Original Article
Adjuvant Therapy in Stage I and Stage II Epithelial Ovarian Cancer — Results of Two Prospective Randomized Trials
N Engl J Med 1990; 322:1021-1027April 12, 1990
- Abstract
- Abstract
About a third of patients with ovarian cancer present with localized disease; despite surgical resection, up to half the tumors recur. Since it has not been established whether adjuvant treatment can benefit such patients, we conducted two prospective, randomized national cooperative trials of adjuvant therapy in patients with localized ovarian carcinoma (International Federation of Gynecology and Obstetrics Stages la to lie). All patients underwent surgical resection plus comprehensive staging and, 18 months later, surgical reexploration.
In the first trial, 81 patients with well-differentiated or moderately well differentiated cancers confined to the ovaries (Stages lai and lbi) were assigned to receive either no chemotherapy or melphalan (0.2 mg per kilogram of body weight per day for five days, repeated every four to six weeks for up to 12 cycles). After a median follow-up of more than six years, there were no significant differences between the patients given no chemotherapy and those treated with melphalan with respect to either five-year disease-free survival (91 vs. 98 percent; P = 0.41) or overall survival (94 vs. 98 percent; P = 0.43).
In the second trial, 141 patients with poorly differentiated Stage I tumors or with cancer outside the ovaries but limited to the pelvis (Stage II) were randomly assigned to treatment with either melphalan (in the same regimen as above) or a single intraperitoneal dose of 32P (15 mCi) at the time of surgery. In this trial (median follow-up, >6 years) the outcomes for the two treatment groups were similar with respect to five-year disease-free survival (80 percent in both groups) and overall survival (81 percent with melphalan vs. 78 percent with 32P; P = 0.48).
We conclude that in patients with localized ovarian cancer, comprehensive staging at the time of surgical resection can serve to identify those patients (as defined by the first trial) who can be followed without adjuvant chemotherapy. The remaining patients with localized ovarian cancer should receive adjuvant therapy, and with adjuvant melphalan or intraperitoneal 32P should have a five-year disease-free survival of about 80 percent. (N Engl J Med 1990;322:1021–7.)
Media in This Article
Figure 1
Disease-free Survival of Patients with Localized Ovarian Cancer, According to Protocol and Treatment.Figure 2
Overall Survival of Patients with Stage I or Stage II Epithelial Ovarian Cancer, According to Protocol and Treatment.Article Activity
- Article
APPROXIMATELY 20,000 new epithelial ovarian cancers are reported annually in the United States, and about 30 percent of these are apparently localized (Stages I and II according to the classification of the International Federation of Gynecology and Obstetrics [FIGO]) at initial diagnosis.1 The published five-year survival rates for such patients range from 50 to 70 percent for Stage I cancer to only 38 to 60 percent for Stage II.2 , 3 Prognostic factors such as cell type and histologie grade provide only a partial explanation for the widely variable results. Earlier studies have demonstrated the need for thorough surgical staging to define the extent of disease and for a prospective comparison of treatments in groups of patients balanced for known prognostic factors. Few if any single institutions in the United States have enough patients to perform randomized clinical trials of patients with early disease. As a result, two collaborative clinical trials were begun by the Ovarian Cancer Study Group (composed of physicians at the Mayo Clinic, the M.D. Anderson Hospital and Tumor Institute, the National Cancer Institute, and the Roswell Park Memorial Institute) and the Gynecologic Oncology Group. Both trials required carefully predefined surgical staging before patients were entered in the study. The first trial included patients with Stage la and lb disease with well-differentiated or moderately well differentiated histologie grades, and the second trial included patients with poorly differentiated Stage I disease and all patients with Stage II disease. The median follow-up of the surviving patients from the two randomized trials now exceeds six years.
Methods
The two clinical trials were begun in 1976 by the Ovarian Cancer Study Group, which was joined in 1978 by the Gynecologic Oncology Group. Both used the staging criteria established by FIGO in 1976.4 Only patients with Stage I disease (limited to the ovaries) or Stage II disease (limited to the pelvis) were included, and all such patients were assigned to subgroups as defined in Table 1Table 1
Definitions of Stages I and II Ovarian Cancer, According to the International Federation of Gynecology and Obstetrics.. No patients with Stage I or II disease were excluded from the study except those with bulky Stage II tumors that could not be resected. After complete surgical staging, the patients in the first trial were randomly assigned to receive no further therapy or therapy with melphalan (0.2 mg per kilogram of body weight orally, daily for five days), with repeat courses every four to six weeks for 12 cycles or 18 months, whichever came first. A total of 92 patients were randomly assigned, 48 to receive melphalan and 44 to receive no further therapy. Patient enrollment ended in October 1984.The patients in the second trial were randomly assigned to receive either melphalan (in the same dose and according to the same schedule as in the first trial) or intraperitoneal 32P (15 mCi of chromic phosphate [before 1979 the dose was 7.5 mCi]). One hundred forty-five patients were randomly assigned, 71 to receive melphalan and 74 to receive 32P. The study was closed to new patients in November 1986.
Eligibility for either trial required a histopathological diagnosis of epithelial ovarian cancer. No patient had received any previous therapy except surgery, and all patients were required to have adequate bone marrow function as evidenced by a white-cell count above 4000 per cubic millimeter and a platelet count above 150,000 per cubic millimeter, as well as a blood urea nitrogen level below 7.1 mmol per liter (<20 mg per deciliter), a serum creatinine level below 106 μmol per liter (<1.2 mg per deciliter), and normal results of liver-function testing. Initial noninvasive staging procedures included chest radiography, intravenous pyelography, and before March 1983, lymphangiography. In addition, pelvic ultrasonography, barium enemas, pelvic and abdominal CT scanning, and proctosigmoidoscopy were performed when clinically indicated.
Surgical staging was performed through a vertical incision of sufficient length to allow the evaluation of the abdominal contents and the sites at high risk for surface metastases. For all patients the surgery included a total abdominal hysterectomy, a bilateral salpingo-oophorectomy, and partial infracolic omentectomy. In addition, the tumor capsule was examined for rupture, excrescences, or any adherence requiring sharp dissection; ascitic fluid was examined for malignant cells, and if no ascites was present, separate 250-ml saline washings were obtained from the pelvis and both abdominal gutters and examined cytologically. Biopsies of suspicious lesions were performed, along with random biopsies of the pelvic peritoneum, the cul-de-sac peritoneum, the right and left abdominal gutter peritoneum, and the undersurface of the right diaphragm. Biopsies of any suspicious omental nodule were performed. To assess the nodal spread of disease, the paraaortic and pelvic lymph nodes were palpated, sampled, and examined histologically.
A complete pathological review of all tissue specimens and cytologie findings was performed before randomization at the primary institution. Subsequently, all pathological findings were reviewed by the central pathology office in accordance with the established procedures of the Pathology Review Committee of the Gynecologic Oncology Group.
A stratified randomization plan was developed with computer-generated random numbers and implemented by telephone contact between the clinical site and the data-coordinating center. The stratifications were made on the basis of cell type and histologie grade (well, moderately, or poorly differentiated, according to the pattern-grading classification5 , 6). In addition, the patients in the second trial were stratified according to stage into three groups —Group A (those with Stage Iai or Ibi disease with poorly differentiated histologie grades and those with Stage Iaii or Ibii disease), Group B (those with Stage Ha or lib disease), and Group C (those with Stage Ic or lie disease and any patient with disease detectable microscopically). Randomization within each stratum was done in blocks of two, so that for each consecutive pair of patients within each stratum, one was assigned to each treatment. Because the clinical site was not a factor in the stratification, the assignment to treatment could not be predicted by individual physicians. At randomization, no patient included in the trials had macroscopic residual disease (any nodule more than 2 cm in transverse diameter). Informed consent was obtained from all patients before entry into either trial.
Both protocols required that patients who were free of symptoms suggestive of recurrent disease 18 months after entry into the study undergo routine reexploration. Symptomatic patients underwent reexploration earlier unless obvious recurrent disease was documented by noninvasive study. At second-look surgery, all patients had peritoneal washings, and multiple biopsies were performed of the right and left paracolic gutters, the cul-de-sac, the lateral pelvic wall, the small-bowel mesentery, and the omentum. In addition, biopsies were performed of adhesions and known sites of previous disease. The results of this second-look surgery have been published previously.7
Life-table probabilities of survival and disease-free survival were calculated by the method of Kaplan and Meier.8 Disease-free survival was defined as the time to a first event — recurrence or death. Comparisons of the survival distributions were made with the log-rank test.9 The Cox proportional-hazards regression model was used to perform comparisons after adjustment for the base-line characteristics and to investigate the prognostic value of the baseline variables. Confidence limits for the measures of interest were calculated according to the methods described by Simon.10
The target samples for these studies were 110 patients in the first trial and 142 in the second. The goal for the second trial was achieved. In the first trial, accrual was terminated at 74 percent of the accrual goal (after eight years during which patients were entered) because of an observed rate of relapse so low as to preclude with any reasonable probability the eventual detection of moderate differences between the two groups.
Results
First Trial
The first trial included patients who had Stage la or lb disease with well-differentiated or moderately well differentiated epithelial ovarian cancer. After comprehensive staging, 92 patients were randomly assigned — 44 to receive no additional therapy and 48 to receive melphalan. However, 11 patients were deemed ineligible and were excluded from analysis (6 of the patients assigned to observation and 5 of those assigned to melphalan). Eight patients were found ineligible on the basis of stage: 2 were found in the review by the central pathology office to have benign tumors, and 1 had a poorly differentiated tumor. Thus, a total of 81 patients were available for analysis — 38 assigned to observation and 43 assigned to treatment with melphalan.
One of the 38 patients assigned to observation alone received melphalan. She was initially classified as ineligible, and her physician elected to treat her with melphalan. Subsequent central review established her eligibility, and she was therefore included in the analysis. Of the 43 patients assigned to chemotherapy with melphalan, 1 received no drug, 2 received only one course, and 2 received only three courses. Thirty-one (72 percent) received 10 or more courses. The survival analysis included all patients randomized, regardless of whether they received the assigned therapy or completed their full course. A secondary analysis omitting patients who received inappropriate, limited, or no therapy yielded similar results. Three patients randomly assigned to melphalan who were subsequently found to be ineligible for the first trial but eligible for the second were followed and included in the analysis of toxic effects and pathological findings for the second trial, but not in the comparisons of treatment efficacy. Five patients were lost to follow-up before five years: two assigned to observation were lost at 35 and 43 months, and three assigned to melphalan were lost at 15, 18, and 50 months. Our analysis treated these as random losses, and the patients were included in the analyses of survival and disease-free survival up to the date of their last contact with the study.
The characteristics of the randomized patients are shown in Table 2Table 2
Characteristics of Patients with Stage I or Stage II Ovarian Cancer.. The two groups were well matched with respect to histologie type, histologie grade, and stage, but the patients assigned to melphalan were somewhat younger. The histologie type and grade were based on the classifications made in the central pathology review. The histologie grades were well-differentiated, moderately well differentiated, and poorly differentiated tumors, as well as tumors of borderline malignancy. A central pathological review was made for 72 of 81 patients who could be evaluated (89 percent), and the results compared with those of the review by the original institution (data not shown). There were no major differences in histologie type noted. Although the design of the trial sought to exclude patients with tumors of borderline malignancy, the difficulty of making this exclusion is evident. As shown in Table 2, 27 of the patients in the first trial (33 percent) were later declared on central pathological review to have tumors of borderline malignancy, even though the original pathologist considered that the criteria for a more malignant process had been met. The patients with tumors of borderline malignancy were reasonably evenly distributed between the two study groups.Toxicity
The patients assigned to observation did not receive placebo, so the frequency of placebo-related toxic effects was not assessed. For the patients receiving melphalan, the immediate toxic effects were mild and tolerable. Seventy-nine percent of the patients had some degree of myelosuppression. Seven patients (16 percent) had severe myelosuppression at some point in their course, five (12 percent) had platelet-count nadirs under 50,000 per cubic millimeter, and four (9 percent) had white-count nadirs under 2000 per cubic millimeter. There were no infectious complications related to leukopenia and no bleeding episodes related to thrombocytopenia induced by the chemotherapy. Eleven patients (26 percent) reported mild-to-moderate gastrointestinal side effects. No other adverse reactions were reported. One patient treated with melphalan died six years after completing treatment, with a diagnosis of aplastic anemia. No autopsy was performed. No other myeloproliferative disorders or second cancers have been seen in these patients treated with melphalan after more than 250 person-years of follow-up.
Survival
With a median follow-up of more than six years in the surviving patients and 71 of 75 surviving patients who were followed for three or more years, only six deaths have been observed (Table 3Table 3
Tumor Recurrences and Deaths among Patients with Stage I or Stage II Ovarian Cancer.). Four of the deaths occurred in the observation group, and two in the melphalan group. One of the deaths in the observation group was that of the patient who received melphalan inadvertently. One of the six deaths was that of a patient who had been classified as having a tumor of borderline malignancy. Five deaths were attributed primarily or secondarily to ovarian cancer, and one to aplastic anemia; four of the six patients who died had documented recurrences of disease. The sites of recurrence were reviewed for the presence of distinctive patterns, but as shown in Table 3, none were apparent. Life-table plots of disease-free and overall survival according to treatment group are shown in Figures 1Figure 1Disease-free Survival of Patients with Localized Ovarian Cancer, According to Protocol and Treatment. and 2Figure 2Overall Survival of Patients with Stage I or Stage II Epithelial Ovarian Cancer, According to Protocol and Treatment., respectively. The estimated five-year disease-free and overall survival rates for untreated patients were 91 and 94 percent, respectively. For the patients treated with melphalan, both the estimated disease-free survival and the overall five-year survival rates were 98 percent. Reliable confidence intervals for differences in rates are difficult to calculate when the rates are close to 111; however, the results of the log-rank test for the differences between groups in survival distributions were not significant or even suggestive (for survival, P = 0.43; for disease-free survival, P = 0.41). With the assumption that the use of melphalan has no effect on the long-term survival of this group of patients, we calculated the overall five-year survival rate for both groups at 96 percent, with a lower 90 percent confidence limit for five-year survival of 92 percent.Second Trial
The second trial included all patients who after comprehensive surgical staging were found to have disease of Stage Iaii, Ibii, Ic, Ha, lib, or lie; or of Stage la or lb with poorly differentiated histologie features. The patients were randomly assigned to receive either melphalan (in a dose and according to a schedule similar to those in the first trial) or 15 mCi of intraperitoneal 32P as chromic phosphate. A total of 145 patients were entered in the trial. Four patients (3 percent) — three randomly assigned to melphalan and one to 32P — were ineligible (one because of Stage III disease, one with a benign tumor, one with idiopathic thrombocytopenic purpura, and one for whom the primarily ovarian origin of the tumor was uncertain). Therefore, a total of 141 patients were evaluated; 73 were randomly assigned to receive 32P, and 68 to receive melphalan. The characteristics of the patients are shown in Table 2.
Of the 73 patients assigned to receive 32P, 5 (7 percent) did not receive it because of difficulties in catheter implantation; one additional patient refused this treatment. Five of these received melphalan according to the regimen prescribed for the patients in the other group. Sixty-eight patients were assigned to melphalan. Only one patient refused chemotherapy before beginning treatment; she was treated with intraperitoneal 32P. All the other patients assigned to melphalan received at least 10 courses of the drug, except for six patients who had early progressive disease. The data analysis included all patients randomly assigned to the therapy regardless of whether they received the treatment assigned. A secondary analysis, comparing the patients as actually treated rather than as randomized, produced similar results. Three patients were lost to follow-up before the end of five years; one (lost at 28 months) was assigned to 32P, and two (lost at 15 and 19 months) were assigned to melphalan. As in the first trial, our analysis treated these as random losses.
The two groups in the study were well balanced with respect to histologie type, histologie grade, disease stage, extent of residual tumor, and age. The histologie type and grade were based on the findings of the central pathological review, and the histologie grade was coded as in the first trial. Central pathological review was performed for 130 of the 141 patients (92 percent), and there were no major differences between the determinations of histologie type made by the original institution and the central pathology office (data not shown). As in the first trial, the patients with tumors of borderline malignancy were to be excluded from entry into this trial. However, after reanalysis in the central pathological review, 17 percent were reclassified as having tumors of borderline malignancy. These patients were reasonably well distributed between the two treatment groups (Table 2).
Toxicity
The immediate side effects were generally mild and manageable in both treatment groups. Of the 68 patients treated with 32P, 14 (21 percent) reported mild-to-moderate abdominal pain, and 4 (6 percent) had severe pain. One patient had chemical peritonitis, and one had infectious peritonitis. Four patients (6 percent) underwent exploratory surgery for bowel obstruction, and no tumor was identified. Approximately two thirds of all patients treated with 32P had no side effects. Of the patients treated with melphalan, 74 percent had some myelosuppression, and in 20 percent the myelosuppression was classified as severe. The median white-count nadir in the patients with myelosuppression was 2400 per cubic millimeter, and 12 patients (18 percent) had white-count nadirs below 2000 per cubic millimeter. The median platelet-count nadir was 81,000 per cubic millimeter, and 5 (7 percent) had platelet counts under 25,000 per cubic millimeter. No serious infectious complications or bleeding episodes were reported. Eleven patients who were treated with melphalan (16 percent) reported mild-to-moderate gastrointestinal toxicity. One patient received 12 courses of melphalan in 1977 and 1978 and died in March 1982, 15 months after being given a diagnosis of preleukemia. In January 1986 acute myelogenous leukemia developed in a second patient, who was treated with seven courses of melphalan in 1981 and 1982 and who died in July 1987.
Survival
In 27 patients (19 percent), tumors have recurred — 14 (19 percent) in the group receiving 32P and 13 (19 percent) in the group receiving melphalan (Table 3). Twenty-two (81 percent) of the recurrences were seen in the first two years of follow-up. Five recurrences were observed after two years — at 30, 34, 61, 78, and 84 months. The patterns of recurrence are listed in Table 3; there were no major differences between groups. Thirty-one patients have died (22 percent) — 16 who received 32P and 15 who received melphalan. Twenty-four of the deaths (77 percent) were attributed primarily or secondarily to ovarian cancer. The deaths not due to ovarian cancer were from various causes — cerebral vascular accidents (in two), myeloproliferative disorders (two), gram-negative pneumonia (one), lung cancer (one), and unknown cause (one).
The follow-up in the surviving patients now exceeds six years, and 86 percent of these patients have been observed for at least three years. The distributions of survival and disease-free survival in the two groups are virtually identical (Fig. 1 and 2; P = 0.87 and 0.48, respectively). The five-year disease-free survival rate is 80 percent in each arm. The five-year survival rates are 78 percent in the patients assigned to 32P and 81 percent in those assigned to melphalan. The 90 percent confidence intervals for the differences in these rates are from −0.11 to 0.11 for disease-free survival and from −0.08 to 0.16 for survival, with a negative number indicating an advantage for 32P and a positive number indicating an advantage for melphalan. Thus, even a moderate advantage of one treatment over the other is unlikely on the basis of the observed data.
Prognostic Factors
A multivariate analysis was performed to identify the base-line characteristics that might influence prognosis. Age, previous hysterectomy, histologie type, histologie grade, and FIGO stage were considered. Residual tumors were present in six patients, four of whom had recurrences; however, this characteristic was not included in the multivariate analysis because of the small number of patients affected. Only age and histologie grade were treated as ordinal variables. The end point of the analysis was disease-free survival.
The only variables that appeared to be strongly and independently related to outcome were clear-cell tumor type and histologie grade. However, histologie grade appeared to be highly prognostic only when patients with tumors of borderline malignancy were included. Clear-cell tumors were associated with poorer outcomes.
Pathological Findings
The number of recurrences observed in both trials is shown in Table 4Table 4
Recurrences of Ovarian Cancer According to Histologie Type. according to pathological classification. Although the number of patients with clear-cell carcinomas in each trial was small, this was the only histologie type associated with a higher-than-expected frequency of relapse. If one analyzes only patients who had a central pathological review, a total of 3 of 8 patients who had clear-cell tumors in the first trial (38 percent) had relapses, as compared with 2 of 63 patients with other tumor types (3 percent). In the second trial, relapses occurred in 9 of 26 patients with clear-cell tumors (35 percent), as compared with 16 of 107 patients with tumors of other histologie types (15 percent).Discussion
Comprehensive surgical staging allows the selection of the appropriate treatment for early ovarian carcinomas (FIGO Stages la to lib). It is clear that the entire abdomen is at risk for metastases. Adjuvant therapies, if required, must treat these sites of high risk. Unfortunately, the surgical evaluation of patients with ovarian cancer is commonly incomplete.12 , 13 Such deficiencies of staging make it hard to interpret earlier clinical studies and select appropriate therapy for patients with FIGO Stage I or II disease.
These two trials were designed to include only patients in whom a careful, standardized, comprehensive surgical exploration confirmed the presence of localized disease, so that the true benefit of adjuvant therapy, if any, could be assessed. With a median follow-up in excess of six years and a follow-up of more than two years in all patients, several conclusions are clear. For patients who underwent surgical staging as defined by this study and were found to have Stage Iai or Ibi disease with well-differentiated or moderately well differentiated histologie features, the five-year survival was excellent (≥90 percent), and adjuvant therapy with melphalan did not significantly improve the results. In view of the toxicity, the expense, the inconvenience, and the risk of second cancers, the identification of a group of patients who do not require adjuvant therapy represents a substantial benefit. Three patients in these two trials who received melphalan therapy had myeloproliferative disorders or acute leukemia that were most likely a result of treatment. Although such complications are uncommon, they are a well-known catastrophic risk.14 , 15
For patients with localized ovarian cancer as defined by the entry criteria of the second trial, the five-year survival was 80 percent, with similar results in both the 32P group and the melphalan group. Although this result is substantially better than the five-year survival rates of 40 to 60 percent published previously for patients with Stages Ic to lie disease, it is impossible to determine whether the surgical staging simply served to define a group of patients with a better prognosis. However, even with the staging as performed in this study, 20 percent of this group have had relapses and died of ovarian cancer, making it appear likely that some adjuvant treatment is required in such patients. In the absence of a therapeutic difference between the two groups in the second trial, we have concluded that the group receiving the single dose of intraperitoneal 32P, with its limited toxicity (and no known risk of leukemia), is the preferred standard group for subsequent study. Since the evidence from trials in advanced ovarian cancer suggests that platinum-containing combination drugs administered in intensive doses are effective,16 17 18 the Gynecologic Oncology Group has initiated a replacement trial comparing intraperitoneal 32P therapy with treatment involving three cycles of cyclophosphamide and cisplatin.
Unfortunately, most trials of therapy for localized ovarian cancer have not been randomized,19 20 21 22 have not required comprehensive surgical staging,23 24 25 or have included patients with Stage II or III disease who have minimal residual disease.26 , 27 Because these trials contained a mixture of patients with various stages of disease, extent of residual disease, and histologie grades, it is impossible to determine the benefit, if any, of adjuvant treatment. However, in the absence of thorough surgical staging, patients in all the early stages of disease combined have substantial relapse rates at 5 and 10 years, and no subgroup of these patients can safely be left without adjuvant therapy. Our trial confirms the risk of upper abdominal relapse seen in earlier trials.23 24 25 26 The site of the majority of recurrences in this study (71 percent) was either distant (32 percent) or abdominal (39 percent).
Ovarian tumors of borderline malignancy have been difficult to define histologically, but there is virtually complete agreement that their usual course is more indolent than that of tumors in patients with invasive disease.28 , 29 In both trials described here, the patients with tumors of borderline malignancy were evenly distributed between groups, and the comparisons of therapeutic efficacy were unaffected by the exclusion of these patients. The five-year survival of the patients in the first trial was unchanged when the patients with tumors of borderline malignancy were excluded. After a similar exclusion in the second trial, the five-year survival became 76 percent rather than 80 percent. The substantial number of reclassifications emphasizes how difficult it is to be certain whether stromal invasion is present unless a large number of slides from tumors sectioned at 1-cm intervals are available for review. Only 2 of the 51 patients in our trial who were considered to have tumors of borderline malignancy (4 percent) have died. In neither patient was the death clearly caused by the underlying cancer. Given the risks, costs, and inconvenience of adjuvant therapy, our results would suggest that patients with Stage I or II disease who have tumors of borderline malignancy should not receive adjuvant treatment.
The presence of clear-cell varieties of epithelial ovarian cancer, whether alone or with other epithelial-cell elements, may be associated with a higher risk of recurrent disease. Although only 35 of the 204 patients who had a central pathological review (17 percent) had clear-cell histologie features, 12 of 30 recurrences (40 percent) involved this histologie element. The clinical behavior of this type of tumor has been defined incompletely in the literature, probably because of the inclusion of widely divergent histologie features such as endodermal sinus tumors and endometrioid tumors with clear-cell features.30 , 31
Comprehensive surgical staging of patients with early ovarian cancer serves to define a group of patients who require no further therapy and allows the selection of suitable adjuvant therapy for the remaining patients. Both groups identified and treated in this manner have excellent long-term disease-free and overall survival.
Source Information
From the Gynecologic Oncology Group, Philadelphia (L.A.W., H.D.H., G.D.W., A.M., R.P., F.M.), and the Ovarian Cancer Study Group (D.G.D.) and the National Cancer Institute (R.C.Y., S.S.E.), Bethesda, Md. Address reprint requests to Dr. Young at the Fox Chase Cancer Center, 7701 Burholme Ave., Philadelphia, PA 19111.
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