Assessing Natural Conception Rates after Laparoscopic Intervention for Endometriosis-Induced Infertility

in the predictive capability of the revised American Fertility Society (r-AFS) classification for fertility outcomes post-surgery emphasize the necessity for more effective prognostic tools like the Endometriosis Fertility Index (EFI). Debate persists regarding the effectiveness of laparoscopic surgery in early-stage endometriosis cases, despite established improvements in fertility rates for minimal and mild endometriosis. Additionally, there’s a pressing need for research exploring optimal management strategies across different endometriosis stages and comparing treatment modalities’ outcomes, from surgery to expectant or medical therapies. Addressing these gaps through further investigation is imperative for enhancing our insights into fertility outcomes following laparoscopy for endometriosis- related infertility [29-32] . The primary aim of this assessment is to evaluate the rate of spontaneous pregnancies in individuals diagnosed with infertility attributed to endometriosis post-laparoscopy. This study seeks to contribute essential insights into the understanding and management of infertility specifically associated with endometriosis, shedding light on the effectiveness of laparoscopic surgery as a potential treatment option for improving natural pregnancy rates in these individuals. 19 www.ijpsonline.com Special Issue 4, 2024 Indian Journal of Pharmaceutical Sciences 20

Research design: The retrospective study was conducted on 550 patients who were presented with infertility and later diagnosed with endometriosis and the data was obtained by examining medical records from the hospital. The patients were infertile women who had undergone surgical laparoscopy in our hospital. The participants from the prior study were also examined closely and excluded if they did not meet the criteria. The recruitment process had the following eligibility criteria. Participants must meet the following criteria; age between 22 y and 35 y, experiencing infertility for at least 12 mo despite unprotected intercourse, having regular menstrual cycles lasting between 28 d and 37 d, diagnosed with endometriosis based on surgical and histological evidence, absence of other infertility factors and confirmed normal fallopian tube function as determined by hysterosalpingography, and no use of ovulatory drug therapy, ART or hormone therapy within 1 y after surgery. This investigation was authorized by the review board for human research at our University Hospital, and signed informed consent was obtained from each woman. Surgical procedures known as laparoscopies were conducted while the patient was under the influence of general anesthesia. The illness stage was assessed using the rAFS classification of the American Society for Reproductive Medicine (ASRM). The laparoscopic surgical procedure entailed the eradication or extraction of all observable endometriotic implants and the dissolution of adhesions. Inclusion and exclusion criteria: Inclusion criteria: Patients who presented with infertility and later diagnosed as endometriosis; patients who are between the ages of 22 y to 35 y old; participants must have been infertile for 12 mo despite unprotected sexual activity; women with a regular menstrual cycle 28 d-37 d, and surgical and histological diagnosis of endometriosis were included in this study. Exclusion criteria: Women without infertility for 24 mo despite unprotected sexual activity; intermittent menstrual periods outside 28 d-37 d and no surgical or histological evidence of endometriosis were excluded from this study. Statistical analysis: A pregnancy that was detected within the uterus occurred within a year following the laparoscopy. In a study comparing pregnant and non-pregnant women, age, Body Mass Index (BMI), length of infertility, CA-125 levels, endometriosis stage, laparoscopic results, and surgical type were compared. All data analyses were done in Statistical Package for the Social Sciences (SPSS) 12.0 (Chicago, Illinois, United States of America (USA)). Fisher’s exact and Mann-Whitney U tests were used as needed. The significance criterion for all analyses was p<0.05.

AND DISCUSSION Patient characteristics of pregnant (n=226) and non- pregnant (n=324) persons are compared in the Table 1. The average age of pregnant patients is 29.9 y, which is lower than the average age of non-pregnant patients, which is 33.1 y. The rates of primary infertility are comparable in both groups. Pregnant individuals exhibit a somewhat elevated BMI (21.9 kg/m2) compared to non-pregnant individuals (21.0 kg/m2). Pregnant patients have a shorter period of infertility, with an average of 31.9 mo, compared to non-pregnant patients who have an average length of 42.9 mo. In pregnant women, CA-125 levels are elevated at 36.9 µ/ml, compared to non-pregnant patients who have levels of 22.0 u/ml. In addition, this study has found a significant p<0.03 of CA-125 levels among pregnant and non-pregnant patients. The prevalence of rAFS stages varies, with stages I-II being more frequent in pregnant individuals and stages III-IV being more prevalent in non-pregnant individuals. In Table 2, the distribution of patients across different rAFS stages is presented. Among the total 550 patients, the majority were classified into stage III, constituting 66.66 % (200 patients). Stage II follows with 150 patients (60.00 %), while stage I and stage IV have 100 patients each, representing 40.00 % and 33.33 % of the total, respectively. The overall percentage distribution indicates that stage III has the highest proportion among the rAFS stages, contributing to 54.55 % of the entire patient population. This table provides a concise overview of the distribution of patients based on their rAFS stage, offering insights into the prevalence of different stages within the studied population. Fig. 1 depicts the pregnancy rate in relation to the rAFS stage among two groups of patients: Those who are pregnant (n=226) and those who are not pregnant (n=324). The patient distribution among the four rAFS phases is as follows; stage I has a www.ijpsonline.com Special Issue 4, 2024Indian Journal of Pharmaceutical Sciences 21 patients. Endometriomas are present in 15.43 % of pregnant individuals and 18.51 % of non-pregnant individuals. Small endometriomas are more common in both groups. There are also reported incidences that affect both sides. The prevalence of peritubal/ subovarian adhesions is higher in non-pregnant patients (44.44 %) compared to pregnant patients (33.62 %). Posterior cul-de-sac obliteration is observed in 26.31 % of pregnant individuals and 25.00 % of non-pregnant individuals. The degree of obliteration varies, with lesions being categorized as partial, total or superficial. These findings offer valuable understanding of the laparoscopic features of endometriosis in both pregnant and non-pregnant populations. prevalence of 22.12 % in pregnant individuals and 24.69 % in non-pregnant individuals. Stage II has a prevalence of 22.12 % in pregnant individuals and 30.86 % in non-pregnant individuals. Stage III has a prevalence of 26.54 % in pregnant individuals and 21.60 % in non-pregnant individuals. Stage IV has a prevalence of 29.20 % in pregnant individuals and 22.83 % in non-pregnant individuals. The data shown in the picture indicates that pregnancy rates change across different stages, hence emphasizing potential correlations between the severity of endometriosis (rAFS stage) and the outcomes of pregnancy. Table 3 displays laparoscopic observations in a group of 226 pregnant patients and 324 non-pregnant Patient characteristics Pregnant patients (n=226) Non-pregnant patients (n=324) p Age (y) 29.9±3.4 33.1±4.0 0.06 Primary infertility (%) 152 (67.25 %) 210 (64.81) 0.06 BMI (kg/m2) 21.9±2.4 21.0±2.3 0.07 Duration of infertility (mo) 31.9±13.9 42.9±32.0 0.08 CA-125 (µ/ml) 36.9±42.9 22.0±16.1 0.03 rAFS stage I-II 100 (44.24 %) 180 (55.55 %) 0.07 III-IV 126 (55.75 %) 144 (44.44 %) TABLE 1: PATIENT CHARACTERISTICS IN PREGNANT AND NON-PREGNANT PATIENTS rAFS Stage Patients Total I 100 (40.00 %) 250 (45.46 %) II 150 (60.00 %) III 200 (66.66 %) 300 (54.55 %) IV 100 (33.33 %) Total 550 (100 %) TABLE 2: NUMBER OF PATIENTS IN EACH rAFS STAGE Fig. 1: Pregnancy rate with respect to rAFS stage Note: ( ): Pregnant patient and ( ): Non-pregnant patient www.ijpsonline.com Special Issue 4, 2024 Indian Journal of Pharmaceutical Sciences 22 Laparoscopic finding Pregnant patients (n=226) Non-pregnant patients (n=324) p Endometrioma 50 (15.43 %) 60 (18.51 %) 0.06 Unilateral 50 (15.43 %) 60 (18.51 %) 0.08 Small 30 (60.00 %) 45 (75.00 %) 0.07 Large 20 (40.00 %) 15 (25.00 %) 0.07 Bilateral 50 (15.43 %) 60 (18.51 %) 0.11 Small Endometrioma 30 (60.00 %) 50 (83.33 %) 0.06 Large Endometrioma 20 (40.00 %) 10 (16.66 %) 0.07 Peritubal/subovarian adhesion 76 (33.62 %) 144 (44.44 %) 0.09 Posterior cul-de-sac obliteration 20 (26.31 %) 36 (25.00 %) 0.11 Partial 16 (21.05 %) 40 (27.77 %) 0.07 Complete 20 (26.31 %) 32 (22.22 %) 0.08 Superficial lesion only 20 (26.31 %) 36 (25.00 %) 0.07 TABLE 3: LAPAROSCOPIC FINDINGS IN PREGNANT AND NON-PREGNANT PATIENTS In a study by Pantou et al. [22] which delved into the efficacy of laparoscopic surgery as a diagnostic and therapeutic measure for infertility among women with undetermined causes despite standard investigations and multiple failed IVF attempts. Out of the 107 eligible women, laparoscopic intervention revealed endometriosis in 62 patients (57.94 %), pelvic adhesions in 25 patients (23.3 %), and unexplained infertility in 20 cases (18.69 %). Following corrective procedures for endometriosis and adhesions, patients were encouraged to conceive naturally, while those with unexplained infertility underwent a single IVF cycle. Within the 1 st y after laparoscopy, 48.38 % of those with diagnosed endometriosis achieved natural conception, resulting in live births for 93.4 % of them. Similarly, 44 % of patients with adhesions attained natural conception. However, among those with unexplained infertility, only 20 % achieved clinical pregnancy after the first IVF cycle. These findings underscore laparoscopy’s promising role in diagnosing and addressing infertility, notably through revealing pertinent diagnostic details, offering a valuable alternative to excessive reliance on IVF for patients with undetermined infertility issues and recurrent IVF failures. In a study by Porpora et al. [33] 47 infertile women underwent laparoscopic treatment for endometriosis. The distribution of endometriosis stages among the patients was 11 % for stage I, 11 % for stage II, 53.3 % for stage III, and 24.4 % for stage IV . Over an average follow-up of 48.5+/-18.44 mo, the overall pregnancy rate reached 64.4 %. The majority, 69 % Table 4 presents the laparoscopic observations in a group of 226 pregnant patients and 324 non- pregnant patients. The predominant procedures in both categories are fulguration, with a prevalence of 30.97 % in pregnant individuals and 31.17 % in non-pregnant individuals, and endometrioma enucleation, with a prevalence of 22.12 % in pregnant individuals and 21.60 % in non-pregnant individuals. Fenestration and fulguration are carried out in 17.69 % of pregnant patients and 18.51 % of non-pregnant instances. In addition, the significant p value was 0.04 among pregnant and non-pregnant patients. The occurrence of unilateral salpingo-oophorectomy is higher in pregnant individuals (13.27 %) compared to non-pregnant patients (9.87 %). The procedure of adhesiolysis is carried out in 8.84 % of pregnant cases and 9.87 % of non-pregnant cases, whereas myomectomy is performed in 7.07 % of pregnant instances and 8.95 % of non-pregnant cases and p value was 0.04. The cumulative intrauterine pregnancy rate in endometriosis patients following laparoscopy follows the guidelines shown in fig. 2. There is a clear upward trend in the cumulative pregnancy rate as seen in the graph. A rate of 0 % is seen at the outset (0 d following laparoscopy), which increases to 18 % at 30 d and 30 % at 120 d. At 360 d after laparoscopy, the trend continues to rise, reaching 50 %. This provides more evidence that laparoscopy may enhance reproductive outcomes for endometriosis patients, since intrauterine pregnancy rates seem to have improved gradually over the year after surgery. www.ijpsonline.com Special Issue 4, 2024Indian Journal of Pharmaceutical Sciences 23 (18 out of 26 women), conceived within 6 mo post- laparoscopy, with 23 % conceiving at 12 mo, 11 % within 24 mo, and another 11 % after 2 y (p<0.01). In addition, this study has found a significant p<0.03 of CA-125 levels among pregnant and non- pregnant patients. Adhesions in the adnexa and tubal conditions notably influenced pregnancy rates. However, no significant differences were observed concerning the disease stage or the presence of ovarian endometrioses. These findings highlight that laparoscopic treatment significantly improves fertility, particularly within the initial 6 mo following surgery, where adnexal adhesions and tubal status play key roles in determining reproductive outcomes. In a retrospective study by Centini et al. [34] at an endometriosis tertiary center, 115 patients who underwent laparoscopic surgery for deep endometriosis-related infertility were assessed. Analysis of fertility outcomes post-surgery correlated pregnancy rates with lesion characteristics; number, size, and location (anterior, posterolateral, pouch of Douglas, or multiple locations). Over an average follow-up of 22 mo, the overall pregnancy rate was 54.78 % (n=63), resulting in a live birth rate of 42.6 % (n=49). Of the patients with the opportunity for spontaneous conception (n=70), the overall pregnancy rate was 60 % (n=42), with 38.5 % (n=27) conceived spontaneously and 21.4 % (n=15) via Assisted Reproductive Technology (ART). Removal of multiple lesions correlated with higher post-surgery pregnancy rates. Interestingly, isolated lesion size and disease location didn’t significantly affect the pregnancy rate, whereas patients receiving their first surgical treatment for multiple lesions exhibited higher pregnancy rates (odds ratio, 4.18). This study highlights that laparoscopic excision of deep endometriosis significantly enhances pregnancy rates, emphasizing the impact of initial surgical intervention on multiple lesions for improved fertility outcomes. Fig. 2: 1 y cumulative intrauterine pregnancy rate in endometriosis patients after laparoscopy Laparoscopic finding Pregnant patients (n=226) Non-pregnant patients (n=324) p Fulguration 70 (30.97 %) 101 (31.17 %) 0.04 Endometrioma enucleation 50 (22.12 %) 70 (21.60 %) 0.07 Fenestration and fulguration 40 (17.69 %) 60 (18.51 %) 0.08 Unilateral salpingo- oophorectomy 30 (13.27 %) 32 (9.87 %) 0.09 Adhesiolysis 20 (8.84 %) 32 (9.87 %) 0.08 Myomectomy 16 (7.07 %) 29 (8.95 %) 0.04 TABLE 4: LAPAROSCOPIC PROCEDURE IN PREGNANT AND NON-PREGNANT PATIENTS www.ijpsonline.com Special Issue 4, 2024 Indian Journal of Pharmaceutical Sciences 24 A prospective cohort study by Bianchi et al. [35] involved 179 infertile women under 38 y exhibiting symptoms or signs of Deep Infiltrative Endometriosis (DIE) in Sao Paulo, Brazil. They were divided into two groups; group A (IVF only, n=105) and group B (extensive laparoscopic DIE excision before IVF, n=64). Out of these, 10 were lost to follow-up. Group B underwent laparoscopic excision of approximately 5±2 DIE lesions. In addition, the significant p value was 0.04 among pregnant and non-pregnant patients. The patient characteristics between groups were similar in terms of age, infertility duration and d 3 serum follicle-stimulating hormone levels. However, group B had more previous IVF attempts. IVF outcomes differed notably between the groups; the total dose of recombinant follicle-stimulating hormone required for ovulation induction was slightly higher in group B (2542 IU) compared to group A (2380 IU), and the number of oocytes retrieved was slightly lower in group B (9) compared to group A (10). Despite these differences, the pregnancy rate after IVF was significantly higher in group B (41 %) than in group A (24 %). Importantly, the odds of achieving pregnancy were 2.45 times greater in the extensive laparoscopic excision group (B) than in the IVF-only group (A). Pregnancy rates post-laparoscopy are influenced by multiple variables. The presence of tubal adhesions may diminish cumulative pregnancy rates, contrasting with cases lacking adhesions. Severity levels of endometriosis significantly impact these rates. Factors such as younger age, superior ovarian reserve, and enhanced sperm parameters are linked to increased pregnancy probabilities. Tubal status, endometriosis severity, age, ovarian reserve, and sperm quality collectively play roles in determining post-laparoscopy pregnancy outcomes [36,37] . Research demonstrates that laparoscopic surgery effectively boosts natural pregnancy rates in women grappling with endometriosis-related infertility, particularly within the initial 6 mo post-surgery. Adnexal adhesions and tubal conditions significantly influence reproductive outcomes, while disease stage and ovarian endometriomas seem less impactful. These findings advocate for laparoscopy as a viable therapeutic avenue for individuals with minimal to moderate endometriosis-related infertility, facilitating the removal of visible endometriotic areas, pelvic restoration and improved fertility. Clinically, this underscores the importance of counselling patients, emphasizing the optimal pregnancy window post-surgery and the significance of pre-surgical assessment for adhesions and tubal conditions. Laparoscopy emerges as a valuable tool in managing endometriosis-related infertility, yet tailored considerations for each patient’s unique characteristics are pivotal in treatment decisions [33,38,39] . The existing literature highlights potential areas for further exploration regarding laparoscopic treatment in endometriosis-related infertility. Studies often exhibit limited long-term follow-up, necessitating comprehensive research to gauge sustained pregnancy rates post-surgery. Understanding how different stages and locations of endometriosis affect natural pregnancy rates after laparoscopy is crucial for tailored treatment approaches. Investigating the impact of adjuvant therapies combined with surgery on fertility outcomes is a pertinent avenue for future research. Developing predictive models considering patient-specific factors like age and severity of endometriosis is pivotal for informed patient selection. Moreover, assessing the surgery’s impact on patients’ overall quality of life beyond just achieving pregnancy would offer a more comprehensive perspective. In summary, addressing these aspects- long-term follow-up, diverse endometriosis types, adjuvant therapies, patient selection, and quality of life-remains essential for advancing understanding and optimizing treatment strategies [23-26,33,34,37,40] . This study concluded that the current study concludes that among infertile women with endometriosis alone, the natural conception rate was 50.00 % 1 y following laparoscopic surgery. With this knowledge, infertile patients who are seeking treatment for endometriosis and the physicians who are counseling them should find it helpful. There are still significant knowledge gaps about the natural conception rates following laparoscopy for infertility caused by endometriosis, while this area of research has made significant contributions. For starters, when it comes to severe endometriosis, there is a dearth of randomized controlled trials that are designed to evaluate the success of reproductive treatments after surgery. There is a need for better prognostic tools like the EFI because the r-AFS classification is not very good at predicting fertility outcomes. This study found that significantly more pregnant and non-pregnant than pregnant patients and fulguration, and myomectomy was done. We need further studies comparing surgical, expectant and medicinal www.ijpsonline.com Special Issue 4, 2024Indian Journal of Pharmaceutical Sciences 25 treatments for endometriosis so we may better care for patients and make informed treatment decisions. Optimal management options should be the focus of this research. Funding: The project was supported by Suzhou University Horizontal Research Project, (Grant/Award Number: XY202110301612) and Suzhou University Horizontal Research Project, (Grant/Award Number: H230971). Conflict of interests: The authors declared no conflict of interests.

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This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms This article was originally published in a special issue, “Drug Discovery and Repositioning Studies in Biopharmaceutical Sciences” Indian J Pharm Sci 2024:86(4) Spl Issue “18-26”