Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme

UKMenCar4 and ‘Be on the TEAM’ Study Collaborators; Jeremy P. Carr; Jenny M. MacLennan; Emma Plested; Holly B. Bratcher; Odile B. Harrison; Parvinder K. Aley; Jennifer Oliver; Begonia Morales-Aza; Hannah Christensen; Martin C Maiden; al et

doi:10.1016/j.cmi.2022.07.004

Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme

UKMenCar4 and ‘Be on the TEAM’ Study Collaborators, Jeremy P. Carr, Jenny M. MacLennan, Emma Plested, Holly B. Bratcher, Odile B. Harrison, Parvinder K. Aley, Jennifer Oliver, Begonia Morales-Aza, Hannah Christensen, Martin C Maiden^*, al et

^*Corresponding author for this work

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Abstract

Objectives
Serogroup W and Y invasive meningococcal disease (IMD) increased globally from 2000 onwards. Responding to a rapid increase in serogroup W clonal complex 11 (W:cc11) IMD, the UK replaced an adolescent booster dose of meningococcal C conjugate vaccine with quadrivalent MenACWY conjugate vaccine in 2015. By 2018, vaccine coverage in the eligible school cohorts aged 14-19 years-old was 84%. We assessed the impact of the MenACWY vaccination programme on meningococcal carriage.

Methods
An observational study of culture-defined oropharyngeal meningococcal carriage prevalence before and after the start of the MenACWY vaccination programme in UK school students, aged 15–19 years, using two cross-sectional studies: 2014–15 “UKMenCar4” and 2018 “Be on the TEAM” (ISRCTN75858406).

Results
A total of 10625 participants pre-implementation and 13434 post-implementation were included. Carriage of genogroups C, W, and Y (combined) decreased from 2·03% to 0·71% (OR 0·34 [95% CI 0·27–0·44] p<0·001). Carriage of genogroup B meningococci did not change (1·26% vs 1·23% [95% CI 0.77–1.22] p=0·80) and genogroup C remained rare (n = 7/10625 vs 17/13488, p=0·135). The proportion of serogroup positive isolates, i.e., those expressing capsule, decreased for genogroup W by 53.8% (95% CI -5.0%–79.8%, p=0·016) and for genogroup Y by 30·1% (95% CI 8·9%–46·3%, p=0·0025).

Conclusions
The UK MenACWY vaccination programme reduced carriage acquisition of genogroup and serogroup Y and W meningococci and sustained low levels of genogroup C carriage. These data support the use of quadrivalent MenACWY conjugate vaccine for indirect (herd) protection.

Original language	English
Pages (from-to)	1649.e1-1649.e8
Journal	Clinical Microbiology and Infection
Volume	28
Issue number	12
Early online date	12 Jul 2022
DOIs	https://doi.org/10.1016/j.cmi.2022.07.004
Publication status	Published - 1 Dec 2022

Bibliographical note

Funding Information:
The authors would like to thank the NIHR Oxford Biomedical Research Centre, Children's Research team, Nottingham University Hospitals NHS Trust; Women's & Children's Research team, University Hospitals Bristol and Weston NHS Foundation Trust; the ‘Be on the TEAM’ Scientific Advisory Board; Chair, Prof Sir Brian Greenwood; Deputy Chair James Stuart, Simon Nadel, Helen Marshall, Helen Bedford, Nick Andrews; James Adamson, Public Health Wales; Andrew Walker & Lloyd Walsh, UKHSA Meningococcal Reference Unit; Melanie Carr; Yama Farooq, Simon Kerridge, Annabel Giddings, and Hannah Robinson, Oxford Vaccine Group; Helen Watson, Heather Murdoch, Laura Walsh, and Laura Macdonald, Public Health Scotland; Karen Duffy, NHS Greater Glasgow and Clyde Clinical Research Unit; NHS Greater Glasgow and Clyde Public Health Department; Thomas Bower, Stephen Saich, Alasdair Munro, Robert Dorey, Louise Haskell, Jane Martin, Helen Gale, Anne Magee, and Anna Hardy, NIHR Southampton Clinical Research Facility; Margaret Varga, University of Oxford; Clarendon Scholarship Fund, University of Oxford (JPC). We thank the study team from all sites for recruitment, data, and sampling; the UKHSA Meningococcal Reference Unit (Manchester UK) and the Maiden Lab (University of Oxford UK) for microbiological and genomics expertise. We acknowledge the Meningitis Research Foundation and Meningitis Now for their input into the Be on the TEAM study. We thank the schools, staff, and participating students for their enthusiasm and support of this research.

Funding Information:
This study was funded by the Wellcome Trust (087622 and 218205/Z/19/Z) and the National Institute for Health Research (NIHR) Policy Research Programme (PR-ST-0915-10015 and PR-R18-0117-21001). The views expressed are those of the authors and not necessarily those of the NIHR or the Department of Health and Social Care. MenB-fHbp for the ‘Be on the TEAM’ study donated by Pfizer. The study funders had no role in the study design or in the collection, analysis or interpretation of data, manuscript preparation, or the decision to submit for publication.

Publisher Copyright:
© 2022 The Author(s)

Keywords

ACWY
Adolescents
Conjugate vaccines
Herd immunity
Meningococcal Disease
Neisseria meningitidis
Pharyngeal carriage

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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UKMenCar4 and ‘Be on the TEAM’ Study Collaborators, Carr, J. P., MacLennan, J. M., Plested, E., Bratcher, H. B., Harrison, O. B., Aley, P. K., Oliver, J., Morales-Aza, B., Christensen, H., Maiden, M. C., & et, A. (2022). Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme. Clinical Microbiology and Infection, 28(12), 1649.e1-1649.e8. https://doi.org/10.1016/j.cmi.2022.07.004

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title = "Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme",

abstract = "ObjectivesSerogroup W and Y invasive meningococcal disease (IMD) increased globally from 2000 onwards. Responding to a rapid increase in serogroup W clonal complex 11 (W:cc11) IMD, the UK replaced an adolescent booster dose of meningococcal C conjugate vaccine with quadrivalent MenACWY conjugate vaccine in 2015. By 2018, vaccine coverage in the eligible school cohorts aged 14-19 years-old was 84%. We assessed the impact of the MenACWY vaccination programme on meningococcal carriage.MethodsAn observational study of culture-defined oropharyngeal meningococcal carriage prevalence before and after the start of the MenACWY vaccination programme in UK school students, aged 15–19 years, using two cross-sectional studies: 2014–15 “UKMenCar4” and 2018 “Be on the TEAM” (ISRCTN75858406).ResultsA total of 10625 participants pre-implementation and 13434 post-implementation were included. Carriage of genogroups C, W, and Y (combined) decreased from 2·03% to 0·71% (OR 0·34 [95% CI 0·27–0·44] p<0·001). Carriage of genogroup B meningococci did not change (1·26% vs 1·23% [95% CI 0.77–1.22] p=0·80) and genogroup C remained rare (n = 7/10625 vs 17/13488, p=0·135). The proportion of serogroup positive isolates, i.e., those expressing capsule, decreased for genogroup W by 53.8% (95% CI -5.0%–79.8%, p=0·016) and for genogroup Y by 30·1% (95% CI 8·9%–46·3%, p=0·0025).ConclusionsThe UK MenACWY vaccination programme reduced carriage acquisition of genogroup and serogroup Y and W meningococci and sustained low levels of genogroup C carriage. These data support the use of quadrivalent MenACWY conjugate vaccine for indirect (herd) protection.",

keywords = "ACWY, Adolescents, Conjugate vaccines, Herd immunity, Meningococcal Disease, Neisseria meningitidis, Pharyngeal carriage",

author = "{UKMenCar4 and {\textquoteleft}Be on the TEAM{\textquoteright} Study Collaborators} and Carr, {Jeremy P.} and MacLennan, {Jenny M.} and Emma Plested and Bratcher, {Holly B.} and Harrison, {Odile B.} and Aley, {Parvinder K.} and Bray, {James E.} and Susana Camara and Rodrigues, {Charlene M.C.} and Kimberly Davis and Angela Bartolf and David Baxter and Cameron, {J. Claire} and Richard Cunningham and Faust, {Saul N} and Katy Fidler and Rohit Gowda and Heath, {Paul T.} and Stephen Hughes and Sujata Khajuria and David Orr and Mala Raman and Andrew Smith and Turner, {David P.J.} and Elizabeth Whittaker and Jennifer Oliver and Begonia Morales-Aza and Hannah Christensen and Adam Finn and Maiden, {Martin C} and al et",

note = "Funding Information: The authors would like to thank the NIHR Oxford Biomedical Research Centre, Children's Research team, Nottingham University Hospitals NHS Trust; Women's & Children's Research team, University Hospitals Bristol and Weston NHS Foundation Trust; the {\textquoteleft}Be on the TEAM{\textquoteright} Scientific Advisory Board; Chair, Prof Sir Brian Greenwood; Deputy Chair James Stuart, Simon Nadel, Helen Marshall, Helen Bedford, Nick Andrews; James Adamson, Public Health Wales; Andrew Walker & Lloyd Walsh, UKHSA Meningococcal Reference Unit; Melanie Carr; Yama Farooq, Simon Kerridge, Annabel Giddings, and Hannah Robinson, Oxford Vaccine Group; Helen Watson, Heather Murdoch, Laura Walsh, and Laura Macdonald, Public Health Scotland; Karen Duffy, NHS Greater Glasgow and Clyde Clinical Research Unit; NHS Greater Glasgow and Clyde Public Health Department; Thomas Bower, Stephen Saich, Alasdair Munro, Robert Dorey, Louise Haskell, Jane Martin, Helen Gale, Anne Magee, and Anna Hardy, NIHR Southampton Clinical Research Facility; Margaret Varga, University of Oxford; Clarendon Scholarship Fund, University of Oxford (JPC). We thank the study team from all sites for recruitment, data, and sampling; the UKHSA Meningococcal Reference Unit (Manchester UK) and the Maiden Lab (University of Oxford UK) for microbiological and genomics expertise. We acknowledge the Meningitis Research Foundation and Meningitis Now for their input into the Be on the TEAM study. We thank the schools, staff, and participating students for their enthusiasm and support of this research. Funding Information: This study was funded by the Wellcome Trust (087622 and 218205/Z/19/Z) and the National Institute for Health Research (NIHR) Policy Research Programme (PR-ST-0915-10015 and PR-R18-0117-21001). The views expressed are those of the authors and not necessarily those of the NIHR or the Department of Health and Social Care. MenB-fHbp for the {\textquoteleft}Be on the TEAM{\textquoteright} study donated by Pfizer. The study funders had no role in the study design or in the collection, analysis or interpretation of data, manuscript preparation, or the decision to submit for publication. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2022",

month = dec,

day = "1",

doi = "10.1016/j.cmi.2022.07.004",

language = "English",

volume = "28",

pages = "1649.e1--1649.e8",

journal = "Clinical Microbiology and Infection",

issn = "1198-743X",

publisher = "Elsevier Limited",

number = "12",

}

UKMenCar4 and ‘Be on the TEAM’ Study Collaborators, Carr, JP, MacLennan, JM, Plested, E, Bratcher, HB, Harrison, OB, Aley, PK, Oliver, J, Morales-Aza, B , Christensen, H, Maiden, MC & et, A 2022, 'Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme', Clinical Microbiology and Infection, vol. 28, no. 12, pp. 1649.e1-1649.e8. https://doi.org/10.1016/j.cmi.2022.07.004

Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme. / UKMenCar4 and ‘Be on the TEAM’ Study Collaborators; Carr, Jeremy P.; MacLennan, Jenny M. et al.
In: Clinical Microbiology and Infection, Vol. 28, No. 12, 01.12.2022, p. 1649.e1-1649.e8.

Research output: Contribution to journal › Article (Academic Journal) › peer-review

TY - JOUR

T1 - Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents

T2 - evidence for herd protection from the UK MenACWY programme

AU - UKMenCar4 and ‘Be on the TEAM’ Study Collaborators

AU - Carr, Jeremy P.

AU - MacLennan, Jenny M.

AU - Plested, Emma

AU - Bratcher, Holly B.

AU - Harrison, Odile B.

AU - Aley, Parvinder K.

AU - Bray, James E.

AU - Camara, Susana

AU - Rodrigues, Charlene M.C.

AU - Davis, Kimberly

AU - Bartolf, Angela

AU - Baxter, David

AU - Cameron, J. Claire

AU - Cunningham, Richard

AU - Faust, Saul N

AU - Fidler, Katy

AU - Gowda, Rohit

AU - Heath, Paul T.

AU - Hughes, Stephen

AU - Khajuria, Sujata

AU - Orr, David

AU - Raman, Mala

AU - Smith, Andrew

AU - Turner, David P.J.

AU - Whittaker, Elizabeth

AU - Oliver, Jennifer

AU - Morales-Aza, Begonia

AU - Christensen, Hannah

AU - Finn, Adam

AU - Maiden, Martin C

AU - et, al

N1 - Funding Information: The authors would like to thank the NIHR Oxford Biomedical Research Centre, Children's Research team, Nottingham University Hospitals NHS Trust; Women's & Children's Research team, University Hospitals Bristol and Weston NHS Foundation Trust; the ‘Be on the TEAM’ Scientific Advisory Board; Chair, Prof Sir Brian Greenwood; Deputy Chair James Stuart, Simon Nadel, Helen Marshall, Helen Bedford, Nick Andrews; James Adamson, Public Health Wales; Andrew Walker & Lloyd Walsh, UKHSA Meningococcal Reference Unit; Melanie Carr; Yama Farooq, Simon Kerridge, Annabel Giddings, and Hannah Robinson, Oxford Vaccine Group; Helen Watson, Heather Murdoch, Laura Walsh, and Laura Macdonald, Public Health Scotland; Karen Duffy, NHS Greater Glasgow and Clyde Clinical Research Unit; NHS Greater Glasgow and Clyde Public Health Department; Thomas Bower, Stephen Saich, Alasdair Munro, Robert Dorey, Louise Haskell, Jane Martin, Helen Gale, Anne Magee, and Anna Hardy, NIHR Southampton Clinical Research Facility; Margaret Varga, University of Oxford; Clarendon Scholarship Fund, University of Oxford (JPC). We thank the study team from all sites for recruitment, data, and sampling; the UKHSA Meningococcal Reference Unit (Manchester UK) and the Maiden Lab (University of Oxford UK) for microbiological and genomics expertise. We acknowledge the Meningitis Research Foundation and Meningitis Now for their input into the Be on the TEAM study. We thank the schools, staff, and participating students for their enthusiasm and support of this research. Funding Information: This study was funded by the Wellcome Trust (087622 and 218205/Z/19/Z) and the National Institute for Health Research (NIHR) Policy Research Programme (PR-ST-0915-10015 and PR-R18-0117-21001). The views expressed are those of the authors and not necessarily those of the NIHR or the Department of Health and Social Care. MenB-fHbp for the ‘Be on the TEAM’ study donated by Pfizer. The study funders had no role in the study design or in the collection, analysis or interpretation of data, manuscript preparation, or the decision to submit for publication. Publisher Copyright: © 2022 The Author(s)

PY - 2022/12/1

Y1 - 2022/12/1

N2 - ObjectivesSerogroup W and Y invasive meningococcal disease (IMD) increased globally from 2000 onwards. Responding to a rapid increase in serogroup W clonal complex 11 (W:cc11) IMD, the UK replaced an adolescent booster dose of meningococcal C conjugate vaccine with quadrivalent MenACWY conjugate vaccine in 2015. By 2018, vaccine coverage in the eligible school cohorts aged 14-19 years-old was 84%. We assessed the impact of the MenACWY vaccination programme on meningococcal carriage.MethodsAn observational study of culture-defined oropharyngeal meningococcal carriage prevalence before and after the start of the MenACWY vaccination programme in UK school students, aged 15–19 years, using two cross-sectional studies: 2014–15 “UKMenCar4” and 2018 “Be on the TEAM” (ISRCTN75858406).ResultsA total of 10625 participants pre-implementation and 13434 post-implementation were included. Carriage of genogroups C, W, and Y (combined) decreased from 2·03% to 0·71% (OR 0·34 [95% CI 0·27–0·44] p<0·001). Carriage of genogroup B meningococci did not change (1·26% vs 1·23% [95% CI 0.77–1.22] p=0·80) and genogroup C remained rare (n = 7/10625 vs 17/13488, p=0·135). The proportion of serogroup positive isolates, i.e., those expressing capsule, decreased for genogroup W by 53.8% (95% CI -5.0%–79.8%, p=0·016) and for genogroup Y by 30·1% (95% CI 8·9%–46·3%, p=0·0025).ConclusionsThe UK MenACWY vaccination programme reduced carriage acquisition of genogroup and serogroup Y and W meningococci and sustained low levels of genogroup C carriage. These data support the use of quadrivalent MenACWY conjugate vaccine for indirect (herd) protection.

AB - ObjectivesSerogroup W and Y invasive meningococcal disease (IMD) increased globally from 2000 onwards. Responding to a rapid increase in serogroup W clonal complex 11 (W:cc11) IMD, the UK replaced an adolescent booster dose of meningococcal C conjugate vaccine with quadrivalent MenACWY conjugate vaccine in 2015. By 2018, vaccine coverage in the eligible school cohorts aged 14-19 years-old was 84%. We assessed the impact of the MenACWY vaccination programme on meningococcal carriage.MethodsAn observational study of culture-defined oropharyngeal meningococcal carriage prevalence before and after the start of the MenACWY vaccination programme in UK school students, aged 15–19 years, using two cross-sectional studies: 2014–15 “UKMenCar4” and 2018 “Be on the TEAM” (ISRCTN75858406).ResultsA total of 10625 participants pre-implementation and 13434 post-implementation were included. Carriage of genogroups C, W, and Y (combined) decreased from 2·03% to 0·71% (OR 0·34 [95% CI 0·27–0·44] p<0·001). Carriage of genogroup B meningococci did not change (1·26% vs 1·23% [95% CI 0.77–1.22] p=0·80) and genogroup C remained rare (n = 7/10625 vs 17/13488, p=0·135). The proportion of serogroup positive isolates, i.e., those expressing capsule, decreased for genogroup W by 53.8% (95% CI -5.0%–79.8%, p=0·016) and for genogroup Y by 30·1% (95% CI 8·9%–46·3%, p=0·0025).ConclusionsThe UK MenACWY vaccination programme reduced carriage acquisition of genogroup and serogroup Y and W meningococci and sustained low levels of genogroup C carriage. These data support the use of quadrivalent MenACWY conjugate vaccine for indirect (herd) protection.

KW - ACWY

KW - Adolescents

KW - Conjugate vaccines

KW - Herd immunity

KW - Meningococcal Disease

KW - Neisseria meningitidis

KW - Pharyngeal carriage

U2 - 10.1016/j.cmi.2022.07.004

DO - 10.1016/j.cmi.2022.07.004

M3 - Article (Academic Journal)

C2 - 35840033

AN - SCOPUS:85140883332

SN - 1198-743X

VL - 28

SP - 1649.e1-1649.e8

JO - Clinical Microbiology and Infection

JF - Clinical Microbiology and Infection

IS - 12

ER -

UKMenCar4 and ‘Be on the TEAM’ Study Collaborators, Carr JP, MacLennan JM, Plested E, Bratcher HB, Harrison OB et al. Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme. Clinical Microbiology and Infection. 2022 Dec 1;28(12):1649.e1-1649.e8. Epub 2022 Jul 12. doi: 10.1016/j.cmi.2022.07.004

Impact of meningococcal ACWY conjugate vaccines on pharyngeal carriage in adolescents: evidence for herd protection from the UK MenACWY programme

Abstract

Bibliographical note

Keywords

UN SDGs

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