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Home / Equine Research Bank / Front Vet Sci / Collagen and Microvascularization in Placentas From Young an...
Frontiers in veterinary science2022; 8; 772658; doi: 10.3389/fvets.2021.772658

Collagen and Microvascularization in Placentas From Young and Older Mares.

Abstract: In older mares, increasing collagen fibers (fibrosis) in the endometrium and oviduct predisposes to sub-fertility and infertility. In this study, (i) gene transcription of collagen (qPCR: COL1A1, COL1A2, COL3A1, COL5A1); (ii) total collagen protein (hydroxyproline); (iii) collagen distribution (Picrosirius red staining; polarized light microscopy); and (iv) microvascular density (Periodic acid-Schiff staining), were evaluated in mares' placenta, and related to mares age, and placenta and neonate weights. Samples were collected from the gravid horn, non-gravid horn, and body of the placenta from younger (n = 7), and older mares (n = 9) of different breeds. Transcripts of COL1A1, COL3A1 and COL5A1, total collagen protein, chorionic plate connective tissue thickness, and microvascularization increased in the gravid horn of older mares' placentas, compared to the youngest (P < 0.05). Although in other species placenta fibrosis may indicate placental insufficiency and reduced neonate weight, this was not observed here. It appears that older fertile mares, with more parities, may develop a heavier, more vascularized functional placenta with more collagen, throughout a longer gestation, which enables the delivery of heavier foals. Thus, these features might represent morphological and physiological adaptations of older fertile mares' placentas to provide the appropriate nutrition to the equine fetus.
Copyright © 2022 Neto da Silva, Costa, Teixeira, Alpoim-Moreira, Fernandes, Fradinho, Rebordão, Silva, Ferreira da Silva, Bliebernicht, Alexandre-Pires and Ferreira-Dias.
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Publication Date: 2022-01-04 PubMed ID: 35059454PubMed Central: PMC8764314DOI: 10.3389/fvets.2021.772658Google 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.

This research examined the association between the increased collagen fibers in the endometrium and oviduct of older mares and their predisposition to sub-fertility and infertility. The study focused on the role, quantity, and distribution of collagen in mares’ placentas and its impact on their fertility, placenta and neonate weights. The evidence suggests that older fertile mares, despite having more collagen and microvascularization in their placentas, can still produce heavier foals, demonstrating physiological adaptations to ensure proper fetus nutrition.

Research Methodology

  • The study followed a methodical approach where researchers evaluated four aspects: collagen gene transcription (using qPCR), total collagen protein (using hydroxyproline), collagen distribution (using Picrosirius red staining and polarized light microscopy), and microvascular density (using Periodic acid-Schiff staining).
  • These parameters were studied in the placentas of younger (7) and older mares (9) and the results were related to mares age, placenta weight, and neonate weights.
  • Placenta samples were collected from different sections: the gravid horn, non-gravid horn, and body.

Findings

  • The study demonstrated that transcripts of collagen, total collagen protein, thickness of the chorionic plate connective tissue, and microvascularization increased in the gravid horn of the placenta from older mares compared to the younger mares.
  • Despite the increase in collagen (which is linked to placenta fibrosis in other species and potentially to reduced neonate weight), no such correlation was seen in these mares.
  • Evidence indicated that older fertile mares with more parities developed a heavier and denser placenta during a longer gestation period, facilitating the birth of heavier foals.

Conclusion

  • The research concludes that the increased collagen and vascularization present in the placentas of older mares might represent physiological adaptations.
  • These adaptations appear to enable older mares to adequately nourish the fetus, despite the increase in collagen typically associated with sub-fertility and infertility.

Cite This Article

APA
Neto da Silva AC, Costa AL, Teixeira A, Alpoim-Moreira J, Fernandes C, Fradinho MJ, Rebordão MR, Silva E, Ferreira da Silva J, Bliebernicht M, Alexandre-Pires G, Ferreira-Dias G. (2022). Collagen and Microvascularization in Placentas From Young and Older Mares. Front Vet Sci, 8, 772658. https://doi.org/10.3389/fvets.2021.772658

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 8
Pages: 772658

Researcher Affiliations

Neto da Silva, Ana Catarina
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Costa, Ana Luísa
  • Embriovet, Muge, Portugal.
Teixeira, Ana
  • Pole Reprodución Haras de La Gesse, Boulogne-sur-Gesse, France.
Alpoim-Moreira, Joana
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Fernandes, Carina
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Fradinho, Maria João
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Rebordão, Maria Rosa
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
  • Coimbra College of Agriculture, Polytechnic Institute of Coimbra, Coimbra, Portugal.
Silva, Elisabete
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Ferreira da Silva, José
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Bliebernicht, Miguel
  • Embriovet, Muge, Portugal.
Alexandre-Pires, Graça
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.
Ferreira-Dias, Graça
  • Faculdade de Medicina Veterinária, CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Universidade de Lisboa, Lisboa, Portugal.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 56 references
  1. Enders AC, Blankenship TN. Comparative placental structure. Adv Drug Deliv Rev (1999) 38:3–15.
    doi: 10.1016/S0169-409X(99)00003-4pubmed: 10837743google scholar: lookup
  2. Caixeta ES, Fagundes NS, Caixeta MS, Pyles ESS. Desenvolvimento embrionário inicial eqüino – revisão. Rev Port Ciências Veterinárias (2008). 103:25–34.
  3. McKinnon AO, Squires EL, Vaala WE, Varner DD. Equine Reproduction. Second Ed. (2011). Ames, USA: Wiley-Blackwell.
  4. Pozor M. Equine placenta–A clinician's perspective. Part 1: Normal placenta - Physiology and evaluation. Equine Vet Educ (2016) 28:327–34.
    doi: 10.1111/eve.12499google scholar: lookup
  5. Morresey P. How to perform a field assessment of the equine placenta. In Abstract retrieved from Abstracts of the 50th Annual Convention of the American Association of Equine Practitioners. Lexington, USA: American Association of Equine Practitioners (AAEP) (2004) p. 4−8.
  6. Canisso IF, Loux SC, Lima FS. Biomarkers for placental disease in mares. Theriogenology (2020) 150:302–7.
    doi: 10.1016/j.theriogenology.2020.01.073pubmed: 32088026google scholar: lookup
  7. Pirrone A, Antonelli C, Mariella J, Castagnetti C. Gross placental morphology and foal serum biochemistry as predictors of foal health. Theriogenology (2014) 81:1293–9.
    doi: 10.1016/j.theriogenology.2014.02.011pubmed: 24661433google scholar: lookup
  8. Bianco C, Pirrone A, Boldini S, Sarli G, Castagnetti C. Histomorphometric parameters and fractal complexity of the equine placenta from healthy and sick foals. Theriogenology (2014) 82:1106–12.
    doi: 10.1016/j.theriogenology.2014.07.036pubmed: 25193631google scholar: lookup
  9. Barron JK. The effect of maternal age and parity on the racing performance of thoroughbred horses. Equine Vet J (1995) 27:73–5.
    doi: 10.1111/j.2042-3306.1995.tb03036.xpubmed: 7774552google scholar: lookup
  10. Foote AK, Ricketts SW, Whitwell KE. A racing start in life? The hurdles of equine feto-placental pathology. Equine Vet J (2012) 44:120–9.
    doi: 10.1111/j.2042-3306.2011.00507.xpubmed: 22594040google scholar: lookup
  11. Leiser R, Dantzer V. Structural and functional aspects of porcine placental microvasculature. Anat Embryol (Berl) (1988) 177:409–19.
    doi: 10.1007/BF00304738pubmed: 3364745google scholar: lookup
  12. Cottrill C, Jeffers-Lo J, Ousey J, McGladdery A, Ricketts S, Silver M. The placenta as a determinant of fetal wellbeing in normal and abnormal equine pregnancies. J Reprod Fertil Suppl (1991) 44:591–601.
    pubmed: 1795302
  13. Abd-Elnaeim MM, Leiser R, Wilsher S, Allen WR. Structural and haemovascular aspects of placental growth throughout gestation in young and aged mares. Placenta (2006) 27:1103–13.
    doi: 10.1016/j.placenta.2005.11.005pubmed: 16406511google scholar: lookup
  14. Sarli G, Castagnetti C, Bianco C, Ballotta G, Tura G, Caporaletti M. Canine placenta histological findings and microvascular density: The histological basis of a negative neonatal outcome?. Animals (Basel) (2021) 11:1418.
    doi: 10.3390/ani11051418pmc: PMC8157207pubmed: 34063427google scholar: lookup
  15. Kenney RM, Doig PA. Equine endometrial biopsy. Current Therapy in Theriogenology Philadelphia: DA Morrow and WB Saunders Company. (1986).
  16. Rebordão MR, Amaral A, Lukasik K, Szóstek-Mioduchowska A, Pinto-Bravo P, Galvão A. Impairment of the antifibrotic prostaglandin E2pathway may influence neutrophil extracellular traps-induced fibrosis in the mare endometrium. Domest Anim Endocrinol (2019) 67:1–10.
    doi: 10.1016/j.domaniend.2018.10.004pubmed: 30522057google scholar: lookup
  17. Pinto-Bravo P, Rebordão MR, Amaral A, Fernandes C, Cuello C, Parrilla I. Is mare endometrosis linked to oviduct fibrosis?. Pferdeheilkunde–Equine Medicine (2018) 34:43–6.
    doi: 10.21836/PEM20180107google scholar: lookup
  18. Bracher V, Mathias S, Allen WR. Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Equine Vet J (1996) 28:180–8.
    doi: 10.1111/j.2042-3306.1996.tb03771.xpubmed: 28976715google scholar: lookup
  19. Ahmed A, Perkins J. Angiogenesis and intrauterine growth restriction. Baillieres Best Pract Res Clin Obstet Gynaecol (2000) 14:981–98.
    doi: 10.1053/beog.2000.0139pubmed: 11141345google scholar: lookup
  20. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: One function, multiple origins. Am J Pathol (2007) 170:1807–16.
    doi: 10.2353/ajpath.2007.070112pmc: PMC1899462pubmed: 17525249google scholar: lookup
  21. Weber KT. Fibrosis and hypertensive heart disease. Curr Opin Cardiol (2000) 15:264–72.
    doi: 10.1097/00001573-200007000-00010pubmed: 11139090google scholar: lookup
  22. Van Linthout S, Miteva K, Tschöpe C. Crosstalk between fibroblasts and inflammatory cells. Cardiovasc Res (2014) 102:258–69.
    doi: 10.1093/cvr/cvu062pubmed: 24728497google scholar: lookup
  23. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest (2007) 117:524–9.
    doi: 10.1172/JCI31487pmc: PMC1804380pubmed: 17332879google scholar: lookup
  24. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol (2008) 214:199–210.
    doi: 10.1002/path.2277pmc: PMC2693329pubmed: 18161745google scholar: lookup
  25. Hirayama H. Biochemical studies on collagen in human placenta- relation of collagen to the construction and function of human placenta. Nihon Sanka Fujinka Gakkai Zasshi (1983) 35:2395–403.
    pubmed: 6686603
  26. Rukosuev VS, Nanaev AK, Milovanov AP. Participation of collagen types I, III, IV, V, and fibronectin in the formation of villi fibrosis in human term placenta. Acta Histochem (1990) 89:11–6.
    doi: 10.1016/S0065-1281(11)80308-9pubmed: 1705376google scholar: lookup
  27. Pollack RN, Divon MY. Intrauterine Growth Retardation: Definition, Classification, and Etiology. Clin Obstet Gynecol (1992) 35:99–107.
    doi: 10.1097/00003081-199203000-00015pubmed: 1544253google scholar: lookup
  28. Pinto-Bravo P, Rebordão MR, Amaral A, Fernandes C, Galvão A, Silva E. Microvascularization and expression of fibroblast growth factor and vascular endothelial growth factor and their receptors in the mare oviduct. Animals (Basel) (2021). 11:1099.
    doi: 10.3390/ani11041099pmc: PMC8070128pubmed: 33921416google scholar: lookup
  29. Dheda K, Huggett JF, Bustin SA, Johnson MA, Rook G, Zumla A. Validation of housekeeping genes for normalizing RNA expression in real-time PCR. Biotechniques (2004) 37:112–9.
    doi: 10.2144/04371RR03pubmed: 15283208google scholar: lookup
  30. Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol (2005) 12:1047–64.
    doi: 10.1089/cmb.2005.12.1047pmc: PMC2716216pubmed: 16241897google scholar: lookup
  31. Rebordão MR, Amaral A, Lukasik K, Szóstek-Mioduchowska A, Pinto-Bravo P, Galvão A. Constituents of neutrophil extracellular traps induce in vitro collagen formation in mare endometrium. Theriogenology (2018) 113:8–18.
    doi: 10.1016/j.theriogenology.2018.02.001pubmed: 29452855google scholar: lookup
  32. Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet (2012) 13:227–32.
    doi: 10.1038/nrg3185pmc: PMC3654667pubmed: 22411467google scholar: lookup
  33. Junqueira LC, Carneiro J. Histologia Básica. 12th ed. Rio de Janeiro: Koogan G. (2013).
  34. Lattouf R, Younes R, Lutomski D, Naaman N, Godeau G, Senni K. Picrosirius red staining: a useful tool to appraise collagen networks in normal and pathological tissues. J Histochem Cytochem (2014) 62:751–8.
    doi: 10.1369/0022155414545787pubmed: 25023614google scholar: lookup
  35. Luna LG. Polysaccharides and mucopolysaccharides. Histopathologic methods and color atlas of special stains and tissue artifact. Gaithersburg, MD: American Histolabs Inc. (1992) p. 364–98.
  36. Ferreira-Dias G, Bravo PP, Mateus L, Redmer DA, Medeiros JA. Microvascularization and angiogenic activity of equine corpora lutea throughout the estrous cycle. Domest Anim Endocrinol (2006) 30:247–59.
    doi: 10.1016/j.domaniend.2005.07.007pubmed: 16140491google scholar: lookup
  37. Steven DH, Samuel CA. Anatomy of the placental barrier in the mare. J Reprod Fertil (1975) 23:579–82.
    pubmed: 1060848
  38. Samuel CA, Allen WR, Steven DH. Ultra-structural development of the equine placenta. J Reprod Fertil (1975) 23:575–8.
    pubmed: 1060847
  39. Gerstenberg C, Allen WR, Stewart F. Cell proliferation patterns during development of the equine placenta. J Reprod Fertil (1999) 117:143–52.
    doi: 10.1530/jrf.0.1170143pubmed: 10645255google scholar: lookup
  40. Elliott C, Morton J, Chopin J. Factors affecting foal birth weight in thoroughbred horses. Theriogenology (2009) 71:683–9.
    doi: 10.1016/j.theriogenology.2008.09.041pubmed: 18980778google scholar: lookup
  41. Teixeira AR, Leão MT, Costa AL, Maerten C, Abreu P, Bliebernicht M. Biometric and ponderal evaluation of neonate foals: influence of maternal factors. Abstract retrieved from Book of Abstracts of the 71st Annual Meeting of the European Federation of Animal Science Virtual Meeting, 1st−4th December. Wageningen: Wageningen Academic Publishers; (2020) p. 469.
  42. Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdal PD. Influence of maternal size on placental, fetal and postnatal growth in the horse: I Development in utero. Reproduction (2002) 123:445–53.
    doi: 10.1530/rep.0.1230445pubmed: 11882022google scholar: lookup
  43. Wilsher S, Allen WR. Factors influencing placental development and function in the mare. Equine Vet J Suppl (2012) 41:113–9.
    doi: 10.1111/j.2042-3306.2011.00452.xpubmed: 22594039google scholar: lookup
  44. Fowden AL, Ward JW, Wooding FPB, Forhead AJ, Constancia M. Programming placental nutrient transport capacity. J Physiol (2006) 572:5–15.
    doi: 10.1113/jphysiol.2005.104141pmc: PMC1779642pubmed: 16439433google scholar: lookup
  45. Fowden AL, Giussani DA, Forhead AJ. Physiological development of the equine fetus during late gestation. Equine Vet J (2020) 52:165–73.
    doi: 10.1111/evj.13206pubmed: 31721295google scholar: lookup
  46. Beythien E, Aurich C, Wulf M, Aurich J. Effects of season on placental, foetal and neonatal development in horses. Theriogenology (2017) 15:98–103.
    doi: 10.1016/j.theriogenology.2017.04.027pubmed: 28583616google scholar: lookup
  47. Iwahashi M, Ooshima A, Nakano R. Increase in the relative level of type V collagen during development and ageing of the placenta. J Clin Pathol (1996) 49:916–9.
    doi: 10.1136/jcp.49.11.916pmc: PMC500832pubmed: 8944612google scholar: lookup
  48. Lunelli D, Cirio SM, Leite SC, Camargo CE, Kozicki LE. Collagen types in relation to expression of estradiol and progesterone receptors in equine endometrial fibrosis. Adv Biosci Biotechnol (2013) 4:599–605.
    doi: 10.4236/abb.2013.44078google scholar: lookup
  49. Dayan D, Hiss Y, Hirshberg A, Bubis JJ, Wolman M. Are the polarization colors of picrosirius red-stained collagen determined only by the diameter of the fibers?. Histochemistry (1989) 93:27–9.
    doi: 10.1007/BF00266843pubmed: 2482274google scholar: lookup
  50. Coleman R. Picrosirius red staining revisited. Acta Histochem (2011) 113:231–3.
    doi: 10.1016/j.acthis.2010.02.002pubmed: 20188402google scholar: lookup
  51. Wilsher S, Allen WR. The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet J (2003) 35:476–83.
    doi: 10.2746/042516403775600550pubmed: 12875326google scholar: lookup
  52. Sibley C, Glazier J, D'Souza S. Placental transporter activity and expression in relation to fetal growth. Exp Physiol (1997) 82:389–402.
    doi: 10.1113/expphysiol.1997.sp004034pubmed: 9129953google scholar: lookup
  53. Jellis C, Martin J, Narula J, Marwick TH. Assessment of nonischemic myocardial fibrosis. J Am Coll Cardiol (2010) 56:89–97.
    doi: 10.1016/j.jacc.2010.02.047pubmed: 20620723google scholar: lookup
  54. Ricketts SW, Alonso S. The effect of age and parity on the development of equine chronic endometrial disease. Equine Vet J (1991) 23:189–92.
    doi: 10.1111/j.2042-3306.1991.tb02752.xpubmed: 1884699google scholar: lookup
  55. Carnevale EM, Ginther OJ. Relationships of age to uterine function and reproductive effeciency in mares. Theriogenology 37(5. (1992) 1101–15.
    doi: 10.1016/0093-691X(92)90108-4pubmed: 16727108google scholar: lookup
  56. Kenney RM. The aetiology, diagnosis and classification of chronic degenerative endometritis. Equine Vet J (1992) 25:186.

Citations

This article has been cited 2 times.
  1. Alpoim-Moreira J, Fernandes C, Rebordão MR, Costa AL, Bliebernicht M, Nunes T, Szóstek-Mioduchowska A, Skarzynski DJ, Ferreira-Dias G. Collagen Type III as a Possible Blood Biomarker of Fibrosis in Equine Endometrium. Animals (Basel) 2022 Jul 21;12(14).
    doi: 10.3390/ani12141854pubmed: 35883401google scholar: lookup
  2. Katila T, Ferreira-Dias G. Evolution of the Concepts of Endometrosis, Post Breeding Endometritis, and Susceptibility of Mares. Animals (Basel) 2022 Mar 19;12(6).
    doi: 10.3390/ani12060779pubmed: 35327176google scholar: lookup
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