The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana

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

*Corresponding author for this work

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Background: Nearly half of child pneumonia deaths occur in sub-Saharan Africa. Microbial communities in the nasopharynx are a reservoir for pneumonia pathogens and remain poorly described in African children. Methods: Nasopharyngeal swabs were collected from children with pneumonia (N = 204), children with upper respiratory infection symptoms (N = 55) and healthy children (N = 60) in Botswana between April 2012 and April 2014. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used partitioning around medoids to cluster samples into microbiota biotypes. We then used multivariable logistic regression to examine whether microbiota biotypes were associated with pneumonia and upper respiratory infection symptoms. Results: Mean ages of children with pneumonia, children with upper respiratory infection symptoms and healthy children were 8.2, 11.4 and 8.0 months, respectively. Clustering of nasopharyngeal microbiota identified 5 distinct biotypes: Corynebacterium/Dolosigranulum-dominant (23%), Haemophilus-dominant (11%), Moraxella-dominant (24%), Staphylococcus-dominant (13%) and Streptococcus-dominant (28%). The Haemophilus-dominant [odds ratio (OR): 13.55; 95% confidence interval (CI): 2.10-87.26], the Staphylococcus-dominant (OR: 8.27; 95% CI: 2.13-32.14) and the Streptococcus-dominant (OR: 39.97; 95% CI: 6.63-241.00) biotypes were associated with pneumonia. The Moraxella-dominant (OR: 3.71; 95% CI: 1.09-12.64) and Streptococcus-dominant (OR: 12.26; 95% CI: 1.81-83.06) biotypes were associated with upper respiratory infection symptoms. In children with pneumonia, HIV infection was associated with a lower relative abundance of Dolosigranulum (P = 0.03). Conclusions: Pneumonia and upper respiratory infection symptoms are associated with distinct nasopharyngeal microbiota biotypes in African children. A lower abundance of the commensal genus Dolosigranulum may contribute to the higher pneumonia risk of HIV-infected children.

Original languageEnglish (US)
Pages (from-to)e211-e218
JournalPediatric Infectious Disease Journal
Volume36
Issue number9
DOIs
StatePublished - Sep 1 2017

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Botswana
Microbiota
Respiratory Tract Infections
Pneumonia
Odds Ratio
Confidence Intervals
Streptococcus
Moraxella
Haemophilus
Staphylococcus
16S Ribosomal RNA
Corynebacterium
Nasopharynx
Africa South of the Sahara
rRNA Genes
HIV Infections
Cluster Analysis

Keywords

  • children
  • microbial communities
  • microbiota
  • pneumonia
  • respiratory infections

ASJC Scopus subject areas

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

Cite this

Kelly, Matthew S. ; Surette, Michael G. ; Smieja, Marek ; Pernica, Jeffrey M. ; Rossi, Laura ; Luinstra, Kathy ; Steenhoff, Andrew P. ; Feemster, Kristen A. ; Goldfarb, David M. ; Arscott-Mills, Tonya ; Boiditswe, Sefelani ; Rulaganyang, Ikanyeng ; Muthoga, Charles ; Gaofiwe, Letang ; Mazhani, Tiny ; Rawls, John F. ; Cunningham, Coleen K. ; Shah, Samir S. ; Seed, Patrick C. / The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana. In: Pediatric Infectious Disease Journal. 2017 ; Vol. 36, No. 9. pp. e211-e218.
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abstract = "Background: Nearly half of child pneumonia deaths occur in sub-Saharan Africa. Microbial communities in the nasopharynx are a reservoir for pneumonia pathogens and remain poorly described in African children. Methods: Nasopharyngeal swabs were collected from children with pneumonia (N = 204), children with upper respiratory infection symptoms (N = 55) and healthy children (N = 60) in Botswana between April 2012 and April 2014. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used partitioning around medoids to cluster samples into microbiota biotypes. We then used multivariable logistic regression to examine whether microbiota biotypes were associated with pneumonia and upper respiratory infection symptoms. Results: Mean ages of children with pneumonia, children with upper respiratory infection symptoms and healthy children were 8.2, 11.4 and 8.0 months, respectively. Clustering of nasopharyngeal microbiota identified 5 distinct biotypes: Corynebacterium/Dolosigranulum-dominant (23{\%}), Haemophilus-dominant (11{\%}), Moraxella-dominant (24{\%}), Staphylococcus-dominant (13{\%}) and Streptococcus-dominant (28{\%}). The Haemophilus-dominant [odds ratio (OR): 13.55; 95{\%} confidence interval (CI): 2.10-87.26], the Staphylococcus-dominant (OR: 8.27; 95{\%} CI: 2.13-32.14) and the Streptococcus-dominant (OR: 39.97; 95{\%} CI: 6.63-241.00) biotypes were associated with pneumonia. The Moraxella-dominant (OR: 3.71; 95{\%} CI: 1.09-12.64) and Streptococcus-dominant (OR: 12.26; 95{\%} CI: 1.81-83.06) biotypes were associated with upper respiratory infection symptoms. In children with pneumonia, HIV infection was associated with a lower relative abundance of Dolosigranulum (P = 0.03). Conclusions: Pneumonia and upper respiratory infection symptoms are associated with distinct nasopharyngeal microbiota biotypes in African children. A lower abundance of the commensal genus Dolosigranulum may contribute to the higher pneumonia risk of HIV-infected children.",
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author = "Kelly, {Matthew S.} and Surette, {Michael G.} and Marek Smieja and Pernica, {Jeffrey M.} and Laura Rossi and Kathy Luinstra and Steenhoff, {Andrew P.} and Feemster, {Kristen A.} and Goldfarb, {David M.} and Tonya Arscott-Mills and Sefelani Boiditswe and Ikanyeng Rulaganyang and Charles Muthoga and Letang Gaofiwe and Tiny Mazhani and Rawls, {John F.} and Cunningham, {Coleen K.} and Shah, {Samir S.} and Seed, {Patrick C.}",
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Kelly, MS, Surette, MG, Smieja, M, Pernica, JM, Rossi, L, Luinstra, K, Steenhoff, AP, Feemster, KA, Goldfarb, DM, Arscott-Mills, T, Boiditswe, S, Rulaganyang, I, Muthoga, C, Gaofiwe, L, Mazhani, T, Rawls, JF, Cunningham, CK, Shah, SS & Seed, PC 2017, 'The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana', Pediatric Infectious Disease Journal, vol. 36, no. 9, pp. e211-e218. https://doi.org/10.1097/INF.0000000000001607

The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana. / Kelly, Matthew S.; Surette, Michael G.; Smieja, Marek; Pernica, Jeffrey M.; Rossi, Laura; Luinstra, Kathy; Steenhoff, Andrew P.; Feemster, Kristen A.; Goldfarb, David M.; Arscott-Mills, Tonya; Boiditswe, Sefelani; Rulaganyang, Ikanyeng; Muthoga, Charles; Gaofiwe, Letang; Mazhani, Tiny; Rawls, John F.; Cunningham, Coleen K.; Shah, Samir S.; Seed, Patrick C.

In: Pediatric Infectious Disease Journal, Vol. 36, No. 9, 01.09.2017, p. e211-e218.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana

AU - Kelly, Matthew S.

AU - Surette, Michael G.

AU - Smieja, Marek

AU - Pernica, Jeffrey M.

AU - Rossi, Laura

AU - Luinstra, Kathy

AU - Steenhoff, Andrew P.

AU - Feemster, Kristen A.

AU - Goldfarb, David M.

AU - Arscott-Mills, Tonya

AU - Boiditswe, Sefelani

AU - Rulaganyang, Ikanyeng

AU - Muthoga, Charles

AU - Gaofiwe, Letang

AU - Mazhani, Tiny

AU - Rawls, John F.

AU - Cunningham, Coleen K.

AU - Shah, Samir S.

AU - Seed, Patrick C.

PY - 2017/9/1

Y1 - 2017/9/1

N2 - Background: Nearly half of child pneumonia deaths occur in sub-Saharan Africa. Microbial communities in the nasopharynx are a reservoir for pneumonia pathogens and remain poorly described in African children. Methods: Nasopharyngeal swabs were collected from children with pneumonia (N = 204), children with upper respiratory infection symptoms (N = 55) and healthy children (N = 60) in Botswana between April 2012 and April 2014. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used partitioning around medoids to cluster samples into microbiota biotypes. We then used multivariable logistic regression to examine whether microbiota biotypes were associated with pneumonia and upper respiratory infection symptoms. Results: Mean ages of children with pneumonia, children with upper respiratory infection symptoms and healthy children were 8.2, 11.4 and 8.0 months, respectively. Clustering of nasopharyngeal microbiota identified 5 distinct biotypes: Corynebacterium/Dolosigranulum-dominant (23%), Haemophilus-dominant (11%), Moraxella-dominant (24%), Staphylococcus-dominant (13%) and Streptococcus-dominant (28%). The Haemophilus-dominant [odds ratio (OR): 13.55; 95% confidence interval (CI): 2.10-87.26], the Staphylococcus-dominant (OR: 8.27; 95% CI: 2.13-32.14) and the Streptococcus-dominant (OR: 39.97; 95% CI: 6.63-241.00) biotypes were associated with pneumonia. The Moraxella-dominant (OR: 3.71; 95% CI: 1.09-12.64) and Streptococcus-dominant (OR: 12.26; 95% CI: 1.81-83.06) biotypes were associated with upper respiratory infection symptoms. In children with pneumonia, HIV infection was associated with a lower relative abundance of Dolosigranulum (P = 0.03). Conclusions: Pneumonia and upper respiratory infection symptoms are associated with distinct nasopharyngeal microbiota biotypes in African children. A lower abundance of the commensal genus Dolosigranulum may contribute to the higher pneumonia risk of HIV-infected children.

AB - Background: Nearly half of child pneumonia deaths occur in sub-Saharan Africa. Microbial communities in the nasopharynx are a reservoir for pneumonia pathogens and remain poorly described in African children. Methods: Nasopharyngeal swabs were collected from children with pneumonia (N = 204), children with upper respiratory infection symptoms (N = 55) and healthy children (N = 60) in Botswana between April 2012 and April 2014. We sequenced the V3 region of the bacterial 16S ribosomal RNA gene and used partitioning around medoids to cluster samples into microbiota biotypes. We then used multivariable logistic regression to examine whether microbiota biotypes were associated with pneumonia and upper respiratory infection symptoms. Results: Mean ages of children with pneumonia, children with upper respiratory infection symptoms and healthy children were 8.2, 11.4 and 8.0 months, respectively. Clustering of nasopharyngeal microbiota identified 5 distinct biotypes: Corynebacterium/Dolosigranulum-dominant (23%), Haemophilus-dominant (11%), Moraxella-dominant (24%), Staphylococcus-dominant (13%) and Streptococcus-dominant (28%). The Haemophilus-dominant [odds ratio (OR): 13.55; 95% confidence interval (CI): 2.10-87.26], the Staphylococcus-dominant (OR: 8.27; 95% CI: 2.13-32.14) and the Streptococcus-dominant (OR: 39.97; 95% CI: 6.63-241.00) biotypes were associated with pneumonia. The Moraxella-dominant (OR: 3.71; 95% CI: 1.09-12.64) and Streptococcus-dominant (OR: 12.26; 95% CI: 1.81-83.06) biotypes were associated with upper respiratory infection symptoms. In children with pneumonia, HIV infection was associated with a lower relative abundance of Dolosigranulum (P = 0.03). Conclusions: Pneumonia and upper respiratory infection symptoms are associated with distinct nasopharyngeal microbiota biotypes in African children. A lower abundance of the commensal genus Dolosigranulum may contribute to the higher pneumonia risk of HIV-infected children.

KW - children

KW - microbial communities

KW - microbiota

KW - pneumonia

KW - respiratory infections

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