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Animals : an open access journal from MDPI2021; 11(2); doi: 10.3390/ani11020361

Overfeeding Extends the Period of Annual Cyclicity but Increases the Risk of Early Embryonic Death in Shetland Pony Mares.

Abstract: Obesity has been associated with altered reproductive activity in mares, and may negatively affect fertility. To examine the influence of long-term high-energy (HE) feeding on fertility, Shetland pony mares were fed a diet containing 200% of net energy (NE) requirements during a three-year study. The incidence of hemorrhagic anovulatory follicles (HAF) and annual duration of cyclicity were compared to those in control mares receiving a maintenance diet. Day-7 embryos were flushed and transferred between donor and recipient mares from both groups; the resulting conceptuses were collected 21 days after transfer to assess conceptus development. HE mares became obese, and embryos recovered from HE mares were more likely to succumb to early embryonic death. The period of annual cyclicity was extended in HE compared to control mares in all years. The incidence of HAFs did not consistently differ between HE and control mares. No differences in embryo morphometric parameters were apparent. In conclusion, consuming a HE diet extended the duration of cyclicity, and appeared to increase the likelihood of embryos undergoing early embryonic death following embryo transfer.
Publication Date: 2021-02-01 PubMed ID: 33535548PubMed Central: PMC7912773DOI: 10.3390/ani11020361Google Scholar: Lookup
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  • Journal Article

Summary

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This research investigates the impact of long-term high-energy feeding on the reproductive health and fertility of Shetland pony mares, highlighting that obesity resulting from such feeding can lead to extended annual cyclicity but also an elevated likelihood of early embryonic death.

Objective and Methodology

  • The objective of this study was to examine the effects of long-term overfeeding on the reproductive activity and fertility of Shetland pony mares. The researchers fed the mares a high-energy (HE) diet (200% of net energy requirements) over a three-year period.
  • The researchers conducted comparative investigations on the incidence of hemorrhagic anovulatory follicles (HAF) and the annual duration of cyclicity between the test group and control mares that received a normal maintenance diet.
  • To evaluate the influence of such feeding on the growth and health of embryos, day-7 embryos were flushed from the mares, transferred between donor and recipient mares from both groups, and later collected for assessment 21 days post-transfer.

Findings

  • The study revealed that the mares that ate the high-energy diet became obese.
  • An obesity-induced risk was noted with the embryos from these high-energy-fed mares, as they were more likely to experience early embryonic death compared to those from the control mares.
  • The study also found that the period of annual cyclicity extended for the mares that consumed a high-energy diet compared to those that did not.
  • The incidence of hemorrhagic anovulatory follicles (HAF), however, did not consistently differ between the two groups of mares.
  • There were no noticeable differences in embryo morphometric parameters (structural/size aspects) between both the groups of mares.

Conclusion

  • The results suggest that while a high-energy diet can extend the duration of cyclicity, it also carries a potential risk by increasing the chance of early embryonic death in transferred embryos.

Cite This Article

APA
D'Fonseca NMM, Gibson CME, Hummel I, van Doorn DA, Roelfsema E, Stout TAE, van den Broek J, de Ruijter-Villani M. (2021). Overfeeding Extends the Period of Annual Cyclicity but Increases the Risk of Early Embryonic Death in Shetland Pony Mares. Animals (Basel), 11(2). https://doi.org/10.3390/ani11020361

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 2

Researcher Affiliations

D'Fonseca, Nicky M M
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
Gibson, Charlotte M E
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
Hummel, Iris
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
van Doorn, David A
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
  • Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584 CL Utrecht, The Netherlands.
Roelfsema, Ellen
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
Stout, Tom A E
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.
van den Broek, Jan
  • Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, 3584 CL Utrecht, The Netherlands.
de Ruijter-Villani, Marta
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.

Grant Funding

  • 317146 / FP7 People: Marie-Curie Actions

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 34 references
  1. Hoffman RM, Boston RC, Stefanovski D, Kronfeld DS, Harris PA. 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
  2. Treiber KH, Kronfeld DS, Hess TM, Byrd BM, Splan RK, Staniar WB. Evaluation of genetic and metabolic predispositions and nutritional risk factors for pasture-associated laminitis in ponies.. J. Am. Vet. Med. Assoc. 2006;228:1538–1545.
    doi: 10.2460/javma.228.10.1538pubmed: 16677122google scholar: lookup
  3. Heliczer N. Cardiovascular findings in ponies with equine metabolic syndrome.. J. Am. Vet. Med. Assoc. 2017;250:1027–1035.
    doi: 10.2460/javma.250.9.1027pubmed: 28414603google scholar: lookup
  4. Durham AE, Frank N, McGowan CM, Menzies-Gow N, Roelfsema E, Vervuert I, Feige K, Fey KE. ECEIM consensus statement on equine metabolic syndrome.. J. Vet. Intern. Med. 2019;33:335–349.
    doi: 10.1111/jvim.15423pmc: PMC6430910pubmed: 30724412google scholar: lookup
  5. Vick MM, Sessions DR, Murphy BA, Kennedy EL, Reedy SE, Fitzgerald BP. Obesity is associated with altered metabolic and reproductive activity in the mare: Effects of metformin on insulin sensitivity and reproductive cyclicity.. Reprod. Fertil. Dev. 2006;18:609–617.
    doi: 10.1071/RD06016pubmed: 16930507google scholar: lookup
  6. Nagy P, Guillaume D, Daels P. Seasonality in mares.. Anim. Reprod. Sci. 2000;60:245–262.
    doi: 10.1016/S0378-4320(00)00133-0pubmed: 10844199google scholar: lookup
  7. Aurich C. Reproductive cycles of horses.. Anim. Reprod. Sci. 2011;124:220–228.
  8. Salazar-Ortiz J, Camous S, Briant C, Lardic L, Chesneau D, Guillaume D. Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus). Reprod. Biol. Endocrinol. 2011;9:130.
    doi: 10.1186/1477-7827-9-130pmc: PMC3195710pubmed: 21958120google scholar: lookup
  9. Fitzgerald BP, McManus CJ. Photoperiodic Versus Metabolic Signals as Determinants of Seasonal Anestrus in the Mare1.. Biol. Reprod. 2000;63:335–340.
    doi: 10.1095/biolreprod63.1.335pubmed: 10859276google scholar: lookup
  10. Cuervo-Arango J, Newcombe JR. Risk factors for the development of haemorrhagic anovulatory follicles in the mare.. Reprod. Domest. Anim. 2010;45:473–480.
  11. McCue PM, Squires EL. Persistent anovulatory follicles in the mare.. Theriogenology. 2002;58:541–543.
  12. Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet. J. 1983;15:371–372.
  13. Rittenberg V, Seshadri S, Sunkara SK, Sobaleva S, Oteng-Ntim E, El-Toukhy T. Effect of body mass index on IVF treatment outcome: An updated systematic review and meta-analysis.. Reprod. Biomed. Online. 2011;23:421–439.
    doi: 10.1016/j.rbmo.2011.06.018pubmed: 21885344google scholar: lookup
  14. Sohrabi M, Mohammadi Roushandeh A, Alizadeh Z, Vahidinia A, Vahabian M, Hosseini M. Effect of a high fat diet on ovary morphology, in vitro development, in vitro fertilisation rate and oocyte quality in mice.. Singap. Med. J. 2015;56:573–579.
    doi: 10.11622/smedj.2015085pmc: PMC4613934pubmed: 26512150google scholar: lookup
  15. Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL, Jansson T. High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice.. FASEB J. 2008;23:271–278.
    doi: 10.1096/fj.08-116889pmc: PMC2626621pubmed: 18827021google scholar: lookup
  16. D’ Fonseca NMM, Gibson CME, Doorn DA, Ruijter-Villani M, Stout TAE, Roelfsema E. Effect of long-term overfeeding of a high-energy diet on glucose tolerance in Shetland pony mares.. J. Vet. Intern. Med. 2020;34:1339–1349.
    doi: 10.1111/jvim.15788pmc: PMC7255650pubmed: 32374454google scholar: lookup
  17. Centraal Veevoederbureau. Het EWpa en VREp systeem.. CVB documentatierapport No. 31 Centraal Veevoederbureau; Lelystad, The Netherlands: 2004. (In Dutch).
  18. Carter RA, McCutcheon LJ, George LA, Smith TL, Frank N, Geor RJ. Effects of diet-induced weight gain on insulin sensitivity and plasma hormone and lipid concentrations in horses.. Am. J. Vet. Res. 2009;70:1250–1258.
    doi: 10.2460/ajvr.70.10.1250pubmed: 19795940google scholar: lookup
  19. Cuervo-Arango J, Newcombe JR. Ultrasound characteristics of experimentally induced luteinized unruptured follicles (LUF) and naturally occurring hemorrhagic anovulatory follicles (HAF) in the mare.. Theriogenology. 2012;77:514–524.
  20. Stout TAE. Equine embryo transfer: Review of developing potential.. Equine Vet. J. 2010;38:467–478.
    doi: 10.2746/042516406778400529pubmed: 16986609google scholar: lookup
  21. Clark KE, Squires EL, McKinnon AO, Seidel GE Jr. Viability of stored equine embryos.. J. Anim. Sci. 1987;65:534–542.
    doi: 10.2527/jas1987.652534xpubmed: 3624099google scholar: lookup
  22. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B. Fiji: An open-source platform for biological-image analysis.. Nat. Methods. 2012;9:676–682.
    doi: 10.1038/nmeth.2019pmc: PMC3855844pubmed: 22743772google scholar: lookup
  23. Gibson C, de Ruijter-Villani M, Stout TAE. Negative uterine asynchrony retards early equine conceptus development and upregulation of placental imprinted genes.. Placenta. 2017;57:175–182.
  24. Shan G, Wang W. ExactCIdiff: An R Package for Computing Exact Confidence Intervals for the Difference of Two Proportions.. R J. 2013;5:62–71.
    doi: 10.32614/RJ-2013-026google scholar: lookup
  25. Sleutjens J, Serra Bragança FM, van Empelen MW, ten Have RE, de Zwaan J, Roelfsema E, Oosterlinck M, Back W. Mouldable, thermoplastic, glue-on frog-supportive shoes change hoof kinetics in normal and obese Shetland ponies.. Equine Vet. J. 2018;50:684–689.
    doi: 10.1111/evj.12814pmc: PMC6099505pubmed: 29356062google scholar: lookup
  26. Ginther OJ, Gastal MO, Gastal EL, Jacob JC, Beg MA. Induction of haemorrhagic anovulatory follicles in mares.. Reprod. Fertil. Dev. 2008;20:947–954.
    doi: 10.1071/RD08136pubmed: 19007559google scholar: lookup
  27. Bamford NJ. Effect of increased adiposity on insulin sensitivity and adipokine concentrations in different equine breeds adapted to cereal-rich or fat-rich meals.. Vet. J. 2016;214:14–20.
    doi: 10.1016/j.tvjl.2016.02.002pubmed: 27387720google scholar: lookup
  28. De Laat MA. Equine hyperinsulinemia: Investigation of the enteroinsular axis during insulin dysregulation.. Am. J. Physiol. Endocrinol. Metab. 2015;310:E61–E72.
    doi: 10.1152/ajpendo.00362.2015pubmed: 26530154google scholar: lookup
  29. Blache D, Chagas LM, Blackberry MA, Vercoe PE, Martin GB. Metabolic factors affecting the reproductive axis in male sheep.. J. Reprod. Fertil. 2000;120:1–11.
    doi: 10.1530/jrf.0.1200001pubmed: 11006140google scholar: lookup
  30. Sessions-Bresnahan DR, Carnevale EM. The effect of equine metabolic syndrome on the ovarian follicular environment.. J. Anim. Sci. 2014;92:1485–1494.
    doi: 10.2527/jas.2013-7275pubmed: 24663160google scholar: lookup
  31. Sessions-Bresnahan DR, Schauer KL, Heuberger AL, Carnevale EM. Effect of Obesity on the Preovulatory Follicle and Lipid Fingerprint of Equine Oocytes.. Biol. Reprod. 2016;94:15.
    doi: 10.1095/biolreprod.115.130187pubmed: 26632608google scholar: lookup
  32. Laskowski D, Båge R, Humblot P, Andersson G, Sirard M-A, Sjunnesson Y. Insulin during in vitro oocyte maturation has an impact on development, mitochondria, and cytoskeleton in bovine day 8 blastocysts.. Theriogenology. 2017;101:15–25.
  33. Lange Consiglio A, Dell’Aquila ME, Fiandanese N, Ambruosi B, Cho YS, Bosi G, Arrighi S, Lacalandra GM, Cremonesi F. Effects of leptin on in vitro maturation, fertilization and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse.. Reprod. Biol. Endocrinol. 2009;7:113.
    doi: 10.1186/1477-7827-7-113pmc: PMC2774312pubmed: 19835605google scholar: lookup
  34. Kšiňanová M, Čikoš Š, Babel’Ová J, Šefčíková Z, Špirková A, Koppel J, Fabian D. The Responses of Mouse Preimplantation Embryos to Leptin In Vitro in a Transgenerational Model for Obesity.. Front. Endocrinol. 2017;8:233.
    doi: 10.3389/fendo.2017.00233pmc: PMC5604062pubmed: 28959235google scholar: lookup

Citations

This article has been cited 3 times.
  1. Hallman I, Karikoski N, Kareskoski M. The effects of obesity and insulin dysregulation on mare reproduction, pregnancy, and foal health: a review. Front Vet Sci 2023;10:1180622.
    doi: 10.3389/fvets.2023.1180622pubmed: 37152686google scholar: lookup
  2. D' Fonseca NMM, Gibson CME, van Doorn DA, Roelfsema E, de Ruijter-Villani M, Stout TAE. Effect of Overfeeding Shetland Pony Mares on Embryonic Glucose and Lipid Accumulation, and Expression of Imprinted Genes. Animals (Basel) 2021 Aug 26;11(9).
    doi: 10.3390/ani11092504pubmed: 34573470google scholar: lookup
  3. Benammar A, Derisoud E, Vialard F, Palmer E, Ayoubi JM, Poulain M, Chavatte-Palmer P. The Mare: A Pertinent Model for Human Assisted Reproductive Technologies?. Animals (Basel) 2021 Aug 4;11(8).
    doi: 10.3390/ani11082304pubmed: 34438761google scholar: lookup