Elsevier

Domestic Animal Endocrinology

Volume 69, October 2019, Pages 75-83
Domestic Animal Endocrinology

Ultrasonographic measures of body fatness and their relationship with plasma levels and adipose tissue expression of four adipokines in Welsh pony mares

https://doi.org/10.1016/j.domaniend.2019.02.002Get rights and content

Abstract

Obesity is responsible for metabolic dysregulations that alter fertility and induce pathologies. The objectives of the present study were to validate a reliable method for the evaluation of body fatness in mares and to associate the body fat estimation data to metabolic changes, including adipokines at the plasma and adipose tissue levels. To reach this purpose, animals were subjected to two extreme breeding conditions to study the variation of morphological, ultrasound, and physiological parameters. Twenty Welsh mares were followed up monthly from April to October before and after animals were moved outdoors to grasslands. Body weight (BW), body length (BL), height at the withers (HW), thoracic perimeter (TP), 5-point body condition score (BCS), and subcutaneous fat thickness (SFT) at the level of the shoulder, the lumbar region, and the rump, measured by ultrasonography, and plasma and adipose tissue metabolic indicators were assessed in parallel. Statistical analysis was performed using a linear mixed-effects model, whereas Pearson tests were used for the analysis of the correlations between the different parameters. Although mean BW did not increase significantly (P = 0.0940), TP (P = 0.0002) and BCS (P < 0.0001) increased during the study period. Ultrasonographic examination of subcutaneous adipose tissue showed an increase in SFT at the level of the shoulder (P < 0.0001), lumbar region (P < 0.0001), and rump (P < 0.0001). Plasma concentrations of nonesterified fatty acids (P < 0.0001), phospholipids (P < 0.0001), and cholesterol (P < 0.0001) increased significantly, whereas triglycerides (P < 0.0001) decreased significantly during the study period. Although both plasma concentrations and adipose tissue expression of leptin (P < 0.0001) and resistin (P < 0.0001) increased significantly, adiponectin (P < 0.0001) significantly decreased and visfatin remained unchanged (P = 0.8401). Expression of adipokine receptors studied showed the opposite pattern compared with their ligand. Ultrasonographic measurements of subcutaneous adipose tissue thickness at the shoulder, lumbar region, and rump are relevant indicators of fatness related with adipokine plasma concentrations and expression of adipokine-related receptors in adipose tissue, and particularly highlight seasonal effects.

Introduction

Obesity in the mare is responsible for various metabolic dysregulations that alter fertility and induce different pathologies [1]. Often included in what is called the equine metabolic syndrome (a cluster of clinical abnormalities whose key feature is insulin insensitivity resulting from hypersecretion of cortisol in adipose tissue, in absence of pituitary involvement), these pathologies are very diverse, ranging from problems affecting locomotion such as laminitis [2] to much more serious metabolic disorders such as insulin dysregulation [3] or the impairment of energy metabolism in the entire organism [4]. In our Welsh pony herd, we are constantly looking for the healthy body habitus for our animals. Our lush pastures are very different from the environment in which the Welsh breed was developed, causing our animals to become obese over successive years, which leads to various pathologies related to overweight condition such as lameness and frequent reproductive problems, making them a good model to study these pathologies.

Apart from body weight (BW), there is a lack of objective and reliable in-field methods for assessing body fatness in equidae. To have reliable fatness indicators, we were first interested in ultrasound measurements by transposing some of the indicators that had already been validated in cattle such as backfat thickness [5]. Moreover, recent works have shown that ultrasound is an interesting approach for monitoring subcutaneous fat deposits in ponies [6], [7]. In parallel, we have been interested in the cytokines of white adipose tissue and focused on leptin [8], [9], [10], [11], adiponectin [9], [10], [11], [12], [13], resistin [9], [14], [15], and visfatin [16], which have been largely studied in plasma and adipose tissue of cattle [17]. These adipokines are not specific to cattle as they are expressed in other domestic animals including chicken [18] and rodents, in which species they have important regulatory functions and in which plasma concentrations or adipose tissue expression changes when energy balance is increased or decreased [13], [14], [16], [19].

Recent reports have shown that the assessment of adipokines provides important information on the growth kinetics of adipose tissue [20], [21]. The objective of this work was first to generate two different extreme states and validate a reliable method for the evaluation of body fatness in Welsh pony mares and second to associate these measures of fatness with metabolic changes including adipokine expression in both plasma and white adipose tissue that occur during summer and early autumn. We assume here that simple and easily achievable ultrasound measurements in the field could replace the use of subjective evaluation methods, and we propose to verify to what extent ultrasound measurements are correlated with physiometabolic parameters.

Section snippets

Animals and experimental design

Experimentation was conducted on 20 Welsh pony mares in accordance with the French National Guidelines for the care and use of animals for research purposes and after approval of the local ethics committee (C2EA 19—Comité d’éthique en experimentation animale Val de Loire—authorization number 2015032309182840–APAFiS#363). Mares aged from 5 to 17 yr (mean age ± SEM = 12.4 ± 3.5). They were housed in boxes during the winter with a natural photoperiod. They were fed twice a day with straw (3.3 kg

Morphological parameters

There was a trend for an increase of BW across the study period, mean BW increasing from 295.0 ± 61.1 kg (mean ± SEM) in April before mares had access to grasslands to 351.0 ± 70.4 kg in October before mares had been rehoused, although this increase was not statistically significant (P = 0.0940). Thoracic perimeter increased significantly from 153.9 ± 10.6 cm in April to 171.1 ± 10.8 cm in October (P = 0.0002), whereas BCS increased from 3.0 ± 0.9 to 4.6 ± 0.6 (P < 0.0001) during the same

Discussion

The abundance of our grasslands, which does not correspond to the scarce environment in which the Welsh breed was developed, leads to the fact that a high proportion of our mares (at least half of them reached a BCS of 5/5) become obese every season. We have demonstrated an average increase in mares' weight between April and October, but this increase in weight was not significant because of the high heterogeneity of the animal population studied. Despite this interindividual variation, the

CRediT authorship contribution statement

C. Staub: Conceptualization, Funding acquisition, Formal analysis, Methodology, Investigation, Writing - review & editing. E. Venturi: Project administration, Methodology, Data curation, Formal analysis, Investigation. M. Cirot: Methodology, Data curation, Formal analysis, Investigation. L. Léonard: Methodology, Data curation, Formal analysis, Investigation. P. Barrière: Methodology, Investigation. T. Blard: Methodology, Investigation. Y. Gaudé: Methodology, Investigation. T. Gascogne:

Acknowledgments

The authors thank J-P. Dubois, C. Moussu, F. Elleboudt, G. Gomot, and all the staff of CIRE (INRA, Centre d’imagerie pour la recherche et l’enseignement, Nouzilly, F37380, France) for preparing the mare for CT scanning, Francois Laperruque and Edmond Ricard (INRA UMR1388 GenPhySE, Castanet-Tolosan, France) for developing the SIDEx (Système d’Information des Données d’Expérimentation) application and its informatics link with the TEO-A weighing device, and Flavie Derouin-Tochon and Auréline

References (47)

  • S.L. Giles et al.

    Obesity prevalence and associated risk factors in outdoor living domestic horses and ponies

    PeerJ

    (2014)
  • K.H. Treiber et al.

    Evaluation of genetic and metabolic predispositions and nutritional risk factors for pasture-associated laminitis in ponies

    J Am Vet Med Assoc

    (2006)
  • R.M. Hoffman et al.

    Obesity and diet affect glucose dynamics and insulin sensitivity in Thoroughbred geldings

    J Anim Sci

    (2003)
  • A. Ertelt et al.

    Metabolic syndrome: is equine disease comparable to what we know in humans?

    Endocr Connect

    (2014)
  • U.J. Schröder et al.

    Invited review: methods to determine body fat reserves in the dairy cow with special regard to ultrasonographic measurement of backfat thickness

    J Dairy Sci

    (2006)
  • A.H.A. Dugdale et al.

    Effects of season and body condition on appetite, body mass and body composition in ad libitum fed mares

    Vet J

    (2011)
  • E.W. Siegers et al.

    Ultrasonographic measurements of localized fat accumulation in Shetland pony mares fed a normal v. a high energy diet for 2 years

    Animal

    (2018)
  • R.A. Ehrhardt et al.

    Development of a specific radioimmunoassay to measure physiological changes of circulating leptin in cattle and sheep

    J Endocrinol

    (2000)
  • N. Mellouk et al.

    Involvement of plasma adipokines in metabolic and reproductive parameters in Holstein dairy cows fed with diets with differing energy levels

    J Dairy Sci

    (2017)
  • S. Mann et al.

    Short communication: the association of adiponectin and leptin concentrations with prepartum dietary energy supply, parity, body condition, and postpartum hyperketonemia in transition dairy cows

    J Dairy Sci

    (2018)
  • S.L. Giesy et al.

    Adiponectin deficit during the precarious glucose economy of early lactation in dairy cows

    Endocrinology

    (2012)
  • J. De Koster et al.

    Relationship between serum adiponectin concentration, body condition score, and peripheral tissue insulin response of dairy cows during the dry period

    Domest Anim Endocrinol

    (2017)
  • C.S. Krumm et al.

    Effect of hormonal and energy-related factors on plasma adiponectin in transition dairy cows

    J Dairy Sci

    (2017)
  • M. Reverchon et al.

    Resistin in dairy cows: plasma concentrations during early lactation, expression and potential role in adipose tissue

    PLoS One

    (2014)
  • M. Weber et al.

    Longitudinal changes in adipose tissue of dairy cows from late pregnancy to lactation. Part 1: the adipokines apelin and resistin and their relationship to receptors linked with lipolysis

    J Dairy Sci

    (2016)
  • A. Lemor et al.

    Transition period-related changes in the abundance of the mRNAs of adiponectin and its receptors, of visfatin, and of fatty acid binding receptors in adipose tissue of high-yielding dairy cows

    Domest Anim Endocrinol

    (2009)
  • M. Reverchon et al.

    Adipokines and the female reproductive tract

    Int J Endocrinol

    (2014)
  • N. Mellouk et al.

    Effect of different levels of feed restriction and fish oil fatty acid supplementation on fat deposition by using different techniques, plasma levels and mRNA expression of several adipokines in broiler breeder hens

    PLoS One

    (2018)
  • S.S. Block et al.

    Decreased concentration of plasma leptin in periparturient dairy cows is caused by negative energy balance

    J Endocrinol

    (2001)
  • J. Ungru et al.

    Effects of body weight reduction on blood adipokines and subcutaneous adipose tissue adipokine mRNA expression profiles in obese ponies

    Vet Rec

    (2012)
  • S. Selim et al.

    Relationships among body condition, insulin resistance and subcutaneous adipose tissue gene expression during the grazing season in mares

    PLoS One

    (2015)
  • G. Arnaud

    Notation de l’état corporel des chevaux de selle et de sport

  • A.H.A. Dugdale et al.

    Body condition scoring as a predictor of body fat in horses and ponies

    Vet J

    (2012)
  • Cited by (8)

    View all citing articles on Scopus
    View full text