Introduction
Traditional surgery for advanced ovarian cancer is typically performed via vertical midline laparotomy and includes total abdominal hysterectomy, bilateral salpingo-oophorectomy, peritoneal washings, omentectomy, lymphadenectomy, and metastasectomy. Complete cytoreduction often involves upper abdominal procedures such as splenectomy, liver wedge resection, and diaphragmatic stripping [
1,
2]. Recently, minimally invasive surgeries, including laparoscopy and robotic-assisted surgery, have gained popularity because of their comparable surgical outcomes and benefits, such as reduced blood loss, less postoperative pain, fewer wound complications, shorter hospital stays, and faster recovery [
3-
6]. Since the USA Food and Drug Administration approved the da Vinci Surgical System (model Xi; Intuitive Surgical Inc., Sunnyvale, CA, USA) for gynecologic procedures in 2005, the use of robotic surgery has become increasingly widespread [
7].
However, advanced ovarian cancer often necessitates extensive upper abdominal procedures, such as diaphragmatic peritonectomy, splenectomy, distal pancreatectomy, and liver resection, which rely heavily on laparotomy for optimal visualization and precise manual palpation [
8]. These challenges limit the feasibility of robotic cytoreductive surgery to selected patients [
7].
To address these limitations, we developed the hybrid approach for robotic and minimal open abdominal cytoreduction (HARMONY) technique, which integrates robotic-assisted pelvic and lower abdominal surgery with laparotomic upper abdominal cytoreduction. This novel approach aims to combine the precision of robotic surgery in the pelvis with the direct visualization and access afforded by laparotomy in the upper abdomen. Whether this integration confers advantages in postoperative recovery or functional outcomes, such as the preservation of lower abdominal muscle integrity or voiding and defecation functions, remains to be evaluated in prospective studies using validated instruments. This study aims to share our experience with this innovative hybrid technique and evaluate its feasibility and potential benefits in the treatment of advanced ovarian cancer.
Materials and methods
This retrospective cohort study included 20 patients with advanced ovarian cancer (2014 International Federation of Gynecology and Obstetrics [FIGO] stage III or IV) who underwent hybrid surgery between July 2023 and September 2024. Patients were not excluded based on histologic subtype, as selection for the hybrid approach was determined by the anticipated surgical complexity and disease distribution rather than tumor biology. Hybrid surgery was considered acceptable in the absence of severe adhesions or conglomerated tumors involving the bowel or posterior cul-de-sac. Patients anticipated to require bowel resection or presenting with diffuse peritoneal carcinomatosis were managed with full laparotomy, where-as those presumed to have early-stage disease underwent fully robotic staging surgery. Although patients anticipated to require planned bowel resection were directed toward full laparotomy, intraoperative findings of suspicious bowel involvement in two cases necessitated an unplanned sigmoid colectomy during the hybrid procedure. A fully robotic approach was not feasible in cases with extensive upper abdominal disease, such as large diaphragmatic, hepatic, or splenic implants, where adequate exposure and retraction could not be achieved robotically. In such cases, robotic pelvic cytoreduction was combined with an open upper abdominal procedure (hybrid approach) to facilitate complete tumor removal. In this study, the term hybrid surgery refers to a combined approach that integrates robotic-assisted pelvic cytoreduction with open upper abdominal surgery via a limited midline incision. This approach is not a fully minimally invasive procedure but rather a hybrid technique that incorporates the precision of robotic surgery in the pelvis with the direct visualization and access afforded by open surgery in the upper abdomen. The triage algorithm applied to all surgical candidates during the study period is shown in
Supplementary Fig. 1. Patient demographics, surgical procedures, and outcomes were retrospectively reviewed from medical records under the approval of the Institutional Review Board (IRB) of our institution (IRB No. NCC2024-0265). The requirement for informed consent was waived because of the retrospective nature of the study. However, written informed consent for publication of clinical images was separately obtained from the patient presented in
Fig. 1.
The demographic data included age, tumor histology, FIGO stage, timing of cytoreductive surgery, presence of ascites, American Society of Anesthesiologists physical status classification, preoperative cancer antigen-125 (CA-125) levels, and body mass index. For patients with high-grade serous carcinoma undergoing interval cytoreductive surgery after three cycles of neoadjuvant chemotherapy (NAC) with paclitaxel and carboplatin, the CA-125 elimination rate constant K (KELIM) score was calculated to assess chemotherapy response. A KELIM score <1 was considered indicative of low chemosensitivity, whereas a score ≥1 was associated with a more favorable prognosis [
9,
10]. In this study, KELIM was recorded as a descriptive baseline characteristic for patients undergoing interval surgery; no formal association analysis with surgical outcomes was performed given the limited sample size.
Robotic-assisted procedures were performed using the da Vinci Surgical System (model Xi; Intuitive Surgical Inc.). Patients were placed in the dorsal lithotomy position with both arms tucked. A multiport robotic approach was used, with one camera port at the umbilicus and three working ports placed bilaterally along the lateral abdominal wall. After completing the robotic surgery, the procedure transitioned to laparotomy for upper abdominal surgeries via an 8-10 cm incision above the umbilicus (
Figs. 1,
2).
Robotic cytoreductive surgery was performed for pelvic and lower abdominal procedures, including hysterectomy, salpingo-oophorectomy, pelvic/lower paraaortic lymphadenectomy, and peritonectomy of the bladder, cul-de-sac, rectum, and lower paracolic gutter. Upper abdominal procedures performed via laparotomy included upper para-aortic lymphadenectomy, omentectomy, splenectomy, distal pancreatectomy, liver resection, cholecystectomy, diaphragmatic peritonectomy, and cardiophrenic lymph node dissection. These procedures often required collaboration with hepatobiliary or thoracic surgical teams. The surgical specimen was extracted through the laparotomy incision and drains were placed through the trocar sites at the end of the procedure. Predefined criteria for intraoperative conversion to full laparotomy included unexpected extensive peritoneal spread, inability to achieve safe pelvic cytoreduction robotically, and intraoperative hemodynamic instability.
The assessed surgical outcomes included residual tumor status, operation time, estimated blood loss, number of intraoperatively transfused red blood cells, intraoperative events, length of hospital stay, time to Foley catheter removal and first bowel gas passage, postoperative complications, unplanned readmission within 30 days, and time to first adjuvant chemotherapy. Postoperative recovery was evaluated based on the need for additional pro re nata (PRN) pain relief.
Residual tumors were categorized as either no gross residual disease (R0) or residual tumors measuring <1 cm. Complete cytoreduction was defined as no gross residual disease, whereas a residual tumor measuring <1 cm was considered suboptimal cytoreduction. PRN pain relief requirements were classified according to the use of nonsteroidal anti-inflammatory drugs (NSAIDs), opioids, and extended patient-controlled analgesia (PCA) beyond 24 hours.
Results
Between July 2023 and September 2024, 452 patients underwent either robotic surgery or laparotomy for ovarian cancer at our institution. Among the 121 patients who underwent robotic surgery, 20 (16.5 [20/121]) underwent the hybrid surgical approach combining robotic-assisted pelvic and lower abdominal surgery with laparotomic upper abdominal cytoreductive surgery (
Supplementary Fig. 1). Patient demographics are summarized in
Table 1. The median age was 53 years (range, 40.0-68.0). Among the 20 patients, 15 (75.0%) were diagnosed with high-grade serous carcinoma, 2 (10.0%) with low-grade serous carcinoma, and 3 (15.0%) with other histologies, including adult granulosa cell tumor, poorly differentiated carcinoma with marked neutrophilic infiltration, and undifferentiated carcinoma.
Ten patients (50.0%) were diagnosed with FIGO stage III, whereas the remaining 10 (50.0%) had stage IV disease. Of these, 10 patients (50.0%) underwent upfront cytoreductive surgery and 10 (50.0%) underwent interval cytoreductive surgery. Ascites was present in nine patients (45.0%) and absent in 11 patients (55.0%). According to the American Society of Anesthesiologists physical status classification, 15 patients (75.0%) had a score of 2, three patients (15.0%) had a score of 1, and two patients (10%) had a score of 3. The median baseline serum CA-125 level was 200.5 (range, 38.0-2,855.0). Among patients undergoing interval cytoreductive surgery after three cycles of NAC, the median KELIM score was 1.45 (range, 0.58-1.8).
Table 2 outlines the surgical procedures performed during hybrid surgery. Robotic cytoreductive procedures included hysterectomy, salpingo-oophorectomy, pelvic/lower para-aortic lymphadenectomy, and peritonectomy. Laparotomic upper abdominal cytoreductive procedures included upper para-aortic lymphadenectomy, omentectomy, splenectomy, distal pancreatectomy, liver resection, cholecystectomy, diaphragmatic peritonectomy, and cardiophrenic lymph node dissection. Additional procedures included bowel resection, ureteral catheter placement, mediastinal pleurectomy, inguinal lymph node dissection, hilar lymph node excision following bronchovascular dissection via video-assisted thoracic surgery, and breast-conserving surgery for coexisting breast cancer. Bowel resection was performed in two patients, both involving segmental resection of the sigmoid colon. Extensive peritonectomies were performed in a significant number of patients, including those involving the diaphragmatic (65.0%), paracolic gutter (60.0%), and bladder (65.0%) sites (
Fig. 1D). Procedures requiring hepatobiliary surgeons included distal pancreatectomy (5.0%), liver resection (10.0%), and cholecystectomy (15.0%). Cardiophrenic lymph node dissection was primarily performed by thoracic surgeons (25.0%). At the end of the procedure, surgical drains were placed through the trocar sites used for the robotic approach.
Surgical outcomes are detailed in
Table 3. Complete cytoreduction with no gross residual disease was achieved in 19 patients (95.0%), with a median operation time of 342.5 minutes (range, 200.0-505.0). One patient (5.0%) had a 1-mm residual tumor on the bowel serosa. The median estimated blood loss was 300 mL (range, 5.0-1,500.0) and 16 patients (80.0%) did not require red blood cell transfusion. Two patients (10.0%) required 1 unit of red blood cells, whereas another 2 (10.0%) required 2 units. Intraoperative complications occurred in two patients (10.0%): one experienced a ureteral injury, which was managed with ureteral catheter placement, and the other a vessel injury, which was successfully treated with suturing. The median length of hospital stay was 8 days (range, 6.0-14.0). Foley catheter removal and first bowel gas passage occurred at a median of postoperative days 3.5 and 3.0, respectively. Postoperative complications within 30 days included ileus (10.0%), pleural effusion (10.0%), bowel perforation (5.0%), thromboembolism (5.0%), and wound complications (5.0%). Unplanned readmissions occurred in three patients (15.0%) within 30 days because of ileus, wound complications, and bowel perforation, respectively. Postoperative complications were classified according to the Clavien-Dindo system [
11]. Most complications were minor (grade I-II, 85%), with 2 grade IIIa (10.0%) and 1 grade IIIb (5.0%). No grade IV or V complications or perioperative mortality occurred, indicating that the hybrid approach was safely performed. Adjuvant chemotherapy was initiated at a median of 17 days after surgery (range, 10.0-36.0). Most patients (95.0%) required additional pain relief, with 95% using NSAIDs, 45% using opioids, and 15% requiring prolonged PCA use beyond 24 hours.
One case of a critical postoperative complication involving bowel perforation was observed. The patient, a 60-year-old woman with FIGO stage III ovarian cancer, underwent hysterectomy, bilateral salpingo-oophorectomy, lymphadenectomy, omentectomy, appendectomy, unilateral ureteral catheter placement, and segmental resection of the sigmoid colon with anastomosis for suspicious metastasis. She was discharged after a 7-day hospitalization and received her first cycle of adjuvant chemotherapy on postoperative day 24. On postoperative day 32, she presented to the emergency department with abdominal pain. A pelvic computed tomography (CT) scan revealed increased pneumoperitoneum, indicative of bowel perforation. She underwent emergency surgery, which revealed significant fecal impaction and perforation beneath the previous anastomosis site. The bowel perforation occurred at the anastomotic site following sigmoid colectomy performed during the laparotomic component of the procedure and was not directly attributable to the robotic pelvic phase. Low anterior resection with temporary ileostomy formation was performed. Subsequent adjuvant chemotherapy was resumed 20 days after the emergency surgery, with a delay of 7 days from the planned schedule. This case highlights the importance of close postoperative monitoring, particularly in patients undergoing extensive procedures, such as bowel resection with anastomosis.
Discussion
This study demonstrated the feasibility and safety of a novel hybrid surgical approach that combines robotic-assisted pelvic and lower abdominal surgery with laparotomic upper abdominal cytoreduction for advanced ovarian cancer. Achieving complete cytoreduction with no visible residual tumor is a critical prognostic factor in ovarian cancer [
12]. In this study, complete cytoreduction was achieved in 95% of cases, with one patient having a residual tumor <1 cm on the bowel serosa. Extensive upper abdominal procedures, such as diaphragmatic peritonectomy, splenectomy, and liver resection, were successfully performed using the hybrid approach in collaboration with hepatobiliary and thoracic surgeons. These findings demonstrate the technical feasibility of the hybrid approach in achieving R0 resection across a range of disease extents. However, R0 status alone does not establish oncologic equivalence to conventional open cytoreductive surgery, and in the absence of survival and recurrence data, these results should be interpreted strictly as evidence of perioperative feasibility rather than oncologic adequacy.
The intraoperative complication rate was 10% and all complications were managed effectively. Postoperative complications within 30 days occurred in 25% of patients, including 1 case of bowel perforation requiring reoperation. This complication underscores the importance of close postoperative monitoring, particularly after bowel resection and anastomosis. Despite these challenges, the unplanned readmission rate (15.0%) and overall complication rates are consistent with those reported in previous studies, which report rates between 5.0% and 14.0% for laparoscopic cytoreductive surgery [
13,
14]. Foley catheter was removed at a median of 3.5 days postoperatively and bowel movement resumed at a median of 3 days. These perioperative outcomes are presented descriptively, as no concurrent comparator group was available in this study. Direct comparison with conventional laparotomy or fully minimally invasive surgery was not feasible given the retrospective design and the inherent selection differences between surgical approaches. Nevertheless, contextual comparison with published data suggests broadly similar perioperative profiles. In the enhanced recovery after surgery pathway cohort reported by Reuter et al. [
15], median hospital stay following open cytoreductive surgery was 9 days, complication rate was approximately 30%, and time to adjuvant chemotherapy was 21 days, consistent with the outcomes observed in the present series (hospital stay, 8 days; complication rate, 25%; time to adjuvant chemotherapy, 17 days). These comparisons should be interpreted with caution, as patient selection, disease extent, and institutional expertise differ substantially across studies. The absence of a matched control group remains a primary limitation of this study.
The laparoscopic cytoreduction after neoadjuvant chemotherapy (LANCE) trial is an international, prospective, randomized, multicenter, non-inferiority phase III study comparing minimally invasive surgery with traditional laparotomy in patients with advanced ovarian cancer [
16,
17]. The primary inclusion criteria were complete or partial response to three or four cycles of NAC and normalization of CA-125 levels, with disease-free survival as the primary endpoint. Preliminary findings suggest comparable complete cytoreduction rates and support the feasibility of minimally invasive approaches in selected patients. In this study, eight of 10 patients who underwent interval surgery had favorable KELIM scores (>1), and seven of these achieved R0 resection. While this observation is consistent with the known association between chemosensitivity and surgical outcome, the small sample size precludes any formal inference. KELIM data are reported here as descriptive baseline context and whether the KELIM score may inform patient selection for the hybrid approach warrants prospective evaluation in larger dedicated cohorts.
A study by Carbajal-Mamani et al. [
1] supports the feasibility and safety of robotic-assisted interval cytoreductive surgery, reporting optimal cytoreduction in all 12 patients, with low blood loss and short hospital stays. Notably, their study included two robotic cases with supraumbilical laparotomy for upper abdominal procedures, highlighting the potential of a hybrid approach in complex cases requiring extensive cytoreduction.
This study aligns with these findings, demonstrating that the hybrid technique is a viable option for achieving complete cytoreduction while minimizing the morbidity associated with traditional open surgery. The hybrid approach allows delicate tissue manipulation and precise dissection using robotic systems in the lower abdomen while enabling manual palpation and comprehensive exploration via laparotomy in the upper abdomen. This combination enhances surgical precision and expands the applicability of minimally invasive techniques to cases requiring extensive cytoreduction.
Formal patient selection criteria for the HARMONY technique have not yet been established in the literature. Based on our institutional experience and existing evidence for minimally invasive cytoreductive surgery, we suggest that suitable candidates share the following features: absence of diffuse peritoneal carcinomatosis or severe pelvic adhesions on preoperative imaging, upper abdominal disease of limited extent manageable through a small laparotomy incision, and favorable chemotherapy response based on post-NAC CT imaging and KELIM score in the interval surgery setting. The LANCE randomized trial demonstrated that patients with a complete or partial response to NAC and normalized CA-125 levels achieved comparable cytoreductive outcomes with minimally invasive versus open surgery [
16,
17], providing indirect support for these selection principles. Similarly, Ackroyd et al. [
14] and Carbajal-Mamani et al. [
1] identified the absence of extensive upper abdominal disease and favorable chemotherapy response as key determinants of the feasibility of minimally invasive interval cytoreduction, with the latter series explicitly including hybrid cases with supraumbilical laparotomy. Prospective studies using predefined selection algorithms are required to formally validate these criteria for the hybrid approach.
Despite these promising results, this study has limitations. First, the most critical limitation is the absence of survival and recurrence data. Given the short study period (July 2023-September 2024), progression-free and overall survival outcomes were not evaluable at the time of this report. Oncologic adequacy cannot be assumed based on R0 status alone and the 95% R0 rate reported in this study should not be interpreted as evidence of oncologic equivalence to conventional open cytoreductive surgery. Long-term follow-up in larger prospective series is essential to determine whether the HARMONY technique achieves oncologic outcomes comparable to those of standard surgical care. Second, this study did not assess whether the HARMONY technique confers advantages in postoperative voiding or defecation function through preservation of lower abdominal muscle integrity. Future prospective studies with long-term follow-up and standardized functional assessments are necessary to confirm the potential benefits of the hybrid approach. Third, the hybrid approach was applied under stringent selection criteria, and a comparative analysis with full laparotomy or fully robotic surgery groups was not feasible because of the retrospective design and heterogeneous disease extent. The peritoneal carcinomatosis index (PCI) was not prospectively documented during the study period, which represents a major limitation in interpreting the reported R0 rate of 95%. Retrospective reconstruction of PCI from operative notes and imaging findings was not feasible to a reliable standard. Instead, the distribution of involved disease sites was extracted from operative records and preoperative imaging for all 20 patients and is presented in
Supplementary Table 1. All 20 patients had pelvic peritoneal involvement, 17 (85.0%) had paracolic gutter disease, 13 (65.0%) had diaphragmatic involvement, and 12 (60.0%) had perihepatic or liver surface disease. Bowel serosal disease was documented in three patients (15.0%), of whom two required unplanned sigmoid colectomy. Although this site-based characterization provides descriptive context, it is a qualitative surrogate for validated tumor burden quantification, and the high R0 rate must be interpreted within the context of the stringent patient selection criteria applied. Fourth, the small sample size of 20 patients limits generalizability and the retrospective design introduces potential selection bias. Approximately half of patients received NAC, with KELIM scores ranging from 0.58 to 1.8, reflecting variable chemosensitivity. However, because of the limited sample size and heterogeneity in disease extent, subgroup analyses stratified by NAC status and KELIM score were not feasible. Therefore, further studies with larger cohorts are warranted. Additionally, the hybrid approach requires highly specialized surgical expertise, multidisciplinary collaboration, and advanced robotic equipment, which may not be universally accessible. The hybrid technique also presents logistical challenges, such as the need for coordination between robotic and open surgical teams. Moreover, the associated learning curve for robotic systems and hybrid procedures highlights the importance of specialized training and experience in optimizing outcomes. Finally, the cohort was histologically heterogeneous, including 15 patients (75.0%) with high-grade serous carcinoma and five patients (25.0%) with other subtypes: low-grade serous carcinoma (n=2), adult granulosa cell tumor (n=1), poorly differentiated carcinoma with marked neutrophilic infiltration (n=1), and undifferentiated carcinoma (n=1). These tumors differ substantially in their biology, patterns of peritoneal spread, and response to NAC. Although histologic subtype did not influence surgical eligibility in this feasibility study, it precludes generalization of oncologic observations across the cohort. Future studies evaluating the HARMONY technique should focus on histologically homogeneous populations, preferably restricted to high-grade serous carcinoma.
Despite these limitations, the hybrid approach achieved comprehensive cytoreduction comparable to that of open surgery in terms of completeness and morbidity. These results suggest that the hybrid technique can serve as a feasible and effective option for selected patients with advanced ovarian cancer, particularly those who require extensive cytoreduction. Incorporation of minimally invasive components in cytoreductive surgery may be appropriate in carefully chosen cases, provided that oncologic safety and technical feasibility can be maintained. Further prospective studies with larger cohorts and comparative analyses with conventional laparotomy are necessary to validate these findings and establish guidelines for integrating hybrid techniques into standard surgical practice.
In conclusion, this study highlights the feasibility and potential advantages of a hybrid surgical approach that combines robotic-assisted pelvic and lower abdominal procedures with laparotomic upper abdominal cytoreduction. This technique achieved satisfactory cytoreductive outcomes with acceptable morbidity in a carefully selected cohort. Whether this approach represents a viable alternative to conventional laparotomy in terms of long-term oncologic outcomes remains to be established in future prospective studies with adequate follow-up. Future research should focus on refining patient selection criteria, evaluating long-term outcomes, and exploring the impact on quality of life and recurrence rates to better define the role of hybrid approaches in ovarian cancer surgery.