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.
Management of the Ovarian/Adnexal Mass
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.
Staging of Apparent Early-Stage Disease
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.
1. Montz FJ, Schlaerth JB: Laparoscopic surgery: Does it have a role
in the management of gynecologic malignancies? Clin Obstet Gynecol
2. Childers JM, Nasseri A: Minimal access surgery in gynecologic
cancer: We can, but should we? Curr Opin Obstet Gynecol 7:57-62, 1995.
3. Chi DS, Curtin JP, Barakat RR: Laparoscopic management of adnexal
masses in women with a history of nongynecologic malignancy. Obstet
Gynecol 86:964-968, 1995.
4. Childers JM, Nasseri A, Surwit EA: Laparoscopic management of
suspicious adnexal masses. Am J Obstet Gynecol 175:1451-1459, 1996.
5. Curtin JP: Management of the adnexal mass. Gynecol Oncol
6. McGowan L, Lesher LP, Norris HJ, et al: Misstaging of ovarian
cancer. Obstet Gynecol 65:568-572, 1985.
7. Maiman M, Seltzer V, Boyce J: Laparoscopic excision of ovarian
neoplasms subsequently found to be malignant. Obstet Gynecol
8. Rubin SC, Wong GYC, Curtin JP, et al: Platinum-based chemotherapy
of high-risk stage I epithelial ovarian cancer following
comprehensive surgical staging. Obstet Gynecol 82:143-147, 1993.
9. Bagley CM, Young RC, Schein PS, et al: Ovarian carcinoma
metastatic to the diaphragm—frequently undiagnosed at
laparotomy. Am J Obstet Gynecol 116:397-400, 1973.
10. Rosenoff SH, Young RC, Anderson T, et al: Peritoneoscopy: A
valuable staging tool in ovarian carcinoma. Ann Intern Med 83:37-41, 1975.
11. Piver MS, Barlow JJ, Lele SB: Incidence of subclinical metastasis
in stage I and II ovarian carcinoma. Obstet Gynecol 52:100-104, 1978.
12. Young RC, Decker DG, Wharton JT, et al: Staging laparotomy in
early ovarian cancer. JAMA 250:3072-3076, 1983.
13. Staging announcement: FIGO Cancer Committee. Gynecol Oncol
14. Querleu D: Laparoscopic para-aortic node sampling in gynecologic
oncology: A preliminary experience. Gynecol Oncol 49:24-29, 1993.
15. Querleu D, LeBlanc E: Laparoscopic infrarenal para-aortic lymph
node dissection for restaging of carcinoma of the ovary or fallopian
tube. Cancer 73:1467-1471, 1994.
16. Possover M, Krause N, Plaul K, et al: Laparoscopic para-aortic
and pelvic lymphadenectomy: Experience with 150 patients and review
of the literature. Gynecol Oncol 71:19-28, 1998.
17. Ozols RF, Fisher RI, Anderson T, et al: Peritoneoscopy in the
management of ovarian cancer. Am J Obstet Gynecol 140:611-619, 1981.
18. Abu-Rustum NR, Barakat RR, Siegel PL, et al: Second-look
operation for epithelial ovarian cancer: Laparoscopy or laparotomy?
Obstet Gynecol 88:549-553, 1996.
19. Casey AC, Farias-Eisner R, Pisani AL, et al: What is the role of
reassessment laparoscopy in the management of gynecologic cancers in
1995? Gynecol Oncol 60:454-461, 1996.
20. Creasman WT: Second-look laparotomy in ovarian cancer. Gynecol
Oncol 55 (suppl):122-127, 1994.
21. National Institutes of Health Consensus Development Conference
Statement: Ovarian cancer: Screening, treatment, and follow-up: April
5-7, 1994. Gynecol Oncol 55(suppl):4-11, 1994.
22. Fleming ID, Cooper JS, Henson DE, et al: Cervix uteri, in Fleming
ID, Cooper JS, Henson DE, et al (eds): AJCC Cancer Staging Manual,
5th ed, pp 189-194. Philadelphia, Lippincott-Raven, 1997.
23. Querleu D, Leblanc E, Castelain B: Laparoscopic pelvic
lymphadenectomy in the staging of early carcinoma of the cervix. Am J
Obstet Gynecol 164:579-581, 1991.
24. Dargent D: Laparoscopic surgery and gynecologic cancer. Curr Opin
Obstet Gynecol 5:294-300, 1993.
25. Chi DS, Curtin JP: Gynecologic cancer and laparoscopy. Obstet
Gynecol Clin North Am, 1999 (in press).
26. Dargent D, Roy M, Keita N, et al: The Schauta Operation: Its
place in the management of cervical cancer in 1993 (abstract).
Gynecol Oncol 49:109, 1993.
27. Hatch K, Hallum A, Nour M, et al: Comparison of radical abdominal
hysterectomy with laparoscopic assisted radical vaginal hysterectomy
for treatment of early cervical cancer (abstract). Gynecol Oncol
28. Possover M, Krause N, Schneider A: Identification of the ureter
and dissection of the bladder pillar in laparoscopic-assisted radical
vaginal hysterectomy. Obstet Gynecol 91:139-143, 1998.
29. Averette HE, Nguyen HN, Donato DM, et al: Radical hysterectomy
for invasive cervical cancer: A 25-year prospective experience with
the Miami technique. Cancer 71:1422-1437, 1993.
30. Dargent D, Brun JL, Roy M, et al: Pregnancies following radical
trachelectomy for invasive cervical cancer (abstract). Gynecol Oncol
31. Plante M, Roy M: Radical trachelectomy. Operative Techniques in
Gynecologic Surgery 2:187-199, 1997.
32. Canis M, Mage G, Wattiez A, et al: Vaginally assisted
laparoscopic radical hysterectomy. J Gynecol Surg 8:103-105, 1992.
33. Nezhat CR, Burrell MO, Nezhat FR, et al: Laparoscopic radical
hysterectomy with paraaortic and pelvic node dissection. Am J Obstet
Gynecol 166:864-865, 1992.
34. Spirtos NM, Ballon SC, Perez GM, et al: Laparoscopic radical
hysterectomy (type III) with aortic and pelvic lymphadenectomy:
Surgical morbidity and short-term follow-up. Gynecol Oncol 68:106, 1998.
35. Potish RA, Twiggs LB, Okagaki T, et al: Therapeutic implications
of the natural history of advanced cervical cancer as defined by
pretreatment surgical staging. Cancer 56:956-960, 1985.
36. Weiser EB, Bundy BN, Hoskins WJ, et al: Extraperitoneal vs
transperitoneal selective para-aortic lymphadenectomy in the
pretreatment surgical staging of advanced cervical carcinoma (a
Gynecologic Oncology Group study). Gynecol Oncol 33:283-289, 1989.
37. Fowler JM, Hartenbach EM, Reynolds HT, et al: Pelvic adhesion
formation after pelvic lymphadenectomy: Comparison between
transperitoneal laparoscopy and extraperitoneal laparotomy in a
porcine model. Gynecol Oncol 55:25-28, 1994.
38. Lanvin D, Elhage A, Henry B, et al: Accuracy and safety of
laparoscopic lymphadenectomy: An experimental prospective randomized
study. Gynecol Oncol 67:83-87, 1997.
39. Childers JM, Hatch K, Surwit EA: The role of laparoscopic
lymphadenectomy in the management of cervical carcinoma. Gynecol
Oncol 47:38-43, 1992.
40. Childers JM, Hatch KD, Tran AN, et al: Laparoscopic para-aortic
lymphadenectomy in gynecologic malignancies. Obstet Gynecol
41. Chu KK, Chang SD, Chen FP, et al: Laparoscopic surgical staging
in cervical cancer—preliminary experience among Chinese. Gynecol
Oncol 64:49-53, 1997.
42. Creasman WT, Morrow CP, Bundy BN, et al: Surgical pathologic
spread patterns of endometrial cancer: A Gynecologic Oncology Group
study. Cancer 60:2035-2041, 1987.
43. International Federation of Gynecology and Obstetrics: Annual
report on the treatment of gynecologic cancer. Int J Gynecol Obstet
44. Childers JM, Brzechffa PR, Hatch KD, et al: Laparoscopically
assisted surgical staging (LASS) of endometrial cancer. Gynecol Oncol
45. Gemignani M, Curtin JP, Barakat RR, et al: Laparoscopic-assisted
vaginal hysterectomy (LAVH) vs total abdominal hysterectomy (TAH) for
endometrial adenocarcinoma: A comparison of clinical outcomes and
hospital charges. Gynecol Oncol, 1999 (in press).
46. Boike G, Lurain J, Burke J: A comparison of laparoscopic
management of endometrial cancer with traditional laparotomy
(abstract). Gynecol Oncol 52:105, 1994.
47. Childers JM, Spirtos NM, Brainard P, et al: Laparoscopic staging
of the patient with incompletely staged early adenocarcinoma of the
endometrium. Obstet Gynecol 83:597-600, 1994.
48. Montz FJ: Complications of gynecologic oncology laparoscopic
surgery. Operative Techniques in Gynecologic Surgery 2:219-229, 1997.
49. Abu-Rustum N, Barakat RR, Curtin JP: Laparoscopic complications
in gynecologic surgery for benign or malignant disease. Gynecol Oncol