Research ArticleClinical Studies

Concurrent Chemoradiotherapy With Docetaxel, Cisplatin, and 5-Fluorouracil (DCF-RT) for Patients With Potentially Resectable Esophageal Cancer

MAKOTO SAKAI, MAKOTO SOHDA, SHINTARO UCHIDA, ARISA YAMAGUCHI, TAKAYOSHI WATANABE, HIDEYUKI SAITO, YASUNARI UBUKATA, NOBUHIRO NAKAZAWA, KENGO KURIYAMA, AKIHIKO SANO, HIROOMI OGAWA, TAKEHIKO YOKOBORI, SHIN-EI NODA, TATSUYA OHNO, KEN SHIRABE and HIROSHI SAEKI
Anticancer Research October 2022, 42 (10) 4929-4935; DOI: https://doi.org/10.21873/anticanres.15999

Abstract

Background/Aim: We evaluated the long-term outcome of docetaxel, cisplatin, and 5-fluorouracil as combination chemoradiotherapy (DCF-RT) for patients with potentially resectable esophageal cancer (EC) in clinical settings. Patients and Methods: Twenty-eight patients with potentially resectable thoracic EC were included in this study. Chemotherapy consisted of intravenous docetaxel at 50 mg/m2 (day 1), CDDP at 60 mg/m2 (day 1), and 5-FU at 600 mg/m2 (days 1 to 4), repeated every four weeks for two cycles along with radiotherapy (60 Gy in 30 fractions). Potentially resectable esophageal cancer was defined as clinical stage (cStage) I, II, III, and IV with supraclavicular lymph node metastasis [M1(Lym)]. Results: The overall complete response (CR) rate was 88.5%. The 5-year overall survival (OS) rates for cStage I, cStage II-III, and IV [M1(lym)] patients were 79.5%, 76.2%, and 50.0%, respectively. The most frequent grade 3 or 4 acute toxicities were leucopenia (85.7%), neutropenia (78.5%), and febrile neutropenia (FN) (21.4%). The rate of any grade 3 or 4 late toxicity was 7.7%. Conclusion: DCF-RT demonstrated a satisfactory CR rate and OS with a higher rate of FN for potentially resectable thoracic EC patients. Prophylactic treatment with granulocyte-colony-stimulating factor and antibiotics may be appropriate supportive care for patients undergoing DCF-RT.

Key Words:

Esophageal cancer (EC) is the sixth leading cause of death from cancer and the eighth most common cancer worldwide. Five-year survival ranges from 15%-25% (1). Concurrent chemoradiotherapy (CRT) is the standard therapy for unresectable esophageal cancer and is also recognized as an option for resectable cancer. Definitive CRT is a treatment option for patients who refuse or cannot tolerate surgery (2). Neoadjuvant chemotherapy followed by surgery (NAC-S) represents the standard treatment for patients with clinical stage (cStage) II/III esophageal squamous cell carcinoma (ESCC) in Japan. In the JCOG1406-A study, a comparison between NAC-S and definite CRT for stage II/III ESCC showed that the 5-year overall survival (OS) was better in the NAC-S group than the CRT group (54.8% and 38.3%, respectively) (3). To date, the most commonly employed regimen with concurrent radiation therapy for esophageal cancer was a combination of cisplatin and 5-fluorouracil (CF) (4-6); however, the outcome of this regimen remains unsatisfactory in terms of local control and survival rate (6-8). Thus, RT with more effective regimens is needed as a treatment option for patients with resectable esophageal cancer that have contraindications to surgery or for esophageal preservation. We previously reported that docetaxel, cisplatin, and 5-fluorouracil as combination chemoradiotherapy (DCF-RT) led to a high complete response (CR) rate and favorable prognosis compared with CF-RT for advanced esophageal cancer (9). Several studies also reported the efficacy of the DCF regimen for EC (10-12). However, the efficacy and safety of DCF-RT for resectable EC remain unclear. This study aimed to explore the efficacy, safety, and long-term outcomes of DCF-RT for potentially resectable thoracic EC.

Patients and Methods

Patients. This retrospective study was approved by the Ethics Committee of the Graduate School of Medicine, Gunma University (Protocol number HS2019-319). Informed consent was obtained by an opt-out on the website. We usually perform DCF-RT for patients with unresectable EC or those who refuse or cannot tolerate surgery unless they have severe myelosuppression or renal dysfunction. Between July 2008 and December 2017, 99 patients underwent DCF-RT for primary thoracic EC at our institute. This study defined potentially resectable esophageal cancer as cStage I, II, III, and IV with supraclavicular lymph node metastasis [M1(Lym)]. Of these 99 patients, 28 patients with potentially resectable EC were enrolled. Hospital patient records were reviewed for tumor characteristics and patient outcomes. The tumor stage and disease grade were classified according to the 8th edition of the TNM classification of the International Union Against Cancer (13). The tumor stage was determined conventionally using computed tomography (CT) and positron emission tomography (PET)-CT of the neck, chest, and abdomen, and endoscopic ultrasonography, endoscopy, and esophagography.

Treatment. Patients received concurrent radiotherapy and chemotherapy for six weeks after the diagnostic procedures. Chemotherapy consisted of intravenous docetaxel (50 mg/m2) on day 1, intravenous CDDP (60 mg/m2) on day 1, and intravenous 5-FU (600 mg/m2) on days 1 to 4 (DCF), repeated every four weeks for two cycles. Details of the radiotherapy regimen were previously described (9).

Response evaluation. Standard clinical measurements and radiological examinations were used to assess the tumor response according to RECIST criteria. The treatment response of the primary lesion (non-target lesion) was evaluated according to the Japanese Classification of Esophageal Cancer, 11th edition (14). Details of response evaluation were previously described (9). Response evaluation was performed except in two cases of insufficient examination.

Toxicity. Toxicities were assessed using the Common Terminology Criteria for Adverse Events v4.0. An adverse event developing more than 90 days after CRT was defined as late toxicity. Late toxicity evaluation was performed except in two cases with missing data.

Follow-up. Patients were assessed every three months after treatment completion for the first 2 years and every 6 months thereafter. CR was confirmed by endoscopy, biopsy specimens, CT, and PET-CT.

Statistical analysis. Locoregional failure was defined as the persistence or recurrence of the primary tumor or regional lymph nodes. Distant failure was defined as metastasis to any site beyond the primary tumor and regional lymph nodes. OS was calculated from the start of treatment to the last follow-up or death. Progression-free survival (PFS) was calculated from the starting day of treatment to the date of disease progression, evidence of residual disease, or any cause of death. Kaplan-Meier curves were generated for OS and PFS. A probability value of <0.05 was considered significant. All statistical analyses were performed using EZR software (Saitama Medical Center, Jichi Medical University, Saitama, Japan) (15).

Results

Patient characteristics. The patient characteristics are detailed in Table I. Four patients with supraclavicular lymph node metastasis were categorized as M1 (Lym). The median follow-up period was 42.1 months (range=2.8-82.0). The average relative dose intensity in the first cycle of DCF was 97.9%, and that in the second cycle of DCF was 73.4%. The patient characteristics according to the reason for CRT are detailed in Table II. Seven patients were considered unfit for surgery [poor respiratory function (n=4), diabetes mellitus and liver cirrhosis (n=1), dementia (n=1), and poor performance status (n=1)]. Twenty-one patients refused surgery. There were no significant differences in the patient backgrounds according to the reason for CRT.

View this table:
Table I.

Patient characteristics.

View this table:
Table II.

Comparison of patient’s characteristics by reason for chemoradiation (CRT).

Treatment outcome. The overall CR rate was 88.5% [95% confidence interval (CI)= 69.8-97.6]. The overall CR rate was 90.9% (95%CI= 58.7-99.8) in patients with cStage I (n=11), 90.9% (95%CI=58.7-99.8) in patients with cStage II-III (n=11), and 75.0% (95%CI=19.4-99.4) in patients with cStage IV [M1(Lym)] disease (n=4). For all patients, the 5-year OS and 5-year PFS were 75.4% (95%CI=50.3-89.0) and 45.7% (95%CI=18.6-69.5), respectively (Figure 1A and B). The 5-year OS for cStage I, II-III, and IV [M1(Lym)] patients was 79.5% (95%CI=39.3-94.5), 76.2% (95%CI=33.2-93.5), and 50.0% (95%CI=0.6-91.0), respectively (Figure 2A). The 2-year PFS for cStage I, II-III, and IV [M1(Lym)] patients was 81.8% (95%CI=44.7-95.1), 91.7% (95%CI= 53.9-98.8), and 50.0% (95%CI=5.8-84.5), respectively (Figure 2B). One patient with stage IV disease (3.6%) died from cancer, and four patients [14.3%, stage I (n=2), stage II-III (n=2)] died from non-cancer-related causes within 5 years from the start of treatment.

Figure 1.
Figure 1.

Kaplan–Meier curves for (A) overall survival (OS) and (B) progression-free survival (PFS) for all patients.

Figure 2.
Figure 2.

Kaplan–Meier curves for (A) overall survival (OS) and (B) progression-free survival (PFS) according to clinical stage.

Failure pattern and salvage treatment. The initial failure pattern is detailed in Table III. Ten patients (35.4%) had recurrence or residual disease of any type at the time of analysis. In these patients, locoregional failure was identified in seven patients (25.0%), and distant failure in three patients (10.7%). Among the seven patients with locoregional failure, four patients (57.1%) underwent salvage treatment without severe complications. One patient [refused surgery (n=1)] underwent esophagectomy, and three [refused surgery (n=2), unfit for surgery (n=1)] underwent endoscopic submucosal dissection. Of the remaining three patients [refused surgery (n=1), unfit for surgery (n=2)] with locoregional failure, all patients received chemotherapy. Among the three patients with distant failure, two had node recurrence outside the elective nodal irradiation area [paraaortic abdominal (n=2)]. The remaining one patient had lung metastases. For cStage I disease, all three patients (25%) with locoregional failure underwent salvage treatment. For cStage II-III disease, one patient with locoregional failure underwent salvage treatment. For cStage IV [M1(Lym)] patients, no patients underwent salvage treatment.

View this table:
Table III.

Initial failure pattern.

Toxicities. The acute toxicity profile is presented in Table IV. The most frequently observed grade 3 and 4 acute toxicities were leucopenia, neutropenia, febrile neutropenia (FN), and anorexia. The late toxicity profile is presented in Table V. Twenty-six patients were available for evaluation of late toxicity. The most frequently observed grade 3 or 4 late toxicity was pleural effusion and esophageal stenosis. The rate of any grade 3 or 4 late toxicity was 7.7%. One patient (3.8%, cT3N0M0) was considered to have died of treatment-related late toxicity. The cause of death was pleural effusion. There was no evidence of residual or recurrent disease in this patient.

View this table:
Table IV.

Acute toxicity.

View this table:
Table V.

Late toxicity.

Discussion

In this study, the 5-year OS rate was 75.4% for patients with potentially resectable thoracic EC who underwent DCF-RT. Especially, the 5-year OS rate for cStage II-III patients was 76.2%. These findings were higher than previous CF-RT studies. To the best of our knowledge, this is the first study investigating the long-term outcome of potentially resectable thoracic EC patients undergoing DCF-RT in a real-world clinical setting.

For cStage I patients, the CR rate (90.9%) and the 5-year OS (79.5%) in our study were equivalent to those in previous CF studies. The JCOG0502 study, which compared surgical resection to CRT in patients with clinical T1bN0M0 EC (16), reported that CR rate and 5-year OS were 87.3% and 85.5%, respectively, and the locoregional and distant failure rates were 20.9% and 9.4%, respectively. In the JCOG9708 study, a phase 2 trial of CF-RT for patients with stage IA [T1N0M0] EC (17), CR rate and 4-year OS were 87.5% and 80.5%, respectively. The rate of relapses inside the radiation field was 8.3%, and that outside the radiation field was 18.1%. Although these studies included only T1N0 patients, distant failure was observed. On the other hand, cStage I patients, including N(+) patients in our study, had only locoregional failure (25%) and all underwent salvage treatment; furthermore, no patients had distant failure. These results indicate that DCF-RT may have a better effect on local control and for preventing distant metastasis.

For cStage II-III patients, the CR rate (90.9%) and the 5-year OS (76.2%) in our study were higher than those of previous CF studies. JCOG9906 (a Phase II trial evaluating CF-RT for stage II-III EC) reported a 62.2% complete response rate and a 36.8% 5-year OS (18). The local failure rate of our study (16.6%) was also lower than JCOG9906 (34.2%). Docetaxel has been reported to be a potent enhancer of tumor radioresponse (19). Although elective nodal irradiation was not performed in our study, the higher CR and lower local failure rate suggest the efficacy of the addition of docetaxel to CF-RT.

Our study’s distant failure rate (16.6%) was equivalent to previous CF studies (7, 20). One possible strategy to improve the treatment efficacy of DCF may be the precise management of myelotoxicity. Our study’s incidence rates of grade 3 and 4 leukopenia and neutropenia were high, which was similar to those of previous DCF studies (9, 21-23). The rate of FN was 21.4% in our study, which is higher than that reported in a previous CF-RT study (1.3%) (18). In our study, severe myelosuppression or late recovery from myelosuppression caused a decrease in relative dose intensity. To date, the American Society of Clinical Oncology guidelines recommend not to use colony-stimulating factor (CSF) during CRT, particularly CRT involving the mediastinum. However, Gomes et al. reported the safety of prophylactic granulocyte-CSF (G-CSF) with chemoradiation in lung cancer and concluded that G-CSF supports CRT delivery by maintaining the treatment dose intensity (24). With modern radiotherapy techniques, such as 3-dimensional conformal radiotherapy (3D-conformal RT), the combination of G-CSF and CRT is thought to be safe with no abnormal infield event (25). The prophylactic use of G-CSF and antibiotics may prevent hematological toxicities and increase the safety and efficacy of DCF-RT.

Late toxicity after CRT causes severe, life-threatening complications. In our study, the grade 3 or 4 late toxicity rate was 7.7%, which was lower than previous studies (7, 18), which was partly attributed to the improvement of radiation technologies. 3D-conformal RT may have potential advantages over conventional two-dimensional radiotherapy in terms of reduced doses for non-targeted organs surrounding the esophagus (26). However, 3D-conformal RT was not mandatory in previous studies (17, 18). In our study, one (3.6%) patient was assumed to have died of treatment-related late toxicity without residual or recurrent disease. Long-term follow-up is essential even for patients with CR after DCF-RT.

This study has several limitations. First, there was a selection bias because this was a retrospective single-institution analysis. Second, dose reduction was performed according to the physician’s discretion based on the patient’s clinical status and grade of adverse events. Further multicenter, large-population-based investigations are needed to confirm the effects of advances in DCF-RT for potentially resectable thoracic EC.

In conclusion, DCF-RT demonstrated a satisfactory CR rate and OS with a higher rate of FN for potentially resectable thoracic EC patients. Prophylactic treatment with G-CSF and antibiotics may be appropriate supportive care for patients undergoing DCF-RT.

Footnotes

  • Authors’ Contributions

    Study conception and design: Sakai; acquisition of data: Uchida, Yamaguchi, Watanabe, Saito, Ubukata, Nakazawa, Kuriyama; analysis and interpretation of data: Sakai, Sohda, Sano, Ogawa, Yokobori, Noda; drafting of manuscript: Sakai; critical revision: Ohno, Shirabe, Saeki.

  • Conflicts of Interest

    The Authors declare no conflicts of interest associated with this manuscript.

  • Received July 24, 2022.
  • Revision received August 6, 2022.
  • Accepted August 8, 2022.

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Concurrent Chemoradiotherapy With Docetaxel, Cisplatin, and 5-Fluorouracil (DCF-RT) for Patients With Potentially Resectable Esophageal Cancer
MAKOTO SAKAI, MAKOTO SOHDA, SHINTARO UCHIDA, ARISA YAMAGUCHI, TAKAYOSHI WATANABE, HIDEYUKI SAITO, YASUNARI UBUKATA, NOBUHIRO NAKAZAWA, KENGO KURIYAMA, AKIHIKO SANO, HIROOMI OGAWA, TAKEHIKO YOKOBORI, SHIN-EI NODA, TATSUYA OHNO, KEN SHIRABE, HIROSHI SAEKI
Anticancer Research Oct 2022, 42 (10) 4929-4935; DOI: 10.21873/anticanres.15999
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