This chapter should be cited as follows:
Tortorella L, Certelli C, et al., Glob Libr Women's Med
ISSN: 1756-2228; DOI 10.3843/GLOWM.420743
The Continuous Textbook of Women’s Medicine Series – Gynecology Module
Volume 8
Gynecological endoscopy
Volume Editors:
Professor Alberto Mattei, Director Maternal and Child Department, USL Toscana Centro, Italy
Dr Federica Perelli, Obstetrics and Gynecology Unit, Ospedale Santa Maria Annunziata, USL Toscana Centro, Florence, Italy
Chapter
Role of Laparoscopy in Ovarian Cancer
First published: March 2025
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INTRODUCTION
Ovarian cancer remains one of the most lethal gynecological malignancies, which is often diagnosed at an advanced stage due to its insidious onset and non-specific symptoms. Management of ovarian cancer involves a multidisciplinary approach, including surgery, chemotherapy and sometimes radiotherapy. Surgery for ovarian cancer has traditionally been open; however, in recent decades, laparoscopy has emerged as a pivotal technique, revolutionizing diagnostic, staging and therapeutic procedures. The minimally invasive approach provides significant benefits in terms of reduced morbidity, faster recovery and improved quality of life, making it an important option in the management of ovarian cancer.
EARLY-STAGE OVARIAN CANCER
Approximately one-third of patients with ovarian cancer are diagnosed with FIGO stage I–II.1 The standard treatment includes intensive surgical staging in order to establish a diagnosis, to remove the tumor and to assess the extent of the disease. The 10-year follow-up study by the European Organisation for Research and Treatment of Cancer on adjuvant chemotherapy in ovarian neoplasm (EORTC-ACTION) has demonstrated that complete surgical staging is associated with improved survival rates.2,3 Surgical procedures encompass hysterectomy, bilateral salpingo-oophorectomy, omentectomy, pelvic and para-aortic lymph node dissection, peritoneal biopsy and peritoneal washing. Unfortunately, patients with apparent early stages sometimes have microscopic disease in the upper abdomen or retroperitoneum. The upstaging rates reported in the literature vary from 4.5% to 38.5%,4 confirming the importance of complete surgical staging in early-stage ovarian cancers. Although the standard approach for surgical staging in ovarian cancer is laparotomy, the use of minimally invasive surgery (MIS) has become increasingly widespread in recent years, and even international ovarian cancer guidelines, both American and European, accept its use in selected patients in high-volume centers with experienced surgeons. Use of MIS has been widely reported by several studies in the literature, although the evidence is based on only case–control and retrospective cohort studies.5,6,7,8,9,10,11,12,13,14,15,16,17,18
In 2017, Melamed et al. compared overall survival in ovarian cancer patients in those who underwent MIS vs open surgical staging, with a median follow-up of 30 months.16 They showed no difference in the 4-year overall survival rates between MIS and laparotomy (91.5% vs 86.3%, respectively; hazard ratio 0.77, p = 0.13). In 2020, Facer et al. compared 1901 patients who underwent MIS staging of ovarian cancer (66.5% by laparoscopy and 33.5% robotic) and, in multivariable analyses, there were no significant differences in survival between patients treated with robotic-assisted laparoscopy and those treated with traditional laparoscopy, with a median follow-up of approximately 30 months; only 14.6% of patients had follow-up data for 5 years.13 In 2021, Gallotta et al. published data on oncological outcomes with a median follow-up of 61 months, which is one of the longest follow-up periods described for early-stage ovarian cancer patients treated by MIS.17 They showed 5-year overall survival, progression-free survival and disease-free survival rates of 84.0%, 92.5% and 93.8%, respectively. The recurrence rate was 15.3% and, interestingly, they showed a 38.5% recurrence rate after 24 months, highlighting the importance of a long follow-up period in this type of patient. More recently, Mokarram Dorri et al. compared laparoscopic and robotic surgery in the treatment of early-stage ovarian cancer, showing equivalent surgical and oncological outcomes over a mean follow-up period of 61 months.19 Table 1 shows the survival outcomes and follow-up duration for patients treated by MIS for early-stage ovarian cancer reported in the literature (Table 1).
1
Survival outcomes of minimally invasive management of early-stage ovarian cancer.
First author (year) | n | Upstaged (%) | Follow-up (months) | Recurrence (%) | Disease-free survival (%) | Overall survival (%) |
Leblanc (2004)20 | 42 | 19 | 54 | 7.1 | 90.5 | 97.6 |
Nezhat (2009)21 | 36 | 19.4 | 55.9 | 8.3 | 83.3 | 100 |
Ghezzi (2012)22 | 82 | 25.6 | 28.5 | 7.3 | 95.1 | 98.8 |
Brockbank (2013)7 | 35 | 23 | 18 | 5.7 | 94 | 100 |
Bogani (2014)23 | 35 | 43 | 64 | 11.4 | 89 | NR |
Koo (2014)15 | 24 | NR | 31 | 8.3 | 96.2 | 86.1 |
Chen (2015)24 | 65 | NR | LS 29.6 | NR | LS 95.2 | LS 100 |
Melamed (2017)16 | 1096 | 12.2 | 28.7 | NR | NR | 91.5 |
Minig (2016)25 | 50 | 24 | 26 | 12 | 98 | 98 |
Lu (2016)26 | 42 | 21.4 | 82 | 11.9 | NR | 92.9 |
Ditto (2017)27 | 50 | 20 | 49.5 | 14 | NR | NR |
Ye (2017)28 | 19 | NR | 24 | 0 | NR | NR |
Lee (2018)29 | 24 | 17.9 | 31.5 | 8.3 | 83 | 95 |
Facer (2020)13 | 1901 | LS 11.5 | LS 37.5 | NR | NR | NR |
Gallotta (2021)17 | 254 | 18.1 | 61 | 15.3 | 84 | 92.5 |
Mokarram Dorri (2024)19 | 140 | 19.2 | 60.7 | 20.7 | 79.3 | 88.6 |
Table adapted from Mokarram Dorri et al.19 LS, laparoscopy; RLS, robotic-assisted laparoscopy; NR, not reported.
However, despite the absence of robust scientific support regarding oncological outcomes of MIS in early-stage ovarian cancer, perioperative data are extremely favorable compared with the open approach. Among the advantages of laparoscopic and robotic surgery, authors reported less blood loss, shorter operation times, a lower rate of postoperative complications, a reduction in postoperative pain and shorter hospital stay, as well as esthetic advantages.5,15,18,30
Furthermore, laparoscopic and robotic surgery have played a role in sentinel lymph node mapping in early-stage ovarian cancer, which has been evaluated in a prospective multicenter study (SELLY).31 However, in this study, sentinel lymph node mapping through injection of indocyanine green in the ovarian vessels did not reach the expected sensitivity in identifying metastatic lymphatic disease. In fact, the final results showed that 1 in 4 patients had metastatic lymphatic disease that was unrecognized by sentinel lymph node biopsy.31
Although the advantages of MIS are easily understood, the pitfalls of this approach should be borne in mind. First, there is a risk of developing port-site metastasis, although this rate is actually very low, especially in early stages. One review showed a port-site metastasis rate of 0.18%,32 and in their meta-analysis on early-stage ovarian cancer treated by MIS, Park et al. reported just one case in 11 studies.33 The study by Gallotta et al., with its long follow-up period, reported just one case of port-site metastasis (0.4%).17 Taking precautions, such as the use of endobags, reduced manipulations of surgical specimens and controlled exsufflation, may minimize this risk. Second, there is a risk of tumor spillage. The capsule rupture rate reported in the literature varies between 11.4 and 30.3%,33 and seems to be associated with a lower overall survival and an increase in all-cause mortality compared with women with non-ruptured tumors.34 Recently, Ghirardi et al. analyzed preoperative or intraoperative patient and tumor characteristics associated with the risk of tumor spillage during MIS for early-stage ovarian cancer, and using multivariate analysis, showed that a larger tumor diameter (p < 0.001) and adhesions to ovarian fossa peritoneum (p = 0.007) were the only factors that were significantly associated with intraoperative cancer spillage.35 The tumor diameter plays an important role in selection of patients for the minimally invasive approach, as it is associated not only with risk of capsule rupture but also with risk of conversion to laparotomy. Another aspect to take into consideration is the extraction of the ovarian mass and the fact that its morcellation may alter the pathological evaluation, especially in a frozen-section setting.
A further important consideration is the adequacy of the surgical staging, which is difficult to evaluate because most publications did not report or only partially reported the surgical procedures performed.13,16 However, the studies in the literature did not show differences between laparotomy and MIS in terms of surgical procedures performed or upstaging rates.
These issues become even more relevant when considering the requests for fertility-sparing surgery for apparent early-stage ovarian cancer in young women who have not yet started or completed their family, which encompass unilateral salpingo-oophorectomy, omentectomy, pelvic and aortic nodal dissection and peritoneal biopsy. Fertility-sparing surgery necessarily implies incomplete staging, thus possibly translating into a higher risk of disease recurrence. However, survival and recurrence data reported in literature regarding laparoscopic and robotic fertility-sparing surgery are comparable with those for fully staged patients,36,37,38 and the advantages provided by MIS in terms of the higher likelihood of reducing adhesions, pelvic inflammation and functional anomalies that potentially impair fertility are of utmost importance in this subset of patients, with a reported pregnancy rate of approximately 60%.6
To summarize, in carefully selected patients with apparent early-stage ovarian cancer, the minimally invasive approach may be safely used in oncological centers by expert surgeons. However, patients should always be informed about the absence of randomized trials on this approach in ovarian cancer.
ADVANCED-STAGE DISEASE
The therapeutic options in advanced epithelial ovarian cancer include both surgery and chemotherapy. Cytoreductive surgery is still the cornerstone of treatment in ovarian cancer patients. For decades, we have known that there is an inverse relationship between residual disease and the patient prognosis, and complete resection is associated with the best survival. On the basis of preoperative and intraoperative evaluation, if resection of all macroscopic disease can be achieved with acceptable operative and postoperative morbidity, primary debulking surgery (PDS) is the mainstay of treatment in patients with advanced epithelial ovarian cancer. Surgery is then followed by platinum-based chemotherapy. However, if primary debulking surgery is not feasible due to the tumor spread and/or the performance status of the patient, neoadjuvant chemotherapy (NACT) followed by interval debulking surgery (IDS) must be considered. Many studies have shown that NACT/IDS is not inferior to primary debulking surgery in terms of survival, and is associated with fewer postoperative complications.39,40,41 The possibility of achieving complete resection is strictly linked to the extent of disease, and, in this context, laparoscopy has been included in international guidelines as an important tool to assess the tumor load in order to predict the likelihood of complete resection.42
Fagotti et al. developed the prognostic index value, a reliable score to assess the tumor load in a quantitative way to predict the chances of optimal cytoreduction.43,44 In the modified laparoscopy score, six parameters retained high predictive performance: omental cake, peritoneal extensive carcinomatosis, diaphragmatic confluent carcinomatosis, bowel infiltration, infiltration of the stomach and/or spleen and/or lesser omentum, and superficial liver metastases.45 Miliary carcinomatosis on the serosa of the small bowel (Figure 1a) and mesenteric retraction (Figure 1b) are considered as absolute criteria for unresectability, and so these two parameters were excluded from the updated version of the model.45 We give a score of 2 if the parameter is present and 0 if it is absent (Table 2). There is a low rate of inappropriate lack of explorations at a cut-off value of 10. This means that patients with a prognostic index value >10 may be referred for NACT without laparotomic exploration with a lower rate of postoperative complications and no delay in the start of chemotherapy.
|
|
(a)
(b)1
Miliary carcinomatosis on the serosa of the small bowel (a) and mesenteric retraction (b), which are considered as criteria for tumor unresectability.
2
Criteria for assigning scores to laparoscopic parameters.
| Score = 0 | Score = 2 |
Peritoneal carcinomatosis | Absence or carcinosis involving a limited area (e.g. along the paracolic gutter or the pelvic peritoneum) | Massive peritoneal involvement and/or a miliary pattern of distribution for parietal peritoneal carcinomatosis |
Diaphragmatic involvement | Absence or carcinosis involving a limited area | Widespread infiltrating carcinomatosis, and/or confluent nodules over most of the diaphragmatic surface |
Omental involvement | No tumor diffusion or isolated location | Tumor diffusion along the omentum up to the large stomach curvature |
Bowel infiltration | No bowel resection assumed | Possible large/small bowel resection (excluding rectosigmoid involvement) |
Stomach infiltration | No obvious neoplastic involvement of the gastric wall | Obvious neoplastic involvement of the stomach and/or lesser omentum and/or spleen |
Liver metastasis | No liver surface lesions | Liver surface lesions larger than 2 cm |
Primary debulking surgery is extensive surgery that is associated with a high rate of morbidity. Many attempts have been made to find predictors of complications. A nomogram for the prediction of complications showed how frailty affects both complications and survival.46 Frail patients were more likely to experience postoperative grade 3–4 complications or death within 90 days of surgery, were less likely to initiate chemotherapy within 42 days of surgery, and had a shorter overall survival than non-frail patients.
Vizzielli et al. developed a predictive score that utilized laparoscopic evaluation using the Fagotti score and performance status, ascites and CA 125 to predict early surgical complications.47 The aim was to evaluate, in a comprehensive way, the tumor load of the patient and the possibility of achieving complete resection compared with the risk of postoperative complications due to this extensive surgery. A model was provided and the risk of postoperative complication was considered acceptable if lower than 30%.
Thus laparoscopy may help not only in assessment of tumor load to predict the possibility of cytoreduction, but also in the decision of the surgeon to adopt tailored strategies on an individual basis.
INTERVAL DEBULKING SURGERY
Many studies have evaluated the role of MIS for performing IDS in carefully selected patients.48,49,50,51,52,53,54 Neoadjuvant chemotherapy followed by IDS has become an accepted therapeutic approach for patients with advanced epithelial ovarian cancer to reduce the disease burden and improve optimal cytoreduction. In the USA, the rate of IDS increased from 8.6% to 22.6% between 2004 and 2014, with increased use of MIS.55 Several studies have shown that MIS/IDS appears to be feasible and safe in terms of perioperative outcomes, psycho-oncological impact and survival rate in patients with a clinically complete response to NACT. In a phase-II multicenter study, the MISSION trial, Gueli Alletti et al. enrolled 30 patients who had a clinical complete response after NACT to undergo laparoscopic or robotic IDS, and observed seven recurrences after a median follow-up of 10.5 months.53 Thus this trial demonstrated the feasibility of use of MIS/IDS in advanced epithelial ovarian cancer patients, but confirmation using a higher number of patients with long-term follow-up is needed.
MIS shows several advantages in terms of perioperative complications, blood loss, hospital stay, postoperative pain and timing of NACT. The largest retrospective cohort study comparing MIS vs laparotomy for IDS showed that the main benefit of MIS was a shorter hospital stay.49 Furthermore, current evidence suggests that survival after MIS in selected patients with advanced epithelial ovarian cancer is not inferior to that in those operated on by laparotomy. In particular, Pereira et al. reported a 5-year overall survival that was 17.5% higher for MIS/IDS patients compared with laparotomy patients.55
Corrado et al. reported the findings of a retrospective analysis of 30 patients who underwent laparoscopic cytoreduction after three cycles of NACT, and concluded that MIS/IDS is feasible with good perioperative outcomes when performed by an experienced surgeon. The outcome of no residual disease was achieved for all patients.50 The median follow-up was 15 months (range 2–54 months), and no recurrence was found in 26 patients.
The ongoing LANCE trial aims to provide an assessment of the oncological safety of MIS after NACT.56 This is an international, randomized, multicenter, non-inferiority phase III trial to compare MIS vs laparotomy in women with advanced-stage high-grade epithelial ovarian cancer who had a complete or partial response to NACT and normalization of CA 125, with disease-free survival as the primary endpoint. The results of this trial may change the standard of care for carefully selected patients undergoing IDS after NACT if non-inferiority of MIS is demonstrated.
Robotic surgery is becoming increasingly central to MIS due to its shorter learning curve and aspects of its technology, which overcome a few disadvantages of standard laparoscopy. The advantages of robotic surgery compared to laparoscopy are multiple, and include elimination of surgeon tremor, 3D visualization, magnification of the view and full-wrist movement. Use of the robotic approach in advanced epithelial ovarian cancer patients in the IDS setting has been evaluated in various recent studies, confirming its oncological safety in selected patients.52,57,58,59
The main concern about MIS remains the challenging nature of abdominal exploration, particularly of the upper abdomen, which may lead to incorrect evaluation of the initial tumor burden and consequently of the residual disease. It is mandatory to have a holistic vision of the patient, which must take into account the whole disease history, from first diagnosis to the moment of surgery, and it is important to discuss with the patient the best therapeutic option in every clinical situation, according to the scientific evidence.
The literature data available may lead to varying conclusions about the role of MIS in the treatment of advanced epithelial ovarian cancer. The studies reported in the literature are mainly retrospective and are characterized by a generally low number of patients in each. Thus the results of the LANCE trial and other larger prospective trials are needed to better understand the role of MIS in advanced epithelial ovarian cancer, and in particular for IDS in terms of oncological outcome.
RECURRENCE
Recurrence in ovarian cancer occurs in around 70% of women within 5 years of diagnosis.60 and management of these patients represents a significant clinical challenge due to the heterogeneity of the recurrent disease, which is influenced by several factors, including the anatomical site of relapse, primary treatments, chemosensitivity, clinical characteristics of the patient and the biology of the tumor. Two randomized controlled trials (DESKTOP‑III and SOC‑1) showed an oncological advantage of surgery plus chemotherapy over chemotherapy alone in the treatment of platinum-sensitive recurrence.61,62 The recommendations of the ESGO-ESMO-ESP Consensus Conference on Ovarian Cancer presented at the ESGO Congress in 2022 concluded that ovarian cancer patients experiencing their first relapse more than 6 months after the end of first-line platinum-based chemotherapy should be assessed for eligibility for secondary cytoreductive surgery in a gynecological oncology center.63
In recent years, MIS techniques have been increasingly used in gynecological oncology practice because of the benefits reported in comparison to the open approach. The most relevant finding emerging from the results of randomized controlled trials of secondary cytoreductive surgery is that patients with complete resection have the most favorable outcome. For this reason, patient selection to identify optimal candidates for secondary cytoreductive surgery is crucial, especially if MIS is chosen. So far, there is no guidance defining the ideal candidate for minimally invasive secondary cytoreductive surgery, and no predictors of its feasibility are currently available. Therefore, the choice regarding use of the minimally invasive approach for secondary cytoreductive surgery is left to the surgeon’s discretion, but there are various factors to consider, such as age, clinical conditions, history (previous surgery or radiotherapy), body mass index, the patient’s ability to tolerate steep positions (Trendelenburg) and the presence of pneumoperitoneum. For these reasons, the anesthesiological evaluation plays an important role in the planning of surgery.64,65
In a recent analysis of 276 patients, comparing laparotomic and minimally invasive secondary cytoreduction, predictors of a successful minimally invasive approach were analyzed using uni- and multivariate analyses. In the multivariate analysis, single disease and oligometastatic disease at recurrence, NACT at primary diagnosis and lymph node site were confirmed to be independent predictors of the feasibility of minimally invasive secondary cytoreductive surgery.66 The study showed a surprisingly higher rate of NACT and IDS at first diagnosis (p = 0.030) in the MIS group. It is possible that patients undergoing NACT underwent less complex surgery, with consequently fewer adhesions and/or a different pattern of recurrence, making them potentially more amenable to a minimally invasive approach.
Given the increased complexity of management of recurrent ovarian cancer, the detection of recurrence and its distribution are crucial to identify the best therapeutic option. The precise description of recurrence sites, the potential involvement of adjacent organs, and possible anatomical variants may affect surgical planning in terms of possible technical difficulties and potential complications. Although PET-CT (positron emission tomography with computed tomography) showed better results than CT alone or MRI in detecting recurrent ovarian cancer,67 CT is usually the technique of choice in the follow-up of and surgical planning for patients with ovarian cancer because of the reproducibility of imaging for comparison and the excellent spatial resolution for the study of anatomy and relationships with adjacent structures. Furthermore, imaging may play a role even during surgery, providing a guide for precise detection of the site of recurrence. Mascilini et al. showed how use of intraoperative ultrasound helped to identify single relapses and achieve complete cytoreduction by MIS in approximately 25% of the cases, thus avoiding conversion to laparotomy.68 Thus, wide application of intraoperative ultrasound may offer a valuable contribution in complete surgical resection of recurrent disease. Unfortunately, preoperative imaging is less accurate in the detection of small foci of the recurrent tumor and miliary peritoneal involvement, with lower sensitivity than laparoscopy or surgical exploration. For this reason, laparoscopy still appears to be a good option in the final decision-making process, and has a favorable impact in terms of better visualization and improvement of adhesiolysis procedures, reducing the risk of unnecessary exploratory laparotomy.
Furthermore, MIS seems not to be inferior to laparotomy in terms of oncological outcomes. The rate of complete gross resection by minimally invasive secondary cytoreductive surgery is consistent across studies, ranging from 79% to 98%, with no differences reported between MIS and laparotomy.69,70,71,72,73,74 However, there are some criticisms to consider: few papers compared MIS and laparotomy in the treatment of recurrent ovarian cancer, and most of the studies reported on only a small number of selected cases of minimally invasive secondary cytoreductive surgery. As all the studies are retrospective, the choice of the approach used depended on the surgeon, and in recurrent disease there are a lot of variables to take into account, making homogeneous data evaluation difficult, and thus it is difficult to draw firm conclusions. Furthermore, MIS requires a high level of expertise and skills, especially in patients with recurrent cancer, and should be performed in high-volume oncological centers with adequate experience in advanced surgical procedures.75,76,77,78,79,80,81,82,83 Discussion of the management of recurrent lesions on an individual-patient basis in an interdisciplinary context is crucial to offer the best possible oncological and surgical approach.
FUTURE PERSPECTIVES
Targeted therapies and immunotherapies have emerged as novel treatment strategies for ovarian cancer, and obtaining more comprehensive information on the molecular characteristics of tumors represents a priority. Surgery contributes by enabling pathological and molecular characterization of the surgical specimen, allowing for a comprehensive study of the disease from diagnosis to possible biological modification during its natural history. Thus, it is conceivable that, in the future, a larger number of cases will benefit from integration of MIS and a multimodal therapeutic approach.
PRACTICE RECOMMENDATIONS
- Patients with apparent early-stage ovarian cancer may be treated by MIS for staging purposes in oncological centers by expert surgeons without affecting survival.
- Tumor dimensions and presence of adhesions should be evaluated to reduce the risk of capsule rupture.
- In advanced ovarian cancer, laparoscopy provides the diagnosis through minimally invasive biopsy and enables assessment of the tumor load in order to predict the likelihood of complete resection. Furthermore, laparoscopic scores may be a useful tool to predict the likelihood of postoperative complications.
- Minimally invasive surgery may also be therapeutic: for some carefully selected patients, interval debulking surgery may be safely performed using MIS.
- A comprehensive evaluation of the patient's clinical history and counseling based on current scientific evidence are mandatory to tailor treatment and optimize quality of life.
- Laparoscopy can be a valuable tool for identifying and obtaining histological confirmation of recurrent disease. In selected cases, single or oligometastatic disease may be treated using MIS in referral centers, without an apparent impact on prognosis.
CONFLICTS OF INTEREST
The author(s) of this chapter declare that they have no interests that conflict with the contents of the chapter.
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