One of the cornerstones of gynecologic cancer surgery is the assessment and removal of the retroperitoneal lymph nodes. Numerous reports have demonstrated that, when performed by highly skilled individuals, laparoscopic
ABSTRACT: One of the cornerstones of gynecologic cancer surgery is the assessment and removal of the retroperitoneal lymph nodes. Numerous reports have demonstrated that, when performed by highly skilled individuals, laparoscopic lymphadenectomies can be performed safely. This has led to the investigation of laparoscopy in the surgical staging and treatment of patients with ovarian, cervical, and endometrial cancers. This very promising approach has the potential to revolutionize numerous aspects of the management of gynecologic malignancies. However, it must be emphasized that the use of laparoscopy for gynecologic malignancies is still in its infancy. Studies that provide complication rates and long-term results are just beginning to be reported. More clinical data are necessary before the laparoscopic techniques are accepted as new surgical standards. Ongoing, prospective clinical trials will help answer many of the questions regarding the safety and efficacy of gynecologic laparoscopy. Until more data accumulate, operative laparoscopy will remain a promising, but unproven, tool in the management of patients with gynecologic malignancies. [ONCOLOGY 13(6):773-782, 1999]
As the end of the 20th century approaches, the surgical world will remember the 1990s as the decade during which the use of operative laparoscopy grew astronomically. Rapid technologic and surgical advances, combined with the desire to contain health care costs, have pushed the frontiers of endoscopic surgery beyond what was envisioned by even the most avid laparoscopists just a few short years ago.
With the development of special operative laparoscopic instruments and devices, operative gynecologic laparoscopy has evolved from simple tubal ligations to complex oncologic procedures. Over the past few years, there has been a steady increase in the number of reports describing the use of laparoscopy in patients with gynecologic malignancies. Moreover, in numerous institutions, operative laparoscopic techniques are now being routinely offered to patients with ovarian, cervical, or endometrial cancer.
However, it must be remembered that the use of laparoscopy for gynecologic malignancies is still in its infancy. Data are just now beginning to accrue regarding operative times, costs, the thoroughness of this minimal-access approach, its resultant complications, and patients’ long-term survival. Many of the techniques described are currently undergoing critical evaluation in prospective, multicenter clinical trials.
Until our experience grows and the data from these trials accumulate, many of the crucial questions regarding the safety and efficacy of the laparoscopic approach will remain unanswered. Therefore, although operative laparoscopy promises to be an effective tool, its exact role in the management of gynecologic malignancies has yet to be completely defined.
Historically, laparoscopy, or “peritoneoscopy,” was used for patients with ovarian cancer in one of two settings: (1) prior to the initiation of chemotherapy in patients whose initial laparotomy was felt to be inadequate; and (2) as a “second-look” procedure to determine whether patients had persistent disease after completing their primary chemotherapy. A more recent application is the surgical staging of apparent
early-stage disease done completely through the laparoscope. Overall, however, the majority of reports in the literature focus on the potential risks and benefits of the laparoscopic management of ovarian/adnexal masses.
In recent years, numerous authors have reported on the laparoscopic management of suspicious adnexal masses.[3,4] Laparoscopy enables the surgeon to make an accurate visual assessment of the mass and the other structures within the peritoneal cavity. The patient can then be triaged to the appropriate surgical management.
However, it must be emphasized that if an ovarian malignancy is the likely diagnosis, the patient is best served when the primary surgeon is a gynecologic oncologist. Although fewer than 3% of adnexal masses managed laparoscopically prove to be malignant, that possibility must always be kept in mind. Therefore, the surgeon who plans to evaluate an adnexal mass laparoscopically should do so in a setting in which accurate frozen-section diagnosis is available. In the event that an ovarian cancer is encountered, immediate conversion to laparotomy and surgical staging is indicated.
If there was no preoperative discussion with the patient regarding the course of action in the case of malignancy, or a surgeon experienced in ovarian cancer staging is unavailable, laparotomy is best postponed. Patients who do not undergo immediate conversion to a laparotomy should be referred expeditiously to a gynecologic oncologist so that laparotomy, surgical staging, and the initiation of definitive therapy are not delayed. Unfortunately, delays of up to 4 to 6 weeks appear to be the rule, rather than the exception.
Rupture of an early ovarian malignancy is another concern when the patient with an adnexal mass is managed laparoscopically. Compared with laparotomy, laparoscopic management of an adnexal mass poses an increased likelihood of intraoperative ovarian capsule rupture. If the mass contains a malignancy, the resultant tumor spillage into the peritoneal cavity is thought by some to worsen prognosis.
In addition, although the actual impact of intraoperative rupture on prognosis, independent of other factors, remains a controversial issue, in some patients it may be the single factor that determines the necessity for adjuvant chemotherapy. Therefore, when there is a strong suspicion that an ovarian mass is malignant, planned rupture with intraperitoneal tumor spillage should be avoided.
Bagley and coworkers were the first to describe the use of laparoscopy, or peritoneoscopy, in patients with ovarian cancer in 1973. Before beginning a chemotherapy protocol, 14 patients underwent peritoneoscopy 4 weeks after their initial laparotomy for ovarian cancer. Using a single port site and visualizing the peritoneal cavity directly through the scope, Bagley et al found diaphragmatic metastases in 11 patients. In seven of these patients, the diaphragmatic tumor represented the only site of metastatic disease.
Other early investigators subsequently confirmed that previously undetected metastases, particularly those located on the diaphragm, could be identified laparoscopically.[10,11]
In 1983, the Ovarian Cancer Study Group published the results of a prospective, multicenter, restaging study of 100 patients who had been referred to one of the member institutions with a diagnosis of “early” ovarian cancer. At surgical restaging, 31 (31%) patients were found to have a more advanced stage of disease than was initially reported. Sites of metastatic disease that originally went undetected included the omentum, diaphragm, and retroperitoneal lymph nodes.
Due to the numerous potential sites of occult metastatic disease, the International Federation of Gynecology and Obstetrics (FIGO) subsequently recommended that the surgical staging of
apparent early-stage ovarian cancer include an infracolic omentectomy, peritoneal washings, and multiple biopsies from the peritoneal surfaces and diaphragms, as well as pelvic and para-aortic lymph node biopsies. With the false-negative rate for peritoneoscopy reported to be as high as 60% when compared to laparotomy, it was clear that laparoscopic surgery before its “modernization” could not be used to adequately stage ovarian carcinoma.
In 1993, Querleu described the first complete laparoscopic surgical staging procedure for ovarian carcinoma. This report was later updated to include eight referred patients with adnexal carcinomas who underwent complete laparoscopic staging after inadequate initial surgical staging. In addition to multiple staging biopsies and pelvic lymphadenectomies, all eight patients underwent laparoscopic para-aortic lymph node sampling up to the level of the renal veins. The number of para-aortic lymph nodes obtained per patient ranged from 5 to 17. There were no complications, and the average hospital stay was 2.8 days.
Subsequently, other authors reported on small series of patients who underwent complete laparoscopic staging for apparent early-stage ovarian carcinoma. With essentially no long-term follow-up and fewer than 50 total patients in these reports, it remains unclear whether apparent early-stage ovarian cancer can be adequately staged laparoscopically. The obvious concern is the possibility of missing metastatic disease that could have been detected at laparotomy. If metastastic disease goes undetected, potentially curative postoperative therapy may be withheld.
Until more information is collected, laparotomy will remain the standard surgical approach for staging apparent early ovarian cancer, with laparoscopic staging reserved for clinical trials. The Gynecologic Oncology Group (GOG) is currently performing a prospective trial to evaluate the feasibility and adverse effects of laparoscopic staging of patients with incompletely staged ovarian carcinoma. The results of this study may help clarify the role of laparoscopy in early-stage disease.
The second-look operation is the most accurate method for assessing the disease status of patients who have undergone staging/cytoreductive surgery and primary chemotherapy for ovarian carcinoma. Traditionally, the operation is performed through a large midline vertical incision as a second-look laparotomy. Candidates for second-look surgery are those who had advanced-stage disease at the time of diagnosis and who have achieved an apparent clinical remission after completing their initial course of chemotherapy. The chances of detecting persistent disease at the time of second-look operation depend on multiple factors, but overall the probability is about 50%.
In 1981, Ozols and colleagues described their experience with second-look peritoneoscopy in 66 ovarian cancer patients. Persistent disease was detected laparoscopically in 33 (50%) of these patients. Consequently, they were spared from having a formal second-look laparotomy. A total of 22 patients with negative peritoneoscopies underwent immediate laparotomy, and residual ovarian cancer was detected in 12 patients (55%).
This 55% false-negative rate for peritoneoscopy when compared with laparotomy underscored the limitations of laparoscopy at that time, while also emphasizing the need for subsequent laparotomy in patients who appeared to be disease-free at laparoscopy. However, the 50% reduction in the need for laparotomy to diagnose persistent disease illustrated one of the significant benefits of the minimally invasive approach.
Two recent studies have compared “modern” laparoscopy with laparotomy in the second-look setting in patients with ovarian cancer.[18,19] Abu-Rustum and colleagues compared the results of 31 second-look
laparoscopies with 70 second-look laparotomies. Laparoscopy was associated with less blood loss, shorter operative times and hospital stays, and lower hospital charges per case. The only intraoperative and immediate postoperative complications occurred in patients who underwent laparotomy. With a median follow-up of 22 months, recurrence after a negative second-look operation was 14% for both groups. Casey et al analyzed 121 second-look procedures, and found essentially identical results as those of Abu-Rustum et al.
Second-look operations have contributed enormously to our understanding of the biological behavior of ovarian cancer and to the development of effective chemotherapy. However, critics of second-look procedures point out that there is no objective evidence that they have a major impact on survival. Despite this opposition, second-look surgery remains the gold standard in clinical protocols for determining the effectiveness of a specific treatment.
Outside of clinical trials, second-look operations should be undertaken only if the anticipated findings will alter subsequent management. Moreover, second-look laparoscopy should be attempted only by a surgeon with extensive experience and expertise in both advanced laparoscopic techniques and gynecologic oncology procedures.
The recommended FIGO staging system for cervical cancer is a clinical one. The role of surgery in primary management is reserved for the treatment of early-stage disease. Patients whose disease is confined to the cervix, with or without upper vaginal involvement, are often treated with a radical hysterectomy and bilateral pelvic lymphadenectomy. Patients who have more advanced disease generally receive radiation therapy with or without chemotherapy. Over the past few years, several authors have investigated the use of laparoscopy for both the treatment of early-stage disease and the surgical staging of advanced disease.
Two different laparoscopic approaches have been used in the treatment of early-stage cervical cancer. In the first approach, laparoscopy is used to perform a bilateral pelvic lymphadenectomy, transect the upper uterine attachments, and divide the uterine vessels. The procedure is completed vaginally using a modified version of the Schauta radical vaginal hysterectomy.
The second method involves the performance of a radical hysterectomy and bilateral pelvic lymphadenectomy almost completely through the laparoscope. Although the two approaches differ in many aspects, they both must be considered experimental, since neither method has been adequately studied, and only a few surgeons in the world are fully qualified to perform either one.
Laparoscopic-Assisted Radical Vaginal Hysterectomy-In 1991, Querleu and colleagues described their transperitoneal laparoscopic approach to pelvic lymphadenectomy in early-stage cervical cancer. They performed laparoscopic pelvic lymph node dissections in 39 patients. The dissection was limited to the area below the common iliac vessels, with a mean of 8.7 lymph nodes removed per patient. Subsequently, 33 patients underwent a laparotomy with radical hysterectomy and removal of all remaining lymph node tissue. No residual lymph node metastases were found.
With the apparent thoroughness of laparoscopic lymph node dissection, investigators then began combining laparoscopic lymphadenectomy with modifications of the Schauta radical vaginal hysterectomy for the treatment of early cervical cancer as an alternative to traditional radical abdominal hysterectomy with pelvic lymphadenectomy. However, even surgeons who have extensive experience with the Schauta technique do not perform the entire radical hysterectomy vaginally.
To date, over 250 cases of laparoscopic-assisted radical vaginal hysterectomy (LARVH) have been reported. In 1993, Dargent and colleagues presented not only one of the largest series of LARVH (51 cases) but also the one with the longest follow-up. They reported a 3-year actuarial survival rate of 95.5% for patients with node-negative, stage IB or IIA disease. Furthermore, no patient developed urinary tract fistulas or needed reoperation for complications.
Comparison of Radical Hysterectomy Approaches
The more limited American experience with LARVH differs somewhat from that of Dargent et al. This difference reflects the fact that the majority of gynecologic oncologists in the United States have never performed a radical vaginal hysterectomy. In the largest American series, Hatch et al reported a mean operative time of 225 minutes (Table 1). In their 37 cases, there were 2 bladder injuries, 2 ureterovaginal fistulas, and 1 large-bowel injury, for a major complication rate of 14%.
Thus, although LARVH seems to be feasible, and its successful completion appears to reduce blood loss, decrease febrile morbidity, and shorten hospital stays when compared to traditional abdominal radical hysterectomy, the relatively high major complication rate highlights many of the substantial questions that remain regarding the safety of the procedure (Table 1).
Laparoscopic Lymphadenectomy Plus Radical Vaginal Trachelectomy-Perhaps the most ingenious application of laparoscopy in the management of early cervical cancer was initiated by Dargent et al in 1987. In women who desired to maintain their fertility, they combined laparoscopic pelvic lymphadenectomy with radical vaginal trachelectomy (Table 1). By retaining the body of the uterus, these women preserved their reproductive function while theoretically receiving a satisfactory oncologic procedure.
Currently, a total of 62 such procedures have been reported in the world literature, and over a dozen healthy babies have been born from women who have undergone the procedure. Thus far, there have been only four documented recurrences.
The GOG recently closed a prospective trial evaluating laparoscopic lymphadenectomy in patients with early-stage cervical cancer. The 73 enrolled patients underwent immediate laparotomy after laparoscopic pelvic and para-aortic lymph node sampling. The results and conclusions of the trial are not yet available. Although this GOG study will not be able to address any issues related to the safety and efficacy of radical vaginal hysterectomy or radical vaginal trachelectomy, it may be the first step in answering some of the questions about the thoroughness and adverse effects of laparoscopic lymphadenectomy in these patients.
Laparoscopic Radical Hysterectomy was first described by Canis et al and Nezhat et al in 1992. These initial reports were criticized due to the length of the procedure (8 and 7 hours, respectively) and lymph node yield (10 and 14 pelvic nodes removed, respectively). More recent reports have demonstrated shorter operative times and higher lymph node yields.
Spirtos and colleagues recently presented the largest series of laparoscopic radical hysterectomy to date (Table 1). In this series, 43 patients underwent laparoscopic radical hysterectomy with aortic and pelvic lymphadenectomy. The average operating time was 225 minutes, with an average blood loss of 250 mL. The mean number of lymph nodes removed was 32 (range, 19 to 65). One patient suffered an intraoperative cystotomy, which was repaired laparoscopically, and another developed a postoperative ureterovaginal fistula, which required a reoperation. There has been one documented recurrence.
Although the English literature currently contains fewer than 100 reported cases of laparoscopic radical hysterectomy, the technique offers many potential advantages over LARVH. First, US gynecologic oncologists have much greater experience performing a traditional radical abdominal hysterectomy than a radical vaginal hysterectomy. Therefore, performance of a laparoscopic radical hysterectomy would require mastering the use of new surgical tools, rather than learning an entirely new, very difficult procedure.
Second, even for the most experienced vaginal surgeon, visualization of essential structures can be difficult during a radical vaginal hysterectomy. This problem should very rarely occur during a laparoscopic radical hysterectomy.
Finally, LARVH frequently requires perineal or vulvar incisions to facilitate the dissection. These quite painful incisions are avoided with the laparoscopic radical hysterectomy technique.
Table 1 compares the results of the largest recent series that employed the various approaches to radical hysterectomy.
As stated previously, the FIGO staging system for cervical cancer is a clinical one, and the standard management for patients who present with advanced disease does not include surgery for staging or treatment. However, over 30% of patients with advanced disease are inaccurately staged by clinical methods. For this reason, many investigators have studied the role of pretreatment surgical staging in these patients.
The pretreatment surgical staging of cervical cancer is based on its known pattern of lymphatic spread and, therefore, involves bilateral retroperitoneal lymph node assessment. The main proposed benefit of pretreatment staging is that it provides a more accurate definition of the extent of disease spread so that irradiation and/or chemotherapy can be better individualized.
The disadvantages relate to the morbidity associated with a major surgical procedure that gives information that will benefit fewer than 10% of patients undergoing the operation. Furthermore, a prolonged recovery period after pretreatment laparotomy can lead to significant delays in the initiation of definitive therapy.
Due to these disadvantages, the pretreatment surgical staging of patients with advanced cervical cancer remains a controversial issue. Adding to the controversy, many authors are now reporting the use of operative laparoscopy for pretreatment surgical staging. The purported advantage of the laparoscopic approach is that it provides the same delineation of the extent of disease as is achieved with laparotomy, but with less morbidity and essentially no delay in the initiation of definitive therapy.
One of the most significant problems with pretreatment laparotomy is the subsequent formation of intraabdominal adhesions that can lead to significant postirradiation enteric morbidity. This morbidity can be reduced if the laparotomy and lymphadenectomy are performed via an extraperitoneal, rather than a transperitoneal, approach. Although clinical studies have not compared adhesion formation after extraperitoneal laparotomy vs laparoscopic lymphadenectomy, animal studies have shown that the two techniques have the same incidence of adhesion formation.[37,38]
In 1992, Childers and colleagues reported the results of pretreatment laparoscopic staging in six patients with advanced cervical cancer. All of these patients had negative lymph nodes on preoperative computed tomography (CT) and underwent pelvic and para-aortic lymph node sampling. Two patients were found to have positive pelvic nodes, one of whom also had positive para-aortic nodes.
These 6 patients were part of a larger group of 18 patients with cervical cancer who underwent laparoscopic lymphadenectomy. The average number of lymph nodes removed laparoscopically in the whole group was 31, and there were no significant short-term complications.
Although this study by Childers et al demonstrated that laparoscopic pelvic lymphadenectomy was feasible and could be performed safely in patients with advanced cervical cancer, its clinical utility is debatable. Since most patients with advanced disease receive whole-pelvic radiotherapy, the status of their pelvic lymph nodes does not have any impact on their management. Therefore, most authors, including Childers and colleagues, currently sample only the high pelvic and low para-aortic lymph nodes that lie outside of the standard pelvic radiation field.[40,41] If these lymph nodes are found to be positive, the radiation field can be extended to include the para-aortic nodes and/or chemotherapy can be given.
The largest series of laparoscopic staging of advanced cervical cancer was recently reported by Chu and coworkers. Laparoscopic bilateral para-aortic lymph node dissections were performed in 28 patients. An average of eight nodes were removed per patient, and the average operation time was 95 minutes. The one complication (3.6%) was bleeding from the inferior vena cava, which required laparotomy for repair.
Ten patients (36%) had positive para-aortic nodes and were subsequently treated with extended-field radiation or chemotherapy and whole-pelvic irradiation. The patients with negative para-aortic nodes were given pelvic radiation alone. With a short mean follow-up of 18 months, only one patient has suffered a recurrence.
This series by Chu et al again demonstrates the feasibility of laparoscopic lymphadenectomy but also underscores the dearth of studies with large patient numbers and long-term follow-up. The GOG trial that is evaluating laparoscopic lymphadenectomy in women with early cervical cancer was originally proposed to also include laparoscopic staging for patients with advanced disease. However, the protocol was later amended to investigate only those patients with early-stage disease. Therefore, it is unlikely that the questions regarding the safety of preirrad-iation laparoscopic staging will be answered anytime in the foreseeable future.
The majority of women with endometrial cancer present with disease that is clinically confined to the uterus. Surgical removal of the uterus is the most important step in the treatment of these patients. However, over 20% of patients with endometrial cancer apparently confined to the uterus will be found to have disease outside the uterus at staging laparotomy. Therefore, the staging system recommended by FIGO is a surgical one that requires peritoneal washings, removal of the uterus and adnexae, and retroperitoneal lymph node sampling.
For patients with endometrial cancer, the status of the pelvic and para-aortic lymph nodes is the most significant piece of staging information that bears on future prognosis and further therapy. Although most of the original series of laparoscopic lymph node dissection described the use of the procedure in patients with cervical cancer, its greatest clinical utility may be in women with endometrial cancer.
By combining operative laparoscopy with simple vaginal hysterectomy, laparoscopic-assisted surgical staging (LASS) has been proposed as an alternative to laparotomy for patients with early endometrial cancer. With a LASS procedure, operative laparoscopy allows for the assessment of the peritoneal cavity, the ability to obtain peritoneal washings, and the guaranteed removal of the adnexae.
Most importantly, lymph node sampling can also be performed laparoscopically in indicated cases. (Indications vary depending on the institution but generally include those cases with high-grade tumors and/or tumor invasion to the outer half of the myometrium). The uterus, cervix, and attached adnexae are removed during the vaginal portion of the procedure as in a laparoscopic-assisted vaginal hysterectomy (LAVH) for benign disease.
Childers and colleagues published the first series of LASS procedures for endometrial cancer in 1993. A total of 59 patients with endometrial carcinoma clinically confined to the uterus underwent laparoscopic evaluation. Six patients were found to have intraperitoneal disease and did not undergo further laparoscopic staging.
Of the remaining 53 patients, 52 underwent an LAVH and 29 were considered candidates for laparoscopic lymph node sampling. The lymphadenectomy was performed successfully by laparoscopy in 93% of these patients. The estimated blood loss was less than 200 mL per patient, and the average hospital stay was 2.9 days.
Although this study demonstrated the feasibility of the LASS procedure and identified obesity as a limiting factor, the number of lymph nodes removed laparoscopically, the comparative costs of the procedure, and long-term follow-up were not discussed.
Many of these issues have been addressed recently. Gemignani and coworkers compared the clinical outcomes and hospital charges for 320 patients with endometrial cancer who were staged by laparoscopy vs traditional laparotomy. The patients managed laparoscopically had significantly fewer complications, shorter hospitalizations, and lower overall hospital charges than those who underwent laparotomy. Furthermore, there was no statistically significant difference in recurrence rates between the two groups.
An earlier series of 44 patients presented by Boike et al demonstrated similar findings, and reported no statistical difference in the total number of lymph nodes removed by laparoscopy compared to laparotomy.
The safety, efficacy, and cost savings of LASS are currently being evaluated in a prospective manner. The GOG is performing a randomized, phase III trial designed to compare the differences between LASS vs staging laparotomy in the management of women with early endometrial cancer. Variables that will be assessed include adequacy of staging, complications, operative time, hospital stay, total procedural costs, and quality of life.
A second application of operative laparoscopy is the staging of endometrial cancer patients who were incompletely staged initially. Gynecologic oncologists are frequently faced with the problem of recommending further management for a patient with endometrial cancer who had a hysterectomy but did not receive adequate surgical staging. Given this dilemma, the clinician has traditionally had one of three options: (1) recommend no adjuvant therapy, thereby risking potential undertreatment; (2) offer adjuvant therapy, risking possible overtreatment; or (3) perform a thorough staging laparotomy, subjecting the patient to its associated potential morbidity, mortality, and delayed adjuvant treatment.
Childers et al recently described a fourth option. They reported on a series of 13 patients with incompletely staged endometrial cancer who underwent laparoscopic staging. Extrauterine disease was found in three patients (23%), and an average of 17.5 lymph nodes were removed per patient. There were no introperative complications, the average estimated blood loss was less than 50 mL, and the mean hospital stay was 1.5 days. Although this small series does not confirm the value of laparoscopic staging, it does demonstrate that, in highly skilled hands, it can be completed safely and successfully.
The GOG is currently evaluating the feasibility and adverse effects of laparoscopic staging in patients with incompletely staged endometrial cancer. Pending the results of this trial, laparoscopic staging of patients with incompletely staged endometrial cancer should be performed only in an investigational setting.
Numerous technologic and surgical advances have led to the application of operative laparoscopic techniques in the management of patients with gynecologic cancers. Operative laparoscopy has been described in the surgical staging and treatment of patients with ovarian, cervical, and endometrial cancers. It appears to be a very promising approach with the potential to revolutionize numerous aspects of the management of gynecologic malignancies.
However, despite all of the enthusiasm for the use of laparoscopy for gynecologic malignancies, its potential is unconfirmed and its hazards are unknown. Reports regarding complications and long-term results are just now beginning to surface.[48,49] More clinical data are required before the minimally invasive techniques can be accepted as new surgical standards.
Ongoing, prospective clinical trials will help answer many of the questions regarding safety and efficacy of laparoscopic procedures. Until more data accumulate, operative laparoscopy will remain a promising, but unproven, tool in the management of patients with gynecologic malignancies.
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