Retrospective Study of the Efficacy of Docetaxel/Carboplatin Combination Therapy as Postoperative Adjuvant Chemotherapy for Nonsquamous Cell Carcinoma of the Cervix

doi:10.21203/rs.3.rs-2849912/v1

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Retrospective Study of the Efficacy of Docetaxel/Carboplatin Combination Therapy as Postoperative Adjuvant Chemotherapy for Nonsquamous Cell Carcinoma of the Cervix

https://doi.org/10.21203/rs.3.rs-2849912/v1

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Journal Publication

published 16 Aug, 2023

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Objective

Optimal adjuvant chemotherapy for nonsquamous cervical carcinoma has not yet been established. This study investigated the efficacy and safety of docetaxel/carboplatin (DC) for early stage nonsquamous cell cervical carcinoma after radical hysterectomy (RH).

Methods

We evaluated 157 patients with stage IB-IIB nonsquamous cervical carcinoma with intermediate risk and high risk treated at our institution with DC after type II or III RH from 2007 to 2021. Patients received docetaxel (60–70 mg/m²) and carboplatin (area under the curve 5–6) every 3 weeks for six cycles. The primary endpoint was 2-year recurrence-free survival (RFS) and the secondary endpoint was adverse events (AEs).

Results

There were 106 intermediate-risk and 51 high-risk patients. The high-risk patients included 11 with positive parametrial involvement, 20 with pelvic lymph node metastases, and 20 with both parametrial involvement and pelvic lymph node metastases. The 2-year RFS rates for intermediate- risk, high-risk, and positive pelvic lymph nodes were 94.8% (95% confidence interval [CI], 87.9–97.8), 80.1% (95% CI, 64.1–89.5), and 74.5% (95% CI, 55.4–86.4), respectively. Sixteen patients had recurrence, including local recurrence (n = 6), distant metastasis (n = 9), and local and distant metastasis (n = 1). Hematologic toxicity was the most frequent AE, especially leukopenia and neutropenia. Nausea and constipation were the most frequent nonhematologic toxicities.

Conclusion

DC therapy at our institution showed good 2-year RFS, and postoperative adjuvant therapy with DC therapy is suggested as a useful strategy for patients with nonsquamous cervical carcinoma.

cervical cancer

nonsquamous carcinoma

adjuvant chemotherapy

The incidence and mortality rates of cervical cancer in developed countries are decreasing due to cervical cancer screening and vaccination against cervical cancer. The number of cervical cancer patients in Japan in 2018 was 10,978, with a flat, not decreasing, annual trend [1]. In terms of histological types, squamous cell carcinoma accounts for approximately 70%, and nonsquamous cell carcinomas, such as adenocarcinoma and adenosquamous cell carcinoma, account for approximately 30% [2]. In terms of advanced stages, stage I and II early stage cancers account for approximately 75% of cases [3]. Comparing squamous with nonsquamous cell carcinoma of the cervix, many reports indicate that nonsquamous cell carcinoma has a worse prognosis [4]. Nonsquamous carcinoma is generally considered less radiosensitive than squamous carcinoma [5].

The main treatment options for early-stage cervical cancer are surgical and radiation therapy combined with chemotherapy (CCRT). In Japan, the selection rate for surgical therapy is higher than in other countries, with 63–65% of the patients reported to have undergone surgical therapy [6]. When surgical therapy is performed for early-stage cervical cancer, patients are classified as low-, intermediate-, or high-risk for postoperative recurrence based on clinical and pathological factors [7]. The standard postoperative treatment is follow-up for low-risk patients, radiation therapy (RT) or CCRT for intermediate-risk patients, and CCRT for high-risk patients. In Japan, however, chemotherapy (CT), a systemic treatment that can also be remotely controlled, has replaced RT because surgical therapy provides adequate local control, and RT causes serious and irreversible complications, such as bowel obstruction and intractable lymphedema [8]. Statistics from the Japanese Society of Obstetrics and Gynecology report that RT is used as a postoperative treatment for cervical cancer in approximately 5% of cases, CCRT in about 10%, and CT in about 15% [6]. Some retrospective studies have reported that postoperative CT is as effective as postoperative RT [9–10]. Many centers actively choose CT for nonsquamous cell carcinomas because they are less radiosensitive than squamous cell carcinomas. In a multicenter study, Shimada et al. reported no difference in survival rates among the postoperative RT, CCRT, and CT groups for nonsquamous carcinoma of the cervix, suggesting that CT may be useful as an adjuvant therapy after surgery [11]. Sato et al. reported a safety study of taxane/carboplatin combination therapy as postoperative therapy for early stage nonsquamous cell carcinoma, comparing progression-free survival between paclitaxel/carboplatin (TC) combination therapy and docetaxel/carboplatin (DC) combination therapy, and although not significantly different, the 2-year progression-free survival rate was 80% for DC versus 50% for TC, suggesting that DC may be a useful strategy for postoperative treatment of nonsquamous carcinoma of the cervix [12]. There are no randomized controlled trials of postoperative adjuvant chemotherapy for nonsquamous cell carcinoma, and there is no evidence-based standard regimen. Therefore, we have based our DC therapy on the results of a retrospective study by Sato et al., however, the number of reported patients receiving DC therapy is small (15 patients). In the present study, we investigated the efficacy and safety of DC therapy as an adjuvant therapy in patients who underwent radical hysterectomy (RH) for early-stage nonsquamous cell carcinoma and were diagnosed as having intermediate or high risk for postoperative recurrence.

・Study design and patient population

This was a retrospective cohort study of patients with stage IB–IIB cervical cancer according to the International Federation of Gynecology and Obstetrics (FIGO) 2008 classification who underwent type II or III RH [13] between April, 2007 and March, 2021. The eligibility criteria for the study were histologically confirmed nonsquamous carcinoma and RH followed by DC therapy. The main exclusion criteria were neuroendocrine carcinomas and positive resection margins. The following definitions were based on the pathological recurrence risk factors indicated in the Japanese guidelines for the treatment of cervical cancer [9]. Intermediate risk for postoperative recurrence: mass ≥ 4 cm, cervical stromal invasion ≥ 1/2, positive vascular-lymphatic involvement, high risk for postoperative recurrence, positive parametrial involvement, and positive pelvic lymph node metastasis. This study was approved by the Institutional Review Board (IRB No. 2021-GB-021).

・Treatment and Assessment

All patients underwent type II or III RH and systematic pelvic lymph node dissection. Indications for laparoscopic surgery were tumor diameter < 4 cm, stage IB1 or IIA1 by FIGO classification, meeting the institutional criteria for laparoscopic uterine malignancy surgery (limited to cervical cancer), and performed by a board-certified surgeon. A vaginal cuff was created to prevent tumor cell spillage, and a collection bag was used [14].

The patients with intermediate or high risk received docetaxel (60–70 mg/m²) and carboplatin (dose based on area under the curve (AUC) 5–6) intravenously on day 1. This cycle was repeated every 3 weeks for a maximum of six cycles. Treatment postponement, dose reduction, or discontinuation was determined by a gynecologist skilled in CT based on the protocol established at our institution. After treatment completion, patients were examined every 3 months, and computed tomography scans were performed every 12 months to evaluate for recurrence. A comprehensive diagnosis was made when subjective symptoms or clinical signs of suspected recurrence were present [12].

・Endpoints

Recurrence-free survival (RFS) was defined as the time from the date of surgical therapy to the date of recurrence or death. Overall Survival (OS) was defined as the date of surgical therapy to the date of the last confirmed survival or the date of death. The primary endpoint was the 5-year RFS rate. The secondary endpoint was adverse events (AEs). Recurrence was assessed radiographically or histologically according to the Response Evaluation Criteria in Solid Tumors, version 1.1. In addition, the sites of recurrence and treatment were recorded. Local recurrence was defined as a recurrence at or near the vaginal stump. AEs were evaluated based on the National Cancer Institute's Common Terminology Criteria for AEs, version 5.0.

・Statistical analysis

RFS and OS proportions were estimated using the Kaplan–Meier method. The Greenwood's formula was used to calculate the confidence intervals (CI) for survival time. EZR version 1.55 [15] was used for statistical analyses. EZR extends the functionality of R and R Commander.

・Patient Characteristics

A CONSORT diagram of this study is shown in Fig. 1. Between April, 2007 and March, 2021, 219 patients diagnosed with stage IB-IIB nonsquamous carcinoma of the cervix (excluding special types) and at intermediate or high risk of postoperative recurrence underwent type II or III RH, 157 of whom received DC therapy. The patient characteristics are shown in Table 1. The median age of the patients was 44 years (range, 17–70 years). Stage IB disease accounted for 82% of the patients. As for surgical procedures, laparotomy was used in 119 and laparoscopy in 38 patients. Postoperative pathology revealed 106 and 51 patients at intermediate and high risks of postoperative recurrence, respectively. Of those at high risk, 11 had only positive parametrial involvement, 20 had only positive pelvic lymph node metastasis, and 20 had both positive parametrial involvement and positive pelvic lymph node metastasis.

・Outcomes

The median observation period for intermediate- and high-risk postoperative recurrence was 65 (range, 1–145) and 44 months (range, 0–135), respectively, with 2-year RFS rates of 94.8% (95% CI, 87.9–97.8) and 80.1% (95% CI, 64.1–89.5), and 5-year RFS rates of 92.5% (95% CI, 84.9–96.4) and 76.3% (95% CI, 58.9–87.1), respectively (Fig. 2). The 2-year OS rates for intermediate and high risk of postoperative recurrence were 97.9% (95% CI, 91.9–99.5) and 97.4% (95% CI, 83.2–99.6), respectively, and the 5-year OS rates were 97.9% (95% CI, 99.1–99.5) and 89.5% (95% CI, 74.3–95.9), respectively (Fig. 3). The 2-year RFS rates for only positive parametrial involvement, only positive pelvic lymph node metastasis, and positive parametrial involvement with positive pelvic lymph node metastasis were 100%, 82.6% (95% CI, 55.2–94.1) and 65% (95% CI, 35.1–83.7), respectively (Fig. 4). The 2-year RFS rate for positive pelvic lymph nodes was 74.5% (95% CI, 55.4–86.4). Recurrence cases are shown in Table 2. Sixteen patients had recurrence, with local recurrence in six patients, distant metastasis in nine patients, and local recurrence and distant metastasis in one patient. Of the patients with local recurrence only, five patients with pelvic mass or pelvic lymph node metastasis underwent CCRT, one underwent resection of the recurrent tumor, and two were still alive at last follow-up.

The site of distant metastasis was the lungs in four patients, the lungs and lymph nodes in one, the liver in one, the liver and lymph nodes in one, the liver and lungs in one, peritoneal dissemination and multiple lymph nodes in one, and pleural dissemination in one. In the treatment of cases with distant metastasis, three patients underwent resection of the recurrent tumor, five received chemotherapy, and two received palliative therapy, six of whom were alive at last follow-up. Overall, of the 16 patients with recurrent disease, 8 died of the disease.

・AEs

The AEs are shown in Table 3. The major AEs were hematologic toxicities: leukopenia (91.7%), neutropenia (91.7%), and anemia (78.9%). Nausea (85.3%) and constipation (66.8%) were major nonhematologic toxicities. Serious AEs of grade 3 or higher were febrile neutropenia (14%), anemia (10.8%), and diarrhea (3.3%). Early discontinuation due to serious AEs included an allergic reaction in one patient, hepatic dysfunction in one patient, and peripheral neuropathy in one patient. Docetaxel or carboplatin was reduced or postponed in 49 (31%) and 45 (28.6%) patients, respectively. No treatment-related deaths occurred during this period.

In this study, we investigated the efficacy and safety of DC therapy as a postoperative treatment for nonsquamous cell carcinoma of the cervix.

The Southwest Oncology Group (SWOG) 8797 study demonstrated the usefulness of CCRT as adjuvant therapy for cervical cancer patients at high risk of postoperative recurrence [16]. Based on these results, CCRT is recommended for patients at high-risk of postoperative recurrence in Japan. However, CCRT after RH is associated with AEs that are difficult to resolve. Acute complications include myelosuppression, diarrhea, nausea, and cystitis, as well as grade 3 or higher AEs [17]. Late complications can also occur, such as radiation enteritis, radiation cystitis, bowel obstruction, lower extremity edema, and secondary cancers [18–19]. Long-term reduction in patient quality of life due to severe late effects after treatment is a major problem in postoperative CCRT [20–22].

Because distant metastasis is generally considered to affect survival, both local and distant control is necessary. Therefore, in Japan, surgical therapy, which provides adequate local control, and CT, which has less severe and irreversible complications than RT in postoperative adjuvant therapy, have been used. However, when CT is selected as adjuvant therapy, it is important that surgical therapy be performed by a gynecologic oncologist at a cancer treatment center hospital because of the importance of adequate local control in surgical therapy. Matsuo et al. reported that a high-volume center is an important prognostic factor for RH in early-stage cervical cancer, and that the local recurrence rate is lower when surgical therapy is performed in a high-volume center [23]. Our hospital is a high-volume center with the largest number of RH in Japan, and five patients (9.8%) at a high risk of postoperative recurrence had local recurrence. Compared with the local recurrence rate of 8.6% in the group that underwent postoperative CCRT, as reported in the SWOG8797 study [16], this suggests that the curative effect of surgical therapy is high at our hospital. Therefore, we suggest that postoperative adjuvant chemotherapy may be an option in institutions where local control with surgical therapy is adequate.

Ongoing randomized phase II trials include the Radiation Therapy Oncology Group (RTOG) 0724 trial [24] and the Japan Gynecologic Oncology Group (JGOG) 1082 trial [25]. The RTOG0724 trial evaluates whether adjuvant CT after CCRT prolongs disease-free survival compared with CCRT alone in cervical cancer patients at a high risk of postoperative recurrence. The JGOG 1082 trial compared postoperative RT with postoperative chemotherapy in patients undergoing RH for stage IB-IIB cervical cancer. Based on the results of these trials, we expect that CT will be useful as an adjuvant therapy after surgery. Nonsquamous cell carcinoma of the cervix is often reported to have a poorer prognosis than squamous cell carcinoma of the cervix and is considered less radiosensitive [5]. Shimada et al. conducted a retrospective study comparing the efficacy of RT (including CCRT) versus CT versus the combination of RT and CT as adjuvant therapy in patients with cervical nonsquamous cell carcinoma at high risk of postoperative recurrence [11]. The 5-year OS rates were 70.9%, 79.2%, and 66.2% in the RT, CT, and RT and CT groups, respectively, suggesting the efficacy of CT as an adjuvant therapy for cervical nonsquamous cell carcinoma. However, as mentioned above, the efficacy of CT as an adjuvant therapy has only been studied retrospectively, and needs to be studied prospectively.

In the JGOG1067 study [26], a phase II study of irinotecan/nedaplatin combination therapy in squamous cell carcinoma of the cervix, 62 patients at high risk of postoperative recurrence of early-stage cervical cancer with positive pelvic lymph nodes were treated, and favorable results were reported, with a 2-year RFS rate of 87% and a 5-year RFS rate of 77%. Based on these results, this regimen has been used for squamous cell carcinoma of the cervix in some institutions. However, since nonsquamous cell carcinoma of the cervix is not eligible, no prospective studies have examined effective regimens for nonsquamous cell carcinoma of the cervix. Takekida et al. conducted a phase II study using DC therapy for advanced or recurrent cervical cancer and reported a response rate of 67.9%for nonsquamous cell carcinoma of the cervix [27]. Based on these results, Sato et al. conducted a safety study using a taxane/carboplatin combination as adjuvant CT in patients with stage IB-IIB cervical nonsquamous cell carcinoma after RH who were at a high risk of postoperative recurrence [12]. This study suggests that DC therapy is more effective than TC therapy. Comparing the Kaplan-Meier curves of the 15 patients treated with DC therapy reported in that study with the results of our study, the 2-year RFS rate in that study was 80% and that in our study was 80.1%, as shown in Supplementary Fig. 1. These results suggest the efficacy of DC therapy for nonsquamous cell carcinoma of the cervix, and further prospective studies are required.

Grade 4 neutropenia (66.2%) and grade 3 leukopenia (57.9%) were the most frequent hematological toxicities, suggesting a risk of febrile neutropenia and dose reduction, postponement, or interruption. Dose reductions occurred in 33 patients (21%) with grade 3–4 hematologic toxicity and in 16 patients (10.1%) with nonhematologic toxicity, with most dose reductions attributed to grade 3–4 hematologic toxicity. Hematologic toxicities should be adequately managed when administering DC therapy, and prophylactic granulocyte colony stimulating factor (G-CSF) products may be necessary to maintain relative dose intensity.

The Gynecologic Oncology Group (GOG) 92 trial is a randomized controlled trial investigating intermediate risk for postoperative recurrence [28]. In this study, the effect and risk of RT alone were evaluated in patients with stage IB pelvic lymph node-negative cervical cancer who had two or more of the following three risk factors for postoperative recurrence: stromal invasion greater than 1/3, vascular-lymphatic involvement, and cervical enlargement. The 2-year and 5-year RFS rates of the RT group were 88% and 82%, respectively. The 2-year and 5-year RFS rates in our study were 94.8% and 92.5%, respectively, which were higher to those in the RT alone group compared to the results of that study. Although there are differences in patient background and study design, these results for non-squamous cell carcinoma of the cervix, which is reported to have a worse prognosis than squamous cell carcinoma of the cervix, suggest that CT is effective as adjuvant therapy for patients at intermediate risk of postoperative recurrence. In addition, when combined with the 100% 2-year RFS rate for only positive parametrial involvement in this study of factors for a high risk of postoperative recurrence, it may be necessary to consider more individualized adjuvant therapy selection by level of risk.

This was a single-arm retrospective study and was not compared with postoperative RT or CCRT. Therefore, it cannot be determined whether CT is more effective than RT or CCRT, which is the standard of care. However, postoperative DC therapy may be an option for nonsquamous carcinoma of the cervix. In addition, the use of novel agents, such as bevacizumab and pembrolizumab, for metastatic or recurrent cervical cancer has been shown to prolong survival. In the future, it is necessary to select more effective regimens using novel agents for postoperative adjuvant therapy.

In this study, we evaluated the efficacy and safety of DC as an adjuvant therapy for nonsquamous carcinoma of the cervix. Further prospective and retrospective studies are needed because there is no evidence to support the choice of CCRT, RT, or CT as a postoperative adjuvant therapy for cervical nonsquamous cell carcinoma.

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Tables 1 to 3 are available in the Supplementary Files section.

SupplementalFigurecervicalcancerDC20230423.pptx
Supplemental Fig 1 Comparison of Kaplan-Meier curves of DC therapy for high risk of postoperative recurrence in Sato et al. and our study
TablecervicalcancerDC20230423.pptx
Table 1Patient characteristics (N = 157) Table 2Patterns of recurrence, disease status, and prognosis (N = 16) Table 3Adverse events suspected to be study-related (N = 157)

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Journal Publication

published 16 Aug, 2023

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Editorial decision: Major revisions
20 May, 2023
Reviewers agreed at journal
25 Apr, 2023
Reviewers invited by journal
25 Apr, 2023
Editor assigned by journal
24 Apr, 2023
First submitted to journal
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Retrospective Study of the Efficacy of Docetaxel/Carboplatin Combination Therapy as Postoperative Adjuvant Chemotherapy for Nonsquamous Cell Carcinoma of the Cervix

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