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. 2011;4(3-4):117–122.

Laparoscopic Surgical Staging of Early Ovarian Cancer

Sarah Weber 1, Christopher K McCann 1, David M Boruta 1, John O Schorge 1, Whitfield B Growdon 1
PMCID: PMC3250973  PMID: 22229064

Abstract

Since its advent in the early 1990s, laparoscopic surgical staging for early ovarian cancer has been explored as an option with the potential to offer women equivalent cancer control and survival as provided by laparotomy but with the clear benefits of minimally invasive surgery. A limited but expanding body of literature suggests aggressive surgical staging can be performed with equivalent tissue assessment compared with laparotomy. Given the lack of randomized, controlled trials, the risks and benefits of such a procedure remain ambiguous. This review summarizes the current body of literature regarding the role of laparoscopy in upfront surgical staging of ovarian cancer. This review presents the history, rationale, and established benefits and risks of utilizing this approach in women who present with malignancy that appears confined to the ovary. Although retrospective data confirm the feasibility, safety, and efficacy of laparoscopic staging of early ovarian cancer, more prospective data will be required to confirm equivalent survival in a patient population that has the potential to be cured.

Key words: Ovarian cancer, Cancer staging, Laparoscopic surgical staging, Minimally invasive surgery

Ovarian cancer accounts for one-quarter of all malignancies of the female genital tract and is the most deadly of these malignancies.1 The current treatment paradigm involves upfront surgical debulking followed by adjuvant platinum-based chemotherapy to eradicate any disease that may have persisted.2,3 Despite initial response rates of 70% to 80%, the majority of women with ovarian cancer experience a recurrence of disease within 12 to 24 months.3 This high recurrence rate translates into 5-year survival rates of less than 50% for women with advanced disease.1 However, women with stage I ovarian cancers, in which disease is confined to the ovaries, have been observed to have 5-year survival rates of 85% to 90%.4–6 This marked difference in survival rates underscores the importance of comprehensive surgical staging because up to 35% of stage I diagnoses are upstaged after the discovery of microscopic metastatic disease.7 Complete surgical staging for early ovarian cancers has clear benefits for disease management and has been recommended by the International Federation of Obstetrics and Gynecology (FIGO).8,9

Surgical staging for ovarian cancer originally necessitated an exploratory laparotomy to perform the various procedures advised by FIGO: hysterectomy and salpingo-oophorectomy, pelvic and paraaortic lymph node dissections, omentectomy, peritoneal washings, and peritoneal biopsies.8,10 With the modernization of equipment and technique in the late 1980s and early 1990s, surgical pioneers began to use laparoscopic surgery for the treatment of gynecologic cancers with more regularity and success. In 1990, the first report of partial surgical staging of an early ovarian cancer appeared.11 By 1994, Querleu and LeBlanc had published the first report on laparoscopic surgical staging of nine early ovarian cancers.12

A decade and a half later, published studies on laparoscopic surgical staging of early ovarian cancer are small in size and relatively scarce. Questions still remain regarding its performance compared with a traditional laparotomy and its proper application to diverse populations of patients. This review examines the current research on surgical and oncologic outcomes after laparoscopic staging of early ovarian cancer, and provides an overview of the laparoscopic technique’s feasibility, benefits, possible risks, and future directions with the aim of standardizing and advancing its use in staging of early ovarian cancer.

Feasibility and Adequacy of Laparoscopic Surgical Staging

Retrospective, case-controlled studies suggest that laparoscopy is a reliable and accurate modality to assess for metastatic ovarian cancer. Chi and colleagues performed a case-controlled, retrospective comparison of staging via laparoscopy or laparotomy in 50 patients with early ovarian or fallopian tube cancer.13 They found no significant differences between the groups in number of lymph nodes removed or size of omentum resected, and reported no conversions to laparotomy. Park and colleagues performed a similar case-controlled, retrospective analysis of 52 surgeries.14 In addition to confirming the Chi findings, they reported no significant between-group differences in rates of upstaging and no recurrence of disease or death in either group at 20 months.14 Ghezzi and colleagues and Hua and coworkers also reported equivalent lymph node removal, upstaging rate, and no conversions to laparotomy in case-controlled, retrospective studies on a total of 55 early ovarian cancer patients.15,16 Finally, several retrospective reviews have reported that successful laparoscopic stagings of ovarian cancer were technically performed, the majority of which had previous oophorectomy demonstrating cancer.17–20 Although most of the literature suggests that laparoscopic staging takes significantly longer,13,15 some reports suggest equivalent if not shorter operative times.14 The preponderance of the available literature indicates that laparoscopic staging may take a longer time to complete, but is technically feasible and can provide equivalent surgical assessment when compared with laparotomy.21,22

Established Benefits of Laparoscopic Staging

Laparoscopic surgical staging of ovarian cancer offers a number of clearly defined benefits when compared with laparotomy. In endometrial cancer there is both randomized and retrospective literature that suggests that laparoscopic staging offers lower estimated blood loss (EBL), shorter hospital stay, and fewer postoperative complications with an improved quality of life and faster return of normal functioning.23–25 Although no randomized data exist for patients with ovarian cancer, the body of retrospective investigations suggests these benefits can be extrapolated to include patients undergoing comprehensive staging for early ovarian cancer.

Although limited, the retrospective literature examining staging for ovarian cancer confirms that the laparoscopic approach is associated with decreased EBL, shorter hospital stay, quicker return of bowel function, and shorter interval to adjuvant chemotherapy administration. In a case-controlled study of 21 early ovarian cancer cases, Hua and colleagues reported a significantly lower blood loss in laparoscopically staged patients (280 ± 156 mL) versus laparotomy patients (346 ± 170 mL).16 Three additional retrospective studies that analyzed a total of 138 early ovarian cancer patients collectively observed statistically significant less EBL in patients who underwent laparoscopic staging.13,14,26 Two of these reviews on 88 total patients found laparoscopy was associated with a 2.8% blood transfusion rate compared with 19.2%, the rate observed in those who underwent laparotomy.14,26

In addition to lower EBL, numerous reviews suggest patients staged laparoscopically exhibit a shorter latency to first bowel movement (BM), experience fewer postoperative complications, and require a shorter hospital stay. Most importantly, these patients began secondary treatment, such as chemotherapy, sooner than laparotomy patients. In a case-controlled study of 34 early ovarian cancer patients, Ghezzi and colleagues reported significantly shorter postoperative hospital stays (3 days vs 7 days; P < .05) and a smaller number of postoperative complications (2 vs 8 complications; P = .13) for patients staged by laparoscopy.15. Three retrospective studies that analyzed a total of 138 early ovarian cancer patients from 2000 to 2007 confirmed this association with significantly shorter hospital stays (2.6 vs 8 days; P < .05) and also observed a shorter latency to BM in patients who underwent laparoscopic staging. Of these 138 patients, 3.2% of laparoscopy patients and 30.5% of laparotomy patients experienced postoperative complications, including febrile morbidity, ileus, wound dehiscence, and wound infection.13,14,26

Among the patients (n = 88) in these studies for whom interval to adjuvant chemotherapy was reported,14,26 the interval was shorter in patients who underwent laparoscopic staging. Park and colleagues found a significantly (P < .05) shorter interval to chemotherapy in patients staged by laparoscopy (12.8 ± 4.9 days) than in patients staged by laparotomy (17.6 ± 8.3 days).14 A second series by the same group found a difference in interval to chemotherapy that did not reach significance: 11.1 ± 2.9 days for laparoscopy patients versus 14.1 ± 6.2 days for laparotomy patients (P = .14).26 Although the observed differences in interval to chemotherapy are small in magnitude, they confirm that a minimally invasive approach does not delay important adjuvant treatment, especially when surgery results in upstaging of disease, including cases of intraoperative tumor rupture or discovery of unresectable disease.

Potential Benefits of Laparoscopic Staging

Several potential benefits of laparoscopic staging for early ovarian cancer are currently supported by conflicting or anecdotal data in the literature. These potential benefits include a lower overall cost of treatment, higher patient and surgeon satisfaction, and improved fecundity after fertility-sparing staging procedures.

Laparoscopic staging may offer improved cost containment, both from a medical system and societal perspective. Several studies on laparoscopic surgical staging for endometrial cancer, a similar procedure to laparoscopic staging of early ovarian cancer, report lower overall hospital costs for laparoscopy compared with laparotomy.27,28 It is unclear whether patients return to work faster after laparoscopic ovarian cancer staging, especially if adjuvant chemotherapy is required. Further cost analyses on the laparoscopic management of early ovarian cancer are needed, but in general, laparoscopic techniques tend to decrease hospital stay, decrease complications, and improve patient postoperative performance status, all of which tend to increase hospital, patient, and societal cost-effectiveness.25

Numerous reviews indicate that systematic research is also needed to assess both patient and surgeon satisfaction with laparoscopic surgical staging.29,30 Anecdotal evidence suggests that the increased visibility and precision afforded by a laparoscopic approach, as well as shorter patient recovery time, provide more satisfactory outcomes for surgeons trained in the technique.30 Similarly, reduced postoperative pain, shorter recovery time, and more aesthetic results support the anecdotal existence of patient preference for laparoscopic staging when the procedure is available.29

Laparoscopic staging may offer reproductive benefits to premenopausal women seeking fertility preservation in the setting of a unilateral ovarian malignancy. Fertility sparing, or conservative laparoscopic staging, entails pelvic and para-aortic lymph node dissection, omentectomy, and unilateral salpingo-oophorectomy with the preservation of the uterus as well as the contralateral ovary and tube that do not appear to contain cancer. Muzii and colleagues conducted a prospective study of 27 unexpected ovarian cancer patients who underwent fertility-saving laparoscopic surgical staging. They reported two term pregnancies and two instances of spontaneous abortion after 20-month follow-up.31 Laparoscopic staging has been indicated as preferable to laparotomy for fertility-sparing surgeries due to the smaller number of adhesions caused by laparoscopy and avoidance of laparotomy, known to decrease fecundity.19,31 However, several studies have reported recurrence in patients who underwent a more conservative, fertility-sparing laparoscopic staging.17,19 More research is needed to determine whether laparoscopy affects the reproductive outcome and the oncologic safety of this deliberately incomplete staging in this specialized population.

Possible Risks of Laparoscopic Staging

The existence of port site metastasis, a higher incidence of intraoperative tumor rupture, and an unknown rate of disease recurrence all represent tangible risks associated with laparoscopic staging. Although these factors portend unresolved risk, the literature suggests that these risks may not outweigh the clearly established benefits in the setting of careful patient selection, preoperative assessment, and patient counseling.

Metastatic disease recurrence at laparoscopic port sites is a poorly understood phenomenon that is a known risk faced by all minimally invasive surgical oncologists.32–39 In gynecologic oncology, recent reports have suggested that this problem is quite rare, with a prevalence of 0% to 2% in patients with ovarian cancer staged by laparoscopy.40,41 This rate has been reported as higher (5%–20%), however, primarily in patients with ascites at the time of staging or patients with invasive, recurrent disease undergoing multiple laparoscopic procedures.30,41–43 Although no surgical technique has been demonstrated to lower the rate of port site metastasis, some authors advocate for layered closure of the trocar site as well as avoidance of tumor rupture.30,32,44,45 Most authors agree that the clear benefits of laparoscopic staging in the setting of cervical and endometrial cancer outweigh the remote risks posed by port site metastasis; however, prospective study of ovarian cancer staging will be required to better understand the true risk and prognostic implications.40

Experienced laparoscopists continually seek to avoid intraoperative rupture without tumor or cystic spillage. Inadvertent intraoperative tumor rupture results in immediate upstaging of disease to at least stage IC and may cause spread and peritoneal seeding of ovarian cancer cells necessitating adjuvant chemotherapy6 and possibly leading to worsened disease prognosis.46 Intraoperative rupture has been reported to occur in 12% to 20% of laparoscopic cases compared with 10% of those performed by laparotomy, suggesting that the rate of intraoperative rupture is higher in patients who have undergone laparoscopic ovarian cancer staging.14,15,47,48

Although most surgeons seek to remove ovarian tumors without cyst or tumor spillage by placing the ovarian tumor in a watertight plastic bag that can then be removed through a 10- to 15-mm port, the meaning of iatrogenic rupture of an ovarian cancer remains a source of controversy. One large retrospective review of 1545 patients with all stages of ovarian carcinoma confirmed that cystic rupture was associated with a decreased progression-free survival,49 although this cohort had a low percentage of comprehensively staged patients. Another retrospective review of 394 patients confirmed that tumor rupture had no impact on survival.50 However, in a smaller study of only comprehensively staged patients with stage I disease, inadvertent tumor rupture predicted worse outcomes in terms of disease recurrence and survival (hazard ratio [HR], 4.2), and this effect was augmented in patients who also had positive cytologic washings and/or surface involvement before tumor rupture.51 Other authors echo these concerns and advocate for strict avoidance of iatrogenic rupture.46 Larger tumor size has been associated with significantly more inadvertent tumor ruptures; a study of 263 tumors found a significant difference in size between tumors that were ruptured (7.6 ± 3.7 cm) and those that were not (6.5 ± 2.8 cm).48 Although no clear size cutoff has been established in the literature, some authors recommend laparoscopic staging be either avoided or conducted in concert with minilaparotomy in patients with large tumor size to lower the risk of intraoperative tumor rupture.41,48,51

Disease recurrence and overall survival present a serious concern associated with laparoscopic staging. Nezhat and colleagues reported a series of 20 ovarian and fallopian tube cancer patients who underwent laparoscopic staging and observed an 100% survival rate with no evidence of disease after close to 5 years of follow-up.17 These results are echoed by other case series of early ovarian cancer cases that report no recurrence or death in patients staged by laparoscopy at an approximate follow-up time of 2 years.14,15 In contrast, other reviews have found that disease recurrence was identified in two patients (11.8%) who underwent laparoscopic staging (n = 17) within 14 months of surgery, which included one mortality 22 months postsurgery compared with no recurrences in the laparotomy group (n = 19). No differences in progression-free and overall survival were observed.26 Tozzi and colleagues observed two disease recurrences (8.3%) among a cohort of patients staged by laparoscopy (n = 24) at a median follow-up of 46.4 months, but reported no deaths from disease.47 Finally, a prospective study by Ghezzi and colleagues of 26 patients staged by laparoscopy reports one recurrence (3.8% of patients) that resulted in death 12 months postsurgery.52

Preservation of the low recurrence rates and high overall survival observed for stage I ovarian cancers are of utmost importance when considering laparoscopic surgical staging of early ovarian cancer. Although retrospective evidence suggests recurrence rates after laparoscopic and open staging to be similar, further characterization via randomized, prospective clinical trials will be required to determine whether the surgical and oncologic outcomes are equivalent.

Fertility-sparing surgery that results in a deliberately incomplete staging poses a clinical challenge and may increase the risk of recurrence. Nezhat and colleagues reported on a cohort of patients (n = 11) who chose to have a laparoscopic fertility-sparing surgery. Nearly 28% of patients (n = 3) who underwent fertility-sparing staging experienced a recurrence of cancer in the remaining ovary. Despite the recurrence, interval resection prevented mortality in these patients after a mean follow-up time of nearly 5 years.17 It is unclear if this high recurrence rate can be attributed to the initial technique used or the inherent limitations of fertility-sparing staging.

Conclusions

Despite concerns regarding the ability to explore the full extent of peritoneal ovarian cancer cells, the literature confirms that laparoscopic surgical staging of early ovarian cancer is a feasible and adequate procedure associated with multiple established and potential benefits. Although concern still exists regarding recurrence and survival rates in patients staged by laparoscopy, most of the retrospective literature reports survival rates of approximately 90% at follow-up, rates similar to that observed in patients staged by laparotomy. Although prospective trials on laparoscopic staging of early ovarian cancer will be a challenge to conduct due to the low prevalence of ovary-confined ovarian cancers, this level of data will be required to understand how laparoscopy impacts cancer recurrence and mortality for this specialized population. Given these clear limitations, proper patient selection and counseling, in addition to careful surgical technique, remains the mainstay of successful laparoscopic staging.

Main Points.

  • Complete surgical staging for early ovarian cancers has clear benefits for disease management and has been recommended by the International Federation of Obstetrics and Gynecology.

  • Retrospective, case-controlled studies suggest that laparoscopy is a reliable and accurate modality to assess for metastatic ovarian cancer.

  • Laparoscopic surgical staging of ovarian cancer offers a number of clearly defined benefits when compared with laparotomy. Although limited, the retrospective literature examining staging for ovarian cancer confirms that the laparoscopic approach is associated with decreased estimated blood loss, shorter hospital stay, quicker return of bowel function, and shorter interval to adjuvant chemotherapy administration.

  • Several potential benefits of laparoscopic staging for early ovarian cancer are currently supported by conflicting or anecdotal data in the literature. These potential benefits include a lower overall cost of treatment, higher patient and surgeon satisfaction, and improved fecundity after fertility-sparing staging procedures.

  • The existence of port site metastasis, a higher incidence of intraoperative tumor rupture, and an unknown rate of disease recurrence all represent tangible risks associated with laparoscopic staging. Although these factors portend unresolved risk, the literature suggests that these risks may not outweigh the clearly established benefits in the setting of careful patient selection, preoperative assessment, and patient counseling.

  • Fertility-sparing surgery that results in a deliberately incomplete staging poses a clinical challenge and may increase the risk of recurrence.

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