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

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

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
Number of pages	30
Journal	Cell
Volume	187
Issue number	17
Early online date	1 Aug 2024
DOIs	https://doi.org/10.1016/j.cell.2024.07.008
Publication status	Published - 22 Aug 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors

Funding

This work was executed with the National Institute for Public Health and the Environment (RIVM) strategic project TRIuMPH. The serosurveys in the Netherlands (PIENTER-3) and in the Caribbean Netherlands (HSCN) were conducted by the RIVM, in close collaboration with the local Public Health Services (GGD) and Statistics Netherlands (CBS). Our gratitude extends to all the volunteers who took part in this study. This work was supported in part by the Netherlands Organization for Scientific Research (NWO-VIDI; grant number 91715359, recipient: D.B.) and the Chief Scientist Office/NHS Research Scotland Scottish Senior Clinical Fellowship award (SCAF/16/03, recipient: D.B.). M.-L.O. pre-processed, analyzed, and visualized the data. M.-L.O. W.A.A.d.S.P. E.F. R.P. L.A.M.S. R.M. K.T. and D.B. assisted in the statistical analyses and interpretation of the results and were responsible for the writing of the original draft. E.F. F.R.M.v.d.K. E.A.M.S. D.B. and T.B. were responsible for conceptualizing the study and acquiring funding. M.L.J.N.C. J.A.G. E.M.v.L. R.H. S.K. and R.M. were responsible for the execution and quality control of the laboratory work. All authors contributed to interpretation of the results, critically revised the manuscript for important intellectual content, and approved the final manuscript. The authors declare no competing interests. This work was executed with the National Institute for Public Health and the Environment (RIVM) strategic project TRIuMPH. The serosurveys in the Netherlands (PIENTER-3) and in the Caribbean Netherlands (HSCN) were conducted by the RIVM, in close collaboration with the local Public Health Services (GGD) and Statistics Netherlands (CBS). Our gratitude extends to all the volunteers who took part in this study. This work was supported in part by the Netherlands Organization for Scientific Research (NWO-VIDI; grant number 91715359 , recipient: D.B.) and the Chief Scientist Office/NHS Research Scotland Scottish Senior Clinical Fellowship award ( SCAF/16/03 , recipient: D.B.).

Funders	Funder number
National Institute for Public Health and the Environment
Chief Scientist Office
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	91715359
NHS Research Scotland Scottish	SCAF/16/03
Rijksinstituut voor Volksgezondheid en Milieu	PIENTER-3

Keywords

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

UN SDGs

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

Access to Document

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

PIIS0092867424007682Final published version, 8 MBLicence: CC BY-NC-ND

Cite this

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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Odendaal, M-L, 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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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

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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.

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KW - exposure

KW - health outcomes

KW - host

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KW - microbiome

KW - microbiota

KW - population-wide

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SN - 0092-8674

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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

Abstract

Bibliographical note

Funding

Keywords

UN SDGs

Access to Document

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Cite this