First delivery and ovariectomy affect biomechanical and structural properties of the vagina in the ovine model.

[en] INTRODUCTION AND HYPOTHESIS: Animal models are useful for investigating the genesis of pelvic floor dysfunction and for developing novel therapies for its treatment. There is a need for an alternative large-animal model to the nonhuman primate. Therefore we studied the effects of the first vaginal delivery, ovariectomy and systemic hormonal replacement therapy (HRT) on the biomechanical and structural properties of the ovine vagina. METHODS: We examined the gross anatomical properties of nulliparous, primiparous, ovariectomized multiparous, and ovariectomized hormone-replaced multiparous sheep (six animals per group). We also harvested mid-vaginal and distal vaginal tissue to determine smooth muscle contractility and passive biomechanical properties, for morphometric assessment of the vaginal wall layers, to determine collagen and elastin content, and for immunostaining for alpha-smooth muscle actin and estrogen receptor-alpha. RESULTS: There were no regional differences in the nulliparous vagina. One year after the first vaginal delivery, stiffness and contractility of the distal vagina were decreased, whereas the elastin content increased. The mid-vagina of ovariectomized sheep was stiff, and its epithelium was thin and lacked glycogen. HRT decreased the stiffness of the mid-vagina by 45% but had no measurable effect on contractility or elastin content, and increased epithelial thickness and glycogen content. HRT also increased the epithelial thickness and glycogen content of the distal vagina. At this location, there were no changes in morphology or stiffness. CONCLUSION: In sheep, life events including delivery and ovariectomy affect the biomechanical properties of the vagina in a region-specific way. Vaginal delivery mainly affects the distal region by decreasing stiffness and contractility. HRT can reverse the increase in stiffness of the mid-vagina observed after surgical induction of menopause. These observations are in line with scanty biomechanical measurements in comparable clinical specimens.

Disciplines :

Reproductive medicine (gynecology, andrology, obstetrics)

Author, co-author :

Urbankova, Iva

Callewaert, Geertje

Blacher, Silvia ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Deprest, Dries

Hympanova, Lucie

Feola, Andrew

DE LANDSHEERE, Laurent ; Centre Hospitalier Universitaire de Liège - CHU > Service de gynécologie-obstétrique (CHR)

Deprest, Jan

Language :

English

Title :

First delivery and ovariectomy affect biomechanical and structural properties of the vagina in the ovine model.

Publication date :

2019

Journal title :

International Urogynecology Journal

ISSN :

0937-3462

eISSN :

1433-3023

Publisher :

Springer, Germany

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 31 January 2018

Statistics

Number of views

62 (9 by ULiège)

Number of downloads

4 (3 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

DeLancey JOL, Kane Low L, Miller JM, et al. Graphic integration of causal factors of pelvic floor disorders: an integrated life span model. Am J Obstet Gynecol. 2008;199:610.e1–610.e5. 10.1016/j.ajog.2008.04.001.
Glazener C, Elders A, MacArthur C, et al. Childbirth and prolapse: long-term associations with the symptoms and objective measurement of pelvic organ prolapse. BJOG. 2013;120:161–168. 10.1111/1471-0528.12075.
Smith FJ, Holman CDJ, Moorin RE, Tsokos N. Lifetime risk of undergoing surgery for pelvic organ prolapse. Obstet Gynecol. 2010;116:1096–1100. 10.1097/AOG.0b013e3181f73729.
Callewaert G, Albersen M, Janssen K et al (2015) The impact of vaginal delivery on pelvic floor function – delivery as a time point for secondary prevention. BJOG 123:678–681. doi: 10.1111/1471-0528.13505.
Couri B, Lenis A, Borazjani A (2012) Animal models of female pelvic organ prolapse: lessons learned. Expert Rev Obs Gynecol 7:249–260. 10.1586/eog.12.24.Animal.
Ulrich D, Edwards SL, Su K (2014) Influence of reproductive status on tissue composition and biomechanical properties of ovine vagina. PLoS One 9:e93172. 10.1371/journal.pone.0093172.
de Tayrac R, Alves A, Thérin M (2007) Collagen-coated vs noncoated low-weight polypropylene meshes in a sheep model for vaginal surgery. A pilot study. Int Urogynecol J Pelvic Floor Dysfunct 18:513–520. 10.1007/s00192-006-0176-9.
Urbankova I, Vdoviakova K, Rynkevic R (2017) Comparative anatomy of the ovine and female pelvis. Gynecol Obstet Invest. 10.1159/000454771.
Urbankova I, Callewaert G, Sindhwani N et al (2017) Transvaginal mesh insertion in the ovine model. J Vis Exp. 10.3791/55706.
Barron AM, Cake M, Verdile G, Martins RN (2009) Ovariectomy and 17beta-estradiol replacement do not alter beta-amyloid levels in sheep brain. Endocrinology 150:3228–3236. 10.1210/en.2008-1252.
Ayen E, Noakes DE, Baker SJ (1998) Changes in the capacity of the vagina and the compliance of the vaginal wall in ovariectomized, normal cyclical and pregnant ewes, before and after treatment with exogenous oestradiol and progesterone. Vet J 156:133–143.
Brasted M, White C, Kennedy T, Salamonsen L (2003) Mimicking the events of menstruation in the murine uterus. Biol Reprod 69:1273–1280. 10.1095/biolreprod.103.016550.
Feola A, Endo M, Urbankova I et al (2015) Host reaction to vaginally inserted collagen containing polypropylene implants in sheep. Am J Obstet Gynecol 212:474.e1–474.e8. 10.1016/j.ajog.2014.11.008.
Ozog Y, Konstantinovic ML, Werbrouck E et al (2011) Shrinkage and biomechanical evaluation of lightweight synthetics in a rabbit model for primary fascial repair. Int Urogynecol J 22:1099–108. 10.1007/s00192-011-1440-1.
Balsat C, Blacher S, Signolle N et al (2011) Whole slide quantification of stromal lymphatic vessel distribution and peritumoral lymphatic vessel density in early invasive cervical cancer: a method description. ISRN Obstet Gynecol. 2011:354861. 10.5402/2011/354861.
de Landsheere L, Blacher S, Munaut C et al (2014) Changes in elastin density in different locations of the vaginal wall in women with pelvic organ prolapse. Int Urogynecol J 25:1673–1681. 10.1007/s00192-014-2431-9.
Söderberg MW, Johansson B, Masironi B et al (2007) Pelvic floor sex steroid hormone receptors, distribution and expression in pre- and postmenopausal stress urinary incontinent women. Acta Obstet Gynecol Scand 86:1377–1384. 10.1080/00016340701625446.
Feola A, Endo M, Deprest J (2014) Biomechanics of the rat vagina during pregnancy and postpartum: a 3-dimensional ultrasound approach. Int Urogynecol J Pelvic Floor Dysfunct 25:915–920. 10.1007/s00192-013-2313-6.
Chantereau P, Brieu M, Kammal M et al (2014) Mechanical properties of pelvic soft tissue of young women and impact of aging. Int Urogynecol J 25:1547–1553. 10.1007/s00192-014-2439-1.
Gandhi J, Chen A, Dagur G et al (2016) Genitourinary syndrome of menopause: an overview of clinical manifestations, pathophysiology, etiology, evaluation, and management. Am J Obstet Gynecol 215:704–711. doi: 10.1016/j.ajog.2016.07.045.
Feola A, Abramowitch S, Jones K et al (2010) Parity negatively impacts vaginal mechanical properties and collagen structure in rhesus macaques. Am J Obstet Gynecol 203:595.e1–595e.8. 10.1016/j.ajog.2010.06.035.
Feola A, Moalli P, Alperin M et al (2011) Impact of pregnancy and vaginal delivery on the passive and active mechanics of the rat vagina. Ann Biomed Eng 39:549–558. 10.1007/s10439-010-0153-9.
Knight KM, Moalli PA, Nolfi A et al (2016) Impact of parity on ewe vaginal mechanical properties relative to the nonhuman primate and rodent. Int Urogynecol J 27:1255–1263. 10.1007/s00192-016-2963-2.
Ulrich D, Edwards SL, Letouzey V et al (2014) Regional variation in tissue composition and biomechanical properties of postmenopausal ovine and human vagina. PLoS One 9:e104972. 10.1371/journal.pone.0104972.
Rubod C, Boukerrou M, Brieu M et al (2007) Biomechanical properties of vaginal tissue. Part 1: new experimental protocol. J Urol 178:320–325; discussion 325. 10.1016/j.juro.2007.03.040.
Moalli PA, Debes KM, Meyn LA et al (2008) Hormones restore biomechanical properties of the vagina and supportive tissues after surgical menopause in young rats. Am J Obstet Gynecol 199:161.e1–161e.8. 10.1016/j.ajog.2008.01.042.
Rizk DEE, Fahim MA, Hassan HA et al (2007) The effect of ovariectomy on biomarkers of urogenital ageing in old versus young adult rats. Int Urogynecol J Pelvic Floor Dysfunct 18:1077–1085. 10.1007/s00192-006-0278-4.
Shuster L, Gostout B, Grossardt B, Rocca WA (2009) Prophylactic oophorectomy in pre-menopausal women and long term health – a review. Menopause Int 14:111–116. 10.1258/mi.2008.008016.
Robert C, Lesty C, Robert A (1988) Ageing of the skin: study of elastic fiber network modifications by computerized image analysis. Gerontology 34:291–296.
Onol FF, Ercan F, Tarcan T (2006) The effect of ovariectomy on rat vaginal tissue contractility and histomorphology. J Sex Med 3:233–241. 10.1111/j.1743-6109.2006.00216.x.
Fuermetz A, Schoenfeld M, Ennemoser S et al (2015) Change of steroid receptor expression in the posterior vaginal wall after local estrogen therapy. Eur J Obstet Gynecol Reprod Biol 187:45–50. 10.1016/j.ejogrb.2015.02.021.
Kim N, Min K, Pessina M et al (2004) Effects of ovariectomy and steroid hormones on vaginal smooth muscle contractility. Int J Impot Res 16:43–50. 10.1038/sj.ijir.3901138.
Vizintin Z, Rivera M, Fistonić I, Saraçoğlu F, Guimares P, Gaviria J et al (2012) Novel minimally invasive VSP Er:YAG laser treatments in gynecology. J Laser Health Acad 1:45–58.