Laparoscopy and Oncology: Where Do We Stand Today?

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Ann. N.Y. Acad. Sci. 997: 282–291 (2003). © 2003 New York Academy of Sciences.doi: 10.1196/annals.1290.032

Laparoscopy and Oncology:Where Do We Stand Today?

THEODOROS D. THEODORIDIS AND JOHN N. BONTIS

First Department of Obstetrics and Gynaecology,Aristotle University of Thessaloniki, Hippokration Hospital,546 42, Thessalonoki, Greece

ABSTRACT: The clinical application of laparoscopic surgery has grown rapidlyover the last few years. Since the first documentations of laparoscopic lym-phadenectomy, many reports highlight the use of modern laparoscopy in thefield of gynecologic oncology. Laparoscopic treatment of early-stage cervicaland endometrial cancer, and laparoscopic evaluation and staging of cervical,ovarian, and endometrial carcinomas, are feasible procedures. The place ofminimal-access surgery in the arsenal of gynecologic oncological surgery hasbeen established, especially after the recent developments and practical appli-cation of video laparoscopy, novel instrumentation, and advanced surgicaltechniques. Although operative laparoscopy in gynecologic oncology is still inits infancy the potentiality of the procedure is underscored. Many patients maybenefit from the treatment or staging of gynecologic malignancies with laparo-scopic means. Literature reports highlight that laparoscopy may be an effectiveprocedure with lower morbidity and complication rates than traditional ab-dominal surgery. The short hospital stay and recovery time have a positive im-pact in a cancer patient’s quality of life, as they return to normal activitiesrapidly. Many risks, though, may arise from the application of minimal-accesssurgery in cancer patients, and many questions regarding safety and efficacyneed answers, based on prospective clinical trials. We must emphasize thatsuch studies with large patient numbers and long-term follow-up are lacking.Until results from these trials are available, laparoscopic oncologic proceduresshould be performed only in an investigational setting by expert teams.

KEYWORDS: laparoscopy; oncology; gynecological cancer; malignancy

INTRODUCTION

The clinical application of laparoscopic surgery has grown rapidly over the lastfew years. Since the first documentations of laparoscopic lymphadenectomy, manyreports highlight the use of modern laparoscopy in the field of gynecologic oncolo-gy. Laparoscopic treatment of early-stage cervical and endometrial cancer, and lap-aroscopic evaluation and staging of cervical, ovarian, and endometrial carcinomasare feasible procedures. The place of minimal-access surgery in the arsenal of gyne-

Address for correspondence: Theodoros D. Theodoridis, M.D., 8, Agias Theodoras Street, 64623, Thessaloniki, Greece. Voice/fax: +30-2310-240333.

[email protected]

283THEODORIDIS & BONTIS: LAPAROSCOPY & ONCOLOGY

cologic oncological surgery has been established, especially after the recent devel-opments and practical application of video laparoscopy, novel instrumentation, andadvanced surgical techniques. Although operative laparoscopy in gynecologic on-cology is still in its infancy, the potentiality of the procedure is underscored. Manyrisks may also arise from the application of minimal-access surgery in cancer pa-tients, and many questions regarding safety and efficacy need answers based on pro-spective clinical trials.

LAPAROSCOPY AND CERVICAL CANCER

Laparoscopic Management of Early-Stage Cervical Cancer

Cervical cancer is staged clinically and surgery is applied in management of theearly stages of the disease. During the last few years reports regarding laparoscopicinput in surgical treatment of early-stage cervical cancer, or in surgical staging, havebeen published. Dargent1 described his experience in combining laparoscopic retro-peritoneal pelvic lymphadenectomy with radical hysterectomy in patients with earlycervical cancer. Querleu and coworkers2 pioneered a transperitoneal approach to thesampling of pelvic lymph nodes. Dargent et al.,3 in a retrospective study, confirmedthe feasibility of the left extraperitoneal route for systematic para-aortic lym-phadenectomy in patients with cervical cancer. After the initial reports gynecologiconcologists have begun combining laparoscopic lymphadenectomy with modifica-tions of the Schauta radical vaginal hysterectomy instead of performing radical ab-dominal hysterectomy and lymphadenectomy for the treatment of early cervicalcancer.

A learning curve was associated with the laparoscopic lymphadenectomy inmany reports. A clear improvement in yield was evident as surgeons gained experi-ence with the technique. The procedure has an acceptable safety profile with lowmorbidity and complication rate.4,5 In a retrospective study, Malur et al.6 comparedlaparoscopic-assisted radical vaginal hysterectomy (LARVH) and radical abdominalhysterectomy (RAH) for treatment of patients with cervical cancer. In the LARVHgroup, significantly more pelvic lymph nodes were removed by laparoscopy (27 vs.10.7), blood loss was less, and hospital stays were shorter.

Recently, the Gynecologic Oncology Group (GOG) completed a prospective clin-ical trial evaluating laparoscopic lymphadenectomy in women with early-stage cer-vical cancer.7 The patients have undergone immediate laparotomy after laparoscopictransperitoneal pelvic and para-aortic lymphadenectomy. The objectives of thisstudy were to obtain information on the adverse effects and difficulties associatedwith laparoscopic lymph-node removal and to determine the adequacy of the lymph-node removal. Four methods were used to determine the adequacy of node sampling.All cases of para-aortic lymphadenectomy were judged adequate by all four methodsof evaluation, and the procedure appears to be reasonably safe and feasible. Six casesof pelvic lymphadenectomy were judged incomplete at laparotomy, a fact that dem-onstrates problems regarding adequacy that are propably correctable.

Cervical carcinoma frequently occurs in young women who would like to pre-serve their childbearing potential. For the management of these patients (stage IA1,IA2, IB, and IIB), Dargent et al.8 performed a combination of vaginal radical trache-

284 ANNALS NEW YORK ACADEMY OF SCIENCES

lectomy and laparoscopic pelvic lymphadenectomy. In their personal series, 82 caseswere gathered and 3 recurrences reported. There were 47 registered pregnancies, 35of which went on after the fourteenth week and 27 finished with the birth of a livingbaby.9 Although radical trachelectomy carries a relative risk of late miscarriage, itmakes it possible for some patients with early-stage cervical cancer to become preg-nant and deliver a normal new-born. Thus it seems reasonable to offer this procedurein selected cases.8,10

In 1992, Canis et al.11 and Nezhat et al.12 described a complete laparoscopic rad-ical hysterectomy. Their patients benefited from short hospital stays; however, theoperatation times were long. Recent reports demonstrated shorter operatation timesand higher lymph-node yields. The largest series to date was reported by Spirtos etal.13 Seventy-eight patients underwent laparoscopic radical hysterectomy and retro-peritoneal lymphadenectomy. The average operation time was 225 minutes (range:150–430 min) and the average blood loss 225 mL (range: 50–700 mL). The averagelymph-node count was 34 (range: 19–68) and 5.1% (4 cases) presented with arecurrence.

Laparoscopic Management of Advanced-Stage Cervical Cancer

Lymph-node biopsy remains the only reliable method of appraising the pelviclymph-node status. Noninvasive methods of lymphatic exploration only moderatelyagree with the pathological results,14 and more than 30% of the patients of advanceddisease cases will be inaccurately staged by clinical methods.15 The information ob-tained from the surgical staging of cervical cancer allows individualization of ther-apy, which may improve the overall clinical outcome.14,16 Goff et al.14 reported thatsurgical staging of women with cervical cancer resulted in modification of the stan-dard pelvic radiation field for 43% of patients. The disadvantages of laparotomicsurgical procedure relate to the morbidity associated with a major surgical proce-dure, the prolonged recovery time after pretreatment laparotomy, and significant de-lays in the initiation of definite therapy. The procedure may lead to adhesionformation with a higher incidence of postirradiation enteric morbidity. Surgical stag-ing by laparoscopy was proposed to avoid some of these complications.17,18

Childers et al.17 pioneered the laparoscopic procedure in patients with advancedcervical cancer (stage IIb or greater) and negative nodes on preoperative CT scan-ning. No significant short-term complications were reported. In another study Pos-sover et al.19 reported that the sensitivity and specificity of laparoscopic evaluationfor identifying positive para-aortic and pelvic lymph nodes was 92.3% and that acombination of laparoscopic evaluation and frozen section helped to correctly diag-nose all patients with involved lymph nodes. In 15.4% of cases the laparoscopic eval-uation and frozen section changed primary therapy. Vergote et al.20 published astudy on a series of 38 patients with IB2–IIIB cervical carcinoma without suspiciousnodes on CT scanning that underwent laparoscopic lower para-aortic lymphadenec-tomy. Metastatic disease was present in 18% of these patients, who therefore weretreated with extended field para-aortic radiotherapy. Although few reports in the lit-erature have shown the feasibility of laparoscopic staging in advanced cervical can-cer, studies with large patient numbers and long-term follow-up are lacking.Prospective clinical trials are needed to justify the safety of preirradiation laparo-scopic staging in patients with advanced cervical carcinoma.


LAPAROSCOPY AND ENDOMETRIAL CANCER

FIGO recommended that the staging system of endometrial cancer should be sur-gical rather than clinical, as studies performed by the GOG emphasized that morethan 20% of patients with endometrial cancer clinically confined to the uterus willbe found to have disease outside the uterus at staging laparotomy.21 The surgicalstaging for endometrial cancer includes intraperitoneal exploration, peritoneal wash-ings for cytological examination, total hysterectomy and bilateral salpingo-oophorectomy, and pelvic and para-aortic lymph-node sampling. Oncologists indi-vidualize their recommendations for adjuvant treatment (i.e., chemotherapy or ra-diotherapy) on the information obtained from the surgical staging.22–24

Laparoscopy became an attractive option not only for the cancer patients whoseuterine corpus had not yet been removed, but also for those who had hysterectomywithout proper surgical staging at the time of the initially procedure. The combina-tion of laparoscopically assisted vaginal hysterectomy (LAVH) and laparoscopicallyassisted surgical staging (LASS) has been proposed as an alternative to laparotomyfor women with early-stage carcinoma of the uterus. Childers et al.25 reported thefirst series of 59 women with clinical stage I endometrial carcinoma that underwentLASS and LAVH. The lymphadenectomy was performed successfully by laparosco-py in 93% of these patients. This series clearly demonstrated that metastatic diseasecan be discovered at the same rate one would expect if laparotomy were used. Met-astatic disease was present in 14% of patients when all grades were considered, andin 36% of patients when just grades 2 and 3 were considered. The estimated bloodloss reported was less than 200 mL, and the overall average hospital stay was 2.9days, including the patients with complications.

Although obesity was the most significant limitation in this series, other authorsclearly stated that obesity is not a contraindication in the laparoscopic managementof endometrial cancer.26–29 Eltabbakh and coworkers26 conducted a prospectivestudy applying laparoscopic surgery to women with clinical stage I endometrial can-cer and BMI’s between 28 and 60 who can tolerate such surgery. Women with thesame characteristics who underwent laparotomy for stage I endometrial cancer wereused as the control group. Laparoscopic surgery was successful in 88.1% of all obesewomen. Compared to the control group, they had significantly longer operative time(194.8 vs. 137.7 min), more pelvic lymph nodes removed (11.3 vs. 5.3), a smallerdrop in postoperative hematocrit (3.9 vs. 5.4), and shorter hospitalization stays (2.5vs. 5.6 days).

Laparoscopy is generally associated with short hospital stays, and this was report-ed for women operated on laparoscopically for endometrial cancer.27–31 Comparinghospitalization times after laparoscopy or laparotomy for the management of en-dometrial cancer, Holub et al.31 reported that the mean postoperative stay was 3.9days for the laparoscopy group and 7.3 days for the laparotomy group, Manolitsasand McCarney27 stated that the hospital stay was 4.3 vs. 8.5 days, while the findingsof both Langebrekke et al.29 and Boike et al.32 were similar (4.3 vs. 6.2 and 2.4 vs.5.0 days, respectively). Rapid postoperative recovery and early discharge seem to bethe most astonishing outcomes of laparoscopic surgery, as patients return to theirnormal activities sooner and experience a great impact on the quality of their lives.

The literature reports no significant difference in the number of lymph nodes re-moved by laparoscopy and laparotomy.30,32–34 The issues of recurrence and survival


after laparoscopic management of endometrial cancer have been addressed and Ma-grina et al.,35 in a retrospective review, reported 3-year recurrence and 3-year cause-specific survival rates similar to those of the traditional abdominal approach. Com-plications may also occur during laparoscopic procedures for treatment of endome-trial cancer; in all the studies reported in the literature, the patients managedlaparoscopically had significantly fewer complications than patients who underwentlaparotomy.25,27,29–31,34

LASS is a feasible, safe, and adequate procedure that offers remarkably shorthospital stays and recovery times for patients with endometrial cancer. A learningcurve is demonstrated in the laparoscopic management of these women. As sur-geons’ experience increases, there is a significant decrease in the operating time andincrease in the number of pelvic lymph nodes removed.36,37 Laparoscopic staging inpatients with incompletely staged endometrial cancer was also proposed,38 althoughboth the feasibility and the adverse effects of this procedure need evaluation.

LAPAROSCOPY AND OVARIAN CANCER

Diagnosis and Staging by Laparoscopy

Laparoscopic surgery has become the gold standard in the treatment of benign ad-nexal masses, whereas exploratory laparotomy remains the standard treatment ofmalignant tumors.39 Several authors have questioned the place for laparoscopy intreatment of ovarian cancer.40,41 Reich et al.42 reported for the first time the laparo-scopic treatment of ovarian cancer with a complete staging system. Laparoscopy,which still is one of the most controversial problems facing the gynecologist today,permits accurate visual assessment of the mass, followed by appropriate triage intofurther management.43 When an adnexal mass is present, there should be no absolutelimitation to the decision to perform either laparoscopy or laparotomy.44 When ma-lignancy is unexpectedly encountered, the primary issue is the appropriate manage-ment of the patient and not the method of surgery.45 Unfortunately, malignantmasses of the ovaries are often mismanaged,41,46,47 and this has resulted in the es-tablishment of strict criteria for patients who undergo laparoscopy for adnexal mass-es.48 Maiman et al.’s41 study was the primary impetus for creating these guidelines,and was based on the results of a survey questionnaire sent to gynecologic oncolo-gists, who were asked whether they had been involved in cases in which laparoscopywas employed and had resulted in mismanagement of ovarian malignancies. Forty-two referred cases were inappropriately managed. Laparotomy was employed duringthe initial procedure in only 17% of patients, and 71% of women required laparoto-my as a second procedure. The average delay was reported to be 4.8 weeks. Craw-ford et al.47 surveyed the members of the British Gynaecologic Cancer Society, and21 cases of ovarian malignancy in which laparoscopy was performed were identi-fied. None of these patients underwent immediate laparotomy for staging, and themean delay between diagnosis and surgery was 6.5 weeks. Four national surveysabout laparoscopic management of adnexal masses were published.41,49–52 All con-firmed that the pre- and intraoperative diagnosis of ovarian cancer may be difficult,and that an inadequate laparoscopic procedure may be dangerous. Capsule rupture,tumor morcellement and unprotected biopsy in the intra-abdominal cavity, and addi-


tional delay of adequate cancer surgery are the main pitfalls of this procedure.51

However, surgical mismanagement can occur with any surgical approach. Indeed the22.4% incidence of upstaging found in the French survey was similar to the resultsfound at restaging after inadequate surgical management by laparotomy.53,54

The initial staging of ovarian cancers is often incomplete. According to a multi-center study carried out by Averette et al.,55 the surgical exploration is insufficientin 75% of cases. In another study,53 31% of patients who had surgical restaging werefound to have a more advanced stage of disease than was initially suspected. Lap-aroscopy can identify previously undetected metastatic disease, particularly that lo-cated on the diaphragm. The first adequate laparoscopic surgical staging for ovariancancer reported by Querleu56 and other reports44 conclude that laparoscopic stagingfor ovarian carcinoma can be an accurate staging technique that may be valid as analternative to traditional laparotomic surgical staging. The results are encouraging,but lack of number of patients necessary to suggest the need for prospective clinicalstudies to establish the safety and the efficacy of this approach.

Laparoscopy as Second-Look Procedure

Candidates for second-look (SL) surgery are patients who were in an advancedstage of the disease at the time of diagnosis and who have achieved an apparent clin-ical remission after their initial course of chemotherapy. The procedure should in-clude peritoneal washings for cytological evaluation, careful inspection of theperitoneum and the diaphragm, and several biopsies that must be performed at vari-ous levels: the zone of the initial tumor, where there are any suspect lesions, as wellas on an apparently healthy peritoneum, especially on the paracolic sulci anddiaphragm.44,57

The need for laparotomy was reduced dramatically after the application of lap-aroscopy as an SL procedure for the follow-up of ovarian malignancies. In a studycomparing laparoscopy with laparotomy as SL procedures, Casey et al.58 concludedthat laparoscopy appears to be equally as effective as laparotomy in detecting persis-tent or recurrent malignant disease. Blood loss and hospitalization times were sig-nificantly lower in the laparoscopy group (33.9 mL vs. 164.9 mL and 0.3 days vs.6.8 days, respectively). In another comparative retrospective study of SL laparosco-py versus laparotomy, Abu-Rustum et al.59 reported that laparoscopy was associatedwith lower blood loss (27 mL vs. 208 mL), shorter operating times (129 min vs. 153min), shorter hospital stays (1.6 days vs. 6.8 days), and fewer complications. The re-currence rates after a negative SL surgery, with a median follow-up of 22 months,were similar for laparoscopy and laparotomy (14.3% vs. 14.8 %). Husain et al.,60 inevaluating the accuracy and safety of SL laparoscopy in women with ovarian cancer,reported a 46% rate of pathologically negative SL laparoscopies and recurrencerates, which are equivalent to those described in studies of SL assessment bylaparotomy.

Another important issue in laparoscopic management of ovarian cancer is thespread of the disease after surgery. From the current literature the incidence of thespread of ovarian cancer and of trocar site metastasis is difficult to establish.61 Sincethe ovary is an intraperitoneal organ and ovarian cancer a peritoneal disease, the riskof peritoneal spread may be higher in ovarian cancer than in other gynecologic ma-lignancies. To prevent these risks, a careful patient selection is necessary. The lap-


aroscopic management of ovarian cancer remains controversial. It should beperformed only in prospective clinical trials. Until the results of such studies becomeavailable, an immediate vertical midline laparotomy remains the gold standard pro-cedure if a cancer is encountered.

CONCLUSION

Minimal-access surgery is now more frequently used for the management of gy-necological malignancies, as it appears to be feasible. Many patients may benefitfrom the laparoscopic treatment of early-stage cervical and endometrial cancer, aswell as from laparoscopic evaluation and staging of cervical, ovarian, and endome-trial carcinomas. Reports in the literature show that laparoscopy may be an effectiveprocedure, with lower morbidity and complication rates than traditional abdominalsurgery. Short hospital stays and recovery times have a positive impact in patients’quality of life. Many risks may arise from the application of minimal-access surgeryin cancer patients, however, and many questions regarding safety and efficacy needanswers based on prospective clinical trials. We must emphasise that such studieswith large patient numbers and long-term follow-up are lacking. Until results fromthese trials become available, laparoscopic oncologic procedures should be per-formed only in an investigational setting by expert teams and surgeons accredited inthese fields.

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