Research Papers

In Vivo Properties of Uterine Suspensory Tissue in Pelvic Organ Prolapse

[+] Author and Article Information
Jiajia Luo

Biomechanics Research Laboratory,
Department of Mechanical Engineering,
2350 Hayward Street,
GG Brown Building 3212,
University of Michigan,
Ann Arbor, MI 48109;
Pelvic Floor Research Group,
University of Michigan,
Ann Arbor, MI 48109
e-mail: jjluo@umich.edu

Tovia M. Smith, John O. L. DeLancey

Department of Obstetrics and Gynecology,
University of Michigan,
Ann Arbor, MI 48109;
Pelvic Floor Research Group,
University of Michigan,
Ann Arbor, MI 48109

James A. Ashton-Miller

Biomechanics Research Laboratory,
Department of Mechanical Engineering,
University of Michigan,
Ann Arbor, MI 48109;
Pelvic Floor Research Group,
University of Michigan,
Ann Arbor, MI 48109

1Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the Journal of Biomechanical Engineering. Manuscript received September 6, 2013; final manuscript received November 26, 2013; accepted manuscript posted December 3, 2013; published online February 5, 2014. Editor: Victor H. Barocas.

J Biomech Eng 136(2), 021016 (Feb 05, 2014) (6 pages) Paper No: BIO-13-1415; doi: 10.1115/1.4026159 History: Received September 06, 2013; Revised November 26, 2013; Accepted December 03, 2013

The uterine suspensory tissue (UST), which includes the cardinal (CL) and uterosacral ligaments (USL), plays an important role in resisting pelvic organ prolapse (POP). We describe a technique for quantifying the in vivo time-dependent force-displacement behavior of the UST, demonstrate its feasibility, compare data from POP patients to normal subjects previously reported, and use the results to identify the properties of the CL and USL via biomechanical modeling. Fourteen women with prolapse, without prior surgeries, who were scheduled for surgery, were selected from an ongoing study on POP. We developed a computer-controlled linear servo actuator, which applied a continuous force and simultaneously recorded cervical displacement. Immediately prior to surgery, the apparatus was used to apply three “ramp and hold” trials. After a 1.1 N preload was applied to remove slack in the UST, a ramp rate of 4 mm/s was used up to a maximum force of 17.8 N. Each trial was analyzed and compared with the tissue stiffness and energy absorbed during the ramp phase and normalized final force during the hold phase. A simplified four-cable model was used to analyze the material behavior of each ligament. The mean ± SD stiffnesses of the UST were 0.49 ± 0.13, 0.61 ± 0.22, and 0.59 ± 0.2 N/mm from trial 1 to 3, with the latter two values differing significantly from the first. The energy absorbed significantly decreased from trial 1 (0.27 ± 0.07) to 2 (0.23 ± 0.08) and 3 (0.22 ± 0.08 J) but not from trial 2 to 3. The normalized final relaxation force increased significantly with trial 1. Modeling results for trial 1 showed that the stiffnesses of CL and USL were 0.20 ± 0.06 and 0.12 ± 0.04 N/mm, respectively. Under the maximum load applied in this study, the strain in the CL and USL approached about 100%. In the relaxation phase, the peak force decreased by 44 ± 4% after 60 s. A servo actuator apparatus and intraoperative testing strategy proved successful in obtaining in vivo time-dependent material properties data in representative sample of POP. The UST exhibited visco-hyperelastic behavior. Unlike a knee ligament, the length of UST could stretch to twice their initial length under the maximum force applied in this study.

Copyright © 2014 by ASME
Your Session has timed out. Please sign back in to continue.


Olsen, A. L., Smith, V. J., Bergstrom, J. O., Colling, J. C., and Clark, A. L., 1997, “Epidemiology of Surgically Managed Pelvic Organ Prolapse and Urinary Incontinence,” Obstet. Gynecol., 89(4), pp. 501–506. [CrossRef] [PubMed]
Boyles, S. H., Weber, A. M., and Meyn, L., 2003, “Procedures for Pelvic Organ Prolapse in the United States, 1979–1997,” Am. J. Obstet. Gynecol., 188(1), pp. 108–115. [CrossRef] [PubMed]
Subak, L. L., Waetjen, L. E., Van Den Eeden, S., Thom, D. H., Vittinghoff, E., and Brown, J. S., 2001, “Cost of Pelvic Organ Prolapse Surgery in the United States,” Obstet. Gynecol., 98(4), pp. 646–651. [CrossRef] [PubMed]
Chen, L., Ashton-Miller, J. A., Hsu, Y., and DeLancey, J. O., 2006, “Interaction Among Apical Support, Levator Ani Impairment, and Anterior Vaginal Wall Prolapse,” Obstet. Gynecol., 108(2), pp. 324–332. [CrossRef] [PubMed]
Kearney, R., Miller, J. M., Ashton-Miller, J. A., and DeLancey, J. O., 2006, “Obstetric Factors Associated With Levator Ani Muscle Injury After Vaginal Birth,” Obstet. Gynecol., 107(1), pp. 144–149. [CrossRef] [PubMed]
Ashton-Miller, J. A., and DeLancey, J. O., 2009, “On the Biomechanics of Vaginal Birth and Common Sequelae,” Annu. Rev. Biomed. Eng., 11, pp. 163–176. [CrossRef] [PubMed]
Pearce, M., Swift, S., and Goodnight, W., 2008, “Pelvic Organ Prolapse: Is There a Difference in POPQ Exam Results Based on Time of Day, Morning or Afternoon?,” Am. J. Obstet. Gynecol., 199(2), pp. 200.e1–200.e5. [CrossRef]
Summers, A., Winkel, L. A., Hussain, H. K., and DeLancey, J. O., 2006, “The Relationship Between Anterior and Apical Compartment Support,” Am. J. Obstet. Gynecol., 194(5), pp. 1438–1443. [CrossRef] [PubMed]
DeLancey, J. O., 1992, “Anatomic Aspects of Vaginal Eversion After Hysterectomy,” Am. J. Obstet. Gynecol., 166(6 Pt 1), pp. 1717–1724. [CrossRef] [PubMed]
Ramanah, R., Berger, M. B., Chen, L. Y., Riethmuller, D., and DeLancey, J. O. L., 2012, “See It in 3D! Researchers Examined Structural Links Between the Cardinal and Uterosacral Ligaments,” Am. J. Obstet. Gynecol., 207(5), pp. 437.e1–437.e7. [CrossRef]
Luo, J., Ashton-Miller, J. A., and DeLancey, J. O. L., 2011, “A Model Patient: Female Pelvic Anatomy can be Viewed in Diverse 3-Dimensional Images With a New Interactive Tool,” Am. J. Obstet. Gynecol., 205(4), pp. 391.e1–391.e2. [CrossRef]
Fung, Y., 1993, Biomechanics: Mechanical Properties of Living Tissues, 2nd ed., Springer, New York.
Woo, S. L.-Y., Hollis, J. M., Adams, D. J., Lyon, R. M., and Takai, S., 1991, “Tensile Properties of the Human Femur-Anterior Cruciate Ligament-Tibia Complex the Effects of Specimen Age and Orientation,” Am. J. Sports Med., 19(3), pp. 217–225. [CrossRef] [PubMed]
Campbell, R. M., 1950, “The Anatomy and Histology of the Sacrouterine Ligaments,” Am. J. Obstet. Gynecol., 59(1), pp. 1–12. [PubMed]
Range, R. L., and Woodburne, R. T., 1964, “The Gross and Microscopic Anatomy of the Transverse Cervical Ligament,” Am. J. Obstet. Gynecol., 90, pp. 460–467. [PubMed]
Cole, E. E., Leu, P. B., Gomelsky, A., Revelo, P., Shappell, H., Scarpero, H. M., and Dmochowski, R. R., 2006, “Histopathological Evaluation of the Uterosacral Ligament: Is This a Dependable Structure for Pelvic Reconstruction?,” BJU Int., 97(2), pp. 345–348. [CrossRef] [PubMed]
Ramanah, R., Berger, M. B., Parratte, B. M., and DeLancey, J. O., 2012, “Anatomy and Histology of Apical Support: A Literature Review Concerning Cardinal and Uterosacral Ligaments,” Int. Urogynecol. J., 23(11), pp. 1483–1494. [CrossRef] [PubMed]
Vu, D., Haylen, B. T., Tse, K., and Farnsworth, A., 2010, “Surgical Anatomy of the Uterosacral Ligament,” Int. Urogynecol. J., 21(9), pp. 1123–1128. [CrossRef] [PubMed]
Bump, R. C., Mattiasson, A., Bo, K., Brubaker, L. P., DeLancey, J. O., Klarskov, P., Shull, B. L., and Smith, A. R., 1996, “The Standardization of Terminology of Female Pelvic Organ Prolapse and Pelvic Floor Dysfunction,” Am. J. Obstet. Gynecol., 175(1), pp. 10–17. [CrossRef] [PubMed]
Bartscht, K. D., and DeLancey, J. O., 1988, “A Technique to Study the Passive Supports of the Uterus,” Obstet. Gynecol., 72(6), pp. 940–943. [PubMed]
Foon, R., Agur, W., Kingsly, A., White, P., and Smith, P., 2012, “Traction on the Cervix in Theatre Before Anterior Repair: Does It Tell Us When to Perform a Concomitant Hysterectomy?,” Eur. J. Obstet. Gynecol. Reprod. Biol., 160(2), pp. 205–209. [CrossRef] [PubMed]
Chen, L., Ramanah, R., Hsu, Y., Ashton-Miller, J. A., and DeLancey, J. O., 2013, “Cardinal and Deep Uterosacral Ligament Lines of Action: MRI Based 3D Technique Development and Preliminary Findings in Normal Women,” Int. Urogynecol. J., 24(1), pp. 37–45. [CrossRef] [PubMed]
Hsu, Y., Summers, A., Hussain, H. K., Guire, K. E., and DeLancey, J. O., 2006, “Levator Plate Angle in Women With Pelvic Organ Prolapse Compared to Women With Normal Support Using Dynamic MR Imaging,” Am. J. Obstet. Gynecol., 194(5), pp. 1427–1433. [CrossRef] [PubMed]
Luo, J., Betschart, C., Chen, L., Ashton-Miller, J. A., and DeLancey, J. O., 2013, “Using Stress MRI to Analyze the 3D Changes in Apical Ligament Geometry From Rest to Maximal Valsalva: A Pilot Study,” Int. Urogynecol. J. (in press). [CrossRef]
Reay Jones, N., Healy, J., King, L., Saini, S., Shousha, S., and Allen-Mersh, T., 2003, “Pelvic Connective Tissue Resilience Decreases With Vaginal Delivery, Menopause and Uterine Prolapse,” Br. J. Surg., 90(4), pp. 466–472. [CrossRef] [PubMed]
Rivaux, G., Rubod, C., Dedet, B., Brieu, M., Gabriel, B., and Cosson, M., 2013, “Comparative Analysis of Pelvic Ligaments: A Biomechanics Study,” Int. Urogynecol. J., 24(1), pp. 135–139. [CrossRef] [PubMed]
Martins, P., Silva-Filho, A. L., Fonseca, A. M., Santos, A., Santos, L., Mascarenhas, T., Jorge, R. M., and Ferreira, A. M., 2013, “Strength of Round and Uterosacral Ligaments: A Biomechanical Study,” Arch. Gynecol. Obstet., 287(2), pp. 313–318. [CrossRef] [PubMed]
Moalli, P. A., Shand, S. H., Zyczynski, H. M., Gordy, S. C., and Meyn, L. A., 2005, “Remodeling of Vaginal Connective Tissue in Patients With Prolapse,” Obstet. Gynecol., 106(5 Pt 1), pp. 953–963. [CrossRef] [PubMed]
Gabriel, B., Watermann, D., Hancke, K., Gitsch, G., Werner, M., Tempfer, C., and Zur Hausen, A., 2006, “Increased Expression of Matrix Metalloproteinase 2 in Uterosacral Ligaments Is Associated With Pelvic Organ Prolapse,” Int. Urogynecol. J., 17(5), pp. 478–482. [CrossRef]
Ewies, A. A., Al-Azzawi, F., and Thompson, J., 2003, “Changes in Extracellular Matrix Proteins in the Cardinal Ligaments of Post-Menopausal Women With or Without Prolapse: A Computerized Immunohistomorphometric Analysis,” Hum. Reprod., 18(10), pp. 2189–2195. [CrossRef] [PubMed]
Rahn, D. D., Ruff, M. D., Brown, S. A., Tibbals, H. F., and Word, R. A., 2008, “Biomechanical Properties of the Vaginal Wall: Effect of Pregnancy, Elastic Fiber Deficiency, and Pelvic Organ Prolapse,” Am. J. Obstet. Gynecol., 198(5), pp. 590.e1–590.e6. [CrossRef]
Chen, L., Ashton-Miller, J. A., and DeLancey, J. O., 2009, “A 3D Finite Element Model of Anterior Vaginal Wall Support to Evaluate Mechanisms Underlying Cystocele Formation,” J. Biomech., 42(10), pp. 1371–1377. [CrossRef] [PubMed]
Lipps, D. B., Oh, Y. K., Ashton-Miller, J. A., and Wojtys, E. M., 2012, “Morphologic Characteristics Help Explain the Gender Difference in Peak Anterior Cruciate Ligament Strain During a Simulated Pivot Landing,” Am. J. Sports Med., 40(1), pp. 32–40. [CrossRef] [PubMed]


Grahic Jump Location
Fig. 1

Anatomy of female uterine suspensory tissue in a 3D model based on MRI of a healthy control. Note the pelvis (P) and sacrum (S) are transparent in (a) and have been deleted in (b), as viewed from the left, and in (c) in a left oblique view. U denotes uterus; Cx: cervix; V: vagina; CL: cardinal ligament; and USL: uterosacral ligament. Modified from Luo, et al. [11] © Luo, Ashton-Miller, and DeLancey.

Grahic Jump Location
Fig. 2

Schematic of the test setup. Zero indicates the location of the hymen, with –/+ meaning above or below the hymen. S denotes sacrum; U: uterus; P: pubic bone; and Cx: cervix. A, B and C denote the servo actuator, force transducer, and surgical tenaculum, respectively; D the tripod; E the motor controller; and F the microprocessor. Vertical dashed-dotted line represents the initial location of the hymenal ring. This defines the origin (“0”) for the pelvic organ prolapse measurement system used to assess uterine position. The dashed long and short lines represent the CL and USL, respectively, under load. Note the 1 m long vertical suture suspending the weight of C © Luo, Ashton-Miller, and DeLancey.

Grahic Jump Location
Fig. 3

Results from a typical “ramp and hold” test of UST (Study ID S005, trial 1). (a) shows displacement versus time, (b) force versus time, and (c) force versus displacement. In (b), arrows indicate respiratory cycles wherein the downward force created by lung expansion caused a temporary force decrease.

Grahic Jump Location
Fig. 4

MR-based four-cable 3D biomechanical model of UST. (a) Cardinal ligament (CL), uterosacral ligament (USL), uterus (U), cervix (Cx), vagina (V), and outline of rectum (R) and levator plate. At right (b) are shown the four-cable free body diagram at time 0 and time t (c). The applied test force was assumed to be parallel to the levator plate. LPA denotes levator plate angle.

Grahic Jump Location
Fig. 5

Force and displacement behavior of prolapse women (trial 1, 2, and 3) compared to women without prolapse (Bartscht and DeLancey) displayed as mean and SD (whisker plot and shaded area). The data are shown in interval format for comparison with the Bartscht and DeLancey results

Grahic Jump Location
Fig. 6

UST geometric stiffness, energy absorbed, and normalized final force by trial

Grahic Jump Location
Fig. 7

Fit hyperelastic properties of CL/USL

Grahic Jump Location
Fig. 8

The fitted normalized force relaxation function for UST, CL, and USL during the hold phase



Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In