The suture fixation of the levonorgestrel-releasing intrauterine device with hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion

The suture fixation of the levonorgestrel-releasing intrauterine device with hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article The suture fixation of the levonorgestrel-releasing intrauterine device with hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion Min Mao, Yuanqin Gou, Zhigui Luo, Yuanhong Li, Yu Tong This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4303936/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 09 Oct, 2024 Read the published version in BMC Women's Health → Version 1 posted 14 You are reading this latest preprint version Abstract Background: This study aimed to investigate the safety and efficacy ofsuture fixation of the levonorgestrel-releasing intrauterine device (LNG-IUD) by hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion. Methods: 21 patients with large symptomaticadenomyosis were sewed and fixed with the LNG-IUD in the uterus by hysteroscopy to prevent the device expulsion. Results: In this prospective case series, all 21 patients were successfully sewed and fixed with the LNG-IUD in the uterus by hysteroscopy. The amount of menstruation was significantly decreased and dysmenorrhea was significantlyrelieved in 3, 6, and 12 months after surgery compared with before surgery. Only one patient underwent a laparoscopic hysterectomy due to dysmenorrhea which was not alleviated one month later. Serious IUD complications including expulsion and perforation were not observed. There was no development of new side effects than LNG-IUD insertion. Conclusion: Suture fixation of the LNG-IUD by hysteroscope is a safe, effective, and minimally invasive surgical procedure to prevent the device expulsion. It is a good solution for the treatment of patients with large symptomatic adenomyosis. Levonorgestrel-releasing intrauterine device (LNG-IUD) Adenomyosis Hysteroscope Suture fixation Figures Figure 1 Background Uterine adenomyosis is a common clinical gynecological disease, affecting approximately 20 to 35 percent of females [1] . Hypermenorrhea, secondary anemia, and dysmenorrhea are the typical symptoms of adenomyosis [2] that seriously affect the life quality of patients. Hormonal medications used for the treatment of adenomyosis require daily administration. Enlargement of the uterus and recurrence of symptoms are usually documented within six months after hormonal medications are discontinued [3-6] . Since adenomyosis is confined to the uterine corpus, the effect of the surgical resection of the uterus is ideal, but it will cause the permanent loss of fertility and the uterus, which is usually unacceptable to women. Studies on UAE (uterine artery embolisation) for adenomyosis showed a 25 percent reduction in uterine volume and overall symptom reduction [7, 8] . However, some data demonstrate high failure rates of treatments [9] . The levonorgestrel-releasing intrauterine device (LNG-IUD) has steadily been replacing medication and surgery as a satisfactory management option for women with adenomyosis. Studies have shown that the LNG-IUD effectively improved adenomyosis-associated hypermenorrhea and dysmenorrhea [10] . However, one study reported a 25 percent LNG-IUD expulsion rate in patients with adenomyosis [11] . It is the clinical requirement to find a method to prevent the LNG-IUD expulsion, especially in patients who are unlikely to receive hysterectomy surgeries. The first case of hysteroscopic suture fixation of the LNG-IUD was described by Zhu L in 2021 [12] , and there is limited data regarding the use of this approach to treat adenomyosis. As the feasibility and safety of this invasive procedure are unclear, we present our experience of 21 patients with large symptomatic adenomyosis treated with hysteroscopic suture fixation of the LNG-IUD. Methods Patients The diagnosis of adenomyosis was suggested by characteristic clinical manifestations (i.e., heavy menstrual bleeding or dysmenorrhea with uniformly enlarged uterus) and ultrasound findings. A total of 21 large symptomatic adenomyosis patients admitted to Chengdu First People’s Hospital from October 2022 to March 2023 were enrolled to study. Inclusion criteria: (a) patients who required uterus preservation; (b) patients with symptoms of hypermenorrhea or dysmenorrhea; (c) patients with preoperative uterine depth ≥ 9 cm or had experienced IUD expulsion; (d) patients without pregnancy and had no fertility requirements in the short term; (e) patients not allergic to LNG-IUS, and (f) patients with good compliance. Exclusion criteria: (a) patients with leiomyoma; (b) patients with cervical or endometrial pathology; (c) Patients with breast tumors; (d) patients who cannot be treated with hormones; (e) patients with abnormal reproductive organs; and (f) patients with hormonal therapy within 6 months. All patients signed informed consent forms, and ethics approval was obtained from the Ethics Committee of Chengdu First People’s Hospital. Operative procedure Before treatment, a series of examinations were carried out on the patients, including routine gynecological examination, transvaginal ultrasonography, and basic general check-ups to exclude contraindications. Preoperative cervical cytological examination and diagnostic uterine curettage were performed to exclude malignant diseases if necessary. All of the hysteroscopic suture fixations of the LNG-IUD (Mirena) operations were performed by one experienced surgeon (Yuan-Hong Li) under general anesthesia. The procedure was performed as follows: Step 1 join ethibond suture and the LNG-IUD together; Step 2 Insertion and suture fixation of the LNG-IUD; Step 3 Endoscopic knots; Step 4 Confirm the location of the LNG-IUD. All patients were successfully performed with hysteroscopic suture fixation of the LNG-IUD in the uterine cavity with a non-absorbable suture through an endoscopic needle driver and a knot-pushing device (Figure 1). Statistical analyses Statistical tests were performed using SPSS Statistics. Measurement data were expressed as the mean ± standard deviation, and compared between groups using the t-test, and correlation between groups using the linear regression. Enumeration data were presented by n (%). Results Demographic and clinical characteristics of the patient population are reported in Table 1 . We succeeded in hysteroscopic suture fixation of the LNG-IUD in 21 cases. No differences were observed in age, BMI, parity, preoperative uterine depth, operative time, and intraoperative blood loss between the patients who with or without a history of IUD expulsion (P>0.05). In our study, ten patients had experienced IUD expulsion 1-3 times, and 80% of them had a history of cesarean section and no vaginal delivery. The average uterine depth was 9.69 ± 0.95 cm. The operative time was 41.38 ± 11.50 min. The intraoperative blood loss was 16.90 ± 12.40 mL, which was minimal and no additional hemostatic methods were required during the surgery. The operative time and blood loss had no significant correlation with the uterine volume or the uterine depth (P >0.05). There were no complications or major adverse events at the time of surgery. The patients were discharged 24 hours postoperatively. Unfortunately, during the first month follow-up, a patient underwent laparoscopic hysterectomy in another hospital due to dysmenorrhea which was not alleviated, and the patient was not included in the follow-up. In this study, twenty patients were followed up for twelve months, and all had symptoms of hypermenorrhea (4/20), dysmenorrhea (3/20), or both (13/20). Efficacy in patients after treatment are shown in Table 2. The pictorial blood loss assessment chart (PBAC) was adopted to evaluate menstrual blood loss among patients [13] . A PBAC score ≥ 100 is used to predict heavy menstrual bleeding. Participants were instructed by the research doctor to fill in the PBAC. A significant decrease in PBAC was observed in the 3, 6, and 12 months after treatment compared with the baseline value (p < .05). Women with anemia, defined as a hemoglobin level < 110 g/L. Among 20 patients, 16 women had anemia, among which ten women had a hemoglobin level of < 90 g/L before treatment. It turned out that women had significantly higher hemoglobin levels after treatment (p < .05) . The visual analogue scale (VAS) from 0 to 10 was used to assess dysmenorrhea in patients and evaluate treatment response. It is considered the gold standard of pain measurement [14] . The VAS of dysmenorrhea showed a significant decrease 3, 6, and 12 months after treatment (p < .05). The location of the LNG-IUD was assessed by transvaginal ultrasonography. No patient experienced expulsion of the LNG-IUD during follow-up. The adverse reactions in patients after treatment were recorded. We evaluated the number of patients who experienced adverse events. The total number of patients with adverse events was 13 (65.0%) in the first 3 months and 5 (25.0%) in the 12 months. Most patients complained of irregular bleeding, breast discomfort, abdominal discomfort, and weight gain. Women in our study were able to tolerate the adverse reactions and it did not appear to impact the device continuation rates. No dyspareunia was observed in our study after treatment. Discussion Adenomyosis is considered a notable health problem that challenges physicians all over the world. The etiology of adenomyosis is still unclear, and its presentation tends to be increasingly severe over time until menopause, and the response to treatments is not always successful. Among patients using the LNG-IUD for the treatment of adenomyosis, the rate of LNG-IUD expulsion was found in about 25 percent of the cases. Women who have previously expelled an IUD are at higher risk of IUD expulsion again. Rates of reported IUD expulsion after prior expulsion range from 14 to 31 percent [15, 16] . Enlargement of the uterus and recurrence of symptoms are usually documented within six months after the LNG-IUD expulsion. In the present research, we performed hysteroscopic suture fixation of the LNG-IUD in the uterine cavity to prevent the IUD expulsion, which did not affect the structure of the LNG-IUD, and the safety and efficacy of the technique were evaluated. In our study, it turned out that hysteroscopic suture fixation of the LNG-IUD was significantly effective in improving heavy menstrual bleeding, alleviating pain, and preventing IUD expulsion. All follow-up patients reported obvious relief of menorrhagia and dysmenorrhea at 12 months follow-up. Serious IUD complications including expulsion and perforation were not observed in our study. Less serious side effects including irregular bleeding, leukorrhea, abdomen discomfort, headache, breast discomfort, and weight gain were observed, which are consistent with adverse reactions reported for LNG-IUD insertion in the literature. Further, there is no development of new side effects. In 2022, Zhang et al. reported the role of LNG-IUD fixation [17] , and they stitched and fixed the LNG-IUD on the posterior wall of the uterus. In our experience, the LNG-IUD can also be stitched on the anterior wall of the uterus when the posterior wall suture does not go well. We here summarized several experiences on precautions during surgery. First, the cervix needs to be fully dilated before surgery. Second, in the suture technique, the needle should be inserted into the superficial layer of the myometrium to ensure an effective suture and prevent withdrawing the needle difficultly. Third, to identify the knot position, scale marks can be made on the knotting rod, as a reference of the preoperative depth of the uterine during the hysteroscopic surgery. This study has demonstrated the safety and feasibility of the surgery. We recommend this procedure as a first-line option for the treatment of adenomyosis patients at high risk of IUD expulsion. The disadvantage of this approach is that suture fixation and removal of the LNG-IUD are procedures that should be performed through a hysteroscope, which may increase the financial burden on patients. However, the overall cost decreases year by year, as no additional expenditure is required. The most important limitation of the present study was: that due to the small number of patients in the study, this may limit the generalizability of the results. Nonetheless, this study was the second to evaluate the safety and efficacy of hysteroscopic suture fixation of the LNG-IUD to treat adenomyosis patients. For now, we have performed suture fixation of the LNG-IUD in 40 patients. We will continue to evaluate the practicability of this surgical method. Conclusion Hysteroscopic suture fixation of the LNG-IUD can prevent the IUD expulsion from the uterus without affecting its efficacy and increasing adverse reactions. Therefore, hysteroscopic suture fixation of the LNG-IUD is worthy of clinical application in adenomyosis patients at high risk of LNG-IUD expulsion. Declarations Ethics approval and consent to participate The study was approved by the Ethics Committee of Chengdu First People’s Hospital, and all subjects have signed written informed consent. Consent to publication Not applicable. Availability of data and materials The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request. Funding Not applicable. Acknowledgements We greatly appreciate the patients who participated in the study. References Abbott JA. Adenomyosis and Abnormal Uterine Bleeding (AUB-A)-Pathogenesis, diagnosis, and management. Best Pract Res Clin Obstet Gynaecol. 2017. 40: 68-81. McElin TW, Bird CC. Adenomyosis of the uterus. Obstet Gynecol Annu. 1974. 3(0): 425-41. Osuga Y, Fujimoto-Okabe H, Hagino A. Evaluation of the efficacy and safety of dienogest in the treatment of painful symptoms in patients with adenomyosis: a randomized, double-blind, multicenter, placebo-controlled study. Fertil Steril. 2017. 108(4): 673-678. Osuga Y, Watanabe M, Hagino A. Long-term use of dienogest in the treatment of painful symptoms in adenomyosis. J Obstet Gynaecol Res. 2017. 43(9): 1441-1448. Kavoussi SK, Esqueda AS, Jukes LM. Elagolix to medically treat a uterine adenomyoma: A case report. Eur J Obstet Gynecol Reprod Biol. 2020. 247: 266-267. Schlaff WD, Ackerman RT, Al-Hendy A, et al. Elagolix for Heavy Menstrual Bleeding in Women with Uterine Fibroids. N Engl J Med. 2020. 382(4): 328-340. Nijenhuis RJ, Smeets AJ, Morpurgo M, et al. Uterine artery embolisation for symptomatic adenomyosis with polyzene F-coated hydrogel microspheres: three-year clinical follow-up using UFS-QoL questionnaire. Cardiovasc Intervent Radiol. 2015. 38(1): 65-71. de Bruijn AM, Smink M, Hehenkamp W, et al. Uterine Artery Embolization for Symptomatic Adenomyosis: 7-Year Clinical Follow-up Using UFS-Qol Questionnaire. Cardiovasc Intervent Radiol. 2017. 40(9): 1344-1350. Pelage JP, Jacob D, Fazel A, et al. Midterm results of uterine artery embolization for symptomatic adenomyosis: initial experience. Radiology. 2005. 234(3): 948-53. Sheng J, Zhang WY, Zhang JP, Lu D. The LNG-IUS study on adenomyosis: a 3-year follow-up study on the efficacy and side effects of the use of levonorgestrel intrauterine system for the treatment of dysmenorrhea associated with adenomyosis. Contraception. 2009. 79(3): 189-93. Peng FS, Wu MY, Yang JH, Chen SU, Ho HN, Yang YS. Insertion of the Mirena intrauterine system for treatment of adenomyosis-associated menorrhagia: a novel method. Taiwan J Obstet Gynecol. 2010. 49(2): 160-4. Zhu L, Yang X, Cao B, Tang S, Tong J. The suture fixation of levonorgestrel-releasing intrauterine device using the hysteroscopic cold-knife surgery system: an original method in treatment of adenomyosis. Fertil Steril. 2021. 116(4): 1191-1193. Higham JM, O', Brien PM, Shaw RW. Assessment of menstrual blood loss using a pictorial chart. Br J Obstet Gynaecol. 1990. 97(8): 734-9. Bourdel N, Alves J, Pickering G, Ramilo I, Roman H, Canis M. Systematic review of endometriosis pain assessment: how to choose a scale. Hum Reprod Update. 2015. 21(1): 136-52. Aoun J, Dines VA, Stovall DW, Mete M, Nelson CB, Gomez-Lobo V. Effects of age, parity, and device type on complications and discontinuation of intrauterine devices. Obstet Gynecol. 2014. 123(3): 585-592. Bahamondes L, Díaz J, Marchi NM, Petta CA, Cristofoletti ML, Gomez G. Performance of copper intrauterine devices when inserted after an expulsion. Hum Reprod. 1995. 10(11): 2917-8. Zhang H, Cao B, Tong J, et al. An innovative surgical approach: suture fixation of the levonorgestrel-releasing intrauterine system in the treatment of adenomyosis. BMC Womens Health. 2022. 22(1): 451. Tables Tables 1-2 is available in the Supplementary Files section. Additional Declarations No competing interests reported. Supplementary Files table1.docx table2.docx Cite Share Download PDF Status: Published Journal Publication published 09 Oct, 2024 Read the published version in BMC Women's Health → Version 1 posted Editorial decision: Revision requested 15 Jul, 2024 Reviews received at journal 12 Jul, 2024 Reviews received at journal 10 Jul, 2024 Reviews received at journal 30 Jun, 2024 Reviewers agreed at journal 30 Jun, 2024 Reviewers agreed at journal 29 Jun, 2024 Reviewers agreed at journal 27 Jun, 2024 Reviewers agreed at journal 27 Jun, 2024 Reviewers agreed at journal 27 Jun, 2024 Reviewers invited by journal 11 May, 2024 Editor invited by journal 24 Apr, 2024 Submission checks completed at journal 23 Apr, 2024 Editor assigned by journal 23 Apr, 2024 First submitted to journal 22 Apr, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4303936","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":294966950,"identity":"e23ed371-b09a-4d25-9ca0-4234926f0293","order_by":0,"name":"Min Mao","email":"","orcid":"","institution":"Chengdu First People’s Hospital","correspondingAuthor":false,"prefix":"","firstName":"Min","middleName":"","lastName":"Mao","suffix":""},{"id":294966951,"identity":"7a5bdddc-e562-4d37-8c06-842771480539","order_by":1,"name":"Yuanqin Gou","email":"","orcid":"","institution":"Chengdu First People’s Hospital","correspondingAuthor":false,"prefix":"","firstName":"Yuanqin","middleName":"","lastName":"Gou","suffix":""},{"id":294966953,"identity":"99b5902e-a48a-4513-a648-ceb75a453008","order_by":2,"name":"Zhigui Luo","email":"","orcid":"","institution":"Chengdu First People’s Hospital","correspondingAuthor":false,"prefix":"","firstName":"Zhigui","middleName":"","lastName":"Luo","suffix":""},{"id":294966955,"identity":"205461c8-2acd-4ea3-a036-6ac7a32f5b85","order_by":3,"name":"Yuanhong Li","email":"","orcid":"","institution":"Chengdu First People’s Hospital","correspondingAuthor":false,"prefix":"","firstName":"Yuanhong","middleName":"","lastName":"Li","suffix":""},{"id":294966957,"identity":"daaf3b9a-5272-4c58-a4ad-82e1745394f6","order_by":4,"name":"Yu Tong","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAq0lEQVRIiWNgGAWjYDACZgglx8befoA0LcZ8PGcSSLMscZ6EgwFxSuXb2Z9JMLYdTm+TYEhg+FGxjbAWxmYeM5CW3DbpxgOMPWduE9bCzMzDBtEicyCBmbGNCC1szFCHsUkkGBCnhYeZAeywBOK1SDDzGFswnEs3bAMG8kGi/CLff/zhDYYya3n59vaDD35UEKEFBJj/skEYB4hTDwZ/SFA7CkbBKBgFIw8AABP8MiEWxLIvAAAAAElFTkSuQmCC","orcid":"","institution":"West China Second University Hospital, Sichuan University","correspondingAuthor":true,"prefix":"","firstName":"Yu","middleName":"","lastName":"Tong","suffix":""}],"badges":[],"createdAt":"2024-04-22 07:31:03","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4303936/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4303936/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12905-024-03390-8","type":"published","date":"2024-10-09T15:57:32+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":55636236,"identity":"f1e2e1c8-86b6-4ca8-8012-89c93c04b5ce","added_by":"auto","created_at":"2024-04-30 20:47:16","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":982378,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend.\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-4303936/v1/7d8cdc81aaf1d281c99e345e.png"},{"id":66597372,"identity":"73025c34-1f5f-4b95-a8bc-51a66f6784a9","added_by":"auto","created_at":"2024-10-14 16:10:09","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1778057,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4303936/v1/0014d835-122d-4428-b9cb-521481456c37.pdf"},{"id":55636238,"identity":"c587f5ea-5f2a-4036-b971-b1af16245496","added_by":"auto","created_at":"2024-04-30 20:47:16","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":15958,"visible":true,"origin":"","legend":"","description":"","filename":"table1.docx","url":"https://assets-eu.researchsquare.com/files/rs-4303936/v1/f4d8f2ec2cb0387b678a0996.docx"},{"id":55637363,"identity":"fd968de5-f300-4a2c-87c9-651d18d30da5","added_by":"auto","created_at":"2024-04-30 20:55:16","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":14469,"visible":true,"origin":"","legend":"","description":"","filename":"table2.docx","url":"https://assets-eu.researchsquare.com/files/rs-4303936/v1/e20fa8d4b2eefb677b88e290.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"The suture fixation of the levonorgestrel-releasing intrauterine device with hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion","fulltext":[{"header":"Background","content":"\u003cp\u003eUterine adenomyosis is a common clinical gynecological disease, affecting approximately 20 to 35 percent of females\u003csup\u003e[1]\u003c/sup\u003e. Hypermenorrhea,\u0026nbsp;secondary anemia,\u0026nbsp;and dysmenorrhea\u0026nbsp;are the typical symptoms of adenomyosis\u003csup\u003e[2]\u003c/sup\u003e that seriously affect the life quality of patients. Hormonal medications used for the treatment of adenomyosis require daily administration. Enlargement of the uterus and recurrence of symptoms are usually documented within six months after hormonal medications are discontinued\u003csup\u003e[3-6]\u003c/sup\u003e. Since adenomyosis is confined to the uterine corpus,\u0026nbsp;the effect of the surgical resection\u0026nbsp;of the uterus\u0026nbsp;is ideal,\u0026nbsp;but\u0026nbsp;it will\u0026nbsp;cause\u0026nbsp;the permanent loss\u0026nbsp;of fertility\u0026nbsp;and the uterus, which is usually unacceptable to women.\u0026nbsp;Studies on UAE (uterine artery embolisation) for adenomyosis showed a 25 percent reduction in uterine volume and overall symptom reduction\u003csup\u003e[7, 8]\u003c/sup\u003e.\u0026nbsp;However, some data demonstrate high failure rates\u0026nbsp;of treatments\u003csup\u003e[9]\u003c/sup\u003e.\u003c/p\u003e\n\u003cp\u003eThe\u0026nbsp;levonorgestrel-releasing intrauterine device (LNG-IUD)\u0026nbsp;has steadily been replacing medication and surgery as a satisfactory management option for women with\u0026nbsp;adenomyosis.\u0026nbsp;Studies have shown that the LNG-IUD effectively improved adenomyosis-associated hypermenorrhea and dysmenorrhea\u003csup\u003e[10]\u003c/sup\u003e. However, one study reported a 25 percent LNG-IUD expulsion rate\u0026nbsp;in patients with adenomyosis\u003csup\u003e[11]\u003c/sup\u003e.\u0026nbsp;It is\u0026nbsp;the clinical requirement\u0026nbsp;to\u0026nbsp;find a method to\u0026nbsp;prevent\u0026nbsp;the LNG-IUD expulsion, especially in patients who are\u0026nbsp;unlikely to receive\u0026nbsp;hysterectomy\u0026nbsp;surgeries.\u0026nbsp;The first case of hysteroscopic\u0026nbsp;suture fixation\u0026nbsp;of\u0026nbsp;the LNG-IUD\u0026nbsp;was\u0026nbsp;described\u0026nbsp;by\u0026nbsp;Zhu L\u0026nbsp;in\u0026nbsp;2021\u003csup\u003e[12]\u003c/sup\u003e, and there is limited data regarding the use of this approach to treat adenomyosis. As the feasibility and safety of this invasive procedure are unclear, we present our experience of 21 patients with large symptomatic adenomyosis treated with hysteroscopic suture fixation of the LNG-IUD.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003e\u003cstrong\u003ePatients\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe diagnosis of adenomyosis was suggested by characteristic clinical manifestations (i.e., heavy menstrual bleeding or dysmenorrhea with uniformly enlarged uterus) and ultrasound findings. A total of\u0026nbsp;21\u0026nbsp;large symptomatic adenomyosis\u0026nbsp;patients admitted to\u0026nbsp;Chengdu First People\u0026rsquo;s\u0026nbsp;Hospital from\u0026nbsp;October\u0026nbsp;2022\u0026nbsp;to\u0026nbsp;March\u0026nbsp;2023\u0026nbsp;were enrolled\u0026nbsp;to study.\u0026nbsp;Inclusion criteria: (a)\u0026nbsp;patients who required\u0026nbsp;uterus\u0026nbsp;preservation;\u0026nbsp;(b) patients with symptoms of hypermenorrhea or dysmenorrhea;\u0026nbsp;(c)\u0026nbsp;patients with\u0026nbsp;preoperative uterine depth \u0026ge; 9 cm or had experienced IUD expulsion; (d)\u0026nbsp;patients\u0026nbsp;without pregnancy and\u0026nbsp;had no fertility requirements in the short term;\u0026nbsp;(e)\u0026nbsp;patients not allergic to\u0026nbsp;LNG-IUS, and\u0026nbsp;(f)\u0026nbsp;patients\u0026nbsp;with good compliance.\u0026nbsp;Exclusion criteria:\u0026nbsp;(a) patients\u0026nbsp;with\u0026nbsp;leiomyoma;\u0026nbsp;(b)\u0026nbsp;patients with cervical or endometrial pathology;\u0026nbsp;(c)\u0026nbsp;Patients with\u0026nbsp;breast\u0026nbsp;tumors;\u0026nbsp;(d) patients who cannot be treated with hormones;\u0026nbsp;(e)\u0026nbsp;patients with\u0026nbsp;abnormal reproductive organs;\u0026nbsp;and\u0026nbsp;(f) patients\u0026nbsp;with\u0026nbsp;hormonal therapy within 6 months.\u0026nbsp;All patients signed informed consent forms, and\u0026nbsp;ethics approval was obtained from\u0026nbsp;the Ethics Committee of\u0026nbsp;Chengdu First People\u0026rsquo;s\u0026nbsp;Hospital.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eOperative procedure\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eBefore treatment,\u0026nbsp;a series of examinations\u0026nbsp;were\u0026nbsp;carried\u0026nbsp;out\u0026nbsp;on\u0026nbsp;the patients, including\u0026nbsp;routine gynecological examination,\u0026nbsp;transvaginal ultrasonography,\u0026nbsp;and\u0026nbsp;basic general check-ups to exclude contraindications.\u0026nbsp;Preoperative cervical cytological examination and diagnostic uterine curettage were performed to exclude malignant diseases if necessary.\u0026nbsp;All of the\u0026nbsp;hysteroscopic suture fixations of the LNG-IUD (Mirena)\u0026nbsp;operations were performed by\u0026nbsp;one\u0026nbsp;experienced\u0026nbsp;surgeon\u0026nbsp;(Yuan-Hong Li)\u0026nbsp;under general anesthesia.\u0026nbsp;The procedure\u0026nbsp;was performed\u0026nbsp;as follows: Step 1 join ethibond suture and the LNG-IUD together; Step 2 Insertion and suture fixation of the LNG-IUD; Step 3 Endoscopic knots; Step 4 Confirm the location of the LNG-IUD. All patients were\u0026nbsp;successfully performed\u0026nbsp;with\u0026nbsp;hysteroscopic suture\u0026nbsp;fixation of the LNG-IUD in the uterine cavity\u0026nbsp;with a non-absorbable suture through an endoscopic needle driver and a knot-pushing device (Figure 1).\u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eStatistical analyses\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eStatistical tests were performed using SPSS Statistics. Measurement data were expressed as the mean \u0026plusmn; standard deviation, and compared between groups using the t-test, and correlation between groups using the linear regression. Enumeration data were presented by n (%).\u0026nbsp;\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eDemographic and clinical characteristics of the patient population are reported in \u003ca href=\"https://europepmc.org/articles/PMC5739955/table/T1/\" target=\"https://europepmc.org/article/MED/table\"\u003eTable 1\u003c/a\u003e.\u0026nbsp;We succeeded in hysteroscopic suture fixation of the LNG-IUD in\u0026nbsp;21\u0026nbsp;cases. No differences were observed in age, BMI, parity, preoperative uterine depth, operative time, and intraoperative blood loss between the patients who with or without a history of IUD expulsion\u0026nbsp;(P\u0026gt;0.05). In our study,\u0026nbsp;ten patients had experienced IUD expulsion 1-3 times, and 80% of them had a history of cesarean section and no vaginal delivery. The\u0026nbsp;average\u0026nbsp;uterine depth was 9.69\u0026nbsp;\u0026plusmn;\u0026nbsp;0.95\u0026nbsp;cm. The\u0026nbsp;operative time was 41.38\u0026nbsp;\u0026plusmn;\u0026nbsp;11.50\u0026nbsp;min.\u0026nbsp;The intraoperative blood loss\u0026nbsp;was\u0026nbsp;16.90\u0026nbsp;\u0026plusmn;\u0026nbsp;12.40\u0026nbsp;mL, which\u0026nbsp;was minimal and no additional hemostatic methods were required\u0026nbsp;during the surgery.\u0026nbsp;The operative time\u0026nbsp;and blood loss had no significant\u0026nbsp;correlation with the uterine volume or the uterine depth\u0026nbsp;(P \u0026gt;0.05). There were no complications or major adverse events\u0026nbsp;at the time of\u0026nbsp;surgery. The patients were discharged 24 hours postoperatively.\u0026nbsp;Unfortunately, during\u0026nbsp;the first month\u0026nbsp;follow-up, a patient\u0026nbsp;underwent laparoscopic hysterectomy in another hospital due to\u0026nbsp;dysmenorrhea which was not alleviated, and the\u0026nbsp;patient was not included in the follow-up.\u003c/p\u003e\n\u003cp\u003eIn this study,\u0026nbsp;twenty\u0026nbsp;patients were followed up for twelve months, and all had symptoms of hypermenorrhea (4/20), dysmenorrhea (3/20), or both (13/20).\u0026nbsp;Efficacy\u0026nbsp;in patients after treatment\u0026nbsp;are shown in Table 2.\u0026nbsp;The pictorial blood loss assessment chart (PBAC) was adopted to evaluate\u0026nbsp;menstrual blood loss among patients\u003csup\u003e[13]\u003c/sup\u003e.\u0026nbsp;A PBAC score \u0026ge;\u0026nbsp;100\u0026nbsp;is used to predict heavy menstrual bleeding.\u0026nbsp;Participants were instructed by the research doctor to fill in the PBAC. A\u0026nbsp;significant\u0026nbsp;decrease in PBAC was\u0026nbsp;observed\u0026nbsp;in the 3, 6, and 12 months after treatment\u0026nbsp;compared with the baseline value\u0026nbsp;(p\u0026nbsp;\u0026lt; .05).\u0026nbsp;Women with anemia, defined as a hemoglobin level \u0026lt; 110 g/L. Among 20 patients, 16 women had anemia, among which ten women had a hemoglobin level of \u0026lt; 90 g/L before treatment.\u0026nbsp;It turned out that\u0026nbsp;women had significantly higher hemoglobin levels\u0026nbsp;after\u0026nbsp;treatment\u0026nbsp;(p\u0026nbsp;\u0026lt; .05)\u0026nbsp;.\u0026nbsp;The visual analogue scale (VAS) from 0 to 10 was used to assess dysmenorrhea in patients and evaluate treatment response. It is considered the gold standard of pain measurement\u003csup\u003e[14]\u003c/sup\u003e. The VAS of dysmenorrhea showed a significant decrease 3, 6, and 12 months after\u0026nbsp;treatment\u0026nbsp;(p\u0026nbsp;\u0026lt; .05).\u0026nbsp;The location of the LNG-IUD was assessed by transvaginal ultrasonography.\u0026nbsp;No patient experienced expulsion of the LNG-IUD during follow-up.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe adverse reactions in patients after treatment were recorded. We evaluated the number of patients who experienced adverse events. The total number of patients with adverse events was 13 (65.0%) in the first 3 months and 5 (25.0%) in the 12 months. Most patients complained of irregular bleeding, breast discomfort, abdominal discomfort, and weight gain. Women in our study were able to tolerate the adverse reactions and it did not appear to impact the device continuation rates. No dyspareunia was observed in our study after treatment.\u0026nbsp;\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eAdenomyosis is considered a notable health problem that challenges physicians all over the world. The etiology of adenomyosis is still unclear, and its presentation tends to be increasingly severe over time until menopause, and the response to treatments is not always successful. Among patients using the LNG-IUD for the treatment of adenomyosis, the rate of LNG-IUD expulsion was found in about 25 percent of the cases. Women who have previously expelled an IUD are at higher risk of IUD expulsion again. Rates of reported IUD expulsion after prior expulsion range from 14 to 31 percent\u003csup\u003e[15, 16]\u003c/sup\u003e. Enlargement of the uterus and recurrence of symptoms are usually documented within six months after the LNG-IUD expulsion.\u0026nbsp;In the present research, we performed hysteroscopic suture fixation of the LNG-IUD in the uterine cavity to prevent the IUD expulsion, which did not affect the structure of the LNG-IUD, and the\u0026nbsp;safety and efficacy of the technique were evaluated.\u003c/p\u003e\n\u003cp\u003eIn our study, it turned out that hysteroscopic suture fixation of the\u0026nbsp;LNG-IUD was significantly effective in\u0026nbsp;improving heavy menstrual bleeding,\u0026nbsp;alleviating pain, and preventing IUD expulsion.\u0026nbsp;All follow-up patients reported obvious relief of menorrhagia and dysmenorrhea at 12 months follow-up.\u0026nbsp;Serious IUD complications including expulsion and perforation were not observed in our study. Less serious side effects including irregular bleeding,\u0026nbsp;leukorrhea, abdomen discomfort, headache, breast discomfort, and weight gain were observed,\u0026nbsp;which\u0026nbsp;are consistent with\u0026nbsp;adverse reactions\u0026nbsp;reported for\u0026nbsp;LNG-IUD insertion\u0026nbsp;in the literature. Further, there is no development of new side effects.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eIn 2022, \u003cem\u003eZhang\u003c/em\u003e\u003cem\u003e\u0026nbsp;et al.\u0026nbsp;\u003c/em\u003ereported the role of LNG-IUD fixation\u003csup\u003e[17]\u003c/sup\u003e, and they stitched and fixed the LNG-IUD on the posterior wall of the uterus. In our experience, the LNG-IUD can also be stitched on the anterior wall of the uterus when the posterior wall suture does not go well.\u0026nbsp;We here\u0026nbsp;summarized several experiences on precautions during surgery. First, the cervix needs to be fully dilated before surgery. Second,\u0026nbsp;in the\u0026nbsp;suture technique,\u0026nbsp;the needle should be inserted into\u0026nbsp;the\u0026nbsp;superficial\u0026nbsp;layer of the myometrium\u0026nbsp;to ensure an\u0026nbsp;effective suture and\u0026nbsp;prevent withdrawing the needle difficultly.\u0026nbsp;Third, to identify the knot position, scale marks can be made on the knotting rod, as a reference of\u0026nbsp;the preoperative depth of the uterine during the\u0026nbsp;hysteroscopic surgery.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThis\u0026nbsp;study\u0026nbsp;has\u0026nbsp;demonstrated the safety and feasibility of\u0026nbsp;the surgery.\u0026nbsp;We recommend this procedure as a first-line option for the treatment of adenomyosis patients at high risk of IUD expulsion. The disadvantage\u0026nbsp;of this approach is that suture fixation and removal of the LNG-IUD are procedures that should be performed through a hysteroscope,\u0026nbsp;which may increase the financial burden on patients. However, the overall cost decreases year by year, as no additional expenditure is required. The most important limitation of the present study was: that due to the small number of patients in the study,\u0026nbsp;this may limit the generalizability of the results.\u0026nbsp;Nonetheless, this study was the\u0026nbsp;second\u0026nbsp;to evaluate the\u0026nbsp;safety and\u0026nbsp;efficacy of\u0026nbsp;hysteroscopic suture fixation of the\u0026nbsp;LNG-IUD\u0026nbsp;to treat\u0026nbsp;adenomyosis patients.\u0026nbsp;For now, we have performed suture fixation of the\u0026nbsp;LNG-IUD in 40 patients.\u0026nbsp;We will continue to evaluate the practicability of this surgical method.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eHysteroscopic suture fixation of the LNG-IUD can prevent the IUD expulsion from the uterus without affecting its efficacy and increasing adverse reactions. Therefore, hysteroscopic suture fixation of the LNG-IUD is worthy of clinical application in adenomyosis patients at high risk of LNG-IUD expulsion.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe study was approved by the Ethics Committee of Chengdu First People\u0026rsquo;s Hospital, and all subjects have signed written informed consent.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and/or analysed during the current study are available from\u0026nbsp;\u003c/p\u003e\n\u003cp\u003ethe corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe greatly appreciate the patients who participated in the study.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAbbott JA. Adenomyosis and Abnormal Uterine Bleeding (AUB-A)-Pathogenesis, diagnosis, and management. Best Pract Res Clin Obstet Gynaecol. 2017. 40: 68-81.\u003c/li\u003e\n\u003cli\u003eMcElin TW, Bird CC. Adenomyosis of the uterus. Obstet Gynecol Annu. 1974. 3(0): 425-41.\u003c/li\u003e\n\u003cli\u003eOsuga Y, Fujimoto-Okabe H, Hagino A. Evaluation of the efficacy and safety of dienogest in the treatment of painful symptoms in patients with adenomyosis: a randomized, double-blind, multicenter, placebo-controlled study. Fertil Steril. 2017. 108(4): 673-678.\u003c/li\u003e\n\u003cli\u003eOsuga Y, Watanabe M, Hagino A. Long-term use of dienogest in the treatment of painful symptoms in adenomyosis. J Obstet Gynaecol Res. 2017. 43(9): 1441-1448.\u003c/li\u003e\n\u003cli\u003eKavoussi SK, Esqueda AS, Jukes LM. Elagolix to medically treat a uterine adenomyoma: A case report. Eur J Obstet Gynecol Reprod Biol. 2020. 247: 266-267.\u003c/li\u003e\n\u003cli\u003eSchlaff WD, Ackerman RT, Al-Hendy A, et al. Elagolix for Heavy Menstrual Bleeding in Women with Uterine Fibroids. N Engl J Med. 2020. 382(4): 328-340.\u003c/li\u003e\n\u003cli\u003eNijenhuis RJ, Smeets AJ, Morpurgo M, et al. Uterine artery embolisation for symptomatic adenomyosis with polyzene F-coated hydrogel microspheres: three-year clinical follow-up using UFS-QoL questionnaire. Cardiovasc Intervent Radiol. 2015. 38(1): 65-71.\u003c/li\u003e\n\u003cli\u003ede Bruijn AM, Smink M, Hehenkamp W, et al. Uterine Artery Embolization for Symptomatic Adenomyosis: 7-Year Clinical Follow-up Using UFS-Qol Questionnaire. Cardiovasc Intervent Radiol. 2017. 40(9): 1344-1350.\u003c/li\u003e\n\u003cli\u003ePelage JP, Jacob D, Fazel A, et al. Midterm results of uterine artery embolization for symptomatic adenomyosis: initial experience. Radiology. 2005. 234(3): 948-53.\u003c/li\u003e\n\u003cli\u003eSheng J, Zhang WY, Zhang JP, Lu D. The LNG-IUS study on adenomyosis: a 3-year follow-up study on the efficacy and side effects of the use of levonorgestrel intrauterine system for the treatment of dysmenorrhea associated with adenomyosis. Contraception. 2009. 79(3): 189-93.\u003c/li\u003e\n\u003cli\u003ePeng FS, Wu MY, Yang JH, Chen SU, Ho HN, Yang YS. Insertion of the Mirena intrauterine system for treatment of adenomyosis-associated menorrhagia: a novel method. Taiwan J Obstet Gynecol. 2010. 49(2): 160-4.\u003c/li\u003e\n\u003cli\u003eZhu L, Yang X, Cao B, Tang S, Tong J. The suture fixation of levonorgestrel-releasing intrauterine device using the hysteroscopic cold-knife surgery system: an original method in treatment of adenomyosis. Fertil Steril. 2021. 116(4): 1191-1193.\u003c/li\u003e\n\u003cli\u003eHigham JM, O\u0026amp;#x27, Brien PM, Shaw RW. Assessment of menstrual blood loss using a pictorial chart. Br J Obstet Gynaecol. 1990. 97(8): 734-9.\u003c/li\u003e\n\u003cli\u003eBourdel N, Alves J, Pickering G, Ramilo I, Roman H, Canis M. Systematic review of endometriosis pain assessment: how to choose a scale. Hum Reprod Update. 2015. 21(1): 136-52.\u003c/li\u003e\n\u003cli\u003eAoun J, Dines VA, Stovall DW, Mete M, Nelson CB, Gomez-Lobo V. Effects of age, parity, and device type on complications and discontinuation of intrauterine devices. Obstet Gynecol. 2014. 123(3): 585-592.\u003c/li\u003e\n\u003cli\u003eBahamondes L, D\u0026iacute;az J, Marchi NM, Petta CA, Cristofoletti ML, Gomez G. Performance of copper intrauterine devices when inserted after an expulsion. Hum Reprod. 1995. 10(11): 2917-8.\u003c/li\u003e\n\u003cli\u003eZhang H, Cao B, Tong J, et al. An innovative surgical approach: suture fixation of the levonorgestrel-releasing intrauterine system in the treatment of adenomyosis. BMC Womens Health. 2022. 22(1): 451.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1-2 is available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Levonorgestrel-releasing intrauterine device (LNG-IUD), Adenomyosis, Hysteroscope, Suture fixation","lastPublishedDoi":"10.21203/rs.3.rs-4303936/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4303936/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eBackground: \u003c/strong\u003eThis study aimed to investigate the safety and efficacy ofsuture fixation of the levonorgestrel-releasing intrauterine device (LNG-IUD) by hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMethods: \u003c/strong\u003e21 patients with large symptomaticadenomyosis were sewed and fixed with the LNG-IUD in the uterus by hysteroscopy to prevent the device expulsion.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults:\u003c/strong\u003eIn this prospective case series, all 21 patients were successfully sewed and fixed with the LNG-IUD in the uterus by hysteroscopy. The amount of menstruation was significantly decreased and dysmenorrhea was significantlyrelieved \u0026nbsp;in 3, 6, and 12 months after surgery compared with before surgery. Only one patient underwent a laparoscopic hysterectomy due to dysmenorrhea which was not alleviated one month later. Serious IUD complications including expulsion and perforation were not observed. There was no development of new side effects than LNG-IUD insertion.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusion: \u003c/strong\u003eSuture fixation of the LNG-IUD by hysteroscope is a safe, effective, and minimally invasive surgical procedure to prevent the device expulsion. It is a good solution for the treatment of patients with large symptomatic adenomyosis.\u003c/p\u003e","manuscriptTitle":"The suture fixation of the levonorgestrel-releasing intrauterine device with hysteroscope for the treatment of adenomyosis in patients at high risk of device expulsion","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-04-30 20:47:11","doi":"10.21203/rs.3.rs-4303936/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-07-15T07:18:55+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-07-12T16:50:30+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-07-10T22:19:38+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-06-30T04:57:59+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"135691719338407520251328668693963593365","date":"2024-06-30T04:46:39+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"329537349933243009313163017912142026136","date":"2024-06-29T09:52:55+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"256274483375577194165486897867044597423","date":"2024-06-27T11:15:45+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"157984413755088104801174220738191574010","date":"2024-06-27T09:44:03+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"180587170332839588641944006782516036976","date":"2024-06-27T08:18:59+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-05-11T11:21:23+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2024-04-24T05:13:57+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-04-23T23:46:08+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-04-23T23:46:08+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Women's Health","date":"2024-04-22T07:24:20+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"9a564817-dd25-4266-952d-5315f2a2671c","owner":[],"postedDate":"April 30th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-10-14T16:05:18+00:00","versionOfRecord":{"articleIdentity":"rs-4303936","link":"https://doi.org/10.1186/s12905-024-03390-8","journal":{"identity":"bmc-womens-health","isVorOnly":false,"title":"BMC Women's Health"},"publishedOn":"2024-10-09 15:57:32","publishedOnDateReadable":"October 9th, 2024"},"versionCreatedAt":"2024-04-30 20:47:11","video":"","vorDoi":"10.1186/s12905-024-03390-8","vorDoiUrl":"https://doi.org/10.1186/s12905-024-03390-8","workflowStages":[]},"version":"v1","identity":"rs-4303936","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4303936","identity":"rs-4303936","version":["v1"]},"buildId":"_2-kVJe1T_tPrBINL-cwx","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}