Abstract
Introduction and hypothesis
Parity is the leading risk factor for the development of pelvic organ prolapse. To assess the impact of pregnancy and delivery on vaginal tissue, researchers commonly use nonhuman primate (NHP) and rodent models. The purpose of this study was to evaluate the ewe as an alternative model by investigating the impact of parity on the ewe vaginal mechanical properties and collagen structure.
Methods
Mechanical properties of 15 nulliparous and parous ewe vaginas were determined via uniaxial tensile tests. Collagen content was determined by hydroxyproline assay and collagen fiber thickness was analyzed using picrosirius red staining. Outcome measures were compared using Independent samples t or Mann–Whitney U tests. ANOVA (Gabriel’s pairwise post-hoc test) or the Welch Alternative for the F-ratio (Games Howell post-hoc test) was used to compare data with previously published NHP and rodent data.
Results
Vaginal tissue from the nulliparous ewe had a higher tangent modulus and tensile strength compared with the parous ewe (p < 0.025). The parous ewe vagina elongated 42 % more than the nulliparous ewe vagina (p = 0.015). No significant differences were observed in collagen structure among ewe vaginas. The tangent modulus of the nulliparous ewe vagina was not different from that of the NHP or rodent (p = 0.290). Additionally, the tangent moduli of the parous ewe and NHP vaginas did not differ (p = 0.773).
Conclusions
Parity has a negative impact on the mechanical properties of the ewe vagina, as also observed in the NHP. The ewe may serve as an alternative model for studying parity and ultimately prolapse development.
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References
Barber MD, Visco AG, Wyman JF, Fantl JA, Bump RC (2002) Sexual function in women with urinary incontinence and pelvic organ prolapse. Obstet Gynecol 99(2):281–289. doi:10.1016/S0029-7844(01)01727-6
Jelovsek JE, Barber MD (2006) Women seeking treatment for advanced pelvic organ prolapse have decreased body image and quality of life. Am J Obstet Gynecol 194(5):1455–1461. doi:10.1016/j.ajog.2006.01.060
MacLennan AH, Taylor AW, Wilson DH, Wilson D (2000) The prevalence of pelvic floor disorders and their relationship to gender, age, parity and mode of delivery. Br J Obstet Gynaecol 107(12):1460–1470
Mant J, Painter R, Vessey M (1997) Epidemiology of genital prolapse: observations from the Oxford Family Planning Association Study. Br J Obstet Gynaecol 104(5):579–585
Swift SE (2000) The distribution of pelvic organ support in a population of female subjects seen for routine gynecologic health care. Am J Obstet Gynecol 183(2):277–285
Olsen AL, Smith VJ, Bergstrom JO, Colling JC, Clark AL (1997) Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 89(4):501–506
Wu JM, Matthews CA, Conover MM, Pate V, Jonsson Funk M (2014) Lifetime risk of stress urinary incontinence or pelvic organ prolapse surgery. Obstet Gynecol 123(6):1201–1206
Moalli PA, Jones Ivy S, Meyn LA, Zyczynski HM (2003) Risk factors associated with pelvic floor disorders in women undergoing surgical repair. Obstet Gynecol 101(5):869–874
Ashton-Miller JA, DeLancey JOL (2007) Functional anatomy of the female pelvic floor. Ann N Y Acad Sci 1101:266–296
Lien K-C, Mooney B, DeLancey JOL, Ashton-Miller JA (2004) Levator ani muscle stretch induced by simulated vaginal birth. Obstet Gynecol 103(1):31–40. doi:10.1097/01.AOG.0000109207.22354.65
Alperin M, Feola A, Duerr R, Moalli P, Abramowitch S (2010) Pregnancy-and delivery-induced biomechanical changes in rat vagina persist postpartum. Int Urogynecol J Pelvic Floor Dysfunct 21(9):1169–1174
Daucher JA, Clark KA, Stolz DB, Meyn LA, Moalli PA (2007) Adaptations of the rat vagina in pregnancy to accommodate delivery. Obstet Gynecol 109(1):128–135
Feola A, Abramowitch S, Jones K, Stein S, Moalli P (2010) Parity negatively impacts vaginal mechanical properties and collagen structure in rhesus macaques. Am J Obstet Gynecol 203(6):595.e1–595.e8
Feola A, Moalli P, Alperin M, Duerr R, Gandley RE, Abramowitch S (2011) Impact of pregnancy and vaginal delivery on the passive and active mechanics of the rat vagina. Ann Biomed Eng 39(1):549–558
Lowder JL, Debes KM, Moon DK, Howden N, Abramowitch SD, Moalli PA (2007) Biomechanical adaptations of the rat vagina and supportive tissues in pregnancy to accommodate delivery. Obstet Gynecol 109(1):136–143. doi:10.1097/01.AOG.0000250472.96672.6c
Abramowitch SD, Feola A, Jallah Z, Moalli PA (2009) Tissue mechanics, animal models, and pelvic organ prolapse: a review. Eur J Obstet Gynecol Reprod Biol 144(Suppl 1):S146–S158
Otto LN, Slayden OD, Clark AL, Brenner RM (2002) The rhesus macaque as an animal model for pelvic organ prolapse. Am J Obstet Gynecol 186(3):416–421
Ayen E, Noakes DE, Ayen E (1997) Displacement of the tubular genital tract of the ewe during pregnancy. Vet Rec 141(20):509–512
Low JC, Sutherland HK (1987) A census of the prevalence of vaginal prolapse in sheep flocks in the Borders region of Scotland. Vet Rec 120(24):571–575
Mosdol G (1999) Spontaneous vaginal rupture in pregnant ewes. Vet Rec 144(2):38–41
Couri BM, Lenis AT, Borazjani A, Paraiso MFR, Damaser MS (2012) Animal models of female pelvic organ prolapse: lessons learned. Expert Rev Obstet Gynecol 7(3):249–260. doi:10.1586/eog.12.24
Thomas DL, Waldron DF, Lowe GD, Morrical DG, Meyer HH, High RA, Berger YM, Clevenger DD, Fogle GE, Gottfredson RG, Loerch SC, McClure KE, Willingham TD, Zartman DL, Zelinsky RD (2003) Length of docked tail and the incidence of rectal prolapse in lambs. J Anim Sci 81(11):2725–2732
Bump RC, Mattiasson A, Bo K, Brubaker LP, DeLancey JOL, Klarskov P, Shull BL, Smith ARB (1996) The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 175(1):10–17
Liang R, Abramowitch S, Knight K, Palcsey S, Nolfi A, Feola A, Stein S, Moalli PA (2013) Vaginal degeneration following implantation of synthetic mesh with increased stiffness. BJOG 120(2):233–243
Neuman RE, Logan MA (1950) The determination of hydroxyproline. J Biol Chem 184(1):299–306
Wolf MT, Carruthers CA, Dearth CL, Crapo PM, Huber A, Burnsed OA, Londono R, Johnson SA, Daly KA, Stahl EC, Freund JM, Medberry CJ, Carey LE, Nieponice A, Amoroso NJ, Badylak SF (2013) Polypropylene surgical mesh coated with extracellular matrix mitigates the host foreign body response. J Biomed Mater Res A. doi:10.1002/jbm.a.34671
Woo SLY, Orlando CA, Camp JF, Akeson WH (1986) Effects of postmortem storage by freezing on ligament tensile behavior. J Biomech 19(5):399–404
Rubod C, Boukerrou M, Brieu M, Dubois P, Cosson M (2007) Biomechanical properties of vaginal tissue. I. New experimental protocol. J Urol 178(1):320–325
Lee TQ, Woo SLY (1988) A new method for determining cross-sectional shape and area of soft tissues. J Biomech Eng 110(2):110–114
Ulrich D, Edwards SL, Su K, White JF, Ramshaw JAM, Jenkin G, Deprest J, Rosamilia A, Werkmeister JA, Gargett CE (2014) Influence of reproductive status on tissue composition and biomechanical properties of ovine vagina. PLoS One 9(4):e93172
Acknowledgements
We are grateful to the National Institutes of Health for funding support R01 HD-061811. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE-1247842. The assistance of Matthew Falcioni from the University of Pittsburgh, Department of Statistics, in statistical analysis, and Dr. Bryan N. Brown from the University of Pittsburgh, Department of Bioengineering, in examining collagen fiber thickness, is gratefully acknowledged. Additionally, we would like to thank Christopher A. Carruthers from the University of Pittsburgh, Department of Bioengineering, for providing the MatLab code.
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This study was funded by the National Institutes of Health R01 HD-061811.
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K.M. Knight, A. Nolfi, S. Palcsey, and W. Barone have no conflicts of interest to disclose. P.A. Moalli received a research grant from the National Institutes of Health, R01 HD-061811, and has a cooperative research agreement with ACell. S.D. Abramowitch received a research grant from the National Institutes of Health, R01 HD-061811, and has a cooperative research agreement with ACell.
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Knight, K.M., Moalli, P.A., Nolfi, A. et al. Impact of parity on ewe vaginal mechanical properties relative to the nonhuman primate and rodent. Int Urogynecol J 27, 1255–1263 (2016). https://doi.org/10.1007/s00192-016-2963-2
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DOI: https://doi.org/10.1007/s00192-016-2963-2