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Article: Geographical migration and fitness dynamics of Streptococcus pneumoniae

TitleGeographical migration and fitness dynamics of Streptococcus pneumoniae
Authors
Belman, SophieLefrancq, NoémieNzenze, SusanDowns, Sarahdu Plessis, MignonLo, Stephanie W.McGee, LesleyMadhi, Shabir A.von Gottberg, AnneBentley, Stephen D.Salje, HenrikCorso, AlejandraGagetti, PaulaBrooks, Abdullah W.Hasanuzzaman, MdSaha, Samir K.Saha, SenjutiDavydov, AlexanderTitov, LeonidAlmeida, Samanta Cristine GrassiTurner, PaulZhao, ChunjiangWang, HuiIp, MargaretHo, Pak LeungLaw, PierraKeenan, Jeremy D.Cohen, RobertVaron, EmmanuelleSampane-Donkor, EricVeeraraghavan, BalajiNagaraj, GeethaRavikumar, K. L.Yuvaraj, J.Shamanna Noga, VarunBenisty, RachelDagan, RonBigogo, GodfreyVerani, JenniferKiran, AnmolEverett, Dean B.Cornick, JenniferAlaerts, MaaikeSekaran, Shamala DeviClarke, Stuart C.Moiane, BenildSigauque, BetuelMucavele, HelioPollard, Andrew J.Kandasamy, RamaCarter, Philip E.Obaro, Stephen K.Lehmann, DeborahFord, RebeccaOchoa, Theresa J.Skoczynska, AnnaSadowy, EwaHryniewicz, WaleriaPuzia, WeronikaDoiphode, SanjayEgorova, EkaterinaVoropaeva, ElenaUrban, YuliaKastrin, TamaraNdlangisa, KediboneDe Gouveia, LindaAli, MushalWolter, NicoleLekhuleni, CebileAlmagro, Carmen MuñozAlonso, Alba RedinHenares, DesireeSrifuengfung, SompornKwambana-Adams, BrendaFoster-Nyarko, EbenezerBojang, EbrimaAntonio, MartinTientcheu, Peggy EstelleMoïsi, JenniferNurse-Lucas, MicheleAkpaka, Patrick E.Eser, Özgen KöseogluScott, AnthonyAanensen, DavidCroucher, NicholasLees, John A.Gladstone, Rebecca A.Tonkin-Hill, GerryChaguza, ChrispinCleary, DavidMellor, KateBeall, BernardKlugman, Keith P.Rodgers, GailHawkins, Paulina A.Blaschke, Anne J.Pershing, Nicole L.
Issue Date3-Jul-2024
PublisherNature Research
Citation
Nature, 2024, v. 631, n. 8020, p. 386-392 How to Cite?
AbstractStreptococcus pneumoniae is a leading cause of pneumonia and meningitis worldwide. Many different serotypes co-circulate endemically in any one location1,2. The extent and mechanisms of spread and vaccine-driven changes in fitness and antimicrobial resistance remain largely unquantified. Here using geolocated genome sequences from South Africa (n = 6,910, collected from 2000 to 2014), we developed models to reconstruct spread, pairing detailed human mobility data and genomic data. Separately, we estimated the population-level changes in fitness of strains that are included (vaccine type (VT)) and not included (non-vaccine type (NVT)) in pneumococcal conjugate vaccines, first implemented in South Africa in 2009. Differences in strain fitness between those that are and are not resistant to penicillin were also evaluated. We found that pneumococci only become homogenously mixed across South Africa after 50 years of transmission, with the slow spread driven by the focal nature of human mobility. Furthermore, in the years following vaccine implementation, the relative fitness of NVT compared with VT strains increased (relative risk of 1.68; 95% confidence interval of 1.59–1.77), with an increasing proportion of these NVT strains becoming resistant to penicillin. Our findings point to highly entrenched, slow transmission and indicate that initial vaccine-linked decreases in antimicrobial resistance may be transient.
Persistent Identifierhttp://hdl.handle.net/10722/354910
ISSN
2023 Impact Factor: 50.5
2023 SCImago Journal Rankings: 18.509

 

DC FieldValueLanguage
dc.contributor.authorBelman, Sophie-
dc.contributor.authorLefrancq, Noémie-
dc.contributor.authorNzenze, Susan-
dc.contributor.authorDowns, Sarah-
dc.contributor.authordu Plessis, Mignon-
dc.contributor.authorLo, Stephanie W.-
dc.contributor.authorMcGee, Lesley-
dc.contributor.authorMadhi, Shabir A.-
dc.contributor.authorvon Gottberg, Anne-
dc.contributor.authorBentley, Stephen D.-
dc.contributor.authorSalje, Henrik-
dc.contributor.authorCorso, Alejandra-
dc.contributor.authorGagetti, Paula-
dc.contributor.authorBrooks, Abdullah W.-
dc.contributor.authorHasanuzzaman, Md-
dc.contributor.authorSaha, Samir K.-
dc.contributor.authorSaha, Senjuti-
dc.contributor.authorDavydov, Alexander-
dc.contributor.authorTitov, Leonid-
dc.contributor.authorAlmeida, Samanta Cristine Grassi-
dc.contributor.authorTurner, Paul-
dc.contributor.authorZhao, Chunjiang-
dc.contributor.authorWang, Hui-
dc.contributor.authorIp, Margaret-
dc.contributor.authorHo, Pak Leung-
dc.contributor.authorLaw, Pierra-
dc.contributor.authorKeenan, Jeremy D.-
dc.contributor.authorCohen, Robert-
dc.contributor.authorVaron, Emmanuelle-
dc.contributor.authorSampane-Donkor, Eric-
dc.contributor.authorVeeraraghavan, Balaji-
dc.contributor.authorNagaraj, Geetha-
dc.contributor.authorRavikumar, K. L.-
dc.contributor.authorYuvaraj, J.-
dc.contributor.authorShamanna Noga, Varun-
dc.contributor.authorBenisty, Rachel-
dc.contributor.authorDagan, Ron-
dc.contributor.authorBigogo, Godfrey-
dc.contributor.authorVerani, Jennifer-
dc.contributor.authorKiran, Anmol-
dc.contributor.authorEverett, Dean B.-
dc.contributor.authorCornick, Jennifer-
dc.contributor.authorAlaerts, Maaike-
dc.contributor.authorSekaran, Shamala Devi-
dc.contributor.authorClarke, Stuart C.-
dc.contributor.authorMoiane, Benild-
dc.contributor.authorSigauque, Betuel-
dc.contributor.authorMucavele, Helio-
dc.contributor.authorPollard, Andrew J.-
dc.contributor.authorKandasamy, Rama-
dc.contributor.authorCarter, Philip E.-
dc.contributor.authorObaro, Stephen K.-
dc.contributor.authorLehmann, Deborah-
dc.contributor.authorFord, Rebecca-
dc.contributor.authorOchoa, Theresa J.-
dc.contributor.authorSkoczynska, Anna-
dc.contributor.authorSadowy, Ewa-
dc.contributor.authorHryniewicz, Waleria-
dc.contributor.authorPuzia, Weronika-
dc.contributor.authorDoiphode, Sanjay-
dc.contributor.authorEgorova, Ekaterina-
dc.contributor.authorVoropaeva, Elena-
dc.contributor.authorUrban, Yulia-
dc.contributor.authorKastrin, Tamara-
dc.contributor.authorNdlangisa, Kedibone-
dc.contributor.authorDe Gouveia, Linda-
dc.contributor.authorAli, Mushal-
dc.contributor.authorWolter, Nicole-
dc.contributor.authorLekhuleni, Cebile-
dc.contributor.authorAlmagro, Carmen Muñoz-
dc.contributor.authorAlonso, Alba Redin-
dc.contributor.authorHenares, Desiree-
dc.contributor.authorSrifuengfung, Somporn-
dc.contributor.authorKwambana-Adams, Brenda-
dc.contributor.authorFoster-Nyarko, Ebenezer-
dc.contributor.authorBojang, Ebrima-
dc.contributor.authorAntonio, Martin-
dc.contributor.authorTientcheu, Peggy Estelle-
dc.contributor.authorMoïsi, Jennifer-
dc.contributor.authorNurse-Lucas, Michele-
dc.contributor.authorAkpaka, Patrick E.-
dc.contributor.authorEser, Özgen Köseoglu-
dc.contributor.authorScott, Anthony-
dc.contributor.authorAanensen, David-
dc.contributor.authorCroucher, Nicholas-
dc.contributor.authorLees, John A.-
dc.contributor.authorGladstone, Rebecca A.-
dc.contributor.authorTonkin-Hill, Gerry-
dc.contributor.authorChaguza, Chrispin-
dc.contributor.authorCleary, David-
dc.contributor.authorMellor, Kate-
dc.contributor.authorBeall, Bernard-
dc.contributor.authorKlugman, Keith P.-
dc.contributor.authorRodgers, Gail-
dc.contributor.authorHawkins, Paulina A.-
dc.contributor.authorBlaschke, Anne J.-
dc.contributor.authorPershing, Nicole L.-
dc.date.accessioned2025-03-15T00:35:17Z-
dc.date.available2025-03-15T00:35:17Z-
dc.date.issued2024-07-03-
dc.identifier.citationNature, 2024, v. 631, n. 8020, p. 386-392-
dc.identifier.issn0028-0836-
dc.identifier.urihttp://hdl.handle.net/10722/354910-
dc.description.abstractStreptococcus pneumoniae is a leading cause of pneumonia and meningitis worldwide. Many different serotypes co-circulate endemically in any one location1,2. The extent and mechanisms of spread and vaccine-driven changes in fitness and antimicrobial resistance remain largely unquantified. Here using geolocated genome sequences from South Africa (n = 6,910, collected from 2000 to 2014), we developed models to reconstruct spread, pairing detailed human mobility data and genomic data. Separately, we estimated the population-level changes in fitness of strains that are included (vaccine type (VT)) and not included (non-vaccine type (NVT)) in pneumococcal conjugate vaccines, first implemented in South Africa in 2009. Differences in strain fitness between those that are and are not resistant to penicillin were also evaluated. We found that pneumococci only become homogenously mixed across South Africa after 50 years of transmission, with the slow spread driven by the focal nature of human mobility. Furthermore, in the years following vaccine implementation, the relative fitness of NVT compared with VT strains increased (relative risk of 1.68; 95% confidence interval of 1.59–1.77), with an increasing proportion of these NVT strains becoming resistant to penicillin. Our findings point to highly entrenched, slow transmission and indicate that initial vaccine-linked decreases in antimicrobial resistance may be transient.-
dc.languageeng-
dc.publisherNature Research-
dc.relation.ispartofNature-
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.-
dc.titleGeographical migration and fitness dynamics of Streptococcus pneumoniae-
dc.typeArticle-
dc.identifier.doi10.1038/s41586-024-07626-3-
dc.identifier.pmid38961295-
dc.identifier.scopuseid_2-s2.0-85197560021-
dc.identifier.volume631-
dc.identifier.issue8020-
dc.identifier.spage386-
dc.identifier.epage392-
dc.identifier.eissn1476-4687-
dc.identifier.issnl0028-0836-

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