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A mosaic tetracycline resistance gene tet(S/M) detected in an MDR pneumococcal CC230 lineage that underwent capsular switching in South Africa

A mosaic tetracycline resistance gene tet(S/M) detected in an MDR pneumococcal CC230 lineage that underwent capsular switching in South Africa
A mosaic tetracycline resistance gene tet(S/M) detected in an MDR pneumococcal CC230 lineage that underwent capsular switching in South Africa
Objectives: we reported tet(S/M) in Streptococcus pneumoniae and investigated its temporal spread in relation to nationwide clinical interventions. Methods: we whole-genome sequenced 12 254 pneumococcal isolates from 29 countries on an Illumina HiSeq sequencer. Serotype, multilocus ST and antibiotic resistance were inferred from genomes. An SNP tree was built using Gubbins. Temporal spread was reconstructed using a birth–death model. Results: we identified tet(S/M) in 131 pneumococcal isolates and none carried other known tet genes. Tetracycline susceptibility testing results were available for 121 tet(S/M)-positive isolates and all were resistant. A majority (74%) of tet(S/M)-positive isolates were from South Africa and caused invasive diseases among young children (59% HIV positive, where HIV status was available). All but two tet(S/M)-positive isolates belonged to clonal complex (CC) 230. A global phylogeny of CC230 (n=389) revealed that tet(S/M)-positive isolates formed a sublineage predicted to exhibit resistance to penicillin, co-trimoxazole, erythromycin and tetracycline. The birth–death model detected an unrecognized outbreak of this sublineage in South Africa between 2000 and 2004 with expected secondary infections (effective reproductive number, R) of ∼2.5. R declined to ∼1.0 in 2005 and <1.0 in 2012. The declining epidemic could be related to improved access to ART in 2004 and introduction of pneumococcal conjugate vaccine (PCV) in 2009. Capsular switching from vaccine serotype 14 to non-vaccine serotype 23A was observed within the sublineage. Conclusions: the prevalence of tet(S/M) in pneumococci was low and its dissemination was due to an unrecognized outbreak of CC230 in South Africa. Capsular switching in this MDR sublineage highlighted its potential to continue to cause disease in the post-PCV13 era.
0305-7453
512–520
Lo, Stephanie W.
607ccad6-93b1-484c-ba8d-9821432fce90
Gladstone, Rebecca
6a2011bf-2561-4956-9928-46e6b927ba6d
van Tonder, Andries J.
1a37668a-1318-443b-b504-c16249723441
Clarke, Stuart
f7d7f7a2-4b1f-4b36-883a-0f967e73fb17
The Global Pneumococcal Sequencing Consortium
Lo, Stephanie W.
607ccad6-93b1-484c-ba8d-9821432fce90
Gladstone, Rebecca
6a2011bf-2561-4956-9928-46e6b927ba6d
van Tonder, Andries J.
1a37668a-1318-443b-b504-c16249723441
Clarke, Stuart
f7d7f7a2-4b1f-4b36-883a-0f967e73fb17

Lo, Stephanie W., Gladstone, Rebecca and van Tonder, Andries J. , The Global Pneumococcal Sequencing Consortium (2020) A mosaic tetracycline resistance gene tet(S/M) detected in an MDR pneumococcal CC230 lineage that underwent capsular switching in South Africa. Journal of Antimicrobial Chemotherapy, 75 (3), 512–520. (doi:10.1093/jac/dkz477).

Record type: Article

Abstract

Objectives: we reported tet(S/M) in Streptococcus pneumoniae and investigated its temporal spread in relation to nationwide clinical interventions. Methods: we whole-genome sequenced 12 254 pneumococcal isolates from 29 countries on an Illumina HiSeq sequencer. Serotype, multilocus ST and antibiotic resistance were inferred from genomes. An SNP tree was built using Gubbins. Temporal spread was reconstructed using a birth–death model. Results: we identified tet(S/M) in 131 pneumococcal isolates and none carried other known tet genes. Tetracycline susceptibility testing results were available for 121 tet(S/M)-positive isolates and all were resistant. A majority (74%) of tet(S/M)-positive isolates were from South Africa and caused invasive diseases among young children (59% HIV positive, where HIV status was available). All but two tet(S/M)-positive isolates belonged to clonal complex (CC) 230. A global phylogeny of CC230 (n=389) revealed that tet(S/M)-positive isolates formed a sublineage predicted to exhibit resistance to penicillin, co-trimoxazole, erythromycin and tetracycline. The birth–death model detected an unrecognized outbreak of this sublineage in South Africa between 2000 and 2004 with expected secondary infections (effective reproductive number, R) of ∼2.5. R declined to ∼1.0 in 2005 and <1.0 in 2012. The declining epidemic could be related to improved access to ART in 2004 and introduction of pneumococcal conjugate vaccine (PCV) in 2009. Capsular switching from vaccine serotype 14 to non-vaccine serotype 23A was observed within the sublineage. Conclusions: the prevalence of tet(S/M) in pneumococci was low and its dissemination was due to an unrecognized outbreak of CC230 in South Africa. Capsular switching in this MDR sublineage highlighted its potential to continue to cause disease in the post-PCV13 era.

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Accepted/In Press date: 16 October 2019
e-pub ahead of print date: 2 December 2019
Published date: 1 March 2020

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Local EPrints ID: 447816
URI: http://eprints.soton.ac.uk/id/eprint/447816
ISSN: 0305-7453
PURE UUID: 7a5ae2ac-5fa2-4129-bd58-e8089de5b88b
ORCID for Stuart Clarke: ORCID iD orcid.org/0000-0002-7009-1548

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Date deposited: 23 Mar 2021 17:36
Last modified: 24 Mar 2021 02:39

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Contributors

Author: Stephanie W. Lo
Author: Rebecca Gladstone
Author: Andries J. van Tonder
Author: Stuart Clarke ORCID iD
Corporate Author: The Global Pneumococcal Sequencing Consortium

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