Tissue mechanics, animal models, and pelvic organ prolapse: A review

European Journal of Obstetrics and Gynecology and Reproductive Biology

Volumn 144, Issue SUPPL 1, 2009, Pages

  Abramowitch, Steven D ^a,b   Feola, Andrew ^a   Jallah, Zegbeh ^a   Moalli, Pamela A ^b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Animal models; Biomechanics; Pelvic organ prolapsed

Indexed keywords

COLLAGEN;

ANIMAL; ANIMAL MODEL; ANISOTROPY; BIOMECHANICS; CHEMISTRY; CONNECTIVE TISSUE; ELASTICITY; FEMALE; HUMAN; MOUSE; PELVIS FLOOR; PHYSIOLOGY; PREGNANCY; PRIMATE; RABBIT; RAT; REVIEW; SHEEP; UTERUS PROLAPSE; VAGINA; VISCERAL PROLAPSE; VISCOSITY;

ANIMALS; ANISOTROPY; BIOMECHANICS; COLLAGEN; CONNECTIVE TISSUE; ELASTICITY; FEMALE; HUMANS; MICE; MODELS, ANIMAL; PELVIC FLOOR; PREGNANCY; PRIMATES; RABBITS; RATS; SHEEP; UTERINE PROLAPSE; VAGINA; VISCERAL PROLAPSE; VISCOSITY;

EID: 67650120964     PISSN: 03012115     EISSN: 18727654     Source Type: Journal    
DOI: 10.1016/j.ejogrb.2009.02.022     Document Type: Review

References (105)

1. Bump RC, Mattiasson A, Bo K, et al. The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 1996;175:10-7.
2. Heit M, Rosenquist C, Culligan P, Graham C, Murphy M, Shott S. Predicting treatment choice for patients with pelvic organ prolapse. Obstet Gynecol 2003;101:1279-84.
3. Barber MD, Visco AG, Wyman JF, Fantl JA, Bump RC. Sexual function in women with urinary incontinence and pelvic organ prolapse. Obstet Gynecol 2002;99:281-9.
4. Weber AM, Walters MD, Schover LR, Mitchinson A. Sexual function in women with uterovaginal prolapse and urinary incontinence. Obstet Gynecol 1995;85:483-7.
5. Olsen AL, Smith VJ, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 1997;89:501-6.
6. Rogers GR, Villarreal A, Kammerer-Doak D, Qualls C. Sexual function in women with and without urinary incontinence and/or pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2001;12:361-5.
7. Subak LL, Waetjen LE, van den Eeden S, Thom DH, Vittinghoff E, Brown JS. Cost of pelvic organ prolapse surgery in the United States. Obstet Gynecol 2001;98:646-51.
8. Boyles SH, Weber AM, Meyn L. Procedures for pelvic organ prolapse in the United States, 1979-1997. Am J Obstet Gynecol 2003;188:108-15.
9. Brown JS, Waetjen LE, Subak LL, Thom DH, Van den Eeden S, Vittinghoff E. Pelvic organ prolapse surgery in the United States, 1997. Am J Obstet Gynecol 2002;186:712-6.
10. DeLancey JO. Anatomy and biomechanics of genital prolapse. Clin Obstet Gynecol 1993;36:897-909.
11. DeLancey JO. The anatomy of the pelvic floor. Curr Opin Obstet Gynecol 1994;6:313-6.
12. Norton PA. Pelvic floor disorders: the role of fascia and ligaments. Clin Obstet Gynecol 1993;36:926-38.
13. Carley ME, Turner RJ, Scott DE, Alexander JM. Obstetric history in women with surgically corrected adult urinary incontinence or pelvic organ prolapse. J Am Assoc Gynecol Laparosc 1999;6:85-9.
14. Gurel H, Gurel SA. Pelvic relaxation and associated risk factors: the results of logistic regression analysis. Acta Obstet Gynecol Scand 1999;78:290-3.
15. Hendrix SL, Clark A, Nygaard I, Aragaki A, Barnabei V, McTiernan A. Pelvic organ prolapse in the Women's Health Initiative: gravity and gravidity. Am J Obstet Gynecol 2002;186:1160-6.
16. Lukacz ES, Lawrence JM, Contreras R, Nager CW, Luber KM. Parity, mode of delivery, and pelvic floor disorders. Obstet Gynecol 2006;107: 1253-60.
17. Moalli PA, Jones Ivy S, Meyn LA, Zyczynski HM. Risk factors associated with pelvic floor disorders in women undergoing surgical repair. Obstet Gynecol 2003;101:869-74.
18. O'Boyle AL, O'Boyle JD, Calhoun B, Davis GD. Pelvic organ support in pregnancy and postpartum. Int Urogynecol J Pelvic Floor Dysfunct 2005;16:69-72. [discussion 72]
19. DeLancey JO, Kearney R, Chou Q, Speights S, Binno S. The appearance of levator ani muscle abnormalities in magnetic resonance images after vaginal delivery. Obstet Gynecol 2003;101:46-53.
20. DeLancey JO, Morgan DM, Fenner DE, et al. Comparison of levator ani muscle defects and function in women with and without pelvic organ prolapse. Obstet Gynecol 2007;109:295-302.
21. Stoffel JT, Morgan D, Dunn R, et al. Urinary incontinence after stress incontinence surgery: a risk factor for depression. Urology 2008.
22. Fung YC. Biomechanics: mechanical properties of living tissues, 2nd ed., New York, NY: Springer; 1993.
23. Humphrey JD. Mechanics of the arterial wall: review and directions. Crit Rev Biomed Eng 1995;23:1-162.
24. Woo SL, Thomas M, Chan Saw SS. Contribution of biomechanics, orthopaedics and rehabilitation: the past present and future. Surgeon 2004;2: 125-36.
25. Hall RJ, Rogers RG, Saiz L, Qualls C. Translabial ultrasound assessment of the anal sphincter complex: normal measurements of the internal and external anal sphincters at the proximal, mid-, and distal levels. Int Urogynecol J Pelvic Floor Dysfunct 2007;18:881-8.
26. DeLancey JO. Anatomic aspects of vaginal eversion after hysterectomy. Am J Obstet Gynecol 1992;166:1717-24 [discussion 1724-1718].
27. Barber MD. Contemporary views on female pelvic anatomy. Cleve Clin J Med 2005;72(Suppl. 4):S3-11.
28. Wittman AB, Wall LL. The evolutionary origins of obstructed labor: bipedalism, encephalization, and the human obstetric dilemma. Obstet Gynecol Surv 2007;62:739-48.
29. Schimpf M, Tulikangas P. Evolution of the female pelvis and relationships to pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2005;16: 315-20.
30. Moalli PA, Howden NS, Lowder JL, et al. A rat model to study the structural properties of the vagina and its supportive tissues. Am J Obstet Gynecol 2005;192:80-8.
31. Chow BF, Agustin CE. Induction of premature birth in rats by a methionine antagonist. J Nutr 1965;87:293-6.
32. Champlin AK, DorrDL, Gates AH. Determining the stage of the oestrous cycle in the mouse by the appearance of the vagina. Biol Reprod 1973;8:491-4.
33. Huffaker RK, Muir TW, Rao A, Baumann SS, Kuehl TJ, Pierce LM. Histologic response of porcine collagen-coated and uncoated polypropylene grafts in a rabbit vagina model. Am J Obstet Gynecol 2008;198:582.e1-7.
34. Otto LN, Slayden OD, Clark AL, Brenner RM. The rhesus macaque as an animal model for pelvic organ prolapse. Am J Obstet Gynecol 2002;186:416-21.
35. Coates KW, Galan HL, Shull BL, Kuehl TJ. The squirrel monkey: an animal model of pelvic relaxation. Am J Obstet Gynecol 1995;172:588-93.
36. Lien KC, Mooney B, DeLancey JO, Ashton-Miller JA. Levator ani muscle stretch induced by simulated vaginal birth. Obstet Gynecol 2004;103:31-40.
37. Moalli PA, Shand SH, Zyczynski HM, Gordy SC, Meyn LA. Remodeling of vaginal connective tissue in patients with prolapse. Obstet Gynecol 2005;106:953-63.
38. Moalli PA, Talarico LC, Sung VW, et al. Impact of menopause on collagen subtypes in the arcus tendineous fasciae pelvis. Am J Obstet Gynecol 2004;190:620-7.
39. Pierce LM, Coates KW, Kramer LA, Bradford JC, Thor KB, Kuehl TJ. Effects of bilateral levator ani nerve injury on pelvic support in the female squirrel monkey. Am J Obstet Gynecol 2008;198:585.e1-8.
40. Ayen E, Noakes DE. Displacement of the tubular genital tract of the ewe during pregnancy. Vet Rec 1997;141:509-12.
41. Davies FG. The occurrence of vaginal eversion and allied disorders in fat ewes. Res Vet Sci 1970;11:86-90.
42. Hilson R, Jackson R, Perkins NR. An epidemiological study of vaginal prolapse in ewes. In Society of sheep and beef cattle veterinarians NZVA. Massey University; 21-23 May 2003. p. 203-17.
43. Hosie BD. Vaginal prolapse and rupture in sheep. In Pract 1989;11:215-8.
44. Low JC, Sutherland HK. A census of the prevalence of vaginal prolapse in sheep flocks in the Borders region of Scotland. Vet Rec 1987;120:571-5.
45. Shepherd PR. Vaginal prolapse in ewes. Vet Rec 1992;130:564.
46. Winter AC. Prolapse of the vagina and cervix in ewes. In: Raw ME, Parkinson TJ, editors. The veterinary annual, 36th issue. Oxford: Blackwell Science; 1996. p. 385-90.
47. Wen Y, Zhao YY, Li S, Polan ML, Chen BH. Differences in mRNA and protein expression of small proteoglycans in vaginal wall tissue from women with and without stress urinary incontinence. Hum Reprod 2007;22: 1718-24.
48. Goh JT. Biomechanical and biochemical assessments for pelvic organ prolapse. Curr Opin Obstet Gynecol 2003;15:391-4.
49. Doillon CJ, Dunn MG, Bender E, Silver FH. Collagen fiber formation in repair tissue: development of strength and toughness. Coll Relat Res 1985;5:481-92.
50. Niyibizi C, Eyre DR. Structural characteristics of cross-linking sites in type V collagen of bone. Chain specificities and heterotypic links to type I collagen. Eur J Biochem 1994;224:943-50.
51. Mizuno T, Mickle DA, Kiani CG, Li RK. Overexpression of elastin fragments in infarcted myocardium attenuates scar expansion and heart dysfunction. AmJ Physiol Heart Circ Physiol 2005;288:H2819-27.
52. Dobrin PB. Mechanical properties of arterises. Physiol Rev 1978;58:397-460.
53. Chen BH, Wen Y, Li H, Polan ML. Collagen metabolism and turnover in women with stress urinary incontinence and pelvic prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2002;13:80-7 [discussion 87].
54. Phillips CH, Anthony F, Benyon C, Monga AK. Collagen metabolism in the uterosacral ligaments and vaginal skin of womenwith uterine prolapse. BJOG 2006;113:39-46.
55. Lee UJ, Gustilo-Ashby AM, Daneshgari F, et al. Lower urogenital tract anatomical and functional phenotype in lysyl oxidase like-1 knockout mice resembles female pelvic floor dysfunction in humans. Am J Physiol Renal Physiol 2008;295:F545-55.
56. Liu X, Zhao Y, Gao J, et al. Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat Genet 2004;36:178-82.
57. Ulmsten U, Falconer C. Connective tissue in female urinary incontinence. Curr Opin Obstet Gynecol 1999;11:509-15.
58. Nakashima Y, Wight TN, Sueishi K. Early atherosclerosis in humans: role of diffuse intimal thickening and extracellular matrix proteoglycans. Cardiovasc Res 2008;79:14-23.
59. Kuettner KE, Kimura JH. Proteoglycans: an overview. J Cell Biochem 1985;27:327-36.
60. Yanagishita M. Proteoglycans and hyaluronan in female reproductive organs. EXS 1994;70:179-90.
61. Jackson SR, Avery NC, Tarlton JF, Eckford SD, Abrams P, Bailey AJ. Changes in metabolism of collagen in genitourinary prolapse. Lancet 1996;347:1658- 61.
62. Wong MY, Harmanli OH, Agar M, Dandolu V, Grody MH. Collagen content of nonsupport tissue in pelvic organ prolapse and stress urinary incontinence. Am J Obstet Gynecol 2003;189:1597-9 [discussion 1599-1600].
63. Woo SL, Ritter MA, Amiel D, et al. The biomechanical and biochemical properties of swine tendons-long term effects of exercise on the digital extensors. Connect Tissue Res 1980;7:177-83.
64. Prantil RL, Jankowski RJ, Kaiho Y, et al. Ex vivo biomechanical properties of the female urethra in a rat model of birth trauma. Am J Physiol Renal Physiol 2007;292:F1229-37.
65. Lowder JL, Debes KM, Moon DK, Howden N, Abramowitch SD, Moalli PA. Biomechanical adaptations of the rat vagina and supportive tissues in pregnancy to accommodate delivery. Obstet Gynecol 2007;109:136-43.
66. Damaser MS, Whitbeck C, Chichester P, Levin RM. Effect of vaginal distension on blood flow and hypoxia of urogenital organs of the female rat. J Appl Physiol 2005;98:1884-90.
67. Lin YH, Liu G, Daneshgari F. A mouse model of simulated birth trauma induced stress urinary incontinence. Neurourol Urodyn 2008;27:353-8.
68. Moalli PA, Debes KM, Meyn LA, Howden NS, Abramowitch SD. Hormones restore biomechanical properties of the vagina and supportive tissues after surgical menopause in young rats. Am J Obstet Gynecol 2008;199:161.e1-8.
69. Carley ME, Schaffer J. Urinary incontinence and pelvic organ prolapse in women with Marfan or Ehlers Danlos syndrome. Am J Obstet Gynecol 2000;182:1021-3.
70. Alperin M, Debes K, Abramowitch S, Meyn L, Moalli PA. LOXL1 deficiency negatively impacts the biomechanical properties of the mouse vagina and supportive tissues. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:977-86.
71. Rahn DD, Ruff MD, Brown SA, Tibbals HF, Word RA. Biomechanical properties of the vaginal wall: effect of pregnancy, elastic fiber deficiency, and pelvic organ prolapse. Am J Obstet Gynecol 2008;198:590.e1-6.
72. Drewes PG, Yanagisawa H, Starcher B, et al. Pelvic organ prolapse in fibulin-5 knockout mice: pregnancy-induced changes in elastic fiber homeostasis in mouse vagina. Am J Pathol 2007;170:578-89.
73. Lee TQ, Woo SL. A new method for determining cross-sectional shape and area of soft tissues. J Biomech Eng 1988;110:110-4.
74. Moon DK, Abramowitch SD, Woo SL. The development and validation of a charge-coupled device laser reflectance system to measure the complex cross-sectional shape and area of soft tissues. J Biomech 2006;39:3071-5.
75. Weiss JA, Gardiner JC, Bonifasi-Lista C. Ligament material behavior is nonlinear, viscoelastic and rate-independent under shear loading. J Biomech 2002;35:943-50.
76. Abramowitch SD, Papageorgiou CD, Debski RE, Clineff TD, Woo SL. A biomechanical and histological evaluation of the structure and function of the healing medial collateral ligament in a goat model. Knee Surg Sports Traumatol Arthrosc 2003;11:155-62.
77. Woo SL. Mechanical properties of tendons and ligaments. I. Quasi-static and nonlinear viscoelastic properties. Biorheology 1982;19:385-96.
78. Woo SL, Debski RE, Withrow JD, Janaushek MA. Biomechanics of knee ligaments. Am J Sports Med 1999;27:533-43.
79. Scheffler SU, Clineff TD, Papageorgiou CD, Debski RE, Ma CB, Woo SL. Structure and function of the healing medial collateral ligament in a goat model. Ann Biomed Eng 2001;29:173-80.
80. Woo SL, Orlando CA, Camp JF, Akeson WH. Effects of postmortem storage by freezing on ligament tensile behavior. J Biomech 1986;19:399-404.
81. Haut RC, Powlison AC. The effects of test environment and cyclic stretching on the failure properties of human patellar tendons. J Orthop Res 1990;8:532-40.
82. Lanir Y, Fung YC. Two-dimensional mechanical properties of rabbit skin. II. Experimental results. J Biomech 1974;7:171-82.
83. Pinto JG, Fung YC. Mechanical properties of the heart muscle in the passive state. J Biomech 1973;6:597-616.
84. Rubod C, Boukerrou M, Brieu M, Dubois P, Cosson M. Biomechanical properties of vaginal tissue. Part 1: new experimental protocol. J Urol 2007;178:320-5 [discussion 325].
85. Woo SL, Fisher MB, Feola AJ. Contribution of biomechanics to management of ligament and tendon injuries. Mol Cell Biomech 2008;5:49-68.
86. Woo SL, Hollis JM, Adams DJ, Lyon RM, Takai S. Tensile properties of the human femur-anterior cruciate ligament-tibia complex. The effects of specimen age and orientation. Am J Sports Med 1991;19:217-25.
87. Woo SL, Lee TQ, Gomez MA, Sato S, Field FP. Temperature dependent behavior of the canine medial collateral ligament. J Biomech Eng 1987;109: 68-71.
88. Yin FC, Fung YC. Mechanical properties of isolated mammalian ureteral segments. Am J Physiol 1971;221:1484-93.
89. Moon DK, Woo SL, Takakura Y, Gabriel MT, Abramowitch SD. The effects of refreezing on the viscoelastic and tensile properties of ligaments. J Biomech 2006;39:1153-7.
90. Humphrey JD. Continuum biomechanics of soft biological tissues. Royal Soc 2003;459:3-46.
91. Sacks MS. Biaxial mechanical evaluation of planar biological materials. J Elast 2000;61:199-246.
92. Abramowitch SD, Woo SL, Clineff TD, Debski RE. An evaluation of the quasilinear viscoelastic properties of the healing medial collateral ligament in a goat model. Ann Biomed Eng 2004;32:329-35.
93. Chan RW, Titze IR. Viscoelastic shear properties of human vocal fold mucosa: measurement methodology and empirical results. J Acoust Soc Am 1999; 106:2008-21.
94. Funk JR, Hall GW, Crandall JR, Pilkey WD. Linear and quasi-linear viscoelastic characterization of ankle ligaments. J Biomech Eng 2000;122:15-22.
95. Haut RC, Little RW. A constitutive equation for collagen fibers. J Biomech 1972;5:423-30.
96. Provenzano P, Lakes R, Keenan T, Vanderby Jr R. Nonlinear ligament viscoelasticity. Ann Biomed Eng 2001;29:908-14.
97. Rubod C, Boukerrou M, Brieu M, Jean-Charles C, Dubois P, Cosson M. Biomechanical properties of vaginal tissue: preliminary results. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:811-6.
98. Cosson M, Lambaudie E, Boukerrou M, Lobry P, Crepin G, Ego A. A biomechanical study of the strength of vaginal tissues. Results on 16 post-menopausal patients presentingwith genital prolapse. Eur J Obstet Gynecol Reprod Biol 2004;112:201-5.
99. Goh JT. Biomechanical properties of prolapsed vaginal tissue in pre- and postmenopausal women. Int Urogynecol J Pelvic Floor Dysfunct 2002;13:76- 9 [discussion 79].
100. Lei L, Song Y, Chen R. Biomechanical properties of prolapsed vaginal tissue in pre- and postmenopausal women. Int Urogynecol J Pelvic Floor Dysfunct 2007;18:603-7.
101. Vakili B, Zheng YT, Loesch H, Echols KT, Franco N, Chesson RR. Levator contraction strength and genital hiatus as risk factors for recurrent pelvic organ prolapse. Am J Obstet Gynecol 2005;192:1592-8.
102. Weidner AC, Barber MD, Visco AG, Bump RC, Sanders DB. Pelvic muscle electromyography of levator ani and external anal sphincter in nulliparous women and women with pelvic floor dysfunction. Am J Obstet Gynecol 2000;183:1390-9 [discussion 1399-1401].
103. Boreham MK, Miller RT, Schaffer JI, Word RA. Smooth muscle myosin heavy chain and caldesmon expression in the anterior vaginal wall of women with and without pelvic organ prolapse. Am J Obstet Gynecol 2001;185:944-52.
104. Ozdegirmenci O, Karslioglu Y, Dede S, et al. Smooth muscle fraction of the round ligament in women with pelvic organ prolapse: a computer-based morphometric analysis. Int Urogynecol J Pelvic Floor Dysfunct 2005;16:39- 43 [discussion 43].
105. Takacs P, Gualtieri M, Nassiri M, Candiotti K, Medina CA. Vaginal smooth muscle cell apoptosis is increased in women with pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:1559-64.