In 1973, Bagley et al were the first to publish a report on the use of laparoscopy in patients with ovarian cancer.16 In 1983, the Ovarian Cancer Study Group described the results of a prospective, multicenter, restaging study of 100 patients with a diagnosis of early ovarian cancer.17 In 1994, Querleu and Leblanc reported the feasibility of complete laparoscopic surgical staging procedures for ovarian cancer.9 Since then several investigators from pioneering centers have reported small case series of comprehensive laparoscopic surgical staging of early stage ovarian cancer with limited follow-up periods. Thus far, however, only 5 studies have included a control group between the laparoscopic and laparotomy procedures10–13 (see Table 4). The use of laparoscopic staging procedures in patients with early ovarian cancer remains controversial.
The first controversial issue regarding laparoscopic surgery for the treatment of ovarian cancer is the accuracy of laparoscopic surgical staging. Among patients with surgical stage I ovarian cancer, those who have undergone comprehensive surgical staging have a lower risk of recurrence than do those who have not.18 It has been argued that laparoscopy does not allow for a thorough inspection of the pelvis, mesentery, and peritoneum leading to failure of upstaging and in adequate administration of chemotherapy.12 Alternative evaluations of the accuracy of comprehensive surgical staging can be inferred by comparing the rate of upstaging and lymph node yield between laparoscopic and laparotomic cases. A case-control series of 34 patients showed no difference in the lymph node yield between laparoscopy and laparotomy. Additionally, a meta-analysis of 3 comparative studies revealed no significant difference between the upstaging rates of laparoscopy and laparotomy.19 Likewise, in the present study, there were no significant differences in the upstaging rate or lymph node yield between the 2 groups.
The second controversial issue is the rate of tumor rupture between the laparoscopic and laparotomic approaches and the prognostic value of tumor rupture during surgery. In general, reported tumor rupture rates range from 11.4% to 30.3%.13,20–23 However, the risk of tumor rupture is not only limited to laparoscopic surgery, and some studies have reported that the risk of tumor rupture is similar between laparoscopic and laparotomic surgery. One previous study reported that the incidence of tumor rupture in patients with ovarian cancer was similar between the laparoscopy and laparotomy groups (10.5% versus 12.1%, respectively; P = 1.000).13 Other studies demonstrated that the rate of tumor rupture was 8% in both procedures.22,24 The clinical significance of tumor rupture during surgery remains uncertain. The largest study of cyst rupture was a retrospective, multicenter study involving >1500 patients. The study demonstrated that tumor rupture was an independent predictor of disease-free survival. In contrast, no difference in survival was noted in a retrospective review of 394 patients.25 However, these findings have not been confirmed in prospective studies. The prognostic value of intraoperative tumor rupture must be more clearly examined based on large-scale randomized controlled trials (RCTs) in patients with early ovarian cancer.19 All efforts should be made to reduce the incidence of tumor contamination of the abdominal cavity, including liberal use of a laparoscopic bag, controlled aspiration, and minimization of the risk of rupture.26 In the present study, thorough irrigation of the intraperitoneal cavity was performed using distilled water and cisplatin at the end of the surgical procedure, which may have reduced the negative impact of potential tumor rupture on recurrence and survival. Intraperitoneal administration of anticancer drugs has many pharmacokinetic advantages and induces high response rates in the abdomen because the “peritoneal plasma barrier” provides dose-intensive therapy.27,28
The third point of controversy is port-site metastasis. Large series of patients with malignant disease undergoing transperitoneal laparoscopy suggested that the incidence of port site implantation was <1%.29,30 Zivanovic et al reported that the port site recurrence rate of 1.96% following laparoscopy for ovarian, fallopian tube, or primary peritoneal cancer among 796 patients was comparable with the wound recurrence rate following laparotomy.31,32 Nezhat et al found that the rate of port-site metastasis in laparoscopic management of ovarian cancer was not higher than that in laparotomic management.33 The precise origin of port-site metastasis remains unclear. Several mechanisms of the development of port-site metastasis have been proposed. Among the most common are hematogenous spread, direct wound contamination and implantation, multiple effects of pneumoperitoneum, the effects of the gases used for insufflation, the “chimney effect,” aerosolization of tumor cells, local immune reactions, and the surgical technique used.30 We observed no port-site metastasis in the present study. We placed a pipe in the vaginal canal and removed the specimen from the pipe through the vaginal canal to avoid contact with the vaginal wall; the vaginal was then thoroughly irrigated before suturing.
The fourth point of controversy is the efficiency of laparoscopic staging compared with that of traditional laparotomic procedures. Standard survival outcomes must not be compromised for a procedure to be accepted as the standard treatment for early ovarian carcinoma. In agreement with this, we found no significant differences in survival analyses based on surgical management approaches. The overall and 5-year survival rates were 92.9% and 91.3% in the laparoscopy group and 90.0% and 88.4% in the laparotomy group. Ghezzi et al34 reported the largest study to date of laparoscopically managed early ovarian cancer. In their prospective study of 82 patients with a median follow-up time of 28.5 (range, 3–86) months, the overall and disease-free survival rates were 98.8% and 95.1%, respectively. These findings of similar survival outcomes between laparoscopic and laparotomic approaches could be the first step in accepting laparoscopy as the standard surgical approach for patients with early ovarian cancer. In the present study, the median follow-up period was 82 months in the laparoscopy and laparotomy group, respectively. To the best of our knowledge, our follow-up time is the longest among all published studies. Our survival rate is not as satisfactory as that in other studies, however, because all cases of recurrence and death occurred in the upstaging group. Excluding the upstaged patients, the overall and 5-year survival rates of patients with stage I disease were 100% in both the laparoscopy and laparotomy groups.
The fifth controversial issue is whether laparoscopic staging is actually minimally invasive. Our data indicate that both laparoscopic and laparotomic approaches are feasible in patients with early ovarian cancer but that laparoscopy may have more advantages than laparotomy with respect to operative blood loss and length of hospitalization. The optical magnification of laparoscopy provides an excellent view of the peritoneal surface, even better than direct visualization during laparotomy. However, a shortcoming of laparoscopic staging is the lack of tactile sensation. Therefore, some surgeons propose the use of hand-assisted laparoscopic surgery. Hand-assisted laparoscopic surgery is a unique surgical approach that combines traditional laparoscopy with the ability to place a hand intraperitoneally, thus retaining tactile sensation for the surgeon.35
The risk of bias in our series should not be overlooked. Only 19% of patients with a diagnosis of ovarian cancer are classified as having FIGO stage I disease. Stage I disease is usually diagnosed incidentally during laparoscopic or laparotomic surgery for benign-looking ovarian tumors. Therefore, prospective randomized studies have been difficult to conduct.
Our findings suggests that laparoscopic staging surgery of early ovarian cancer has an adequacy and accuracy similar to those of laparotomic staging surgery, with a similar long-term survival rate and significantly reduced hospital stay. A prospective multicenter randomized trial is required to more fully evaluate the overall oncologic outcomes.
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