Concurrent Chemotherapy and Radiotherapy for Organ Preservation in Advanced Laryngeal Cancer
Arlene A. Forastiere, M.D., Helmuth Goepfert, M.D., Moshe Maor, M.D., Thomas F. Pajak, Ph.D., Randal Weber, M.D., William Morrison, M.D., Bonnie Glisson, M.D., Andy Trotti, M.D., John A. Ridge, M.D., Ph.D., Clifford Chao, M.D., Glen Peters, M.D., Ding-Jen Lee, M.D., Ph.D., Andrea Leaf, M.D., John Ensley, M.D., and Jay Cooper, M.D.
Background Induction chemotherapy with cisplatin plus fluorouracilfollowed by radiotherapy is the standard alternative to totallaryngectomy for patients with locally advanced laryngeal cancer.The value of adding chemotherapy to radiotherapy and the optimaltiming of chemotherapy are unknown.
Methods We randomly assigned patients with locally advancedcancer of the larynx to one of three treatments: induction cisplatinplus fluorouracil followed by radiotherapy, radiotherapy withconcurrent administration of cisplatin, or radiotherapy alone.The primary end point was preservation of the larynx.
Results A total of 547 patients were randomly assigned to oneof the three study groups. The median follow-up period was 3.8years. At two years, the proportion of patients who had an intactlarynx after radiotherapy with concurrent cisplatin (88 percent)differed significantly from the proportions in the groups giveninduction chemotherapy followed by radiotherapy (75 percent,P=0.005) or radiotherapy alone (70 percent, P<0.001). Therate of locoregional control was also significantly better withradiotherapy and concurrent cisplatin (78 percent, vs. 61 percentwith induction cisplatin plus fluorouracil followed by radiotherapyand 56 percent with radiotherapy alone). Both of the chemotherapy-basedregimens suppressed distant metastases and resulted in betterdisease-free survival than radiotherapy alone. However, overallsurvival rates were similar in all three groups. The rate ofhigh-grade toxic effects was greater with the chemotherapy-basedregimens (81 percent with induction cisplatin plus fluorouracilfollowed by radiotherapy and 82 percent with radiotherapy withconcurrent cisplatin, vs. 61 percent with radiotherapy alone).The mucosal toxicity of concurrent radiotherapy and cisplatinwas nearly twice as frequent as the mucosal toxicity of theother two treatments during radiotherapy.
Conclusions In patients with laryngeal cancer, radiotherapywith concurrent administration of cisplatin is superior to inductionchemotherapy followed by radiotherapy or radiotherapy alonefor laryngeal preservation and locoregional control.
To determine the contributions of chemotherapy and radiotherapyto larynx-preserving treatment, the Radiation Therapy OncologyGroup and the Head and Neck Intergroup conducted a randomizedtrial (RTOG 91-11) to investigate three radiation-based treatments:induction cisplatin plus fluorouracil followed by radiotherapyif there was a response to the chemotherapy (a regimen identicalto that given the "experimental" group in the Department ofVeterans Affairs Laryngeal Cancer Study Group trial), radiotherapywith concurrent administration of cisplatin, and radiotherapyalone. The rationale for the second group was based on the enhancementof radiation effects on tumor cells by concurrent treatmentwith cisplatin. The primary objective of the trial was to comparethe rates of laryngeal preservation associated with the threetreatments. The study involved investigators from the RadiationTherapy Oncology Group (the coordinating group), the SouthwestOncology Group, and the Eastern Cooperative Oncology Group.
Methods
Patients
Patients were eligible if they had biopsy-proven, previouslyuntreated stage III or IV (according to the staging system ofthe American Joint Commission on Cancer) squamous-cell carcinomaof the glottic or supraglottic larynx, the surgical treatmentof which would require total laryngectomy. Patients with a stageT1 primary tumor (defined as tumor limited to one subsite ofthe supraglottis or limited to the vocal cords, with normalvocal-cord mobility, according to the tumor–node–metastasis[TNM] staging system) or with large-volume stage T4 disease(defined as a tumor penetrating through the cartilage or extendingmore than 1 cm into the base of the tongue) were not eligible.The disease had to be considered curable with surgery and postoperativeradiotherapy. A Karnofsky performance score of at least 60 (ona scale from 0 to 100, with higher scores indicating betterperformance and with a score of 60 indicating that the patientrequires occasional assistance but is able to care for mostof his or her own needs) was required. To be eligible, patientsalso had to have a white-cell count of at least 3500 per cubicmillimeter, a platelet count of at least 100,000 per cubic millimeter,a normal serum calcium level, and a creatinine clearance ofat least 50 ml per minute. All the patients gave written informedconsent in accordance with institutional guidelines.
Pretreatment staging, involving laryngoscopy, measurement ofthe tumor, and high-resolution computed tomographic (CT) scanningof the primary tumor and the neck, was performed within fourweeks before entry into the study. To rule out synchronous primarycancers, either CT imaging of the chest and barium esophagographyor pan-endoscopy (i.e., esophagoscopy and bronchoscopy) wasperformed. Imaging was performed as clinically indicated torule out metastatic disease.
Treatment
Chemotherapy
Induction chemotherapy consisted of cisplatin given intravenouslyat a dose of 100 mg per square meter of body-surface area onday 1 and fluorouracil given at a dose of 1000 mg per squaremeter every 24 hours by continuous intravenous infusion for120 hours, every three weeks for two courses. Patients thenunderwent evaluation by indirect laryngoscopy and CT imagingof the neck. If these examinations showed a complete or partialresponse of the primary tumor and no sign of progression inthe neck, a third course of cisplatin plus fluorouracil wasgiven, followed by radiotherapy. Patients with a less than partialresponse of the primary tumor or with progression in the neckunderwent laryngectomy followed by adjuvant radiotherapy. Patientsassigned to radiotherapy with concurrent cisplatin receivedintravenous cisplatin at a dose of 100 mg per square meter ondays 1, 22, and 43 of radiotherapy.
Radiotherapy
The dose of radiation and radiotherapy schedule were the samein all three study groups. The dose of radiation to the primarytumor and clinically positive nodes was 70 Gy, given in 35 fractionsof 2 Gy each over a seven-week period. The entire neck, includingthe supraclavicular areas and the posterior neck, was irradiatedwith a minimum of 50 Gy. The dose to the clinically positivenodes was supplemented with the beams that covered the primarytumor, with electrons, or with tangential anteroposterior beams.The patients assigned to induction chemotherapy followed byradiotherapy who underwent salvage surgery because of a poorresponse to the chemotherapy received adjuvant radiotherapy(50 to 70 Gy), depending on the status of the margins on pathologicalreview.
Surgery
Patients who had either a single lymph node 3 cm or greaterin diameter or multiple lymph-node metastases on initial clinicalstaging of the neck were required to undergo neck dissectioneight weeks after the completion of radiotherapy. Laryngectomywas performed in patients who had histologically proven persistentor recurrent carcinoma after the completion of treatment orwho had an inadequate response after two courses of inductionchemotherapy.
Follow-up after the Completion of Treatment
All the patients were evaluated eight weeks after the completionof therapy by examination of the head and neck and CT imaging.If persistent disease was suspected, examination while the patientwas under anesthesia and direct laryngoscopy were performed.Complete examination of the head and neck, with evaluation forlate toxicity, was performed at scheduled follow-up visits.
Two questionnaires, to be completed by the patients, were usedto evaluate quality of life: the Functional Assessment of CancerTherapy — Head and Neck Scale, version 2,4 and the Universityof Washington Quality of Life instrument.5 These questionnaireswere to be filled out at base line and at each follow-up visit.Results with respect to swallowing ability and speech are reportedin this article.
Study Design
Randomization
Patients were stratified according to the site of the primarytumor (glottic or supraglottic), N stage (stage N0 or N1 orstage N2 or N3), and primary tumor stage (T2; T3 with fixedcord involvement; T3 with no cord fixation but with invasionof the postcricoird area, medial wall of the pyriform sinus,or preepiglottic tissues; or T4). The randomization scheme describedby Zelen6 was used to achieve balance in the treatment assignmentsamong the institutions.
Study End Points
The primary end point was preservation of the larynx. Treatmentwas considered to have failed on the date laryngectomy was performed.Other end points analyzed were overall survival, disease-freesurvival, local control, locoregional control, the time to distantmetastasis, and laryngectomy-free survival. All events weremeasured from the date of randomization to the date of theiroccurrence or the date of the last follow-up visit. Toxic effectswere graded according to the National Cancer Institute CommonToxicity Criteria, version 1.0, during induction chemotherapyand according to the Radiation Therapy Oncology Group toxicitycriteria during radiotherapy. All deaths occurring during treatmentor within 30 days after the completion of treatment were consideredto be possibly treatment-related.
Statistical Analysis
The trial was designed to test whether concurrent chemotherapyand radiotherapy or radiotherapy alone resulted in higher ratesof laryngeal preservation than that achieved with standard inductionchemotherapy followed by radiotherapy. Since the protocol involvedthe comparison of two groups receiving experimental treatmentswith a single control group, Dunnett's two-sided test7 was usedto adjust for multiple comparisons. The sample size was calculatedwith the use of Bristol's modification.8 The study was designedto detect an absolute difference of 15 percent with type I andtype II error rates of 0.05 and 0.20. The sample size was furtherincreased by 10 percent to account for patients deemed ineligibleor lost to follow-up before two years had elapsed. The targetedsample size was 546 patients, assuming a two-year laryngectomy-freesurvival rate of 65 percent.
Rates of overall survival, disease-free survival, and laryngectomy-freesurvival were estimated by means of the Kaplan–Meier methodwith the log-rank test.9 Rates of laryngeal preservation, localcontrol, locoregional control, and distant metastasis were estimatedby the method of cumulative incidence10 and were tested accordingto Gray's method.11
Differences in the timing of protocol-specified assessmentsof disease among the treatment groups could bias the results.For example, patients in the induction-chemotherapy group couldproceed to laryngectomy earlier than the other patients becauseof the evaluation performed at six weeks. To minimize such bias,all laryngectomies performed within the first six months afterthe start of treatment were considered to be early treatmentfailures and were analyzed as if they had occurred at the sametime.
Results
Patient Population
From August 1992 to May 2000, 547 patients were enrolled andrandomly assigned to one of the three treatment groups. Twenty-oneof these patients proved to be ineligible, one withdrew consentafter randomization, and seven were excluded because eligibilityor outcome information was not submitted. Thus, data from 518patients were included in the analysis. The characteristicsof the patients are shown in Table 1. The site of the primarytumor and stage of disease were balanced among the three treatmentgroups.
Table 1. Characteristics of the Patients According to the Treatment Group.
Toxic Effects
Severe acute toxic effects are listed in Table 2. During inductionchemotherapy with cisplatin and fluorouracil, toxicity was manifestedprimarily as neutropenia, stomatitis, and nausea or vomiting.
Table 2. Grade 3 or 4 Acute Toxic Effects, According to the Treatment Group.
The grade and frequency of toxic effects occurring during radiotherapyrecorded in the group that received induction cisplatin plusfluorouracil followed by radiotherapy and the group that receivedradiotherapy alone were nearly identical and consisted mainlyof grade 3 in-field effects on the skin and mucous membrane.In contrast, patients receiving radiotherapy with concurrentcisplatin had chemotherapy-related toxic effects (e.g., neutropeniaand nausea or vomiting) and increased rates of severe radiation-relatedmucosal, pharyngeal, and esophageal effects.
The incidence of grade 3 or 4 late toxic effects was 24 percentin the group that received induction cisplatin plus fluorouracilfollowed by radiotherapy, 30 percent in the group that receivedradiotherapy with concurrent cisplatin, and 36 percent in thegroup that received radiotherapy alone. Most of these effectswere grade 3 and referable to the larynx, pharynx and esophagus,salivary glands, and subcutaneous tissues.
The total rates of severe toxic effects (acute and late) reportedfor all phases of the study were 81 percent in the group assignedto induction cisplatin plus fluorouracil followed by radiotherapy,82 percent in the group assigned to radiotherapy with concurrentcisplatin, and 61 percent in the group assigned to radiotherapyalone. The total numbers of deaths that may have been relatedto treatment were five (3 percent), nine (5 percent), and five(3 percent), respectively; the relation of the death to treatmentwas confirmed for four, eight, and two of these deaths, respectively.
Response to Treatment and Compliance
A total of 168 of the 173 patients assigned to receive inductioncisplatin plus fluorouracil followed by radiotherapy receivedinduction chemotherapy. The response of the primary tumor aftertwo courses of cisplatin and fluorouracil was complete in 36of these patients (21 percent) and partial in 108 (64 percent).Eighty-four patients had nodal involvement, and the responsewas complete in 19 of them (23 percent), partial in 34 (40 percent),and stable in 15 (18 percent). Thus, 144 patients could proceedto receive a third course of chemotherapy and a full courseof radiotherapy. Of these, 134 received the third course; theremaining 10 discontinued chemotherapy.
Among the 24 patients in whom the response of the primary tumorto induction chemotherapy was less than partial, only 7 proceededto immediate laryngectomy. Of the remaining 17 patients, 11received additional chemotherapy or radiotherapy. All 11 hada complete response, and only 1 subsequently required a laryngectomy.Of the 172 patients randomly assigned to receive radiotherapywith concurrent cisplatin, 120 (70 percent) received all threeplanned doses of cisplatin and 40 (23 percent) received twodoses.
Most of the patients (84 percent of those assigned to inductioncisplatin plus fluorouracil followed by radiotherapy, 91 percentof those assigned to radiotherapy with concurrent cisplatin,and 94 percent of those assigned to radiotherapy alone) receivedmore than 95 percent of the intended dose of radiotherapy (i.e.,at least 67 Gy). At the completion of radiotherapy, 150 of thepatients assigned to induction cisplatin plus fluorouracil followedby radiotherapy, 154 of those assigned to radiotherapy withconcurrent cisplatin, and 148 of those assigned to radiotherapyalone had had a complete response.
Preservation of the Larynx
The rate of laryngeal preservation at a median follow-up of3.8 years was significantly higher among patients receivingradiotherapy with concurrent cisplatin (145 of 172 patients[84 percent]) than among those receiving induction chemotherapyfollowed by radiotherapy (125 of 173 patients [72 percent],P=0.005) or radiotherapy alone (116 of 173 patients [67 percent],P<0.001). There was no significant difference between thegroup receiving induction chemotherapy followed by radiotherapyand the group receiving radiotherapy alone (P=0.27) (Figure 1).
Figure 1. Rates of Laryngeal Preservation According to the Treatment Group.
At two years, the rates of laryngeal preservation were as follows: 75 percent (95 percent confidence interval, 68 to 81 percent) among the patients who received induction cisplatin plus fluorouracil followed by radiotherapy, 88 percent (95 percent confidence interval, 83 to 93 percent) among those who received radiotherapy with concurrent cisplatin, and 70 percent (95 percent confidence interval, 63 to 76 percent) among those who received radiotherapy alone (P=0.005 for the comparison between induction cisplatin plus fluorouracil followed by radiotherapy and radiotherapy with concurrent cisplatin, P=0.27 for the comparison between induction cisplatin plus fluorouracil followed by radiotherapy and radiotherapy alone, and P<0.001 for the comparison between radiotherapy with concurrent cisplatin and radiotherapy alone, by Gray's test).
Speech and Swallowing
Information on speech and swallowing collected from patientswho were disease-free and had an intact larynx was availablefrom 74 percent of those assigned to induction cisplatin plusfluorouracil followed by radiotherapy, 78 percent of those assignedto radiotherapy with concurrent cisplatin, and 80 percent ofthose assigned to radiotherapy alone. There was no differenceamong the three treatment groups with regard to speech at either12 or 24 months of follow-up. The reporting of moderate speechimpairment (difficulty in pronouncing some words and being understoodon the telephone) or worse speech impairment did not differamong the groups at one year (6 percent, 11 percent, and 13percent, respectively) or two years (3 percent, 6 percent, and8 percent, respectively).
For the composite end point of laryngectomy-free survival (onwhich the sample size of the trial was predicated), either laryngectomyor death from any cause constituted treatment failure. The two-yearand five-year estimated rates of this end point were 59 percentand 43 percent, respectively, for patients assigned to inductioncisplatin plus fluorouracil followed by radiotherapy, 66 percentand 45 percent for those assigned to radiotherapy with concurrentcisplatin, and 53 percent and 38 percent for those assignedto radiotherapy alone. The protocol-specified test of statisticalsignificance did not yield a significant difference (P<0.05)in pairwise comparisons between induction cisplatin plus fluorouracilfollowed by radiotherapy and radiotherapy with concurrent cisplatin(P=0.49) or between induction cisplatin plus fluorouracil followedby radiotherapy and radiotherapy alone (P=0.08). However, therewas a significant difference in laryngectomy-free survival whenconcurrent radiotherapy and cisplatin was compared with radiotherapyalone (P=0.01).
Survival Outcomes
The median follow-up among surviving patients was 3.8 years.Two-year and five-year estimates of overall survival did notdiffer significantly according to the treatment: they were 76percent and 55 percent, respectively, for induction cisplatinplus fluorouracil followed by radiotherapy, 74 percent and 54percent for radiotherapy with concurrent cisplatin, and 75 percentand 56 percent for radiotherapy alone. Two-year and five-yearestimates of disease-free survival were 52 percent and 38 percent,respectively, for induction cisplatin plus fluorouracil followedby radiotherapy, 61 percent and 36 percent for radiotherapywith concurrent cisplatin, and 44 percent and 27 percent forradiotherapy alone. Patients who received chemotherapy had significantlyimproved disease-free survival as compared with those who receivedradiotherapy alone (P=0.02 for the comparison between inductioncisplatin plus fluorouracil followed by radiotherapy and radiotherapyalone, and P=0.006 for the comparison between radiotherapy withconcurrent cisplatin and radiotherapy alone).
Pattern of Failure
At two years, the number of local treatment failures was 61for induction cisplatin plus fluorouracil followed by radiotherapy,35 for radiotherapy with concurrent cisplatin, and 72 for radiotherapyalone. The rates of local control were 64 percent, 80 percent,and 58 percent, respectively. Patients who received radiotherapywith concurrent cisplatin had significantly fewer failures thanthose who received induction cisplatin plus fluorouracil followedby radiotherapy (P=0.004) and significantly fewer than thosewho received radiotherapy alone (P<0.001). There was no significantdifference with respect to treatment failures between patientswho received induction cisplatin plus fluorouracil followedby radiotherapy and those who received radiotherapy alone (P=0.15).Locoregional control was significantly better among the patientswho received radiotherapy with concurrent cisplatin than amongthose who received either of the other treatments (Figure 2).
Figure 2. Rates of Locoregional Control According to the Treatment Group.
At two years, the rates of locoregional control were as follows: 61 percent (95 percent confidence interval, 54 to 69 percent) among the patients who received induction cisplatin plus fluorouracil followed by radiotherapy, 78 percent (95 percent confidence interval, 72 to 85 percent) among those who received radiotherapy with concurrent cisplatin, and 56 percent (95 percent confidence interval, 48 to 63 percent) among those who received radiotherapy alone (P=0.003 for the comparison between induction cisplatin plus fluorouracil followed by radiotherapy and radiotherapy with concurrent cisplatin, P=0.16 for the comparison between induction cisplatin plus fluorouracil followed by radiotherapy and radiotherapy alone, and P<0.001 for the comparison between radiotherapy with concurrent cisplatin and radiotherapy alone).
Distant Metastasis
Chemotherapy reduced the rate of distant metastasis. At twoyears, distant metastases had developed in 9 percent of thepatients who had received induction cisplatin plus fluorouracilfollowed by radiotherapy, 8 percent of those who had receivedradiotherapy with concurrent cisplatin, and 16 percent of thosewho had received radiotherapy alone. At five years, the cumulativerecurrence rates were 15 percent, 12 percent, and 22 percent,respectively. Overall, only the difference between the ratesamong those who received radiotherapy with concurrent cisplatinand those who received radiotherapy alone was significant (P=0.03).
Supported by research grants (CA21661, CA37422, CA32115, CA06294,CA-32102, CA-20319, CA-46282, and CA49957) from the NationalCancer Institute.
We are indebted to Dr. Victor Marcial for the development ofthis trial; to the clinical investigators, statisticians, clinicalresearch associates, administrative staff, and dosimetristswho contributed to the success of this trial for their dedicationand hard work; to Mr. Brian A. Berkey for contributions to thestatistical analysis; to Ms. JoAnn Stetz and Ms. Rebecca Allegrettofor contributions to data management; and to Ms. Elizabeth Martinfor contributions to quality assurance.
Source Information
From the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore (A.A.F., D.-J.L.); the University of Texas M.D. Anderson Cancer Center, Houston (H.G., M.M., R.W., W.M., B.G., C.C.); Radiation Therapy Oncology Group Headquarters, Philadelphia (T.F.P.); the H. Lee Moffitt Cancer Center and Research Institute, University of South Florida, Tampa (A.T.); Fox Chase Cancer Center, Philadelphia (J.A.R.); the Department of Radiation Oncology, University of Alabama, Birmingham (G.P.); the Department of Veterans Affairs New York Harbor Healthcare System, Brooklyn (A.L.); the Karmanos Cancer Institute, Wayne State University School of Medicine, Detroit (J.E.); and the Department of Radiation Oncology, New York University Medical Center, New York (J.C.).
Address reprint requests to Dr. Forastiere at the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, 1650 Orleans St., Suite G90, Baltimore, MD 21231-1000, or at af{at}jhmi.edu.
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(2006). Postoperative radiotherapy for squamous cell carcinoma of the head and neck.. Clin Med Res
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Pfister, D. G., Laurie, S. A., Weinstein, G. S., Mendenhall, W. M., Adelstein, D. J., Ang, K. K., Clayman, G. L., Fisher, S. G., Forastiere, A. A., Harrison, L. B., Lefebvre, J.-L., Leupold, N., List, M. A., O'Malley, B. O., Patel, S., Posner, M. R., Schwartz, M. A., Wolf, G. T.
(2006). American Society of Clinical Oncology Clinical Practice Guideline for the Use of Larynx-Preservation Strategies in the Treatment of Laryngeal Cancer. JCO
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Cohen, E. E.W., Haraf, D. J., List, M. A., Kocherginsky, M., Mittal, B. B., Rosen, F., Brockstein, B., Williams, R., Witt, M. E., Stenson, K. M., Kies, M. S., Vokes, E. E.
(2006). High Survival and Organ Function Rates After Primary Chemoradiotherapy for Intermediate-Stage Squamous Cell Carcinoma of the Head and Neck Treated in a Multicenter Phase II Trial. JCO
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(2006). Head and Neck Cancer: Recent Advances and New Standards of Care. JCO
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(2006). Concurrent Chemoradiotherapy for Locally Advanced, Nonmetastatic, Squamous Carcinoma of the Head and Neck: Consensus, Controversy, and Conundrum. JCO
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(2006). Does Induction Chemotherapy Have a Role in the Management of Locoregionally Advanced Squamous Cell Head and Neck Cancer?. JCO
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(2006). Locally Recurrent, Previously Irradiated Head and Neck Cancer: Concurrent Re-Irradiation and Chemotherapy, or Chemotherapy Alone?. JCO
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(2006). Rate of pathologic complete responses to docetaxel, Cisplatin, and Fluorouracil induction chemotherapy in patients with squamous cell carcinoma of the head and neck.. Arch Otolaryngol Head Neck Surg
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Lu, S.-L., Herrington, H., Reh, D., Weber, S., Bornstein, S., Wang, D., Li, A. G., Tang, C.-F., Siddiqui, Y., Nord, J., Andersen, P., Corless, C. L., Wang, X.-J.
(2006). Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma.. Genes Dev.
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(2006). Examining the need for neck dissection in the era of chemoradiation therapy for advanced head and neck cancer.. Arch Otolaryngol Head Neck Surg
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Gelbard, A., Garnett, C. T., Abrams, S. I., Patel, V., Gutkind, J. S., Palena, C., Tsang, K.-Y., Schlom, J., Hodge, J. W.
(2006). Combination Chemotherapy and Radiation of Human Squamous Cell Carcinoma of the Head and Neck Augments CTL-Mediated Lysis.. Clin. Cancer Res.
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(2006). Head and neck cancer in primary care: presenting symptoms and the effect of delayed diagnosis of cancer cases.. CMAJ
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(2006). Multiagent Concurrent Chemoradiotherapy for Locoregionally Advanced Squamous Cell Head and Neck Cancer: Mature Results From a Single Institution. JCO
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(2006). Induction Chemotherapy for Larynx Preservation: Patient Selection or Therapeutic Effect?. JCO
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Yang, M.-H., Chiang, W.-C., Chou, T.-Y., Chang, S.-Y., Chen, P.-M., Teng, S.-C., Wu, K.-J.
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(2005). Induction Redux: Once More With Taxanes. JCO
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(2005). Phase III Study Comparing Cisplatin Plus Fluorouracil to Paclitaxel, Cisplatin, and Fluorouracil Induction Chemotherapy Followed by Chemoradiotherapy in Locally Advanced Head and Neck Cancer. JCO
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(2005). Mitomycin and Fluorouracil in Combination with Concomitant Radiotherapy: A Potentially Curable Approach for Locally Advanced Head and Neck Squamous Cell Carcinoma. Jpn J Clin Oncol
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(2005). Long-term Quality of Life for Surgical and Nonsurgical Treatment of Head and Neck Cancer. Arch Otolaryngol Head Neck Surg
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(2005). Paradigm Shift in the Treatment of Head and Neck Cancer: The Role of Neoadjuvant Chemotherapy. The Oncologist
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Wee, J., Tan, E. H., Tai, B. C., Wong, H. B., Leong, S. S., Tan, T., Chua, E. T., Yang, E., Lee, K. M., Fong, K. W., Tan, H. S. K., Lee, K. S., Loong, S., Sethi, V., Chua, E. J., Machin, D.
(2005). Randomized Trial of Radiotherapy Versus Concurrent Chemoradiotherapy Followed by Adjuvant Chemotherapy in Patients With American Joint Committee on Cancer/International Union Against Cancer Stage III and IV Nasopharyngeal Cancer of the Endemic Variety. JCO
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Enepekides, D. J.
(2005). Concurrent Chemoradiotherapy as the Most Appropriate Treatment for Most T3 Laryngeal Carcinomas. Arch Otolaryngol Head Neck Surg
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(2005). Concurrent Chemoradiation as a Treatment Option for Advanced-Stage Laryngeal Cancers. Arch Otolaryngol Head Neck Surg
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Johnson, J. T.
(2005). American Head and Neck Society Presidential Address: Head and Neck Surgery in a New Era of Therapeutic Potential. Arch Otolaryngol Head Neck Surg
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(2005). Laryngeal Penetration and Aspiration During Swallowing After the Treatment of Advanced Oropharyngeal Cancer. Arch Otolaryngol Head Neck Surg
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Yin, X., Zhang, H., Burrows, F., Zhang, L., Shores, C. G.
(2005). Potent Activity of a Novel Dimeric Heat Shock Protein 90 Inhibitor against Head and Neck Squamous Cell Carcinoma In vitro and In vivo. Clin. Cancer Res.
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Ang, K. K., Harris, J., Garden, A. S., Trotti, A., Jones, C. U., Carrascosa, L., Cheng, J. D., Spencer, S. S., Forastiere, A., Weber, R. S.
(2005). Concomitant Boost Radiation Plus Concurrent Cisplatin for Advanced Head and Neck Carcinomas: Radiation Therapy Oncology Group Phase II Trial 99-14. JCO
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Roh, J.-L., Kim, A.-Y., Cho, M. J.
(2005). Xerostomia Following Radiotherapy of the Head and Neck Affects Vocal Function. JCO
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Bucci, M. K., Bevan, A., Roach, M. III
(2005). Advances in Radiation Therapy: Conventional to 3D, to IMRT, to 4D, and Beyond. CA Cancer J Clin
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Posner, M. R.
(2005). Adjuvant Post-Operative Chemoradiotherapy In Head and Neck Cancer: A Standard Of Care?. The Oncologist
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Garden, A. S.
(2005). Is There Still a Role for Induction Chemotherapy for Head and Neck Cancer?. JCO
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Rischin, D., Peters, L., Fisher, R., Macann, A., Denham, J., Poulsen, M., Jackson, M., Kenny, L., Penniment, M., Corry, J., Lamb, D., McClure, B.
(2005). Tirapazamine, Cisplatin, and Radiation Versus Fluorouracil, Cisplatin, and Radiation in Patients With Locally Advanced Head and Neck Cancer: A Randomized Phase II Trial of the Trans-Tasman Radiation Oncology Group (TROG 98.02). JCO
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Urba, S. G., Moon, J., Giri, P.G. S., Adelstein, D. J., Hanna, E., Yoo, G. H., LeBlanc, M., Ensley, J. F., Schuller, D. E.
(2005). Organ Preservation for Advanced Resectable Cancer of the Base of Tongue and Hypopharynx: A Southwest Oncology Group Trial. JCO
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Lefebvre, J.-L.
(2005). Current clinical outcomes demand new treatment options for SCCHN. Ann Oncol
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Ang, K. K.
(2004). Concurrent Radiation Chemotherapy for Locally Advanced Head and Neck Carcinoma: Are We Addressing Burning Subjects?. JCO
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(2004). Is There a New Role for Induction Chemotherapy in the Treatment of Head and Neck Cancer?. JNCI J Natl Cancer Inst
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Zorat, P. L., Paccagnella, A., Cavaniglia, G., Loreggian, L., Gava, A., Mione, C. A., Boldrin, F., Marchiori, C., Lunghi, F., Fede, A., Bordin, A., Da Mosto, M. C., Sileni, V. C., Orlando, A., Jirillo, A., Tomio, L., Pappagallo, G. L., Ghi, M. G.
(2004). Randomized Phase III Trial of Neoadjuvant Chemotherapy in Head and Neck Cancer: 10-Year Follow-Up. JNCI J Natl Cancer Inst
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Dufour, X., Hans, S., De Mones, E., Brasnu, D., Menard, M., Laccourreye, O.
(2004). Local Control After Supracricoid Partial Laryngectomy for "Advanced" Endolaryngeal Squamous Cell Carcinoma Classified as T3. Arch Otolaryngol Head Neck Surg
130: 1092-1099
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Psyrri, A., Kwong, M., DiStasio, S., Lekakis, L., Kassar, M., Sasaki, C., Wilson, L.D., Haffty, B.G., Son, Y.H., Ross, D.A., Weinberger, P.M., Chung, G.G., Zelterman, D., Burtness, B.A., Cooper, D.L.
(2004). Cisplatin, Fluorouracil, and Leucovorin Induction Chemotherapy Followed by Concurrent Cisplatin Chemoradiotherapy for Organ Preservation and Cure in Patients With Advanced Head and Neck Cancer: Long-Term Follow-Up. JCO
22: 3061-3069
[Abstract][Full Text]
Brockstein, B., Haraf, D. J., Rademaker, A. W., Kies, M. S., Stenson, K. M., Rosen, F., Mittal, B. B., Pelzer, H., Fung, B. B., Witt, M.-E., Wenig, B., Portugal, L., Weichselbaum, R. W., Vokes, E. E.
(2004). Patterns of failure, prognostic factors and survival in locoregionally advanced head and neck cancer treated with concomitant chemoradiotherapy: a 9-year, 337-patient, multi-institutional experience. Ann Oncol
15: 1179-1186
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Milano, M. T., Haraf, D. J., Stenson, K. M., Witt, M. E., Eng, C., Mittal, B. B., Argiris, A., Pelzer, H., Kozloff, M. F., Vokes, E. E.
(2004). Phase I Study of Concomitant Chemoradiotherapy with Paclitaxel, Fluorouracil, Gemcitabine, and Twice-Daily Radiation in Patients with Poor-Prognosis Cancer of the Head and Neck. Clin. Cancer Res.
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Garden, A.S., Harris, J., Vokes, E.E., Forastiere, A.A., Ridge, J.A., Jones, C., Horwitz, E.M., Glisson, B.S., Nabell, L., Cooper, J.S., Demas, W., Gore, E.
(2004). Preliminary Results of Radiation Therapy Oncology Group 97-03: A Randomized Phase II Trial of Concurrent Radiation and Chemotherapy for Advanced Squamous Cell Carcinomas of the Head and Neck. JCO
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(2004). Intensive Chemoradiotherapy as a Primary Treatment for Organ Preservation in Patients With Advanced Cancer of the Head and Neck: Efficacy, Toxic Effects, and Limitations. Arch Otolaryngol Head Neck Surg
130: 861-867
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Hanna, E., Sherman, A., Cash, D., Adams, D., Vural, E., Fan, C.-Y., Suen, J. Y.
(2004). Quality of Life for Patients Following Total Laryngectomy vs Chemoradiation for Laryngeal Preservation. Arch Otolaryngol Head Neck Surg
130: 875-879
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Cooper, J. S., Pajak, T. F., Forastiere, A. A., Jacobs, J., Campbell, B. H., Saxman, S. B., Kish, J. A., Kim, H. E., Cmelak, A. J., Rotman, M., Machtay, M., Ensley, J. F., Chao, K.S. C., Schultz, C. J., Lee, N., Fu, K. K., the Radiation Therapy Oncology Group 9501/Intergro,
(2004). Postoperative Concurrent Radiotherapy and Chemotherapy for High-Risk Squamous-Cell Carcinoma of the Head and Neck. NEJM
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Cohen, E. E.W., Lingen, M. W., Vokes, E. E.
(2004). The Expanding Role of Systemic Therapy in Head and Neck Cancer. JCO
22: 1743-1752
[Abstract][Full Text]
Weinstein, G. S., Myers, E. N., Shapshay, S. M., Colvett, K. T., Gupta, T., Agarwal, J., Lashkar, S. G., Langer, M., Guntinas-Lichius, O., Haddad, R. I., Tishler, R. B., Posner, M. R., Forastiere, A. A., Pajak, T. F., Maor, M., Weber, R.
(2004). Nonsurgical Treatment of Laryngeal Cancer. NEJM
350: 1049-1053
[Full Text]
A correction has been published: N Engl J Med 2004;350(10):1049.
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