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Articles| Volume 401, ISSUE 10373, P294-302, January 28, 2023

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Safety, tolerability, and immunogenicity of the chimpanzee adenovirus type 3-vectored Marburg virus (cAd3-Marburg) vaccine in healthy adults in the USA: a first-in-human, phase 1, open-label, dose-escalation trial

Published:January 28, 2023DOI:https://doi.org/10.1016/S0140-6736(22)02400-X

      Summary

      Background

      WHO has identified Marburg virus as an emerging virus requiring urgent vaccine research and development, particularly due to its recent emergence in Ghana. We report results from a first-in-human clinical trial evaluating a replication-deficient recombinant chimpanzee adenovirus type 3 (cAd3)-vectored vaccine encoding a wild-type Marburg virus Angola glycoprotein (cAd3-Marburg) in healthy adults.

      Methods

      We did a first-in-human, phase 1, open-label, dose-escalation trial of the cAd3-Marburg vaccine at the Walter Reed Army Institute of Research Clinical Trials Center in the USA. Healthy adults aged 18–50 years were assigned to receive a single intramuscular dose of cAd3-Marburg vaccine at either 1 × 1010 or 1 × 1011 particle units (pu). Primary safety endpoints included reactogenicity assessed for the first 7 days and all adverse events assessed for 28 days after vaccination. Secondary immunogenicity endpoints were assessment of binding antibody responses and T-cell responses against the Marburg virus glycoprotein insert, and assessment of neutralising antibody responses against the cAd3 vector 4 weeks after vaccination. This study is registered with ClinicalTrials.gov, NCT03475056.

      Findings

      Between Oct 9, 2018, and Jan 31, 2019, 40 healthy adults were enrolled and assigned to receive a single intramuscular dose of cAd3-Marburg vaccine at either 1 × 1010 pu (n=20) or 1 × 1011 pu (n=20). The cAd3-Marburg vaccine was safe, well tolerated, and immunogenic. All enrolled participants received cAd3-Marburg vaccine, with 37 (93%) participants completing follow-up visits; two (5%) participants moved from the area and one (3%) was lost to follow-up. No serious adverse events related to vaccination occurred. Mild to moderate reactogenicity was observed after vaccination, with symptoms of injection site pain and tenderness (27 [68%] of 40 participants), malaise (18 [45%] of 40 participants), headache (17 [43%] of 40 participants), and myalgia (14 [35%] of 40 participants) most commonly reported. Glycoprotein-specific antibodies were induced in 38 (95%) of 40 participants 4 weeks after vaccination, with geometric mean titres of 421 [95% CI 209–846] in the 1 × 1010 pu group and 545 [276–1078] in the 1 × 1011 pu group, and remained significantly elevated at 48 weeks compared with baseline titres (39 [95% CI 13–119] in the 1 ×1010 pu group and 27 [95–156] in the 1 ×1011 pu group; both p<0·0001). T-cell responses to the glycoprotein insert and neutralising responses against the cAd3 vector were also increased at 4 weeks after vaccination.

      Interpretation

      This first-in-human trial of this cAd3-Marburg vaccine showed the agent is safe and immunogenic, with a safety profile similar to previously tested cAd3-vectored filovirus vaccines. 95% of participants produced a glycoprotein-specific antibody response at 4 weeks after a single vaccination, which remained in 70% of participants at 48 weeks. These findings represent a crucial step in the development of a vaccine for emergency deployment against a re-emerging pathogen that has recently expanded its reach to new regions.

      Funding

      National Institutes of Health.
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      References

      1. 1.
        • Mehand MS
        • Al-Shorbaji F
        • Millett P
        • Murgue B
        The WHO R&D Blueprint: 2018 review of emerging infectious diseases requiring urgent research and development efforts.
        Antiviral Res. 2018; 159: 63-67
      2. 2.
        • Pigott DM
        • Golding N
        • Mylne A
        • et al.
        Mapping the zoonotic niche of Marburg virus disease in Africa.
        Trans R Soc Trop Med Hyg. 2015; 109: 366-378
      3. 3.
        • Pigott DM
        • Golding N
        • Mylne A
        • et al.
        Mapping the zoonotic niche of Ebola virus disease in Africa.
        eLife. 2014; 3e04395
      4. 4.
        • Bausch DG
        • Nichol ST
        • Muyembe-Tamfum JJ
        • et al.
        Marburg hemorrhagic fever associated with multiple genetic lineages of virus.
        N Engl J Med. 2006; 355: 909-919
      5. 5.
        • Towner JS
        • Khristova ML
        • Sealy TK
        • et al.
        Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola.
        J Virol. 2006; 80: 6497-6516
      6. 6.
        • World Health Organization
        Uganda ends Marburg virus disease outbreak.
        World Health Organization, Geneva2017
      7. 7.
        • Bonney JHK
        • Sanders T
        • Adams P
        • et al.
        First-ever outbreak of Marburg virus disease declared in Ghana, 2022.
      8. 8.
        • Burk R
        • Bollinger L
        • Johnson JC
        • et al.
        Neglected filoviruses.
        FEMS Microbiol Rev. 2016; 40: 494-519
      9. 9.
        • Reynolds P
        • Marzi A
        Ebola and Marburg virus vaccines.
        Virus Genes. 2017; 53: 501-515
      10. 10.
        • Manicassamy B
        • Wang J
        • Rumschlag E
        • et al.
        Characterization of Marburg virus glycoprotein in viral entry.
        Virology. 2007; 358: 79-88
      11. 11.
        • Swenson DL
        • Warfield KL
        • Negley DL
        • Schmaljohn A
        • Aman MJ
        • Bavari S
        Virus-like particles exhibit potential as a pan-filovirus vaccine for both Ebola and Marburg viral infections.
        Vaccine. 2005; 23: 3033-3042
      12. 12.
        • Hunegnaw R
        • Honko AN
        • Wang L
        • et al.
        A single-shot ChAd3-MARV vaccine confers rapid and durable protection against Marburg virus in nonhuman primates.
        Sci Transl Med. 2022; 14eabq6364
      13. 13.
        • Dulin N
        • Spanier A
        • Merino K
        • et al.
        Systematic review of Marburg virus vaccine nonhuman primate studies and human clinical trials.
        Vaccine. 2021; 39: 202-208
      14. 14.
        • Sullivan NJ
        • Sanchez A
        • Rollin PE
        • Yang ZY
        • Nabel GJ
        Development of a preventive vaccine for Ebola virus infection in primates.
        Nature. 2000; 408: 605-609
      15. 15.
        • Sullivan NJ
        • Geisbert TW
        • Geisbert JB
        • et al.
        Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates.
        Nature. 2003; 424: 681-684
      16. 16.
        • Callendret B
        • Vellinga J
        • Wunderlich K
        • et al.
        A prophylactic multivalent vaccine against different filovirus species is immunogenic and provides protection from lethal infections with Ebolavirus and Marburgvirus species in non-human primates.
        PLoS One. 2018; 13e0192312
      17. 17.
        • Swenson DL
        • Wang D
        • Luo M
        • et al.
        Vaccine to confer to nonhuman primates complete protection against multistrain Ebola and Marburg virus infections.
        Clin Vaccine Immunol. 2008; 15: 460-467
      18. 18.
        • Colloca S
        • Barnes E
        • Folgori A
        • et al.
        Vaccine vectors derived from a large collection of simian adenoviruses induce potent cellular immunity across multiple species.
        Sci Transl Med. 2012; 4115ra2
      19. 19.
        • Quinn KM
        • Da Costa A
        • Yamamoto A
        • et al.
        Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T cells following human-, simian-, and chimpanzee-derived recombinant adenoviral vector immunization.
        J Immunol. 2013; 190: 2720-2735
      20. 20.
        • Stanley DA
        • Honko AN
        • Asiedu C
        • et al.
        Chimpanzee adenovirus vaccine generates acute and durable protective immunity against ebolavirus challenge.
        Nat Med. 2014; 20: 1126-1129
      21. 21.
        • Peruzzi D
        • Dharmapuri S
        • Cirillo A
        • et al.
        A novel chimpanzee serotype-based adenoviral vector as delivery tool for cancer vaccines.
        Vaccine. 2009; 27: 1293-1300
      22. 22.
        • Tapia MD
        • Sow SO
        • Ndiaye BP
        • et al.
        Safety, reactogenicity, and immunogenicity of a chimpanzee adenovirus vectored Ebola vaccine in adults in Africa: a randomised, observer-blind, placebo-controlled, phase 2 trial.
        Lancet Infect Dis. 2020; 20: 707-718
      23. 23.
        • Ledgerwood JE
        • DeZure AD
        • Stanley DA
        • et al.
        Chimpanzee adenovirus vector Ebola vaccine.
        N Engl J Med. 2017; 376: 928-938
      24. 24.
        • De Santis O
        • Audran R
        • Pothin E
        • et al.
        Safety and immunogenicity of a chimpanzee adenovirus-vectored Ebola vaccine in healthy adults: a randomised, double-blind, placebo-controlled, dose-finding, phase 1/2a study.
        Lancet Infect Dis. 2016; 16: 311-320
      25. 25.
        • Ewer K
        • Rampling T
        • Venkatraman N
        • et al.
        A monovalent chimpanzee adenovirus Ebola vaccine boosted with MVA.
        N Engl J Med. 2016; 374: 1635-1646
      26. 26.
        • Venkatraman N
        • Ndiaye BP
        • Bowyer G
        • et al.
        Safety and Immunogenicity of a heterologous prime-boost Ebola virus vaccine regimen in healthy adults in the United Kingdom and Senegal.
        J Infect Dis. 2019; 219: 1187-1197
      27. 27.
        • Tapia MD
        • Sow SO
        • Mbaye KD
        • et al.
        Safety, reactogenicity, and immunogenicity of a chimpanzee adenovirus vectored Ebola vaccine in children in Africa: a randomised, observer-blind, placebo-controlled, phase 2 trial.
        Lancet Infect Dis. 2020; 20: 719-730
      28. 28.
        • Kennedy SB
        • Bolay F
        • Kieh M
        • et al.
        Phase 2 placebo-controlled trial of two vaccines to prevent Ebola in Liberia.
        N Engl J Med. 2017; 377: 1438-1447
      29. 29.
        • Sarwar UN
        • Costner P
        • Enama ME
        • et al.
        Safety and immunogenicity of DNA vaccines encoding Ebolavirus and Marburgvirus wild-type glycoproteins in a phase I clinical trial.
        J Infect Dis. 2015; 211: 549-557
      30. 30.
        • Swanson 2nd, PA
        • Padilla M
        • Hoyland W
        • et al.
        AZD1222/ChAdOx1 nCoV-19 vaccination induces a polyfunctional spike protein-specific TH1 response with a diverse TCR repertoire.
        Sci Transl Med. 2021; 13eabj7211
      31. 31.
        • Monaco G
        • Chen H
        • Poidinger M
        • Chen J
        • de Magalhães JP
        • Larbi A
        flowAI: automatic and interactive anomaly discerning tools for flow cytometry data.
        Bioinformatics. 2016; 32: 2473-2480
      32. 32.
        • Kibuuka H
        • Berkowitz NM
        • Millard M
        • et al.
        Safety and immunogenicity of Ebola virus and Marburg virus glycoprotein DNA vaccines assessed separately and concomitantly in healthy Ugandan adults: a phase 1b, randomised, double-blind, placebo-controlled clinical trial.
        Lancet. 2015; 385: 1545-1554
      33. 33.
        • Ledgerwood JE
        • Costner P
        • Desai N
        • et al.
        A replication defective recombinant Ad5 vaccine expressing Ebola virus GP is safe and immunogenic in healthy adults.
        Vaccine. 2010; 29: 304-313
      34. 34.
        • Zhu FC
        • Hou LH
        • Li JX
        • et al.
        Safety and immunogenicity of a novel recombinant adenovirus type-5 vector-based Ebola vaccine in healthy adults in China: preliminary report of a randomised, double-blind, placebo-controlled, phase 1 trial.
        Lancet. 2015; 385: 2272-2279
      35. 35.
        • Folegatti PM
        • Bittaye M
        • Flaxman A
        • et al.
        Safety and immunogenicity of a candidate Middle East respiratory syndrome coronavirus viral-vectored vaccine: a dose-escalation, open-label, non-randomised, uncontrolled, phase 1 trial.
        Lancet Infect Dis. 2020; 20: 816-826
      36. 36.
        • Barnes E
        • Folgori A
        • Capone S
        • et al.
        Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man.
        Sci Transl Med. 2012; 4115ra1
      37. 37.
        • Sabin Vaccine Institute
        Sabin Vaccine Institute receives additional $34·5 million from BARDA for further development of Ebola Sudan and Marburg vaccines.

      Linked Articles

      • Developing a vaccine against Marburg virus disease
        • Marburg virus disease is a severe infection in people and non-human primates (NHPs), with a case-fatality rate of 23–90%.1 The disease is caused by the Marburg virus, a member of the Filoviridae family, which includes the viruses responsible for Ebola virus disease.1 Marburg virus disease is extremely rare. Since its discovery in 1967, when two outbreaks occurred simultaneously in laboratories in Marburg and Frankfurt in Germany, and in Belgrade, Yugoslavia (now Serbia), causing 31 cases and seven deaths, there have been 16 known outbreaks with a cumulative total of fewer than 500 reported cases.
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