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Theriogenology2024; 230; 107-114; doi: 10.1016/j.theriogenology.2024.09.003

The influence of lactation on insulin and glucose metabolism, lipid profile, and cytokines in pregnant mares.

Abstract: Glucose metabolism adapts to gestation, resulting in progressive physiological insulin resistance and increased insulin secretion to maintain maternal euglycemia and glucose availability for the developing fetus. These changes can impact mare fertility and maternal and neonatal health. This is the first comparison of body condition, regional adiposity, insulin and glucose dynamics, lipid metabolism, and cytokine production between lactating and non-lactating mares before, during pregnancy, and early postpartum. Twelve pregnancies from 9 broodmares, five nonlactating (NL) and seven lactating (L), were used. Evaluations were performed on the day of ovulation, at 55, 110, 165, 220, 275, and 330 days of gestation (D55, D110, D165, D220, D275, D330) and 21 days postpartum (21pp). Mares in the L group had lower basal insulin and glucose at the beginning of pregnancy, smaller area under the curve of insulin and glucose, and greater insulin sensitivity and glucose tolerance. Resistin was higher in D110 and D165 than in D0, D275, 330 and 21pp, while leptin was higher in D55, and in D110, at D110 it was equal to D0, D220, and D275, but higher than at D330 and D21pp. As for the groups, L presented lower body condition score (BCS), crest neck score (CNS), rump fat thickness (RUM), basal insulin, glucose area under the curve (AUCg), MIRG and higher RISQI, adiponectin and tumor necrosis factor (TNFα). There was no effect over time in non-esterified fatty acids (NEFA) concentrations between the L mares; in the NL, D275 presented higher concentrations than those of D0, D55, and D110, which in turn were equal to the other time points; there were higher concentrations in NL mares than L in samples D165 and D275. In conclusion, a different metabolic profile during pregnancy was detected, and NL mares were closer to the metabolic threshold for the occurrence of metabolic syndrome during pregnancy. Understanding the impacts of these differences on mare's health and their offspring's future is fundamental as most of our recipient mares for embryo transfer are non-lactating. Therefore, we suggest that further studies be performed to evaluate lactation's influence on mares' metabolic parameters.
Publication Date: 2024-09-10 PubMed ID: 39293172DOI: 10.1016/j.theriogenology.2024.09.003Google Scholar: Lookup
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  • Journal Article

Summary

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Overview

  • This study investigated how lactation affects insulin and glucose metabolism, lipid profiles, and cytokine levels throughout pregnancy and early postpartum in mares.
  • It compared metabolic and physiological differences between lactating and non-lactating pregnant mares at multiple stages of gestation and after birth.

Background and Purpose

  • During pregnancy, glucose metabolism changes to support fetal development, leading to increased insulin resistance and insulin secretion to maintain stable blood glucose.
  • These metabolic adjustments can influence mare fertility, maternal health, and neonatal outcomes.
  • Prior to this study, the effects of lactation on metabolic parameters during pregnancy in mares had not been compared directly to non-lactating mares.
  • The purpose was to analyze differences in body condition, fat distribution, insulin and glucose dynamics, lipid metabolism, and cytokine production between lactating vs. non-lactating mares across pregnancy and postpartum periods.

Study Design and Methods

  • Twelve pregnancies were studied involving nine broodmares divided into two groups: five non-lactating (NL) and seven lactating (L) mares.
  • Measurements were taken at the day of ovulation (baseline), at several gestational time points (55, 110, 165, 220, 275, 330 days), and 21 days after foaling.
  • Key parameters evaluated included:
    • Body condition score (BCS), crest neck score (CNS), and rump fat thickness (RUM) to assess adiposity.
    • Basal and stimulated insulin and glucose; area under the curve measurements for glucose (AUCg) and insulin.
    • Insulin sensitivity and glucose tolerance indices such as RISQI (insulin sensitivity) and MIRG (insulin secretion).
    • Cytokines like resistin, leptin, adiponectin, and tumor necrosis factor alpha (TNFα).
    • Lipid metabolism assessed via non-esterified fatty acids (NEFA).

Key Findings

  • Lactating mares (L) exhibited:
    • Lower basal insulin and glucose levels early in pregnancy compared to non-lactating mares (NL).
    • Smaller insulin and glucose responses over time, indicating better insulin sensitivity and glucose tolerance.
    • Lower body fat and condition scores (BCS, CNS, RUM), suggesting less adiposity.
    • Higher insulin sensitivity (RISQI) and adiponectin levels, which help regulate metabolism.
    • Higher tumor necrosis factor alpha (TNFα), a cytokine involved in inflammation.
  • Non-lactating mares (NL) showed:
    • Higher basal insulin and glucose areas under the curve, indicating reduced insulin sensitivity.
    • Increasing levels of NEFA (fatty acids) towards late pregnancy (D275), a pattern not seen in lactating mares.
    • Metabolic profiles closer to thresholds associated with metabolic syndrome, a condition linked to insulin resistance and obesity.
  • Cytokine fluctuations during pregnancy:
    • Resistin peaked mid-gestation (D110 and D165) and declined later.
    • Leptin was elevated early-mid pregnancy but decreased later and postpartum.
    • The variation in cytokines corresponds with shifts in metabolism and adiposity throughout pregnancy.

Conclusions and Implications

  • The study demonstrated that lactation significantly influences metabolic, hormonal, and inflammatory markers during pregnancy in mares.
  • Lactating mares maintained better insulin sensitivity and healthier lipid metabolism compared to non-lactating ones, possibly reducing the risk of metabolic syndrome.
  • Since many embryo transfer recipient mares are non-lactating, understanding these differences is critical for managing mare health and optimizing offspring development.
  • The authors recommend further research to explore how lactation affects metabolic health and reproductive outcomes in mares, contributing to improved management strategies.

Cite This Article

APA
Affonso FJ, Alonso MA, Bringel B, Douglas R, de Paula Nogueira G, Boakari YL, Fernandes CB. (2024). The influence of lactation on insulin and glucose metabolism, lipid profile, and cytokines in pregnant mares. Theriogenology, 230, 107-114. https://doi.org/10.1016/j.theriogenology.2024.09.003

Publication

ISSN: 1879-3231
NlmUniqueID: 0421510
Country: United States
Language: English
Volume: 230
Pages: 107-114
PII: S0093-691X(24)00372-8

Researcher Affiliations

Affonso, Fernanda Jordão
  • Department of Pathology, Theriogenology, and One Healthy, School of Agricultural and Veterinarian Sciences (FCAV), São Paulo State University (UNESP), Via de Acesso Prof.Paulo Donato Castellane, Jaboticabal, SP, 14884-900, Brazil.
Alonso, Maria Augusta
  • Department of Animal Reproduction, School of Veterinary Medicine and Animal Science School of Veterinary Medicine and Animal Science, USP - University of São Paulo, 87, Prof. Dr. Orlando Marques de Paiva Avenue, Cidade Universitária, São Paulo, SP, 05508-270, Brazil.
Bringel, Beatriz
  • BET Labs, 2225, Borges de Medeiros Avenue, Jockey Club Brasileiro - Lagoa, Rio de Janeiro, RJ, 22470-002, Brazil.
Douglas, Robert
  • BET Labs, University of Kentucky Coldstream, Research Campus, 1501 Bull Lea Road, Suite 102, Lexington, KY, USA, 40511.
de Paula Nogueira, Guilherme
  • Laboratory of Endocrinology, School of Veterinary Medicine, São Paulo State University (UNESP), Campus Araçatuba, 793 Clovis Pestana Street, Araçatuba, SP, 16050-680, Brazil.
Boakari, Yatta Linhares
  • Department of Large Animal Clinical Sciences, School of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX, USA.
Fernandes, Claudia Barbosa
  • Department of Animal Reproduction, School of Veterinary Medicine and Animal Science School of Veterinary Medicine and Animal Science, USP - University of São Paulo, 87, Prof. Dr. Orlando Marques de Paiva Avenue, Cidade Universitária, São Paulo, SP, 05508-270, Brazil. Electronic address: fernandescp@usp.br.

MeSH Terms

  • Animals
  • Female
  • Pregnancy
  • Horses / physiology
  • Lactation / physiology
  • Insulin / blood
  • Insulin / metabolism
  • Cytokines / metabolism
  • Cytokines / blood
  • Pregnancy, Animal / metabolism
  • Pregnancy, Animal / blood
  • Blood Glucose / metabolism
  • Lipid Metabolism / physiology
  • Lipids / blood

Citations

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