Analyze Diet
Veterinary sciences2023; 10(12); doi: 10.3390/vetsci10120691

Obesity during Pregnancy in the Horse: Effect on Term Placental Structure and Gene Expression, as Well as Colostrum and Milk Fatty Acid Concentration.

Abstract: In horses, the prevalence of obesity is high and associated with serious metabolic pathologies. Being a broodmare has been identified as a risk factor for obesity. In other species, maternal obesity is known to affect the development of the offspring. This article is a follow-up study of previous work showing that Obese mares (O, n = 10, body condition score > 4.25 at insemination) were more insulin resistant and presented increased systemic inflammation during pregnancy compared to Normal mares (N, n = 14, body condition score < 4 at insemination). Foals born to O mares were more insulin-resistant, presented increased systemic inflammation, and were more affected by osteoarticular lesions. The objective of the present study was to investigate the effect of maternal obesity on placental structure and function, as well as the fatty acid profile in the plasma of mares and foals, colostrum, and milk until 90 days of lactation, which, to our knowledge, has been poorly studied in the horse. Mares from both groups were fed the same diet during pregnancy and lactation. During lactation, mares were housed in pasture. A strong heat wave, followed by a drought, occurred during their 2nd and 3rd months of lactation (summer of 2016 in the Limousin region, France). In the present article, term placental morphometry, structure (stereology), and gene expression (RT-qPCR, genes involved in nutrient transport, growth, and development, as well as vascularization) were studied. Plasma of mares and their foals, as well as colostrum and milk, were sampled at birth, 30 days, and 90 days of lactation. The fatty acid composition of these samples was measured using gas chromatography. No differences between the N and O groups were observed for term placental morphometry, structure, or gene expression. No difference in plasma fatty acid composition was observed between groups in mares. The plasma fatty acid profile of O foals was more pro-inflammatory and indicated an altered placental lipid metabolism between birth and 90 days of age. These results are in line with the increased systemic inflammation and altered glucose metabolism observed until 18 months of age in this group. The colostrum fatty acid profile of O mares was more pro-inflammatory and indicated an increased transfer and/or desaturation of long-chain fatty acids. Moreover, O foals received a colostrum poorer in medium-chain saturated fatty acid, a source of immediate energy for the newborn that can also play a role in immunity and gut microbiota development. Differences in milk fatty acid composition indicated a decreased ability to adapt to heat stress in O mares, which could have further affected the metabolic development of their foals. In conclusion, maternal obesity affected the fatty acid composition of milk, thus also influencing the foal's plasma fatty acid composition and likely participating in the developmental programming observed in growing foals.
Publication Date: 2023-12-04 PubMed ID: 38133242PubMed Central: PMC10748288DOI: 10.3390/vetsci10120691Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article focuses on the impacts of maternal obesity in horses on placental structure, gene expression, and the fatty acid concentration in colostrum and milk. While the study found no noticeable changes to placental features, it observed an increased pro-inflammatory fatty acid profile in obese mares’ offspring, indicating an altered placental lipid metabolism. Evident was also a negative impact on colostrum and milk quality, which likely influenced the offspring’s metabolic development.

Understanding the Study

  • The study followed up on previous conclusions indicating high insulin resistance and systemic inflammation in obese mares during pregnancy. By comparing these with normal mares, it was discovered that obesity might affect the health and growth of horse offspring.
  • The research aims to dig deeper into the effects of maternal obesity on the structure and function of the placenta. It also seeks to explore the fatty acid profile in the plasma of mares and foals along with the colostrum and milk over 90 days of lactation – a component that had not been given much attention in horse studies.
  • The pregnant mares in both the obese and normal groups were subjected to the same diet during pregnancy and lactation, and were kept in a pasture during lactation. The conditions during lactation included a heatwave and drought.

Methodology

  • Researchers used various methods to examine term placental morphometry, structure, and gene expression – this included stereology and RT-qPCR, targeting genes involved in nutrient transport, growth, development, and vascularization.
  • Numerous samples were collected during the study – plasma from mares and foals, and colostrum and milk – at birth, after 30 days, and after 90 days of lactation. The fatty acid composition of these samples was assessed using gas chromatography.

Key Findings

  • No significant differences were noted in placental morphometry, structure, or gene expression between normal and obese mares.
  • The plasma fatty acid profile of offspring from obese mares was more pro-inflammatory and indicated altered placental lipid metabolism up to the age of 90 days. This outcome is consistent with previous findings of increased systemic inflammation and altered glucose metabolism in this group until 18 months of age.
  • The fatty acid profile of colostrum from obese mares was also more pro-inflammatory; it suggested a heightened transfer and/or desaturation of long-chain fatty acids.
  • The milk from obese mares had a lesser quantity of medium-chain saturated fatty acid that serves as an immediate energy source for newborns and is critical in immunity and gut microbiota development.
  • Obese mares also showed a lessened ability to adapt to heat stress, likely affecting the metabolic development of their foals.

Conclusion

  • The study concludes that maternal obesity can influence the fatty acid composition in milk, which in turn might impact the plasma fatty acid composition in foals and has potential effects on their metabolic development.

Cite This Article

APA
Robles M, Rousseau-Ralliard D, Dubois C, Josse T, Nouveau É, Dahirel M, Wimel L, Couturier-Tarrade A, Chavatte-Palmer P. (2023). Obesity during Pregnancy in the Horse: Effect on Term Placental Structure and Gene Expression, as Well as Colostrum and Milk Fatty Acid Concentration. Vet Sci, 10(12). https://doi.org/10.3390/vetsci10120691

Publication

ISSN: 2306-7381
NlmUniqueID: 101680127
Country: Switzerland
Language: English
Volume: 10
Issue: 12

Researcher Affiliations

Robles, Morgane
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
  • Institut Polytechnique Unilasalle, 76130 Mont-Saint-Aignan, France.
Rousseau-Ralliard, Delphine
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
Dubois, Cédric
  • Institut Français du Cheval et de l'Equitation, Station Expérimentale de la Valade, 19370 Chamberet, France.
Josse, Tiphanie
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
Nouveau, Émilie
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
Dahirel, Michele
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
Wimel, Laurence
  • Institut Français du Cheval et de l'Equitation, Station Expérimentale de la Valade, 19370 Chamberet, France.
Couturier-Tarrade, Anne
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.
Chavatte-Palmer, Pascale
  • BREED, Domaine de Vilvert, Université Paris Saclay, UVSQ, INRAE, 78350 Jouy en Josas, France.
  • BREED, Ecole Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France.

Grant Funding

  • FOETALIM / Institut Français du Cheval et de l'Équitation
  • FOETALIM / Fonds Eperon

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 108 references
  1. Peugnet P, Robles M, Wimel L, Tarrade A, Chavatte-Palmer P. Management of the Pregnant Mare and Long-Term Consequences on the Offspring. Theriogenology 2016;86:99–109.
  2. Robles M, Hammer C, Staniar B, Chavatte-Palmer P. Nutrition of Broodmares. Vet. Clin. Equine Pract. 2021;37:177–205.
    doi: 10.1016/j.cveq.2021.01.001pubmed: 33820606google scholar: lookup
  3. Chavatte-Palmer P, Derisoud E, Robles M. Pregnancy and Placental Development in Horses: An Update. Domest. Anim. Endocrinol. 2022;79:106692.
  4. Derisoud E, Auclair-Ronzaud J, Palmer E, Robles M, Chavatte-Palmer P, Derisoud E, Auclair-Ronzaud J, Palmer E, Robles M, Chavatte-Palmer P. Female Age and Parity in Horses: How and Why Does It Matter?. Reprod. Fertil. Dev. 2021;34:52–116.
    doi: 10.1071/RD21267pubmed: 35231230google scholar: lookup
  5. Peugnet P, Wimel L, Duchamp G, Sandersen C, Camous S, Guillaume D, Dahirel M, Dubois C, Jouneau L, Reigner F. Enhanced or Reduced Fetal Growth Induced by Embryo Transfer into Smaller or Larger Breeds Alters Post-Natal Growth and Metabolism in Pre-Weaning Horses. PLoS ONE 2014;9:e102044.
  6. Peugnet P, Mendoza L, Wimel L, Duchamp G, Dubois C, Reigner F, Caudron I, Deliège B, Toquet M, Richard E. Longitudinal Study of Growth and Osteoarticular Status in Foals Born to Between-Breed Embryo Transfers. J. Equine Vet. Sci. 2016;37:24–38.
  7. Giussani D, Forhead A, Gardner D, Fletcher A, Allen W, Fowden A. Postnatal Cardiovascular Function after Manipulation of Fetal Growth by Embryo Transfer in the Horse. J. Physiol. 2003;547:67–76.
  8. Forhead A, Ousey J, Allen W, Fowden A. Postnatal Insulin Secretion and Sensitivity after Manipulation of Fetal Growth by Embryo Transfer in the Horse. J. Endocrinol. 2004;181:459–467.
    doi: 10.1677/joe.0.1810459pubmed: 15171694google scholar: lookup
  9. Tischner M, Klimczak M. The Development of Polish Ponies Born after Embryo Transfer to Large Recipients. Equine Vet. J. 1989;21:62–63.
  10. Kubiak J, Evans J, Potter G, Harms P, Jenkins W. Parturition in the Multiparous Mare Fed to Obesity. Equine Vet. Sci. 1988;8:135–140.
  11. Kubiak J, Evans J, Potter G, Harms P, Jenkins W. Milk Yield Composition in the Multiparous Mare Fed to Obesity. Equine Vet. Sci. 1991;11:158–162.
  12. Henneke D, Potter G, Kreider J. Body Condition during Pregnancy and Lactation and Reproductive Efficiency of Mares. Theriogenology 1984;21:897–909.
  13. Bradbery A.N, Coverdale J.A, Hammer C.J, Dunlap K.A, Leatherwood J.L, Satterfield M.C. Effect of Maternal Overnutrition on Predisposition to Insulin Resistance in the Foal: Foal Skeletal Muscle Development and Insulin Signaling. Domest. Anim. Endocrinol. 2021;77:106648.
  14. Wilsher S, Allen W. Effects of a Streptococcus Equi Infection—Mediated Nutritional Insult during Mid-Gestation in Primiparous Thoroughbred Fillies. Part 1: Placental and Fetal Development. Equine Vet. J. 2006;38:549–557.
    doi: 10.2746/042516406X156497pubmed: 17124846google scholar: lookup
  15. Peugnet P, Robles M, Mendoza L, Wimel L, Dubois C, Dahirel M, Guillaume D, Camous S, Berthelot V, Toquet M.-P. Effects of Moderate Amounts of Barley in Late Pregnancy on Growth, Glucose Metabolism and Osteoarticular Status of Pre-Weaning Horses. PLoS ONE 2015;10:e0122596.
  16. Robles M, Gautier C, Mendoza L, Peugnet P, Dubois C, Dahirel M, Lejeune J, Caudron I, Guenon I, Camous S. Maternal Nutrition during Pregnancy Affects Testicular and Bone Development, Glucose Metabolism and Response to Overnutrition in Weaned Horses up to Two Years. PLoS ONE 2017;12:e0169295.
  17. Robles M, Nouveau E, Gautier C, Mendoza L, Dubois C, Dahirel M, Lagofun B, Aubrière M, Lejeune J, Caudron I. Maternal Obesity Increases Insulin Resistance, Low-Grade Inflammation and Osteochondrosis Lesions in Foals and Yearlings until 18 Months of Age. PLoS ONE 2018;13:e0190309.
  18. Giles S, Rands S, Nicol C, Harris P. Obesity Prevalence and Associated Risk Factors in Outdoor Living Domestic Horses and Ponies. PeerJ 2014;2:e299.
    doi: 10.7717/peerj.299pmc: PMC3970797pubmed: 24711963google scholar: lookup
  19. Potter S, Bamford N, Harris P, Bailey S. Prevalence of Obesity and Owners’ Perceptions of Body Condition in Pleasure Horses and Ponies in South-Eastern Australia. Aust. Vet. J. 2016;94:427–432.
    doi: 10.1111/avj.12506pubmed: 27785793google scholar: lookup
  20. Hoffman C, Costa L, Freeman L. Survey of Feeding Practices, Supplement Use, and Knowledge of Equine Nutrition among a Subpopulation of Horse Owners in New England. J. Equine Vet. Sci. 2009;29:719–726.
  21. Furtado T, Perkins E, Pinchbeck G, McGowan C, Watkins F, Christley R. Exploring Horse Owners’ Understanding of Obese Body Condition and Weight Management in UK Leisure Horses. Equine Vet. J. 2021;53:752–762.
    doi: 10.1111/evj.13360pubmed: 33002214google scholar: lookup
  22. Hoffman R.M, Boston R.C, Stefanovski D, Kronfeld D.S, Harris P.A. Obesity and Diet Affect Glucose Dynamics and Insulin Sensitivity in Thoroughbred Geldings. J. Anim. Sci. 2003;81:2333–2342.
    doi: 10.2527/2003.8192333xpubmed: 12968709google scholar: lookup
  23. Siwinska N, Janus I, Zak-Bochenek A, Noszczyk-Nowak A. Influence of Obesity on Histological Tissue Structure of the Cardiovascular System in Horses. Animals 2022;12:732.
    doi: 10.3390/ani12060732pmc: PMC8944453pubmed: 35327129google scholar: lookup
  24. Lovett A.L, Gilliam L.L, Sykes B.W, McFarlane D. Thromboelastography in Obese Horses with Insulin Dysregulation Compared to Healthy Controls. J. Vet. Intern. Med. 2022;36:1131–1138.
    doi: 10.1111/jvim.16421pmc: PMC9151488pubmed: 35429197google scholar: lookup
  25. Pearson W, Wood K, Stanley S, Macnicol J. Exploring Relationships between Body Condition Score, Body Fat, Activity Level and Inflammatory Biomarkers. J. Anim. Physiol. Anim. Nutr. 2018;102:1062–1068.
    doi: 10.1111/jpn.12893pubmed: 29707811google scholar: lookup
  26. Salinas C, Espinosa G, Morales N, Henríquez C, Morán G, Gajardo G, Burgos R.A, Uberti B. Evaluation of Peripheral Blood Polymorphonuclear Cell Functions after an Oral Carbohydrate Overload in Obese and Insulin Dysregulated Horses. Vet. Immunol. Immunopathol. 2022;250:110455.
    doi: 10.1016/j.vetimm.2022.110455pubmed: 35716440google scholar: lookup
  27. Frank N. Equine Metabolic Syndrome. Vet. Clin. North Am. Equine Pract. 2011;27:73–92.
    doi: 10.1016/j.cveq.2010.12.004pubmed: 21392655google scholar: lookup
  28. Alford P, Geller S, Richrdson B, Slater M, Honnas C, Foreman J, Robinson J, Messer M, Roberts M, Goble D. A Multicenter, Matched Case-Control Study of Risk Factors for Equine Laminitis. Prev. Vet. Med. 2001;49:209–222.
    doi: 10.1016/S0167-5877(01)00188-Xpubmed: 11311954google scholar: lookup
  29. Garber A, Hastie P, Murray J.-A. Factors Influencing Equine Gut Microbiota: Current Knowledge. J. Equine Vet. Sci. 2020;88:102943.
    doi: 10.1016/j.jevs.2020.102943pubmed: 32303307google scholar: lookup
  30. Roth P, Stanley J, Chamoun-Emanuelli A, Whitfield-Cargile C, Coleman M. Fecal Extract from Obese Horses Induces an Inflammatory Response by Murine Macrophages in Vitro. Am. J. Vet. Res. 2022;83:419–425.
    doi: 10.2460/ajvr.21.02.0024pubmed: 35113795google scholar: lookup
  31. Pratt-Phillips S, Munjizun A. Impacts of Adiposity on Exercise Performance in Horses. Anim. Open Access J. 2023;13:666.
    doi: 10.3390/ani13040666pmc: PMC9951652pubmed: 36830453google scholar: lookup
  32. Jansson A, Gunnarsson V.Þ., Ringmark S, Ragnarsson S, Söderroos D, Ásgeirsson E, Jóhannsdóttir T.R, Liedberg C, Stefánsdóttir G.J. Increased Body Fat Content in Horses Alters Metabolic and Physiological Exercise Response, Decreases Performance, and Increases Locomotion Asymmetry. Physiol. Rep. 2021;9:e14824.
    doi: 10.14814/phy2.14824pmc: PMC8191395pubmed: 34110691google scholar: lookup
  33. Jaqueth A.L, Iwaniuk M.E, Burk A.O. Characterization of the Prevalence and Management of Over-Conditioned Ponies and Horses in Maryland. J. Equine Vet. Sci. 2018;68:26–32.
    doi: 10.1016/j.jevs.2018.02.007pubmed: 31256884google scholar: lookup
  34. Shrestha N, Ezechukwu H.C, Holland O.J, Hryciw D.H. Developmental Programming of Peripheral Diseases in Offspring Exposed to Maternal Obesity during Pregnancy. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2020;319:R507–R516.
    doi: 10.1152/ajpregu.00214.2020pubmed: 32877239google scholar: lookup
  35. Kelly A.C, Powell T.L, Jansson T. Placental Function in Maternal Obesity. Clin. Sci. 2020;134:961–984.
    doi: 10.1042/CS20190266pmc: PMC8820171pubmed: 32313958google scholar: lookup
  36. Schoonejans J.M, Ozanne S.E. Developmental Programming by Maternal Obesity: Lessons from Animal Models. Diabet. Med. 2021;38:e14694.
    doi: 10.1111/dme.14694pubmed: 34553414google scholar: lookup
  37. Lecoutre S, Maqdasy S, Breton C. Maternal Obesity as a Risk Factor for Developing Diabetes in Offspring: An Epigenetic Point of View. World J. Diabetes 2021;12:366–382.
    doi: 10.4239/wjd.v12.i4.366pmc: PMC8040079pubmed: 33889285google scholar: lookup
  38. Kislal S, Shook L.L, Edlow A.G. Perinatal Exposure to Maternal Obesity: Lasting Cardiometabolic Impact on Offspring. Prenat. Diagn. 2020;40:1109–1125.
    doi: 10.1002/pd.5784pmc: PMC7719098pubmed: 32643194google scholar: lookup
  39. Rodgers A, Sferruzzi-Perri A.N. Developmental Programming of Offspring Adipose Tissue Biology and Obesity Risk. Int. J. Obes. 2021;45:1170–1192.
    doi: 10.1038/s41366-021-00790-wpmc: PMC8159749pubmed: 33758341google scholar: lookup
  40. Kong L, Chen X, Gissler M, Lavebratt C. Relationship of Prenatal Maternal Obesity and Diabetes to Offspring Neurodevelopmental and Psychiatric Disorders: A Narrative Review. Int. J. Obes. 2020;44:1981–2000.
    doi: 10.1038/s41366-020-0609-4pmc: PMC7508672pubmed: 32494038google scholar: lookup
  41. Menting M.D, van de Beek C, Mintjens S, Wever K.E, Korosi A, Ozanne S.E, Limpens J, Roseboom T.J, Hooijmans C, Painter R.C. The Link between Maternal Obesity and Offspring Neurobehavior: A Systematic Review of Animal Experiments. Neurosci. Biobehav. Rev. 2019;98:107–121.
  42. Derisoud E, Auclair-Ronzaud J, Rousseau-Ralliard D, Philau S, Aujean E, Durand A, Dahirel M, Charlier M, Boutinaud M, Wimel L. Maternal Age, Parity and Nursing Status at Fertilization Affects Postpartum Lactation Up to Weaning in Horses. J. Equine Vet. Sci. 2023;128:104868.
    doi: 10.1016/j.jevs.2023.104868pubmed: 37329928google scholar: lookup
  43. Robles M, Loux S.C, de Mestre A.M, Chavatte-Palmer P. Environmental Constraints and Pathologies That Modulate Equine Placental Genes and Development. Reprod. Camb. Engl. 2022;163:R25–R38.
    doi: 10.1530/REP-21-0116pubmed: 35019860google scholar: lookup
  44. Allen W, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale P, Fowden A, Turnbull C, Stewart F, Ousey J. Influence of Maternal Size on Placental, Fetal and Postnatal Growth in the Horse. I. Development in Utero. Reproduction 2002;172:445–453.
    doi: 10.1530/rep.0.1230445pubmed: 11882022google scholar: lookup
  45. Robles M, Peugnet P, Dubois C, Piumi F, Jouneau L, Bouchez O, Aubrière M, Dahirel M, Aioun J, Wimel L. Placental Function and Structure at Term Is Altered in Broodmares Fed with Cereals from Mid-Gestation. Placenta 2018;64:44–52.
  46. Auclair-Ronzaud J, Jaffrézic F, Wimel L, Dubois C, Laloë D, Chavatte-Palmer P. Estimation of Milk Production in Suckling Mares and Factors Influencing Their Milk Yield. Animal 2022;16:100498.
    doi: 10.1016/j.animal.2022.100498pubmed: 35338904google scholar: lookup
  47. Reed M, Howard C, DE Yanés G. One-Stop Stereology: The Estimation of 3D Parameters Using Isotropic Rulers. J. Microsc. 2010;239:54–65.
  48. Chomczynski P, Sacchi N. Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate-Phenol-Chloroform Extraction. Anal. Biochem. 1987;162:156–159.
    doi: 10.1016/0003-2697(87)90021-2pubmed: 2440339google scholar: lookup
  49. Tarrade A, Rousseau-Ralliard D, Aubrière M, Peynot N, Dahirel M, Bertrand-Michel J, Aguirre-Lavin T, Morel O, Beaujean N, Duranthon V. Sexual Dimorphism of the Feto-Placental Phenotype in Response to a High Fat and Control Maternal Diets in a Rabbit Model. PLoS ONE 2013;8:e83458.
  50. Folch J, Lees M, Stanley G.S. A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues. J. Biol. Chem. 1957;226:497–509.
    doi: 10.1016/S0021-9258(18)64849-5pubmed: 13428781google scholar: lookup
  51. Morrison W.R, Smith L.M. Preparation of Fatty Acid Methyl Esters and Dimethylacetals from Lipids with Boron Fluoride–Methanol. J. Lipid Res. 1964;5:600–608.
    doi: 10.1016/S0022-2275(20)40190-7pubmed: 14221106google scholar: lookup
  52. Rousseau D, Héliès-Toussaint C, Moreau D, Raederstorff D, Grynberg A. Dietary N-3 PUFAs Affect the Blood Pressure Rise and Cardiac Impairments in a Hyperinsulinemia Rat Model in Vivo. Am. J. Physiol.-Heart Circ. Physiol. 2003;285:H1294–H1302.
    doi: 10.1152/ajpheart.00651.2002pubmed: 12521943google scholar: lookup
  53. Dubé E, Gravel A, Martin C, Desparois G, Moussa I, Ethier-Chiasson M, Forest J.-C, Giguère Y, Masse A, Lafond J. Modulation of Fatty Acid Transport and Metabolism by Maternal Obesity in the Human Full-Term Placenta1. Biol. Reprod. 2012;87:14.
    doi: 10.1095/biolreprod.111.098095pubmed: 22553224google scholar: lookup
  54. Tian L, Dong S.S, Hu J, Yao J.J, Yan P.S. The Effect of Maternal Obesity on Fatty Acid Transporter Expression and Lipid Metabolism in the Full-Term Placenta of Lean Breed Swine. J. Anim. Physiol. Anim. Nutr. 2018;102:e242–e253.
    doi: 10.1111/jpn.12735pubmed: 28508539google scholar: lookup
  55. Song L, Wang N, Peng Y, Sun B, Cui W. Placental Lipid Transport and Content in Response to Maternal Overweight and Gestational Diabetes Mellitus in Human Term Placenta. Nutr. Metab. Cardiovasc. Dis. 2022;32:692–702.
    doi: 10.1016/j.numecd.2021.12.018pubmed: 35109996google scholar: lookup
  56. Nogues P, Dos Santos E, Couturier-Tarrade A, Berveiller P, Arnould L, Lamy E, Grassin-Delyle S, Vialard F, Dieudonne M.-N. Maternal Obesity Influences Placental Nutrient Transport, Inflammatory Status, and Morphology in Human Term Placenta. J. Clin. Endocrinol. Metab. 2020;12:dgaa660.
    doi: 10.1210/clinem/dgaa660pubmed: 32936881google scholar: lookup
  57. Rasool A, Mahmoud T, Mathyk B, Kaneko-Tarui T, Roncari D, White K.O, O’Tierney-Ginn P. Obesity Downregulates Lipid Metabolism Genes in First Trimester Placenta. Sci. Rep. 2022;12:19368.
    doi: 10.1038/s41598-022-24040-9pmc: PMC9653480pubmed: 36371454google scholar: lookup
  58. Napso T, Lean S.C, Lu M, Mort E.J, Desforges M, Moghimi A, Bartels B, El-Bacha T, Fowden A.L, Camm E.J. Diet-induced Maternal Obesity Impacts Feto-placental Growth and Induces Sex-specific Alterations in Placental Morphology, Mitochondrial Bioenergetics, Dynamics, Lipid Metabolism and Oxidative Stress in Mice. Acta Physiol. 2022;234:e13795.
    doi: 10.1111/apha.13795pmc: PMC9286839pubmed: 35114078google scholar: lookup
  59. Powell T.L, Barner K, Madi L, Armstrong M, Manke J, Uhlson C, Jansson T, Ferchaud-Roucher V. Sex-Specific Responses in Placental Fatty Acid Oxidation, Esterification and Transfer Capacity to Maternal Obesity. Biochim. Biophys. Acta BBA Mol. Cell Biol. Lipids 2021;1866:158861.
  60. Bucher M, Montaniel K.R.C, Myatt L, Weintraub S, Tavori H, Maloyan A. Dyslipidemia, Insulin Resistance, and Impairment of Placental Metabolism in the Offspring of Obese Mothers. J. Dev. Orig. Health Dis. 2021;12:738–747.
    doi: 10.1017/S2040174420001026pmc: PMC8606174pubmed: 33185172google scholar: lookup
  61. Jarvie E, Hauguel-de-Mouzon S, Nelson S.M, Sattar N, Catalano P.M, Freeman D.J. Lipotoxicity in Obese Pregnancy and Its Potential Role in Adverse Pregnancy Outcome and Obesity in the Offspring. Clin. Sci. 2010;119:123–129.
    doi: 10.1042/CS20090640pmc: PMC2860697pubmed: 20443782google scholar: lookup
  62. Saben J, Lindsey F, Zhong Y, Thakali K, Badger T.M, Andres A, Gomez-Acevedo H, Shankar K. Maternal Obesity Is Associated with a Lipotoxic Placental Environment. Placenta 2014;35:171–177.
  63. Stewart F.M, Freeman D.J, Ramsay J.E, Greer I.A, Caslake M, Ferrell W.R. Longitudinal Assessment of Maternal Endothelial Function and Markers of Inflammation and Placental Function throughout Pregnancy in Lean and Obese Mothers. J. Clin. Endocrinol. Metab. 2007;92:969–975.
    doi: 10.1210/jc.2006-2083pubmed: 17192290google scholar: lookup
  64. Challier J.C, Basu S, Bintein T, Minium J, Hotmire K, Catalano P.M, Hauguel-de Mouzon S. Obesity in Pregnancy Stimulates Macrophage Accumulation and Inflammation in the Placenta. Placenta 2008;29:274–281.
  65. Roberts K.A, Riley S.C, Reynolds R.M, Barr S, Evans M, Statham A, Hor K, Jabbour H.N, Norman J.E, Denison F.C. Placental Structure and Inflammation in Pregnancies Associated with Obesity. Placenta 2011;32:247–254.
  66. Aye I.L.M.H, Lager S, Ramirez V.I, Gaccioli F, Dudley D.J, Jansson T, Powell T.L. Increasing Maternal Body Mass Index Is Associated with Systemic Inflammation in the Mother and the Activation of Distinct Placental Inflammatory Pathways1. Biol. Reprod. 2014;90:129.
  67. Zhou Y, Xu T, Wu Y, Wei H, Peng J. Oxidative Stress and Inflammation in Sows with Excess Backfat: Up-Regulated Cytokine Expression and Elevated Oxidative Stress Biomarkers in Placenta. Animals 2019;9:796.
    doi: 10.3390/ani9100796pmc: PMC6826773pubmed: 31615033google scholar: lookup
  68. Pietro L, Daher S, Rudge M.V.C, Calderon I.M.P, Damasceno D.C, Sinzato Y.K, Bandeira C, Bevilacqua E. Vascular Endothelial Growth Factor (VEGF) and VEGF-Receptor Expression in Placenta of Hyperglycemic Pregnant Women. Placenta 2010;31:770–780.
  69. Pazinato F.M, Curcio B.D.R, Fernandes C.G, Santos C.A, Feijó L.S, Varela A.S, Nogueira C.E.W. Histomorphometry of the Placental Vasculature and Microcotyledons in Thoroughbred Mares with Chronic Laminitis. Theriogenology 2017;91:77–81.
  70. Sessions-Bresnahan D.R, Heuberger A.L, Carnevale E.M. Obesity in Mares Promotes Uterine Inflammation and Alters Embryo Lipid Fingerprints and Homeostasis. Biol. Reprod. 2018;99:761–772.
    doi: 10.1093/biolre/ioy107pubmed: 29741587google scholar: lookup
  71. Dunbar B, Bauer J. Metabolism of Dietary Essential Fatty Acids and Their Conversion to Long-Chain Polyunsaturated Metabolites. J. Am. Vet. Med. Assoc. 2002;220:1621–1626.
    doi: 10.2460/javma.2002.220.1621pubmed: 12051499google scholar: lookup
  72. King S, AbuGhazaleh A, Webel S, Jones K. Circulating Fatty Acid Profiles in Response to Three Levels of Dietary Omega-3 Fatty Acid Supplementation in Horses. J. Anim. Sci. 2007;86:1114–1123.
    doi: 10.2527/jas.2007-0682pubmed: 18192545google scholar: lookup
  73. Hodge L.B, Rude B.J, Dinh T.N, Lemley C.O. Effect of ω-3 Fatty Acid Supplementation to Gestating and Lactating Mares: On Milk IgG, Mare and Foal Blood Concentrations of IgG, Insulin and Glucose, Placental Efficiency, and Fatty Acid Composition of Milk and Serum from Mares and Foals. J. Equine Vet. Sci. 2017;51:70–78.
  74. . Principles of Animal Nutrition. CRC Press; Boca Raton, FL, USA 2018. Chapter 6: Metabolism and Nutrition of Lipids; p. 800.
  75. Islam A, Kodama T, Yamamoto Y, Ebrahimi M, Miyazaki H, Yasumoto Y, Kagawa Y, Sawada T, Owada Y, Tokuda N. Omega-3 Fatty Acids Transport through the Placenta. Asian J. Med. Biol. Res. 2016;2:1–8.
    doi: 10.3329/ajmbr.v2i1.27561google scholar: lookup
  76. Ortega-Senovilla H, Alvino G, Taricco E, Cetin I, Herrera E. Gestational Diabetes Mellitus Upsets the Proportion of Fatty Acids in Umbilical Arterial but Not Venous Plasma. Diabetes Care 2009;32:120–122.
    doi: 10.2337/dc08-0679pmc: PMC2606843pubmed: 18852337google scholar: lookup
  77. Elzinga S, Wood P, Adams A.A. Plasma Lipidomic and Inflammatory Cytokine Profiles of Horses with Equine Metabolic Syndrome. J. Equine Vet. Sci. 2016;40:49–55.
  78. O’Connor C.I, Lawrence L.M, Hayes S.H. Dietary Fish Oil Supplementation Affects Serum Fatty Acid Concentrations in Horses1. J. Anim. Sci. 2007;85:2183–2189.
    doi: 10.2527/jas.2006-528pubmed: 17504965google scholar: lookup
  79. Dervishi E, Joy M, Sanz A, Alvarez-Rodriguez J, Molino F, Calvo J.H. Forage Preservation (Grazing vs. Hay) Fed to Ewes Affects the Fatty Acid Profile of Milk and CPT1B Gene Expression in the Sheep Mammary Gland. BMC Vet. Res. 2012;8:106.
    doi: 10.1186/1746-6148-8-106pmc: PMC3416728pubmed: 22776723google scholar: lookup
  80. Pietrzak-Fiećko R, Kamelska-Sadowska A.M. The Comparison of Nutritional Value of Human Milk with Other Mammals’ Milk. Nutrients 2020;12:1404.
    doi: 10.3390/nህ1404pmc: PMC7284997pubmed: 32422857google scholar: lookup
  81. Zentek J, Buchheit-Renko S, Ferrara F, Vahjen W, Van Kessel A.G, Pieper R. Nutritional and Physiological Role of Medium-Chain Triglycerides and Medium-Chain Fatty Acids in Piglets. Anim. Health Res. Rev. 2011;12:83–93.
    doi: 10.1017/S1466252311000089pubmed: 21676342google scholar: lookup
  82. Takase S, Goda T. Effects of Medium-Chain Triglycerides on Brush Border Membrane-Bound Enzyme Activity in Rat Small Intestine. J. Nutr. 1990;120:969–976.
    doi: 10.1093/jn/120.9.969pubmed: 2398418google scholar: lookup
  83. Dierick N.A, Decuypere J.A, Molly K, Van Beek E, Vanderbeke E. The Combined Use of Triacylglycerols (TAGs) Containing Medium Chain Fatty Acids (MCFAs) and Exogenous Lipolytic Enzymes as an Alternative to Nutritional Antibiotics in Piglet Nutrition. Livest. Prod. Sci. 2002;76:1–16.
  84. Kono H, Fujii H, Asakawa M, Maki A, Amemiya H, Hirai Y, Matsuda M, Yamamoto M. Medium-Chain Triglycerides Enhance Secretory IgA Expression in Rat Intestine after Administration of Endotoxin. Am. J. Physiol.-Gastrointest. Liver Physiol. 2004;286:G1081–G1089.
    doi: 10.1152/ajpgi.00457.2003pubmed: 15132951google scholar: lookup
  85. Wang J, Wu X, Simonavicius N, Tian H, Ling L. Medium-Chain Fatty Acids as Ligands for Orphan G Protein-Coupled Receptor GPR84. J. Biol. Chem. 2006;281:34457–34464.
    doi: 10.1074/jbc.M608019200pubmed: 16966319google scholar: lookup
  86. de la Garza Puentes A, Martí Alemany A, Chisaguano A.M, Montes Goyanes R, Castellote A.I, Torres-Espínola F.J, García-Valdés L, Escudero-Marín M, Segura M.T, Campoy C. The Effect of Maternal Obesity on Breast Milk Fatty Acids and Its Association with Infant Growth and Cognition—The PREOBE Follow-Up. Nutrients 2019;11:2154.
    doi: 10.3390/nᄉ2154pmc: PMC6770754pubmed: 31505767google scholar: lookup
  87. Armand M, Bernard J.Y, Forhan A, Heude B, Charles M.-A, Annesi-Maesano I, Bernard J.Y, Botton J, Charles M.-A, Dargent-Molina P. Maternal Nutritional Determinants of Colostrum Fatty Acids in the EDEN Mother-Child Cohort. Clin. Nutr. 2018;37:2127–2136.
    doi: 10.1016/j.clnu.2017.10.007pubmed: 29146525google scholar: lookup
  88. Rydlewski A.A, Manin L.P, Pizzo J.S, Silva P.D, da Silveira R, Tavares C.B.G, de Paula M, Pereira O, Santos O.O, Visentainer J.V. Lipid Profile by Direct Infusion ESI-MS and Fatty Acid Composition by GC-FID in Human Milk: Association with Nutritional Status of Donors. J. Food Compos. Anal. 2021;100:103797.
  89. Tang J. Advances in Dietary Lipids and Human Health. Elsevier; Amsterdam, The Netherlands 2022. Palmitoleic Acid in Health and Disease; pp. 293–302.
  90. Duckett S.K, Volpi Lagreca G, Alende M, Long N. Palmitoleic Acid Reduces Intramuscular Lipid and Restores Insulin Sensitivity in Obese Sheep. Diabetes Metab. Syndr. Obes. Targets Ther. 2014;7:553–563.
    doi: 10.2147/DMSO.S72695pmc: PMC4243576pubmed: 25429233google scholar: lookup
  91. de Souza C.O, Teixeira A.A.S, Biondo L.A, Lima Junior E.A, Batatinha H.A.P, Rosa Neto J.C. Palmitoleic Acid Improves Metabolic Functions in Fatty Liver by PPARα-Dependent AMPK Activation: PALMITOLEATE CONTROLLING PPARα-AMPK ON LIVER. J. Cell. Physiol. 2017;232:2168–2177.
    doi: 10.1002/jcp.25715pubmed: 27925195google scholar: lookup
  92. Yao D, Luo J, He Q, Shi H, Li J, Wang H, Xu H, Chen Z, Yi Y, Loor J.J. SCD1 Alters Long-Chain Fatty Acid (LCFA) Composition and Its Expression Is Directly Regulated by SREBP-1 and PPARγ 1 in Dairy Goat Mammary Cells: SCD1 AND FATTY ACID METABOLISM. J. Cell. Physiol. 2017;232:635–649.
    doi: 10.1002/jcp.25469pubmed: 27341271google scholar: lookup
  93. di Martino O, Troiano A, Addi L, Guarino A, Calabrò S, Tudisco R, Murru N, Cutrignelli M.I, Infascelli F, Calabrò V. Regulation of Stearoyl Coenzyme A Desaturase 1 Gene Promoter in Bovine Mammary Cells. Anim. Biotechnol. 2015;26:251–259.
    doi: 10.1080/10495398.2015.1022182pubmed: 26158455google scholar: lookup
  94. Dobrzyn P, Jazurek M, Dobrzyn A. Stearoyl-CoA Desaturase and Insulin Signaling—What Is the Molecular Switch?. Biochim. Biophys. Acta BBA Bioenerg. 2010;1797:1189–1194.
    doi: 10.1016/j.bbabio.2010.02.007pubmed: 20153289google scholar: lookup
  95. Shi H.B, Zhao W.S, Luo J, Yao D.W, Sun Y.T, Li J, Shi H.P, Loor J.J. Peroxisome Proliferator-Activated Receptor Γ1 and Γ2 Isoforms Alter Lipogenic Gene Networks in Goat Mammary Epithelial Cells to Different Extents. J. Dairy Sci. 2014;97:5437–5447.
    doi: 10.3168/jds.2013-7863pubmed: 25022676google scholar: lookup
  96. Flint D.J, Travers M.T, Barber M.C, Binart N, Kelly P.A. Diet-Induced Obesity Impairs Mammary Development and Lactogenesis in Murine Mammary Gland. Am. J. Physiol.-Endocrinol. Metab. 2005;288:E1179–E1187.
    doi: 10.1152/ajpendo.00433.2004pubmed: 15671082google scholar: lookup
  97. Marko R.C, Branislava B, Bojan T, Aleksandar P, Milenko S, Branislav L, Ivan R. Metabolic Acclimation to Heat Stress in Farm Housed Holstein Cows with Different Body Condition Scores. Afr. J. Biotechnol. 2011;10:10293–10303.
    doi: 10.5897/AJB11.847google scholar: lookup
  98. Liu Z, Ezernieks V, Wang J, Arachchillage N.W, Garner J.B, Wales W.J, Cocks B.G, Rochfort S. Heat Stress in Dairy Cattle Alters Lipid Composition of Milk. Sci. Rep. 2017;7:961.
    doi: 10.1038/s41598-017-01120-9pmc: PMC5430412pubmed: 28424507google scholar: lookup
  99. Bolzan A.M.S, Bonnet O.J.F, Wallau M.O, Basso C, Neves A.P, Carvalho P.C.d.F. Foraging Behavior Development of Foals in Natural Grassland. Rangel. Ecol. Manag. 2020;73:243–251.
  100. Contu L, Hawkes C. A Review of the Impact of Maternal Obesity on the Cognitive Function and Mental Health of the Offspring. Int. J. Mol. Sci. 2017;18:1093.
    doi: 10.3390/ijms18051093pmc: PMC5455002pubmed: 28534818google scholar: lookup
  101. Thompson J.R, Valleau J.C, Barling A.N, Franco J.G, De Capo M, Bagley J.L, Sullivan E.L. Exposure to a High-Fat Diet during Early Development Programs Behavior and Impairs the Central Serotonergic System in Juvenile Non-Human Primates. Front. Endocrinol. 2017;8:164.
    doi: 10.3389/fendo.2017.00164pmc: PMC5519527pubmed: 28785241google scholar: lookup
  102. Muhlhausler B, Adam C, Findlay P, Duffield J, McMillen I. Increased Maternal Nutrition Alters Development of the Appetite-Regulating Network in the Brain. FASEB J. 2006;20:1257–1259.
    doi: 10.1096/fj.05-5241fjepubmed: 16684802google scholar: lookup
  103. Purcell R, Sun B, Pass L, Power M, Moran T, Tamashiro K. Maternal Stress and High-Fat Diet Effect on Maternal Behavior, Milk Composition, and Pup Ingestive Behavior. Physiol. Behav. 2011;104:474–479.
  104. Borengasser S.J, Lau F, Kang P, Blackburn M.L, Ronis M.J.J, Badger T.M, Shankar K. Maternal Obesity during Gestation Impairs Fatty Acid Oxidation and Mitochondrial SIRT3 Expression in Rat Offspring at Weaning. PLoS ONE 2011;6:e24068.
  105. Isganaitis E, Woo M, Ma H, Chen M, Kong W, Lytras A, Sales V, De Coste-Lopez J, Lee K.-J, Leatherwood C. Developmental Programming by Maternal Insulin Resistance: Hyperinsulinemia, Glucose Intolerance, and Dysregulated Lipid Metabolism in Male Offspring of Insulin-Resistant Mice. Diabetes 2014;63:688–700.
    doi: 10.2337/db13-0558pmc: PMC3900545pubmed: 24186867google scholar: lookup
  106. Boyle K.E, Patinkin Z.W, Shapiro A.L.B, Bader C, Vanderlinden L, Kechris K, Janssen R.C, Ford R.J, Smith B.K, Steinberg G.R. Maternal Obesity Alters Fatty Acid Oxidation, AMPK Activity, and Associated DNA Methylation in Mesenchymal Stem Cells from Human Infants. Mol. Metab. 2017;6:1503–1516.
  107. Musaev A, Sadykova S, Anambayeva A, Saizhanova M, Balkanay G, Kolbaev M. Mare’s Milk: Composition, Properties, and Application in Medicine. Arch. Razi Inst. 2021;76:1125–1135.
  108. . State of the Climate in Europe 2022. WMO 2023. p. 40.