Cited by 1,124Hepatocellular Carcinoma Treatment and PrognosisCancer Immunotherapy and BiomarkersColorectal Cancer Treatments and Studies

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Sintilimab plus a bevacizumab biosimilar (IBI305) versus sorafenib in unresectable hepatocellular carcinoma (ORIENT-32): a randomised, open-label, phase 2–3 study

Ren, Zhenggang, Xu, Jianming, Bai, Yuxian, Xu, Aibing, Cang, Shundong, Du, Chengyou, Li, Qiu, Lu, Yinying, Chen, Yajin, Guo, Yabing, Chen, Zhendong, Liu, Baorui, Jia, Weidong, Wu, Jian, Wang, Junye, Shao, Guoliang, Zhang, Bixiang, Shan, Yunfeng, Meng, Zhiqiang, Wu, Jianbing, Gu, Shanzhi, Yang, Wei, Liu, Chao, Shi, Xuetao, Gao, Zhenyuan, Yin, Tao, Cui, Jiuwei, Huang, Ming, Xing, Baocai, Mao, Yilei, Teng, Gaojun, Qin, Yanru, Wang, Jinhai, Xia, Feng, Yin, Guowen, Yang, Yong, Chen, Mingxia, Wang, Yan, Zhou, Hui, Fan, Jia·2021·The Lancet Oncology

DOI 10.1016/s1470-2045(21)00252-7

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Abstract

Background China has a high burden of hepatocellular carcinoma, and hepatitis B virus (HBV) infection is the main causative factor. Patients with hepatocellular carcinoma have a poor prognosis and a substantial unmet clinical need. The phase 2-3 ORIENT-32 study aimed to assess sintilimab (a PD-1 inhibitor) plus IBI305, a bevacizumab biosimilar, versus sorafenib as a first-line treatment for unresectable HBV-associated hepatocellular carcinoma.Methods This randomised, open-label, phase 2-3 study was done at 50 clinical sites in China. Patients aged 18 years or older with histologically or cytologically diagnosed or clinically confirmed unresectable or metastatic hepatocellular carcinoma, no previous systemic treatment, and a baseline Eastern Cooperative Oncology Group (ECOG) performance status of 0 or 1 were eligible for inclusion. In the phase 2 part of the study, patients received intravenous sintilimab (200 mg every 3 weeks) plus intravenous IBI305 (15 mg/kg every 3 weeks). In the phase 3 part, patients were randomly assigned (2:1) to receive either sintilimab plus IBI305 (sintilimab-bevacizumab biosimilar group) or sorafenib (400 mg orally twice daily; sorafenib group), until disease progression or unacceptable toxicity. Randomisation was done using permuted block randomisation, with a block size of six, via an interactive web response system, and stratified by macrovascular invasion or extrahepatic metastasis, baseline α-fetoprotein, and ECOG performance status. The primary endpoint of the phase 2 part of the study was safety, assessed in all patients who received at least one dose of study drug. The co-primary endpoints of the phase 3 part of the study were overall survival and independent radiological review committee (IRRC)-assessed progression-free survival according to Response Evaluation Criteria in Solid Tumors (RECIST) version 1.1 in the intention-to-treat population. The study is registered with ClinicalTrials.gov, NCT03794440. The study is closed to new participants and follow-up is ongoing for long-term outcomes.Findings Between Feb 11, 2019 and Jan 15, 2020, we enrolled 595 patients: 24 were enrolled directly into the phase 2 safety run-in and 571 were randomly assigned to sintilimab-bevacizumab biosimilar (n=380) or sorafenib (n=191). In the phase 2 part of the trial, 24 patients received at least one dose of the study drug, with an objective response rate of 25·0% (95% CI 9·8-46·7). Based on the preliminary safety and activity data of the phase 2 part, in which grade 3 or worse treatment-related adverse events occurred in seven (29%) of 24 patients, the randomised phase 3 part was started. At data cutoff (Aug 15, 2020), the median follow-up was 10·0 months (IQR 8·5-11·7) in the sintilimab-bevacizumab biosimilar group and 10·0 months (8·4-11·7) in the sorafenib group. Patients in the sintilimab-bevacizumab biosimilar group had a significantly longer IRRC-assessed median progression-free survival (4·6 months [95% CI 4·1-5·7]) than did patients in the sorafenib group (2·8 months [2·7-3·2]; stratified hazard ratio [HR] 0·56, 95% CI 0·46-0·70; p<0·0001). In the first interim analysis of overall survival, sintilimab-bevacizumab biosimilar showed a significantly longer overall survival than did sorafenib (median not reached [95% CI not reached-not reached] vs 10·4 months [8·5-not reached]; HR 0·57, 95% CI 0·43-0·75; p<0·0001). The most common grade 3-4 treatment-emergent adverse events were hypertension (55 [14%] of 380 patients in the sintilimab-bevacizumab biosimilar group vs 11 [6%] of 185 patients in the sorafenib group) and palmar-plantar erythrodysaesthesia syndrome (none vs 22 [12%]). 123 (32%) patients in the sintilimab-bevacizumab biosimilar group and 36 (19%) patients in the sorafenib group had serious adverse events. Treatment-related adverse events that led to death occurred in six (2%) patients in the sintilimab-bevacizumab biosimilar group (one patient with abnormal liver function, one patient with both hepatic failure and gastrointestinal haemorrhage, one patient with interstitial lung disease, one patient with both hepatic faliure and hyperkalemia, one patient with upper gastrointestinal haemorrhage, and one patient with intestinal volvulus) and two (1%) patients in the sorafenib group (one patient with gastrointestinal haemorrhage and one patient with death of unknown cause).Interpretation Sintilimab plus IBI305 showed a significant overall survival and progression-free survival benefit versus sorafenib in the first-line setting for Chinese patients with unresectable, HBV-associated hepatocellular carcinoma, with an acceptable safety profile. This combination regimen could provide a novel treatment option for such patients.Funding Innovent Biologics.Translation For the Chinese translation of the abstract see Supplementary Materials section.

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Additional file 2 of Efficacy and safety of immune checkpoint inhibitors in Proficient Mismatch Repair (pMMR)/ Non-Microsatellite Instability-High (non-MSI-H) metastatic colorectal cancer: a study based on 39 cohorts incorporating 1723 patients
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Additional file 3 of Combination of alpha-fetoprotein and neutrophil-to-lymphocyte ratio to predict treatment response and survival outcomes of patients with unresectable hepatocellular carcinoma treated with immune checkpoint inhibitors
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Additional file 6 of Combination of alpha-fetoprotein and neutrophil-to-lymphocyte ratio to predict treatment response and survival outcomes of patients with unresectable hepatocellular carcinoma treated with immune checkpoint inhibitors
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Additional file 1 of Combination of alpha-fetoprotein and neutrophil-to-lymphocyte ratio to predict treatment response and survival outcomes of patients with unresectable hepatocellular carcinoma treated with immune checkpoint inhibitors
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Additional file 3 of Efficacy and safety of tislelizumab plus lenvatinib as first-line treatment in patients with unresectable hepatocellular carcinoma: a multicenter, single-arm, phase 2 trial
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Additional file 2 of Efficacy and safety of tislelizumab plus lenvatinib as first-line treatment in patients with unresectable hepatocellular carcinoma: a multicenter, single-arm, phase 2 trial
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Additional file 1 of Identification of a new gene signature for prognostic evaluation in cervical cancer: based on cuproptosis-associated angiogenesis and multi-omics analysis
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Additional file 1 of Efficacy and safety of PD-1/PD-L1 inhibitors combined with anti-angiogenic therapy for the unresectable hepatocellular carcinoma and the benefit for hepatitis B virus etiology subgroup: a systematic review and meta-analysis of randomized controlled trials
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Additional file 2 of Combination of alpha-fetoprotein and neutrophil-to-lymphocyte ratio to predict treatment response and survival outcomes of patients with unresectable hepatocellular carcinoma treated with immune checkpoint inhibitors
Zhu, H.-F., Feng, J.-K., Xiang, Y.-J., Wang, K., Zhou, L.-P., Liu, Z., Cheng, Y.-Q., Shi, J., Guo, W.-X., & Cheng, S.-Q. (2023) · Figshare · doi:10.6084/m9.figshare.23529061
Additional file 5 of Combination of alpha-fetoprotein and neutrophil-to-lymphocyte ratio to predict treatment response and survival outcomes of patients with unresectable hepatocellular carcinoma treated with immune checkpoint inhibitors
Zhu, H.-F., Feng, J.-K., Xiang, Y.-J., Wang, K., Zhou, L.-P., Liu, Z.-H., Cheng, Y.-Q., Shi, J., Guo, W.-X., & Cheng, S.-Q. (2023) · Figshare · doi:10.6084/m9.figshare.23529070
Additional file 1 of Radiotherapy plus anti-PD1 versus radiotherapy for hepatic toxicity in patients with hepatocellular carcinoma
Zhang, R.-J., Zhou, H.-M., Lu, H.-Y., Yu, H., Tang, W.-Z., Qiu, M.-Q., Yan, L.-Y., Long, M.-Y., Su, T.-S., Xiang, B.-D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23884414
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Additional file 1 of Cost-effectiveness analysis of sorafenib, lenvatinib, atezolizumab plus bevacizumab and sintilimab plus bevacizumab for the treatment of advanced hepatocellular carcinoma in China
Gong, H., Ong, S. C., Li, F., Weng, Z., Zhao, K., & Jiang, Z. (2024) · Figshare · doi:10.6084/m9.figshare.26579570
Additional file 3 of Radiotherapy plus anti-PD1 versus radiotherapy for hepatic toxicity in patients with hepatocellular carcinoma
Zhang, R.-J., Zhou, H.-M., Lu, H.-Y., Yu, H., Tang, W., Qiu, M.-Q., Yan, L.-Y., Long, M.-Y., Su, T.-S., Xiang, B.-D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23884420
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Authors: Ren, Z., Xu, J., Bai, Y., Xu, A., Cang, S., Du, C., Li, Q., Lu, Y., Chen, Y., Guo, Y., Chen, Z., Liu, B., Jia, W., Wu, J., Wang, J., Shao, G., Zhang, B., Shan, Y., Meng, Z., Wu, J., Gu, S., Yang, W., Liu, C., Shi, X., Gao, Z., Yin, T., Cui, J., Huang, M., Xing, B., Mao, Y., Teng, G., Qin, Y., Wang, J., Xia, F., Yin, G., Yang, Y., Chen, M., Wang, Y., Zhou, H., & Fan, J.
Affiliations: Shanghai Medical College of Fudan University (CN)
Chinese PLA General Hospital (CN)
Third Affiliated Hospital of Harbin Medical University (CN)
Nantong University (CN)
Henan Provincial People's Hospital (CN)
The Affiliated Yongchuan Hospital of Chongqing Medical University (CN)
Sichuan University (CN)
Sun Yat-sen University (CN)
Nanfang Hospital (CN)
Second Affiliated Hospital of Anhui Medical University (CN)
Nanjing Drum Tower Hospital (CN)
Anhui Provincial Hospital (CN)
Second Affiliated Hospital of Nanchang University (CN)
Second Affiliated Hospital of Xi'an Jiaotong University (CN)
Zhejiang Cancer Hospital (CN)
Huazhong University of Science and Technology (CN)
First Affiliated Hospital of Wenzhou Medical University (CN)
Fudan University (CN)
Hunan Cancer Hospital (CN)
First Affiliated Hospital of Xi'an Jiaotong University (CN)
Shandong Tumor Hospital (CN)
First Affiliated Hospital of Bengbu Medical College (CN)
Hubei Cancer Hospital (CN)
First Hospital of Jilin University (CN)
Peking Union Medical College Hospital (CN)
First Affiliated Hospital of Zhengzhou University (CN)
Southwest Hospital (CN)
Jiangsu Cancer Hospital (CN)
Innovent Biologics (China) (CN)
Corresponding author: Fan, Jia
ORCID: Ren, Zhenggang
Xu, Jianming
Bai, Yuxian
Xu, Aibing
Cang, Shundong
Du, Chengyou
Li, Qiu
Lu, Yinying
Chen, Yajin
Guo, Yabing
Chen, Zhendong
Liu, Baorui
Jia, Weidong
Wu, Jian
Wang, Junye
Shao, Guoliang
Zhang, Bixiang
Shan, Yunfeng
Meng, Zhiqiang
Wu, Jianbing
Gu, Shanzhi
Yang, Wei
Liu, Chao
Gao, Zhenyuan
Yin, Tao
Cui, Jiuwei
Huang, Ming
Mao, Yilei
Qin, Yanru
Wang, Jinhai
Yin, Guowen
Yang, Yong
Chen, Mingxia
Zhou, Hui
Fan, Jia
Venue: The Lancet Oncology
Publisher: Elsevier BV
Published: 2021-07
Volume: 22
Issue: 7
Pages: 977-990
ISSN: 1470-2045 (ISSN-L)
DOI: 10.1016/s1470-2045(21)00252-7
OpenAlex: W3166753505
Cited by: 1,124
References: 30
Citations by year: 2026: 162 · 2025: 241 · 2024: 273 · 2023: 247 · 2022: 178 · 2021: 21
FWCI: 100.04
Type: journal article
Language: en
Update notices: erratum (2021-08-01)
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: The Lancet Oncology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
Keywords: sintilimab, bevacizumab biosimilar, sorafenib, hepatocellular carcinoma, PD-1 inhibitors, first-line therapy, unresectable liver cancer, hepatitis B virus, overall survival, progression-free survival, combination immunotherapy, anti-angiogenic therapy, China, safety and tolerability, macrovascular invasion
MeSH terms: Bevacizumab, Sorafenib, Progression-Free Survival, Adult, Aged, Aged, 80 and over, Antineoplastic Combined Chemotherapy Protocols, China, Female, Hepatitis B, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Male, Middle Aged, Time Factors, Disease Progression, Young Adult, Biosimilar Pharmaceuticals, Antibodies, Monoclonal, Humanized

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Sintilimab plus a bevacizumab biosimilar (IBI305) versus sorafenib in unresectable hepatocellular carcinoma (ORIENT-32): a randomised, open-label, phase 2–3 study

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