley, C. O., Kuemper, E. A., Yunusova, R. D., Borowicz, P. P., Kirsch, J. D., Vonnahme, K. A., Caton, J. S., & Swanson, K. C. (2016). Effects of realimentation after nutrient restriction during mid- to late gestation on pancreatic digestive enzymes, serum insulin and glucose levels, and insulin-contating cell cluster morphology. Journal of Animal Physiology and Animal Nutrition, 101(3), 589-604.

Kleemann, D. O., Kelly, J. M., Rudiger, S. R., McMillen, I. C., Morrison, J. L., Zhang, S., MacLaughlin, S. M., Smith, D. H., Grimson, R. J., Jaensch, K. S., Brien, F. D., Plush, K. S., Hiendleder, S., & Walker S. K. (2015). Effect of periconceptional nutrition on the growth, behaviour and survival of the neonatal lamb. Animal Reproduction Science, 160(1), 12–22.

Larson, D. M., Martin, J. L., Adams, D. C., & Funston, R. N. (2009). Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny. Journal Animal Science, 87(1), 1147-1155.

LeMaster, C. T., Taylor, R. K., Ricks, R. E., & Long, N. M. (2017). The effects of late gestation maternal nutrient restriction whit or without protein supplementation on endocrine regulation of newborn and postnatal beef calves. Theriogenology, 87, 64-71.

Maresca, S., Lopes Valiente, S., Rodrigues, A. M., Long, N. M., Pavan, E., & Quintans, G. (2018). Effect of protein restriction of bovine dams during late gestation on offspring postnatal growth, glucose-insulin metabolism and IGF-1 concentration. Livestock Science, 212, 120-126.

Maresca, S., López Valiente, S., Rodriguez, A. M., Testa, L. M., Long, N. M., Quintans, G. I., Pavan, E. (2019). The influence of protein restriction during mid- to late gestation on beef offspring growth, carcass characteristic and meat quality. Meat Science, 153, 103-108.

McCarty, K. J., Washburn, J. L., Taylor, R. K., & Long, N. M. (2020). The effects of early or mid-gestation nutrient restriction on bovine fetal pancreatic development. Domestic Animal Endocrinology, 70, 1-6.

Mentch, S. J. & Locasale, J. W. (2016). One carbon metabolism and epigenetics: understanding the specificity. Annals of the New York Academy of Sciences, 1363(1), 91-98.

Micke, G. C., Sullivan, T. M., Kennaway, D. J., Hernadez-Mendrano, J., & Perry, V. E. A. (2015). Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: consequences for sexually dimorphic programming of thyroid hormones and development of their progeny. Theriogenology, 83(1), 604–615.

Miguel-Pacheco, G. G., Perry, V. E. A., Hernadez-Mendrano, J. H., Wapenaar, W., Keisler, D. H., & Voigt, J. P. (2019). Low protein intake during the preconception period in beff heifers affects offspring and maternal behaviour. Applied Animal Behaviour Science, 215(1), 1-6.

Mohrhauser, D. A., Taylor, A. R., Underwood, K. R., Pritchard, R. H., Wertz-Lutz, A. E., & Blair, D. A. (2015b). The influence of maternal energy status during midgestation on beef offspring carcass characteristics and meat quality. Journal of Animal Science, 93, 786-793.

Payolla, T. B., Lemes, S. F., Fante, T., Reginato, A., Silva, G. M., Micheletti, T. O., Rodrigues, H. G., Torsoni, A. S., Milanski, M., & Torsoni, M. A. (2016). High-fat diet during pregnancy and lactation impairs the cholinergic anti-inflammatory pathway in the liver and white adipose tissue of mouse offspring. Molecular and Cellular Endocrinology, 422(1), 192-202.

Prezotto, L. D., Camacho, L. E., Lemley, C. O., Keomanivong, F. E., Caton, J. S., Vonnahme, K. A., & Swanson, K. C. (2016). Nutrient restrition and realimentation in beef cows during early and mid-gestation and maternal and fetal hepatic and small intestinal in vitro oxygen consumption. Animal, 10(5), 829-837.

Ramírez, M., Testa, L. M., López Valiente, S., Latorre, M. E., Long, N. M., Rodriguez, A. M., Pavan, E., & Maresca, S. (2020). Maternal energy status during late gestation: Effects on growth performance, carcass characteristics and meat quality of steers progeny. Meat Science, 164, 1-7.

Radunz, A. E., Fluharty, F. L., Relling, A. E., Fleix, T. L., Shoup, L. M., Zerby, H. N., & Loerch, S. C. (2012). Prepartum dietary energy source fed to beef cows: II. Effects on progeny postnatal growth, glucose tolerance, and carcass composition. Journal of Animal Science, 90(13), 4962-4974.

Relling, A. E., Velazquez, M. R., & Batistel, F. (2019). Maternal supply of polyunsaturated fatty acids and methionine during late-gestation alters amino acid transportes and global DNA methylation in the lamb small intestine. Journal of Animal Science, 97(1), e323.

Reynolds, L. P., & Caton, J. S. (2012). Role of the pre- and post-natal environment in developmental programming of health and productivity. Molecular and Cellular Endocrinology, 354(1), 54-59.

Reynolds, L. P., Borowicz, P. P., Caton, J. S., Crouse, M. S., Dahlen C. R., & Ward, A. K. (2019). Developmental Programming of Fetal Growth and Development. Veterinary Clinics Food Animal, 35(2), 229-247.

Silva, G. M. Chalk, C. D., Ranches, J., Schulmeister, T. M., Henry, D. D., DiLorenzo, N., Arthington, J. D., Moriel, P., & Lancaster, P. A. (2021). Effect of rumen-protected methionine supplementation to beef cows during the periconception period on performance of cows, calves and subsequent offspring. Animal, 15(1), 100055.

Sinclair, K. D., Rutherford, K. M. D., Wallace, J. M., Brameld, J. M., Stöger, R., Alberio, R., Sweetman, D., Gardner, D. S., Perry, V. E. A., Adam, C. L., Ashworth, C. J., Robinson, J. E., & Dwyer, C. M. (2016). Epigenetics and developmental programming of welfare and production traits in farm animals. Reproduction and Fertilidad, 28(1), 1443–1478.

Stalker, L. A., Adams, D. C., Klopfenstein, T. J., Feuz, D. M., & Funston, R. N. (2006). Effects of pre- and postpartum nutrition on reproduction in spring calving cows and calf feedlot performance. Journal of Animal Science, 84(1), 2582–2589.

Symonds, M. E., Sebert, S. P., & Budge, H. (2010). Nutritional regulation of fetal growth and implications for productive life in ruminants. Animal, 4(7), 1075-1083.

Taylor, R. K., LeMaster, C. T., Mangrun, K. S., Ricks, R. E., & Long, N. M. (2018). Effects of maternal nutrient restriction during early or mid-gestation without realimentation on maternal physiology and foetal growth and development in beef cattle. Animal, 12(1), 312-321.

Tong, J. F., Yan, X., Zhu, M. J., Ford, S. P., Nathanielsz, P. W., & Du, M. (2009). Maternal obesity downregulates myogenesis and β-catenin signaling in fetal skeletal muscle. American Journal of Physiology-Endocrinology and Metabolism, 296(1), e917–e924.

Vaag, A. A., Grunnet, L. G., Arora, G. P., & Brons, C. (2012). The thrifty phenotype hypothesis revisited. Diabetologia, 55, 2085-2088.

Zago, D., Canozzi, M. E. A., & Barcellos, J. O. J. (2020). Pregnant beef cow’s nutrition and its effects on postnatal weigth and carcass quality of their progeny. Plos One, 15(8), e0237941.

Zhu, M. J., Ford, S. P., Means, W. J., Hess, B. W., Nathaniels, P. W., & Du, M. (2006). Maternal nutrient restriction affects properties of skeletal muscle in offspring. The Journal of Physiology, 575(1), 241-250.

Wang, P., Mariman, E., Renes, J., & Keijer, J. (2008). The secretory function of adipocytes in the physiology of white adipose tissue. Journal of Cell Physiology, 216(1), 3–13.

Washburn, J. L., Taylor, R. K., & Long, N. M. (2016). The effects of early or mid-gestation nutrient restriction on bovine fetal pancreatic development. Journal of Animal Science, 94(10), 67.

Wilson, T. B., Schroeder, A. R., Ireland, F. A., Faulkner, D. B., & Shike, D. W. (2015). Effects of late gestation distillers grains supplementation on fall-calving beef cow performance and steer calf growth and carcass characteristics. Journal of Animal Science, 93(1), 4843-4851.

Wilson, T. B., Long, N. M., Faulkner, D. B., & Shike, D. W. (2016). Influence of excessive dietary protein intake during late gestation on drylot beef cow performance and progeny growth, carcass characteristics, and plasma glucose and insulin concentrations. Journal of Animal Science, 94(1), 2035–2046.

Published

01/10/2021

How to Cite

KLEIN, J. L.; ADAMS, S. M.; ALVES FILHO, D. C.; BRONDANI, I. L.; PIZUTTI, L. Ângelo D.; ANTUNES, D. P.; POLETTO, V.; KARSTEN, M. dos S.; BEM, P. H. T. de .; MELLO, D. A. da S. . Fetal programming and the consequences on progeny development - a review. Research, Society and Development, [S. l.], v. 10, n. 12, p. e557101220766, 2021. DOI: 10.33448/rsd-v10i12.20766. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/20766. Acesso em: 23 dec. 2024.

Issue

Section

Review Article