Surgery for Severe Endometriosis and ART Outcome and Effect of Time Interval Between Surgery and FET

& Objective: To evaluate fertility outcomes in infertile women with severe endometriosis who underwent Frozen embryo transfer (FET) after laparoscopic surgery and assess the optimal time interval between laparoscopy and FET.

& Methods: Number of 215 females with advanced-stage endometriosis were included in this retrospective cohort study. At first embryo were then laparoscopic surgery was performed. Patients received gonadotropin-releasing hormone agonist (GnRH agonist) for the next three months after the laparoscopic surgery. FET was scheduled during the next several time-points after the laparoscopic surgery. The

of treatment such as live birth, the interval between the operation and pregnancy, improved dysmenorrhea/dyspareunia, and post - operative complications were evaluated.

A total of 215 patients with a mean ± SD age of 34.33 ± 6.62 were included, among which, 143 cases (86.2%) had no past medical history. Ninety-three individuals (44%) were referred for the first IVF procedure. The mean ± SD of the infertility period was 4.71 ± 5.43 years. The mean ± SD number of frozen embryos was 2.53 ± 3.36 and the period between the laparoscopic intervention and IVF was 1.58 ± 2.65 months.

Women with severe endometriosis may benefit from embryo freezing before laparoscopic surgery then FET. The optimal time between laparoscopy and embryo transfer is seemed to be between two and four months.

Endometriosis, Laparoscopic Surgery, In vitro fertilization, Fertility Received: 2024/03/04; Accepted: 2024/06/25; Published Online: 18 Aug 2024; Use your device to scan and read the article online Corresponding Information: Fatemeh Davari Tanha, Department of Infertility, Yas Hospital, Tehran University of Medical Sciences, Tehran, Iran Email: [email protected] Copyright © 2024, This is an original open-access article distributed under the terms of the Creative Commons Attribution-noncommercial 4.0 International License which permits copy and redistribution of the material just in noncommercial usages with proper citation.

Endometriosis has been considered as a persistent inflammatory situation that plays a crucial role in fertility, with a prevalence rate of 25 –40% in infertile women (1). Endometriosis is accountable for about 10% of the indications for In vitro fertilization (IVF) (2). This disease can make the in vivo atmosphere destructive for oocyte/embryo and reduce the ovarian reserve. Treatment of endometriosis depends on several factors, such as the severity of symptoms, extent and location of lesions, the patient's desire to become pregnant, and the age of the patient. In mild to moderate endometriosis, surgery may not have a significant and satisfactory result on PR (pregnancy rate). However, tubal blockage, toxicity of the environment, and formation of hydrosalpinx are usually detected in more advanced stages of endometriosis which may impair tube patency, cause infertility, and need excision before assisted conception (3). Pharmaceutical methods such as progestin, danazol, and Gonadotropin releasing hormone (GnRH) analogues are among the treatment’s methods. According to the European society for human reproduction and embriology (ESHRE) guidelines, in women with endometriosis -associated infertility, surgical excision of deep nodular lesions previous to assisted repr oductive technology (ART) is not recognized with regard to reproductive outcome (4). Surgical interventions of severe endometriosis are Maryam Karimi et al. 480 Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research effective in generating a constructive location for victorious conception (5). In addition, in suspicion of severe dysm enorrhea or cancer, surgery before IVF may be essential and warranted. However, some surgical methods may diminish the ovarian reserve, which may culminate in enhancing the risk of infertility (6). Between primary surgery and ART, it is uncertain which gives the greatest managing. Laparoscopy is the most frequent technique applied to identify and treat patients with severe endometriosis, who suffer from pelvic pain. The probability of being pregnant in infertile cases with minimal/mild endometriosis is esti mated to be about 30% several months after surgery, which can be reduced further (7). In complex reproductive technology (ART) -related pregnancies, laparoscopic surgery of mild to moderate endometriosis has been detected to enhance PR as compared with diagnostic laparoscopy alone (8). Colorectal endometriosis was determined by Deep infiltrating endometriosis (DIE) of at least the rectal muscularis. Rectal shaving requires the excision of subserosal/superficial muscularis, and full thickness discoid excision . Segmental colorectal resection also necessitates opening of the bowel lumen, which may culminate in infection and further complications such as suture/anastomotic dehiscence, configuration of rectovaginal fistula, neurogenic bladder, bowel dysfunction, a nd stenosis of the anastomosis (9). The successful role of surgery in the management of endometriosis in patients with infertility is still controversial. In addition, modification of the chronic inflammatory alterations and changes of molecular biology of neighborhood tissue may not be capable by surgery alone (10). Hence, surgery may not be competent to completely renovate the side effects of endometriosis on fertility. Numerous studies have recommended that the surgical removal of DIE and deep endometrio sis nodules might have a favorable impact on IVF outcomes (11) . Additionally, the likelihood of spontaneous pregnancy after the surgery in cases undergoing total resection of DIE was acceptable in previously reported studies (12) . Therefore, it is of great importance to successfully forecast the possibility of fertility, avoid the reappearance of endometriosis, and manage this disease in the long -term. Performing the IVF practice in these patients seems to be logical and cost-effective. There are two definite indications for surgery, severe pain unresponsive to Conservative treatment and hydrosalpinx. In order to discover the fertility rate in patients with severe endometriosis and infertility after laparoscopic surgery, we performed a retrospective cohort study and analyzed the clinical data of patients, with the aim of improving the pregnancy rate, using IVF method.

A total of 215 patients with severe endometriosis, infertility, previous history of laparoscopic surgery or drug therapy, and several previous unsuccessful IVF in Infertility Clinic of Yas and Arash Hospitals from January 2018 to March 2019 were enrolled in this retrospective cohort study. However, 49 patients were excluded from the study and 166 cases were finally included in the study. We had also 72 patients with history of more than two previous IVF, and endometriosis with implantation failure, that underwent surgery for removal of deep DIE. Following DIE resection, they underwent FET for further pregnancy. The diagnosis of advanced stage endometriosis was made, based on American Society of Fertility (ASF) in 1985 (13). Most of the cases had colorectal endometriosis, with length of colorectal specimen 78 (mm) (range: 21–19). These patients had severe endometriosis infiltrating the rectum up to 14 cm from the anus, with more than 21 mm in length, and with at least the muscular layer in depth, and up to 45% of rectal circumference. The diameter of the largest rectal nodule was 28 mm (range: 14-39). Height of the lowest nodule (mm from an al verge) was 83 (range: 29–146). After providing the informed consent, all patients underwent laparoscopic surgery and followed- up for two years. The surgeon -specific method volume is about 50 cases each year. The Committee of Human Research and instituti onal review board at Yas and Arash Hospitals and Tehran University of Medical Sciences approved the using clinical information in our study. The inclusion criteria included patients with histologically confirmed diagnosis of severe endometriosis and infert ility, and women who had entire and detailed clinical, follow -up data evidence. Non-childbearing age patients, cases with previous history of hysterectomy, and any female with incomplete clinical or follow -up data were excluded from the study (54 patients) in Fig1 and Table 1 . Table 1. Demographic data of patient Parameters Number=161 Age (years) 19-45 (34.33±6.62) BMI 16.4–34.2 Surgical antecedents 47 (28.1%) History of IVF 72 (57%) 481 Surgery Endometriosis and ART Outcome Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research Parameters Number=161 Infertility period (years) 0- 27 ( 4.71±5.43) Anti-müllerian hormone (AMH) (pmol/L) 0.1-17 (3.93±4.2) Irregular periods 46 (27.5%) Unsuccessful pregnancy attempt for >12 months 143±3.25 dysmenorrhea 26 (7.2±0.25) Dyschezia 31 (2.42±0.27) Dyspareunia 52 (4.1±0.28) N=numbers of patients, Mean±SD, %=percent of the patients Figure 1. The diagram of allocated patients and fertility outcome of included patients. Managed endometriosis and infertility n=215 54 cases were excluded Surgical treatment n=123 lap endometriosis n=108 Fertility preservation and FET n=72 No referral due to Covid-19 n=17 Spantaneuse pregnancy n=9 Full-term pregnancy n=23 Fail Of FET n=21 Abortion n=1 Ectopic Pregnancy n=1 Total hystrectomy n=15 Reserved GnRH agonist candidate for surrogacy Medical treatment n=38 Dident continue medical intervention due to Covid-19 n=9 GnRH agonist treatment n=29 Maryam Karimi et al. 482 Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research At first fertility preservation was scheduled by embryo freezing, and then all patients underwent laparoscopic surgery by an extremely expert surgeon specializing in treatment for severe endometriosis. We performed rectal shaving for endometriotic invasion to serosal or inadequate infiltration of the rectal muscularis. Depending on multifocality and lesion size, excision of a full -thickness disc or resection of segmental colorectal was performed, if patients confronted with deep muscularis infiltration. All patients received Gonadotropin-releasing hormone agonist (GnRH agonist) for the next three months after the laparoscopic surgery. After this time-point, patients were followed -up after surgery till spontaneous pregnancy was occurred in some cases or accor ding to her accompanied disorders, we performed Frozen embryo transfer (FET) during next several time -points after the laparoscopic surgery and investigated the pregnancy. Only patients with evidence of severe endometriosis in the pathology specimens were included. The purpose of surgery was to correct anatomical disorders, remove hydrosalpinx, cyst, and release pelvic floor adhesions. Fever, infection, bleeding, leukocytosis, and hematoma were considered as minor postoperative complications. The initial outcome would be considered as spontaneous pregnancy after surgical intervention. The secondary outcome was defined as chemical pregnancy (positive human chorionic gonadotropin (hCG) two weeks after FET), clinical pregnancy (detection of gestational sac and detection of heart beat in six weeks of gestation), and take -home baby which is defined as a successful delivery of a healthy baby. All the patients received Diphereline drug for three months after surgery. The follow -up assessments included general information, live birth, the interval between the operation and pregnancy, improved dysmenorrhea/ dyspareunia, and post-operative complications. A beta- hCG test was performed two weeks after embryo transfer. If it was positive, it was considered that the woman had a biochemical pregnancy. Several ultrasound examinations were performed in follow - ups, to confirm the fetal heart and visualization of one or more gestational sacs. Regarding ART, women were supervised as claimed by institutional clinical protocols. Controlled ovarian stimulation (COS) protocols were used with Gonadotrophin-releasing hormone (GnRH) antagonist fixed protocol. Several patients' characteristics such as age, Body mass index (BMI), Antral follicles count (AFC), and AMH were explanatory for starting dose of gonadotropins. Retrieval of oocyte was scheduled 36 hours after HCG injection, and IVF was accomplished according to standard operating procedure. Fertilization was defined as the manifestation of two pronuclei. Embryos were frozen on the third check to fifth day. Specially selected embryos were frozen and we discarded others. Pregnancies were defined by an increasing concentration of serum b-hCG 14 days after ET. Statistical analysis Statistical analysis was performed using SPSS®, v19 (IBM SPSS Statistics, IBM Corporation. Chicago, IL, USA). The distribution of the quantitative variable was checked for normality and then for the study of quantitative data based on the type of distribution, Mann-Whitney U Test or independent t -test. The cumulative pregnancy rate was compared by Kaplan – Meier (KM) method and log rank test. P value < .05 was considered statistically significant.

According to Table 2 , a total of 166 patients with mean ± SD age of 34.33 ± 6.62 (range: 19- 45) were included in this study. When reviewing the past medical history of cases, one patient (0.6%) had hyperthyroidism, 21 individuals (12.6%) had hypothyroidism, and 144 cases (86.8%) had no past medical history. Past abdominal surgical history was reported in 47 women (28.1%); while 71.3% of cases (n=119) had not undergone any surgical procedure. History of IVF was detected in 73 cases (56%); while 93 individuals (44%) were referre d for the first IVF procedure. The mean ± SD of dysmenorrhea, N=numbers of patients, dyschezia, and dyspareunia score according to visual analog pain score (0 -10) was 7.2 ± 0.25, 2.42 ± 0.27, and 4.1 ± 0.28. The mean ± SD of the infertility period was 4.71 ± 5.43 years (ranged: 0- 27). The mean ± SD of anti -müllerian hormone (AMH) was 3.93± 4.2 pmol/L (range: 0-21). A total of 46 women (27.5%) had irregular periods; while regular cycles were detected in 72.5% of included patients (n=120). Analysis of the tr eatment strategy revealed that 30 patients (18.1%) received the drug (Gnrh -a for three months before embryo transfer); while 110 individuals (66.3%) underwent the surgical process. A total of 10 cases (6%) did not receive surgical care due to the COVID -19 pandemic. Those individuals undergoing FET following laparoscopic technique had more take home baby than drugs group (p˂0.0001). Adhesiolysis on posterior cul-de-sac was performed in 28 cases (16.86%); while segmental resect anastomosis and shaving were ap plied in four (3.21%) and 40 (28.07%) patients, respectively. The mean ± SD numbers of frozen embryos transferred were 2.53 ± 3.36 (range: 0-4). The period between the laparoscopic surgery of endometriosis and FET was 2.58 ± 3.65 months (range: 3-12). Rectal endometrial nodules were detected in 87 individuals (52.4%). The rate of minor complications was 3% (n=5). The fertility outcomes are depicted in Figure 1 . A total of 32 live births (19.3%) occurred at the end of the follow-up; while 134 women (80.7%) did not undergo the IVF procedure. Those with a time interval of three to six months after surgery had more favorable outcomes with a significantly higher PR compared with those with six to 12 months (p<0/03). Biochemical pregnancy w as defined as positive B -hCG 14 days after embryo transfer (ET). Ultrasound examinations in follow -ups 483 Surgery Endometriosis and ART Outcome Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research at six weeks after ET also confirmed the fetal heart and clinical pregnancy. Table 2. Intraoperative finding and surgical procedures Parameters Patients N=161 Operative Rout Laparoscopic 108 Laparoscopic converted to open surgery 3 Procedure Performed On The Rectum Adhesiolysis 28 Shaving 29 Full thickness disc excision 1 Colorectal segmental resection 14 Rectal endometrial nodules 84 Diameter of Largest rectal nodule (mm) 28 Length of colorectal specimen (mm) 48 Height of the lowest nodule (mm from anal verge) 78 Management of Urethral Endometriosis Advanced ureterolysis 24 Resection of bladder nodule 3 Bladder endometriosis 12 Colostomy 1 Omentectomy 6 Resection of posterior vagina 6 Appendectomy 3 Adenomyosis 36 R=7 Salpingectomy L=17 Both=15

The results of the current study demonstrated improvement in the fertility rate after FET treatment in infertile women with advanced -stage endometriosis after laparoscopic surgical intervention. We also verified that patients undergoing ET after laparoscopic surgery obtained more satisfactory clinical pregnancy rate compared to group who received drug therapy before FET (p˂0.001). The outcomes depicted higher accomplishment of laparoscopic surgical intervention compared to ART alone. Endometriosis has been considered as the most common gynecologic disease with a negative impact on female fertility rate that can reduce the ovarian reserve (14). There are several available data about the correlation between the severity of endometrios is and infertility (15). This situation can be caused following oxidative stress, exacerbating surgical approach, and improved pelvic inflammatory responses (16, 17). The impact of surgical intervention in mild and severe endometriosis remains controversy regarding reproduction ability (8). Although laparoscopic surgery demonstrated enhancement in fertility outcomes of minimum to mild endometriosis, it is still uncertain by how much it is improved. In addition, there is no obvious and accurate data about t he improvement in the reproductive outcomes by the use of surgical intervention before IVF in advanced -stage endometriosis. However, in one study it was demonstrated that surgical intervention to renovate the uterine anatomy, may improve the results of IVF in women with severe endometriosis and infertility (18) . The results of one study in 2018 demonstrated that IVF Maryam Karimi et al. 484 Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research pregnancy rate was unenthusiastically associated with the severity of the endometriosis. They also concluded that endometrioma had no impact on IVF clinical

(8). We confirmed that in severe endometriosis, surgery may be required prior to any intervention, and IVF technique may assist in contacting with follicles during oocyte recovery, and progress the response of the ovary. Hydrosalpinx is a situation that happens while a fallopian tube is blocked and serous or clear fluid is filled distal to the uterus, which gives the tube a sausage-like or retort-like shape feature. This situation will reduce the PR after the laparoscopic surgery. As a result, in the current study if a noticeable hydrosalpinx was detected in sonography or hysterosalpingography and salpingectomy was scheduled before FET. Bowel surgery for colorectal endometriosis has been considered as a fertility -enhancing interfere nce. Segmental resection is associated with a higher complication rate compared with disk excision; however, the procedure of disk excision is not always practical and preferred choice for colorectal surgeons. Segmental colorectal resection is still freque ntly conducted, particularly in patients with various rectosigmoid nodules and sub-occlusive stenosis of the rectosigmoid junction. In one study in 2017 on 60 patients with severe endometriosis, 15 patients experienced rectal shaving, three full thickness es underwent excision of the disc and 42 cases underwent segmental colorectal resection. The results demonstrated that only one out of ten women was debilitated by colorectal resection (19) . In accordance with the previous mentioned article, present study was obtained satisfactory results following segmental resection anastomosis in infertile women with severe endometriosis. The interval from surgery of severe endometriosis to FET had a noteworthy consequence on the PR in our study. In one study Garcia-Velasco, Mahutte (20), 133 women (147 cycles) who underwent laparoscopic cystectomy due to endometrioma were compared with 56 women (63 cycles) who underwent a transvaginal ultrasound for the diagnosis of endometrioma cysts. The first group entered the IVF cy cle 12 months after surgery, and the second group underwent IVF immediately after the surgery. There was no significant difference between the two groups in terms of number of retrieved oocytes, mature oocytes, number of transferred embryos, fertilization rate, laboratory and clinical pregnancy rate, and abortion rate. They concluded that direct entry into ovarian stimulation cycle in asymptomatic endometrioma reduced the time to reach pregnancy and diminished the cost of treatment and surgical complication s, and that laparoscopic cystectomy improved the IVF outcome. Although Nesbitt-Hawes, Campbell (21) have depicted a one -year median time in patients who conceive naturally following laparoscopic surgery for severe endometriosis, several studies demonstrate d that interval from surgical intervention of endometriosis and FET does not play a crucial role on the PR (22) . The results of the present study showed that the maximum PR was attained in patients undergoing FET cycle in the first three months following endometriosis operation. It seems that FET would be better to be performed during the first months after the endometriosis surgery. In a meta -analysis of women with endometrioma under IVF between 1985 and 2007, twenty studies were assessed, and in five stu dies surgical treatment was compared with expected treatment. The rate of clinical pregnancy was not different between the patients underwent surgical intervention and those with gonadotropin stimulation (23). In the study of Sallam, Garcia‐Velasco (24) patients with surgically diagnosed endometriosis were divided into two groups of patients receiving GnRH agonist treatment for three to six months before IVF and the control group with no intervention before IVF. The result of PR was significantly improved i n study group by diminishing the concentrations of diverse inflammatory cytokines (25, 26). They concluded that extended pituitary down- regulation prior to IVF could be supportive for infertile women with endometriosis. The results of the current study revealed that the PR rate was significantly higher in patients undergoing FET after laparoscopic surgical intervention, compared to patients who received drug therapy without surgery before FET. In the current study, all patients undergoing endometriosis and laparoscopic surgery are candidates for pre-surgery embryo freezing, as the ovarian reserve is reduced, apoptosis will occur, and numerous healthy follicles are removed along with the cyst wall in these types of patients. The remained follicles will not respond satisfactory to induction and the number of M2 follicles is scarce. As a result, in this study at first oocytes retrieval and embryo freezing were scheduled before laparoscopic surgery. Several publications have highlighted the effectiveness of laparoscopic surgery on PRs, in stages I-II of endometriosis (8, 27) . It seems that the efficacy of laparoscopy and further FET in severe form of disease is of great importance (28) . The novelty of the current study is that a triple approach was chosen according to the previously published studies. At first, embryos were collected and frozen and then the patient underwent laparoscopic surgery and finally GnRH agonist for three months. In the next step, the transfer of fetus is conducted via FET with a favor able successful rate. Finding the best approach for treating severe endometriosis is of great importance due to the high incidence of endometriosis among infertile patients. This goal may be more achievable with a long-term study period and large sample si ze, which will be performed in the near future. Further prospective studies are required to ascertain more - detailed strategies for maintaining the fertility of women with severe endometriosis. 485 Surgery Endometriosis and ART Outcome Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research

In this study, the three -phase approaches to severe endometriosis (embryos collection, laparoscopic surgery, GnRH agonist for three months) were scheduled. Here we defined the optimal management such as surgery versus first-line ART for patients with severe deep endometriosis. Despite the lack of definitely recognized relation between severe endometriosis and infertility, IVF treatment may enhance the fertility rates in patients with severe endometriosis. Laparoscopic surgery for endometrioma cysts before FET improved fertility. Additionally, direct entry o f individuals into the ovulation stimulation cycle does not cause surgical complications and saves costs and time. Acknowledgments We appreciate all of the patients for their participating in the study protocol and there was not any conflict of interest or financial disclosures. Conflict of Interest The authors declare that they have no conflict of interest. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for- profit sectors. 1. Ozkan S, Murk W, Arici A. Endometriosis and infertility: epidemiology and evidence‐based treatments. Ann N Y Acad Sci. 2008;1127(1):92- 100. [DOI:10.1196/annals.1434.007] [PMID ] 2. Mneimneh AS, Boulet SL, Sunderam S, Zhang Y, Jamieson DJ, Crawford S, et al. States Monitoring Assisted Reproductive Technology (SMART) Collaborative: data collection, linkage, dissemination, and use. J Womens Health. 2013; 22(7):571-7. [DOI:10.1089/jwh.2013.4452 ] [PMID] 3. Hill CJ, Fakhreldin M, Maclean A, Dobson L, Nancarrow L, Bradfield A, et al. Endometriosis and the fallopian tubes: theories of origin and clinical implications. J Clin Med. 2020;9( 6): 1905. [DOI:10.3390/jcm9061905] [PMID ] [PMCID] 4. Rogers PA, Adamson GD, Al -Jefout M, Becker CM, D'Hooghe TM, Dunselman GA, et al. Research priorities for endometriosis: recommendations from a global consortium of investigators in endometriosis. Reprod Sci. 2017; 24(2):202-26. [PMID] [PMCID ] [DOI:10.1177/1933719116654991] 5. Singh SS, Suen MW. Surgery for endometriosis: beyond medical therapies. Fertil Steril. 2017; 107(3):549-54. [DOI:10.1016/j.fertnstert.2017.01.001] [PMID ] 6. Dunselman G, Vermeulen N, Becker C, Calhaz - Jorge C, D'Hooghe T, De Bie B, et al. ESHRE guideline: management of women with endometriosis. Human Reprod. 2014;29(3):400- 12. [DOI:10.1093/humrep/det457] [PMID ] 7. Xiang Y, Zhu H, Long Y, Huang X, Ouyang Y, Huang W. Endometrial Polyps Effect on Pregnancy Outcomes in Infertile Women with Minimal/Mild Endometriosis: A Retrospective Study. 2021:1- 12. [ DOI:10.21203/rs.3.rs- 145883/v1] 8. AlKudmani B, Gat I, Buell D, Salman J, Zohni K, Librach C, et al. In vitro fertilization success rates after surgically treated endometriosis and effect of time interval between surgery and in vitro fertilization. J Minim Invasive Gynecol. 2018; 25(1):99-104. [DOI:10.1016/j.jmig.2017.08.641 ] [PMID] 9. Nezhat C, Li A, Falik R, Copeland D, Razavi G, Shakib A, et al. Bowel endometriosis: diagnosis and management. Am J Obstet Gynecol. 2018; 218(6):549-62. [DOI:10.1016/j.ajog.2017.09.023] [PMID] 10. Hui Y, Zhao S, Gu J, Hang C. Analysis of factors related to fertility af ter endometriosis combined with infertility laparoscopic surgery. Medicine. 2020;99(21):e20132. [PMCID ] [DOI:10.1097/MD.0000000000020132] [PMID] 11. Bendifallah S, Roman H, d'Argent EM, Touleimat S, Cohen J, Darai E, et al. Colorectal endometriosis-associated infertility: should surgery precede ART? Fertil Steril. 2017;108(3): 525-31. [DOI:10.1016/j.fertnstert.2017.07.002 ] [PMID] 12. Roman H. A national snapshot of the surgical management of deep infiltrating endometriosis of the rectum and colon in France in 2015: a multicenter series of 1135 cases. J Gynecol Obstet Hum Reprod. 2017;46(2):159-65. [DOI:10.1016/j.jogoh.2016.09.004] [PMID ] 13. Li M, Lu M -s, Liu M -l, Deng S, Tang X -h, Han C, et al. An observation of the role of autophagy in patients with endometriosis of different stages during secretory phase and proliferative phase. Curr Gene Ther. 2018;18(5):286-95. [PMID ] [DOI:10.2174/1566523218666181008155039]

Maryam Karimi et al. 486 Volume 9, September – October 2024 Journal of Obstetrics, Gynecology and Cancer Research 14. Taylor HS, Kotlyar AM, Flores VA. Endometriosis is a chronic systemic disease: clinical challenges and novel innovations. Lancet. 2021;397(10276):839-52. [ DOI:10.1016/S0140- 6736(21)00389-5] [PMID] 15. Soriano D, Schonman R, Gat I, Schiff E, Seidman DS, Carp H, et al. Thoracic endometriosis syndrome is s trongly associated with severe pelvic endometriosis and infertility. J Minim Invasive Gynecol. 2012;19(6):742-8. [DOI:10.1016/j.jmig.2012.08.773] [PMID ] 16. Da Broi MG, Navarro PA. Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis -related infertility. Cell Tissue Res. 2016;364(1):1-7. [DOI:10.1007/s00441-015-2339-9] [PMID ] 17. Singh AK, Dutta M, Chattopadhyay R, Chakravarty B, Chaudhury K. Intrafollicular interleukin-8, interleukin-12, and adrenomedullin are the promising prognostic markers of oocyte and embryo quality in women with endometriosis. J Assist Reprod Genet. 2016; 33(10):1363-72. [PMID] [PMCID ] [DOI:10.1007/s10815-016-0782-5] 18. Soriano D, Adler I, Bouaziz J, Zolti M, Eisenberg VH, Goldenberg M, et al. Fertility outcome of laparoscopic treatment in patients with severe endometriosis and repeated in vitro fertilization failures. Fertil Steril. 2016;106(5):1264-9. [DOI:10.1016/j.fertnstert.2016.06.003] [PMID ] 19. Ballester M, Roman H, Mathieu E, Touleimat S, Belghiti J, Daraï E. Prior colorectal surgery for endometriosis-associated infertility improves ICSI-IVF outcomes: results from two expert centres. Eur J Obstet Gynecol Reprod Biol. 2017; 209:95-9. [ DOI:10.1016/j.ejogrb.2016.02.020 ] [PMID] 20. Garcia-Velasco JA, Mahutte NG, Corona J, Zúñiga V, Gilés J, Arici A, et al. Removal of endometriomas before in vitro fertilization does not improve fertility outcomes: a matched, case - control study. Fertil Steril. 2004;81(5) :1194-7. https://doi.org/10.1016/j.fertnstert.2003.04.006 [DOI:10.1016/j.fertnstert.2003.10.032] [PMID ] 21. Nesbitt-Hawes EM, Campbell N, Maley PE, Won H, Hooshmand D, Henry A, et al. The surgical treatment of severe endometriosis positively affects the chance of natural or assisted pregnancy postoperatively. Biomed Res Int. 2015;2015: 438790. [ DOI:10.1155/2015/438790] [ PMID ] [PMCID] 22. Huang X -w, Jie Q, Xia E -l, Ying W. Effect of interval after surgery on in vitro fertilization/ intracytoplasmic sperm injection outcomes in patients with stage III/IV endometriosis. Chin Med J. 2010;123(16):2176-80. 23. Tsoumpou I, Kyrgiou M, Gelbaya TA, Nardo LG. The effect of surgical treatment for endometrioma on in vitro fertilization outcomes: a systematic review and meta -analysis. Fertil Steril. 2009; 92(1):75-87. [DOI:10.1016/j.fertnstert.2008.05.049] [PMID ] 24. Sallam HN, Garcia‐Velasco JA, Dias S, Arici A, Abou‐Setta AM. Long‐term pituitary down‐ regulation before in vitro fertilization (IVF) for women with endometriosis. Cochra ne Database Syst Rev. 2006;2006(1):CD004635. [DOI:10.1002/14651858.CD004635.pub2 ] [PMID] [PMCID] 25. Wu MY, Chen SU, Chao Kh, Chen CD, Yang YS, Ho HN. Mouse embryo toxicity of IL -6 in peritoneal fluids from women with or without endometriosis. Acta Obstet Gynecol Scand. 2001; 80(1):7-11. [ PMID] [ DOI:10.1034/j.1600- 0412.2001.800102.x] 26. Gómez-Torres M-J, Acién P, Campos A, Velasco I. Embryotoxicity of peritoneal fluid in women with endometriosis. Its relation with cytokines and lymphocyte populations. Human Reprod. 2002;17(3):777-81. [DOI:10.1093/humrep/17.3.777] [PMID ] 27. Pabuccu R, Onalan G, Kaya C. GnRH agonist and antagonist protocols for stage I -II endometriosis and endometrioma in in vitro fertilization/intracytoplasmic sperm in jection cycles. Fertil Steril. 2007;88(4):832-9. [DOI:10.1016/j.fertnstert.2006.12.046] [PMID ] 28. Rezaie Keikhaie K, Kaveh M, Bahrami F, Sadegi K, Kamali A, Afshari M. Comparing the Changes of AMH Level Following Two Methods of Laparoscopic Cystectomy for Evaluating Ovarian Reserve in Patients with Endometrioma. J Obstet Gynecol Cancer Res. 2021;6(3):110-5. [DOI:10.30699/jogcr.6.3.110] How to Cite This Article: Karimi, M., Asgari, Z., Rezaee, Z., Davari Tanha, F., Ebrahimi, M., Saeedi, S., et al. Surgery for Severe Endometriosis and ART Outcome and Effect of Time Interval Between Surgery and FET. J Obstet Gynecol Cancer Res. 2024;9(5):479-86. Download citation: RIS | EndNote | Mendeley |BibTeX |