Analyze Diet
Veterinary research communications2023; 47(4); 2221-2228; doi: 10.1007/s11259-023-10122-0

Lipid metabolites, interleukin-6 and oxidative stress markers in follicular fluid and their association with serum concentrations in mares.

Abstract: The application of trans-vaginal ovum pick up (OPU) and intracytoplasmic sperm injection (ICSI) is well established for commercial in vitro embryo production in horses. These assisted reproductive techniques are especially applied during the non-breeding season of the mare. However, little is known about how the health of the oocyte donor may affect the biochemical composition of the follicular fluid (FF) in small and medium-sized follicles routinely aspirated during OPU. This study aimed to investigate associations between systemic and FF concentrations of interleukin-6 (IL-6), total cholesterol, triglycerides, non-esterified fatty acids (NEFA), reactive oxygen metabolites (d-ROMs), biological antioxidant potential (BAP), and oxidative stress index (OSI) during the non-breeding season in mares. At the slaughterhouse, serum and FF of small (5-10 mm in diameter), medium (> 10-20 mm in diameter), and large (> 20-30 mm in diameter) follicles were sampled from 12 healthy mares. There was a strong positive association (P < 0.01) between the concentration of IL-6 in serum and those measured in small (r = 0.846), medium (r = 0.999), and large (r = 0.996) follicles. Serum concentrations of NEFA were positively correlated (P < 0.05) with those measured in small (r = 0.726), medium (r = 0.720), and large (r = 0.974) follicles. Values of total cholesterol and OSI in serum and medium follicles were significantly associated (r = 0.736 and r = 0.696, respectively). The serum concentrations of all lipid metabolites were markedly higher than those measured in FF of small- and medium-sized follicles. Values of IL-6 and OSI did not change significantly between serum and all follicle classes (P ≥ 0.05). To conclude, changes in the blood composition associated with inflammation, oxidative stress, and disturbed lipid metabolism of mares may lead to an inadequate oocyte microenvironment, which could affect oocyte quality and the success rate of OPU/ICSI programs. Further research should indicate whether these changes may ultimately affect in vitro oocyte developmental capacity and subsequent embryo quality.
Publication Date: 2023-04-14 PubMed ID: 37055645PubMed Central: 8625323DOI: 10.1007/s11259-023-10122-0Google 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.

The research article investigates the relationship between the overall health of an oocyte donor horse and the biochemical composition of the follicular fluid within the oocytes, which are extracted for in vitro fertilization using trans-vaginal ovum pick up (OPU) and intracytoplasmic sperm injection (ICSI). The study finds that any changes in the horse’s blood — specifically regarding inflammation, oxidative stress, and disrupted lipid metabolism — could potentially compromise the quality of the oocytes and the overall success of in vitro fertilization.

Objective and Methodology

  • The study aimed to explore the associations between biochemical constituents within a horse’s system and the follicular fluid of the oocytes specifically targeting cholesterol, non-esterified fatty acids (NEFA), interleukin-6 (IL-6), oxidative stress index (OSI), triglycerides, reactive oxygen metabolites (d-ROMs), and biological antioxidant potential (BAP).
  • Serum and follicular fluid samples were collected from small, medium, and large follicles from 12 healthy mares that were brought to a slaughterhouse. The sample collection was carried out during the non-breeding season.

Findings

  • There was a significant association found between the concentration of IL-6 in blood serum and that in small, medium, and large follicles. A similar association was found between NEFA concentrations in blood serum and follicles.
  • The total cholesterol and OSI values in the serum were significantly associated with those in medium follicles.
  • The serum concentrations of all lipid metabolites were noticeably higher than those measured in the follicular fluid of small- and medium-sized follicles.
  • No significant differences were noticed in IL-6 and OSI concentrations between serum and all follicle classes.

Conclusion

  • The research concluded that disturbances in a mare’s blood composition in relation to inflammation, oxidative stress, or lipid metabolism could potentially create an inadequate microenvironment for the oocyte, thereby affecting the quality of the oocyte and the success of in vitro fertilization programs.
  • Further investigation is necessary to fully understand how these changes could possibly influence the in vitro developmental capacity of an oocyte and the resultant quality of embryos.

Cite This Article

APA
Hedia M, Leroy JLMR, Govaere J, Van Soom A, Smits K. (2023). Lipid metabolites, interleukin-6 and oxidative stress markers in follicular fluid and their association with serum concentrations in mares. Vet Res Commun, 47(4), 2221-2228. https://doi.org/10.1007/s11259-023-10122-0

Publication

ISSN: 1573-7446
NlmUniqueID: 8100520
Country: Switzerland
Language: English
Volume: 47
Issue: 4
Pages: 2221-2228

Researcher Affiliations

Hedia, Mohamed
  • Gamete Research Centre, Department of Veterinary Sciences, University of Antwerp, Wilrijk, Belgium. mohammedhedia@cu.edu.eg.
  • Theriogenology Department, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt. mohammedhedia@cu.edu.eg.
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium. mohammedhedia@cu.edu.eg.
Leroy, Jo L M R
  • Gamete Research Centre, Department of Veterinary Sciences, University of Antwerp, Wilrijk, Belgium.
Govaere, Jan
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Van Soom, Ann
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Smits, Katrien
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.

MeSH Terms

  • Horses
  • Animals
  • Female
  • Male
  • Follicular Fluid / chemistry
  • Follicular Fluid / metabolism
  • Interleukin-6 / analysis
  • Interleukin-6 / metabolism
  • Fatty Acids, Nonesterified / analysis
  • Fatty Acids, Nonesterified / metabolism
  • Semen
  • Oxidative Stress
  • Cholesterol / analysis
  • Cholesterol / metabolism
  • Oocytes / metabolism

References

This article includes 48 references
  1. Adamczak R, Ukleja-Sokołowska N, Lis K, Dubiel M. Function of follicular cytokines: roles played during maturation, development and implantation of embryo.. Medicina 57(11):1251.
    doi: 10.3390/medicina57111251pubmed: 34833469pmc: 8625323google scholar: lookup
  2. Annes K, Müller DB, Vilela JA, Valente RS, Caetano DP, Cibin FW, Milazzotto MP, Mesquita FS, Belaz KRA, Eberlin MN, Sudano MJ. Influence of follicle size on bovine oocyte lipid composition, follicular metabolic and stress markers, embryo development and blastocyst lipid content.. Reprod Fertil Dev 31(3):462–472.
    doi: 10.1071/rd18109pubmed: 30282571google scholar: lookup
  3. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus–oocyte complex gene-expression profile.. Hum Reprod 21(7):1705–1719.
    doi: 10.1093/humrep/del065pubmed: 16571642google scholar: lookup
  4. Bertoldo M, Nadal-Desbarats L, Gérard N, Dubois A, Holyoake PK, Grupen CG. Differences in the metabolomic signatures of porcine follicular fluid collected from environments associated with good and poor oocyte quality.. Reproduction 146(3):221–231.
    doi: 10.1530/REP-13-0142pubmed: 23801780google scholar: lookup
  5. Burton AB, Wagner B, Erb HN, Ainsworth DM. Serum interleukin-6 (IL-6) and IL-10 concentrations in normal and septic neonatal foals.. Vet Immunol Immunopathol 132(2–4):122–128.
    doi: 10.1016/j.vetimm.2009.05.006pubmed: 19501415google scholar: lookup
  6. Catandi GD, LiPuma L, Obeidat YM, Maclellan LJ, Broeckling CD, Chen T, Chicco AJ, Caenevale EM. Oocyte metabolic function, lipid composition, and developmental potential are altered by diet in older mares.. Reproduction 163(4):183–198.
    doi: 10.1530/REP-21-0351pubmed: 37379450pmc: 8942336google scholar: lookup
  7. Chaube SK, Prasad PV, Thakur SC, Shrivastav TG. Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro.. Apoptosis 10(4):863–874.
    doi: 10.1007/s10495-005-0367-8pubmed: 16133876google scholar: lookup
  8. Chen CD, Chen HF, Lu HF, Chen SU, Ho HN, Yang YS. Value of serum and follicular fluid cytokine profile in the prediction of moderate to severe ovarian hyperstimulation syndrome.. Hum Reprod 15(5):1037–1042.
    doi: 10.1093/humrep/15.5.1037pubmed: 10783347google scholar: lookup
  9. Claes A, Stout TAE. Success rate in a clinical equine in vitro embryo production program.. Theriogenology 187:215–218.
  10. Claes A, Cuervo-Arango J, Van Den Broek J, Galli C, Colleoni S, Lazzari G, Deelen C, Beitsma M, Stout TA. Factors affecting the likelihood of pregnancy and embryonic loss after transfer of cryopreserved in vitro produced equine embryos.. Equine Vet J 51(4):446–450.
    doi: 10.1111/evj.13028pubmed: 30269336google scholar: lookup
  11. Cuervo-Arango J, Claes AN, Stout TA. Mare and stallion effects on blastocyst production in a commercial equine ovum pick-up–intracytoplasmic sperm injection program.. Reprod Fertil Dev 31(12):1894–1903.
    doi: 10.1071/rd19201pubmed: 31634435google scholar: lookup
  12. da Silveira JC, Winger QA, Bouma GJ, Carnevale EM. Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-β signalling during follicle development in the mare.. Reprod Fertil Devel 27(6):897–905.
    doi: 10.1071/rd14452google scholar: lookup
  13. Deura I, Harada T, Taniguchi F, Iwabe T, Izawa M, Terakawa N. Reduction of estrogen production by interleukin-6 in a human granulosa tumor cell line may have implications for endometriosis-associated infertility.. Fertil Steril 83(4):1086–1092.
  14. Di Rosa A, Albani E, Morenghi E, Iommiello VM, Levi Setti PE. A new method to assess oxidative stress in ART cycles.. Gynecol Endocrinol 32(3):210–212.
    doi: 10.3109/09513590.2015.1110134pubmed: 26608547google scholar: lookup
  15. Dunning KR, Russell DL, Robker RL. Lipids and oocyte developmental competence: the role of fatty acids and b-oxidation.. Reproduction 148(1):R15–R27.
    doi: 10.1530/REP-13-0251pubmed: 24760880google scholar: lookup
  16. El-Shahat KH, Abo-El Maaty AM, Moawad AR. Follicular fluid composition in relation to follicular size in pregnant and non-pregnant dromedary camels (Camelus dromedaries).. Anim Reprod 10(1):16–23.
  17. Field SL, Dasgupta T, Cummings M, Orsi NM. Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation.. Mol Reprod Dev 81(4):284–314.
    doi: 10.1002/mrd.22285pubmed: 24273059google scholar: lookup
  18. Galli C, Duchi R, Colleoni S, Lagutina I, Lazzari G. Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice.. Theriogenology 81(1):138–151.
  19. Hatirnaz Ş, Ata B, Hatirnaz ES, Dahan MH, Tannus S, Tan J, Tan SL. Oocyte in vitro maturation: a sytematic review.. Turk J Obstet Gynecol 15(2):112–125.
    doi: 10.4274/tjod.23911pubmed: 29971189pmc: 6022428google scholar: lookup
  20. Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet J 15(4):371–372.
  21. Hinrichs K. In vitro production of equine embryos: state of the art.. Reprod Domest Anim 45(s2):3–8.
  22. Hinrichs K, Schmidt AL. Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season.. Biol Reprod 62(5):1402–1408.
    doi: 10.1095/biolreprod62.5.1402pubmed: 10775193google scholar: lookup
  23. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Ismail S, El-Belely M. Alterations in the expression profile of serum miR-155, miR-223, miR-17, miR-200a, miR-205, as well as levels of interleukin 6, and prostaglandins during endometritis in arabian mares.. Vet Sci 8(6):98.
    doi: 10.3390/vetsci8060098pubmed: 34199703pmc: 8227551google scholar: lookup
  24. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Sosa AS, Saber YHA, Hasanain MH, Nawito MF, Seidel GE. Extracellular vesicles in low volume uterine lavage and serum: novel and promising biomarker for endometritis in arabian mares.. BMC Vet Res 18(1):1–12.
  25. Jungheim ES, Macones GA, Odem RR, Patterson BW, Lanzendorf SE, Ratts VS, Moley KH. Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization.. Fertil Steril 95(6):1970–1974.
  26. Junior ARP, van Tilburg MF, Lobo MD, Monteiro-Moreira AC, Moreira RA, Melo CH, Souza-Fabjan JMG, Araújo AA, Melo LM, Teixeira DIA, Moura AA, Freitas VJF. Proteomic analysis of follicular fluid from tropically-adapted goats.. Anim Reprod Sci 188:35–44.
  27. Lazzari G, Colleoni S, Crotti G, Turini P, Fiorini G, Barandalla M, Landriscina L, Dolci G, Benedetti M, Duchi R, Galli C. Laboratory production of equine embryos.. J Equine Vet Sci 89:103097.
    doi: 10.1016/j.jevs.2020.103097pubmed: 32563445google scholar: lookup
  28. Leroy JLMR, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.. Reproduction 130(4):48–95.
    doi: 10.1530/rep.1.00735google scholar: lookup
  29. Lin J, Wang L. Oxidative stress in oocytes and embryo development: implications for in vitro systems.. Antioxid Redox Signal 34(17):1394–1406.
    doi: 10.1089/ars.2020.8209google scholar: lookup
  30. Liu T, Qu J, Tian M, Yang R, Song X, Li R, Yan J, Qiao J. Lipid metabolic process involved in oocyte maturation during folliculogenesis.. Front Cell Dev Biol 10:806890.
    doi: 10.3389/fcell.2022.806890pubmed: 35433675pmc: 9009531google scholar: lookup
  31. Luti S, Fiaschi T, Magherini F, Modesti PA, Piomboni P, Semplici B, Morgante G, Amoresano A, Illiano A, Pinto G, Modesti A, Gamberi T. Follicular microenvironment: oxidative stress and adiponectin correlated with steroids hormones in women undergoing in vitro fertilization.. Mol Reprod Dev 88(2):175–184.
    doi: 10.1002/mrd.23447pubmed: 33336494google scholar: lookup
  32. Marei WF, Van den Bosch L, Pintelon I, Mohey-Elsaeed O, Bols PE, Leroy JL. Mitochondria-targeted therapy rescues development and quality of embryos derived from oocytes matured under oxidative stress conditions: a bovine in vitro model.. Hum Reprod 34(10):1984–1998.
    doi: 10.1093/humrep/dez161pubmed: 31625574google scholar: lookup
  33. Papas M, Govaere J, Peere S, Gerits I, Van de Velde M, Angel-Velez D, De Coster T, Van Soom A, Smits K. Anti-müllerian hormone and OPU-ICSI outcome in the mare.. animals 11(7):2004.
    doi: 10.3390/ani11072004google scholar: lookup
  34. Piccinni MP, Vicenti R, Logiodice F, Fabbri R, Kullolli O, Pallecchi M, Paradisi R, Danza G, Macciocca M, Lombardelli L, Seracchioli R. Description of the follicular fluid cytokine and hormone profiles in human physiological natural cycles.. J Clin Endocrinol Metab 106(2):e721–e738.
    doi: 10.1210/clinem/dgaa880pubmed: 33247906google scholar: lookup
  35. Satué K, Fazio E, Ferlazzo A, Medica P. Hematochemical patterns in follicular fluid and blood stream in cycling mares: a comparative note.. J Equine Vet Sci 80:20–26.
    doi: 10.1016/j.jevs.2019.06.016pubmed: 31443828google scholar: lookup
  36. Satué K, Fazio E, Medica P. Can the presence of ovarian corpus luteum modify the hormonal composition of follicular fluid in mares?. animals 10(4):646.
    doi: 10.3390/ani10040646google scholar: lookup
  37. Sessions-Bresnahan DR, Carnevale EM. The effect of equine metabolic syndrome on the ovarian follicular environment.. J Anim Sci 92(4):1485–1494.
    doi: 10.2527/jas.2013-7275pubmed: 24663160google scholar: lookup
  38. Sessions-Bresnahan DR, Schauer KL, Heuberger AL, Carnevale EM. Effect of obesity on the preovulatory follicle and lipid fingerprint of equine oocytes.. Biol Reprod 94(1):1–12.
  39. Sessions-Bresnahan DR, Heuberger AL, Carnevale EM. Obesity in mares promotes uterine inflammation and alters embryo lipid fingerprints and homeostasis.. Biol Reprod 99(4):761–772.
    doi: 10.1093/biolre/ioy107pubmed: 29741587google scholar: lookup
  40. Shono S, Gin A, Minowa F, Okubo K, Mochizuki M. The oxidative stress markers of horses—the comparison with other animals and the influence of exercise and disease.. animals 10(4):617.
    doi: 10.3390/ani10040617google scholar: lookup
  41. Tamura K, Kawaguchi T, Kogo H. Interleukin-6 inhibits the expression of luteinizing hormone receptor mRNA during the maturation of cultured rat granulosa cells.. J Endocrinol 170(1):121–127.
    doi: 10.1677/joe.0.1700121pubmed: 11431144google scholar: lookup
  42. Tarin JJ, Vendrell FJ, Ten J, Blanes R, Van Blerkom J, Cano A. The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes.. Mol Hum Reprod 2(12):895–901.
    doi: 10.1093/molehr/2.12.895pubmed: 9237232google scholar: lookup
  43. Terao H, Wada-Hiraike O, Nagumo A, Kunitomi C, Azhary JM, Harada M, Hirata T, Hirota Y, Koga K, Fuji T, Osuga Y. Role of oxidative stress in follicular fluid on embryos of patients undergoing assisted reproductive technology treatment.. J Obstet Gynaecol Res 45(9):1884–1891.
    doi: 10.1111/jog.14040pubmed: 31257684google scholar: lookup
  44. Valckx SD, Arias-Alvarez M, De Pauw I, Fievez V, Vlaeminck B, Fransen E, Bols PE, Leroy JL. Fatty acid composition of the follicular fluid of normal weight, overweight and obese women undergoing assisted reproductive treatment: a descriptive cross-sectional study.. Reprod Biol Endocrinol 12(1):1–11.
    doi: 10.1186/1477-7827-12-13google scholar: lookup
  45. Valckx SD, Van Hoeck V, Arias-Alvarez M, Maillo V, Lopez-Cardona AP, Gutierrez-Adan A, Berth M, Cortvrindt R, Bols PE, Leroy JL. Elevated non-esterified fatty acid concentrations during in vitro murine follicle growth alter follicular physiology and reduce oocyte developmental competence.. Fertil Steril 102(6):1769–1776.
  46. Wu LLY, Dunning KR, Yang X, Russell DL, Lane M, Norman RJ, Robker RL. High-fat diet causes lipotoxicity responses in cumulus–oocyte complexes and decreased fertilization rates.. Endocrinology 151(11):5438–5445.
    doi: 10.1210/en.2010-adma0551pubmed: 20861227google scholar: lookup
  47. Yesilaltay A, Dokshin GA, Busso D, Wang L, Galiani D, Chavarria T, Vasile E, Quilaqueo L, Orellana JA, Walzer D, Shalgi R, Dekel N, Albertini DF, Rigotti A, Page DC, Krieger M. Excess cholesterol induces mouse egg activation and may cause female infertility.. Proc Natl Acad Sci 111(46):E4972–E4980.
    doi: 10.1073/pnas.1418954111pubmed: 25368174pmc: 4246315google scholar: lookup
  48. Zhang X, Wu XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles.. Cell Res 16(10):841–850.
    doi: 10.1038/sj.cr.7310095pubmed: 16983401google scholar: lookup