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RESEARCH ARTICLE

The degree of maternal nutrient restriction during late gestation influences the growth and endocrine profiles of offspring from beef cows

S. López Valiente https://orcid.org/0000-0002-7743-2798 A * , A. M. Rodriguez https://orcid.org/0000-0001-6445-8780 A , N. M. Long https://orcid.org/0000-0002-0220-7318 B , I. M. Lacau-Mengido https://orcid.org/0000-0003-2547-3819 C and S. Maresca https://orcid.org/0000-0003-2891-9492 A
+ Author Affiliations
- Author Affiliations

A Instituto Nacional de Tecnología Agropecuaria, Cuenca del Salado Experimental Station, Rauch, BA, 7203, Argentina.

B Department of Animal and Veterinary Sciences, Clemson University, Clemson, SC 29634, USA.

C Laboratorio de Regulación Hipofisaria, Instituto de Biología y Medicina Experimental (CONICET), 1428 Buenos Aires, Argentina.

* Correspondence to: lopez.valiente@inta.gob.ar

Handling Editor: David Pacheco

Animal Production Science 62(2) 163-172 https://doi.org/10.1071/AN20527
Submitted: 2 October 2020  Accepted: 21 September 2021   Published: 28 October 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Cow–calf operations in Argentina are managed under extensive grazing condition and the quality of forages is often poor during the second half of gestation. The severity of nutrient restriction in bovine gestation, caused by seasonal pasture production, often results in poor production traits in progeny.

Aims: The objective of the current study was to determine whether different levels of maternal nutrient intake in beef cows during late gestation affect fetal and postnatal growth, glucose metabolism, and insulin-like growth factor 1 (IGF1) concentrations in offspring of beef cattle.

Methods: At 180 ± 4 days of gestation, multiparous Angus cows (n = 56) were blocked by bodyweight (BW) and expected calving date, and assigned to pens (2 or 3 cows/pen). Pens (n = 8 per treatment) were then randomly assigned to the following treatments: severely restricted (SR; 50% of net energy and 58% of CP requirements), moderately restricted (MR; 75% of net energy and 85% of CP requirements), or control (CON; 100% of net energy and 116% of CP requirements). Pen was the experimental unit and data were analysed by ANOVA or repeated measures analysis, as appropriate. After calving, all cows were managed in a single group until weaning.

Key results: Cow BW and body condition score decreased as nutritional restriction increased (P < 0.05). At parturition, birth weight of calves from SR dams and MR dams was lower than that of calves from CON dams (P = 0.05; 4.9 kg and 2.1 kg respectively). Average daily gain of calves from birth to 24 days of age was higher (P = 0.01) in calves from SR dams than in calves from CON and MR dams. Calves from MR dams were lighter (P = 0.04) than were calves from SR and CON dams at weaning. Treatments did not affect milk production or composition (P > 0.10) or glucose–insulin metabolism of offspring during lactation (P > 0.10). Concentration of IGF1 tended to be lower in MR progeny than in SR and CON progeny during lactation (P = 0.09).

Conclusions: Late gestation maternal nutrient restriction, irrespective of the severity of the restriction, decreased birth weight of offspring; however, severe nutrient restriction induced early postnatal compensatory growth.

Implications: The severe nutritional restriction produced calves with weaning weights indistinguishable from the control cows due to early postnatal compensatory growth. However, the longer-term effects of nutritional restriction of the dam in the second half of pregnancy on metabolic and reproductive performance in replacement heifers or meat production/quality in steers is yet to be determined.

Keywords: beef cattle, calves growth, endocrine perfiles, fetal programming, late gestation, milk production, nutrient restriction, offspring performance.


References

Albertsson-Wikland K, Boquszewski M, Karlberg J (1998) Children born small-for-gestational age: postnatal growth and hormonal status. Hormone Research in Paediatrics 49, 7–13.
Children born small-for-gestational age: postnatal growth and hormonal status.Crossref | GoogleScholarGoogle Scholar |

Barker DJP (1998) In utero programming of chronic disease. Clinical Science 95, 115–128.
In utero programming of chronic disease.Crossref | GoogleScholarGoogle Scholar |

Bauer MK, Breier BH, Harding JE, Veldhuis JD, Gluckman PD (1995) The fetal somatotropic axis during long term maternal undernutrition in sheep: evidence for nutritional regulation in utero. Endocrinology 136, 1250–1257.
The fetal somatotropic axis during long term maternal undernutrition in sheep: evidence for nutritional regulation in utero.Crossref | GoogleScholarGoogle Scholar | 7867579PubMed |

Bell AW, Burhans WS, Overton TR (2000) Protein nutrition in late pregnancy, maternal protein reserves and lactation performance in dairy cows. Proceedings of the Nutrition Society 59, 119–126.
Protein nutrition in late pregnancy, maternal protein reserves and lactation performance in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Brameld JM, Mostyn A, Dandrea J, Stephenson TJ, Dawson JM, Buttery PJ, Symonds ME (2000) Maternal nutrition alters the expression of insulin-like growth factors in fetal sheep liver and skeletal muscle. Journal of Endocrinology 167, 429–437.
Maternal nutrition alters the expression of insulin-like growth factors in fetal sheep liver and skeletal muscle.Crossref | GoogleScholarGoogle Scholar |

Corah LR, Dunn TG, Kaltenbach CC (1975) Influence of prepartum nutrition on the reproductive performance of beef females and the performance of their progeny. Journal of Animal Science 41, 819–824.
Influence of prepartum nutrition on the reproductive performance of beef females and the performance of their progeny.Crossref | GoogleScholarGoogle Scholar | 1158813PubMed |

De Blasio MJ, Gatford KL, McMillen IC, Robinson JS, Owens JA (2007) Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb. Endocrinology 148, 1350–1358.
Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb.Crossref | GoogleScholarGoogle Scholar | 17110432PubMed |

Desai M, Hales CN (1997) Role of fetal and infant growth in programming metabolism in later life. Biological Reviews of the Cambridge Philosophical Society 72, 329–348.
Role of fetal and infant growth in programming metabolism in later life.Crossref | GoogleScholarGoogle Scholar | 9155245PubMed |

Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, Means WJ, Han H, Nathanielsz PW (2007) Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. Journal of Animal Science 85, 1285–1294.
Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring.Crossref | GoogleScholarGoogle Scholar | 17224460PubMed |

Freetly HC, Ferrell CL, Jenkins TG (2000) Timing of realimentation of mature cows that were feed-restricted during pregnancy influences calf birth weights and growth rates. Journal of Animal Science 78, 2790–2796.
Timing of realimentation of mature cows that were feed-restricted during pregnancy influences calf birth weights and growth rates.Crossref | GoogleScholarGoogle Scholar | 11063300PubMed |

Funston RN, Martin JL, Adams DC, Larson DM (2010) Winter grazing system and supplementation of beef cows during late gestation influence heifer progeny. Journal of Animal Science 88, 4094–4101.
Winter grazing system and supplementation of beef cows during late gestation influence heifer progeny.Crossref | GoogleScholarGoogle Scholar | 20709872PubMed |

Gardner DS, Tingey K, Van Bon BWM, Ozanne SE, Wilson V, Dandrea J, Keisler DH, Stephenson T, Symonds ME (2005) Programming of glucose–insulin metabolism in adult sheep after maternal undernutrition. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 289, R947–R954.
Programming of glucose–insulin metabolism in adult sheep after maternal undernutrition.Crossref | GoogleScholarGoogle Scholar | 15961536PubMed |

Gunn PJ, Schoonmaker JP, Lemenager RP, Bridges GA (2014) Feeding excess crude protein to gestating and lactating beef heifers: impact on parturition, milk composition, ovarian function, reproductive efficiency and pre-weaning progeny growth. Livestock Science 167, 435–448.
Feeding excess crude protein to gestating and lactating beef heifers: impact on parturition, milk composition, ovarian function, reproductive efficiency and pre-weaning progeny growth.Crossref | GoogleScholarGoogle Scholar |

Hales CN, Desai M, Ozanne SE, Crowther NJ (1996) Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochemical Society Transactions 24, 341–350.
Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis.Crossref | GoogleScholarGoogle Scholar | 8736760PubMed |

Harding JE, Johnston BM (1995) Nutrition and fetal growth. Reproduction, Fertility and Development 7, 539–547.
Nutrition and fetal growth.Crossref | GoogleScholarGoogle Scholar |

Houghton PL, Lemenager RP, Horstman LA, Hendrift KS, Moss GE (1990) Effects of body condition, pre- and postpartum energy level and early weaning on reproductive performance of beef cows and preweaning calf gain. Journal of Animal Science 68, 1438–1446.
Effects of body condition, pre- and postpartum energy level and early weaning on reproductive performance of beef cows and preweaning calf gain.Crossref | GoogleScholarGoogle Scholar | 2365654PubMed |

Iñiguez G, Ong K, Bazaes R, Avila A, Salazar T, Dunger D, Mericq V (2006) Longitudinal changes in insulin-like growth factor-I, insulin sensitivity, and secretion from birth to age three years in small-for-gestational-age children. The Journal of Clinical Endocrinology & Metabolism 91, 4645–4649.
Longitudinal changes in insulin-like growth factor-I, insulin sensitivity, and secretion from birth to age three years in small-for-gestational-age children.Crossref | GoogleScholarGoogle Scholar |

Karlberg J, Albertsson-Wikland K (1995) Growth in full-term small-for-gestational-age infants: from birth to final height. Pediatric Research 38, 733–739.
Growth in full-term small-for-gestational-age infants: from birth to final height.Crossref | GoogleScholarGoogle Scholar | 8552442PubMed |

Lacau-Mengido IM, Mejía ME, Díaz-Torga GS, Gonzalez Iglesias A, Formía N, Libertun C, Becú-Villalobos D (2000) Endocrine studies in ivermectin-treated heifers from birth to puberty. Journal of Animal Science 78, 817–824.
Endocrine studies in ivermectin-treated heifers from birth to puberty.Crossref | GoogleScholarGoogle Scholar | 10784170PubMed |

Lake SL, Scholljegerdes EJ, Atkinson RL, Nayigihugu V, Paisley SI, Rule DC, Moss GE, Robinson TJ, Hess BW (2005) Body condition score at parturition and postpartum supplemental fat effects on cows and calf performance. Journal of Animal Science 83, 2908–2917.
Body condition score at parturition and postpartum supplemental fat effects on cows and calf performance.Crossref | GoogleScholarGoogle Scholar | 16282631PubMed |

Lalman DL, Williams JE, Hess BW, Thomas MG, Keisler DH (2000) Effect of dietary energy on milk production and metabolic hormones in thin, primiparous beef heifers. Journal of Animal Science 78, 530–538.
Effect of dietary energy on milk production and metabolic hormones in thin, primiparous beef heifers.Crossref | GoogleScholarGoogle Scholar | 10764058PubMed |

Larson DM, Martin JL, Adams DC, Funston RN (2009) Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny. Journal of Animal Science 87, 1147–1155.
Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny.Crossref | GoogleScholarGoogle Scholar | 18997078PubMed |

LeMaster CT, Taylor RK, Ricks RE, Long NM (2017) The effects of late gestation maternal nutrient restriction with or without protein supplementation on endocrine regulation of newborn and postnatal beef calves. Theriogenology 87, 64–71.
The effects of late gestation maternal nutrient restriction with or without protein supplementation on endocrine regulation of newborn and postnatal beef calves.Crossref | GoogleScholarGoogle Scholar | 27613252PubMed |

Long NM, Nijland MJ, Nathanielsz PW, Ford SP (2010) The effect of early to mid-gestational nutrient restriction on female offspring fertility and hypothalamic–pituitary–adrenal axis response to stress. Journal of Animal Science 88, 2029–2037.
The effect of early to mid-gestational nutrient restriction on female offspring fertility and hypothalamic–pituitary–adrenal axis response to stress.Crossref | GoogleScholarGoogle Scholar | 20190172PubMed |

Long NM, Vonnahme KA, Hess BW, Nathanielsz PW, Ford SP (2009) Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine. Journal of Animal Science 87, 1950–1959.
Effects of early gestational undernutrition on fetal growth, organ development, and placentomal composition in the bovine.Crossref | GoogleScholarGoogle Scholar | 19213703PubMed |

López Valiente S, Maresca S, Rodríguez A (2014) Efecto de la suplementación proteica durante el último tercio de gestación sobre desarrollo de la progenie. Revista Argentina de Producción Animal 34, 345–463.

López Valiente S, Maresca S, Rodríguez AM, Long NM, Quintans G, Palladino RA (2019) Effect of protein restriction during mid-to late gestation of beef cows on female offspring fertility, lactation performance and calves development. EC Veterinary Science 4, 1–12.
Effect of protein restriction during mid-to late gestation of beef cows on female offspring fertility, lactation performance and calves development.Crossref | GoogleScholarGoogle Scholar |

López Valiente S, Maresca S, Rodríguez AM, Palladino RA, Lacau-Mengido IM, Long NM, Quintans G (2018) Effect of protein restriction of Angus cows during late gestation: subsequent reproductive performance and milk yield. The Professional Animal Scientist 34, 261–268.
Effect of protein restriction of Angus cows during late gestation: subsequent reproductive performance and milk yield.Crossref | GoogleScholarGoogle Scholar |

Maresca S, López Valiente S, Rodríguez AM, Long NM, 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.
Effect of protein restriction of bovine dams during late gestation on offspring postnatal growth, glucose–insulin metabolism and IGF-1 concentration.Crossref | GoogleScholarGoogle Scholar |

Maresca S, Valiente SL, Rodríguez AM, Pavan E, Quintans G, Long NM (2019) Late-gestation protein restriction negatively impacts muscle growth and glucose regulation in steer progeny. Domestic Animal Endocrinology 69, 13–18.
Late-gestation protein restriction negatively impacts muscle growth and glucose regulation in steer progeny.Crossref | GoogleScholarGoogle Scholar | 31103887PubMed |

Marston TT, Lusby KS, Wettemann RP, Purvis HT (1995) Effects of feeding energy or protein supplements before or after calving on performance of spring calving cows grazing native range. Journal of Animal Science 73, 657–664.
Effects of feeding energy or protein supplements before or after calving on performance of spring calving cows grazing native range.Crossref | GoogleScholarGoogle Scholar | 7607998PubMed |

Mericq V, Ong KK, Bazaes RA, Pena V, Avila A, Salazar T, Soto N, Iñiguez G, Dunger DB (2005) Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children. Diabetologia 48, 2609–2614.
Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children.Crossref | GoogleScholarGoogle Scholar | 16283238PubMed |

National Research Council (2000) ‘Nutrient requirements of beef cattle: seventh revised edition: update 2000.’ (The National Academies Press: Washington, DC, USA)
| Crossref |

Quintans G, Banchero G, Carriquiry M, López-Mazz C, Baldi F (2010) Effects of body condition and sucking restriction with and without presence of the calf cow and calf performance. Animal Production Science 50, 931–938.
Effects of body condition and sucking restriction with and without presence of the calf cow and calf performance.Crossref | GoogleScholarGoogle Scholar |

Radunz AE, Fluharty FL, Day ML, Zerby HN, Loerch SC (2010) Prepartum dietary energy source fed to beef cows: I. Effects on pre- and postpartum cow performance. Journal of Animal Science 88, 2717–2728.
Prepartum dietary energy source fed to beef cows: I. Effects on pre- and postpartum cow performance.Crossref | GoogleScholarGoogle Scholar | 20453084PubMed |

Richards MW, Wettemann RP, Schoenemann HM (1989) Nutritional anestrus in beef cows: body weight change, body condition, luteinizing hormone in serum and ovarian activity. Journal of Animal Science 67, 1520–1526.
Nutritional anestrus in beef cows: body weight change, body condition, luteinizing hormone in serum and ovarian activity.Crossref | GoogleScholarGoogle Scholar | 2768109PubMed |

Robinson DL, Cafe LM, Greenwood PL (2013) Meat science and muscle biology symposium: developmental programming in cattle: consequences for growth, efficiency, carcass, muscle, and beef quality characteristics. Journal of Animal Science 91, 1428–1442.
Meat science and muscle biology symposium: developmental programming in cattle: consequences for growth, efficiency, carcass, muscle, and beef quality characteristics.Crossref | GoogleScholarGoogle Scholar | 23230118PubMed |

Rustogi D, Yadav S, Ramji S, Mishra TK (2018) Growth patterns in small for gestational age babies and correlation with Insulin-like Growth Factor-1 levels. Indian Pediatrics 55, 975–978.
Growth patterns in small for gestational age babies and correlation with Insulin-like Growth Factor-1 levels.Crossref | GoogleScholarGoogle Scholar | 30587647PubMed |

Sharma RK, Blair HT, Jenkinson CMC, Kenyon PR, Cockrem JF, Parkinson TJ (2012) Uterine environment as a regulator of birth weight and body dimensions of newborn lambs. Journal of Animal Science 90, 1338–1348.
Uterine environment as a regulator of birth weight and body dimensions of newborn lambs.Crossref | GoogleScholarGoogle Scholar | 22079991PubMed |

Soto N, Bazaes RA, Pena V, Salazar T, Avila A, Iniguez G, Ong KK, Dunger DB, Mericq MV (2003) Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. The Journal of Clinical Endocrinology & Metabolism 88, 3645–3650.
Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort.Crossref | GoogleScholarGoogle Scholar |

Spitzer JC, Morrison DG, Wettemann RP, Faulkner LC (1995) Reproductive responses and calf birth and weaning weights as affected by body condition at parturition and postpartum weight gain in primiparous beef cows. Journal of Animal Science 73, 1251–1257.
Reproductive responses and calf birth and weaning weights as affected by body condition at parturition and postpartum weight gain in primiparous beef cows.Crossref | GoogleScholarGoogle Scholar | 7665355PubMed |

Stalker LA, Adams DC, Klopfenstein TJ, Feuz DM, Funston RN (2006) Effects of pre- and postpartum nutrition on reproduction in spring calving cows and calf feedlot performance. Journal of Animal Science 84, 2582–2589.
Effects of pre- and postpartum nutrition on reproduction in spring calving cows and calf feedlot performance.Crossref | GoogleScholarGoogle Scholar | 16908664PubMed |

Tipton JE, Ricks RE, LeMaster CT, Long NM (2018) The effects of late gestation nutrient restriction of dams on beef heifer intake, metabolites and hormones during an ad libitum feeding trial. Journal of Animal Physiology and Animal Nutrition 102, e877–e884.
The effects of late gestation nutrient restriction of dams on beef heifer intake, metabolites and hormones during an ad libitum feeding trial.Crossref | GoogleScholarGoogle Scholar | 29352494PubMed |

Tudor GD, Uttiny DW, O’Rourke PK (1980) The effect of pre- and post-natal nutrition on the growth of beef cattle. III. The effect of severe restriction in early post-natal life on the development of the body components and chemical composition. Australian Journal of Agricultural Research 31, 191–204.
The effect of pre- and post-natal nutrition on the growth of beef cattle. III. The effect of severe restriction in early post-natal life on the development of the body components and chemical composition.Crossref | GoogleScholarGoogle Scholar |

Underwood KR, Tong JF, Price PL, Roberts AJ, Grings EE, Hess BW, Means WJ, Du M (2010) Nutrition during mid to late gestation affects growth, adipose tissue deposition, and tenderness in cross-bred beef steers. Meat Science 86, 588–593.
Nutrition during mid to late gestation affects growth, adipose tissue deposition, and tenderness in cross-bred beef steers.Crossref | GoogleScholarGoogle Scholar | 20659786PubMed |

Wagner JJ, Lusby KS, Oltjen JW, Rakestraw J, Wettemann RP, Walters LE (1988) Carcass composition in mature Hereford cows: estimation and effect on daily metabolizable energy requirement during winter. Journal of Animal Science 66, 603–612.
Carcass composition in mature Hereford cows: estimation and effect on daily metabolizable energy requirement during winter.Crossref | GoogleScholarGoogle Scholar | 3378920PubMed |

Warrington BG, Byers FM, Schelling GT, Forrest DW, Baker JF, Greene LW (1988) Gestation nutrition, tissue exchange and maintenance requirements of heifers. Journal of Animal Science 66, 774–782.
Gestation nutrition, tissue exchange and maintenance requirements of heifers.Crossref | GoogleScholarGoogle Scholar | 3378933PubMed |

Wilson TB, Faulkner DB, Shike DW (2016) Influence of prepartum dietary energy on beef cow performance and calf growth and carcass characteristics. Livestock Science 184, 21–27.
Influence of prepartum dietary energy on beef cow performance and calf growth and carcass characteristics.Crossref | GoogleScholarGoogle Scholar |

Wittrock JAM, Duffield TF, LeBlanc SJ (2013) Short communication: Validation of a point-of-care glucometer for use in dairy cows. Journal of Dairy Science 96, 4514–4518.
Short communication: Validation of a point-of-care glucometer for use in dairy cows.Crossref | GoogleScholarGoogle Scholar |