RAMY R. GHALI, M.D.*; EMAN EL-SHARAWY, M.D.*; AZZA M. ADEL, M.D.* and SAMER A. IBRAHIM, M.D.**
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1 Med. J. Cairo Univ., Vol. 79, No. 2, June: 13-18, Induction Docetaxel, Cisplatin and 5 Fluorouracil (TPF) Followed by Concomitant Chemoradiotherapy Versus Concomitant Chemoradiotherapy in Unresectable Locally Advanced Head and Neck Cancer: A Phase III Randomized Study RAMY R. GHALI, M.D.*; EMAN EL-SHARAWY, M.D.*; AZZA M. ADEL, M.D.* and SAMER A. IBRAHIM, M.D.** The Departments of Radiation Oncology & Nuclear Medicine* and E.N.T. **, Faculty of Medicine, Ain Shams University Abstract Objective: This phase III randomized trial was designed to assess feasibility (on the basis of efficacy and toxicity) of induction docetaxel, cisplatin, and 5-fluorouracil (TPF) followed by CT/RT versus concomitant chemoradiotherapy (CT/ RT) alone in patients with unresectable locally advanced squamous cell carcinoma of the head and neck (SSCHN). Patients and Methods: Sixty patients were randomly assigned into 2 arms; Arm A: 30 patients received CT/RT in the form of radiotherapy to the primary tumor and neck nodes concomitant with cisplatin 100mg/m 2 on day 1, 22 and 43 of radiotherapy. Arm B: 30 patients received induction TPF regimen (docetaxel: 75mg/m 2, cisplatin: 75mg/m 2 both on day 1, and 5-fluorouracil: 750mg/m 2 /day over 96h). Cycles were repeated every 3 weeks to a maximum of three cycles, after which patients received the same RT regimen as in arm A with cisplatin 30mg/m 2 weekly starting day 1 of radiotherapy. Concomitant chemoradiotherapy commenced 3-5 weeks after the end of induction chemotherapy. Results: From August 2007 to September 2009, 60 patients with stage III-IV M0 SCCHN, ECOG-PS of 0 to 1, were randomly assigned to each of the study arms. Induction TPF, the ORR was 63.33% (19/30 assessable patients) (95% CI : ) and the CR was 23.33% (CI: ) (7/30 assessable patients). Two patients (6.67%) progressed during TPF. Following CT/RT, the CR rate was 13.33% (95% CI: ) in arm A and 42.86% (95% CI ) in arm B p-value= indicating a better activity for arm B. The Corresponding PR rates were 53.33% and 32.14% for arm A and B respectively. The overall response rate was 66% and 75% for both groups respectivly, progressive disease was more in arm A (8 compared to 3 patients in both groups respectivly). There were no early deaths in both arms. During induction TPF, the most common grade 3-4 hematologic toxicity was neutropenia (36.67%), with 3.33% experiencing febrile neutropenia. The rate of grade 3-4 anemia and thrombocytopenia was 3.33%. Grade 3-4 non-hematologic toxic effects as alopecia occurred in 86.67%, stomatitis/mucositis Correspondence to: Dr. Azza M. Adel, The Department of Radiation Oncology and Nuclear Medicine, Faculty of Medicine, Ain Shams University. (6.67%), and nausea (6.67%). Grade 3-4 hematologic toxic effects during CT/RT were not statistically significant between both arms (p-value=0.344). The most relevant non-hematologic toxic effects (mucositis/stomatitis, skin toxicity, and dysphagia) which constituted 46.66% and 39.28% respectively but this difference was not statistically significant ( p-value=0.571). Conclusion: Treatment of unresectable locally advanced squamous cell carcinoma of head neck cancer with induction TPF chemotherapy followed by concomitant CT/RT yields significantly more patients with complete response and is not on the expense of higher toxicity than concomitant chemoradiotherapy alone. Key Words: Concomitant chemoradiotherapy Head and neck cancer Induction chemotherapy. Introduction CONCURRENTLY administered chemotherapy and radiotherapy (chemoradiotherapy) is a highly efficient treatment approach for locally advanced squamous cell carcinoma of the head and neck (SCCHN) [1]. However, its efficacy comes at the expense of substantial acute toxicity and this may limit its use [2-4]. Late toxicities are also an issue with chemoradiotherapy and can cause long-term problems for patients [5]. In terms of disease control, although chemoradiotherapy has improved locoregional tumor control, there is no consistent evidence that it reduces the development of distant disease [1]. The rationale for using induction chemotherapy prior to radiotherapy or chemoradiotherapy in the treatment of locally advanced SCCHN is to reduce the local tumor volume and also to minimize the risk for developing distant metastases [6]. Two phase III trials have confirmed the superiority of the triplet docetaxel, cisplatin, and 5-FU 13
2 14 Induction Docetaxel, Cisplatin & 5 Fluorouracil (TPF) Followed (TPF) regimen over PF, followed by radiotherapy or chemoradiotherapy, in terms of progressionfree and overall survival [7,8], and TPF is now a standard choice for use in induction chemotherapy. Despite the efficacy of TPF as an induction chemotherapy regimen, it is far from clear whether the sequential approach of induction chemotherapy followed by radiotherapy or chemoradiotherapy is as effective as, or more effective than, concurrent chemoradiotherapy alone in locally advanced unresectable disease in terms of survival. A current question of great interest is whether or not the administration of induction chemotherapy prior to concomitant chemoradiotherapy can further improve the results of either approach alone. The current phase III randomized trial was designed to assess feasibility (on the basis of efficacy and acceptable toxicity) at the end of treatment in patients receiving either CT/RT alone or three cycles of induction docetaxel, cisplatin, and 5- fluorouracil (TPF) followed by CT/RT. Patients and Methods This was an open-label, randomized, phase III study, patients aged >_ 18 <70 years were eligible if they had histologically/cytologically proven stage III-IV nonmetastatic unresectable SCCHN (oral cavity, oropharynx, hypopharynx or larynx); one or more measurable lesion; Eastern Cooperative Oncology Group performance status (ECOG-PS) of 0-1; adequate hematologic, hepatic, and renal functions, life expectancy >_6 months; no prior chemotherapy, radiotherapy, or surgery; no peripheral neuropathy and weight loss <20% in 3 months preceding the study. Inoperability criteria were technical unresectability (tumor fixation/invasion to either base of the skull, cervical vertebrae, nasopharynx, or fixed lymph nodes), low surgical curability (T3-T4, N2-N3 excluding T1 N2). All patients provided informed consent. Treatment plan: Patients were randomly assigned to receive either CT/RT alone (arm A) or induction TPF followed by CT/RT (arm B). In Arm A the CT/RT regimen consisted of standard fractionated radiotherapy of 70Gy for the primary tumor (2Gy/day, 5 days/week for 7 weeks). For N2-N3 patients who were candidates for neck dissection, a minimum of 50Gy for the neck was planned. The CT/RT chemotherapy was cisplatin 100mg/m 2 (30min i.v. infusion) on day 1, 22 and 43 of radiotherapy. In arm B, induction TPF consisted of docetaxel 75mg/m 2 (1-h i.v. infusion, day 1) followed by cisplatin 75mg/m 2 (30-min i.v. infusion, day 1) and 5-fluorouracil 750mg/m 2 /day (96h continuous i.v. infusion, starting after the cisplatin infusion). Cycles were repeated every 3 weeks to a maximum of three cycles. Antibiotic prophylaxis (oral ciprofloxacin 500mg twice daily, days 5-15) was administered after each cycle. Patients received the same RT regimen as in arm A with cisplatin 30mg/m 2 weekly starting day 1 of radiotherapy. Chemoradiation commenced 3-5 weeks after the end of induction chemotherapy. All patients were given adequate hydration and antiemetics (5-HT3 antagonists and dexamethasone). Prophylactic granulocyte colony-stimulating factor (G-CSF) was not allowed, but G-CSF was given to patients who experienced grade 4 neutropenia [absolute neutrophil count (ANC) <0.5 x 10 9 /l lasting >7 days], febrile neutropenia, or delayed ANC recovery. Enteral support (feeding tube, percutaneous endoscopic gastrostomy) was considered before starting CT/RT. A reduction or delay in chemotherapy dose was recommended if patients had an ANC <1500/ µl, a platelet count <100000/ µ l, and/or grade 2-4 nonhematologic toxic effects before starting chemotherapy. For a delay in TPF induction cycle >2 weeks, patients were withdrawn from study. Evaluations: Staging was by the International Union Against Cancer 1997 tumor-node-metastasis classification [9]. Before study entry, all patients underwent a computerized tomography (CT) or magnetic resonance imaging (MRI) scan of the head and neck, chest X-ray and/or lung CT scan, abdominal ultrasound or liver CT scan for liver abnormalities, and brain and bone scans in the presence of specific symptoms. Audiogram, and dental examination were also performed prior to treatment. Radiologic head and neck examinations were carried out after induction TPF (arm B) to assess response and 6-8 weeks after ending concomitant CT/RT (all patients). Pathologic confirmation of radiologic CR at the primary site was carried out under anesthesia 8-12 weeks after the end of CT/RT. End points: The primary end point was the feasibility based on efficay and toxicity evaluated 6-8 weeks after the completion of CT/RT. Responses were assessed according to RECIST criteria [10], while toxicity was assessed using National Cancer Institute of Canada-Clinical Trials Group expanded common toxicity criteria [11].
3 Ramy R. Ghali, et al. 15 Statistical analysis: Assessable for response patients were those meeting eligibility criteria, having received treatment assigned at randomization, with all baseline lesions reassessed at least once by the same method as used at baseline. Response rate were compared by means of the chi-square test. Results are presented as point estimates and 95% confidence intervals (CIs). Since the goal of the study was to select the best regimen, the study was not powered for a formal comparison between the two arms. Therefore, all the comparisons made had only explorative purposes. Results Patient characteristics: Overall, 60 patients were randomly allocated to the study from August 2007 to September 2009, with 30 assigned to CT/RT (arm A) and 30 to induction TPF followed by CT/RT (arm B). Baseline characteristics as regards age, sex, PS, anatomic site and clinical stage were balanced between the two arms as shown in Table (1). Response to treatment: After induction TPF, the ORR was 63.33% (19/30 assessable patients) (95% CI: ) and the CR was 23.33% (CI: ) (7/30 assessable patients). Two patients (6.67%) progressed during TPF. Following CT/RT, the CR rate was 13.33% (95% CI: ) in arm A and 42.86% (95% CI ) in arm B (p-value= indicating a better activity for arm B. The Corresponding PR rates were 53.33% and 32.14% for arm A and B respectively. The overall response rate was 66% and 75% for both groups respectivly, progressive disease was more in arm A (8 compared to 3 patients in both groups respectivly), as shown in Table (2). Adverse events and treatment compliance: There were no early deaths in both arms. During induction TPF, the most common grade 3-4 hematologic toxicity was neutropenia (36.67%; 11 of 30 assessable patients), with 3.33% (n=1) experiencing febrile neutropenia. The rate of grade 3-4 anemia and thrombocytopenia was 3.33%. Grade 3-4 non-hematologic toxic effects as alopecia occurred in 86.67%, stomatitis/mucositis (6.67%), and nausea (6.67%). Grade 3-4 hematologic toxic effects during CT/RT were not statistically significant between both arms (p-value=0.344). The most relevant non- hematologic toxic effects (mucositis/stomatitis, skin toxicity, and dysphagia) which constituted 46.66% and 39.28% respectively but this difference was not statistically significant (p-value=0.571) as shown in Table (3). The mean radiation dose, the mean duration of CT/RT, and radiotherapy interruption rates were similar (Table 4). In arm A, more than 90% of patients received two planned cycles of concomitant cisplatin, two patients (6.67%) received only one cycle due to disease progression before the second cycle. In arm B, 93.33% of patients (n=30) received three planned cycles TPF induction while 6.67% (n=2) received only two cycles due to progression. During concomitant treatment, three patients (10%) received only one cycle of cisplatin during radiotherapy (n=1 disease progression; n=2 toxicity). Table (1): Characteristics of the patients. Characteristic CT/RT (arm A) (N=30) TPF + CT/RT (arm B) (N=30) Eligible patients, n (%) 30 (100%) 30 (100%) p value Mean age, years (range) 57 (44-68) 56 (42-69) Male/female, n 19/11 21/ ECOG PS, n (%): (56.67) 19 (63.33) 1 13 (43.33) 11 (36.67) Anatomic site, n (%): Oral cavity/oropharynx 2/9 (36.67) 3/7 (33.33) Hypopharynx 9 (30) 12 (40.0) Larynx 10 (33.33) 8 (26.67) Clinical stage, n (%): III 10 (33.33) 8 (26.67) IV 20 (66.67) 22 (73.33) Stage of primary tumor, n (%): T2 2 (6.67) 3 (10) T3 15 (50) 17 (56.67) T4 13 (43.33) 10 (33.33) Nodal stage, n (%): N0 1 (3.33) 1 (3.33) N1 17 (56.67) 20 (66.67) N2 9 (30) 7 (23.33) N3 3 (10) 2 (6.67) CT/RT : Concomitant chemoradiotherapy. TPF : Docetaxel, cisplatin plus 5-fluorouracil. ECOG : Eastern cooperative oncology group. PS : Performance status.
4 16 Induction Docetaxel, Cisplatin & 5 Fluorouracil (TPF) Followed Table (2): Response rate 6-8 weeks after the end of CT/RT in assessable patients. CT/RT TPF + CT/RT Response (arm A) (N=30), (arm B) (N=28), n (%) n (%) Complete response (95% CI) 4 (13.33) ( ) 12 (42.86) ( ) Partial response 16 (53.33) 9 (32.14) Stable disease 2 (6.67) 4 (14.29) Progressive disease 8 (26.67) 3 (10.71) Overall response rate 20 (66.0) 21 (75) Table (3): Incidence of hematologic and non-hematologic grade 3-4 adverse events during CT/RT. Toxicity CT/RT (arm A) (N=30), n (%) TPF + CT/RT (arm B) (N=28), n (%) Grade 3 Grade 4 Grade 3 Grade 4 p-value Anemia (3.57) 0 Neutropenia 1 (3.33) 1 (3.33) 2 (7.14) 1 (3.57) Thrombocytopenia (3.57) 0 Mucositis/stomatitis 13 (43.33) 1 (3.33) 10 (35.71) 1 (3.57) Dysphagia 14 (46.67) 1 (3.33) 10 (35.71) 1 (3.57) Skin 2 (6.67) 1 (3.33) 4 (14.29) Nausea/vomiting 1 (3.33) 0 1 (3.33) 0 Asthenia 1 (3.33) 0 2 (7.14) 1 (3.57) Neurotoxicity (3.57) 0 CT/RT: Concomitant chemoradiotherapy. TPF : Docetaxel, cisplatin plus 5-fluorouracil. Table (4): Compliance with CT/RT. Compliance Mean dose RT, Gy (range) Mean duration of CT/RT, weeks (range) Patients with radiotherapy interruption duration 3 days, n Median duration of single radiotherapy interruption, days (range) CT/RT: Concomitant chemoradiotherapy. TPF: Docetaxel, cisplatin plus 5-fluorouracil. Discussion Induction chemotherapy for locally advanced SCCHN has shown high overall responses rates (RRs), including complete responses (CRs) [13]. However, The benefit of induction chemotherapy in clinical practice compared with the present standard CT/RT is unclear. Superirity of TPF over PF induction followed by locoregional treatment in form of RT or CT/RT using carboplatin has been confirmed in several studies, however, a limitation of these studies was the absence of a standard control arm (CT/RT only using cisplatin 100mg/m 2 day 1, 22 and 43 of radiotherapy), and consequently, no definitive conclusion was possible [10,11]. In the current study we aimed at comparing induction TPF followed by CT/RT (arm B) to CT/ CT/RT (arm A) (N=30) TPF + CT/RT (arm B) (N=28) 68.4 (66-70) 69.4 (68-70) 7.7 (6.8-8) 7.6 ( ) 4 (13.33) 3 (10.71) 5 (3-8) 4 (3-5) RT (arm A) alone regarding efficacy and toxicity, a CR was recorded in arm B in 42.86% of patients compared to 13.33% of patients treated in arm A which was statistically significant, ( p=0.0105) with no statistically significant Grade 3-4 hematologic or non-hematologic toxic effects at the end of treatment between both arms. Previous reports have indicated that patients with advanced head and neck cancer who achieve complete response to treatment have better survival than patients with response that was less than CR [14,15]. In a phase III randomized trial conducted by the Spanish Head and Neck Cooperative Group which investigated the value of adding paclitaxel to PF before definitive platinum based CT/RT,
5 Ramy R. Ghali, et al. 17 higher CR, greater time to treatment failure as well longer median survival was reported. It was concluded that TPF followed by CT/RT is well tolerated and effective compared to PF followed by CT/RT [16]. Paccagnella et al. [6] reported that the primary endpoint of complete response at 6-8 weeks after chemoradiotherapy was achieved by 50% of patients who received TPF plus chemoradiotherapy, and this was significantly more than in the chemoradiotherapy alone group (21 %; p.004). The median OS time in the chemoradiotherapy arm was 33.3 months, with a 1-year survival rate of 78%, whereas in the TPF plus chemoradiotherapy group the median OS time was 39.6 months and the 1-year survival rate was 86%. Similarly in the study conducted by Ahn et al. [17] on 49 patients with locally advanced HNSCC to determine the feasibility and safety of the use of induction chemotherapy of TPF followed by concurrent chemoradiation therapy for which a CR of 65.2%, Overall survival, and progression-free survival (PFS) at 2 years of 88.7% and 69.7%, respectively were also reported. In that study it was concluded that TPF induction chemotherapy followed by concurrent chemoradiotherapy showed a high level of CR and moderate treatment-induced toxicity. Notably, in the current study as well as other studies [18,19], induction TPF resulted in feasible grade 3 and 4 hematologic and nonhematologic toxicity, and did not compromise the delivery of subsequent CT/RT. In our study patients who were allocated to arm A (concurrent chemoradiotherapy alone) received cisplatin 100mg/m 2 day 1, 22 and 43 of radiotherapy while patients allocated to induction TPF followed by concurrent chemoradiotherapy received cisplatin 30mg/m 2. The uncertainty regarding the optimal scheduling of cisplatin with radiotherapy in Squamous cell carcinoma of head and neck cancer has sparked considerable interest in comparing various doseschedules. The most popular schedule of concurrent cisplatin for SCCHN outside the context of clinical trials is not the three-weekly regimen but a weekly schedule [20] of cisplatin in the dose range of 30-40mg/m 2. In an indirect comparison, Ho and colleagues [21] compared the differences in dose intensity, delays, and toxicity between concurrent 3- weekly (80-100mg/m 2 ) and weekly (40mg/m 2 ) cisplatin-based definitive CRT in 51 patients with advanced SCCHN. More patients received a higher cumulative dose of at least 240mg/m 2 in the weekly arm as compared to the 3-weekly arm ( p=0.04). The 3-weekly regimen was associated with more delays (41% Vs. 29%) and omissions of chemotherapy (17.4% Vs. 5.6%) resulting in lesser patients achieving cumulative doses beyond 200 mg/m 2, potentially lowering dose-intensity. A prospective non-randomized study [22] compared 3-weekly cisplatin (100mg/m 2 ) given to younger patients with good KPS (n=30) with weekly cisplatin (40mg/m 2 ) in patients with older age or poor KPS (n=20) along with radical radiotherapy. The complete response rate (50% Vs. 40%), overall response rate (92% Vs. 90%), and grade III-IV toxicities (53% Vs. 40%) were similar in the two cohorts. The only randomized study comparing daily (6mg/m 2 ), weekly (40mg/m 2 ), and threeweekly (100mg/m 2 ) schedule of cisplatin with conventionally fractionated radiotherapy [23] did not find any significant difference in the efficacy of the regimens (similar response rates and locoregional control), but reported varying degrees of mucosal, renal and hematologic toxicity. Overall the available data suggests that a cumulative cisplatin dose of mg/m 2 given three-weekly, weekly, or daily during radiotherapy yields therapeutic benefit [24]. In conclusion: Our findings indicate that induction chemotherapy with TPF followed by CT/RT is superior to CT/RT alone in terms of CR rate. Induction TPF followed by chemoradiotherapy, appears to be well tolerated and feasible. Survival advantage with this approach needs to be confirmed. The benefits of TPF induction chemotherapy followed by concomitant chemoradiotherapy may be further enhanced by the addition of targeted therapies and such an approach warrants further clinical investigation. References 1- BUDACH V.: TPF Sequential Therapy: When and for Whom? The Oncologist, 15 (Suppl 3): 13-18, DENIS F., GARAUD P., BARDET E., et al.: Final results of the French Head and Neck Oncology and Radiotherapy Group randomized trial comparing radiotherapy alone with concomitant radiochemotherapy in advancedstage oropharynx carcinoma. J. Clin. Oncol., 22: 69-76, FORASTIERE A.A., GOEPFERT H., MAOR M., et al.: Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N. Engl. J. Med., 349: , PACCAGNELLA A., GHI M.G., LOREGGIAN L., et al.: Concomitant chemoradiotherapy versus induction docetaxel, cisplatin and 5 fluorouracil (TPF) followed by concomitant chemoradiotherapy in locally advanced head
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