Genomic epidemiology of Streptococcus pneumoniae serotype 16F lineages

Jolynne Mokaya; Kate C. Mellor; Gemma G. R. Murray; Akuzike Kalizang’oma; Cebile Lekhuleni; Heather J. Zar; Mark P. Nicol; Lesley McGee; Stephen D. Bentley; Stephanie W. Lo; Felix Dube

doi:10.1099/mgen.0.001123

Genomic epidemiology of Streptococcus pneumoniae serotype 16F lineages

Jolynne Mokaya¹, Kate C. Mellor¹, Gemma G. R. Murray^1,2, Akuzike Kalizang’oma^3,4, Cebile Lekhuleni^5,6, Heather J. Zar⁷, Mark P. Nicol⁸, Lesley McGee⁹, Stephen D. Bentley¹, Stephanie W. Lo^1,10 and Felix Dube^11,12
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¹ Parasites and Microbes, Wellcome Sanger Institute, Hinxton, UK ² Department of Genetics, Evolution and Environment, University College London, London, UK ³ NIHR Mucosal Pathogens Research Unit, Research Department of Infection, Division of Infection and Immunity, University College London, London, UK ⁴ Malawi-Liverpool-Wellcome Research Programme, Blantyre, Malawi ⁵ Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a division of the National Health Laboratory Service, Johannesburg, South Africa ⁶ School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa ⁷ Department of Paediatrics and Child Health, Red Cross War Memorial Childrenʼs Hospital and SA-MRC unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa ⁸ Marshall Centre, School of Biomedical Sciences, University of Western Australia, School of Biomedical Sciences, Perth, ACT, Australia ⁹ Centers for Disease Control and Prevention, Atlanta, GA, USA ¹⁰ Milner Centre for Evolution, Life Sciences Department, University of Bath, Bath, UK ¹¹ Department of Molecular and Cell Biology and Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, South Africa ¹² School of Medicine, University of Lusaka, Lusaka, Zambia
*Correspondence: Jolynne Mokaya, [email protected]
Published: 02 November 2023 https://doi.org/10.1099/mgen.0.001123

Abstract

Due to the emergence of non-vaccine serotypes in vaccinated populations, Streptococcus pneumoniae remains a major global health challenge despite advances in vaccine development. Serotype 16F is among the predominant non-vaccine serotypes identified among vaccinated infants in South Africa (SA). To characterize lineages and antimicrobial resistance in 16F isolates obtained from South Africa and place the local findings in a global context, we analysed 10 923 S . pneumoniae carriage isolates obtained from infants recruited as part of a broader SA birth cohort. We inferred serotype, resistance profile for penicillin, chloramphenicol, cotrimoxazole, erythromycin and tetracycline, and global pneumococcal sequence clusters (GPSCs) from genomic data. To ensure global representation, we also included S. pneumoniae carriage and disease isolates from the Global Pneumococcal Sequencing (GPS) project database (n=19 607, collected from 49 countries across 5 continents, 1995–2018, accessed 17 March 2022). Nine per cent (934/10923) of isolates obtained from infants in the Drakenstein community in SA and 2 %(419/19607) of genomes in the GPS dataset were serotype 16F. Serotype 16F isolates were from 28 different lineages of S. pneumoniae, with GPSC33 and GPSC46 having the highest proportion of serotype 16F isolates at 26 % (346/1353) and 53 % (716/1353), respectively. Serotype 16F isolates were identified globally, but most isolates were collected from Africa. GPSC33 was associated with carriage [OR (95 % CI) 0.24 (0.09–0.66); P=0.003], while GPSC46 was associated with disease [OR (95 % CI) 19.9 (2.56–906.50); P=0.0004]. Ten per cent (37/346) and 15 % (53/346) of isolates within GPSC33 had genes associated with resistance to penicillin and co-trimoxazole, respectively, and 18 % (128/716) of isolates within GPSC46 had genes associated with resistance to co-trimoxazole. Resistant isolates formed genetic clusters, which may suggest emerging resistant lineages. Serotype 16F lineages were common in southern Africa. Some of these lineages were associated with disease and resistance to penicillin and cotrimoxazole. We recommend continuous genomic surveillance to determine the long-term impact of serotype 16F lineages on vaccine efficacy and antimicrobial therapy globally. Investing in vaccine strategies that offer protection over a wide range of serotypes/lineages remains essential. This paper contains data hosted by Microreact.

Received: 25/08/2023
Accepted: 09/10/2023
Published Online: 02/11/2023

Keyword(s): antimicrobial resistance , lineages , pneumococci , serotype and virulence

Funding

This study was supported by the:

National Research Foundation of South Africa Grants (Award SRUG2204224295 & SNSF22071239126)
- Principle Award Recipient: FelixDube
Wellcome Trust (Award 098051 and 206194)
- Principle Award Recipient: StephenD Bentley
Bill and Melinda Gates Foundation (Award OPP1034556)
- Principle Award Recipient: StephenD Bentley

This is an open-access article distributed under the terms of the Creative Commons Attribution License.

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/content/journal/mgen/10.1099/mgen.0.001123

Genomic epidemiology of Streptococcus pneumoniae serotype 16F lineages

M Gen 9, 001123 (2023); https://doi.org/10.1099/mgen.0.001123

/content/journal/mgen/10.1099/mgen.0.001123

Microbial Genomics

Volume 9, Issue 11

Research Article

Open Access

Genomic epidemiology of Streptococcus pneumoniae serotype 16F lineages

Abstract

Funding

Supplementary material 1

Supplementary material 2

Supplementary material 3

Supplementary material 4

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