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Infection- or AZD1222 vaccine-mediated immunity reduces SARS-CoV-2 transmission but increases Omicron competitiveness in hamsters

Author

Listed:
  • Julia R. Port

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Claude Kwe Yinda

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Jade C. Riopelle

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Zachary A. Weishampel

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Taylor A. Saturday

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Victoria A. Avanzato

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Jonathan E. Schulz

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Myndi G. Holbrook

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Kent Barbian

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Rose Perry-Gottschalk

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Elaine Haddock

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Craig Martens

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Carl. I. Shaia

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Teresa Lambe

    (University of Oxford
    University of Oxford)

  • Sarah C. Gilbert

    (University of Oxford)

  • Neeltje Doremalen

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Vincent J. Munster

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

Abstract

Limited data is available on the effect of vaccination and previous virus exposure on the nature of SARS-CoV-2 transmission and immune-pressure on variants. To understand the impact of pre-existing immunity on SARS-CoV-2 airborne transmission efficiency, we perform a transmission chain experiment using naïve, intranasally or intramuscularly AZD1222 vaccinated, and previously infected hamsters. A clear gradient in transmission efficacy is observed: Transmission in hamsters vaccinated via the intramuscular route was reduced over three airborne chains (approx. 60%) compared to naïve animals, whereas transmission in previously infected hamsters and those vaccinated via the intranasal route was reduced by 80%. We also find that the Delta B.1.617.2 variant outcompeted Omicron B.1.1.529 after dual infection within and between hosts in naïve, vaccinated, and previously infected transmission chains, yet an increase in Omicron B.1.1.529 competitiveness is observed in groups with pre-existing immunity against Delta B.1.617.2. This correlates with an increase in the strength of the humoral response against Delta B.1.617.2, with the strongest response seen in previously infected animals. These data highlight the continuous need to improve vaccination strategies and address the additional evolutionary pressure pre-existing immunity may exert on SARS-CoV-2.

Suggested Citation

  • Julia R. Port & Claude Kwe Yinda & Jade C. Riopelle & Zachary A. Weishampel & Taylor A. Saturday & Victoria A. Avanzato & Jonathan E. Schulz & Myndi G. Holbrook & Kent Barbian & Rose Perry-Gottschalk , 2023. "Infection- or AZD1222 vaccine-mediated immunity reduces SARS-CoV-2 transmission but increases Omicron competitiveness in hamsters," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42346-8
    DOI: 10.1038/s41467-023-42346-8
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    1. Neeltje van Doremalen & Jonathan E. Schulz & Danielle R. Adney & Taylor A. Saturday & Robert J. Fischer & Claude Kwe Yinda & Nazia Thakur & Joseph Newman & Marta Ulaszewska & Sandra Belij-Rammerstorfe, 2022. "ChAdOx1 nCoV-19 (AZD1222) or nCoV-19-Beta (AZD2816) protect Syrian hamsters against Beta Delta and Omicron variants," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Julia R. Port & Claude Kwe Yinda & Irene Offei Owusu & Myndi Holbrook & Robert Fischer & Trenton Bushmaker & Victoria A. Avanzato & Jonathan E. Schulz & Craig Martens & Neeltje van Doremalen & Chad S., 2021. "SARS-CoV-2 disease severity and transmission efficiency is increased for airborne compared to fomite exposure in Syrian hamsters," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Bo Meng & Adam Abdullahi & Isabella A. T. M. Ferreira & Niluka Goonawardane & Akatsuki Saito & Izumi Kimura & Daichi Yamasoba & Pehuén Pereyra Gerber & Saman Fatihi & Surabhi Rathore & Samantha K. Zep, 2022. "Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity," Nature, Nature, vol. 603(7902), pages 706-714, March.
    4. Bin Zhou & Tran Thi Nhu Thao & Donata Hoffmann & Adriano Taddeo & Nadine Ebert & Fabien Labroussaa & Anne Pohlmann & Jacqueline King & Silvio Steiner & Jenna N. Kelly & Jasmine Portmann & Nico Joel Ha, 2021. "SARS-CoV-2 spike D614G change enhances replication and transmission," Nature, Nature, vol. 592(7852), pages 122-127, April.
    5. Frederik Plesner Lyngse & Laust Hvas Mortensen & Matthew J. Denwood & Lasse Engbo Christiansen & Camilla Holten Møller & Robert Leo Skov & Katja Spiess & Anders Fomsgaard & Ria Lassaunière & Morten Ra, 2022. "Household transmission of the SARS-CoV-2 Omicron variant in Denmark," Nature Communications, Nature, vol. 13(1), pages 1-7, December.
    6. Delphine Planas & David Veyer & Artem Baidaliuk & Isabelle Staropoli & Florence Guivel-Benhassine & Maaran Michael Rajah & Cyril Planchais & Françoise Porrot & Nicolas Robillard & Julien Puech & Matth, 2021. "Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization," Nature, Nature, vol. 596(7871), pages 276-280, August.
    7. Delphine Planas & Nell Saunders & Piet Maes & Florence Guivel-Benhassine & Cyril Planchais & Julian Buchrieser & William-Henry Bolland & Françoise Porrot & Isabelle Staropoli & Frederic Lemoine & Hélè, 2022. "Considerable escape of SARS-CoV-2 Omicron to antibody neutralization," Nature, Nature, vol. 602(7898), pages 671-675, February.
    8. Elisabetta Cameroni & John E. Bowen & Laura E. Rosen & Christian Saliba & Samantha K. Zepeda & Katja Culap & Dora Pinto & Laura A. VanBlargan & Anna Marco & Julia Iulio & Fabrizia Zatta & Hannah Kaise, 2022. "Broadly neutralizing antibodies overcome SARS-CoV-2 Omicron antigenic shift," Nature, Nature, vol. 602(7898), pages 664-670, February.
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