IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39575-2.html
   My bibliography  Save this article

Immunological imprinting of humoral immunity to SARS-CoV-2 in children

Author

Listed:
  • Alexander C. Dowell

    (University of Birmingham)

  • Tara Lancaster

    (University of Birmingham)

  • Rachel Bruton

    (University of Birmingham)

  • Georgina Ireland

    (UK Health Security Agency)

  • Christopher Bentley

    (University of Birmingham)

  • Panagiota Sylla

    (University of Birmingham)

  • Jianmin Zuo

    (University of Birmingham)

  • Sam Scott

    (MRC-University of Glasgow Centre for Virus Research)

  • Azar Jadir

    (University of Birmingham)

  • Jusnara Begum

    (University of Birmingham)

  • Thomas Roberts

    (University of Birmingham)

  • Christine Stephens

    (University of Birmingham)

  • Shabana Ditta

    (Bradford Institute for Health Research, Bradford Teaching Hospitals NHS Foundation Trust)

  • Rebecca Shepherdson

    (Bradford Institute for Health Research, Bradford Teaching Hospitals NHS Foundation Trust)

  • Annabel A. Powell

    (UK Health Security Agency)

  • Andrew J. Brent

    (Oxford University Hospitals NHS Foundation Trust
    University of Oxford, Wellington Square)

  • Bernadette Brent

    (Oxford University Hospitals NHS Foundation Trust)

  • Frances Baawuah

    (UK Health Security Agency)

  • Ifeanyichukwu Okike

    (UK Health Security Agency
    University Hospitals of Derby and Burton NHS Foundation Trust)

  • Joanne Beckmann

    (East London NHS Foundation Trust)

  • Shazaad Ahmad

    (Manchester University NHS Foundation Trust)

  • Felicity Aiano

    (UK Health Security Agency)

  • Joanna Garstang

    (Birmingham Community Healthcare NHS Trust)

  • Mary E. Ramsay

    (UK Health Security Agency)

  • Rafaq Azad

    (Bradford Institute for Health Research, Bradford Teaching Hospitals NHS Foundation Trust)

  • Dagmar Waiblinger

    (Bradford Institute for Health Research, Bradford Teaching Hospitals NHS Foundation Trust)

  • Brian Willett

    (MRC-University of Glasgow Centre for Virus Research)

  • John Wright

    (Bradford Institute for Health Research, Bradford Teaching Hospitals NHS Foundation Trust)

  • Shamez N. Ladhani

    (UK Health Security Agency)

  • Paul Moss

    (University of Birmingham)

Abstract

Omicron variants of SARS-CoV-2 are globally dominant and infection rates are very high in children. We measure immune responses following Omicron BA.1/2 infection in children aged 6-14 years and relate this to prior and subsequent SARS-CoV-2 infection or vaccination. Primary Omicron infection elicits a weak antibody response with poor functional neutralizing antibodies. Subsequent Omicron reinfection or COVID-19 vaccination elicits increased antibody titres with broad neutralisation of Omicron subvariants. Prior pre-Omicron SARS-CoV-2 virus infection or vaccination primes for robust antibody responses following Omicron infection but these remain primarily focussed against ancestral variants. Primary Omicron infection thus elicits a weak antibody response in children which is boosted after reinfection or vaccination. Cellular responses are robust and broadly equivalent in all groups, providing protection against severe disease irrespective of SARS-CoV-2 variant. Immunological imprinting is likely to act as an important determinant of long-term humoral immunity, the future clinical importance of which is unknown.

Suggested Citation

  • Alexander C. Dowell & Tara Lancaster & Rachel Bruton & Georgina Ireland & Christopher Bentley & Panagiota Sylla & Jianmin Zuo & Sam Scott & Azar Jadir & Jusnara Begum & Thomas Roberts & Christine Step, 2023. "Immunological imprinting of humoral immunity to SARS-CoV-2 in children," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39575-2
    DOI: 10.1038/s41467-023-39575-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39575-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39575-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Teresa Aydillo & Alexander Rombauts & Daniel Stadlbauer & Sadaf Aslam & Gabriela Abelenda-Alonso & Alba Escalera & Fatima Amanat & Kaijun Jiang & Florian Krammer & Jordi Carratala & Adolfo García-Sast, 2021. "Immunological imprinting of the antibody response in COVID-19 patients," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Juanjie Tang & Tanya Novak & Julian Hecker & Gabrielle Grubbs & Fatema Tuz Zahra & Lorenza Bellusci & Sara Pourhashemi & Janet Chou & Kristin Moffitt & Natasha B. Halasa & Stephanie P. Schwartz & Trac, 2022. "Cross-reactive immunity against the SARS-CoV-2 Omicron variant is low in pediatric patients with prior COVID-19 or MIS-C," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Ariën Schiepers & Marije F. L. Wout & Allison J. Greaney & Trinity Zang & Hiromi Muramatsu & Paulo J. C. Lin & Ying K. Tam & Luka Mesin & Tyler N. Starr & Paul D. Bieniasz & Norbert Pardi & Jesse D. B, 2023. "Molecular fate-mapping of serum antibody responses to repeat immunization," Nature, Nature, vol. 615(7952), pages 482-489, March.
    4. Angkana T. Huang & Bernardo Garcia-Carreras & Matt D. T. Hitchings & Bingyi Yang & Leah C. Katzelnick & Susan M. Rattigan & Brooke A. Borgert & Carlos A. Moreno & Benjamin D. Solomon & Luke Trimmer-Sm, 2020. "A systematic review of antibody mediated immunity to coronaviruses: kinetics, correlates of protection, and association with severity," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. Zheng Quan Toh & Nadia Mazarakis & Jill Nguyen & Rachel A. Higgins & Jeremy Anderson & Lien Anh Ha Do & David P. Burgner & Nigel Curtis & Andrew C. Steer & Kim Mulholland & Nigel W. Crawford & Shidan , 2022. "Comparison of antibody responses to SARS-CoV-2 variants in Australian children," Nature Communications, Nature, vol. 13(1), pages 1-5, December.
    6. Masahiro Yoshida & Kaylee B. Worlock & Ni Huang & Rik G. H. Lindeboom & Colin R. Butler & Natsuhiko Kumasaka & Cecilia Dominguez Conde & Lira Mamanova & Liam Bolt & Laura Richardson & Krzysztof Polans, 2022. "Local and systemic responses to SARS-CoV-2 infection in children and adults," Nature, Nature, vol. 602(7896), pages 321-327, February.
    7. Juanjie Tang & Tanya Novak & Julian Hecker & Gabrielle Grubbs & Fatema Tuz Zahra & Lorenza Bellusci & Sara Pourhashemi & Janet Chou & Kristin Moffitt & Natasha B. Halasa & Stephanie P. Schwartz & Trac, 2022. "Author Correction: Cross-reactive immunity against the SARS-CoV-2 Omicron variant is low in pediatric patients with prior COVID-19 or MIS-C," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
    8. Peter J. Halfmann & Shun Iida & Kiyoko Iwatsuki-Horimoto & Tadashi Maemura & Maki Kiso & Suzanne M. Scheaffer & Tamarand L. Darling & Astha Joshi & Samantha Loeber & Gagandeep Singh & Stephanie L. Fos, 2022. "SARS-CoV-2 Omicron virus causes attenuated disease in mice and hamsters," Nature, Nature, vol. 603(7902), pages 687-692, March.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Alessia Raineri & Thomas Radtke & Sonja Rueegg & Sarah R. Haile & Dominik Menges & Tala Ballouz & Agne Ulyte & Jan Fehr & Daniel L. Cornejo & Giuseppe Pantaleo & Céline Pellaton & Craig Fenwick & Milo, 2023. "Persistent humoral immune response in youth throughout the COVID-19 pandemic: prospective school-based cohort study," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Jernej Pušnik & Jasmin Zorn & Werner O. Monzon-Posadas & Kathrin Peters & Emmanuil Osypchuk & Sabine Blaschke & Hendrik Streeck, 2024. "Vaccination impairs de novo immune response to omicron breakthrough infection, a precondition for the original antigenic sin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Irene A. Abela & Chloé Pasin & Magdalena Schwarzmüller & Selina Epp & Michèle E. Sickmann & Merle M. Schanz & Peter Rusert & Jacqueline Weber & Stefan Schmutz & Annette Audigé & Liridona Maliqi & Anni, 2021. "Multifactorial seroprofiling dissects the contribution of pre-existing human coronaviruses responses to SARS-CoV-2 immunity," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    2. Kaori Sano & Disha Bhavsar & Gagandeep Singh & Daniel Floda & Komal Srivastava & Charles Gleason & Juan Manuel Carreño & Viviana Simon & Florian Krammer, 2022. "SARS-CoV-2 vaccination induces mucosal antibody responses in previously infected individuals," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    3. Taha Y. Taha & Irene P. Chen & Jennifer M. Hayashi & Takako Tabata & Keith Walcott & Gabriella R. Kimmerly & Abdullah M. Syed & Alison Ciling & Rahul K. Suryawanshi & Hannah S. Martin & Bryan H. Bach , 2023. "Rapid assembly of SARS-CoV-2 genomes reveals attenuation of the Omicron BA.1 variant through NSP6," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Guoli Shi & Tiansheng Li & Kin Kui Lai & Reed F. Johnson & Jonathan W. Yewdell & Alex A. Compton, 2024. "Omicron Spike confers enhanced infectivity and interferon resistance to SARS-CoV-2 in human nasal tissue," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Kevin J. Kramer & Erin M. Wilfong & Kelsey Voss & Sierra M. Barone & Andrea R. Shiakolas & Nagarajan Raju & Caroline E. Roe & Naveenchandra Suryadevara & Lauren M. Walker & Steven C. Wall & Ariana Pau, 2022. "Single-cell profiling of the antigen-specific response to BNT162b2 SARS-CoV-2 RNA vaccine," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Stephen M. Kissler & James A. Hay & Joseph R. Fauver & Christina Mack & Caroline G. Tai & Deverick J. Anderson & David D. Ho & Nathan D. Grubaugh & Yonatan H. Grad, 2023. "Viral kinetics of sequential SARS-CoV-2 infections," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    7. 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.
    8. Leire Campos-Mata & Benjamin Trinité & Andrea Modrego & Sonia Tejedor Vaquero & Edwards Pradenas & Anna Pons-Grífols & Natalia Rodrigo Melero & Diego Carlero & Silvia Marfil & César Santiago & Dàlia R, 2024. "A monoclonal antibody targeting a large surface of the receptor binding motif shows pan-neutralizing SARS-CoV-2 activity," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Meriem Bekliz & Kenneth Adea & Pauline Vetter & Christiane S. Eberhardt & Krisztina Hosszu-Fellous & Diem-Lan Vu & Olha Puhach & Manel Essaidi-Laziosi & Sophie Waldvogel-Abramowski & Caroline Stephan , 2022. "Neutralization capacity of antibodies elicited through homologous or heterologous infection or vaccination against SARS-CoV-2 VOCs," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    10. Sapna Sharma & Thomas Vercruysse & Lorena Sanchez-Felipe & Winnie Kerstens & Madina Rasulova & Lindsey Bervoets & Carolien Keyzer & Rana Abdelnabi & Caroline S. Foo & Viktor Lemmens & Dominique Loover, 2022. "Updated vaccine protects against SARS-CoV-2 variants including Omicron (B.1.1.529) and prevents transmission in hamsters," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Zhennan Zhao & Yufeng Xie & Bin Bai & Chunliang Luo & Jingya Zhou & Weiwei Li & Yumin Meng & Linjie Li & Dedong Li & Xiaomei Li & Xiaoxiong Li & Xiaoyun Wang & Junqing Sun & Zepeng Xu & Yeping Sun & W, 2023. "Structural basis for receptor binding and broader interspecies receptor recognition of currently circulating Omicron sub-variants," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Tomokazu Tamura & Jumpei Ito & Keiya Uriu & Jiri Zahradnik & Izumi Kida & Yuki Anraku & Hesham Nasser & Maya Shofa & Yoshitaka Oda & Spyros Lytras & Naganori Nao & Yukari Itakura & Sayaka Deguchi & Ri, 2023. "Virological characteristics of the SARS-CoV-2 XBB variant derived from recombination of two Omicron subvariants," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    13. James Brett Case & Samantha Mackin & John M. Errico & Zhenlu Chong & Emily A. Madden & Bradley Whitener & Barbara Guarino & Michael A. Schmid & Kim Rosenthal & Kuishu Ren & Ha V. Dang & Gyorgy Snell &, 2022. "Resilience of S309 and AZD7442 monoclonal antibody treatments against infection by SARS-CoV-2 Omicron lineage strains," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Lays Cordeiro Guimaraes & Pedro Augusto Carvalho Costa & Sérgio Ricardo Aluotto Scalzo Júnior & Heloísa Athaydes Seabra Ferreira & Ana Carolina Soares Braga & Leonardo Camilo Oliveira & Maria Marta Fi, 2024. "Nanoparticle-based DNA vaccine protects against SARS-CoV-2 variants in female preclinical models," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    15. Zhuoying Huang & Shuangfei Xu & Jiechen Liu & Linlin Wu & Jing Qiu & Nan Wang & Jia Ren & Zhi Li & Xiang Guo & Fangfang Tao & Jian Chen & Donglei Lu & Yuheng Wang & Juan Li & Xiaodong Sun & Weibing Wa, 2023. "Effectiveness of inactivated COVID-19 vaccines among older adults in Shanghai: retrospective cohort study," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Jakob Ankerhold & Sebastian Giese & Philipp Kolb & Andrea Maul-Pavicic & Reinhard E. Voll & Nathalie Göppert & Kevin Ciminski & Clemens Kreutz & Achim Lother & Ulrich Salzer & Wolfgang Bildl & Tim Wel, 2022. "Circulating multimeric immune complexes contribute to immunopathology in COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Lorenza Bellusci & Gabrielle Grubbs & Shaimaa Sait & Lael M. Yonker & Adrienne G. Randolph & Tanya Novak & Takuma Kobayashi & Surender Khurana, 2023. "Neutralization of SARS-CoV-2 Omicron BQ.1, BQ.1.1 and XBB.1 variants following SARS-CoV-2 infection or vaccination in children," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    18. Scott R. Tyler & Daniel Lozano-Ojalvo & Ernesto Guccione & Eric E. Schadt, 2024. "Anti-correlated feature selection prevents false discovery of subpopulations in scRNAseq," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Alessia Raineri & Thomas Radtke & Sonja Rueegg & Sarah R. Haile & Dominik Menges & Tala Ballouz & Agne Ulyte & Jan Fehr & Daniel L. Cornejo & Giuseppe Pantaleo & Céline Pellaton & Craig Fenwick & Milo, 2023. "Persistent humoral immune response in youth throughout the COVID-19 pandemic: prospective school-based cohort study," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Chun-Kit Yuen & Wan-Man Wong & Long-Fung Mak & Joy-Yan Lam & Lok-Yi Cheung & Derek Tsz-Yin Cheung & Yau-Yee Ng & Andrew Chak-Yiu Lee & Nanshan Zhong & Kwok-Yung Yuen & Kin-Hang Kok, 2023. "An interferon-integrated mucosal vaccine provides pan-sarbecovirus protection in small animal models," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39575-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.