Primary Cytoreductive Surgery Versus Neoadjuvant Chemotherapy Followed by Surgery in Patients with Advanced Primary Epithelial Ovarian Cancer in Low Resources Setting: A Randomized Clinical Trial.

Primary Cytoreductive Surgery Versus Neoadjuvant Chemotherapy Followed by Surgery in Patients with Advanced Primary Epithelial Ovarian Cancer in Low Resources Setting: A Randomized Clinical Trial - PMC Skip to main content An official website of the United States government Here's how you know Here's how you know Search Log in Primary site navigation Search Log in Search PMC Full-Text Archive Search in PMC Journal List User Guide As a library, NLM provides access to scientific literature. Inclusion in an NLM database does not imply endorsement of, or agreement with, the contents by NLM or the National Institutes of Health. Learn more: PMC Disclaimer | PMC Copyright Notice J Obstet Gynaecol India . 2024 Nov 6;75(3):199–205. doi: 10.1007/s13224-024-02061-w Primary Cytoreductive Surgery Versus Neoadjuvant Chemotherapy Followed by Surgery in Patients with Advanced Primary Epithelial Ovarian Cancer in Low Resources Setting: A Randomized Clinical Trial Hisham Abutaleb 1 , Ali Hussien 1, ✉ , Mohamed Khalaf 1 , Dalia M Badary 2 , Alaa M Ismail 1 , Sara Hassanein 3 , Samy AlGizawy 4 , S A M Moustafa 1 , Rabab Mohmed Mumdouh Farghaly 5 , A F Abdel-Kawi 1, 6 Author information Article notes Copyright and License information 1 Obstetrics and Gynecology Department, Assiut University, Assiut, Egypt 2 Clinical Pathology Department, Assiut University, Assiut, Egypt 3 Diagnostic Radiology Department, Assiut University, Assiut, Egypt 4 Clinical Oncology and Nuclear Medicine Department, Assiut University, Assiut, Egypt 5 Medical Oncology and Hematological Malignancy Department, South Egypt Cancer Institute Assiut University, Assiut, Egypt 6 Marien Hospital, Hamburg, Germany ✉ Corresponding author. Received 2024 Apr 27; Accepted 2024 Sep 3; Issue date 2025 Jun. © Federation of Obstetric & Gynecological Societies of India 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. PMC Copyright notice PMCID: PMC12205117  PMID: 40584804 Abstract Introduction Ovarian cancer (OV) stands as the deadliest female reproductive system malignancy. Globally, OV ranks as the seventh most prevalent cancer in women, with an estimated 240,000 new cases annually and being the second most common malignancy among women in Egypt. Objectives We investigate the efficacy of cytoreductive surgery in achieving complete tumor removal (R0 resection) in OV, compared to neoadjuvant chemotherapy followed by surgery. Method This randomized controlled trial at Women Health Hospital, Asyut University, Egypt from 2020 to 2023. Eighty patients were randomized (1:1) to primary surgery (Group I) or NACT (Group II), followed by further randomization (1:1) within each group to bevacizumab-containing chemotherapy or chemotherapy alone. The primary outcome was the rate of complete tumor removal (R0 resection). Secondary outcomes included surgical complexity, operative time, complications, and survival rates. Results Baseline demographic characteristics were similar between the groups (no statistically significant differences). The mean age for group I and group II were (56.3 and 57.23, respectively). Whereas, the BMI for group I and group II were (32.56 and 33.2, respectively). In addition, both groups achieved no significant difference of complete tumor removal (31 vs. 27). However, group II demonstrated significantly shorter operative times (182.34 vs. 219.85 min, p = 0.047), required fewer blood transfusions (9 vs. 21, p value 0.006), and experienced shorter hospital stays (6.13 vs. 11.9 days, p value < 0.001) compared to group I. Notably, no significant differences emerged in complication rates, progression-free survival (11.20 vs. 11.19 months), or overall survival (11.69 vs. 11.76 months) between the groups. Conclusion Our study demonstrates that optimal cytoreduction is more feasible with NACT, with less surgical complexity, shorter operative duration, less blood transfusion and short hospital stay. Clinical Trials registration The study was registered on clincaltrail.gov with number: NCT04257786 . Supplementary Information The online version contains supplementary material available at 10.1007/s13224-024-02061-w. Keywords: Cytoreductive surgery, Neoadjuvant chemotherapy, Ovarian cancer, Bevacizumab Introduction Ovarian cancer (OV) emerges as the most lethal malignancy within the female reproductive system [ 1 ]. Often dubbed the "silent killer," its vague symptomatology frequently delays diagnosis until advanced stages, hindering curative treatment [ 2 ]. OV ranks as the seventh most common cancer in women globally, with an estimated 240,000 new cases [ 3 ]. In addition: OV cancer ranks as the second most common malignancy among women in Egypt [ 4 ]. Recent research suggests a five-year survival rate of only 47.4% for OV [ 5 ]. Extensive tumor spread in OV often necessitates aggressive cytoreductive surgery (CRS) to achieve complete removal of visible tumors (R0 resection) [ 6 ]. This comprehensive approach frequently involves radical pelvic surgery, bowel resection, and removal of upper abdominal lesions (diaphragm, spleen, liver, etc.). In addition, while R0 resection demonstrably improves survival, maximal surgical effort raises concerns about increased perioperative complications, necessitating a careful balancing act between efficacy and patient safety [ 7 ]. Furthermore, a recent studies demonstrated non-inferiority of neoadjuvant chemotherapy (NACT) to primary surgery in OV, with improved perioperative outcomes. However, these findings haven't significantly impacted treatment guidelines due to persisting concerns [ 8 , 9 ]. Bevacizumab, a VEGF-targeting antiangiogenic agent, gained FDA approval in 2014 for recurrent, platinum-resistant OV, used alongside paclitaxel, topotecan, or pegylated liposomal doxorubicin [ 10 ]. Its application expanded to include first-line treatment of advanced OV following surgery, administered in combination with chemotherapy [ 11 ]. This study investigates the efficacy of primary CRS in achieving complete tumor removal (R0 resection) with minimal surgical complications in patients with advanced epithelial OV, compared to NACT followed by surgery. Materials and Methods This randomized controlled trial ( NCT04257786 ) was conducted at the Department of Obstetrics and Gynecology, Women's Health Hospital, Assiut University, Egypt from 2020 to 2023 The study population included women with histologically confirmed advanced epithelial OV admitted to the hospital. Inclusion criteria specified female patients 18 years or older with FIGO stage 2B or higher epithelial OV confirmed by surgical staging (151). They also required a good performance status (ECOG ≤ 2) (152), no prior chemotherapy, and written consent to participate. Conversely, exclusion criteria included prior abdominal or pelvic chemo/radiotherapy, uncontrolled infections, high bleeding risk, surgical unfitness, and contraindications to bevacizumab-based chemotherapy, pregnancy, recent major surgery, or refusal to participate. Randomization Eighty patients were randomized into two equal groups using computer-generated numbers for a parallel study design. Allocation codes were concealed in opaque envelopes. Group I (n = 40) underwent primary surgery followed by randomization to either chemotherapy plus bevacizumab (Group IA, n = 20) or chemotherapy alone (Group IB, n = 20). Group II (n = 40) received NACT followed by surgery, with further randomization to bevacizumab-containing chemotherapy (Group IIA, n = 20) or chemotherapy alone (Group IIB, n = 20). Primary and Secondary Outcomes This study aimed to determine the success rate of achieving complete tumor removal (R0 resection) for patients. Secondly, assessed the operative outcomes (surgical complexity score, operative time, amount of blood transfused, hospital stay, ICU admission), early post-operative complications (≤ 30 days) (deep venous thrombosis, pulmonary embolism, wound dehiscence, sepsis, primary and secondary hemorrhage, respiratory failure, re- exploration, multi-organ failure and death), and later postoperative complications (1–6 months) (pelvic abscess, urinary and rectal dysfunction, liver failure, incisional hernia, thromboembolic: DVT, stroke, death). Additionally, the study tracked overall survival rate and disease-free survival at one year. Sample Size We employed statistical software to determine an appropriate sample size based on our primary outcome, achieving R0 resection. Referencing Fagotti et al., the assumed R0 rate after primary surgery was 45.5%. Anticipating a 30% increase in R0 with neoadjuvant therapy, the calculated sample size considered a 15% dropout rate, resulting in a target recruitment of 80 patients. Statistical Analysis Statistical analysis was performed using SPSS v26 (IBM Inc., Chicago, IL, USA) to assess group differences. Data normality was evaluated with the Shapiro–Wilk test and histograms. Normally distributed quantitative data were presented as mean ± standard deviation (SD) and compared between groups using unpaired Student's t-tests. Non-normally distributed quantitative data were presented as median and interquartile range (IQR) and analyzed using Mann–Whitney U tests. Categorical variables were presented as frequencies and percentages (%) and analyzed using Chi-square tests or Fisher's exact tests, depending on sample size. A two-tailed p -value < 0.05 was considered statistically significant. Additionally, Kaplan Meier curve was used to show the progression and survival analysis. Results A total of 103 patients were evaluated for eligibility. Seventeen did not meet the inclusion criteria, and six declined participation. The remaining 80 patients were randomized into two groups of 40 each, with further subdivision into two subgroups of 20 patients each (supplementary file 1 ). Patient’s characteristics were comparable between the two groups. There were no statistically significant differences in age (mean 56.3 ± 9.64 years), body mass index (BMI, mean 32.88 ± 5.49), parity, WHO performance status (0, 1, or 2), or tumor response on MRI after NACT (33% partial response, 15% stable disease, 2.5% progressive disease) (Resist). Additionally, histopathological results and CA125 tumor marker were similar between the groups Table 1 . Table 1. Patients characterstics Group I (n = 40) Group II (n = 40) p– value Age (years) Mean ± SD 55.37 ± 9.67 57.23 ± 9.61 0.392 Range 39.91–85.25 36.83–74.75 BMI (kg/m 2 ) Mean ± SD 32.56 ± 5.69 33.2 ± 5.3 0.605 Range 21.5–49.18 24.6–45 Parity Median 4 3.5 0.259 IQR 3–6 1–6 Performance status WHO 0 21 (52.5%) 23 (57.5%) 0.277 WHO 1 19 (47.5%) 15 (37.5%) WHO 2 0 (0%) 2 (5%) Histology – PSC 33 (82.5%) 36 (90%) 0.191 MC 3 (7.5%) 4 (10%) End C 4 (10%) 0 (0%) Figo Staging II6 3 (7.5%) 1 (2.5%) III 33 (82.5%) 29 (72.5%) IV 4 (10%) 10 (25%) MRI before surgery – – CR (0%) – PR 33 (82.5%) SD 6 (15%) PD 1 (2.5%) Group I (n = 40 Group II (n = 39) CA125 Mean ± SD 1124.9 ± 1300.57 970.3 ± 1025.3 0.560 Group I (n = 16) Group II (n = 6) CA19–9 Mean ± SD 13.86 ± 16.17 7.28 ± 5.39 0.347 Group I (n = 28) Group II (n = 23) CEA Mean ± SD 3.45 ± 7.9 2.57 ± 1.56 0.604 Open in a new tab BMI, body mass index; DM, diabetes mellitus; HTN, hypertension; WHO 0, asymptomatic; WHO 1, symptomatic, fully ambulatory; WHO 2, symptomatic, in bed < 50% of the day; PSC, papillary serous cystadenocarcinoma; MC, mucinous cystadenocarcinoma; End C, endometroid adenocarcinoma; CR, complete remission; PR, partial regression; SD, stable disease; PD, progressive disease The study found no significant differences between the groups in terms of the extent of tumor resection (R0, R1, and R2). While a higher number of patients in group II achieved complete resection (R0) compared to group I (31 vs. 27), this difference was not statistically significant. However, the analysis revealed significant differences in surgical aspects between the groups. Group II had a lower proportion of complex surgeries compared to group I ( p = 0.029). Additionally, the mean operative time in group II was significantly shorter (182.34 min) compared to group I (219.85 min) ( p = 0.047). Furthermore, significantly fewer patients in group II required blood transfusions compared to group I (9 vs. 21, p -value 0.006). Notably, there were no significant differences between the groups regarding intraoperative complications Table 2 . Table 2. Surgical outcomes of the studied groups Group I Group II P -value Residual R0 27 (67.5%) 31 (77.5%) 0.267 R1 4 (10%) 6 (15%) R2 9 (22.5%) 3 (7.5%) Complexity score group 1 (Low) 12 (30%) 20 (50%) 0.068 2 (Intermediate) 20 (50%) 19 (47.5%) 0.155 3 (High) 8 (20%) 1 (2.5%) 0.029* Operative time (min) Mean ± SD 219.85 ± 101.48 182.43 ± 58.77 0.047* Range 80–410 90–333 Patients transfused 21 (52.5%) 9 (22.5%) 0.006* Complications Intestinal injury 1 (2.5%) 1 (2.5%) 0.068 Bleeding 6 (15%) 1 (2.5%) Ureteric injury 2 (5%) 0 (0%) Bladder injury 0 (0%) 5 (12.5%) Bleeding and bladder injury 1 (2.5%) 1 (2.5%) Intestinal + bladder + IVC 1 (2.5%) 0 (0%) No 29 (72.5%) 32 (80%) Open in a new tab BSO, bilateral salpingo-oophorectomy *Significantly different as P value ≤ 0.05 Analysis of postoperative outcomes revealed significant differences in hospital stay but no major differences in complication rates. The mean length of hospital stay was significantly shorter in group II (6.13 days) compared to group I (11.9 days) ( p -value < 0.001). Additionally, group II exhibited a trend towards better wound healing, with a higher number of patients experiencing good healing (34 vs. 20) and fewer patients experiencing superficial (5 vs. 9) or deep (1 vs. 10) wound gapping. Notably, there were no statistically significant differences between the groups regarding paralytic ileus, deep vein thrombosis, vaginal bleeding, liver failure, stroke, fistula formation (ureteric, vesico-vaginal), incisional hernia, or late deep vein thrombosis Table 3 . Table 3. Postoperative data of the studied groups Group I Group II p -value ICU admission Yes 8 (20%) 5 (12.5%) 0.545 No 32 (80%) 35 (87.5%) Hospital stays Mean ± SD 11.9 ± 7.56 6.13 ± 3.35 < 0.001* Range 3–29 2–15 Gapping of wound No 20 (50%) 34 (85%) < 0.001* Superficial 9 (22.5%) 5 (12.5%) 0.378 Deep 10 (25%) 1 (2.5%) 0.006* Burst 1 (2.5%) 0 (0%) 1 Early complications (≤ 30 days) Ileus 8 (20%) 4 (10%) 0.274 DVT 1 (2.5%) 0 (0%) Vaginal bleeding 1 (2.5%) 0 (0%) No 30 (75%) 36 (90%) Late complications (> 30 days) Liver failure 1 (2.5%) 0 (0%) 0.389 Stroke 1 (2.5%) 1 (2.5%) Ureteric fistula 1 (2.5%) 0 (0%) VVF 1 (2.5%) 0 (0%) Incisional hernia 1 (2.5%) 2 (5%) DVT 0 (0%) 3 (7.5%) Urinary incontinence 0 (0%) 1 (2.5%) No 35 (87.5%) 33 (82.5%) Open in a new tab ICU, intensive care units; DVT, deep vein thrombosis; VVF, vesico vaginal fistula *significantly as P value ≤ 0.05 Analysis of disease recurrence and overall survival showed no significant differences between the groups. The median progression-free survival was similar for both groups (11.20 months in group 1 vs. 11.19 months in group 2), and the same was true for overall survival (11.69 months in group 1 vs. 11.76 months in group 2) Fig. 1 . Fig. 1. Open in a new tab Kaplan Meier A progression analysis B survival analysis of the studied groups Analysis of progression-free and overall survival revealed no significant differences between group’s 1A/2A and 1B/2B. The mean duration of progression-free survival was 10.875 months for group’s 1A/2A and 11.538 months for group’s 1B/2B. Similarly, the mean overall survival was 11.70 months and 11.775 months for group’s 1A/2A and 1B/2B, respectively Fig. 2 . Fig. 2. Open in a new tab Kaplan Meier A progression analysis B survival analysis of the patients in group 1A, 2A and 1B, 2B Discussion This study was conducted on 80 women aged ≥ 18 years with histologically confirmed advanced disease. To evaluates the effectiveness of primary CRS compared to NACT followed by interval cytoreduction. In our study; Group II achieved complete tumor resection (R0) more frequently, although the difference between groups wasn’t statistically significant. Notably, group II also experienced statistically significant reductions in surgical complexity, blood transfusions, operative time, hospital stay, and impaired wound healing. However, no statistically significant differences emerged between groups regarding intraoperative, early, late postoperative complications, side effects of chemotherapy, bevacizumab use, progression-free survival, or overall survival. In contrast, Machida et al. (2020), and Fagotti et al. (2020) reported a statistically significant difference in achieving R0 resection, with higher rates in their NACT groups [ 12 , 13 ]. The systematic review by Machida et al. (2020) encompassing 333 studies (including 4 RCTs) found a higher rate of R0 resection in the NACT group with a statistically significant difference. However, this study lacked details on patient comorbidities and surgeon type (gynecological oncologist vs. general gynecologist), potentially introducing heterogeneity due to varying surgical techniques across included studies [ 12 ]. Conversely, Fagotti et al. (2020) had a larger sample size (171 patients) but reported results more aligned with ours—a trend towards higher R0 rates in the NACT group without statistical significance [ 13 ]. Our study demonstrated a statistically significant decrease in surgical complexity scores and operative time in the group II compared to the primary surgery group I. These findings are consistent with Fagotti et al. (2020) and Machida et al. (2020), who also reported lower surgical complexity and shorter operative times in the NACT arm [ 12 , 13 ]. Prescott et al. (2023) reported no significant difference in surgical complexity between groups in their EORTC trial, which compared primary surgery and NACT [ 14 ]. Our study significantly reduced blood transfusions in the group II compared to group I. This finding is particularly relevant considering the potential drawbacks of blood transfusions highlighted by Prescott et al. (2023), such as increased perioperative morbidity without impacting survival [ 14 ]. Our study found no significant difference in intraoperative complication rates between the primary surgery and NACT groups. This aligns with findings from Fagotti et al. [ 13 ]. However, Ghirardi et al. (2020) reported a higher rate of intraoperative complications in the primary surgery group [ 15 ]. Notably, their retrospective study design and extended timeframe (potentially encompassing changes in surgical techniques and treatments) might contribute to these discrepant results. Regarding to the post-operative outcomes, our study demonstrated a statistically significant reduction in hospital stay for patients in the group II compared group I. This finding aligns with observations by Fagotti et al. (2020) and Ghirardi et al. (2020), who also reported shorter hospital stays following NACT [ 13 , 15 ]. Our study revealed a significantly lower incidence of impaired wound healing in group II compared to the group I. This aligns with findings by Machida et al. [ 12 ]. However, Fagotti et al. (2020) did not report on wound infection rates [ 13 ]. Our analysis revealed no significant difference in overall postoperative complication rates between the primary surgery and NACT groups. However, our results diverge from Fagotti et al. (2020) and Machida et al. (2020), who reported a statistically significant difference with higher complication rates in the primary surgery group [ 12 , 13 ]. Potential explanations for this discrepancy include their larger sample sizes and use of the Memorial Sloan Kettering Cancer Center surgical secondary events grading system, which might provide a more nuanced assessment of complications compared to our reporting of simple frequencies. Furthermore, our analysis revealed no statistically significant difference in progression-free survival or overall survival between group I and group II. This is consistent with Coleridge et al. (2021), who found little to no difference in time to death or disease progression between the two treatments approaches [ 16 , 17 ]. Similarly, Machida et al. (2020) reported that survival after NACT followed by interval debulking surgery (IDS) was not inferior to survival after primary surgery in women with advanced OV [ 12 ]. These findings support the notion that NACT does not negatively impact survival outcomes in this patient population [ 12 , 16 , 17 ]. Our analysis revealed no significant difference in PFS or OS between group I and group II. This aligns with findings reported by Machida et al. (2020) and Fagotti et al. (2020) [ 12 , 13 ]. Similarly, Park et al. (2020) observed comparable PFS with bevacizumab-containing NACT compared to conventional NACT [ 18 ]. Our study also found no significant difference in PFS or OS between patients receiving bevacizumab in the NACT regimen (groups IA and IIA) and those who did not (groups IB and IIB). It's important to acknowledge that three out of five deaths in group 1A were attributed to non-tumor progression causes, potentially influencing overall survival data. Regarding the contrasting results from Ghirardi et al. (2020), the retrospective nature of their study raises questions about generalizability. Our findings, along with the aforementioned studies, suggest no significant difference in PFS or OS between primary surgery and NACT in patients with advanced epithelial OV [ 15 ]. Conclusion This study demonstrates that optimal cytoreduction is more feasible with NACT, with less surgical complexity, shorter operative duration, less blood transfusion and short hospital stay. Supplementary Information Below is the link to the electronic supplementary material. Supplementary file1 (DOCX 86 KB) (86.4KB, docx) Acknowledgment We thank Mahmoud M. Ali, ITMO University, Saint Petersburg, Russia, for his invaluable contributions to drafting this manuscript (mahmoudali@niuitmo.ru). Declarations Conflict of interest The authors declare that they have no conflict of interest. Ethical Approval Research ethics committee approval was obtained (IRB no. 17200456) from Asyut University on 26 July 2020 Supplementary file 2. Informed Consent A written informed consent was obtained from each patient. Footnotes Hisham Abutaleb is a Obstetrics and Gynecology. Ali Hussien is a Obstetrics and Gynecology. Mohamed Khalaf is a Obstetrics and Gynecology. Dalia M. Badary is Clinical Pathology. Alaa M. Ismail is a Obstetrics and Gynecology. Sara Hassanein is a Diagnostic Radiology. Samy AlGizawy is a Clinical Oncology and Nuclear Medicine. SAM Moustafa is a Obstetrics and Gynecology. Rabab Mohmed Mumdouh Farghaly is a Medical Oncology and Hematological Malignancy. A. F. Abdel-Kawi is a Obstetrics and Gynecology. Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. References 1. Shih I-M, Wang Y, Wang T-L. The origin of ovarian cancer species and precancerous landscape. Am J Pathol. 2021;191(1):26–39. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] 2. Nasiri F, et al. CAR-T cell immunotherapy for ovarian cancer: hushing the silent killer. Front Immunol. 2023;14:1302307. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] 3. Nopour R. Screening ovarian cancer by using risk factors: machine learning assists. Biomed Eng Online. 2024;23(1):18. 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