Pneumococcal Colonization and the Nasopharyngeal Microbiota of Children in Botswana

Matthew S. Kelly, Michael G. Surette, Marek Smieja, Laura Rossi, Kathy Luinstra, Andrew P. Steenhoff, David M. Goldfarb, Jeffrey M. Pernica, Tonya Arscott-Mills, Sefelani Boiditswe, Tiny Mazhani, John F. Rawls, Coleen K. Cunningham, Samir S. Shah, Kristen A. Feemster, Patrick Casey Seed

Research output: Contribution to journalArticle

Abstract

BACKGROUND: Nasopharyngeal colonization precedes infections caused by Streptococcus pneumoniae. A more detailed understanding of interactions between S. pneumoniae and the nasopharyngeal microbiota of children could inform strategies to prevent pneumococcal infections.

METHODS: We collected nasopharyngeal swabs from children 1 to 23 months of age in Botswana between August 2012 and June 2016. We tested samples for S. pneumoniae and common respiratory viruses using polymerase chain reaction. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used random forest models to identify clinical variables and bacterial genera that were associated with pneumococcal colonization.

RESULTS: Mean age of the 170 children included in this study was 8.3 months. Ninety-six (56%) children were colonized with S. pneumoniae. Pneumococcal colonization was associated with older age (P = 0.0001), a lack of electricity in the home (P = 0.02) and household use of wood as a cooking fuel (P = 0.002). Upper respiratory symptoms were more frequent in children with S. pneumoniae colonization (60% vs. 32%; P = 0.001). Adjusting for age, nasopharyngeal microbiota composition differed in colonized and noncolonized children (P = 0.001). S. pneumoniae colonization was associated with a higher relative abundance of Moraxella (P = 0.001) and lower relative abundances of Corynebacterium (P = 0.001) and Staphylococcus (P = 0.03). A decision tree model containing the relative abundances of bacterial genera had 81% sensitivity and 85% specificity for the determination of S. pneumoniae colonization status.

CONCLUSIONS: S. pneumoniae colonization is associated with characteristic alterations of the nasopharyngeal microbiota of children. Prospective studies should determine if nasopharyngeal microbial composition alters the risk of pneumococcal colonization and thus could be modified as a novel pneumonia prevention strategy.

Original languageEnglish (US)
Pages (from-to)1176-1183
Number of pages8
JournalThe Pediatric infectious disease journal
Volume37
Issue number11
DOIs
StatePublished - Nov 1 2018

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Botswana
Microbiota
Streptococcus pneumoniae
Pneumococcal Infections
Moraxella
16S Ribosomal RNA
Corynebacterium
Electricity
Decision Trees
Cooking
Staphylococcus
rRNA Genes
Pneumonia
Prospective Studies
Viruses
Sensitivity and Specificity
Polymerase Chain Reaction

ASJC Scopus subject areas

  • Pediatrics, Perinatology, and Child Health
  • Microbiology (medical)
  • Infectious Diseases

Cite this

Kelly, Matthew S. ; Surette, Michael G. ; Smieja, Marek ; Rossi, Laura ; Luinstra, Kathy ; Steenhoff, Andrew P. ; Goldfarb, David M. ; Pernica, Jeffrey M. ; Arscott-Mills, Tonya ; Boiditswe, Sefelani ; Mazhani, Tiny ; Rawls, John F. ; Cunningham, Coleen K. ; Shah, Samir S. ; Feemster, Kristen A. ; Seed, Patrick Casey. / Pneumococcal Colonization and the Nasopharyngeal Microbiota of Children in Botswana. In: The Pediatric infectious disease journal. 2018 ; Vol. 37, No. 11. pp. 1176-1183.
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abstract = "BACKGROUND: Nasopharyngeal colonization precedes infections caused by Streptococcus pneumoniae. A more detailed understanding of interactions between S. pneumoniae and the nasopharyngeal microbiota of children could inform strategies to prevent pneumococcal infections.METHODS: We collected nasopharyngeal swabs from children 1 to 23 months of age in Botswana between August 2012 and June 2016. We tested samples for S. pneumoniae and common respiratory viruses using polymerase chain reaction. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used random forest models to identify clinical variables and bacterial genera that were associated with pneumococcal colonization.RESULTS: Mean age of the 170 children included in this study was 8.3 months. Ninety-six (56{\%}) children were colonized with S. pneumoniae. Pneumococcal colonization was associated with older age (P = 0.0001), a lack of electricity in the home (P = 0.02) and household use of wood as a cooking fuel (P = 0.002). Upper respiratory symptoms were more frequent in children with S. pneumoniae colonization (60{\%} vs. 32{\%}; P = 0.001). Adjusting for age, nasopharyngeal microbiota composition differed in colonized and noncolonized children (P = 0.001). S. pneumoniae colonization was associated with a higher relative abundance of Moraxella (P = 0.001) and lower relative abundances of Corynebacterium (P = 0.001) and Staphylococcus (P = 0.03). A decision tree model containing the relative abundances of bacterial genera had 81{\%} sensitivity and 85{\%} specificity for the determination of S. pneumoniae colonization status.CONCLUSIONS: S. pneumoniae colonization is associated with characteristic alterations of the nasopharyngeal microbiota of children. Prospective studies should determine if nasopharyngeal microbial composition alters the risk of pneumococcal colonization and thus could be modified as a novel pneumonia prevention strategy.",
author = "Kelly, {Matthew S.} and Surette, {Michael G.} and Marek Smieja and Laura Rossi and Kathy Luinstra and Steenhoff, {Andrew P.} and Goldfarb, {David M.} and Pernica, {Jeffrey M.} and Tonya Arscott-Mills and Sefelani Boiditswe and Tiny Mazhani and Rawls, {John F.} and Cunningham, {Coleen K.} and Shah, {Samir S.} and Feemster, {Kristen A.} and Seed, {Patrick Casey}",
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Kelly, MS, Surette, MG, Smieja, M, Rossi, L, Luinstra, K, Steenhoff, AP, Goldfarb, DM, Pernica, JM, Arscott-Mills, T, Boiditswe, S, Mazhani, T, Rawls, JF, Cunningham, CK, Shah, SS, Feemster, KA & Seed, PC 2018, 'Pneumococcal Colonization and the Nasopharyngeal Microbiota of Children in Botswana', The Pediatric infectious disease journal, vol. 37, no. 11, pp. 1176-1183. https://doi.org/10.1097/INF.0000000000002174

Pneumococcal Colonization and the Nasopharyngeal Microbiota of Children in Botswana. / Kelly, Matthew S.; Surette, Michael G.; Smieja, Marek; Rossi, Laura; Luinstra, Kathy; Steenhoff, Andrew P.; Goldfarb, David M.; Pernica, Jeffrey M.; Arscott-Mills, Tonya; Boiditswe, Sefelani; Mazhani, Tiny; Rawls, John F.; Cunningham, Coleen K.; Shah, Samir S.; Feemster, Kristen A.; Seed, Patrick Casey.

In: The Pediatric infectious disease journal, Vol. 37, No. 11, 01.11.2018, p. 1176-1183.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Pneumococcal Colonization and the Nasopharyngeal Microbiota of Children in Botswana

AU - Kelly, Matthew S.

AU - Surette, Michael G.

AU - Smieja, Marek

AU - Rossi, Laura

AU - Luinstra, Kathy

AU - Steenhoff, Andrew P.

AU - Goldfarb, David M.

AU - Pernica, Jeffrey M.

AU - Arscott-Mills, Tonya

AU - Boiditswe, Sefelani

AU - Mazhani, Tiny

AU - Rawls, John F.

AU - Cunningham, Coleen K.

AU - Shah, Samir S.

AU - Feemster, Kristen A.

AU - Seed, Patrick Casey

PY - 2018/11/1

Y1 - 2018/11/1

N2 - BACKGROUND: Nasopharyngeal colonization precedes infections caused by Streptococcus pneumoniae. A more detailed understanding of interactions between S. pneumoniae and the nasopharyngeal microbiota of children could inform strategies to prevent pneumococcal infections.METHODS: We collected nasopharyngeal swabs from children 1 to 23 months of age in Botswana between August 2012 and June 2016. We tested samples for S. pneumoniae and common respiratory viruses using polymerase chain reaction. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used random forest models to identify clinical variables and bacterial genera that were associated with pneumococcal colonization.RESULTS: Mean age of the 170 children included in this study was 8.3 months. Ninety-six (56%) children were colonized with S. pneumoniae. Pneumococcal colonization was associated with older age (P = 0.0001), a lack of electricity in the home (P = 0.02) and household use of wood as a cooking fuel (P = 0.002). Upper respiratory symptoms were more frequent in children with S. pneumoniae colonization (60% vs. 32%; P = 0.001). Adjusting for age, nasopharyngeal microbiota composition differed in colonized and noncolonized children (P = 0.001). S. pneumoniae colonization was associated with a higher relative abundance of Moraxella (P = 0.001) and lower relative abundances of Corynebacterium (P = 0.001) and Staphylococcus (P = 0.03). A decision tree model containing the relative abundances of bacterial genera had 81% sensitivity and 85% specificity for the determination of S. pneumoniae colonization status.CONCLUSIONS: S. pneumoniae colonization is associated with characteristic alterations of the nasopharyngeal microbiota of children. Prospective studies should determine if nasopharyngeal microbial composition alters the risk of pneumococcal colonization and thus could be modified as a novel pneumonia prevention strategy.

AB - BACKGROUND: Nasopharyngeal colonization precedes infections caused by Streptococcus pneumoniae. A more detailed understanding of interactions between S. pneumoniae and the nasopharyngeal microbiota of children could inform strategies to prevent pneumococcal infections.METHODS: We collected nasopharyngeal swabs from children 1 to 23 months of age in Botswana between August 2012 and June 2016. We tested samples for S. pneumoniae and common respiratory viruses using polymerase chain reaction. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used random forest models to identify clinical variables and bacterial genera that were associated with pneumococcal colonization.RESULTS: Mean age of the 170 children included in this study was 8.3 months. Ninety-six (56%) children were colonized with S. pneumoniae. Pneumococcal colonization was associated with older age (P = 0.0001), a lack of electricity in the home (P = 0.02) and household use of wood as a cooking fuel (P = 0.002). Upper respiratory symptoms were more frequent in children with S. pneumoniae colonization (60% vs. 32%; P = 0.001). Adjusting for age, nasopharyngeal microbiota composition differed in colonized and noncolonized children (P = 0.001). S. pneumoniae colonization was associated with a higher relative abundance of Moraxella (P = 0.001) and lower relative abundances of Corynebacterium (P = 0.001) and Staphylococcus (P = 0.03). A decision tree model containing the relative abundances of bacterial genera had 81% sensitivity and 85% specificity for the determination of S. pneumoniae colonization status.CONCLUSIONS: S. pneumoniae colonization is associated with characteristic alterations of the nasopharyngeal microbiota of children. Prospective studies should determine if nasopharyngeal microbial composition alters the risk of pneumococcal colonization and thus could be modified as a novel pneumonia prevention strategy.

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