The Effectiveness and Safety of Transabdominal Oocyte Pick-up Using a Vaginal Ultrasound Probe in Patients with Endometrioma Undergoing Oocyte Cryopreservation

In: Research Square · 2024 · doi:10.21203/rs.3.rs-4479416/v1 · W4399519926
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Transabdominal oocyte retrieval using a vaginal ultrasound probe in patients with endometrioma yielded a mean of 6.1 oocytes, with low complication rates, demonstrating safety and effectiveness for cryopreservation.

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This retrospective cohort study assessed the safety and effectiveness of transabdominal oocyte pick-up using a vaginal ultrasound probe in 20 single patients with endometrioma undergoing oocyte cryopreservation, measuring oocytes retrieved, mature (MII) oocytes frozen, a modified follicle-to-oocyte index (mFOI), and complication rates, along with stimulation/procedure characteristics. The average stimulation duration was 9.7 days with 2195 units of gonadotropins, and the mean numbers of oocytes retrieved and MII oocytes frozen were 6.1 and 4.8, respectively, with mean mFOI of 0.93; endometrioma rupture occurred in 4 patients, and only one patient had temporary hospitalization for 6 hours due to severe pelvic pain. A key limitation is that the study is small, retrospective, and conducted in a preprint format that was not peer reviewed. This paper is centrally about endometriosis—specifically endometrioma—by evaluating a transabdominal oocyte retrieval approach in patients with endometrioma undergoing oocyte cryopreservation.

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Abstract

Abstract Background This retrospective cohort study aimed to assess the safety and effectiveness of transabdominal oocyte pick-up using a vaginal ultrasound probe in single women with endometrioma undergoing oocyte cryopreservation (OC). Methods Twenty single women with endometrioma who underwent transabdominal oocyte pick-up using a vaginal ultrasound probe for the purpose of oocyte cryopreservation were included. Primary outcome measures were number of oocytes retrieved, mature oocytes frozen, a modified follicle to oocyte index (FOI), and complication rates. Results The mean age of patients was 33.1±5.8, mean diameter of the endometrioma was 57.9±33.7 mm, mean antral follicle count was 6.3±3.4, mean serum AMH was 0.78±0.55 ng/ml, and mean day 3 serum FSH and estradiol were 9.2±2.3 IU/ml and 57.8±36.5 pg/ml, respectively. The mean duration of stimulation was 9.7±2.3 days, total gonadotropin consumption was 2195±909 units, and duration of the procedure was 9.9±4.2 min. The mean number of oocytes retrieved, MII oocytes frozen, and mFOI were 6.1±3.6, 4.8±2.9, 0.93±0.19 respectively. Conclusions Endometrioma was ruptured in four patients, and only one patient was temporarily hospitalized for six hours for severe pelvic pain. Transabdominal oocyte retrieval using a vaginal probe is safe and effective technique in patients with endometrioma undergoing OC.
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The Effectiveness and Safety of Transabdominal Oocyte Pick-up Using a Vaginal Ultrasound Probe in Patients with Endometrioma Undergoing Oocyte Cryopreservation | 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 Effectiveness and Safety of Transabdominal Oocyte Pick-up Using a Vaginal Ultrasound Probe in Patients with Endometrioma Undergoing Oocyte Cryopreservation Meltem Sönmezer, Yavuz Emre Şükür, Volkan Turan, Nilüfer Akgün, and 7 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4479416/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 01 Jan, 2023 Read the published version in Türk Üreme Tıbbı ve Cerrahisi Dergisi → Version 1 posted You are reading this latest preprint version Abstract Background This retrospective cohort study aimed to assess the safety and effectiveness of transabdominal oocyte pick-up using a vaginal ultrasound probe in single women with endometrioma undergoing oocyte cryopreservation (OC). Methods Twenty single women with endometrioma who underwent transabdominal oocyte pick-up using a vaginal ultrasound probe for the purpose of oocyte cryopreservation were included. Primary outcome measures were number of oocytes retrieved, mature oocytes frozen, a modified follicle to oocyte index (FOI), and complication rates. Results The mean age of patients was 33.1±5.8, mean diameter of the endometrioma was 57.9±33.7 mm, mean antral follicle count was 6.3±3.4, mean serum AMH was 0.78±0.55 ng/ml, and mean day 3 serum FSH and estradiol were 9.2±2.3 IU/ml and 57.8±36.5 pg/ml, respectively. The mean duration of stimulation was 9.7±2.3 days, total gonadotropin consumption was 2195±909 units, and duration of the procedure was 9.9±4.2 min. The mean number of oocytes retrieved, MII oocytes frozen, and mFOI were 6.1±3.6, 4.8±2.9, 0.93±0.19 respectively. Conclusions Endometrioma was ruptured in four patients, and only one patient was temporarily hospitalized for six hours for severe pelvic pain. Transabdominal oocyte retrieval using a vaginal probe is safe and effective technique in patients with endometrioma undergoing OC. Cryopreservation endometriosis endometrioma abdominal oocyte retrieval Figures Figure 1 Background Since the first description of in vitro fertilization (IVF) in the late 1970’s by Steptoe and Edwards, in which the oocyte retrieval was performed using laparoscopic surgery, there has been remarkable technological and scientific improvements in the field of assisted reproductive technologies (ART) [ 1 ]. With these improvements, not only treatment success, but also patient oriented treatment approaches, short-term and long-term safety have become among one of the integral parts of contemporary ART for an optimal management. It has been consistently demonstrated that endometriosis may compromise ovarian reserve by mechanical stress on ovarian cortex and impairing granulosa cell functions through increased oxidative stress, inflammatory mediated damage, apoptosis and reduced mitochondrial energy metabolism and activity[ 2 , 3 ]. The monthly fecundity rate is also decreased in patients with endometriosis especially in the advanced disease [ 4 ]. Furthermore, not only serum anti-müllerian hormone (AMH) levels are lower especially in patients with bilateral endometriomas, a faster decline in serum AMH occurs compared with healthy subjects across all age groups [ 5 , 6 ]. Available evidence suggest that the number of mature oocytes retrieved, and fertilization rates were demonstrated lower in patients with endometriosis compared to those with other infertility etiologies [ 7 ]. In the light of the existing evidence, counseling patients with endometriosis regarding all appropriate fertility preservation options has become a core element in patient-oriented approaches in the context of modern reproductive medicine. Among one of the established options in single women with endometriosis desiring to preserve fertility is oocyte cryopreservation. The conventional oocyte retrieval procedures are performed using standardized oocyte pick-up needles attached on to a vaginal probe. The advantage of vaginal oocyte retrieval is the proximity of the ovaries with the implementing probe that has an increased resolution. However, ovarian access may sometimes be difficult through the vaginal route due to specific pathologies including uterine fibroids, congenital uterine malformations, endometriosis or pelvic adhesions preventing vaginal access. Furthermore, large endometriomas may also render vaginal access more difficult, especially if the ovaries are translocated into the upper pelvic cavity due to existing dense adhesions. The applicability of transabdominal route was first described by Lenz et al. in 1981 for oocyte retrieval [ 8 ]. Then, the method has been utilized in some specific clinical circumstances such as; patients previously underwent hysterectomy for a surrogate pregnancy, those undergoing ovarian transposition, having Müllerian anomalies, patients with distorted pelvic anatomy and with big fibroids [ 9 , 10 ]. Moreover, the procedure was successfully practiced to retrieve follicles from heterotopically transplanted ovarian cortical fragments by two different teams [ 11 , 12 ]. In a retrospective study, Baldini et al., was the first to review the records of 1972 oocyte pick-up procedures and identified 21 women, in which both transabdominal and transvaginal approaches were performed by using the same ultrasound vaginal probe [ 13 ]. In the year 2012, American Society of Reproductive Medicine has declared oocyte cryopreservation as a standard technique following the reports of increased oocyte survival rates. Nevertheless, a considerable proportion of these women do not wish to undergo vaginal oocyte retrieval due to cultural precepts and religious constrictions. In two previous reports, we demonstrated the safety of transabdominal oocyte retrieval using a vaginal probe in patients undergoing IVF for oocyte cryopreservation, and found it as similarly effective when compared with conventional vaginal oocyte pick up [ 14 , 15 ]. In this retrospective cohort study, we further aimed to analyze whether transabdominal oocyte retrieval is a safe and effective technique in single patients with endometrioma undergoing IVF for the purpose of oocyte cryopreservation. Methods Data of 20 virgin patients with endometrioma who underwent transabdominal oocyte pick-up for the purpose of oocyte cryopreservation between April 2021 and January 2024 were reviewed in this retrospective cohort study. Demographic characteristics, hormonal assessment including AMH, day 3 serum follicle stimulating hormone (FSH), luteinizing hormone (LH), estradiol and progesterone levels, and antral follicle counts were assessed. Primary outcome measures were number of oocytes retrieved, number of metaphase 2 oocytes frozen, and complication rates, while secondary outcome measures were duration of the stimulation, duration of the procedure and cumulative gonadotropin dose utilized. As an additional primary outcome measure, we also used a modified follicle to oocyte index (FOI) calculated by dividing the total number of collected oocytes by total number of antral follicles ≥ 12 mm on the day of trigger to assess the performance of the technique as described by us previously [ 15 ]. 15 The study was performed under the principles of Helsinki Declaration, and ethical approval was provided from the Ankara University Ethical Committee (No: 2023000679-2). All the patients underwent progesterone primed ovarian stimulation using 5 mg medroxyprogesterone acetate tablets three times daily (Tarlusal, Deva, Türkiye) with a fixed gonadotropin starting dose ranging between 150 IU/day and 300 IU/day. For ovarian stimulation a combination of recombinant FSH (Gonal F, Merck, Türkiye) and highly purified human menopausal gonadotropins (Menopur, Ferring Pharmaceuticals, Meriofert, IBSA, Türkiye), or a combination of recombinant FSH and LH (Pergoveris, Merck, Türkiye) were used. Follicle growth was monitored using a transabdominal ultrasound probe, and a serial serum estradiol, luteinizing hormone, and progesterone measurements were performed as required. To calculate endometrioma size in those with multiloculated endometriomas and those having bilateral endometrioma, the sum of all existing cysts was calculated. The duration of the procedure was calculated from the onset of the oocyte retrieval needle insertion to the completion of the last follicle aspiration. Final oocyte maturation was performed using a dual trigger method with 250 mg of recombinant hCG (Ovitrelle, Merck, Türkiye) and 0.2 mg of a GnRH analog (Gonapeptyl, Ferring Pharmaceuticals, Türkiye) as previously described by us when at least 2 follicles > 18 mm was observed [ 16 ]. All transabdominal oocyte pick-up procedures were performed according to an algorithmic approach as previously described by us elsewhere [ 14 ]. Oocyte pick-up procedures were performed using a 17-gauge double lumen oocyte retrieval needle (Cook Medical, Australia, and Geotek Healthcare Products, Türkiye) at 35.5 hours following ovulation trigger under inhalation anesthesia (Fig. 1 ). A suction pressure pump adjusted at 150–180 mmHg was utilized (Labotec precise aspiration pump, Germany). For all oocyte retrieval procedures, a standard transvaginal ultrasound probe was used (4–8 MHz vaginal probe; GE, USA, Logic P5, or Philips Clear Vue 350, Netherlands), and all patients received 1 gram of Cefazolin (Cefamezin, Sanofi, Türkiye) and 50 mg of dexketoprofen (Arveles, Manarini, Türkiye). Results The mean age of patients was 33.1±5.8 years (range; 21–44 years), the mean body mass index was 24.7±2.8 kg/m 2 (range; 19.2–29.4 kg/m 2 ), the mean diameter of the endometriomas was 57.9±33.7 mm (range; 22–100 mm), the mean antral follicle count was 6.3±3.4 (range; 1–11). The mean serum AMH, FSH and estradiol levels were 0.77±0.55 ng/ml (range; 0.14–2.3 ng/ml), 9.2±2.3 IU/ml (range; 3–13 IU/ml) and 57.8±36.5 pg/ml (range; 24–178 pg/ml), respectively (Table 1 ). The mean duration of stimulation was 9.7±2.4 days (range: 5–14 days), total gonadotropin consumption was 2195±909 units (range; 750–3900 units), and duration of the procedure was 9.9±4.2 minutes. (range; 2–17 min.) (Table 2 ). The mean number of oocytes retrieved was 6.1±3.6 (range; 1–15), mean number of MII oocytes frozen was 4.8±2.9 (range; 1–12), and mean modified FOI was 0.93±0.19 (range; 0.66–1.33). Endometrioma was ruptured in 4 patients, and only one patient was temporarily hospitalized for six hours for severe pelvic pain. Table 1 Demographic characteristics and baseline hormonal assessment of the patients. Mean±SD Range Age (years) 33.1±5.8 21–44 BMI (kg/m 2 ) 24.7±2.8 19.2–29.4 AMH (ng/ml) 0.78±0.55 0.14–2.3 D3 FSH (IU/mL) 9.2±2.3 3–13 D3 Estradiol (pg/ml) 57.8±36.5 24–178 Antral follicle count (n) 6.3±3.4 1–11 Diameter of endometriomas (mm) 57.9±33.7 mm 22–100 Note : SD: standard deviation; BMI: body mass index; AMH: anti-müllerian hormone; FSH: follicle stimulating hormone. Table 2 Ovarian stimulation outcome of the patients with endometrioma undergoing transabdominal oocyte retrieval. Mean±SD Range Follicles ≥12 mm on trigger day (n) 6.5±3.6 1–16 Cumulative gonadotropin consumption (units) 2195±909 750–3900 Duration of stimulation (days) 9.7±2.4 5–14 Duration of the procedure (min.) 9.9±4.2 2–17 Oocytes retrieved (n) 6.1±3.6 1–15 Mature oocytes frozen (n) 4.8±2.9 1–12 Modified FOI 0.93±0.19 0.66–1.33 Note : SD: standard deviation; FOI: follicle to oocyte index. Of the patients 16 had unilateral, four had bilateral endometrioma. Only one patient had a previous laparoscopic surgery for endometrioma. In two of the patients, oocyte retrieval was performed vaginally from the unaffected ovary, whereas the procedure was performed transabdominally from the ovary with endometrioma since it could not have been accessed transvaginally. No major intraoperative or postoperative complications occurred in any of the patients. None of the patients returned with an intend to use the cryopreserved oocytes at the time of manuscript writing. Discussion In this retrospective cohort study, we demonstrated that transabdominal oocyte retrieval was a safe and effective method in patients with endometrioma undergoing IVF for the purpose of oocyte cryopreservation. It has been well established that the presence of endometriomas reduces ovarian reserve [ 17 ]. In a recent large population-based cohort study enrolling a total of 106.633 patients, laparoscopically confirmed endometriosis diagnosis (n = 3921) was associated with a 50% increased risk of natural premature menopause (hazard ratio 1.51; 95% CI, 1.30–1.74) [ 18 ]. Furthermore, live birth rate per cycle is significantly reduced in patients with endometrioma undergoing laparoscopic surgery before ART [ 19 ]. In the light of the accumulated evidence, a thorough counseling regarding all available fertility preservation options is of paramount importance not only for patients who are scheduled to undergo an endometriosis surgery, but also is extended to include those diagnosed with endometrioma under medical follow up. Among the available fertility preservation options in patients with endometrioma are embryo, oocyte, and ovarian tissue cryopreservation. In essence, there are two major obstacles in patients with endometrioma undergoing oocyte retrieval, first, the risk of pelvic abscess, second, inability to reach the ovaries due to pelvic adhesions and translocated ovaries. Many studies showed that the risk of pelvic infection following endometrioma rupture is as low as < 0.5% when prophylactic antibiotics are used [ 20 ]. However, some well-designed studies demonstrated that, the formation of tubo-ovarian abscess is not linked to the ART procedure itself, but rather represents a sporadic occurrence in endometriosis [ 21 ]. In none of the four patients in whom the endometrioma was ruptured pelvic infection occurred following the oocyte pick up. Even though the mean size of the endometrioma was 57.9 mm, we were able to complete the procedure in all patients, despite in those with a large endometriotic cysts measuring up to 100 mm. Moreover, endometriomas bigger in size renders the abdominal oocyte pick up procedure easier by moving the ovaries out of the pelvic cavity and closer to abdominal wall. In the first reports of abdominal oocyte retrieval, the authors inserted a needle through the abdominal wall, then traversed a full bladder and a transient hematuria occurred in four patients [ 8 ]. In our technique since the bladder is empty such a complication did not occur in any of the patient. Another essential step to follow is the application of continuous downward pressure to approximate the ovaries as close as possible with the tip of the implementing probe. In a previous paper which we described the procedure in an algorithmic approach, superficial epigastric artery injury occurred in two patients both of which resolved spontaneously [ 14 ]. However, both complications occurred in the initial cases before we optimized the procedure. In the current series, the only complication was severe pelvic pain that resolved spontaneously with analgesic administration and 6-hour hospitalization. Notably, the mean duration of the procedure was quite acceptable as 9.9±4.2 min. This is mainly because of increased experience with time and complying with all the steps described previously as an algorithmic approach. One may question whether transabdominal oocyte retrieval is as efficient as transvaginal route in terms oocytes collection. In a previous report enrolling a total of 149 patients we demonstrated that IVF outcome parameters were not different between those undergoing vaginal vs. abdominal oocyte retrieval [ 8 ]. In this cohort we further calculated a modified FOI, which was measured as 0.94±0.18, indicating the effectiveness of the procedure. Another critical issue to discuss is whether the procedure is practical in patient with high body mass index. Barton et al. investigated 69 women undergoing transabdominal follicular aspiration for oocyte retrieval in patients with inaccessible ovaries via transvaginal route and asserted that high BMI > 40 kg/m 2 is one of the indications for transabdominal oocyte retrieval [ 22 ]. In our previous report there was only one patient with BMI > 30kg/m 2 , and in the current study the highest BMI was 29.4 kg/m 2 . However, we observed that increasing BMI makes the procedure more difficult due to increasing subcutaneous fatty tissue and decreasing the sonographic quality. Conclusions As a conclusion, by complying with the critical steps described for the procedure, transabdominal oocyte retrieval using a vaginal probe is a safe and effective method for the purpose of oocyte cryopreservation. However, future studies with larger samples sizes including a comprehensive comparison of vaginal vs. abdominal oocyte retrieval are definitely required to make a more clear-cut conclusion in terms of safety and effectiveness. Abbreviations ART Assisted Reproductive Technologies AMH Anti-Müllerian Hormone BMI Body Mass Index CI Confidence Interval FOI Follicle to Oocyte Index FSH Follicle Stimulating Hormone GnRH Gonadotropin-Releasing Hormone hCG Human Chorionic Gonadotropin IVF In Vitro Fertilization LH Luteinizing Hormone mFOI Modified Follicle to Oocyte Index OC Oocyte Cryopreservation pg/ml Picogram per Milliliter IU/ml International Unit per Milliliter Declarations Ethics approval and consent to participate All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards, and Institutional Review Board of Ankara University (Ankara, Turkey) approval was obtained before the patient enrollment. A written informed consent for participating in this trial was obtained from all patients. Availability of data The data in this study are available from the corresponding author upon reasonable request. Availability of and materials Not applicable. Competing interest The authors declare no competing interests. Funding The authors received no financial support for the research, authorship, and/or publication of this article. Authors' contributions MS and YES conceived and designed the study. YES, VT, BO, BB, CA and MS * performed the experiments. NA, BA, EA and KGS gathered and analyzed the data. MS, YES, KGS and MS * wrote the draft and revised the manuscript. All authors read and approved the final manuscript. Acknowledgments The findings of the current study have been partly submitted as an oral presentation to “1 st Mediterranean Obstetrics and Gynecology Congress” that will be held in Adana, Türkiye between September 15 and 17. Consent for publication All authors have provided consent for publication. Patients signed informed consent regarding publishing their data. 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Lenz S, Lauritsen JG, Kjellow M. Collection of human oocytes for in vitro fertilisation by ultrasonically guided follicular puncture. Lancet. 1981;1(8230):1163–4. Steigrad S, Hacker NF, Kolb B. vitro fertilization surrogate pregnancy in a patient who underwent radical hysterectomy followed by ovarian transposition, lower abdominal wall radiotherapy, and chemotherapy. Fertil Steril. 2005;83(5):1547–9. Azem F, et al. Surrogate pregnancy in a patient who underwent radical hysterectomy and bilateral transposition of ovaries. Fertil Steril. 2003;79(5):1229–30. Oktay K, et al. Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm. JAMA. 2001;286(12):1490–3. Stern CJ, et al. First reported clinical pregnancy following heterotopic grafting of cryopreserved ovarian tissue in a woman after a bilateral oophorectomy. Hum Reprod. 2013;28(11):2996–9. Baldini D, et al. 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Association Between Laparoscopically Confirmed Endometriosis and Risk of Early Natural Menopause. JAMA Netw Open. 2022;5(1):e2144391. Bourdon M et al. Impact of Endometriosis Surgery on In Vitro Fertilization/Intracytoplasmic Sperm Injection Outcomes: a Systematic Review and Meta-analysis. Reprod Sci, 2024. Benaglia L, et al. Endometrioma and oocyte retrieval-induced pelvic abscess: a clinical concern or an exceptional complication? Fertil Steril. 2008;89(5):1263–6. Villette C, et al. Risks of tubo-ovarian abscess in cases of endometrioma and assisted reproductive technologies are both under-and overreported. Fertil Steril. 2016;106(2):410–5. Barton SE, et al. Transabdominal follicular aspiration for oocyte retrieval in patients with ovaries inaccessible by transvaginal ultrasound. Fertil Steril. 2011;95(5):1773–6. Additional Declarations No competing interests reported. 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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-4479416","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":311168307,"identity":"3caa9abf-58cc-4e91-bbb1-841363c1b422","order_by":0,"name":"Meltem Sönmezer","email":"","orcid":"","institution":"Ankara Ticaret Merkezi","correspondingAuthor":false,"prefix":"","firstName":"Meltem","middleName":"","lastName":"Sönmezer","suffix":""},{"id":311168308,"identity":"c8735ba9-527a-492a-bfdc-8dd760b96840","order_by":1,"name":"Yavuz Emre Şükür","email":"","orcid":"","institution":"Ankara University Faculty of 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Sönmezer","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAzElEQVRIiWNgGAWjYFAD9gYgYWBBihaeAyAtEqRokUgAk4QV6vYfPvboRkWdnPnM51c3/CiQYOBv707Aq8XsRlq6cc4ZNmOZ2zllN3uADpM4c3YDAS08ZtK5bTyJM6Rz0m7wALUYSOQS0HL+DFDLP4n6GZJn0m7+IUrLgRyglgaDBAkJ9mO3ibPlRlqadM6xBMMZPDlst2UMJHgI++X84WPSOTV18hLsx5/dfPPHRo6/vRe/FiTAYwAmiVUOAuwPSFE9CkbBKBgFIwgAAPNHQwaGYICYAAAAAElFTkSuQmCC","orcid":"","institution":"Ankara University Faculty of Medicine","correspondingAuthor":true,"prefix":"","firstName":"Murat","middleName":"","lastName":"Sönmezer","suffix":""}],"badges":[],"createdAt":"2024-05-26 09:08:15","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4479416/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4479416/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.24074/tjrms.2023-99093","type":"published","date":"2023-01-01T20:30:43+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":58152959,"identity":"23baf7aa-1d47-4cf5-b682-038c41805adc","added_by":"auto","created_at":"2024-06-11 20:25:04","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":813516,"visible":true,"origin":"","legend":"\u003cp\u003eThe technique showing transabdominal ultrasound guided follicular aspiration for oocyte retrieval using a vaginal ultrasound probe.\u003c/p\u003e","description":"","filename":"Fig.1.png","url":"https://assets-eu.researchsquare.com/files/rs-4479416/v1/3790f4e780badaa62b5a50a0.png"},{"id":58153714,"identity":"0fdf4083-24a8-4e2a-b728-6e81ea706b5d","added_by":"auto","created_at":"2024-06-11 20:30:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1645998,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4479416/v1/d644a4da-b944-4208-9bd9-d93056f62b1a.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"\u003cp\u003eThe Effectiveness and Safety of Transabdominal Oocyte Pick-up Using a Vaginal Ultrasound Probe in Patients with Endometrioma Undergoing Oocyte Cryopreservation \u003c/p\u003e","fulltext":[{"header":"Background","content":"\u003cp\u003eSince the first description of in vitro fertilization (IVF) in the late 1970\u0026rsquo;s by Steptoe and Edwards, in which the oocyte retrieval was performed using laparoscopic surgery, there has been remarkable technological and scientific improvements in the field of assisted reproductive technologies (ART) [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. With these improvements, not only treatment success, but also patient oriented treatment approaches, short-term and long-term safety have become among one of the integral parts of contemporary ART for an optimal management.\u003c/p\u003e \u003cp\u003eIt has been consistently demonstrated that endometriosis may compromise ovarian reserve by mechanical stress on ovarian cortex and impairing granulosa cell functions through increased oxidative stress, inflammatory mediated damage, apoptosis and reduced mitochondrial energy metabolism and activity[\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. The monthly fecundity rate is also decreased in patients with endometriosis especially in the advanced disease [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. Furthermore, not only serum anti-m\u0026uuml;llerian hormone (AMH) levels are lower especially in patients with bilateral endometriomas, a faster decline in serum AMH occurs compared with healthy subjects across all age groups [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]. Available evidence suggest that the number of mature oocytes retrieved, and fertilization rates were demonstrated lower in patients with endometriosis compared to those with other infertility etiologies [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eIn the light of the existing evidence, counseling patients with endometriosis regarding all appropriate fertility preservation options has become a core element in patient-oriented approaches in the context of modern reproductive medicine. Among one of the established options in single women with endometriosis desiring to preserve fertility is oocyte cryopreservation. The conventional oocyte retrieval procedures are performed using standardized oocyte pick-up needles attached on to a vaginal probe. The advantage of vaginal oocyte retrieval is the proximity of the ovaries with the implementing probe that has an increased resolution. However, ovarian access may sometimes be difficult through the vaginal route due to specific pathologies including uterine fibroids, congenital uterine malformations, endometriosis or pelvic adhesions preventing vaginal access. Furthermore, large endometriomas may also render vaginal access more difficult, especially if the ovaries are translocated into the upper pelvic cavity due to existing dense adhesions.\u003c/p\u003e \u003cp\u003eThe applicability of transabdominal route was first described by Lenz et al. in 1981 for oocyte retrieval [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. Then, the method has been utilized in some specific clinical circumstances such as; patients previously underwent hysterectomy for a surrogate pregnancy, those undergoing ovarian transposition, having M\u0026uuml;llerian anomalies, patients with distorted pelvic anatomy and with big fibroids [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. Moreover, the procedure was successfully practiced to retrieve follicles from heterotopically transplanted ovarian cortical fragments by two different teams [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. In a retrospective study, Baldini et al., was the first to review the records of 1972 oocyte pick-up procedures and identified 21 women, in which both transabdominal and transvaginal approaches were performed by using the same ultrasound vaginal probe [\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eIn the year 2012, American Society of Reproductive Medicine has declared oocyte cryopreservation as a standard technique following the reports of increased oocyte survival rates. Nevertheless, a considerable proportion of these women do not wish to undergo vaginal oocyte retrieval due to cultural precepts and religious constrictions. In two previous reports, we demonstrated the safety of transabdominal oocyte retrieval using a vaginal probe in patients undergoing IVF for oocyte cryopreservation, and found it as similarly effective when compared with conventional vaginal oocyte pick up [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e]. In this retrospective cohort study, we further aimed to analyze whether transabdominal oocyte retrieval is a safe and effective technique in single patients with endometrioma undergoing IVF for the purpose of oocyte cryopreservation.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eData of 20 virgin patients with endometrioma who underwent transabdominal oocyte pick-up for the purpose of oocyte cryopreservation between April 2021 and January 2024 were reviewed in this retrospective cohort study. Demographic characteristics, hormonal assessment including AMH, day 3 serum follicle stimulating hormone (FSH), luteinizing hormone (LH), estradiol and progesterone levels, and antral follicle counts were assessed. Primary outcome measures were number of oocytes retrieved, number of metaphase 2 oocytes frozen, and complication rates, while secondary outcome measures were duration of the stimulation, duration of the procedure and cumulative gonadotropin dose utilized. As an additional primary outcome measure, we also used a modified follicle to oocyte index (FOI) calculated by dividing the total number of collected oocytes by total number of antral follicles\u0026thinsp;\u0026ge;\u0026thinsp;12 mm on the day of trigger to assess the performance of the technique as described by us previously [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e].\u003csup\u003e15\u003c/sup\u003e\u003c/p\u003e \u003cp\u003e The study was performed under the principles of Helsinki Declaration, and ethical approval was provided from the Ankara University Ethical Committee (No: 2023000679-2). All the patients underwent progesterone primed ovarian stimulation using 5 mg medroxyprogesterone acetate tablets three times daily (Tarlusal, Deva, T\u0026uuml;rkiye) with a fixed gonadotropin starting dose ranging between 150 IU/day and 300 IU/day. For ovarian stimulation a combination of recombinant FSH (Gonal F, Merck, T\u0026uuml;rkiye) and highly purified human menopausal gonadotropins (Menopur, Ferring Pharmaceuticals, Meriofert, IBSA, T\u0026uuml;rkiye), or a combination of recombinant FSH and LH (Pergoveris, Merck, T\u0026uuml;rkiye) were used. Follicle growth was monitored using a transabdominal ultrasound probe, and a serial serum estradiol, luteinizing hormone, and progesterone measurements were performed as required.\u003c/p\u003e \u003cp\u003eTo calculate endometrioma size in those with multiloculated endometriomas and those having bilateral endometrioma, the sum of all existing cysts was calculated. The duration of the procedure was calculated from the onset of the oocyte retrieval needle insertion to the completion of the last follicle aspiration.\u003c/p\u003e \u003cp\u003eFinal oocyte maturation was performed using a dual trigger method with 250 mg of recombinant hCG (Ovitrelle, Merck, T\u0026uuml;rkiye) and 0.2 mg of a GnRH analog (Gonapeptyl, Ferring Pharmaceuticals, T\u0026uuml;rkiye) as previously described by us when at least 2 follicles\u0026thinsp;\u0026gt;\u0026thinsp;18 mm was observed [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. All transabdominal oocyte pick-up procedures were performed according to an algorithmic approach as previously described by us elsewhere [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. Oocyte pick-up procedures were performed using a 17-gauge double lumen oocyte retrieval needle (Cook Medical, Australia, and Geotek Healthcare Products, T\u0026uuml;rkiye) at 35.5 hours following ovulation trigger under inhalation anesthesia (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). A suction pressure pump adjusted at 150\u0026ndash;180 mmHg was utilized (Labotec precise aspiration pump, Germany). For all oocyte retrieval procedures, a standard transvaginal ultrasound probe was used (4\u0026ndash;8 MHz vaginal probe; GE, USA, Logic P5, or Philips Clear Vue 350, Netherlands), and all patients received 1 gram of Cefazolin (Cefamezin, Sanofi, T\u0026uuml;rkiye) and 50 mg of dexketoprofen (Arveles, Manarini, T\u0026uuml;rkiye).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eThe mean age of patients was 33.1\u0026plusmn;5.8 years (range; 21\u0026ndash;44 years), the mean body mass index was 24.7\u0026plusmn;2.8 kg/m\u003csup\u003e2\u003c/sup\u003e (range; 19.2\u0026ndash;29.4 kg/m\u003csup\u003e2\u003c/sup\u003e), the mean diameter of the endometriomas was 57.9\u0026plusmn;33.7 mm (range; 22\u0026ndash;100 mm), the mean antral follicle count was 6.3\u0026plusmn;3.4 (range; 1\u0026ndash;11). The mean serum AMH, FSH and estradiol levels were 0.77\u0026plusmn;0.55 ng/ml (range; 0.14\u0026ndash;2.3 ng/ml), 9.2\u0026plusmn;2.3 IU/ml (range; 3\u0026ndash;13 IU/ml) and 57.8\u0026plusmn;36.5 pg/ml (range; 24\u0026ndash;178 pg/ml), respectively (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The mean duration of stimulation was 9.7\u0026plusmn;2.4 days (range: 5\u0026ndash;14 days), total gonadotropin consumption was 2195\u0026plusmn;909 units (range; 750\u0026ndash;3900 units), and duration of the procedure was 9.9\u0026plusmn;4.2 minutes. (range; 2\u0026ndash;17 min.) (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The mean number of oocytes retrieved was 6.1\u0026plusmn;3.6 (range; 1\u0026ndash;15), mean number of MII oocytes frozen was 4.8\u0026plusmn;2.9 (range; 1\u0026ndash;12), and mean modified FOI was 0.93\u0026plusmn;0.19 (range; 0.66\u0026ndash;1.33). Endometrioma was ruptured in 4 patients, and only one patient was temporarily hospitalized for six hours for severe pelvic pain.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eDemographic characteristics and baseline hormonal assessment of the patients.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMean\u0026plusmn;SD\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eRange\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAge (years)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e33.1\u0026plusmn;5.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21\u0026ndash;44\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBMI (kg/m\u003csup\u003e2\u003c/sup\u003e)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e24.7\u0026plusmn;2.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e19.2\u0026ndash;29.4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAMH (ng/ml)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.78\u0026plusmn;0.55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.14\u0026ndash;2.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eD3 FSH (IU/mL)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9.2\u0026plusmn;2.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3\u0026ndash;13\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eD3 Estradiol (pg/ml)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e57.8\u0026plusmn;36.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e24\u0026ndash;178\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAntral follicle count (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6.3\u0026plusmn;3.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;11\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDiameter of endometriomas (mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e57.9\u0026plusmn;33.7 mm\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e22\u0026ndash;100\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"3\"\u003e\u003cb\u003eNote\u003c/b\u003e: SD: standard deviation; BMI: body mass index; AMH: anti-m\u0026uuml;llerian hormone; FSH: follicle stimulating hormone.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eOvarian stimulation outcome of the patients with endometrioma undergoing transabdominal oocyte retrieval.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMean\u0026plusmn;SD\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eRange\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFollicles \u0026ge;12 mm on trigger day (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e6.5\u0026plusmn;3.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;16\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCumulative gonadotropin consumption (units)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e2195\u0026plusmn;909\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e750\u0026ndash;3900\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDuration of stimulation (days)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e9.7\u0026plusmn;2.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5\u0026ndash;14\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDuration of the procedure (min.)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e9.9\u0026plusmn;4.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2\u0026ndash;17\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOocytes retrieved (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e6.1\u0026plusmn;3.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;15\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMature oocytes frozen (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e4.8\u0026plusmn;2.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;12\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eModified FOI\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e0.93\u0026plusmn;0.19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.66\u0026ndash;1.33\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"3\"\u003e\u003cb\u003eNote\u003c/b\u003e: SD: standard deviation; FOI: follicle to oocyte index.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eOf the patients 16 had unilateral, four had bilateral endometrioma. Only one patient had a previous laparoscopic surgery for endometrioma. In two of the patients, oocyte retrieval was performed vaginally from the unaffected ovary, whereas the procedure was performed transabdominally from the ovary with endometrioma since it could not have been accessed transvaginally. No major intraoperative or postoperative complications occurred in any of the patients. None of the patients returned with an intend to use the cryopreserved oocytes at the time of manuscript writing.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn this retrospective cohort study, we demonstrated that transabdominal oocyte retrieval was a safe and effective method in patients with endometrioma undergoing IVF for the purpose of oocyte cryopreservation.\u003c/p\u003e \u003cp\u003eIt has been well established that the presence of endometriomas reduces ovarian reserve [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. In a recent large population-based cohort study enrolling a total of 106.633 patients, laparoscopically confirmed endometriosis diagnosis (n\u0026thinsp;=\u0026thinsp;3921) was associated with a 50% increased risk of natural premature menopause (hazard ratio 1.51; 95% CI, 1.30\u0026ndash;1.74) [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Furthermore, live birth rate per cycle is significantly reduced in patients with endometrioma undergoing laparoscopic surgery before ART [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. In the light of the accumulated evidence, a thorough counseling regarding all available fertility preservation options is of paramount importance not only for patients who are scheduled to undergo an endometriosis surgery, but also is extended to include those diagnosed with endometrioma under medical follow up.\u003c/p\u003e \u003cp\u003eAmong the available fertility preservation options in patients with endometrioma are embryo, oocyte, and ovarian tissue cryopreservation. In essence, there are two major obstacles in patients with endometrioma undergoing oocyte retrieval, first, the risk of pelvic abscess, second, inability to reach the ovaries due to pelvic adhesions and translocated ovaries. Many studies showed that the risk of pelvic infection following endometrioma rupture is as low as \u0026lt;\u0026thinsp;0.5% when prophylactic antibiotics are used [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e]. However, some well-designed studies demonstrated that, the formation of tubo-ovarian abscess is not linked to the ART procedure itself, but rather represents a sporadic occurrence in endometriosis [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. In none of the four patients in whom the endometrioma was ruptured pelvic infection occurred following the oocyte pick up. Even though the mean size of the endometrioma was 57.9 mm, we were able to complete the procedure in all patients, despite in those with a large endometriotic cysts measuring up to 100 mm. Moreover, endometriomas bigger in size renders the abdominal oocyte pick up procedure easier by moving the ovaries out of the pelvic cavity and closer to abdominal wall.\u003c/p\u003e \u003cp\u003eIn the first reports of abdominal oocyte retrieval, the authors inserted a needle through the abdominal wall, then traversed a full bladder and a transient hematuria occurred in four patients [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. In our technique since the bladder is empty such a complication did not occur in any of the patient. Another essential step to follow is the application of continuous downward pressure to approximate the ovaries as close as possible with the tip of the implementing probe. In a previous paper which we described the procedure in an algorithmic approach, superficial epigastric artery injury occurred in two patients both of which resolved spontaneously [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. However, both complications occurred in the initial cases before we optimized the procedure. In the current series, the only complication was severe pelvic pain that resolved spontaneously with analgesic administration and 6-hour hospitalization. Notably, the mean duration of the procedure was quite acceptable as 9.9\u0026plusmn;4.2 min. This is mainly because of increased experience with time and complying with all the steps described previously as an algorithmic approach.\u003c/p\u003e \u003cp\u003eOne may question whether transabdominal oocyte retrieval is as efficient as transvaginal route in terms oocytes collection. In a previous report enrolling a total of 149 patients we demonstrated that IVF outcome parameters were not different between those undergoing vaginal vs. abdominal oocyte retrieval [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. In this cohort we further calculated a modified FOI, which was measured as 0.94\u0026plusmn;0.18, indicating the effectiveness of the procedure.\u003c/p\u003e \u003cp\u003eAnother critical issue to discuss is whether the procedure is practical in patient with high body mass index. Barton et al. investigated 69 women undergoing transabdominal follicular aspiration for oocyte retrieval in patients with inaccessible ovaries via transvaginal route and asserted that high BMI\u0026thinsp;\u0026gt;\u0026thinsp;40 kg/m\u003csup\u003e2\u003c/sup\u003e is one of the indications for transabdominal oocyte retrieval [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. In our previous report there was only one patient with BMI\u0026thinsp;\u0026gt;\u0026thinsp;30kg/m\u003csup\u003e2\u003c/sup\u003e, and in the current study the highest BMI was 29.4 kg/m\u003csup\u003e2\u003c/sup\u003e. However, we observed that increasing BMI makes the procedure more difficult due to increasing subcutaneous fatty tissue and decreasing the sonographic quality.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eAs a conclusion, by complying with the critical steps described for the procedure, transabdominal oocyte retrieval using a vaginal probe is a safe and effective method for the purpose of oocyte cryopreservation. However, future studies with larger samples sizes including a comprehensive comparison of vaginal vs. abdominal oocyte retrieval are definitely required to make a more clear-cut conclusion in terms of safety and effectiveness.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cdiv class=\"DefinitionList\"\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eART\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eAssisted Reproductive Technologies\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eAMH\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eAnti-M\u0026uuml;llerian Hormone\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eBMI\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eBody Mass Index\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eCI\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eConfidence Interval\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eFOI\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eFollicle to Oocyte Index\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eFSH\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eFollicle Stimulating Hormone\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eGnRH\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eGonadotropin-Releasing Hormone\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003ehCG\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eHuman Chorionic Gonadotropin\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eIVF\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eIn Vitro Fertilization\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eLH\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eLuteinizing Hormone\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003emFOI\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eModified Follicle to Oocyte Index\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eOC\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eOocyte Cryopreservation\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003epg/ml\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003ePicogram per Milliliter\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003e\u003cb\u003eIU/ml\u003c/b\u003e\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eInternational Unit per Milliliter\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards, and Institutional Review Board of Ankara University (Ankara, Turkey) approval was obtained before the patient enrollment. A written informed consent for participating in this trial was obtained from all patients.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe data in this study are available from the corresponding author upon reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of and materials\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors received no financial support for the research, authorship, and/or publication of this article.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors\u0026apos; contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eMS and YES\u0026nbsp;conceived and designed the study. YES, VT, BO, BB, CA and MS\u003csup\u003e*\u003c/sup\u003e performed the experiments. NA, BA, EA\u0026nbsp;and KGS\u0026nbsp;gathered and analyzed the data. MS, YES, KGS and MS\u003csup\u003e*\u0026nbsp;\u003c/sup\u003e wrote the draft and revised the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe findings of the current study have been partly submitted as an oral presentation to \u0026ldquo;1\u003csup\u003est\u003c/sup\u003e Mediterranean Obstetrics and Gynecology Congress\u0026rdquo; that will be held in Adana, T\u0026uuml;rkiye between September 15 and 17. \u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll authors have provided consent for publication. Patients signed informed consent regarding publishing their data.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eFishel S. First in vitro fertilization baby-this is how it happened. Fertil Steril. 2018;110(1):5\u0026ndash;11.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKobayashi H, et al. The role of mitochondrial dynamics in the pathophysiology of endometriosis. J Obstet Gynaecol Res. 2023;49(12):2783\u0026ndash;91.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFan W, et al. Decreased oocyte quality in patients with endometriosis is closely related to abnormal granulosa cells. Front Endocrinol (Lausanne). 2023;14:1226687.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGupta S, et al. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247\u0026ndash;57.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNieweglowska D, et al. Age-related trends in anti-Mullerian hormone serum level in women with unilateral and bilateral ovarian endometriomas prior to surgery. Reprod Biol Endocrinol. 2015;13:128.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKasapoglu I, et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertil Steril. 2018;110(1):122\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSanchez AM, et al. Is the oocyte quality affected by endometriosis? A review of the literature. J Ovarian Res. 2017;10(1):43.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLenz S, Lauritsen JG, Kjellow M. Collection of human oocytes for in vitro fertilisation by ultrasonically guided follicular puncture. Lancet. 1981;1(8230):1163\u0026ndash;4.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSteigrad S, Hacker NF, Kolb B. vitro fertilization surrogate pregnancy in a patient who underwent radical hysterectomy followed by ovarian transposition, lower abdominal wall radiotherapy, and chemotherapy. Fertil Steril. 2005;83(5):1547\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAzem F, et al. Surrogate pregnancy in a patient who underwent radical hysterectomy and bilateral transposition of ovaries. Fertil Steril. 2003;79(5):1229\u0026ndash;30.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOktay K, et al. Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm. JAMA. 2001;286(12):1490\u0026ndash;3.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eStern CJ, et al. First reported clinical pregnancy following heterotopic grafting of cryopreserved ovarian tissue in a woman after a bilateral oophorectomy. Hum Reprod. 2013;28(11):2996\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBaldini D, et al. The safe use of the transvaginal ultrasound probe for transabdominal oocyte retrieval in patients with vaginally inaccessible ovaries. Front Women Health. 2018;3(2):1\u0026ndash;3.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eS\u0026ouml;nmezer M, et al. Transabdominal ultrasound guided oocyte retrieval using vaginal ultrasound probe: Definition of the technique. J Obstet Gynaecol Res. 2021;47(2):800\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eS\u0026ouml;nmezer M, et al. Transabdominal ultrasound-guided oocyte retrieval for oocyte cryopreservation using a vaginal probe: a comparison of applicability, effectiveness, and safety with conventional transvaginal approach. J Assist Reprod Genet. 2023;40(2):399\u0026ndash;405.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSeval MM, et al. Dual trigger with gonadotropin-releasing hormone agonist and recombinant human chorionic gonadotropin improves in vitro fertilization outcome in gonadotropin-releasing hormone antagonist cycles. J Obstet Gynaecol Res. 2016;42(9):1146\u0026ndash;51.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLatif S, Saridogan E. Endometriosis, Oocyte, and Embryo Quality. J Clin Med, 2023. 12(13).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eThombre Kulkarni M, et al. Association Between Laparoscopically Confirmed Endometriosis and Risk of Early Natural Menopause. JAMA Netw Open. 2022;5(1):e2144391.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBourdon M et al. Impact of Endometriosis Surgery on In Vitro Fertilization/Intracytoplasmic Sperm Injection Outcomes: a Systematic Review and Meta-analysis. Reprod Sci, 2024.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBenaglia L, et al. Endometrioma and oocyte retrieval-induced pelvic abscess: a clinical concern or an exceptional complication? Fertil Steril. 2008;89(5):1263\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVillette C, et al. Risks of tubo-ovarian abscess in cases of endometrioma and assisted reproductive technologies are both under-and overreported. Fertil Steril. 2016;106(2):410\u0026ndash;5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBarton SE, et al. Transabdominal follicular aspiration for oocyte retrieval in patients with ovaries inaccessible by transvaginal ultrasound. Fertil Steril. 2011;95(5):1773\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e\u003c/ol\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":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Cryopreservation, endometriosis, endometrioma, abdominal oocyte retrieval","lastPublishedDoi":"10.21203/rs.3.rs-4479416/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4479416/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eThis retrospective cohort study aimed to assess the safety and effectiveness of transabdominal oocyte pick-up using a vaginal ultrasound probe in single women with endometrioma undergoing oocyte cryopreservation (OC).\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eTwenty single women with endometrioma who underwent transabdominal oocyte pick-up using a vaginal ultrasound probe for the purpose of oocyte cryopreservation were included. Primary outcome measures were number of oocytes retrieved, mature oocytes frozen, a modified follicle to oocyte index (FOI), and complication rates.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eThe mean age of patients was 33.1\u0026plusmn;5.8, mean diameter of the endometrioma was 57.9\u0026plusmn;33.7 mm, mean antral follicle count was 6.3\u0026plusmn;3.4, mean serum AMH was 0.78\u0026plusmn;0.55 ng/ml, and mean day 3 serum FSH and estradiol were 9.2\u0026plusmn;2.3 IU/ml and 57.8\u0026plusmn;36.5 pg/ml, respectively. The mean duration of stimulation was 9.7\u0026plusmn;2.3 days, total gonadotropin consumption was 2195\u0026plusmn;909 units, and duration of the procedure was 9.9\u0026plusmn;4.2 min. The mean number of oocytes retrieved, MII oocytes frozen, and mFOI were 6.1\u0026plusmn;3.6, 4.8\u0026plusmn;2.9, 0.93\u0026plusmn;0.19 respectively.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eEndometrioma was ruptured in four patients, and only one patient was temporarily hospitalized for six hours for severe pelvic pain. Transabdominal oocyte retrieval using a vaginal probe is safe and effective technique in patients with endometrioma undergoing OC.\u003c/p\u003e","manuscriptTitle":"The Effectiveness and Safety of Transabdominal Oocyte Pick-up Using a Vaginal Ultrasound Probe in Patients with Endometrioma Undergoing Oocyte Cryopreservation","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-06-11 20:25:00","doi":"10.21203/rs.3.rs-4479416/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"bacb174f-3076-4a8b-a158-c868aa9bab17","owner":[],"postedDate":"June 11th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-06-11T20:30:43+00:00","versionOfRecord":{"articleIdentity":"rs-4479416","link":"https://doi.org/10.24074/tjrms.2023-99093","journal":{"identity":"turk-ureme-tibbi-ve-cerrahisi-dergisi","isVorOnly":true,"title":"Türk Üreme Tıbbı ve Cerrahisi Dergisi"},"publishedOn":"2023-01-01 20:30:43","publishedOnDateReadable":"January 1st, 2023"},"versionCreatedAt":"2024-06-11 20:25:00","video":"","vorDoi":"10.24074/tjrms.2023-99093","vorDoiUrl":"https://doi.org/10.24074/tjrms.2023-99093","workflowStages":[]},"version":"v1","identity":"rs-4479416","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4479416","identity":"rs-4479416","version":["v1"]},"buildId":"WvIrzKhiLBfengagbw6Ux","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}

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