Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial

doi:10.1016/S0140-6736(18)32779-X

Randomized Controlled Trial

. 2019 Jan 5;393(10166):40-50.

doi: 10.1016/S0140-6736(18)32779-X. Epub 2018 Nov 15.

Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial

Maura L Gillison¹, Andy M Trotti², Jonathan Harris³, Avraham Eisbruch⁴, Paul M Harari⁵, David J Adelstein⁶, Richard C K Jordan⁷, Weiqiang Zhao⁸, Erich M Sturgis⁹, Barbara Burtness¹⁰, John A Ridge¹¹, Jolie Ringash¹², James Galvin¹³, Min Yao¹⁴, Shlomo A Koyfman¹⁵, Dukagjin M Blakaj¹⁶, Mohammed A Razaq¹⁷, A Dimitrios Colevas¹⁸, Jonathan J Beitler¹⁹, Christopher U Jones²⁰, Neal E Dunlap²¹, Samantha A Seaward²², Sharon Spencer²³, Thomas J Galloway²⁴, Jack Phan²⁵, James J Dignam²⁶, Quynh Thu Le²⁷

Affiliations

¹ Department of Thoracic Head and Neck Medical Oncology, MD Anderson Cancer Center, Houston, TX, USA. Electronic address: mgillison@mdanderson.org.
² Department of Radiation Oncology, Moffitt Cancer Center, Tampa, FL, USA.
³ NRG Oncology Statistics and Data Management Center, American College of Radiology, Philadelphia, PA, USA.
⁴ Department of Radiation Oncology, University of Michigan Comprehensive Cancer Center, Ann Arbor, MI, USA.
⁵ Department of Human Oncology, University of Wisconsin Hospital and Clinics, Madison, WI, USA.
⁶ Department of Hematology and Medical Oncology, Cleveland Clinic Taussig Cancer Institute, Cleveland, OH, USA.
⁷ Department of Orofacial Sciences, University of California San Fransisco, San Francisco, CA, USA; Department of Pathology, University of California San Fransisco, San Francisco, CA, USA.
⁸ Division of Molecular Pathology, Department of Pathology, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Division of Hematopathology, Department of Pathology, The Ohio State University Wexner Medical Center, Columbus, OH, USA; James Molecular Laboratory, Columbus, OH, USA.
⁹ Department of Head and Neck Surgery, MD Anderson Cancer Center, Houston, TX, USA.
¹⁰ Department of Medicine, Yale School of Medicine and Yale Cancer Center, New Haven, CT, USA.
¹¹ Department of Surgical Oncology, Fox Chase Cancer Center, Philadelphia, PA, USA.
¹² Department of Radiation Oncology, Princess Margaret Cancer Centre and the University of Toronto, Toronto, ON, Canada.
¹³ Imaging and Radiation Oncology Core Group, Philadelphia, PA, USA.
¹⁴ Department of Radiation Oncology, Case Western Reserve/University Hospitals Seidman Cancer Center, Cleveland, OH, USA.
¹⁵ Department of Radiation Oncology, Cleveland Clinic Taussig Cancer Institute, Cleveland, OH, USA.
¹⁶ Department of Radiation Oncology, The Ohio State University, Columbus, OH, USA.
¹⁷ Department of Hematology/Oncology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
¹⁸ Department of Medicine (Oncology), Stanford University, Stanford, CA, USA.
¹⁹ Department of Radiation Oncology, Emory University, Atlanta, GA, USA.
²⁰ Department of Radiation Oncology, Sutter Cancer Research Consortium, Novato, CA, USA.
²¹ Department of Radiation Oncology, James Graham Brown Cancer Center, University of Louisville, Louisville, KY, USA.
²² Department of Radiation Oncology, Kaiser Permanente, Oakland, CA, USA.
²³ Department of Radiation Oncology, University of Alabama at Birmingham Medical Center, Birmingham, AL, USA.
²⁴ Department of Radiation Oncology, Fox Chase Cancer Center, Philadelphia, PA, USA.
²⁵ Department of Radiation Oncology, MD Anderson Cancer Center, Houston, TX, USA.
²⁶ Department of Public Health Sciences, University of Chicago, Chicago, IL, USA; NRG Oncology Statistics and Data Management Center, American College of Radiology, Philadelphia, PA, USA.
²⁷ Department of Radiation Oncology, Stanford University, Stanford, CA, USA.

PMID: 30449625
PMCID: PMC6541928
DOI: 10.1016/S0140-6736(18)32779-X

Randomized Controlled Trial

Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial

Maura L Gillison et al. Lancet. 2019.

. 2019 Jan 5;393(10166):40-50.

doi: 10.1016/S0140-6736(18)32779-X. Epub 2018 Nov 15.

Authors

Affiliations

¹ Department of Thoracic Head and Neck Medical Oncology, MD Anderson Cancer Center, Houston, TX, USA. Electronic address: mgillison@mdanderson.org.
² Department of Radiation Oncology, Moffitt Cancer Center, Tampa, FL, USA.
³ NRG Oncology Statistics and Data Management Center, American College of Radiology, Philadelphia, PA, USA.
⁴ Department of Radiation Oncology, University of Michigan Comprehensive Cancer Center, Ann Arbor, MI, USA.
⁵ Department of Human Oncology, University of Wisconsin Hospital and Clinics, Madison, WI, USA.
⁶ Department of Hematology and Medical Oncology, Cleveland Clinic Taussig Cancer Institute, Cleveland, OH, USA.
⁷ Department of Orofacial Sciences, University of California San Fransisco, San Francisco, CA, USA; Department of Pathology, University of California San Fransisco, San Francisco, CA, USA.
⁸ Division of Molecular Pathology, Department of Pathology, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Division of Hematopathology, Department of Pathology, The Ohio State University Wexner Medical Center, Columbus, OH, USA; James Molecular Laboratory, Columbus, OH, USA.
⁹ Department of Head and Neck Surgery, MD Anderson Cancer Center, Houston, TX, USA.
¹⁰ Department of Medicine, Yale School of Medicine and Yale Cancer Center, New Haven, CT, USA.
¹¹ Department of Surgical Oncology, Fox Chase Cancer Center, Philadelphia, PA, USA.
¹² Department of Radiation Oncology, Princess Margaret Cancer Centre and the University of Toronto, Toronto, ON, Canada.
¹³ Imaging and Radiation Oncology Core Group, Philadelphia, PA, USA.
¹⁴ Department of Radiation Oncology, Case Western Reserve/University Hospitals Seidman Cancer Center, Cleveland, OH, USA.
¹⁵ Department of Radiation Oncology, Cleveland Clinic Taussig Cancer Institute, Cleveland, OH, USA.
¹⁶ Department of Radiation Oncology, The Ohio State University, Columbus, OH, USA.
¹⁷ Department of Hematology/Oncology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
¹⁸ Department of Medicine (Oncology), Stanford University, Stanford, CA, USA.
¹⁹ Department of Radiation Oncology, Emory University, Atlanta, GA, USA.
²⁰ Department of Radiation Oncology, Sutter Cancer Research Consortium, Novato, CA, USA.
²¹ Department of Radiation Oncology, James Graham Brown Cancer Center, University of Louisville, Louisville, KY, USA.
²² Department of Radiation Oncology, Kaiser Permanente, Oakland, CA, USA.
²³ Department of Radiation Oncology, University of Alabama at Birmingham Medical Center, Birmingham, AL, USA.
²⁴ Department of Radiation Oncology, Fox Chase Cancer Center, Philadelphia, PA, USA.
²⁵ Department of Radiation Oncology, MD Anderson Cancer Center, Houston, TX, USA.
²⁶ Department of Public Health Sciences, University of Chicago, Chicago, IL, USA; NRG Oncology Statistics and Data Management Center, American College of Radiology, Philadelphia, PA, USA.
²⁷ Department of Radiation Oncology, Stanford University, Stanford, CA, USA.

PMID: 30449625
PMCID: PMC6541928
DOI: 10.1016/S0140-6736(18)32779-X

Erratum in

Department of Error.
[No authors listed] [No authors listed] Lancet. 2020 Mar 7;395(10226):784. doi: 10.1016/S0140-6736(20)30454-2. Lancet. 2020. PMID: 32145794 No abstract available.

Abstract

Background: Patients with human papillomavirus (HPV)-positive oropharyngeal squamous cell carcinoma have high survival when treated with radiotherapy plus cisplatin. Whether replacement of cisplatin with cetuximab-an antibody against the epidermal growth factor receptor-can preserve high survival and reduce treatment toxicity is unknown. We investigated whether cetuximab would maintain a high proportion of patient survival and reduce acute and late toxicity.

Methods: RTOG 1016 was a randomised, multicentre, non-inferiority trial at 182 health-care centres in the USA and Canada. Eligibility criteria included histologically confirmed HPV-positive oropharyngeal carcinoma; American Joint Committee on Cancer 7th edition clinical categories T1-T2, N2a-N3 M0 or T3-T4, N0-N3 M0; Zubrod performance status 0 or 1; age at least 18 years; and adequate bone marrow, hepatic, and renal function. We randomly assigned patients (1:1) to receive either radiotherapy plus cetuximab or radiotherapy plus cisplatin. Randomisation was balanced by using randomly permuted blocks, and patients were stratified by T category (T1-T2 vs T3-T4), N category (N0-N2a vs N2b-N3), Zubrod performance status (0 vs 1), and tobacco smoking history (≤10 pack-years vs >10 pack-years). Patients were assigned to receive either intravenous cetuximab at a loading dose of 400 mg/m² 5-7 days before radiotherapy initiation, followed by cetuximab 250 mg/m² weekly for seven doses (total 2150 mg/m²), or cisplatin 100 mg/m² on days 1 and 22 of radiotherapy (total 200 mg/m²). All patients received accelerated intensity-modulated radiotherapy delivered at 70 Gy in 35 fractions over 6 weeks at six fractions per week (with two fractions given on one day, at least 6 h apart). The primary endpoint was overall survival, defined as time from randomisation to death from any cause, with non-inferiority margin 1·45. Primary analysis was based on the modified intention-to-treat approach, whereby all patients meeting eligibility criteria are included. This study is registered with ClinicalTrials.gov, number NCT01302834.

Findings: Between June 9, 2011, and July 31, 2014, 987 patients were enrolled, of whom 849 were randomly assigned to receive radiotherapy plus cetuximab (n=425) or radiotherapy plus cisplatin (n=424). 399 patients assigned to receive cetuximab and 406 patients assigned to receive cisplatin were subsequently eligible. After median follow-up duration of 4·5 years, radiotherapy plus cetuximab did not meet the non-inferiority criteria for overall survival (hazard ratio [HR] 1·45, one-sided 95% upper CI 1·94; p=0·5056 for non-inferiority; one-sided log-rank p=0·0163). Estimated 5-year overall survival was 77·9% (95% CI 73·4-82·5) in the cetuximab group versus 84·6% (80·6-88·6) in the cisplatin group. Progression-free survival was significantly lower in the cetuximab group compared with the cisplatin group (HR 1·72, 95% CI 1·29-2·29; p=0·0002; 5-year progression-free survival 67·3%, 95% CI 62·4-72·2 vs 78·4%, 73·8-83·0), and locoregional failure was significantly higher in the cetuximab group compared with the cisplatin group (HR 2·05, 95% CI 1·35-3·10; 5-year proportions 17·3%, 95% CI 13·7-21·4 vs 9·9%, 6·9-13·6). Proportions of acute moderate to severe toxicity (77·4%, 95% CI 73·0-81·5 vs 81·7%, 77·5-85·3; p=0·1586) and late moderate to severe toxicity (16·5%, 95% CI 12·9-20·7 vs 20·4%, 16·4-24·8; p=0·1904) were similar between the cetuximab and cisplatin groups.

Interpretation: For patients with HPV-positive oropharyngeal carcinoma, radiotherapy plus cetuximab showed inferior overall survival and progression-free survival compared with radiotherapy plus cisplatin. Radiotherapy plus cisplatin is the standard of care for eligible patients with HPV-positive oropharyngeal carcinoma.

Funding: National Cancer Institute USA, Eli Lilly, and The Oral Cancer Foundation.

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Figures

**Figure 1A.. Overall Survival According to Assigned Treatment.**
Kaplan-Meier estimates of overall survival are shown according to assigned treatment. After a median follow-up of 4·5 years (range, 0·01-6·5), there were 133 deaths; 78 in the cetuximab group and 55 in the cisplatin group. Radiotherapy plus cetuximab did not meet the criterion for non-inferiority in comparison to radiotherapy plus cisplatin: the hazard ratio was 1·45 with 1-sided 95% upper confidence bound 1·94 (p=0·5056 for non-inferiority). In addition, survival was significantly worse with cetuximab (p=0·0163; 2-sided 95%CI 1·03-2·05). The 5-year estimates were 77·9% (95%CI 73·4-82·5) with cetuximab and 84·6% (95%CI 80·6-88·6) with cisplatin.

**Figure 1B.. Overall Survival Treatment Effect in Subgroups.**
Hazard ratios and 5-year overall survival estimates are shown for subgroups. Risk groups are as defined in RTOG 0129. Low-risk is ≤ 10 pack-years (any N stage) or > 10 pack-years and N0-N2a. Intermediate-risk is > 10 pack-years and N2b-N3. The reference line is at 1·45, the upper bound required for non-inferiority. P-values are for the test for interaction between treatment and subgroup. There is a large difference in the treatment effect for Zubrod 0 and 1: The hazard ratio is 1·08 (1-sided 95% upper confidence bound 1·55) for Zubrod 0 and 2·66 (4·32) for Zubrod 1. The test for interaction is not significant after adjustment for multiple comparisons. Abbreviations: CI, confidence interval.

**Figure 2A.. Progression-Free Survival According to Assigned Treatment.**
Kaplan-Meier estimates of progression-free survival (PFS) are shown according to assigned treatment. Patients assigned to cetuximab had significantly worse PFS (p=0·0002) than patients assigned to cisplatin. The estimated 5-year PFS rates were 67·3% (95%CI 62·4-72·2) with cetuximab and 78·4% (95%CI 73·8-83·0) with cisplatin.

**Figure 2B.. Time to Locoregional Failure According to Assigned Treatment.**
Cumulative incidence estimates of locoregional failure are shown according to assigned treatment. Patients assigned to cetuximab had significantly more locoregional failure (p=0·0005) than patients assigned to cisplatin. The estimated 5-year rates of locoregional failure were 17·3% (95%CI 13·7-21·4) with cetuximab and 9·9% (95%CI 6·9-13·6) with cisplatin.

**Figure 3A.. Treatment-Related Grade 3-4 Adverse Event Rates Over Time According to Assigned Treatment.**
Percentages of patients with treatment-related grade 3-4 adverse events, along with 95% exact confidence intervals, are shown according to assigned treatment. Time points 1 month and later are relative to the end of treatment. The following windows around each time point were used: 1 month, −2 to +4 weeks; 3 months, −4 to +6 weeks; 6 months, −6 to +8 weeks; 1 year and later, ± 3 months. Abbreviations: AE, adverse event; CI, confidence interval; Tx, treatment.

**Figure 3B.. Feeding Tube Rates Over Time According to Assigned Treatment.**
Percentages of patients with a feeding tube, along with 95% exact confidence intervals, are shown according to assigned treatment. Time points 1 month and later are relative to the end of treatment. The following windows around each time point were used: 1 month, −2 to +4 weeks; 3 months, −4 to +6 weeks; 6 months, −6 to +8 weeks; 1 year and later, ± 3 months. Abbreviations: CI, confidence interval; Tx, treatment.

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Comment in

De-intensified treatment in human papillomavirus-positive oropharyngeal cancer.
Oosthuizen JC, Doody J. Oosthuizen JC, et al. Lancet. 2019 Jan 5;393(10166):5-7. doi: 10.1016/S0140-6736(18)32930-1. Epub 2018 Nov 15. Lancet. 2019. PMID: 30449624 No abstract available.
De-Escalation Strategies in HPV-Associated Oropharynx Cancer-Are we Putting the Cart Before the Horse?
Anderson CM, Kimple RJ, Lin A, Karam SD, Margalit DN, Chua MLK. Anderson CM, et al. Int J Radiat Oncol Biol Phys. 2019 Jul 15;104(4):705-709. doi: 10.1016/j.ijrobp.2019.02.054. Int J Radiat Oncol Biol Phys. 2019. PMID: 31204653 Free PMC article. No abstract available.
[Radiochemotherapy of HPV-positive oropharyngeal carcinomas: Cisplatin is still to be prioritized].
Clement-Colmou K. Clement-Colmou K. Bull Cancer. 2020 Mar;107(3):293-294. doi: 10.1016/j.bulcan.2020.02.002. Epub 2020 Feb 26. Bull Cancer. 2020. PMID: 32113612 French. No abstract available.

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References

1. Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24–35. - PMC - PubMed
1. Pignon JP, le Maitre A, Maillard E, Bourhis J, Group M-NC. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): an update on 93 randomised trials and 17,346 patients. Radiother Oncol 2009;92:4–14. - PubMed
1. Blanchard P, Baujat B, Holostenco V, et al. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): a comprehensive analysis by tumour site. Radiother Oncol 2011;100:33–40. - PubMed
1. Adelstein DJ, Li Y, Adams GL, et al. An intergroup phase III comparison of standard radiation therapy and two schedules of concurrent chemoradiotherapy in patients with unresectable squamous cell head and neck cancer. J Clin Oncol 2003;21:92–8. - PubMed
1. Machtay M, Moughan J, Trotti A, et al. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: an RTOG analysis. J Clin Oncol 2008;26:3582–9. - PMC - PubMed

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[1] Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24–35. - PMC - PubMed

[2] Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24–35. - PMC - PubMed

[3] Pignon JP, le Maitre A, Maillard E, Bourhis J, Group M-NC. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): an update on 93 randomised trials and 17,346 patients. Radiother Oncol 2009;92:4–14. - PubMed

[4] Pignon JP, le Maitre A, Maillard E, Bourhis J, Group M-NC. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): an update on 93 randomised trials and 17,346 patients. Radiother Oncol 2009;92:4–14. - PubMed

[5] Blanchard P, Baujat B, Holostenco V, et al. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): a comprehensive analysis by tumour site. Radiother Oncol 2011;100:33–40. - PubMed

[6] Blanchard P, Baujat B, Holostenco V, et al. Meta-analysis of chemotherapy in head and neck cancer (MACH-NC): a comprehensive analysis by tumour site. Radiother Oncol 2011;100:33–40. - PubMed

[7] Adelstein DJ, Li Y, Adams GL, et al. An intergroup phase III comparison of standard radiation therapy and two schedules of concurrent chemoradiotherapy in patients with unresectable squamous cell head and neck cancer. J Clin Oncol 2003;21:92–8. - PubMed

[8] Adelstein DJ, Li Y, Adams GL, et al. An intergroup phase III comparison of standard radiation therapy and two schedules of concurrent chemoradiotherapy in patients with unresectable squamous cell head and neck cancer. J Clin Oncol 2003;21:92–8. - PubMed

[9] Machtay M, Moughan J, Trotti A, et al. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: an RTOG analysis. J Clin Oncol 2008;26:3582–9. - PMC - PubMed

[10] Machtay M, Moughan J, Trotti A, et al. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: an RTOG analysis. J Clin Oncol 2008;26:3582–9. - PMC - PubMed

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Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial

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Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial

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