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Adjuvant therapy of early-stage (stage I and II) epithelial ovarian, fallopian tube, or peritoneal cancer

Adjuvant therapy of early-stage (stage I and II) epithelial ovarian, fallopian tube, or peritoneal cancer
Literature review current through: Jan 2024.
This topic last updated: Aug 24, 2023.

INTRODUCTION — Epithelial cancers of ovarian, fallopian tube, and peritoneal origin exhibit similar clinical characteristics and behavior. As such, these are often combined and define epithelial ovarian cancer (EOC) in clinical trials and clinical practice. This topic will consider all three tumor origins under the heading EOC.

EOC is the most common cause of death among women with gynecologic malignancies and the fifth leading cause of cancer death in women in the United States. Only approximately 25 percent of women will be diagnosed with early-stage ovarian cancer, either confined to the ovary (stage I) or confined to the pelvis (stage II). For women with EOC confined to the ovary (IA or IB) and/or well-differentiated (grade 1) tumors, prognosis is excellent with survival of at least 90 percent following surgery alone [1,2]. For all others, adjuvant chemotherapy is recommended.

This section will review adjuvant therapy for early-stage EOC. Initial surgical management, adjuvant therapy for women with advanced (stage III or IV) ovarian cancer, and chemotherapy for women with recurrent disease are discussed separately.

(See "Overview of epithelial carcinoma of the ovary, fallopian tube, and peritoneum".)

(See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Clinical features and diagnosis".)

(See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Surgical staging".)

(See "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer".)

(See "Medical treatment for relapsed epithelial ovarian, fallopian tube, or peritoneal cancer: Platinum-sensitive disease".)

(See "Medical treatment for relapsed epithelial ovarian, fallopian tube, or peritoneal cancer: Platinum-resistant disease".)

SELECTION OF PATIENTS — A subset of women with early-stage disease are at increased risk of relapse and can be identified based on the presence of high-risk features including:

Stage IC (tumor confined to the ovary with positive peritoneal washings) or stage II (tumor involving the pelvis) disease

Clear cell histology (any stage)

High tumor grade (grade 3)

These high-risk features are used as criteria to determine eligibility for adjuvant therapy in clinical trials of women with early-stage disease and for the use of adjuvant therapy outside of clinical trials [3]. For women with these features, five-year disease-free survival rates range from 40 to 80 percent [2,4,5]. This compares with a five year survival rate of at least 90 percent among women with well-differentiated (grade 1) tumors confined to the ovary (stage IA or IB) [1,2]. It is controversial whether women with grade 2 ovarian cancer should be considered as having high-risk disease and offered adjuvant therapy.

The benefit of adjuvant chemotherapy in patients with early-stage EOC has been further shown in two meta-analyses:

In the first, 13 trials conducted between 1965 and 2004 were included, although only eight of these studies were performed exclusively in stage I ovarian cancer [6].

The pooled results for chemotherapy for women with stage I ovarian cancer showed a benefit for adjuvant treatment in terms of recurrence-free survival (relative risk [RR] 0.70, 95% CI 0.58-0.86) and overall survival (RR 0.74, 95% CI 0.58-0.94).

Five-year overall survival was improved with the use of adjuvant platinum-based therapy (hazard ratio [HR] 0.67, 95% CI 0.50-0.90).

In the second, five randomized trials conducted between 1990 and 2003 involving 1277 women were included in the analysis [7]. Again, adjuvant chemotherapy was associated with benefit in terms of both progression-free survival (HR 0.67, 95% CI 0.52-0.84) and overall survival (HR 0.71, 95% CI 0.53-0.93).

For women who had no gross residual following surgery, chemotherapy did not appear to improve overall survival when compared with observation (HR 1.22, 95% CI 0.63-2.37). In comparison, for women who had incompletely resected disease, chemotherapy resulted in superior survival when compared with observation (HR 0.63, 95% CI 0.46-0.85).

Women with high-risk tumors had a survival advantage with the use of adjuvant chemotherapy over observation (HR 0.48, 95% CI 0.32-0.72). Those with low-risk tumors did not derive a benefit from chemotherapy (HR 0.95, 95% CI 0.54-1.66).

A subsequent publication of the Adjuvant Chemotherapy in Ovarian Neoplasms (ACTION) trial has questioned the benefit of adjuvant chemotherapy in early-stage disease following complete surgical staging [8]. The ACTION study enrolled 448 women with early EOC and high-risk features and randomly assigned post-surgical care to adjuvant platinum-based chemotherapy versus observation [9]. While surgical treatment was not protocol mandated, the study incorporated strict definitions of optimal versus non-optimal staging. After a median follow-up of ten years, adjuvant chemotherapy resulted in the following outcomes when compared with observation [8]:

A significant improvement in recurrence-free survival (RFS, 70 versus 62 percent, HR 0.64, 95% CI 0.46-0.89) and a trend towards an improvement in cancer-specific survival (CSS, 82 versus 76 percent, HR 0.73, 95% CI 0.48-1.13).

For women who underwent complete surgical staging, there was no significant improvement in either RFS (78 versus 72 percent, HR 0.73, 95% CI 0.38-1.42) or CSS (85 versus 89 percent, HR 1.58, 95% CI 0.61-4.08). However, for women who had incomplete surgical staging, there was a significant improvement in both RFS (65 versus 56 percent, HR 0.60, 95% CI 0.41-0.87) and CSS (80 versus 69 percent, HR 0.58, 95% CI 0.35-0.95).

Overall, the available evidence supports the use of adjuvant chemotherapy in patients with early-stage ovarian cancer with high-risk features. By contrast, patients with no risk factors do not appear to benefit from chemotherapy. Further prospective clinical trials are needed to determine whether patients with one or more of these high-risk features who have undergone optimal surgical staging may omit adjuvant chemotherapy, although strong evidence of lack of benefit for chemotherapy would be needed to omit treatment, given that the goal of treatment in this population is cure.

Our approach is consistent with that of the National Comprehensive Cancer Network guidelines [10]. For women with resected and fully staged grade 1, stage IA or IB disease, we recommend observation alone rather than the use of adjuvant therapy. For women with high-risk disease (defined as stage IC or II, high-grade or clear cell cancers of any stage), we recommend adjuvant chemotherapy. We also suggest the use of adjuvant chemotherapy for women with grade 2 tumors but acknowledge that observation, in the absence of other risk factors, may be an acceptable alternative for this subgroup of patients.

CHOICE OF ADJUVANT TREATMENT

Intravenous chemotherapy — As described above, adjuvant therapy is offered to women with early-stage EOC with high-risk features, typically between 21 and 35 days from primary debulking surgery, given some evidence of worsened survival with delay beyond 35 days [11]. For such women, adjuvant intravenous chemotherapy is the preferred modality. While the optimal adjuvant chemotherapy regimen is unknown, most clinicians offer treatment with a platinum-based doublet, such as paclitaxel and carboplatin, largely because of its demonstrated efficacy in the adjuvant therapy of women with advanced-stage EOC (table 1). (See "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer".)

Both intravenous platinum-based chemotherapy and intraperitoneal P 32 have been evaluated as the adjuvant treatment in this population. Several trials have compared platinum-based chemotherapy (either cisplatin alone or cisplatin plus cyclophosphamide) with P 32 in women with early-stage disease [4,12,13]. In each of these, P 32 therapy was associated with increased toxicity without improved efficacy. In particular, P 32 therapy was complicated by problems with adequate distribution and bowel toxicity (eg, perforation). Given the effectiveness of chemotherapy, intraperitoneal P 32 has been abandoned and is no longer used in the treatment of early-stage ovarian cancer.

There is a lack of consensus regarding the optimal adjuvant regimen in this setting. We prefer a platinum-based doublet (ie, paclitaxel plus carboplatin) largely based upon indirect evidence that it significantly improves outcomes when administered as adjuvant therapy for more advanced disease (table 1) [10,14]. Single-agent carboplatin has been suggested as an acceptable alternative [14,15]; however, data are insufficient to support single-agent platinum as the optimal chemotherapy regimen in this patient population over a platinum/taxane combination.

Duration — The optimal duration of adjuvant chemotherapy for early-stage EOC is undefined. We administer paclitaxel plus carboplatin for six cycles. We recognize that the benefit of six cycles may be limited to women with serous cancers or women with stage II disease. It is reasonable to individualize the number of cycles based upon patient risk factors and the tolerance of therapy, with a planned minimum of three cycles.

There is a paucity of data regarding the ideal number of treatment cycles in this setting. In Gynecologic Oncology Group Trial 157 (GOG 157), 457 women were treated with either three or six course of paclitaxel (175 mg/m2) plus carboplatin (area under the curve 7.5) given every three weeks to 457 women with high-risk early-stage disease [16]. Compared with three cycles, the administration of six cycles was associated with the following results:

A nonsignificant trend towards lower risk of recurrence (20 versus 25 percent)

Similar five-year survival rate (83 versus 81 percent)

More toxicity (neurotoxicity, granulocytopenia, and anemia)

In a subsequent ad hoc analysis of the same trial, a significantly lower risk of recurrence was seen for six rather than three cycles of chemotherapy in patients with serous tumors (hazard ratio 0.33, 95% CI 0.14-0.77) but not other histologic types [17]. Comparing six versus three cycles, five-year overall survival was not significantly different among women with serous cancers (86 versus 73 percent). Similarly, for women with other tumor types there was no difference in overall survival with three or six cycles. Therefore, our approach for serous tumors is aim to treat for six cycles but consider tolerance of therapy. For nonserous cancers, we treat with at least three cycles and assess the patient for tolerance to the treatment. If there is minimal toxicity, subsequent cycles to a maximum of six can be administered with reassessment at each cycle.

SPECIAL CONSIDERATIONS

Clear cell histology — Clear cell carcinomas are associated with poorer responses to platinum-based chemotherapy compared with serous adenocarcinomas. This was shown in one retrospective study that reported on the outcomes of women with a clear cell carcinoma (n = 101) versus serous carcinomas (n = 235) [18]. Compared with women with serous carcinomas, clear cell carcinomas were associated with:

A significantly lower response rate to platinum-based therapy (11 versus 72.5 percent).

Lower duration of overall survival in those patients with stage I/II (31.8 versus 42.3 months), or stage III disease (12.7 versus 26.8 months), although it was only significant for patients with stage III disease. However, overall survival was similar among patients who presented with stage IV disease (17.8 versus 19.4 months).

Because of the relatively poor prognosis for patients with a clear cell ovarian cancer, we prefer treatment on a clinical trial exploring alternative or novel agents. Such agents include temsirolimus with carboplatin and paclitaxel in GOG 268 (as a first-line therapy) and sunitinib in GOG 254 (for the treatment of recurrent disease).

Unstaged patients — The finding of early-stage EOC is occasionally made during surgery for an emergent (eg, torsion) or benign (ie, ovarian cystectomy) indication. In these cases, women will not have undergone surgical staging and technically speaking would be considered to have apparent early but unstaged ovarian cancer. For women with unstaged apparent early EOC, we suggest staging because both prognosis and adjuvant treatment options are tied to disease stage. Often this surgery can be performed through a minimally invasive approach. Alternatively, some evidence suggests that surgery may not be required if adjuvant chemotherapy is administered:

As described above, the Adjuvant Chemotherapy in Ovarian Neoplasm (ACTION) trial of adjuvant chemotherapy versus observation highlighted the importance of complete surgical staging in patients with early-stage EOC [9]. In this trial, the benefit of adjuvant chemotherapy was limited to patients with incomplete staging:

For the 297 women who were not completely staged, adjuvant chemotherapy was associated with significant improvement in recurrence-free survival (hazard ratio [HR] 1.78, 95% CI 1.15-2.77) and overall survival (HR 1.75, 95% CI 1.04-2.95) compared with observation.

For the 224 women enrolled into the observation arm, complete staging was associated with a significant improvement in recurrence-free (HR 1.82, 95% CI 1.02-3.24) and overall survival (HR 2.31, 95% CI 1.08-4.96) over incomplete staging.

For the 151 women who were completely staged, chemotherapy was not associated with a recurrence-free or overall survival advantage over observation.

In a retrospective study of 88 patients with early-stage ovarian cancer (36 unstaged), all of whom received adjuvant chemotherapy, there was no difference in outcomes among women who underwent staging after a diagnosis of EOC and those who did not undergo a second surgery for staging [19]. The estimated rates of five-year progression-free survival (PFS) were 85 and 80 percent, respectively, with corresponding rates of overall survival of 85 and 88 percent.

In a separate series of 138 patients with tumor confined to the ovary, 53 underwent adjuvant chemotherapy (34 after staging, 19 without staging performed) [20]. The relapse rate at a median follow-up of 58 months was 32 percent among staged patients and 42 percent among unstaged patients.

While these underpowered studies suggest that it might be safe to omit formal surgical staging after a woman has been diagnosed with apparent EOC, prospective studies are needed to confirm this finding before incorporating this into standard practice. For women who choose not to undergo formal surgical staging, we recommend adjuvant chemotherapy. With grade 3 or clear cell tumors, where chemotherapy will be administered regardless of staging outcome, there may be less impetus for a secondary procedure.

Intraperitoneal chemotherapy — The use of adjuvant intraperitoneal (IP) chemotherapy for patients with early-stage disease is experimental and is being evaluated in clinical trials. Interest in its use is based upon studies of IP chemotherapy in optimally resected advanced-stage EOC that demonstrated improvements in both PFS and overall survival, but at the risk of catheter-related complications and serious gastrointestinal toxicity. Results from GOG252, enrolling women with optimally cytoreduced stage II to III ovarian cancer, suggest similar PFS results between dose-dense IV therapy and IV/IP therapy, and are discussed elsewhere. (See "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer", section on 'IV/IP therapy versus IV therapy alone'.)

Maintenance therapy — For most patients with early-stage disease, we suggest observation following adjuvant chemotherapy rather than the use of maintenance therapy for early-stage EOC. However, for those with early BRCA-associated ovarian cancer (with either a somatic or germline mutation), some UpToDate contributors also offer maintenance therapy with a poly(ADP-ribose) polymerase (PARP) inhibitor [21], particularly for stage II disease, extrapolating from PFS benefits observed in more advanced-stage disease. (See "Management of ovarian cancer associated with BRCA and other genetic mutations", section on 'PARP inhibitor maintenance therapy'.)

Maintenance therapy refers to the prolonged administration of agents with low toxicity profiles in patients who have a complete clinical response in an attempt to prevent progression of disease. Studies have investigated the use of maintenance therapy for early-stage EOC. As an example, the benefit of maintenance paclitaxel versus observation was evaluated in a trial in which 571 patients were treated with three courses of paclitaxel (175 mg/m2) and carboplatin (area under the curve 6) followed by either 24 weeks of paclitaxel (40 mg/m2) or observation [22]. When compared with observation, maintenance paclitaxel was not associated with improvements in the five-year risk of recurrence (HR 0.807, 95% CI 0.565-1.15) or estimated rate of survival at five years (85 versus 86 percent, respectively). Grade 2 or greater adverse events were significantly increased with maintenance paclitaxel compared with observation. (See "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer", section on 'Maintenance therapy'.)

PROGNOSIS — Given the relatively uncommon detection of early-stage EOC, there are few reports on survival outcomes. However, in a report from the Gynecologic Oncology Group (GOG) that assessed 506 women treated in two trials of adjuvant therapy for early-stage EOC, recurrence-free and overall survival at five years were 76 and 82 percent, respectively [5]. Independent predictors of inferior survival included older age, stage II disease, high tumor grade, and positive peritoneal washings. In a separate analysis of outcomes for women with early-stage EOC treated on GOG 157, the recurrence rate was 25 percent [3].

POST-TREATMENT SURVEILLANCE — Post-treatment surveillance, including the role of CA-125 measurements, for women who have completed treatment for ovarian cancer is discussed separately. (See "Overview of epithelial carcinoma of the ovary, fallopian tube, and peritoneum", section on 'Posttreatment surveillance'.)

TREATMENT OF RECURRENT DISEASE — Recurrence can be detected either serologically using tumor markers (eg, CA-125) and/or by the development of clinical or radiologic signs of progression. We recommend re-treatment based on signs and/or symptoms of relapsed ovarian cancer and not treating a rising CA-125 alone. This is discussed in more detail separately. In addition, indications and surgical management of recurrent disease are discussed separately. (See "Overview of epithelial carcinoma of the ovary, fallopian tube, and peritoneum", section on 'CA 125 surveillance' and "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer", section on 'Treatment of recurrent disease'.)

The management of relapsed disease is stratified based upon the amount of time that has elapsed between the completion of platinum-based treatment and the detection of relapse, known as the platinum-free interval (PFI):

Patients with a PFI of six months or longer are considered to have “platinum sensitive” disease. (See "Medical treatment for relapsed epithelial ovarian, fallopian tube, or peritoneal cancer: Platinum-sensitive disease".)

Patients with a PFI of less than six months are considered to have “platinum-resistant” disease. (See "Medical treatment for relapsed epithelial ovarian, fallopian tube, or peritoneal cancer: Platinum-resistant disease".)

SOCIETY GUIDELINE LINKS — Links to society and government-sponsored guidelines from selected countries and regions around the world are provided separately. (See "Society guideline links: Ovarian, fallopian tube, and peritoneal cancer".)

INFORMATION FOR PATIENTS — UpToDate offers two types of patient education materials, “The Basics” and “Beyond the Basics.” The Basics patient education pieces are written in plain language, at the 5th to 6th grade reading level, and they answer the four or five key questions a patient might have about a given condition. These articles are best for patients who want a general overview and who prefer short, easy-to-read materials. Beyond the Basics patient education pieces are longer, more sophisticated, and more detailed. These articles are written at the 10th to 12th grade reading level and are best for patients who want in-depth information and are comfortable with some medical jargon.

Here are the patient education articles that are relevant to this topic. We encourage you to print or e-mail these topics to your patients. (You can also locate patient education articles on a variety of subjects by searching on “patient info” and the keyword(s) of interest.)

Beyond the Basics topics (see "Patient education: Treatment of ovarian cancer (Beyond the Basics)")

SUMMARY AND RECOMMENDATIONS

Introduction – Epithelial cancers of ovarian, fallopian tube, and peritoneal origin exhibit similar clinical characteristics and behavior and are collectively referred to as epithelial ovarian cancer (EOC). EOC is the most common cause of death among women with gynecologic malignancies and the fifth leading cause of cancer death in women in the United States. Approximately 25 percent of cases are early-stage ovarian cancer, either confined to the ovary (stage I) or confined to the pelvis (stage II). (See 'Introduction' above.)

Selection of patients – Not all patients with early-stage EOC require adjuvant chemotherapy, but chemotherapy should not be omitted unless the patient has been appropriately surgically staged. A decision to administer chemotherapy is largely based upon the stage of disease and tumor characteristics (see 'Selection of patients' above):

For women with completely resected grade 1, stage IA or IB EOC, we suggest observation alone (Grade 2C).

For women with high-risk EOC (defined as stage IC or II, high-grade or clear cell cancers of any stage), we recommend adjuvant chemotherapy (Grade 1B).

We also suggest adjuvant chemotherapy for grade 2 stage I or II EOC (Grade 2C). Observation is an acceptable alternative for stage I EOC provided there are no high-risk factors.

Choice of adjuvant treatment – When adjuvant chemotherapy is used, we suggest a platinum-based two-drug combination chemotherapy regimen rather than single-agent therapy (Grade 2C). We administer paclitaxel plus carboplatin for six cycles. We recognize that the benefit of six cycles may be limited to women with serous cancers or women with stage II disease. It is reasonable to individualize the number of cycles based upon patient risk factors and the tolerance of therapy. In this case, we prefer a minimum of three cycles be administered. (See 'Duration' above.)

Following adjuvant chemotherapy, we suggest observation rather than maintenance chemotherapy given the lack of an overall survival benefit associated with maintenance therapy (Grade 2B). (See 'Maintenance therapy' above.)

Is there a role for intraperitoneal chemotherapy – Combination intraperitoneal and intravenous chemotherapy is experimental for women with early-stage ovarian cancer and should be reserved for clinical trials. (See 'Intraperitoneal chemotherapy' above.)

Unstaged patients – The finding of early-stage EOC is occasionally made during surgery for an emergent (eg, torsion) or a benign (ie, ovarian cystectomy) indication. For these women with unstaged apparent early EOC, we suggest surgical staging because both prognosis and adjuvant treatment options are intimately tied to disease stage (Grade 2A). Any patient who elects not to undergo staging should receive adjuvant chemotherapy. (See 'Unstaged patients' above.)

Post-treatment surveillance – We agree with the post-treatment surveillance recommendations from expert panels, such as the National Comprehensive Cancer Network. (See "Overview of epithelial carcinoma of the ovary, fallopian tube, and peritoneum", section on 'Posttreatment surveillance'.)

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