Meningococcal carriage in periods of high and low invasive meningococcal disease incidence in the UK: comparison of UKMenCar1-4 cross-sectional survey results.


Journal

The Lancet. Infectious diseases
ISSN: 1474-4457
Titre abrégé: Lancet Infect Dis
Pays: United States
ID NLM: 101130150

Informations de publication

Date de publication:
05 2021
Historique:
received: 25 09 2019
revised: 16 06 2020
accepted: 13 10 2020
pubmed: 23 1 2021
medline: 18 5 2021
entrez: 22 1 2021
Statut: ppublish

Résumé

The incidence of invasive meningococcal disease in the UK decreased by approximately four times from 1999 to 2014, with reductions in serogroup C and serogroup B disease. Lower serogroup C invasive meningococcal disease incidence was attributable to implementation of the meningococcal serogroup C conjugate vaccine in 1999, through direct and indirect protection, but no vaccine was implemented against serogroup B disease. UK Meningococcal Carriage surveys 1-3 (UKMenCar1-3), conducted in 1999, 2000, and 2001, were essential for understanding the impact of vaccination. To investigate the decline in invasive meningococcal disease incidence, we did a large oropharyngeal carriage survey in 2014-15, immediately before the changes to meningococcal vaccines in the UK national immunisation schedule. UKMenCar4 was a cross-sectional survey in adolescents aged 15-19 years who were enrolled from schools and colleges geographically local to one of 11 UK sampling centres between Sept 1, 2014, and March 30, 2015. Participants provided an oropharyngeal swab sample and completed a questionnaire on risk factors for carriage, including social behaviours. Samples were cultured for putative Neisseria spp, which were characterised with serogrouping and whole-genome sequencing. Data from this study were compared with the results from the UKMenCar1-3 surveys (1999-2001). From the 19 641 participants (11 332 female, 8242 male, 67 not stated) in UKMenCar4 with culturable swabs and completed risk-factor questionnaires, 1420 meningococci were isolated, with a carriage prevalence of 7·23% (95% CI 6·88-7·60). Carriage prevalence was substantially lower in UKMenCar4 than in the previous surveys: carriage prevalence was 16·6% (95% CI 15·89-17·22; 2306/13 901) in UKMenCar1 (1999), 17·6% (17·05-18·22; 2873/16 295) in UKMenCar2 (2000), and 18·7% (18·12-19·27; 3283/17 569) in UKMenCar3 (2001). Carriage prevalence was lower for all serogroups in UKMenCar4 than in UKMenCar1-3, except for serogroup Y, which was unchanged. The prevalence of carriage-promoting social behaviours decreased from 1999 to 2014-15, with individuals reporting regular cigarette smoking decreasing from 2932 (21·5%) of 13 650 to 2202 (11·2%) of 19 641, kissing in the past week from 6127 (44·8%) of 13 679 to 7320 (37·3%) of 19 641, and attendance at pubs and nightclubs in the past week from 8436 (62·1%) of 13 594 to 7662 (39·0%) of 19 641 (all p<0·0001). We show that meningococcal carriage prevalence in adolescents sampled nationally during a low incidence period (2014-15) was less than half of that in an equivalent population during a high incidence period (1999-2001). Disease and carriage caused by serogroup C was well controlled by ongoing vaccination. The prevalence of behaviours associated with carriage declined, suggesting that public health policies aimed at influencing behaviour might have further reduced disease. Wellcome Trust, UK Department of Health, and National Institute for Health Research.

Sections du résumé

BACKGROUND
The incidence of invasive meningococcal disease in the UK decreased by approximately four times from 1999 to 2014, with reductions in serogroup C and serogroup B disease. Lower serogroup C invasive meningococcal disease incidence was attributable to implementation of the meningococcal serogroup C conjugate vaccine in 1999, through direct and indirect protection, but no vaccine was implemented against serogroup B disease. UK Meningococcal Carriage surveys 1-3 (UKMenCar1-3), conducted in 1999, 2000, and 2001, were essential for understanding the impact of vaccination. To investigate the decline in invasive meningococcal disease incidence, we did a large oropharyngeal carriage survey in 2014-15, immediately before the changes to meningococcal vaccines in the UK national immunisation schedule.
METHODS
UKMenCar4 was a cross-sectional survey in adolescents aged 15-19 years who were enrolled from schools and colleges geographically local to one of 11 UK sampling centres between Sept 1, 2014, and March 30, 2015. Participants provided an oropharyngeal swab sample and completed a questionnaire on risk factors for carriage, including social behaviours. Samples were cultured for putative Neisseria spp, which were characterised with serogrouping and whole-genome sequencing. Data from this study were compared with the results from the UKMenCar1-3 surveys (1999-2001).
FINDINGS
From the 19 641 participants (11 332 female, 8242 male, 67 not stated) in UKMenCar4 with culturable swabs and completed risk-factor questionnaires, 1420 meningococci were isolated, with a carriage prevalence of 7·23% (95% CI 6·88-7·60). Carriage prevalence was substantially lower in UKMenCar4 than in the previous surveys: carriage prevalence was 16·6% (95% CI 15·89-17·22; 2306/13 901) in UKMenCar1 (1999), 17·6% (17·05-18·22; 2873/16 295) in UKMenCar2 (2000), and 18·7% (18·12-19·27; 3283/17 569) in UKMenCar3 (2001). Carriage prevalence was lower for all serogroups in UKMenCar4 than in UKMenCar1-3, except for serogroup Y, which was unchanged. The prevalence of carriage-promoting social behaviours decreased from 1999 to 2014-15, with individuals reporting regular cigarette smoking decreasing from 2932 (21·5%) of 13 650 to 2202 (11·2%) of 19 641, kissing in the past week from 6127 (44·8%) of 13 679 to 7320 (37·3%) of 19 641, and attendance at pubs and nightclubs in the past week from 8436 (62·1%) of 13 594 to 7662 (39·0%) of 19 641 (all p<0·0001).
INTERPRETATION
We show that meningococcal carriage prevalence in adolescents sampled nationally during a low incidence period (2014-15) was less than half of that in an equivalent population during a high incidence period (1999-2001). Disease and carriage caused by serogroup C was well controlled by ongoing vaccination. The prevalence of behaviours associated with carriage declined, suggesting that public health policies aimed at influencing behaviour might have further reduced disease.
FUNDING
Wellcome Trust, UK Department of Health, and National Institute for Health Research.

Identifiants

pubmed: 33482143
pii: S1473-3099(20)30842-2
doi: 10.1016/S1473-3099(20)30842-2
pmc: PMC8064914
pii:
doi:

Substances chimiques

Meningococcal Vaccines 0
serogroup C meningococcal conjugate vaccine 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

677-687

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom

Commentaires et corrections

Type : ErratumIn
Type : ErratumIn

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Published by Elsevier Ltd.. All rights reserved.

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Auteurs

Jenny M MacLennan (JM)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Charlene M C Rodrigues (CMC)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Holly B Bratcher (HB)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Aiswarya Lekshmi (A)

Meningococcal Reference Unit, Public Health England, Manchester Public Health Laboratory, Manchester Royal Infirmary, Manchester, UK.

Adam Finn (A)

School of Cellular and Molecular Medicine, University of Bristol, Bristol, UK.

Jenny Oliver (J)

School of Cellular and Molecular Medicine, University of Bristol, Bristol, UK.

Mandy Wootton (M)

Division of Public Health Wales, Temple of Peace and Health, Cardiff, UK.

Samantha Ray (S)

Division of Public Health Wales, Temple of Peace and Health, Cardiff, UK.

Claire Cameron (C)

NHS National Services Scotland, Health Protection Scotland, Glasgow, UK.

Andrew Smith (A)

Glasgow Dental School, University of Glasgow, UK; Scottish Microbiology Reference Laboratory, NHS Greater Glasgow & Clyde, Glasgow, UK.

Paul T Heath (PT)

St George's Vaccine Institute, Institute of Infection & Immunity, St George's University of London, London, UK.

Angela Bartolf (A)

St George's Vaccine Institute, Institute of Infection & Immunity, St George's University of London, London, UK.

Tracey Nolan (T)

Research and Development Department, Maidstone and Tunbridge Wells NHS Trust, Maidstone, Kent, UK.

Stephen Hughes (S)

Central Manchester University Hospitals, NHS Foundation Trust, Manchester, UK.

Anu Varghese (A)

Central Manchester University Hospitals, NHS Foundation Trust, Manchester, UK.

Matthew D Snape (MD)

Oxford Vaccine Group, Department of Paediatrics, University of Oxford and the National Institute for Health Research Oxford Biomedical Research Centre, Oxford, UK.

Richard Sewell (R)

Oxford Vaccine Group, Department of Paediatrics, University of Oxford and the National Institute for Health Research Oxford Biomedical Research Centre, Oxford, UK.

Richard Cunningham (R)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Alison Stolton (A)

Microbiology Department, University Hospitals Plymouth NHS Trust, UK.

Carole Kay (C)

Lancashire and South Cumbria NHS Foundation Trust, Preston, Lancashire, UK.

Karen Palmer (K)

Lancashire and South Cumbria NHS Foundation Trust, Preston, Lancashire, UK.

David Baxter (D)

Stockport NHS Foundation Trust, Stepping Hill Hospital, Stockport, UK.

Debbie Suggitt (D)

Stockport NHS Foundation Trust, Stepping Hill Hospital, Stockport, UK.

Christos S Zipitis (CS)

Manchester Academic Health Science Centre, University of Manchester, Manchester, UK; Department of Paediatrics, Wrightington Wigan and Leigh NHS Foundation Trust, Wigan, UK.

Nicola Pemberton (N)

Clinical Trials Department, Wrightington Wigan and Leigh NHS Foundation Trust, Wigan, UK.

Keith A Jolley (KA)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

James E Bray (JE)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Odile B Harrison (OB)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK.

Shamez N Ladhani (SN)

Paediatric Infectious Diseases Research Group, St George's University of London, London, UK; Immunisation and Countermeasures Division, Public Health England, London, UK.

Andrew J Pollard (AJ)

Oxford Vaccine Group, Department of Paediatrics, University of Oxford and the National Institute for Health Research Oxford Biomedical Research Centre, Oxford, UK.

Raymond Borrow (R)

Meningococcal Reference Unit, Public Health England, Manchester Public Health Laboratory, Manchester Royal Infirmary, Manchester, UK.

Stephen J Gray (SJ)

Meningococcal Reference Unit, Public Health England, Manchester Public Health Laboratory, Manchester Royal Infirmary, Manchester, UK.

Caroline Trotter (C)

Disease Dynamics Unit, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.

Martin C J Maiden (MCJ)

Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, Oxford, UK. Electronic address: martin.maiden@zoo.ox.ac.uk.

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