If the Leg to Be Supported Weighs 46.0 N , What Must Be the Weight of W?
Int Urogynecol J. Author manuscript; available in PMC 2017 Aug ane.
Published in final edited form as:
PMCID: PMC4947418
NIHMSID: NIHMS773235
Traction force needed to reproduce physiologically observed uterine movement: technique development, feasibility assessment, and preliminary findings
Carolyn Westward. Swenson
oneDepartment of Obstetrics and Gynecology, Academy of Michigan, L4000 Women'due south Infirmary, 1500 E. Medical Center Dr., SPC 5276, Ann Arbor, MI 48109-5276, USA
Jiajia Luo
iiDepartment of Mechanical Engineering, University of Michigan, L4000 Women's Hospital, 1500 E. Medical Heart Dr., SPC 5276, Ann Arbor, MI 48109-5276, USA
Luyun Chen
threeDepartment of Biomedical Engineering, University of Michigan, L4000 Women's Hospital, 1500 E. Medical Center Dr., SPC 5276, Ann Arbor, MI 48109-5276, United states of america
James A. Ashton-Miller
2Department of Mechanical Engineering, Academy of Michigan, L4000 Women's Hospital, 1500 E. Medical Center Dr., SPC 5276, Ann Arbor, MI 48109-5276, United states
3Department of Biomedical Applied science, Academy of Michigan, L4000 Women's Infirmary, 1500 E. Medical Middle Dr., SPC 5276, Ann Arbor, MI 48109-5276, U.s.a.
John O. L. DeLancey
aneDepartment of Obstetrics and Gynecology, University of Michigan, L4000 Women'south Infirmary, 1500 E. Medical Center Dr., SPC 5276, Ann Arbor, MI 48109-5276, U.s.
Abstract
Introduction and hypothesis
This study aimed to draw a novel strategy to determine the traction forces needed to reproduce physiologic uterine displacement in women with and without prolapse.
Methods
Participants underwent dynamic stress magnetic resonance imaging (MRI) testing equally function of a study examining apical uterine back up. Physiologic uterine displacement was determined past analyzing uterine location in images taken at residue and at maximal Valsalva. Force-displacement curves were calculated based on intraoperative cervical traction testing. The intraoperative force required to achieve the uterine displacement measured during MRI was then estimated from these curves. Women were categorized into three groups based on pelvic organ back up: group 1 (normal upmost and vaginal back up), grouping 2 (normal apical support but vaginal prolapse present), and grouping 3 (apical prolapse).
Results
Data from 19 women were analyzed: five in group 1, five in group ii, and 9 in group iii. Groups were like in terms of age, trunk mass index (BMI), and parity. Median operating room (OR) force required for uterine deportation measured during MRI was 0.8 Northward [interquartile range (IQR) 0.62–3.22], and apical ligament stiffness determined using MRI uterine displacement was 0.04 Northward/mm (IQR 0.02–0.08); differences between groups were nonsignificant. Uterine locations determined at residual and during maximal traction were lower in the OR compared with MRI in all groups.
Conclusions
Using this investigative strategy, we determined that only 0.8 N of traction force in the OR was required to attain maximal physiologic uterine displacement seen during dynamic (maximal Valsalva) MRI testing, regardless of the presence or absenteeism of prolapse.
Keywords: Apical support, Prolapse, Uterine movement
Introduction
Agreement physiological movements of the uterus in healthy women and how it differs in women with prolapse is an essential part of understanding the etiology of pelvic organ prolapse (POP). Clinically, this information is important for surgical decision making regarding which women with prolapse should have a hysterectomy and which should non. At nowadays, wide variations exist among physicians in their opinions virtually this upshot. One survey of doc opinion on this subject field that asked gynecologists whether they would perform a hysterectomy at five different levels of uterine support revealed a l % disagreement charge per unit [1]. This departure of stance exists in part because of an incomplete understanding of how to appropriately assess upmost support and a subsequent lack of noesis regarding the threshold of uterine descent at which hysterectomy should be performed.
The field of biomechanics has a long history of evaluating the functional limits of biological materials. Ideally, measurements should be made that are relevant to the physiological situation encountered during a range of normal activities. At present, much of the available data concerning biomechanical properties of apical suspensory ligaments (central and uterosacral) come from artificial exam situations, which may not necessarily reverberate how they are loaded in vivo. For instance, it is common to perform in vitro uniaxial tension tests on small excised pieces of the uterosacral ligaments and then calculate the tissue stress–strain curves [2, 3]. More recently, in vivo tests performed using cervical traction in the operating room (OR) resulted in force-displacement curves from which the stiffness of the fundamental and uterosacral ligament complexes were calculated [4, 5]. Whether either of these are physiologically relevant measures is unclear.
Dynamic stress magnetic resonance imaging (MRI) provides a means of assessing the relationship betwixt physiological uterine descent and changes in intestinal pressure level [six]. However, the critical question concerning how the forces practical along the ligaments with changes in abdominal pressure chronicle to electric current measurements of in vitro and in vivo ligament backdrop remains unanswered. During our work in measuring the in vivo force-deportation behavior of the cardinal and uterosacral ligaments, information technology became evident that one might be able to estimate the forces placed on the suspensory ligament complex required to reproduce physiologically observed uterine displacement during MRI testing. In other words: How much cervical traction force is required to reproduce the movement seen during a Valsalva maneuver of known pressure level?
The aim of our study was to describe a new investigative strategy to address these cognition gaps, demonstrate the feasibility of using it in women with and without prolapse, and present preliminary data apropos the consequence sizes that tin can exist used in planning future large-scale studies. Results of this mechanistic written report volition be presented in 2 parts. In Role one, we compare force displacement behavior in physiologically observed uterine displacement with intraoperative measures. In Role two, we compare uterus location observed during physiological testing in MRI with intraoperative measurement in the OR.
Methods
This was an analysis of a subset of women who underwent MRI as function of a written report at the Academy of Michigan (Ann Arbor, MI, USA) examining apical uterine support (IRB approving HUM00056743) from September 2012 to September 2013. Women with a full spectrum of pelvic organ support from normal to prolapse were recruited from the gynecology clinics. Inclusion criteria were age ≥18 years planning to have benign gynecologic surgery and willing to undergo MRI. Exclusion criteria were pregnancy (currently or within the past year), prior hysterectomy or surgery for POP, uterine fibroids for >12 weeks or known pelvic inflammatory illness, chronic steroid apply, prior pelvic radiation, electric current handling for cancer, history of organ transplant, history of vasovagal syncope, neurologic diseases or impairments, mobility bug that would prohibit leg positioning in high lithotomy, metal implants, and claustrophobia or any other contraindications to undergoing MRI.
Women were divided into three groups for analysis according to their pelvic support and cervix location as measured past the Pelvic Organ Quantification (Pop-Q) system. We defined upmost prolapse equally C ≥ −4. and vaginal wall prolapse as Ba and/or Bp ≥ 0. Group 1 comprised women with normal upmost and vaginal support, grouping two were women with normal apical support but prolapse of the inductive or posterior vaginal walls, and group three comprised women with apical prolapse. Of the nine individuals in group 3, seven also had prolapse of the anterior and posterior vaginal walls. We chose to analyze these groups separately because they may differ in terms of upmost ligament backdrop.
Women underwent dynamic stress MRI in the supine position prior to surgery using a multiple Valsalva technique to achieve maximal prolapse, which has been previously described and validated [vii]. MRI was reviewed to confirm that the prolapse was similar in size to that seen during clinical Pop-Q examination. Proton-density-weighted fast spin-echo imaging was performed in the axial, sagittal, and coronal planes using a iii-Tesla (three-T) Ingenia MRI scanner (Philips Medical Systems, Best, Kingdom of the netherlands). Slice thickness was 4 mm with a one mm gap. Prior to imaging, a Foley catheter was placed in the float and fastened to a pressure transducer to monitor abdominal pressure. Twenty milliliters of ultrasound gel were placed in the vagina to delineate the borders. Midsagittal images were taken at remainder and during maximal Valsalva. We chose a maximal Valsalva as is washed clinically rather than a standardized target pressure level for two reasons: First, having a standardized pressure that all individuals are required to achieve requires using a low enough value that all women tin generate information technology, thereby preventing many women from reaching pressures where prolapse is maximally developed. Second, it is hard for women to conform their endeavour during scanning considering they are more inhibited, resulting in a suboptimal effort. One time caused, the images were then used to determine 10 and Y coordinates for the post-obit points: posterior pubic bone, inferomedial aspect of the fifth sacral vertebra, midpoint of the external cervical os, and the hymenal ring. These coordinates were measured using ImageJ software (Version one.47, National Institutes of Wellness, Bethesda, Doctor, USA) [viii] and were verified independently past two experienced researchers for all MRIs. Upon reviewing the images, nosotros observed that with Valsalva, the hymenal band also moved; therefore, measurements of cervix location relative to the hymenal ring may actually underestimate truthful uterine movement. In order to more accurately compare uterine move during MRI to that seen in the OR, nosotros had to calculate the change in cervix location along a plane parallel to the long body axis. The Pelvic Inclination Correction Arrangement uses a reference line perpendicular to the long body axis [9]. Therefore, we calculated the vertical distance of the cervix from this reference line at rest (dresidual) and during maximal Valsalva (dValsalva). Total vertical move of the cervix was then= ∣dValsalva – drest∣ (Figs. 1 and 2).
Uterine displacement in magnetic resonance imaging vs in the operating room
Analogy of how to calculate vertical movement of the cervix using the Pelvic Inclination Correction Organization (PICS), accounting for pelvic rotation that occurs during Valsalva. P inferior point of the pubic bone; C midpoint of external cervical bone; SCIPP sacrococcygeal-junior pubic signal; d rest vertical distance of the cervix from the PICS line at remainder (negative values above the PICS line, positive values below the PICS line); d Valsalva vertical distance of the neck from the PICS line during maximal Valsalva. Full vertical movement of the cervix = ∣dValsalva – drest∣
The technique for making measurements of cervix location in the OR using a computer-controlled servoactuator device has been previously described [four] and is shown in Fig. iii. To summarize, after induction of anesthesia, location of the anterior lip of the cervix was assessed in the supine position with the legs slightly spread (frog-leg position). The legs were placed in high lithotomy position, and a brusk-blade Sherback posterior-weight vaginal speculum was placed. A single-molar tenaculum was and so placed across both the anterior and posterior cervical lips and the handle attached to the servoactuator device. Prior to activating the device, resting cervix location was adamant by measuring the altitude of the lateral cervical edge to the hymenal ring (Residuum). The servoactuator so moved at a constant speed to utilise a steadily increasing tensile force to the cervix of upwardly to four lbs (17.8 N) while simultaneously recording the position of the traction arm. Cervix location at maximal force was determined from these information. Using the force-displacement curves generated during OR testing, we calculated the OR strength required to attain the uterine deportation measured under physiological conditions during MRI. For case, if the uterus descended two cm with maximal Valsalva in the MRI, we used the strength-displacement curve information measured in the OR to determine the bodily force needed for ii cm of uterine displacement from the resting location for that patient. An estimated stiffness of apical supports of the uterus was calculated by dividing this strength by the uterine movement seen in MRI.
A computer-controlled servoactuator (a) with strength transducer (b) mounted on a tripod (c) quantifying force-displacement beliefs of the uterine cervix while applying caudally directed tensile force to the handle of a tenaculum (d) supported past a vertical support (e) and attached to the cervix. Blue arrow indicates force vector. Modified from [4]
We performed descriptive statistics on demographic variables of age, parity, and body mass index (BMI, kg/m2), as well every bit clinic Pop-Q points. All data were checked for the assumption of normality. Unremarkably distributed data were analyzed using assay of variance (ANOVA), while Kruskal–Wallis and Wilcoxon signed-rank tests were used for nonnormally distributed data. Data analyses were performed using SPSS xix statistical software. Statistical significance was defined at the 5 % significance level.
Results
Twenty women met inclusion criteria; one adult female was eventually excluded, equally she was unable to effectively perform a Valsalva maneuver during MRI. Therefore, nineteen women were included in the final analyses: v with normal pelvic back up (group i), five with normal apical back up just vaginal prolapse (grouping two), and nine with apical prolapse (group 3). Demographics of the three groups are shown in Table 1. Although there were some differences, groups were statistically like. Past design, women in groups one and 2 had like neck locations, while those in grouping 3 had lower cervix location on POP-Q exam.
Tabular array ane
Demographics of 3 groups of women with varying degrees of pelvic organ support
| Group ane Normal support (n = 5) | Grouping 2 Normal apex/Vaginal prolapse (n = five) | Group 3 Upmost prolapse (northward = nine) | P value | |
|---|---|---|---|---|
| Historic period, years | 46.2 ± 10.four | 52.2 ± 14.3 | 57.7 ± 10.4 | .23 |
| Parity | 1 (0–3) | 3 (2–3) | iii (0–4) | .eleven |
| BMI kg/thou2 | 29.9 ± half dozen.8 | 28.0 ± iv.6 | 28.0 ± 7.70 | .87 |
| Popular-Q betoken C | −6 (−7 to −half-dozen) | −5 (−10 to −five) | −iii (−iv to 5) | .001 |
| Signal Ba | −2 (−3 to −1) | 1 (0 to 3) | 1 (−one to v) | .006 |
| Point Bp | −3 (−3 to −1) | 0 (−2 to 0) | −1 (−3 to 0) | .11 |
Part 1: During MRI, women in group 1 had the smallest amount of total uterine movement (uterine displacement) (Tabular array 2). Compared with group 1, the uterus moved twice as much in group ii and 2.five times further in group 3. Intestinal pressure generated during maximal Valsalva in the MRI machine was then compared across groups. Abdominal pressure was highest in women in grouping i, but the differences across the three groups did not differ significantly. For all groups, the traction strength needed to obtain physiologic uterine move seen in the MRI was <1 N and was similar across groups. Likewise, estimated stiffness was low and similar across groups.
Tabular array 2
Uterine displacement in magnetic resonance imaging (MRI)
| All (n = 19) | Group i Normal back up (n = v) | Group 2 Normal apex/Vaginal prolapse (northward = 5) | Group three Apical prolapse (n = nine) | P value | |
|---|---|---|---|---|---|
| OR force required for MRI uterine displacement (N) | 0.80 (0.62 to 3.22) | 0.79 (0.31 to 3.16) | 0.62 (0.52 to i.39) | 0.88 (0.77 to eight.53) | .06 |
| MRI uterine displacement (cm)a | three.five (2.1 to iv.half-dozen) | i.nine (one.1 to 2.5) | 3.nine (two.iii to four.3) | 4.6 (iii.4 to v.7) | .01 |
| MRI abdominal pressure generated during uterine displacement (mmHg) | 55.0 (46.0 to 71.0) | 71.0 (46.5 to 83.0) | 49.0 (28.0 to 70.0) | 55.0 (47.5 to 64.0) | .38 |
| MRI apical ligament stiffness (North/mm)b | 0.04 (0.02 to 0.08) | 0.04 (0.03 to 0.12) | 0.02 (0.01 to 0.05) | 0.04 (0.02 to 0.14) | .47 |
Part 2: Comparison of cervix locations at rest and during maximal traction in MRI vs OR is shown in Fig. iv and numerical information presented in Supplemental Table S1. In all groups, cervix location at residuum was consistently and significantly more caudal in the OR than in MRI. Similar results were found for neck location at maximal traction. Uterine displacement was significantly greater in the OR vs MRI in women in groups one and 2; however, the uterus moved a similar amount in the OR and MRI in the women in group iii. When we analyzed the human relationship between uterine deportation and abdominal pressure generated during maximal Valsalva, we institute that uterine motion was most highly correlated with intestinal pressure in group 1 (R 2 = 0.91, p = .01) vs group two (R ii = 0.43, p = .23) and grouping 3 (R two = 0.07, p = .48).
Uterine location at rest and during maximal traction in magnetic resonance imaging (MRI) vs operating room (OR). All locations shown as millimeters relative to the hymenal ring, which is defined as 0. *Statistical significance, p < .05
To place whether a difference in leg positioning (supine in MRI and high lithotomy in the OR) was a possible explanation for why cervix location was lower in the OR, nosotros compared resting cervix location in the frog-leg position to that in the lithotomy position (Fig. five). In all iii groups, we plant similar resting cervix locations with MRI and OR frog-leg positioning (data presented in Supplemental Table S2).
Uterine Location at Rest: supine in magnetic resonance imaging (MRI) vs Frog-Leg in operating room (OR). All locations shown as millimeters relative to the hymenal ring, which is divers as 0. No significant differences observed between resting locations in all groups
Give-and-take
We nowadays a novel technique that allows estimation of the amount of tension placed on the upmost supports during measured physiological changes in abdominal pressure level. A remarkably small traction forcefulness, equivalent to <0.two lb (90 k), was required in the OR to replicate the physiologic uterine motility seen during MRI. To add perspective, a standard metallic Grave'southward bivalve speculum weighs ~0.4 lb (181 g), which is double the upper limit of the amount of traction force required for maximal uterine movement in the current report. Therefore, the tension placed on the apical ligaments during physiologic events such equally Valsalva is pocket-size. These findings advise that the factors involved in determining the location of the uterus are more than complex than are simply accounted for by the mechanical properties of the upmost supports.
Regarding clinical relevance of our findings: It is common do for surgeons to apply intraoperative cervical traction in club to appraise the caste of uterine descent. A decision regarding whether or non a hysterectomy and/or apical suspension process will be performed is frequently based on the degree of uterine descent seen during this assessment. A study past Foon et al. constitute that the average traction force applied during this intraoperative assessment for ten gynecologists was 7.9 lb (3.6 kg) [10]. However, our results show that this traction force is 40 times higher than the force required in the OR to achieve maximal physiologic uterine descent during maximal Valsalva in the MRI. Therefore, because supraphysiologic cervical traction may yield a greater caste of uterine descent, this common practice may be biasing surgeons toward performing unnecessary procedures, such as hysterectomy.
Regarding how these findings relate to mechanical backdrop published in the literature: We calculated apical ligament stiffness using the OR force data and uterine deportation seen during MRI. Apical ligament stiffness was low and did non differ by prolapse group. However, results from in vitro ligament stiffness testing have yielded considerably unlike results. Using classical techniques for measuring tensile stiffness, Rivaux et al. determined stress–strain curves for excised segments of the uterosacral ligaments of fresh cadavers without Pop by performing uniaxial tension tests [2]. Based on their reported information, it would take 26 Northward, (or 5.8 lb) to stretch the uterosacral ligament past 1 mm (see "Appendix" for calculation). In comparison, we found that the in vivo strength required for 1 mm of uterine deportation, and therefore, deformation of the uterosacral and cardinal ligament complexes, was simply 0.04 N, or 650 times less. The deviation between results of traditional material properties testing and in vivo testing tin can be understood past recognizing the unlike testing conditions. Traditional tensile testing evaluates the material beliefs of an excised slice of tissue. It is placed in the testing apparatus, and preconditioning is performed that tin can modify the properties of the sample [eleven]. This involves repetitive cyclic loading prior to data drove to amend test reproducibility. Since the fundamental ligaments have a lattice-similar system [12], it seems likely that this preconditioning straightens the fibers so that they are all aligned, making the material properties much stiffer than would be true when loaded in vivo, where the lattice work is open up. Results from our physiologic testing suggest that apical ligament stiffness is not the chief factor contributing to uterine support. In a written report by Smith et al., in vivo ligament stiffness only explained 19 % of the variation in Pop-Q point C [4]. Therefore, when thinking nigh the etiology of upmost back up loss, we may presently take a tendency to overestimate the role of upmost ligament stiffness and underestimate other of import factors, such as ligament length. If then, we must also consider what other factors influence uterine move.
Although the OR traction force required to achieve maximal uterine displacement seen in MRI was similar in the 3 groups of women with varying degrees of prolapse, these groups did differ in regards to the magnitude of correlation between abdominal pressure and uterine deportation in MRI. Abdominal force per unit area accounted for 91 % of the variability seen in uterine displacement in women in group 1. The correlations were low and nonsignificant in women in groups two and three. Therefore, our results show that it takes more than intra-abdominal pressure to move the uterus in women with normal pelvic support compared with women with prolapse. Equally such, nosotros can infer that different factors determine uterine movement in women with prolapse vs those without.
Another observation nosotros made when comparison prolapse groups was the amount of uterine displacement measured in the OR vs MRI. We found that for women in groups 1 and two, uterine deportation was greater in the OR compared with that during MRI; only for women in group 3, uterine displacement was the same in MRI as it was in the OR. This observation led usa to compare the departure in uterine locations seen in the OR vs MRI in Role 2. We institute that uterine location at rest and during maximal traction force was universally lower in the OR compared with MRI. In fact, uterine location at residual in the OR was equal to or lower than the maximal Valsalva location seen in MRI for xc % (17/nineteen) of women. Although this comparison has non been previously reported, Crosby et al. reported that cervix location is, on average, iii.5 cm lower in the OR nether traction vs Pop-Q exam in clinic during maximal Valsalva [13]. We hypothesized that provisional differences between the OR and MRI environments may help explain some of these findings.
Leg positioning was one gene that differed between the OR and MRI. In the OR, women were in high-lithotomy position, while in MRI they were supine. We know from the literature that leg positioning can affect uterine position. In a report past Barber et al., a higher degree of prolapse was seen in women examined in the upright vs low-lithotomy position [14]. When we compared uterine location at remainder during frog-leg position in the OR to supine resting location in MRI, we constitute like locations for all prolapse groups. From this finding, we can hypothesize that high-lithotomy leg positioning may indeed upshot in lower uterine location at balance; however, leg positioning alone does not fully explain the difference in uterine locations we observed between the OR and MRI. The furnishings of anesthesia on uterine location is another variable that may lead to a lower uterine position in the OR, considering general anesthetics could act on the smooth muscle in the uterosacral and fundamental ligaments to crusade lengthening, and also on the skeletal muscle of the levator hiatus to cause a widening effect. Furthermore, OR testing was performed with a posterior-weighted speculum in identify, which also results in a wider genital hiatus compared with MRI testing.
Although our study is limited by a pocket-sized sample size, we institute meaning differences in the small groups, merely we cannot brand conclusions regarding differences that were non statistically pregnant, as these may go pregnant with a larger sample. Yet, our data can provide upshot sizes that may be used in planning subsequent investigations. While information technology would have been platonic to perform the MRI and servoactuator testing simultaneously, the motor in the servoactuator device is not MRI uniform, and therefore, this was non possible in the electric current study. Furthermore, Valsalva strength generated during clinical Popular-Q exam and MRI testing varies by private and is non standardized; nevertheless, our goal is to have the prolapse maximally developed. Finally, we recognize that ultrasound is a more widely attainable imaging tool than MRI. However, being able to make measurements relative to the hymenal ring without artefacts introduced from a transducer pressed on the perineum or a probe in the vagina is essential for the most precise and authentic measurements possible. Strengths of our methods include the use of a custom-designed computer-controlled servoactuator device able to make highly accurate force-displacement measurements, too as the use of well-developed MRI strategies for quantifying physiological movements. It would be ideal to perform these studies in the standing posture, but at the present time, this has non been viable, and comparing of upright and supine images of the pelvic floor do not show major differences [xv]. Additionally, our technique using dynamic stress MRI to appraise physiologic uterine move allows for precise imaging and measurement of uterine location without instrumentation of the vagina.
In conclusion, we depict a novel investigative strategy to decide traction forces needed to reproduce physiologic uterine displacement in women with and without prolapse. Nosotros institute that very little traction strength in the OR is required to achieve maximal physiologic uterine displacement seen during MRI testing, regardless of the presence or absence of prolapse. Our preliminary data may be useful in designing larger, fairly powered, studies to further assess the various factors contributing to observed differences in physiologic uterine position and uterine displacement to that seen in the OR among women with varying degrees of prolapse.
Supplementary Textile
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2
Acknowledgments
This inquiry was supported by the National Institutes of Health Office of Research on Women'due south Health grant P50 HD044406 and the National Institute of Kid Health and Human Evolution grant R01 HD038665. Investigator support for CWS was provided past the National Institute of Child Wellness and Man Evolution WRHR Career Development Award K12 HD065257.
Appendix
Calculation of the force needed to elongate uterosacral ligament by 1 mm based on in vitro ligament stiffness data [2].
Where ε = strain (m/k)
dL= elongation of the uterosacral ligament (mm)
Fifty = length of the uterosacral ligament≈ 38 mm [16]
σ = stress (N/chiliadtwo)
F = force (N)
A = cross sectional expanse of uterosacral ligament ≈ 1 cm ii (based on senior author's in surgery measurement)
E = Young'southward modulus (Northward/chiliad2) ≈ ten MPa [ii]
Footnotes
Electronic supplementary material The online version of this commodity (doi:10.1007/s00192-016-2980-1) contains supplementary material, which is available to authorized users.
Compliance with ethical standards
Conflicts of interest None.
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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4947418/