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

Jenny M MacLennan, Charlene M C Rodrigues, Holly B Bratcher, Aiswarya Lekshmi, Adam Finn, Jenny Oliver, Mandy Wootton, Samantha Ray, Claire Cameron, Andrew Smith, Paul T Heath, Angela Bartolf, Tracey Nolan, Stephen Hughes, Anu Varghese, Matthew D Snape, Richard Sewell, Richard Cunningham, Alison Stolton, Carole KayKaren Palmer, David Baxter, Debbie Suggitt, Christos S Zipitis, Nicola Pemberton, Keith A Jolley, James E Bray, Odile B Harrison, Shamez N Ladhani, Andrew J Pollard, Raymond Borrow, Stephen J Gray, Caroline Trotter, Martin C J Maiden*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

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Abstract

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.

Original languageEnglish
Pages (from-to)677-687
Number of pages11
JournalLancet Infectious Diseases
Volume21
Issue number5
Early online date19 Jan 2021
DOIs
Publication statusPublished - May 2021

Bibliographical note

Funding Information:
AJP chairs the UK Department of Health and Social Care's Joint Committee on Vaccination and Immunisation and the European Medicines Agency Scientific Advisory Group on vaccines; is a member of WHO's Strategic Advisory Group of Experts; is supported by the National Institute for Health Research's Oxford Biomedical Research Centre; and is a National Institute for Health Research senior investigator. MDS is supported by the National Institute for Health Research of Oxford Biomedical Research Centre; and reports grants from Pfizer, Novavax, Medimmune, Janssen, MCM Vaccine, GlaxoSmithKline, outside the submitted work. CT reports personal fees from GlaxoSmithKline, outside the submitted work. SJG works for Public Health England Meningococcal Reference Unit that has supported carriage studies involving immunisation interventions provided by GlaxoSmithKline and Pfizer, outside the submitted work. SH reports personal fees from Sanofi Pasteur and Pfizer, outside the submitted work. RB does contract research on behalf of Public Health England for GlaxoSmithKline, Pfizer, and Sanofi Pasteur, outside the submitted work. KAJ reports grants from Wellcome Trust, during the conduct of the study; and personal fees from GlaxoSmithKline and Pfizer, outside the submitted work. AL does contract research on behalf of Public Health England for GlaxoSmithKline, Pfizer, and Sanofi Pasteur, outside the submitted work. AF reports grants from Wellcome Trust, during the conduct of the study; and grants from GlaxoSmithKline, Sanofi Pasteur, Pfizer, Novovax, and MedImmune, outside the submitted work. All other authors declare no competing interests.

Funding Information:
This study was funded by the Wellcome Trust, the UK Department of Health, and National Institute for Health Research Policy Research Programme (PR-ST-0915?10015). The views expressed are those of the author(s) and not necessarily those of the National Institute for Health Research, the Department of Health and Social Care, or WHO. We thank the 11 study centre staff for their participation in and commitment to the organisation of the study, recruitment of participants and sample and data processing. We also thank Catherine O'Sullivan, Eva Galiza, Susan Baden, Leanne Poulton, Isabelle Hubbard, Hana Tabusa, Tatiana Munera Huertas, Timothy Planche, Irene Monahan, Catherine Cosgrove, Rooba Kauppayamootoo, Syed Ahmed, Rina Duff, and Jennifer Reid. We thank the staff at the Meningococcal Reference Unit (Manchester, UK) for their ongoing support with microbiological expertise, especially Anthony Carr, Michael Fairhurst, Stephen Clark, Laura Campbell, and Andrew Walker, and staff at the Scottish Haemophilus, Legionella, Meningococcus, and Pneumococcus Reference Laboratory (NHS Greater Glasgow & Clyde, Glasgow, UK), especially Roisin Ure for bacterial culture and identification of meningococcal isolates from throat swabs.

Funding Information:
This study was funded by the Wellcome Trust, the UK Department of Health, and National Institute for Health Research Policy Research Programme (PR-ST-0915–10015). The views expressed are those of the author(s) and not necessarily those of the National Institute for Health Research, the Department of Health and Social Care, or WHO. We thank the 11 study centre staff for their participation in and commitment to the organisation of the study, recruitment of participants and sample and data processing. We also thank Catherine O'Sullivan, Eva Galiza, Susan Baden, Leanne Poulton, Isabelle Hubbard, Hana Tabusa, Tatiana Munera Huertas, Timothy Planche, Irene Monahan, Catherine Cosgrove, Rooba Kauppayamootoo, Syed Ahmed, Rina Duff, and Jennifer Reid. We thank the staff at the Meningococcal Reference Unit (Manchester, UK) for their ongoing support with microbiological expertise, especially Anthony Carr, Michael Fairhurst, Stephen Clark, Laura Campbell, and Andrew Walker, and staff at the Scottish Haemophilus, Legionella, Meningococcus, and Pneumococcus Reference Laboratory (NHS Greater Glasgow & Clyde, Glasgow, UK), especially Roisin Ure for bacterial culture and identification of meningococcal isolates from throat swabs.

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

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