Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan

Mari Lee Odendaal; Wouter A.A. de Steenhuijsen Piters; Eelco Franz; Mei Ling J.N. Chu; James A. Groot; Elske M. van Logchem; Raiza Hasrat; Sjoerd Kuiling; Roan Pijnacker; Rob Mariman; Krzysztof Trzciński; Fiona R.M. van der Klis; Elisabeth A.M. Sanders; Lidwien A.M. Smit; Debby Bogaert; Thijs Bosch

doi:10.1016/j.cell.2024.07.008

Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan

Mari Lee Odendaal, Wouter A.A. de Steenhuijsen Piters, Eelco Franz, Mei Ling J.N. Chu, James A. Groot, Elske M. van Logchem, Raiza Hasrat, Sjoerd Kuiling, Roan Pijnacker, Rob Mariman, Krzysztof Trzciński, Fiona R.M. van der Klis, Elisabeth A.M. Sanders, Lidwien A.M. Smit, Debby Bogaert^*, Thijs Bosch^*

^*Corresponding author for this work

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Abstract

Our understanding of the normal variation in the upper respiratory tract (URT) microbiota across the human lifespan and how these relate to host, environment, and health is limited. We studied the microbiota of 3,104 saliva (<10 year-olds)/oropharynx (≥10 year-olds) and 2,485 nasopharynx samples of 3,160 Dutch individuals 0–87 years of age, participating in a cross-sectional population-wide study (PIENTER-3) using 16S-rRNA sequencing. The microbiota composition was strongly related to age, especially in the nasopharynx, with maturation occurring throughout childhood and adolescence. Clear niche- and age-specific associations were found between the microbiota composition and host/environmental factors and health outcomes. Among others, social interaction, sex, and season were associated with the nasopharyngeal microbial community. By contrast, the oral microbiota was more related to antibiotics, tobacco, and alcohol use. We present an atlas of the URT microbiota across the lifespan in association with environment and health, establishing a baseline for future research.

Original language	English
Pages (from-to)	4571-4585.e15
Journal	Cell
Volume	187
Issue number	17
DOIs	https://doi.org/10.1016/j.cell.2024.07.008
Publication status	Published - 22 Aug 2024

Keywords

16S-rRNA sequencing
environment
exposure
health outcomes
host
human lifespan
microbiome
microbiota
population-wide
upper respiratory tract

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10.1016/j.cell.2024.07.008Licence: CC BY-NC-ND

1-s2.0-S0092867424007682-mainFinal published version, 8 MBLicence: CC BY-NC-ND

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Odendaal, M. L., de Steenhuijsen Piters, W. A. A., Franz, E., Chu, M. L. J. N., Groot, J. A., van Logchem, E. M., Hasrat, R., Kuiling, S., Pijnacker, R., Mariman, R., Trzciński, K., van der Klis, F. R. M., Sanders, E. A. M., Smit, L. A. M., Bogaert, D., & Bosch, T. (2024). Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan. Cell, 187(17), 4571-4585.e15. https://doi.org/10.1016/j.cell.2024.07.008

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title = "Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan",

abstract = "Our understanding of the normal variation in the upper respiratory tract (URT) microbiota across the human lifespan and how these relate to host, environment, and health is limited. We studied the microbiota of 3,104 saliva (<10 year-olds)/oropharynx (≥10 year-olds) and 2,485 nasopharynx samples of 3,160 Dutch individuals 0–87 years of age, participating in a cross-sectional population-wide study (PIENTER-3) using 16S-rRNA sequencing. The microbiota composition was strongly related to age, especially in the nasopharynx, with maturation occurring throughout childhood and adolescence. Clear niche- and age-specific associations were found between the microbiota composition and host/environmental factors and health outcomes. Among others, social interaction, sex, and season were associated with the nasopharyngeal microbial community. By contrast, the oral microbiota was more related to antibiotics, tobacco, and alcohol use. We present an atlas of the URT microbiota across the lifespan in association with environment and health, establishing a baseline for future research.",

keywords = "16S-rRNA sequencing, environment, exposure, health outcomes, host, human lifespan, microbiome, microbiota, population-wide, upper respiratory tract",

author = "Odendaal, {Mari Lee} and {de Steenhuijsen Piters}, {Wouter A.A.} and Eelco Franz and Chu, {Mei Ling J.N.} and Groot, {James A.} and {van Logchem}, {Elske M.} and Raiza Hasrat and Sjoerd Kuiling and Roan Pijnacker and Rob Mariman and Krzysztof Trzci{\'n}ski and {van der Klis}, {Fiona R.M.} and Sanders, {Elisabeth A.M.} and Smit, {Lidwien A.M.} and Debby Bogaert and Thijs Bosch",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors",

year = "2024",

month = aug,

day = "22",

doi = "10.1016/j.cell.2024.07.008",

language = "English",

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Odendaal, ML, de Steenhuijsen Piters, WAA, Franz, E, Chu, MLJN, Groot, JA, van Logchem, EM, Hasrat, R, Kuiling, S, Pijnacker, R, Mariman, R, Trzciński, K, van der Klis, FRM, Sanders, EAM, Smit, LAM, Bogaert, D & Bosch, T 2024, 'Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan', Cell, vol. 187, no. 17, pp. 4571-4585.e15. https://doi.org/10.1016/j.cell.2024.07.008

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T1 - Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan

AU - Odendaal, Mari Lee

AU - de Steenhuijsen Piters, Wouter A.A.

AU - Franz, Eelco

AU - Chu, Mei Ling J.N.

AU - Groot, James A.

AU - van Logchem, Elske M.

AU - Hasrat, Raiza

AU - Kuiling, Sjoerd

AU - Pijnacker, Roan

AU - Mariman, Rob

AU - Trzciński, Krzysztof

AU - van der Klis, Fiona R.M.

AU - Sanders, Elisabeth A.M.

AU - Smit, Lidwien A.M.

AU - Bogaert, Debby

AU - Bosch, Thijs

PY - 2024/8/22

Y1 - 2024/8/22

N2 - Our understanding of the normal variation in the upper respiratory tract (URT) microbiota across the human lifespan and how these relate to host, environment, and health is limited. We studied the microbiota of 3,104 saliva (<10 year-olds)/oropharynx (≥10 year-olds) and 2,485 nasopharynx samples of 3,160 Dutch individuals 0–87 years of age, participating in a cross-sectional population-wide study (PIENTER-3) using 16S-rRNA sequencing. The microbiota composition was strongly related to age, especially in the nasopharynx, with maturation occurring throughout childhood and adolescence. Clear niche- and age-specific associations were found between the microbiota composition and host/environmental factors and health outcomes. Among others, social interaction, sex, and season were associated with the nasopharyngeal microbial community. By contrast, the oral microbiota was more related to antibiotics, tobacco, and alcohol use. We present an atlas of the URT microbiota across the lifespan in association with environment and health, establishing a baseline for future research.

AB - Our understanding of the normal variation in the upper respiratory tract (URT) microbiota across the human lifespan and how these relate to host, environment, and health is limited. We studied the microbiota of 3,104 saliva (<10 year-olds)/oropharynx (≥10 year-olds) and 2,485 nasopharynx samples of 3,160 Dutch individuals 0–87 years of age, participating in a cross-sectional population-wide study (PIENTER-3) using 16S-rRNA sequencing. The microbiota composition was strongly related to age, especially in the nasopharynx, with maturation occurring throughout childhood and adolescence. Clear niche- and age-specific associations were found between the microbiota composition and host/environmental factors and health outcomes. Among others, social interaction, sex, and season were associated with the nasopharyngeal microbial community. By contrast, the oral microbiota was more related to antibiotics, tobacco, and alcohol use. We present an atlas of the URT microbiota across the lifespan in association with environment and health, establishing a baseline for future research.

KW - 16S-rRNA sequencing

KW - environment

KW - exposure

KW - health outcomes

KW - host

KW - human lifespan

KW - microbiome

KW - microbiota

KW - population-wide

KW - upper respiratory tract

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U2 - 10.1016/j.cell.2024.07.008

DO - 10.1016/j.cell.2024.07.008

M3 - Article

C2 - 39094567

AN - SCOPUS:85201703720

SN - 0092-8674

VL - 187

SP - 4571-4585.e15

JO - Cell

JF - Cell

IS - 17

ER -

Host and environmental factors shape upper airway microbiota and respiratory health across the human lifespan

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Keywords

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