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

doi:10.1097/INF.0000000000001607

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

Pediatrics

Research output: Contribution to journal › Article › peer-review

39 Scopus citations

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 language	English (US)
Pages (from-to)	e211-e218
Journal	Pediatric Infectious Disease Journal
Volume	36
Issue number	9
DOIs	https://doi.org/10.1097/INF.0000000000001607
State	Published - Sep 1 2017

Funding

This research was supported by an Early Career Award from the Thrasher Research Fund (to M.S.K.), by Children's Hospital of Philadelphia (to A.P.S., K.A.F.) and Pincus Family Foundation, and through core services from the Penn Center for AIDS Research, a National Institutes of Health (NIH)-funded program (P30-AI045008). M.S.K. and C.K.C. received financial support from the NIH through the Duke Center for AIDS Research (P30-AI064518). M.S.K. was supported by NIH T32 training grants (5T32-HD060558-04, 5T32-HD043029-13). J.M.P. was supported by a Hamilton Health Sciences Early Career Award. This research was supported by an Early Career Award from the Thrasher Research Fund (to M.S.K.), by Children’s Hospital of Philadelphia (to A.P.S., K.A.F.) and Pincus Family Foundation, and through core services from the Penn Center for AIDS Research, a National Institutes of Health (NIH)-funded program (P30-AI045008). Funding for this project was also made possible in part by a CIPHER grant (to M.S.K.) from the International AIDS Society, supported by ViiV Healthcare. M.S.K. and C.K.C. received financial support from the NIH through the Duke Center for AIDS Research (P30-AI064518). M.S.K. was supported by NIH T32 training grants (5T32-HD060558-04, 5T32-HD043029-13). J.M.P. was supported by a Hamilton Health Sciences Early Career Award. The other authors have no conflicts of interest to disclose.

Keywords

children
microbial communities
microbiota
pneumonia
respiratory infections

ASJC Scopus subject areas

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

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1097/INF.0000000000001607

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Kelly, M. S., Surette, M. G., Smieja, M., Pernica, J. M., Rossi, L., Luinstra, K., Steenhoff, A. P., Feemster, K. A., Goldfarb, D. M., Arscott-Mills, T., Boiditswe, S., Rulaganyang, I., Muthoga, C., Gaofiwe, L., Mazhani, T., Rawls, J. F., Cunningham, C. K., Shah, S. S., & Seed, P. C. (2017). The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana. Pediatric Infectious Disease Journal, 36(9), e211-e218. https://doi.org/10.1097/INF.0000000000001607

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title = "The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana",

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.",

keywords = "children, microbial communities, microbiota, pneumonia, respiratory infections",

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.}",

note = "Publisher Copyright: {\textcopyright} 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.",

year = "2017",

month = sep,

day = "1",

doi = "10.1097/INF.0000000000001607",

language = "English (US)",

volume = "36",

pages = "e211--e218",

journal = "Pediatric Infectious Disease Journal",

issn = "0891-3668",

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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

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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U2 - 10.1097/INF.0000000000001607

DO - 10.1097/INF.0000000000001607

M3 - Article

C2 - 28399056

AN - SCOPUS:85017460730

SN - 0891-3668

VL - 36

SP - e211-e218

JO - Pediatric Infectious Disease Journal

JF - Pediatric Infectious Disease Journal

IS - 9

ER -

The Nasopharyngeal Microbiota of Children with Respiratory Infections in Botswana

Abstract

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

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