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PloS one2016; 11(2); e0149693; doi: 10.1371/journal.pone.0149693

The Mare Model to Study the Effects of Ovarian Dynamics on Preantral Follicle Features.

Abstract: Ovarian tissue collected by biopsy procedures allows the performance of many studies with clinical applications in the field of female fertility preservation. The aim of the present study was to investigate the influence of reproductive phase (anestrous vs. diestrous) and ovarian structures (antral follicles and corpus luteum) on the quality, class distribution, number, and density of preantral follicles, and stromal cell density. Ovarian fragments were harvested by biopsy pick-up procedures from mares and submitted to histological analysis. The mean preantral follicle and ovarian stromal cell densities were greater in the diestrous phase and a positive correlation of stromal cell density with the number and density of preantral follicles was observed. The mean area (mm2) of ovarian structures increased in the diestrous phase and had positive correlations with number of preantral follicles, follicle density, and stromal cell density. Biopsy fragments collected from ovaries containing an active corpus luteum had a higher follicle density, stromal cell density, and proportion of normal preantral follicles. In conclusion, our results showed: (1) the diestrous phase influenced positively the preantral follicle quality, class distribution, and follicle and stromal cell densities; (2) the area of ovarian structures was positively correlated with the follicle and stromal cell densities; and (3) the presence of an active corpus luteum had a positive effect on the quality of preantral follicles, and follicle and stromal densities. Therefore, herein we demonstrate that the presence of key ovarian structures favors the harvest of ovarian fragments containing an appropriate number of healthy preantral follicles.
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Publication Date: 2016-02-22 PubMed ID: 26900687PubMed Central: PMC4762659DOI: 10.1371/journal.pone.0149693Google Scholar: Lookup
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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 study investigates how different phases of the reproductive cycle and ovarian structures impact the quality and density of preantral follicles, which are crucial for female fertility, in samples collected from mares. The findings suggest that the diestrous phase and the presence of an active corpus luteum positively influence follicle quality, density, and division.

Objective of the Study

  • The research was aimed at understanding the influence of different stages of the reproductive cycle (anestrous vs. diestrous) and the presence of particular ovarian structures (antral follicles and corpus luteum) on the quality, classification, number, and concentration of preantral follicles — immature ovarian follicles that are vital for fertility.

Methodology

  • The scientists obtained ovarian fragments from mares through biopsy pick-up procedures for histological analysis (the study of the microscopic structure of tissues).

Findings

  • The analysis found that the average density of preantral follicles and ovarian stromal cells (connective tissue cells) was higher during the diestrous phase of the reproductive cycle, when the uterus prepares for potential implantation of a fertilized egg.
  • Positive correlations were observed between stromal cell density and the number as well as density of preantral follicles.
  • The average size (in mm²) of ovarian structures increased during the diestrous phase, which was positively correlated with the number and density of preantral follicles and stromal cell density.
  • Ovarian fragments collected from ovaries with an active corpus luteum had a higher density of follicles, stromal cells, and proportion of normal (healthy) preantral follicles.

Conclusion

  • The research concludes that the phase of the reproductive cycle and the presence of an active corpus luteum (a temporary gland formed after ovulation) have a positive impact on the quality and density of preantral follicles, as well as the density of stromal cells.
  • Specifically, the diestrous phase enhances the quality, distribution, and densities of preantral follicles and stromal cells.
  • The presence of larger ovarian structures leads to increased follicle and stromal cell densities.
  • The presence of an active corpus luteum improves the quality of preantral follicles, and follicle and stromal densities.
  • Therefore, the study indicates that the presence of key ovarian structures favors the collection of ovarian fragments with an appropriate number of healthy preantral follicles — an important consideration for fertility preservation strategies.

Cite This Article

APA
Alves KA, Alves BG, Gastal GD, de Tarso SG, Gastal MO, Figueiredo JR, Gambarini ML, Gastal EL. (2016). The Mare Model to Study the Effects of Ovarian Dynamics on Preantral Follicle Features. PLoS One, 11(2), e0149693. https://doi.org/10.1371/journal.pone.0149693

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 11
Issue: 2
Pages: e0149693
PII: e0149693

Researcher Affiliations

Alves, Kele A
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.
  • Center for Studies and Research in Animal Reproductive Biology, College of Veterinary and Animal Science, Federal University of Goiás, Goiânia, GO, Brazil.
Alves, Benner G
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.
Gastal, Gustavo D A
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.
de Tarso, Saulo G S
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.
Gastal, Melba O
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.
Figueiredo, José R
  • Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Fortaleza, CE, Brazil.
Gambarini, Maria L
  • Center for Studies and Research in Animal Reproductive Biology, College of Veterinary and Animal Science, Federal University of Goiás, Goiânia, GO, Brazil.
Gastal, Eduardo L
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, lllinois, United States of America.

MeSH Terms

  • Animals
  • Biopsy
  • Cell Count
  • Female
  • Horses
  • Ovarian Follicle / cytology
  • Ovarian Follicle / physiology
  • Ovary / cytology
  • Ovary / physiology
  • Stromal Cells / cytology

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 52 references
  1. Ginther OJ, Gastal EL, Gastal MO, Bergfelt DR, Baerwald AR, Pierson RA. Comparative study of the dynamics of follicular waves in mares and women.. Biol Reprod 2004 Oct;71(4):1195-201.
    pmc: PMC2891974pubmed: 15189824doi: 10.1095/biolreprod.104.031054google scholar: lookup
  2. Ginther OJ, Beg MA, Gastal EL, Gastal MO, Baerwald AR, Pierson RA. Systemic concentrations of hormones during the development of follicular waves in mares and women: a comparative study.. Reproduction 2005 Sep;130(3):379-88.
    pmc: PMC2881942pubmed: 16123245doi: 10.1530/rep.1.00757google scholar: lookup
  3. Carnevale EM. The mare model for follicular maturation and reproductive aging in the woman.. Theriogenology 2008 Jan 1;69(1):23-30.
    pubmed: 17976712doi: 10.1016/j.theriogenology.2007.09.011google scholar: lookup
  4. Mihm M, Evans AC. Mechanisms for dominant follicle selection in monovulatory species: a comparison of morphological, endocrine and intraovarian events in cows, mares and women.. Reprod Domest Anim 2008 Jul;43 Suppl 2:48-56.
    pubmed: 18638104doi: 10.1111/j.1439-0531.2008.01142.xgoogle scholar: lookup
  5. Baerwald AR. Human antral folliculogenesis: what we have learned from the bovine and equine models.. Anim Reprod 2009; 6:20–29.
  6. Baerwald AR, Walker RA, Pierson RA. Growth rates of ovarian follicles during natural menstrual cycles, oral contraception cycles, and ovarian stimulation cycles.. Fertil Steril 2009 Feb;91(2):440-9.
    doi: 10.1016/j.fertnstert.2007.11.054pubmed: 18249401google scholar: lookup
  7. Gastal EL. Recent advances and new concepts on follicle and endocrine dynamics during the equine periovulatory period.. Anim Reprod 2009; 6:144–158.
  8. Gastal EL, Gastal MO, Wischral A, Davis J. The equine model to study the influence of obesity and insulin resistance in human ovarian function.. Acta Sci Vet 2011; 39:57–70.
  9. Ginther OJ. The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women.. Theriogenology 2012 Mar 15;77(5):818-28.
    doi: 10.1016/j.theriogenology.2011.09.025pubmed: 22115815google scholar: lookup
  10. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. Equine preantral follicles obtained via the Biopsy Pick-Up method: histological evaluation and validation of a mechanical isolation technique.. Theriogenology 2013 Mar 15;79(5):735-43.
    doi: 10.1016/j.theriogenology.2012.10.023pubmed: 23352704google scholar: lookup
  11. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. Quantification, morphology, and viability of equine preantral follicles obtained via the Biopsy Pick-Up method.. Theriogenology 2013 Mar 1;79(4):599-609.
    doi: 10.1016/j.theriogenology.2012.11.012pubmed: 23260865google scholar: lookup
  12. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. In vitro culture of equine preantral follicles obtained via the Biopsy Pick-Up method.. Theriogenology 2013 Apr 1;79(6):911-7.
    doi: 10.1016/j.theriogenology.2013.01.001pubmed: 23434205google scholar: lookup
  13. Alves KA, Alves BG, Rocha CD, Visonná M, Mohallem RF, Gastal MO, Jacomini JO, Beletti ME, Figueiredo JR, Gambarini ML, Gastal EL. Number and density of equine preantral follicles in different ovarian histological section thicknesses.. Theriogenology 2015 Apr 1;83(6):1048-55.
    doi: 10.1016/j.theriogenology.2014.12.004pubmed: 25628263google scholar: lookup
  14. Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and nonhuman primates.. Fertil Steril 2013 May;99(6):1523-33.
    doi: 10.1016/j.fertnstert.2013.03.043pmc: PMC3929501pubmed: 23635350google scholar: lookup
  15. Schmidt KL, Byskov AG, Nyboe Andersen A, Müller J, Yding Andersen C. Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries.. Hum Reprod 2003 Jun;18(6):1158-64.
    pubmed: 12773440doi: 10.1093/humrep/deg246google scholar: lookup
  16. Aerts JM, Oste M, Bols PE. Development and practical applications of a method for repeated transvaginal, ultrasound-guided biopsy collection of the bovine ovary.. Theriogenology 2005 Sep 1;64(4):947-57.
    pubmed: 16054498doi: 10.1016/j.theriogenology.2005.01.011google scholar: lookup
  17. Fransolet M, Labied S, Henry L, Masereel MC, Rozet E, Kirschvink N, Nisolle M, Munaut C. Strategies for using the sheep ovarian cortex as a model in reproductive medicine.. PLoS One 2014;9(3):e91073.
    doi: 10.1371/journal.pone.0091073pmc: PMC3948732pubmed: 24614306google scholar: lookup
  18. Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals.. Anim Reprod Sci 2004 Jul;82-83:431-46.
    pubmed: 15271471doi: 10.1016/j.anireprosci.2004.05.017google scholar: lookup
  19. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development.. Reproduction 2006 Aug;132(2):191-206.
    pubmed: 16885529doi: 10.1530/rep.1.01074google scholar: lookup
  20. Gerritse R, Beerendonk CC, Westphal JR, Bastings L, Braat DD, Peek R. Glucose/lactate metabolism of cryopreserved intact bovine ovaries as a novel quantitative marker to assess tissue cryodamage.. Reprod Biomed Online 2011 Dec;23(6):755-64.
    doi: 10.1016/j.rbmo.2011.08.008pubmed: 22036190google scholar: lookup
  21. Al-Gubory KH, Martinet J. Effect of the corpus luteum on ovarian follicular populations and growth in the ewe.. Anim Reprod Sci 1987; 13:269–281.
  22. Skinner MK. Regulation of primordial follicle assembly and development.. Hum Reprod Update 2005 Sep-Oct;11(5):461-71.
    pubmed: 16006439doi: 10.1093/humupd/dmi020google scholar: lookup
  23. Gupta PS, Ramesh HS, Nandi S, Ravindra JP. Recovery of large preantral follicles from buffalo ovary: effect of season and corpus luteum.. Anim Reprod Sci 2007 Sep;101(1-2):145-52.
    pubmed: 17174490doi: 10.1016/j.anireprosci.2006.11.011google scholar: lookup
  24. Yang MY, Fortune JE. Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro.. Mol Reprod Dev 2007 Sep;74(9):1095-104.
    pubmed: 17290425doi: 10.1002/mrd.20633google scholar: lookup
  25. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, Mann GE. Angiogenesis and vascular function in the ovary.. Reproduction 2009 Dec;138(6):869-81.
    doi: 10.1530/REP-09-0283pubmed: 19786399google scholar: lookup
  26. Thorne JT, Segal TR, Chang S, Jorge S, Segars JH, Leppert PC. Dynamic reciprocity between cells and their microenvironment in reproduction.. Biol Reprod 2015 Jan;92(1):25.
    pmc: PMC4434933pubmed: 25411389doi: 10.1095/biolreprod.114.121368google scholar: lookup
  27. Lass A, Silye R, Abrams DC, Krausz T, Hovatta O, Margara R, Winston RM. Follicular density in ovarian biopsy of infertile women: a novel method to assess ovarian reserve.. Hum Reprod 1997 May;12(5):1028-31.
    pubmed: 9194660doi: 10.1093/humrep/12.5.1028google scholar: lookup
  28. Kwok R, Johnson NP. Ovarian biopsy has no role as a routine diagnostic test of ovarian reserve: a systematic review.. Reprod Biomed Online 2012 May;24(5):492-5.
    doi: 10.1016/j.rbmo.2012.01.020pubmed: 22414372google scholar: lookup
  29. Vanacker J, Luyckx V, Amorim C, Dolmans MM, Van Langendonckt A, Donnez J, Camboni A. Should we isolate human preantral follicles before or after cryopreservation of ovarian tissue?. Fertil Steril 2013 Apr;99(5):1363-1368.e2.
    doi: 10.1016/j.fertnstert.2012.12.016pubmed: 23375199google scholar: lookup
  30. Jorssen EP, Langbeen A, Fransen E, Martinez EL, Leroy JL, Bols PE. Monitoring preantral follicle survival and growth in bovine ovarian biopsies by repeated use of neutral red and cultured in vitro under low and high oxygen tension.. Theriogenology 2014 Aug;82(3):387-95.
    doi: 10.1016/j.theriogenology.2014.04.019pubmed: 24877724google scholar: lookup
  31. Lass A. Assessment of ovarian reserve - is there a role for ovarian biopsy?. Hum Reprod 2001 Jun;16(6):1055-7.
    pubmed: 11387268doi: 10.1093/humrep/16.6.1055google scholar: lookup
  32. Gastal EL, Gastal MO, Bergfelt DR, Ginther OJ. Role of diameter differences among follicles in selection of a future dominant follicle in mares.. Biol Reprod 1997 Dec;57(6):1320-7.
    pubmed: 9408236doi: 10.1095/biolreprod57.6.1320google scholar: lookup
  33. Silva JR, Lucci CM, Carvalho FC, Báo SN, Costa SH, Santos RR, Figueiredo JR. Effect of coconut water and Braun-Collins solutions at different temperatures and incubation times on the morphology of goat preantral follicles preserved in vitro.. Theriogenology 2000 Sep 15;54(5):809-22.
    pubmed: 11101040doi: 10.1016/s0093-691x(00)00392-7google scholar: lookup
  34. Commin L, Buff S, Rosset E, Galet C, Allard A, Bruyere P, Joly T, Guérin P, Neto V. Follicle development in cryopreserved bitch ovarian tissue grafted to immunodeficient mouse.. Reprod Fertil Dev 2012;24(3):461-71.
    doi: 10.1071/RD11166pubmed: 22401278google scholar: lookup
  35. Forabosco A, Sforza C. Establishment of ovarian reserve: a quantitative morphometric study of the developing human ovary.. Fertil Steril 2007 Sep;88(3):675-83.
    pubmed: 17434504doi: 10.1016/j.fertnstert.2006.11.191google scholar: lookup
  36. Fortune JE. The early stages of follicular development: activation of primordial follicles and growth of preantral follicles.. Anim Reprod Sci 2003 Oct 15;78(3-4):135-63.
    pubmed: 12818642doi: 10.1016/s0378-4320(03)00088-5google scholar: lookup
  37. Donadeu FX, Watson ED. Seasonal changes in ovarian activity: lessons learnt from the horse.. Anim Reprod Sci 2007 Aug;100(3-4):225-42.
    pubmed: 17207590doi: 10.1016/j.anireprosci.2006.12.001google scholar: lookup
  38. Thomas FH, Walters KA, Telfer EE. How to make a good oocyte: an update on in-vitro models to study follicle regulation.. Hum Reprod Update 2003 Nov-Dec;9(6):541-55.
    pubmed: 14714591doi: 10.1093/humupd/dmg042google scholar: lookup
  39. Araújo VR, Gastal MO, Figueiredo JR, Gastal EL. In vitro culture of bovine preantral follicles: a review.. Reprod Biol Endocrinol 2014 Aug 13;12:78.
    doi: 10.1186/1477-7827-12-78pmc: PMC4148547pubmed: 25117631google scholar: lookup
  40. Faustino LR, Santos RR, Silva CM, Pinto LC, Celestino JJ, Campello CC, Figueiredo JR, Rodrigues AP. Goat and sheep ovarian tissue cryopreservation: Effects on the morphology and development of primordial follicles and density of stromal cell.. Anim Reprod Sci 2010 Oct;122(1-2):90-7.
    doi: 10.1016/j.anireprosci.2010.08.001pubmed: 20800393google scholar: lookup
  41. Tingen CM, Kiesewetter SE, Jozefik J, Thomas C, Tagler D, Shea L, Woodruff TK. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro.. Reproduction 2011 Jun;141(6):809-20.
    doi: 10.1530/REP-10-0483pmc: PMC4077622pubmed: 21389078google scholar: lookup
  42. Dath C, Dethy A, Van Langendonckt A, Van Eyck AS, Amorim CA, Luyckx V, Donnez J, Dolmans MM. Endothelial cells are essential for ovarian stromal tissue restructuring after xenotransplantation of isolated ovarian stromal cells.. Hum Reprod 2011 Jun;26(6):1431-9.
    doi: 10.1093/humrep/der073pubmed: 21421662google scholar: lookup
  43. Palermo R. Differential actions of FSH and LH during folliculogenesis.. Reprod Biomed Online 2007 Sep;15(3):326-37.
    pubmed: 17854533doi: 10.1016/s1472-6483(10)60347-1google scholar: lookup
  44. Orisaka M, Tajima K, Tsang BK, Kotsuji F. Oocyte-granulosa-theca cell interactions during preantral follicular development.. J Ovarian Res 2009 Jul 9;2(1):9.
    doi: 10.1186/1757-2215-2-9pmc: PMC2715405pubmed: 19589134google scholar: lookup
  45. Young JM, McNeilly AS. Theca: the forgotten cell of the ovarian follicle.. Reproduction 2010 Oct;140(4):489-504.
    doi: 10.1530/REP-10-0094pubmed: 20628033google scholar: lookup
  46. Qiu M, Quan F, Han C, Wu B, Liu J, Yang Z, Su F, Zhang Y. Effects of granulosa cells on steroidogenesis, proliferation and apoptosis of stromal cells and theca cells derived from the goat ovary.. J Steroid Biochem Mol Biol 2013 Nov;138:325-33.
    doi: 10.1016/j.jsbmb.2013.06.005pubmed: 23816690google scholar: lookup
  47. Gao J, Yandong W, Yaxin F, Xuenqing W, Yong G, Liyun G. Relationship between situation of the bovine ovarian corpus luteum and the numbers of isolated preantral follicles from them.. Chin J Vet Sci 2001; 21:181–183.
  48. Auletta FJ, Flint AP. Human ovarian oxytocin and steroid hormones.. Am J Obstet Gynecol 1987 Oct;157(4 Pt 1):1010-11.
    pubmed: 3674143doi: 10.1016/s0002-9378(87)80107-2google scholar: lookup
  49. Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW. Mechanisms controlling the function and life span of the corpus luteum.. Physiol Rev 2000 Jan;80(1):1-29.
    pubmed: 10617764doi: 10.1152/physrev.2000.80.1.1google scholar: lookup
  50. Kezele P, Skinner MK. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly.. Endocrinology 2003 Aug;144(8):3329-37.
    pubmed: 12865310doi: 10.1210/en.2002-0131google scholar: lookup
  51. Al-zi'abi MO, Watson ED, Fraser HM. Angiogenesis and vascular endothelial growth factor expression in the equine corpus luteum.. Reproduction 2003 Feb;125(2):259-70.
    pubmed: 12578540
  52. Martelli A, Palmerini MG, Russo V, Rinaldi C, Bernabò N, Di Giacinto O, Berardinelli P, Nottola SA, Macchiarelli G, Barboni B. Blood vessel remodeling in pig ovarian follicles during the periovulatory period: an immunohistochemistry and SEM-corrosion casting study.. Reprod Biol Endocrinol 2009 Jul 16;7:72.
    doi: 10.1186/1477-7827-7-72pmc: PMC2720392pubmed: 19607713google scholar: lookup

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  1. Brandão FA, de Brito DC, Pereira LM, Alves KA, Ñaupas LV, de Souza SS, de S Cunha DM, de S Filho RP, Alves BG, Rodrigues AP, Teixeira DI. Effects of different subcutaneous sites on heterotopic autotransplantation of canine ovarian tissue. Vet Res Commun 2023 May 18;.
    doi: 10.1007/s11259-023-10139-5pubmed: 37198523google scholar: lookup
  2. Hyde KA, Aguiar FLN, Alvarenga PB, Rezende AL, Alves BG, Alves KA, Gastal GDA, Gastal MO, Gastal EL. Characterization of preantral follicle clustering and neighborhood patterns in the equine ovary. PLoS One 2022;17(10):e0275396.
    doi: 10.1371/journal.pone.0275396pubmed: 36194590google scholar: lookup
  3. Hyde KA, Aguiar FLN, Alves BG, Alves KA, Gastal GDA, Gastal MO, Gastal EL. Preantral follicle population and distribution in the horse ovary. Reprod Fertil 2022 Apr 1;3(2):90-102.
    doi: 10.1530/RAF-21-0100pubmed: 35706578google scholar: lookup
  4. U-Krit W, Wadsungnoen S, Yama P, Jitjumnong J, Sangkate M, Promsao N, Montha N, Sudwan P, Mektrirat R, Panatuk J, Inyawilert W, Intawicha P, Tang PC, Moonmanee T. Understanding the Ovarian Interrelationship with Low Antral Follicle Counts (AFC) in the In Vivo Bos indicus Cow Model: Unilateral and Bilateral Main AFC as Possible Biomarkers of Ovarian Response to Hormonal Synchronisation. Biology (Basel) 2022 Mar 29;11(4).
    doi: 10.3390/biology11040523pubmed: 35453722google scholar: lookup
  5. Souza SS, Aguiar FLN, Alves BG, Alves KA, Brandão FAS, Brito DCC, Raposo RDS, Gastal MO, Rodrigues APR, Figueiredo JR, Teixeira DÍA, Gastal EL. Equine ovarian tissue xenografting: impacts of cooling, vitrification, and VEGF. Reprod Fertil 2021 Dec;2(4):251-266.
    doi: 10.1530/RAF-21-0008pubmed: 35118403google scholar: lookup
  6. Pemayun TGO, Mustofa I, Mahaputra L, Hermadi HA, Wijaya NMR, Mulyati S, Utama S, Restiadi TI, Rimayanti R. Fertility restoration of racing mare with persistent corpus luteum. Vet World 2021 Sep;14(9):2356-2361.
    doi: 10.14202/vetworld.2021.2356-2361pubmed: 34840454google scholar: lookup
  7. Kornicka-Garbowska K, Bourebaba L, Röcken M, Marycz K. Sex Hormone Binding Globulin (SHBG) Mitigates ER Stress in Hepatocytes In Vitro and Ex Vivo. Cells 2021 Mar 30;10(4).
    doi: 10.3390/cells10040755pubmed: 33808055google scholar: lookup
  8. Souza SS, Alves BG, Alves KA, Brandão FAS, Brito DCC, Gastal MO, Rodrigues APR, Figueireod JR, Teixeira DIA, Gastal EL. Heterotopic autotransplantation of ovarian tissue in a large animal model: Effects of cooling and VEGF. PLoS One 2020;15(11):e0241442.
    doi: 10.1371/journal.pone.0241442pubmed: 33147235google scholar: lookup
  9. Satué K, Fazio E, Medica P. Can the Presence of Ovarian Corpus Luteum Modify the Hormonal Composition of Follicular Fluid in Mares?. Animals (Basel) 2020 Apr 9;10(4).
    doi: 10.3390/ani10040646pubmed: 32283596google scholar: lookup
  10. Alves BG, Alves KA, Gastal GDA, Gastal MO, Figueiredo JR, Gastal EL. Spatial distribution of preantral follicles in the equine ovary. PLoS One 2018;13(6):e0198108.
    doi: 10.1371/journal.pone.0198108pubmed: 29897931google scholar: lookup
  11. Gastal GDA, Hamilton A, Alves BG, de Tarso SGS, Feugang JM, Banz WJ, Apgar GA, Nielsen CK, Gastal EL. Ovarian features in white-tailed deer (Odocoileus virginianus) fawns and does. PLoS One 2017;12(5):e0177357.
    doi: 10.1371/journal.pone.0177357pubmed: 28542265google scholar: lookup
  12. Martins SD, Oliveira MAF, Azevedo VAN, Costa FDC, Silva IGMD, de Morais SM, Báo SN, Silva JRV, Ceccatto VM, Araújo VR. Punica granatum L. Modulates Antioxidant Activity in Vitrified Bovine Ovarian Tissue. Int J Mol Sci 2026 Jan 16;27(2).
    doi: 10.3390/ijms27020903pubmed: 41596549google scholar: lookup
  13. Oliveira MAF, Martins SD, de Assis EIT, Martins JER, Alves FL, Bittencourt SRA, da Silva IGM, Báo SN, Fidelis QC, de Morais SM, Silva JRV, Ceccatto VM, Araújo VR. Ethanolic Extract of Pomegranate (Punica granatum L.) Prevents Oxidative Stress and Preserves the Morphology of Preantral Follicles Included in Bovine Ovarian Tissue Cultured In Vitro. Animals (Basel) 2025 Nov 19;15(22).
    doi: 10.3390/ani15223344pubmed: 41302052google scholar: lookup
  14. de Aguiar CMA, Martins SD, Ferreira AS, Santos-Saboia HEO, Cavalcante-Filho JEF, Oliveira MAF, de Moura MJN, Lessa RA, Pereira MG, Borges CDS, Ceccatto VM, Báo SN, Araújo VR. The ability of the polysaccharide extract Cissus sicyoides L. leaves to maintain normal follicle structure in ovarian tissue culture. In Vitro Cell Dev Biol Anim 2025 Oct;61(9):1137-1147.
    doi: 10.1007/s11626-025-01110-6pubmed: 40924338google scholar: lookup
  15. Ferreira AS, Ferreira FGP, Nascimento ERM, Tetaping GM, de Lima LF, Fonseca SGDC, de Figueiredo JR, de Sousa DF, Celestino JJH. Evaluation of the morphology and development of preantral ovarian follicles in mice submitted to a chronic diet of dietary supplementation with Pereskia aculeata Miller leaves. Anim Reprod 2024;21(2):e20240012.
    doi: 10.1590/1984-3143-AR2024-0012pubmed: 39021496google scholar: lookup
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