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    -  Sourati A
    -  Behzadi B
    -  Lesan M
    -  Taghizadeh-Hesary F

 
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ORIGINAL ARTICLE
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A comparison of two chemotherapy regimens in advanced, recurrent, or metastatic salivary gland carcinoma


1 Department of Clinical Oncology, Imam Hossein Educational Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Department of Clinical Oncology, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Submission28-Oct-2020
Date of Decision07-Feb-2021
Date of Acceptance11-Mar-2021
Date of Web Publication29-Jun-2022

Correspondence Address:
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_1226_20

  Abstract 


Background: The efficacy of chemotherapy in locally advanced, recurrent, and metastatic salivary gland carcinomas (LA-R/M SGCs) is still undefined. We aimed to compare the efficacy of two chemotherapy regimens in LA-R/M SGC.
Materials and Methods: This prospective study compared paclitaxel (Taxol) plus carboplatin (TC) versus cyclophosphamide, doxorubicin, plus cisplatin (CAP) regimen in terms of overall response rate (ORR), clinical benefit rate (CBR), progression-free survival (PFS), and overall survival (OS).
Results: Between October 2011 and April 2019, 48 patients with LA-R/M SGCs were recruited. The ORRs of first-line TC and CAP regimens were 54.2% and 36.3%, respectively (P = 0.57). The ORRs in recurrent and de novo metastatic patients were 50.0% and 37.5% for TC and CAP, respectively (P = 0.26). The median PFS of TC and CAP arms were 10.2 and 11.9 months, respectively (P = 0.91). In the subanalysis, patients with adenoid cystic carcinoma (ACC) had longer PFS in the TC arm (14.5 vs. 8.2 months, P = 0.03), irrespective of the tumor grade (low grade: 16.3 vs. 8.9 months, high grade: 11.7 vs. 4.5 months; P = 0.03). The median OS rates were 45.5 and 19.5 months for TC and CAP groups, respectively (P = 0.71).
Conclusion: For patients with LA-R/M SGC, there was no significant difference between first-line TC and CAP in terms of ORR, PFS, and OS.


Keywords: Chemotherapy, locally advanced, metastasis, recurrence, response rate, salivary gland carcinoma, survival
Key Message:

  1. No difference in response rate and survival between TC and CAP regimens in patients with LA-R/M salivary gland carcinoma.
  2. Better PFS in the TC arm in patients with LA-R/M adenoid cystic carcinoma, irrespective of the tumor grade.



How to cite this URL:
Ameri A, Sourati A, Behzadi B, Lesan M, Taghizadeh-Hesary F. A comparison of two chemotherapy regimens in advanced, recurrent, or metastatic salivary gland carcinoma. Indian J Cancer [Epub ahead of print] [cited 2022 Dec 5]. Available from: https://www.indianjcancer.com/preprintarticle.asp?id=348448





  Introduction Top


Salivary gland carcinomas (SGCs) are uncommon neoplasms of the head and neck that constitute 3% of all head and neck tumors.[1] Due to their rarity, limited data are available on the role of chemotherapy in SGCs, and no standard recommendation could be offered in this regard. Chemotherapy could be the single available choice in certain cases, including locally advanced, recurrent, and metastatic (LA-R/M) patients.[2],[3]

Considering the limited clinical evidence, both combinations of paclitaxel (Taxol) plus carboplatin (TC) and cyclophosphamide, doxorubicin, plus cisplatin (CAP) are the most studied regimens of chemotherapy in patients with recurrent and metastatic (R/M) SGC.[2],[3],[4],[5] However, no study has compared the efficacy of these regimens.

Based on these considerations, we examined the efficacy of TC and CAP regimens in terms of response rates and survival in patients with LA-R/M SGC in an educational hospital and a private clinic.


  Materials and Methods Top


Study design and participants

The prospective cohort study design was used. The chemonaïve patients with histologically confirmed locally advanced, recurrent, or de novo metastatic SGCs who were candidates to receive chemotherapy from October 2011 to April 2019 were recruited in the study. In our department, a chemotherapy regimen is chosen based on physician discretion; therefore, sequential randomization without any stratification was applied. By considering the overall response rate (ORR) in the superior arm (i.e., TC) to be 40%,[6] the difference in ORR between TC and CAP 10%,[7] the margin of practical equivalence 2.5%, and the power 80%, the sample size for each arm was equal to 31.[8] However, the slow accrual of participants led to the premature closure of the study with 26 and 22 participants for TC and CAP regimens, respectively.

The recruited patients received TC or CAP regimens in the ratio of 1:1 for three cycles. Subsequently, the response was evaluated by imaging (computed tomography [CT] scan or magnetic resonance imagimg [MRI]) using Response Evaluation Criteria in Solid Tumors (RECIST) Version 1.1 criteria.[9] Demographic and clinical data, including patients' age at diagnosis, gender, primary tumor site, clinical stage at the start of chemotherapy (based on American Joint Committee on Cancer, 7th edition, 2010), treatment of the primary tumor, patterns of recurrence, site of recurrence, and treatment of LA-R/M disease, were collected. The protocol was approved by the institutional review boards and was in accordance with the Helsinki Declaration of 1975 as revised in 1983. All patients provided written informed consent.

Treatment

All patients underwent pretreatment staging, including a complete head and neck exam, CT scan or MRI of the head and neck, chest CT, and/or abdominal CT (if clinically indicated), with the fine-needle aspiration of suspected cervical lymph nodes. The liver function test, complete blood count, and renal function test were obtained at the start of the treatment. Patients assigned to the TC regimen received paclitaxel (175 mg/m2) and carboplatin (AUC (area under the curve) 6 mg/mL per minute) intravenously on Day 1 every 3 weeks for three cycles. Patients assigned to the CAP regimen were administered cyclophosphamide (500 mg/m2), doxorubicin (50 mg/m2), and cisplatin (50 mg/m2) intravenously, starting on Day 1 every 3 weeks for three cycles. Chemotherapy was continued for three more cycles if stable disease or response was achieved in metastatic patients. In the case of disease progression after three cycles, chemotherapy was changed to another (i.e., CAP or TC) regimen. For LA and recurrent locoregional disease, radiotherapy was planned after three cycles of chemotherapy. Chemotherapy was stopped after a maximum of six cycles if no progression happened. Patients were followed up every 3 months with imaging until disease progression. If, on days of chemotherapy, the absolute neutrophil count was lesser than 1,500 cells per microliter or the platelet count was lesser than 50,000 per microliter, the administration of chemotherapies was postponed for a week until recovery above these thresholds. Likewise, dose adjustments were considered based on institutional guidelines. Clinical data were extracted from patients' files to evaluate treatment response and severe toxicities.

End points

ORRs, clinical benefit rates (CBRs), progression-free survival (PFS) rates, and overall survival (OS) rates were evaluated. To calculate these outcomes, we recorded the date of diagnosis, the start date of the first-line chemotherapy, the date of progression, and the date of death or last follow-up. The response rate was defined based on RECIST 1.1 criteria,[9] PFS was defined as the time from the start of first-line chemotherapy to disease progression or death (whichever occurs first), and OS was defined as the time from the start of first-line chemotherapy until death from any cause.

Statistical analysis

To summarize the data, we used frequencies/percentages and means/standard deviations (or medians and ranges) for categorical and continuous variables, respectively. Within the LA-R/M cohort, the patients who received the first-line TC regimen were compared with the CAP group. We used the Chi-square test of independence (or Fisher's exact test) and independent-sample t test to compare categorical and continuous variables, respectively.

Patients with LA-R/M SGCs who received TC or CAP regimen were compared in terms of ORR, CBR, PFS, and OS. Response rates were also secondarily analyzed for salvage chemotherapy, when applicable. Due to different biologies, clinical behaviors, and prognoses, the response rates and survival of patients in the R/M group are reported separately. We used the Kaplan–Meier method to estimate PFS and OS. All analyses were performed using IBM SPSS Statistics, Version 26. The statistical significance level was set at 0.05.


  Results Top


[Figure 1] provides the CONSORT (Consolidated Standards of Reporting Trials) recruitment diagram for the study. Overall, 64 patients were screened for eligibility, 58 patients were randomized, and 48 patients completed the follow-up measures and were analyzed. Thirty patients received the TC regimen, and 28 patients received the CAP regimen. Two patients allocated to the CAP group received TC at the treating physician's discretion because of their cardiac disease. Five patients in each group switched to another regimen after progression. Patients who received salvage chemotherapy were limited because of referring to local oncology centers for the continuing treatment, unfit for the salvage chemotherapy, and expressing unwillingness to continue the treatment. The most common pathological diagnosis (68.5%) was adenoid cystic carcinoma (ACC). Carcinoma ex pleomorphic adenoma, acinic cell carcinoma, and adenocarcinoma not otherwise specified (A-NOS) were more common pathologies, inter alia. Thirty-six (75%) patients were categorized in the R/M group.
Figure 1: CONSORT flow diagram of study recruitment

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The baseline characteristics of all the patients are summarized in [Table 1]. In this study, there was no significant difference between the arms in terms of gender, age at diagnosis, histology, primary tumor site, and clinical stage. Likewise, the distributions of patients in either group of chemotherapy regimens were similar according to the clinical setting. For both groups, the median number of chemotherapy cycles was three. The median follow-up time was 56.4 months (range 5.3–97.1 months).
Table 1: Clinical characteristics of the patients

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The ORRs of first-line TC and CAP regimens were 54.2% and 36.3%, respectively (P = 0.57). In the R/M group, 20 and 16 patients received TC and CAP regimen, respectively, as a first line. Accordingly, ORRs were 50.0% and 37.5%, respectively (P = 0.26). The entire report of the first-line and salvage chemotherapy of all patients is presented in [Table 2].
Table 2: The chemotherapy regimens and response rates

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In patients with ACC who received first-line TC or CAP regimens (18 and 15 patients, respectively), the ORRs were 43.7% and 31.2%, respectively (P = 0.46). Accordingly, for patients with non-ACC pathology, the ORRs were 75.0% and 66.6% for first-line TC and CAP regimens (8 and 7 patients), respectively (P = 0.20). The metastatic patient who had a complete response to the CAP regimen had carcinosarcoma of the parotid gland with metastasis to the lung and liver. The patient who experienced complete response in the nonmetastatic group received induction chemotherapy with TC regimen before radiotherapy for his mucoepidermoid carcinoma of the parotid gland. [Table 3] compares responders and nonresponders to chemotherapy in different clinical settings. It shows that responders to chemotherapy had marginally significant better median survival (45.5 vs. 16.3 months, 95% confidence interval (CI; 4.4, 86.7), P = 0.09). This difference was also true for patients in the R/M group (45.5 vs. 16.3 months, 95% CI (15.2, 22.7), P = 0.13). Evaluation of patients in the LA group was not available due to the fixed right-censoring of all four patients in this group.
Table 3: The response rates and median survivals

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Of the 13 patients who progressed after first-line TC, 3, 1, and 9 patients had local progression, locoregional recurrence, and metastasis, respectively. Among 15 patients who progressed after first-line CAP, 5, 2, and 8 patients had local progression, locoregional recurrence, and metastasis, respectively (P = 0.68). The median survival rates of 13 and 15 patients who progressed after first-line TC or CAP were 22.5 and 19.5 months, respectively (95% CI (12.1, 27.9), P = 0.93). Of the 13 patients who progressed after TC, the median survival for patients who received CAP (n = 5) as a salvage was 22.5 months (since the start of the study) compared with 16.3 months for patients who received no salvage chemotherapy (n = 8; 95% CI (13.1, 31.9), P = 0.58). Of the 15 patients who progressed after CAP, four patients treated with TC had a median survival of 12.2 months while the median survival of other patients who did not receive salvage TC was 19.5 months (95% CI (15.3, 23.7), P = 0.24).

The median PFS and OS rates of all patients who received first-line TC and CAP were 10.2 versus 11.9 months (95% CI [6.7, 13.7], P = 0.91) and 45.5 versus 19.5 months (95% CI (13.2, 77.8), P = 0.71), respectively. The median PFS and OS rates of patients with recurrent or de novo metastasis who received TC or CAP as the first-line chemotherapy were 9.3 versus 11.9 months (95% CI [5.9, 14.5], P = 0.76) and 45.5 versus 19 months, respectively (95% CI (0.0, 41.8), P = 0.59) [Figure 2]. The PFS and OS rates of patients with LA SGCs could not be compared because of small numbers.
Figure 2: Kaplan–Meier curves of progression-free survival (a) and overall survival (b) for patients with locally advanced, recurrent, or metastatic salivary gland carcinomas receiving first-line TC or CAP regimens. Kaplan–Meier curves of progression-free survival (c) and overall survival (d) for patients with recurrent or metastatic salivary gland carcinomas receiving first-line TC or CAP regimens

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[Figure 3] shows the comparison between ACC and non-ACC pathologies in terms of OS. Regarding the TC regimen, the difference between ACC and non-ACC in OS approached the borderline of significance (95% CI (10.2, 80.8), P = 0.09). However, the median OS rates of patients with ACC and non-ACC pathologies treated with CAP were almost similar (19.5 vs. 19.0 months, 95% CI (0.0, 50.5), P = 0.92).
Figure 3: Kaplan–Meier curves of overall survival for patients with locally advanced, recurrent, or metastatic salivary gland carcinomas with ACC or non-ACC pathologies receiving first-line TC (a) or CAP (b)

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Patients with ACC disease had significantly longer median PFS in the TC arm (14.5 vs. 8.2 months, 95% CI [1.3, 16.5], P = 0.03). However, there was no significant difference in OS (57.7 vs. 35.1 months, 95% CI (35.2, 68.1), P = 0.34) [Figure 4]a and [Figure 4]b. The subgroup analysis revealed that PFS benefit for the TC regimen included both low-grade (median PFS: 16.3 vs. 8.9 months, 95% CI [2.7, 15.2]) and high-grade ACC (mean PFS: 11.7 vs. 4.5 months, 95% CI [3.6, 15.1]; P = 0.031) [Figure 4]c and [Figure 4]d.
Figure 4: Kaplan–Meier curves of progression-free survival (a) and overall survival (b) for adenoid cystic carcinoma (ACC) patients receiving first-line TC or CAP regimens. Kaplan-Meier curves of progression-free survival of low-grade (c) and high-grade (d) ACC patients receiving first-line TC or CAP regimens

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The 3- and 5-year OS rates of all patients in the TC and CAP groups were 28% versus 18.2% (95% CI (11.7, 19.4), P = 0.69) and 8.3% versus 4.5% (95% CI (12.3, 18.8), P = 0.60), respectively. The 3- and 5-year OS rates of patients in R/M group receiving TC and CAP were 23.5% versus 11.1% (95% CI (11.2, 19.1), P = 0.66) and 5.9% versus none (95% CI (11.2, 19.1), P = 0.59), respectively. Both chemotherapy regimens were well-tolerated with a few toxicities as follows. No Grade 5 toxicity was reported. The hematologic toxicity was frequently reported in both groups; however, Grade 4 toxicity was 7% and 11% in patients receiving TC and CAP, respectively. Grades 2 and 3 peripheral neuropathy was reported in 19% and 13% of patients receiving TC, respectively.


  Discussion Top


The standard chemotherapy regimens have not been established for patients with LA-R/M SGCs. Most of our knowledge is based on small and single-arm studies.[2],[10],[11],[12],[13],[14] This may be due to the rarity and pathologic heterogeneity of SGCs. This study compared the effectiveness of TC and CAP regimens in patients with LA-R/M SGC, as the most commonly reported regimens in LA-R/M SGCs.[2],[3],[7],[10] To the best of our knowledge, no study has compared the effectiveness of TC and CAP in patients with LA-R/M SGCs. In this cohort study, we compared these regimens in terms of response rate and survival.

Our study demonstrated a moderate response to first-line chemotherapy. While statistically nonsignificant, the ORR was greater for the first-line TC compared with CAP in LA-R/M (54% vs. 36%). This was also true for LA and R/M subgroups (66% vs. 33% and 50% vs. 37.5%, respectively). However, the ORR of salvage chemotherapy and CBR of first-line and salvage chemotherapy showed mixed results. These results may have been confounded by the small number of patients who received salvage chemotherapy and diverse histologies. Furthermore, our results showed that the response rate could potentially predict survival.

The median OS was greater for patients with R/M who received TC compared with CAP (45.5 vs. 19 months). However, this large difference was statistically nonsignificant. This may be due to the small number of patients. As demonstrated in [Figure 2]d, the marked difference between the OS of patients with R/M disease is denoted after the second year. However, this difference was statistically nonsignificant.

In comparison with the CAP regimen, patients who received TC experienced less recurrence (68% vs. 50%) with a longer median OS (19.5 vs. 22.5 months). Notably, patients who progressed after TC and received salvage CAP had longer survival times, while salvage TC for the progressive disease after CAP yielded the opposite result. However, due to the small number of patients, the results are not yet conclusive.

Several small and retrospective studies have reported the response rates and survival of patients with LA-R/M SGC who received TC and CAP regimens. A case series of patients with recurrent SGCs reported an ORR of 14% and an OS of 12.5 months for the TC regimen.[10] In 2019, Okada et al. reported clinical outcomes of 24 patients with LA-R/M who received docetaxel plus carboplatin regimen, demonstrating an ORR of 42% and a median OS of 26.4 months.[13] Our results for the TC regimen were comparable with Okada et al.'s study. A similar retrospective study by Debaere et al. conducted with 15 patients with R/M SGC who received the CAP regimen showed an ORR of 60%, with one complete response and eight partial responses, and a median OS of 15.1 months.[3]

In comparison with our results, greater ORR and shorter median OS in Debaere et al.'s study may have been related to more CAP cycles on average (3.5 vs. 5.4 cycles) and a lower percentage of patients with ACC (68% vs. 40%). We found two related prospective studies in the literature. An Italian Phase II study compared vinorelbine plus cisplatin with vinorelbine alone in 36 patients with recurrent SGC with an ORR of 31.8% and 20%, respectively, showing a trend to improved OS (P = 0.058) for the combination arm.[15] In 2019, Viscuse et al. compared the androgen deprivation therapy with platinum-based chemotherapy, reporting a similar OS of 25 months (95% CI [0.23, 1.28], P = 0.16).[16] This study was limited to patients with salivary duct carcinoma (SDC) and A-NOS. However, our study did not include any patients with SDC and included only three patients with A-NOS. Therefore, the clinical outcomes of Viscuse et al.'s study may not be comparable with ours. Another limitation of Viscuse et al.'s trial was the diversity of chemotherapy regimens. Our study went beyond the previous reports by comparing the most reported chemotherapy regimens in terms of response rates and survival.

In a subgroup analysis, patients with non-ACC pathology had a better response rate to TC in comparison with ACC (75% vs. 43%). This finding is consistent with previous studies.[2],[14] Improved RR was also seen in patients with non-ACC treated with the CAP regimen (66% vs. 31%). Surprisingly, higher response rates to TC did not translate into a survival benefit in the non-ACC group in comparison with ACC. This may have been due to the small number of patients and the distinct biologic behavior of ACC with a slower growth rate.[17],[18] Contrary to the Nakano et al.'s study, we found that ACC patients had significantly better PFS in the TC arm (14.5 vs. 8.2 months, P = 0.03),[6] irrespective of the tumor grade. However, this difference did not translate to a better OS.

The limitations of this study should be considered when interpreting the results. First, conducting sequential randomization resulted in several differences between the clinical features in each group. Second, the small sample size could have biased the results. To resolve this critical issue, large randomized clinical trials are necessary.

Despite these limitations, the present study was the first to compare the efficacy of two common chemotherapy regimens in patients with LA-R/M salivary gland cancer. Our study can be potentially used in the design of larger clinical trials designed to determine the efficacy of chemotherapy in various subtypes of SGCs.

In conclusion, this study revealed no significant difference between TC and CAP regimens in terms of ORR, PFS, and OS in patients with LA-R/M SGCs regardless of histology subtype. However, it suggested a PFS benefit for the TC regimen in patients with ACC. Further studies with large sample sizes are needed to confirm these findings.

Data availability

The data sets used during the current study are available from the corresponding author on request.

Author contributions

A.A. and A.S. designed the research; B.B. and M.L. acquired the data; A.A., B.B., and M.L. performed the research; F.T.H. analyzed the data; and A.A. and F.T.H. wrote the paper. All authors gave final approval of the version to be submitted.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Acknowledgments

The authors would like to express their gratitude to the staff of the Imam Hossein Educational Hospital, Tehran, Iran. Finally, the authors would like to express their gratitude to the physicians and nurses all around the world who are putting their best efforts to treat patients suffering from cancer.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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