Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial
Open accessAbstract
Background No adjuvant treatment has been established for patients who remain at high risk for hepatocellular carcinoma recurrence after curative-intent resection or ablation. We aimed to assess the efficacy of adjuvant atezolizumab plus bevacizumab versus active surveillance in patients with high-risk hepatocellular carcinoma.Methods In the global, open-label, phase 3 IMbrave050 study, adult patients with high-risk surgically resected or ablated hepatocellular carcinoma were recruited from 134 hospitals and medical centres in 26 countries in four WHO regions (European region, region of the Americas, South-East Asia region, and Western Pacific region). Patients were randomly assigned in a 1:1 ratio via an interactive voice-web response system using permuted blocks, using a block size of 4, to receive intravenous 1200 mg atezolizumab plus 15 mg/kg bevacizumab every 3 weeks for 17 cycles (12 months) or to active surveillance. The primary endpoint was recurrence-free survival by independent review facility assessment in the intention-to-treat population. This trial is registered with ClinicalTrials.gov, NCT04102098.Findings The intention-to-treat population included 668 patients randomly assigned between Dec 31, 2019, and Nov 25, 2021, to either atezolizumab plus bevacizumab (n=334) or to active surveillance (n=334). At the prespecified interim analysis (Oct 21, 2022), median duration of follow-up was 17·4 months (IQR 13·9-22·1). Adjuvant atezolizumab plus bevacizumab was associated with significantly improved recurrence-free survival (median, not evaluable [NE]; [95% CI 22·1-NE]) compared with active surveillance (median, NE [21·4-NE]; hazard ratio, 0·72 [adjusted 95% CI 0·53-0·98]; p=0·012). Grade 3 or 4 adverse events occurred in 136 (41%) of 332 patients who received atezolizumab plus bevacizumab and 44 (13%) of 330 patients in the active surveillance group. Grade 5 adverse events occurred in six patients (2%, two of which were treatment related) in the atezolizumab plus bevacizumab group, and one patient (<1%) in the active surveillance group. Both atezolizumab and bevacizumab were discontinued because of adverse events in 29 patients (9%) who received atezolizumab plus bevacizumab.Interpretation Among patients at high risk of hepatocellular carcinoma recurrence following curative-intent resection or ablation, recurrence-free survival was improved in those who received atezolizumab plus bevacizumab versus active surveillance. To our knowledge, IMbrave050 is the first phase 3 study of adjuvant treatment for hepatocellular carcinoma to report positive results. However, longer follow-up for both recurrence-free and overall survival is needed to assess the benefit-risk profile more fully.Funding F Hoffmann-La Roche/Genentech.
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In IMbrave 050, the most common immune-related adverse events were hepatitis, rash, and hypothyroidism, mostly grade 1-2.
“The most common immune-related AEs (irAEs) were hepatitis (32% versus 15%), rash (20% versus 2%) and hypothyroidism (20% versus <1%), mostly of grade 1–2 (ref. 12).”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
The Results (page not available in our copy) identify hepatitis-related events and hypothyroidism as the most common immune-mediated adverse events and say most were grade 1–2. They do not identify rash among those events or give the cited immune-related percentages. Table 2 reports rash and hypothyroidism under adverse events regardless of causality, with different percentages, so it does not verify those figures. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn IMbrave 050, at a median follow-up of 17.4 months, median recurrence-free survival was not reached in either group, but the intervention was favoured over active surveillance (HR 0.72, 95% CI 0.56-0.93; P = 0.012).
“At a median follow-up duration of 17.4 months, median RFS had not been reached in either group, although statistical analyses favoured intervention over active surveillance (HR 0.72, 95% CI 0.56–0.93; P = 0.012).”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
The Results (Figure 2; page not supplied) report that median recurrence-free survival was not reached in either group and that atezolizumab plus bevacizumab was favoured at a median follow-up of 17.4 months (HR 0.72; p=0.012). The reported adjusted 95% CI is 0.53–0.98, not the claimed 0.56–0.93. (LLM, conf=0.94)
Experimental — accuracy not yet measuredCompared with surveillance, inhibitors of the PD-1 pathway with or without bevacizumab can lead to an improvement in relapse-free survival after liver resection.
“Clinical data have shown that, compared with surveillance, inhibitors of the PD-1 pathway with or without bevacizumab can lead to an improvement in relapse-free survival after liver resection.5,6”
From Pathological response following neoadjuvant immune checkpoint inhibitors in patients with hepatocellular carcinoma: a cross-trial, patient-level analysis (2024) · cites this paper as [6]
The Results report improved recurrence-free survival with atezolizumab (a PD-L1 inhibitor) plus bevacizumab versus active surveillance, and Table 1 shows that most participants underwent resection. The trial also included patients treated by ablation and did not test a PD-1-pathway inhibitor without bevacizumab; the Discussion says the relative benefits of single-agent and combination treatment remain to be established. Page numbers were not provided in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAdjuvant therapy has a relatively small benefit in relapse-free survival.
“Based on our results and the relatively small benefit of relapse-free survival conferred by adjuvant therapy,6”
From Pathological response following neoadjuvant immune checkpoint inhibitors in patients with hepatocellular carcinoma: a cross-trial, patient-level analysis (2024) · cites this paper as [6]
The Results report improved recurrence-free survival with adjuvant atezolizumab plus bevacizumab: a 13% difference in event-free rates at 12 months and a hazard ratio of 0.72. The paper does not describe that benefit as relatively small, and its finding concerns this regimen in patients with high-risk hepatocellular carcinoma, not adjuvant therapy generally. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe IMbrave 050 trial showed that adjuvant atezolizumab plus bevacizumab significantly improved recurrence-free survival compared with active surveillance in patients with hepatocellular carcinoma at high risk of recurrence after resection or local ablation.
“In 2023, however, the treatment landscape for patients with early stage HCC evolved following positive results from IMbrave 050, in which adjuvant therapy with the ICI atezolizumab plus the anti-angiogenic agent bevacizumab significantly improved recurrence-free survival (RFS) over active surveillance in patients with a high risk of disease recurrence12.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
In IMbrave 050, independent review facility-assessed time to recurrence was longer in the intervention group (HR 0.67, 95% CI 0.52-0.88; P = 0.003).
“Independent review facility-assessed time to recurrence was longer in the intervention group (HR 0.67, 95% CI 0.52–0.88; P = 0.003).”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
In IMbrave 050, grade 3-4 adverse events occurred in 41% of patients receiving atezolizumab plus bevacizumab versus 13% with active surveillance, and 8.7% discontinued both drugs because of adverse events.
“The incidence of grade 3–4 adverse events was 41% and 13% with intervention and active surveillance, respectively, and 8.7% of patients discontinued both atezolizumab and bevacizumab owing to adverse events.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
In IMbrave 050, 8.4% of patients receiving the intervention versus 1% with active surveillance had immune-related adverse events requiring systemic corticosteroids.
“Additionally, 8.4% versus 1% of patients had irAEs requiring systemic corticosteroids.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
IMbrave 050 is the only phase III trial supporting adjuvant therapy in HCC.
“To date, IMbrave 050 is the only phase III trial that supports such an approach in the setting of HCC12.”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
Positive results from IMbrave 050 have led to a revised management algorithm incorporating adjuvant therapies for early-stage HCC.
“Now the positive results of IMbrave 050 (ref. 12) have led to a revised management algorithm for patients with early stage HCC by incorporating adjuvant therapies in this disease setting7 (Fig. 4).”
From Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma (2024) · cites this paper as [12]
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Adjuvant and neoadjuvant immunotherapies in hepatocellular carcinoma
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- Authors
- Qin, S., Chen, M., Cheng, A.-L., Kaseb, A. O., Kudo, M., Lee, H. C., Yopp, A. C., Zhou, J., Wang, L., Wen, X., Heo, J., Tak, W. Y., Nakamura, S., Numata, K., Uguen, T., Hsiehchen, D., Cha, E., Hack, S. P., Lian, Q., Ma, N., Spahn, J. H., Wang, Y., Wu, C., Chow, P. K. H., Thompson, A., Danta, M., Poursoltan, P., Kiberu, A., Chittajallu, R., Sood, S., Stauber, R., Pinter, M., Peck-Radosavljevic, M., Decaestecker, J., Cuyle, P.-J., Verset, G., Van Vlierberghe, H., De Azevedo, S., Andrade, L., Cunha Júnior, A., Faria, L., Yen, C. T., Colli, L., Asselah, J., Kavan, P., Marquez, V., Brahmania, M., Li, Q., Xing, B., Guo, Y., Chen, Z., Zhao, H., Peng, T., Wang, L., Wang, L., Liu, H., Wu, F., Qin, L., Zheng, Q., Ying, J., Li, H., Wen, T., Qin, S., Wen, X., Liu, Y., Chen, M., Wang, B., Bai, Y., He, Y., Zhao, H., Zhou, D., Dai, C., Teng, G., Cui, S., Gao, Y., Zhang, X., Lu, Z., Yin, T., Ding, Y., Jia, W., Xia, Y., Sun, B., Xia, Q., Yuan, Y., Sun, H., Shi, X., Guzmán, A., Corrales, L., Kral, Z., Priester, P., Kubala, E., Blanc, J. F., Bourliere, M., Peron, J. M., Borg, C., Bronowicki, J.-P., Ganne, N., Decaens, T., Uguen, T., Heurgue, A., Trojan, J., Gonzalez-Carmona, M. A., Roderburg, C., Ettrich, T., Schotten, C., Kandulski, A., Yau, T., Chan, L., Scartozzi, M., Masi, G., Fanello, S., Battezzati, P. M., Leonardi, F., Ghidini, M., Numata, K., Morimoto, M., Hidaka, H., Tsuchiya, K., Yamashita, T., Kato, N., Kudo, M., Hagihara, A., Koga, H., Arakawa, T., Nakamura, I., Kawamura, Y., Kawaoka, T., Shimada, M., Hasegawa, K., Marusawa, H., Nakamura, S., Hiraoka, A., Hayashi, H., Takeda, S., Lee, H. C., Paik, S. W., Kim, D. Y., Lee, J. I., Jeong, S.-H., Kim, W., Tak, W. Y., Heo, J., Kim, H., Chon, H. J., Cheong, J., Yoon, S. K., Yoon, J.-H., Villalobos, R., Martinez Rodriguez, J. L., Oyervides Juarez, V., Hernández, C. A., Klumpen, H.-J., de Vos-Geelen, J., Gane, E., Montenegro, P., Torres Mattos, C., Janczewska, E., Kawecki, M., Nowakowska-Zajdel, E., Fedenko, A., Granov, D., Alyasova, A., Sekacheva, M., Ledin, E., Samol, J., Toh, H. C., Calvo Campos, M., Gomez Martin, C., Lopez Lopez, C., Muñoz Martin, A. J., Calleja Panero, J. L., Montero Alvarez, J. L., Reig Monzón, M., Delgado Mingorance, I., Minguez Rosique, B., Cheng, A. L., Huang, Y.-H., Lin, S.-M., Huang, J.-F., Yu, M.-L., Su, W.-W., Korphaisarn, K., Maneenil, K., Samdaengpan, C., Tharavichitkul, E., Ozguroglu, M., Kose, F., Harputluoglu, H., Buchschacher, G., Thuluvath, P., Xiong, H., Patel, M., Gold, P., Li, D., Brooks, G., Masood, A., Patel, R., George, B., Salgia, R., Manji, G., Crow, M., Kaseb, A., Dugan, M., Kadakia, K., Kardosh, A., Gibbs, J., Shah, A., Burris III, H., & Hsiehchen, D.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Fudan University (CN)
- Himeji Red Cross Hospital (JP)
- Genentech (US)
- Roche (China) (CN)
- SingHealth Duke-NUS Academic Medical Centre (SG)
- Jilin University (CN)
- Fudan University Shanghai Cancer Center (CN)
- Yokohama City University Medical Center (JP)
- Hôpital Pontchaillou (FR)
- Asan Medical Center (KR)
- Pusan National University Hospital (KR)
- Kyungpook National University Hospital (KR)
- Corresponding author
- Chow, Pierce K H
- ORCID
- Yopp, Adam C
- Zhou, Jian
- Cha, Edward
- Hack, Stephen P
- Lian, Qinshu
- Ma, Ning
- Wang, Yulei
- Chow, Pierce K H
- Thompson, Alexander
- Danta, Mark
- Poursoltan, Pirooz
- Chittajallu, Renuka
- Stauber, Rudolf
- Pinter, Matthias
- Decaestecker, Jochen
- Cuyle, Pieter-Jan
- Verset, Gontran
- Colli, Leandro
- Asselah, Jamil
- Kavan, Petr
- Marquez, Vladimir
- Brahmania, Mayur
- Chen, Zhendong
- Zhao, Haitao
- Peng, Tao
- Wang, Liming
- Liu, Hongming
- Wu, Feixiang
- Zheng, Qichang
- Ying, Jieer
- Li, Haitao
- Wen, Tianfu
- Liu, Yunpeng
- Wang, Boqing
- Bai, Yuxian
- He, Yifu
- Zhao, Hong
- Zhou, Dong
- Dai, Chaoliu
- Cui, Shuzhong
- Gao, Yi
- Yin, Tao
- Jia, Weidong
- Xia, Yongxiang
- Sun, Beicheng
- Yuan, Yufeng
- Corrales, Luis
- Borg, Christophe
- Bronowicki, Jean-Pierre
- Decaens, Thomas
- Gonzalez-Carmona, Maria Angeles
- Roderburg, Christoph
- Ettrich, Thomas
- Kandulski, Arne
- Yau, Thomas
- Scartozzi, Mario
- Masi, Gianluca
- Battezzati, Pier Maria
- Leonardi, Francesco
- Ghidini, Michele
- Morimoto, Manabu
- Hidaka, Hisashi
- Tsuchiya, Kaoru
- Yamashita, Tatsuya
- Kato, Naoya
- Hagihara, Atsushi
- Koga, Hironori
- Nakamura, Ikuo
- Kawamura, Yusuke
- Kawaoka, Tomokazu
- Shimada, Mitsuo
- Hasegawa, Kiyoshi
- Marusawa, Hiroyuki
- Hiraoka, Atsushi
- Hayashi, Hiromitsu
- Takeda, Shin
- Paik, Seung Woon
- Kim, Do Young
- Lee, Jung Il
- Jeong, Sook-Hyang
- Kim, Won
- Kim, Hyeyeong
- Chon, Hong Jae
- Yoon, Seung Kew
- Yoon, Jung-Hwan
- Gane, Edward
- Montenegro, Paola
- Janczewska, Ewa
- Kawecki, Maciej
- Alyasova, Anna
- Sekacheva, Marina
- Samol, Jens
- Toh, Han Chong
- Huang, Yi-Hsiang
- Lin, Shi-Ming
- Huang, Jee-Fu
- Yu, Ming-Lung
- Su, Wei-Wen
- Korphaisarn, Krittiya
- Maneenil, Kunlatida
- Samdaengpan, Chayanee
- Buchschacher, Gary
- Thuluvath, Paul
- Li, Daneng
- Masood, Ashiq
- Patel, Reema
- George, Ben
- Salgia, Reena
- Manji, Gulam
- Crow, Mary
- Kadakia, Kunal
- Kardosh, Adel
- Shah, Ashesh
- Venue
- The Lancet
- Publisher
- Elsevier BV
- Published
- 2023-11
- Volume
- 402
- Issue
- 10415
- Pages
- 1835-1847
- ISSN
- 0099-5355 (ISSN-L)
- 0140-6736
- OpenAlex
- W4387803249
- Cited by
- 545
- References
- 43
- Citations by year
- 2026: 164 · 2025: 198 · 2024: 175 · 2023: 7
- FWCI
- 90.99
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Licence
- Locations
- The Lancet (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Pure Amsterdam UMC (acceptedVersion, other-oa)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion, cc-by-nc-nd)
- Funders
- Genentech
- F. Hoffmann-La Roche Ltd
- Topics
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Renal cell carcinoma treatment
- Keywords
- hepatocellular carcinoma, adjuvant therapy, atezolizumab, bevacizumab, active surveillance, recurrence-free survival, hepatectomy, liver ablation, high-risk recurrence, immune checkpoint inhibitors, anti-angiogenic therapy, adverse events, immunotherapy safety, immunotherapy efficacy
- MeSH terms
- Bevacizumab, Adult, Antineoplastic Combined Chemotherapy Protocols, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Watchful Waiting, Antibodies, Monoclonal, Humanized
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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