Journal Pre-proof Levator ani evaluation at transperineal elastography in women with deep infiltrating endometriosis postoperatively Meng Xie, Huan Yu, Peimin Mao, Xuyin Zhang, Yunyun Ren
PII:
S2468-7847(19)30696-8
DOI:
https://doi.org/10.1016/j.jogoh.2019.101663
Reference:
JOGOH 101663
To appear in:
Journal of Gynecology Obstetrics and Human Reproduction
Received Date:
10 July 2019
Revised Date:
13 November 2019
Accepted Date:
28 November 2019
Please cite this article as: Xie M, Yu H, Mao P, Zhang X, Ren Y, Levator ani evaluation at transperineal elastography in women with deep infiltrating endometriosis postoperatively, Journal of Gynecology Obstetrics and Human Reproduction (2019), doi: https://doi.org/10.1016/j.jogoh.2019.101663
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Levator ani evaluation at transperineal elastography in women with deep infiltrating endometriosis postoperatively Short title: assessment of pelvic floor muscle by elastography
Meng Xie1, Huan Yu1, Peimin Mao2, Xuyin Zhang3, Yunyun Ren1 1
Department of Ultrasound,
2
Department of clinical laboratory,
3
Department of
Gynecology, Obstetrics and Gynecology Hospital, Fudan University, 128 Shen yang
ro of
Road, Shanghai 200090, China.
Corresponding to Yunyun Ren. E-mail:yunyunren11@ 163.com
The first 2 authors contributed equally to this article.
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Abstract
Objective: To explore whether operation can change the elasticity of
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levator ani in deep infiltrating endometriosis (DIE) with operation and
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pharmacotherapy using transperineal elastography. Methods: Total thirty-four patients who were diagnosed as DIE were included in the study. Transperineal elastography were performed in all
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cases preoperatively and postoperatively. The levator ani was evaluated by means of the scoring system and strain ratio (SR) values on maximal
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Valsalva and quiescent condition, respectively. Results: On quiescent condition, the preoperative mean elastography
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scores and SR of the levator ani were statistically significantly higher than the postoperative ones in both shaving technique group and segmental colorectal resection group. And on maximal Valsalva, the preoperative mean elastography scores and SR of the levator ani were statistically significantly lower than the postoperative ones in both groups. After surgery and 6 cycles of GnRHa therapy, the mean elastography score and SR of the levator ani were statistically significantly lower than 1
before GnRHa therapy in shaving technique group on quiescent condition. And on maximal Valsalva, the mean elastography score and SR were statistically higher than before GnRHa therapy. However, in segmental colorectal resection group, the differences were not observed before and following 6 cycles of GnRHa therapy. Conclusion: The elasticity of levator ani of DIE was changed by both shaving technique and segmental colorectal resection. And transperineal
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elastography could access the alterations.
Key words: elastography; deep infiltrating endometriosis; ultrasound
Introduction
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As the most severe form of endometriosis, deep infiltrating endometriosis (DIE) affects approximately 1% of women of reproductive
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age [1]. Laparoscopic colorectal surgery is considered to be efficient to
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treat bowel endometriosis[2]. Although the results are controversial, several surgical procedures are performed, such as nodule excision without opening the rectum (shaving), resection of the nodule with
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excision of the anterior rectal wall (disc excision), and segmental colorectal resection [3]. Most patients of DIE suffer severe pain,
[4].
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including dysmenorrhea, deep dyspareunia or nonmenstrual pelvic pain
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The DIE patients have to take the chronic antalgic posture due to the severe sign. As a result, the musculoskeletal stress changes. The patients have to take the position of relief of postural deviations. Then the levator ani overloads. At last, the structure and function of levator ani damage[5,6]. As the form of levator ani damages, muscle spasms and trigger points will exacerbate pain, vice versa[7]. The patients of DIE have more morbility of pelvic floor muscle spasms than those without 2
endometriosis[8]. It was not clear whether the colorectal surgery of DIE could change the levator ani and the methods to evaluate the levator ani. It was reported the levator ani of DIE patients assessed by 3D and 4D transperineal ultrasound[9]. And in our published data, we reported that transperineal elastography could assess the elasticity of levator ani with DIE patients. The results revealed the elasticity of levator ani was decreased and coordination of levator ani was damaged[10]. However, whether surgery
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can change the elasticity of levator ani was not clear. In this study, we
propose to assess the levator ani by transperineal elastography in deep endometriosis undergoing operation.
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Methods
In this retrospective study, a total of 34 consecutive patients with
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colorectal DIE referred to our institute between January 2016 and June
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2018 were included. The study design and protocol were approved by the Institutional Review Board (2015-32), and all patients were given written informed consent after the procedure was explained fully.
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As a form of DIE, colorectal endometriosis meant endometrial tissues grew on the surface or inside of the colon or rectum. Diagnosis of
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colorectal DIE depended on vagino-recto-abdominal examinations, pelvic magnetic resonance imaging (MRI) preoperatively and histological
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examination of the surgical specimens postoperatively. The methods for resecting the endometriotic nodule on the rectum or rectosigmoid included the shaving of the nodule without entering the bowel mucosa and the segmental colorectal resection. The shaving procedure was as follows. The deep subperitoneal space located between the uterosacral ligaments and the bowel was longitudinally opened. Dissection was performed in close contact with the lateral face of the bowel and is 3
directed toward the healthy rectovaginal space located below the endometriosis nodule. Once the lateral faces of the bowel were freed, the shaving was performed as deeply as possible into the thickness of the bowel wall to remove abnormal fibrous lesions involving bowel layers by use of a high-magnification endoscopic view. Thus, the nodule was dissected away from the bowel wall. The choice of surgical procedure was discussed preoperatively in all cases, on the basis of anatomical extension of the disease and the patient symptoms. Although the
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indication for bowel resection was controversial, infiltration up to the
rectal mucosa and invasion of >50% of the circumference were elected segmental colorectal resection. The other cases all underwent shaving nodules[11,12].
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If the patient was in the postmenopausal status, or had previous
non-surgical treatment for endometriosis, such as HIFU (High Intensity
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Focused Ultrasound), or experienced hormonal therapy within 6 months
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before surgery, such as GnRH-a, oral contraceptive agents, or had pelvic organ prolapse, she was excluded.
Clinical characteristic was collected, including age, parity, body
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mass index (BMI) and CA125. The visual analog score (VAS) of algopareunia was used to evaluate the patient’s pain. The patient chose a
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number from 0 to 10 to represent the pain (0 being no pain and 10 being maximum pain). As a standardized gastrointestinal questionnairy, the
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Gastrointestinal Quality of Life Index (GIQLI score) was applied to investigate the preoperative and postoperative digestive function[13]. Transperineal
elastography
were
performed
in
all
cases
preoperatively. Following evacuation, the patients were in the lithotomy position. Evaluation was underwent on maximal Valsalva and quiescent condition, respectively. Imaging was done on the system Hitachi ARIETTA 60 (Hitachi Medical, Tokyo, Japan) by a transperineal 4
3.5-MHz probe. Transperineal elastography was performed by a radiologist (M.X.) with 7 years of experience in sonography and who has specialized in elastography for the last 3 years. The radiologist was blind to clinical examinations and MRI before elastographic procedures. The detail of method was reported as follows, which was present in our publishment [10]. When the levator ani was detected by the general transperineal ultrasound. Transperineal elastography was carried out instantly after the
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conventional gray-scale ultrasound image was acquired. Then, the images of grayscale ultrasound and elastogram appeared concurrently. Images were obtained by applying repetitive light pressure on the skin of the perineum two or three times per second, with the probe positioned
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perpendicular to the skin when applying pressure.The scale of the region
of interest (ROI) was from the levator ani to the adjacent anal canal. The
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mean values of 3 successive measurements were recorded. All records
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were recorded in a separate folder and added to the database for subsequent evaluation. The tissue elasticity information was showed in color, with blue indicating hard tissue, green indicating medium tissue
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stiffness, and red indicating soft tissue.
Strain elastography detects local deformation (strain) under light
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pressure. Its output include a color‐coded representation (qualitative assessment) of the lesion and a semi‐quantitative characterization by
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strain ratio (SR), calculated as the ratio of the surrounding parenchyma to the lesions and providing a measure of lesion stiffness. The estimation of the SR depended on the contrast of the strains surveyed in the levator ani and the adjacent anal canal at the same depth. The operator outlined the contours manually. The levator ani was positioned and labeled as A. After that, the adjacent anal canal of the same depth was selected and labeled as
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B. The stiffness of the tissues was described by strain ratio (B/A) which was accounted by sonographic equipment. All procedures were done 3 times and the average values were calculated to obtain more reliable data to improve reproducibility. For easy to image analysis, the elasticity images were evaluated by a 4-point scoring system that was used in a study of neck masses (Table 1) [14]. All the patients were treated with GnRHa (Triptorelin 3.75mg were administered every 28 days )plus add-back therapy(combined with
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estradiol valerate 0.5 mg and dydrogesterone 5 mg daily, from the 3
cycle)after the operation. VAS and GIQLI score before and following 6
cycles of GnRHa therapy were recorded. Transvaginal ultrasound and
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elastography were repeated before and following 6 cycles of GnRHa therapy.
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Statistical analyses were performed using The SPSS version 11.0 for Windows software package (SPSS Inc, Chicago, IL). To characterize the
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study population, descriptive statistic was carried out. Data were expressed as mean ± standard deviation. A Mann-Whitney U test was
Results
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conducted to compare the measurements between the 2 groups.
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Patients' characteristics, including VAS and GIQLI scores, were summarized in Table 2. Thirty-four consecutive patients had a
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laparoscopic procedure for colorectal endometriosis. 21 patients underwent the colorectal shaving (group I) and 13 patients underwent the segmental colorectal resection (group II). Histological examination postoperatively confirmed the dignosis of endometriosis in all the cases. There were no intraoperative and postoperative complications. Transperineal elastography was successfully achieved in all cases.
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On quiescent condition, the preoperative mean elastography scores and SR of the levator ani were statistically significantly higher than the postoperative ones in both group I and II (3.3±0.4 vs 2.6±0.2, 3.4±0.2 vs 2.8±0.4, 3.38±0.41 vs 2.35±0.21, 3.52±0.57 vs 2.74±0.21, p = 0.027, 0.034, 0.007, 0.011, respectively). And on maximal Valsalva, the preoperative mean elastography scores and SR of the levator ani were statistically significantly lower than the postoperative ones in both group I and II (2.3±0.2 vs 2.9±0.3, 2.5±0.3 vs 3.1±0.2, 2.97±0.32 vs 3.87±0.53,
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3.33 ± 0.48 vs 2.17±0.38, p = 0.030, 0.028, 0.005, 0.007, respectively) (Table 3).
Following 6 cycles of GnRHa therapy, the mean elastography score
and SR of the levator ani were statistically significantly lower than before
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GnRHa therapy in group I on quiescent condition(2.6±0.2 vs 2.1±0.1, 2.35 ± 0.21 vs 1.74 ± 0.32, p = 0.009, 0.019, respectively). And on
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maximal Valsalva, the mean elastography score and SR were statistically
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higher than before GnRHa therapy(2.9±0.3 vs 3.5±0.3, 3.87 ± 0.53 vs 4.51 ± 0.43, p = 0.014, 0.008, respectively) (Table 4). However, in group II, the mean elastography score and SR of the
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levator ani were similar before and following 6 cycles of GnRHa therapy
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on both quiescent condition and maximal Valsalva (Fig 1-3).
Discussion
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There were several reports about the application of elastography in the assessment of levator ani. Katharina revealed that the elastographic evaluation revealed more trauma-suspicious lesions than the B-mode investigation and it may help to identify women with a higher risk of postpartum [15]. Gachon et al applied shear wave elastography in the assessment of the elastic properties of the levator ani muscles. In their study, the stiffness of the levator ani muscle significantly increased from 7
rest to the Valsalva maneuver, which means that the stretched levator ani muscle is stiffer than it is at rest [16]. Our previous study suggested that the change in the elasticity of the levator ani was earlier than structure abnormity in patients with pelvic organ prolapse by transperineal elastography [17]. Generally, the levator ani was in loose state on quiescent condition. And the stiffness was soft. In the contrary, the stiffness of the levator ani was hard when the state of maximal Valsalva. However, in our published
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data, it was revealed the uncoordinated state of levator ani in DIE patients
due to muscle spasms, which were related to pelvic pain and dyspareunia
[18]. We reported that the mean elastography score and SR were higher for the levator ani of DIE cases than ovarian endometrioid cyst and
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ovarian teratoma cases on quiescent condition. However, on maximal
Valsalva, the mean elastography score and SR of DIE cases was lower
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than the other two cases [10]. It was suggested that the elasticity of
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levator ani with DIE patients could be evaluated by transperineal elastography qualitatively.
In our study, the preoperative elastography scores and SR of the
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levator ani were higher than the postoperative ones in both group 1 and 2 on quiescent condition. And the preoperative elastography scores and SR
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of the levator ani were lower than the postoperative ones in both group 1 and 2 on maximal Valsalva. It means surgery can relieve the
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incoordination of the levator ani. Recent studies have shown that patients with colorectal endometriosis may preoperatively present with rectal or bladder dysfunction, anal and urethral sphincter hypertonia, and these troubles may be irreversible and not restored by removal of nodules [19]. So the surgery removed the lesions and relieved the symptoms. It was reported that more than 80%–90% of patients with colorectal rectovaginal endometriosis could be managed by the shaving technique [20,21]. And 8
the complications, such as bowel perforation, seldom occurred [21]. However, shaving was not a radical surgery. So it always could not remove all of the lesions and the postoperative medical therapy was indispensable. As a result, in our study, it was observed that following 6 cycles of GnRHa therapy, the elastography score and SR of the levator ani were lower than before GnRHa therapy in group 1 on quiescent condition. And on maximal Valsalva, the elastography score and SR were higher than before GnRHa therapy. GnRHa have an important place in
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the treatment of endometriosis. Their effect can be described as entering
woman in a state of ‘artificial menopause’. Inhibiting the secretion of pituitary luteinizing hormone lead to a decline in estradiol concentrations. During treatment, menstrual periods should be lost as well because it is
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the determinant of hypoestrogenism and thinning of the endometrium.
Then, we considered that the following pharmacotherapy could change
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stiffness of the levator ani by eliminating the remnant lesions. Of course,
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we have to recognized that change in stiffness of levator ani muscle on the quiescent condition don't necessarily mean improvement of levator ani muscle function. We know that some nerves of the levator ani muscle
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are intrapelvic. It was reported that the inferior hypogastric plexus nerve fibers were solely autonomic, located in between the levator ani muscle
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and pelvic organs (endolevator pathway), supplying innervation to the medial portion of the levator ani muscle[22]. As endometriosis surgery
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can be associated with nerves injury[23]. Thus the change in the stiffness of the levator ani muscle could be associated to important denervation. As a radical surgery, segmental colorectal resection was associated
with a higher risk of complications, such as rectovaginal fistula and pelvic abscess[21]. Furthermore, colorectal segmental resection resulted in uncomfortable urinary and digestive symptoms[24,25]. During the last 10 years, several authors have underlined the functional outcomes and 9
symptoms of the surgical management of the digestive tract. These outcomes are directly related to removal of a part of the digestive tract, bowel denervation, loss of compliance, or hypersensitivity and may lead to unbearable complaints such as anal incontinence, major dyschesia, and fecal urgency [26]. When compared with shaving, colorectal resection always leaded to poor GIQLI scores[27,28]. The cases who underwent segmental colorectal resection had deeper and wider invasive lesions. The scope of operation was extensive and the levator ani was affected
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potentially due to the radical surgery. The advantage of the surgery was
that little remanent lesion was present. So the following pharmacotherapy
could not further improved the stiffness of levator ani. As a result, in
group 2, the elastography score and SR of the levator ani were similar
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before and following 6 cycles of GnRHa therapy on both quiescent condition and maximal Valsalva. Serious adhesion appeared in the radical
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operation involving rectum or colon of DIE postoperatively. The adhesion
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resulted in pelvic pain (the inflammatory status of the pelvis), even defecation disorders. Then, it was possible that the postoperative adhesion influences the stiffness of levator ani. However, an absorbable oxidized
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regenerated cellulose was used in all of the cases intraoperatively. And GnRHa was proved to prevent the adhesion postoperatively. As a result,
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the postoperative adhesion may not influence the stiffness of the levator
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Our study also has several weaknesses. It was not a randomised control trial. And it required a longer postoperative follow-up more than six months. Furthermore, the group is heterogen and the sample is small. Last but not least, the intra-observer differences should be examined in future study.
Conclusion 10
In this study, we investigated the levator ani of DIE patients undergoing surgery could be evaluated by transperineal elastography. And the elasticity of levator ani of DIE was changed by both shaving technique and segmental colorectal resection. Further study about the detailed mechanism was required in the future.
Ethical statements The study design and protocol were approved by the Institutional
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Review Board ofthe Obstetrics and Gynecology Hospital of Fudan University, Shanghai, P. R. China. And all patients were given written informed consent after the procedure was explained fully.
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Conflict of Interest
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We declare that we have no conflict of interest.
Conflict of interest: We declare that we have no conflict of interest.
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This study was supported by a grant from the fund for scientific research of Chinese Preventive Medicine Association (grant no.201809031).
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Manuscript category: original article
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[10]. Xie M, Feng Y, Zhang X, et al.Evaluation of pelvic floor muscle by transperineal elastography in patients with deep infiltrating endometriosis: preliminary observation. J Med Ultrason (2001). 2019; 46:123-8.
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[11]. Abrao MS, Podgaec S, Dias JA Jr, et al. Endometriosis lesions that compromise the rectumdeeper than the inner muscularis layer have more than 40%of the
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[12]. Goncalves MO, Podgaec S, Dias JA Jr, et al. Transvaginal ultrasonography with bowel preparation is able to predict the number of lesions and rectosigmoid layers affected in cases of deep endometriosis, defining surgical strategy. Hum Reprod. 2010; 25:665–71. [13]. Slim K, Bousquet J, Kwiatkowski F, et al. First validation of the French version of the Gastrointestinal Quality of Life Index (GIQLI). Gastroenterologie Clin Biol. 12
1999; 23:25–31. [14]. Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology. 2005; 237: 202–11 [15]. Maßlo K, Möllers M, de Murcia KO, et al. New Method for Assessment of Levator Avulsion Injury: A Comparative Elastography Study. J Ultrasound Med. 2018. [Epub ahead of print] [16].Gachon B, Nordez A, Pierre F, et al. In vivo assessment of the levator ani muscles using shear wave elastography: a feasibility studyin women. Int Urogynecol J. 2019;30(7):1179-1186.
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[17].Xie M, Zhang X, Liu J, et al. Evaluation of levator ani with no defect on elastography in women with POP. Int J Clin Exp Med. 2015; 8:10204-12.
[18].Dos Bispo AP, Ploger C, Loureiro AF, et al. Assessment of pelvic floor muscles in women with deep endometriosis. Arch Gynecol Obstet. 2016; 294: 519–23.
[19].Mabrouk M, Ferrini G, Montanari G, et al. Does colorectal endometriosis alter
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[22].Nyangoh Timoh K, Bessede T, Lebacle C, et al. Levator ani muscle innervation: Anatomical study in human fetus. Neurourol Urodyn. 2017, 36(6):1464-1471.
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[23].Scioscia M, Virgilio BA, Scardapane A, et al. Sometimes complete nerve-sparing surgery is not possible in deep infiltrating endometriosis: Presurgical
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magnetic resonance/ultrasound fusion imaging as a novel diagnostic tool. J Minim Invasive Gynecol. 2019, S1553-4650(19)30306-1. [24] Olivier Donnez, Horace Roman. Choosing the right surgical technique for deep endometriosis: shaving, disc excision, or bowel resection? Fertil Steril. 2017; 108:931-42. [25]. Slack A, Child T, Lindsey I, et al. Urological and colorectal complications following surgery for rectovaginal endometriosis. Br J Obstet Gynecol. 2007; 114:1278–82. 13
[26]Donnez O, Roman H. Choosing the right surgical technique for deep endometriosis: shaving, disc excision,
or bowel
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108(6):931-942. [27]. Roman H, Milles M, et al. Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis. Am J Obstet Gynecol. 2016; 215:762.e1–9. [28]. Roman H, Vassilieff M, Tuech JJ, et al. Postoperative digestive function after radical versus conservative surgical philosophy for deep endometriosis infiltrating the
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rectum. Fertil Steril. 2013; 99:1695–704.
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Fig. 1 Conventional transperineal ultrasound and elastography of a patient with DIE (group I) at quiescent condition preoperatively. SR was 3.46.
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Fig. 2 Conventional transperineal ultrasound and elastography of the same patient at quiescent condition postoperatively. SR was 2.47.(the same case as Fig 1)
Fig. 3 Conventional transperineal ultrasound and elastography of the same patient at quiescent condition after GnRH therapy. SR was 1.58. (the same case as Fig 1)
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Overall impression soft
ES 2
moderately soft
ES 3
moderately stiff
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Elastographic score ES 1
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Table 1 Elastography scoring system (ES 1-4) (The color which indicated stiffness was different in our study, red for soft and blue for hard)
stiff
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ES 4
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Elastographic appearance Predominantly purple, green or yellow with less than 10% displaying red. The node is indistinguishable from surrounding tissues. Predominantly yellow or green and with red areas comprising between 10% and 50%. The node is partially delineated from surrounding tissues. Predominantly red and with yellow or green areas comprising between 10% and 50%. The node is partially delineated from surrounding tissues. Predominantly red and with less than 10% appearing yellow or green. The node is distinguishable from surrounding tissues.
110.2±20.7
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145.8±33.7 8.8±2.7 3.4±1.8
preoperative
p
105.1±25.6
0.001
0.757
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Age (y) Parity body mass index (BMI) CA125 VAS of algopareunia GIQLI
group 1 (n=21) preoperative GnRH therapy 41.6±3.1 1.2±0.3 22.1±4.2
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Table 2. The baseline characteristics of group I and II
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GnRH therapy 39.3±4.4 1.1±0.2 23.5±3.9
137.3±40.2 8.2±3.5 3.8±2.2 85.5±19.5
90.6±22.3
p 0.741 0. 788 0.892 0.657 0.001 0.821
preoperative
p 0.027
2.6±0.2
2.3±0.2
2.9±0.3
3.38 ± 0.41
2.35 ± 0.21
2.97 ± 0.32
3.87 ± 0.53
postoperative
p
2.8±0.4
0.034
2.5±0.3
3.1±0.2
0.028
0.007
3.52 ± 0.57
2.74 ± 0.21
0.011
0.005
3.33 ± 0.48
2.17 ± 0.38
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0.030
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preoperative
group II (n=13)
3.4±0.2
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3.3±0.4
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Elasticity score quiescent condition maximal Valsalva Strain ratio quiescent condition maximal Valsalva
postoperative
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group I (n=21)
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Table 3. Elasticity scores and SR of the levator ani in group I and II (n = 34)
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0.007
quiescent condition
2.35 ± 0.21
4.51 ± 0.43
GnRH therapy
p 0.544
2.7±0.3
3.1±0.2
3.0±0.4
0.621
0.019
2.74 ± 0.21
2.59 ± 0.32
0.365
0.008
2.17 ± 0.38
2.35 ± 0.16
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1.74 ± 0.32
group II (n=13)
2.8±0.4
0.014
3.5±0.3
postoperative
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0.009
2.1±0.1
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maximal Valsalva 3.87 ± 0.53
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Elasticity score quiescent 2.6±0.2 condition maximal Valsalva 2.9±0.3
GnRH therapy
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postoperative
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Table 4. Elasticity scores and SR of the levator ani in group I and II (n = 34) group I (n=21)
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0.768