The Respiratory Tract Microbiome and Its Relationship to Lung Cancer and Environmental Exposures Found in Rural China

Howard D. Hosgood, Emmanuel F. Mongodin, Yunhu Wan, Xing Hua, Nathaniel Rothman, Wei Hu, Roel Vermeulen, Wei Jie Seow, Thomas E. Rohan, Jun Xu, Jihua Li, Jun He, Yunchao Huang, Kaiyun Yang, Guoping Wu, Fusheng Wei, Jianxin Shi, Amy R. Sapkota, Qing Lan

Research output: Contribution to journalArticle

Abstract

We previously reported that bacterial diversity in sputum samples from never-smoking women in rural China varied by lung cancer status and household air pollution (HAP) exposure type. Here, we expand on our associations between environmental exposures and respiratory tract microbiota with an additional 90 never-smoking women from Xuanwei, China. DNA from sputum samples of cases (n = 45) and controls (n = 45) was extracted using a multistep enzymatic and physical lysis, followed by a standardized clean up. V1–V2 regions of 16S rRNA genes were Polymerase chain reaction (PCR) amplified. Purified amplicons were sequenced by 454 FLX Titanium pyrosequencing and high-quality sequences were evaluated for diversity and taxonomic membership. In our population of never-smokers, increased risk of lung cancer was associated with lower alpha diversity compared to higher alpha diversity (Shannon: OR high = 1.00 [reference], OR medium = 3.84 [1.02–14.48], OR low = 3.78 [1.03–13.82]; observed species: OR high = 1.00 [reference], OR medium = 2.37 [0.67–8.48], OR low = 2.01 [0.58–6.97]; Phylogenetic Diversity (PD) whole tree: OR high = 1.00 [reference], OR medium = 3.04 [0.85–10.92], OR low = 2.53 [0.72–8.96]), as well as a decreased relative abundance of Fusobacteria (OR high = 1.00 [reference], OR medium = 1.24 [0.42–3.66], OR low = 2.01 [0.63–6.44], p trend = 0.03). Increasing alpha diversity was associated with smoky coal use compared to clean fuel use among all subjects (observed species, P = 0.001; PD whole tree, P = 0.006; Shannon, P = 0.0002), as well as cases (observed species, P = 0.02; PD whole tree, P = 0.03; Shannon, P = 0.03) and controls (observed species, P = 0.01; PD whole tree, P = 0.05; Shannon, P = 0.002). Increased diversity was also associated with presence of livestock (observed species, P = 0.02; PD whole tree, P = 0.02; Shannon, P = 0.03) in the home for cases. Our study is the first to report that decreased microbial diversity is associated with risk of lung cancer. Larger studies are necessary to elucidate the direct and indirect effects attributed to the disease-specific, HAP-specific, and animal-specific associations. Environ. Mol. Mutagen. 2019.

Original languageEnglish (US)
JournalEnvironmental and Molecular Mutagenesis
DOIs
StatePublished - Jan 1 2019

Fingerprint

Microbiota
Environmental Exposure
Respiratory System
China
Lung Neoplasms
Air Pollution
Sputum
Fusobacteria
Smoking
Coal
Mutagens
Livestock
Titanium
rRNA Genes
Polymerase Chain Reaction
DNA
Population

Keywords

  • animal contact
  • bacteria
  • cancer
  • coal
  • farm
  • lung
  • pulmonary

ASJC Scopus subject areas

  • Epidemiology
  • Genetics(clinical)
  • Health, Toxicology and Mutagenesis

Cite this

The Respiratory Tract Microbiome and Its Relationship to Lung Cancer and Environmental Exposures Found in Rural China. / Hosgood, Howard D.; Mongodin, Emmanuel F.; Wan, Yunhu; Hua, Xing; Rothman, Nathaniel; Hu, Wei; Vermeulen, Roel; Seow, Wei Jie; Rohan, Thomas E.; Xu, Jun; Li, Jihua; He, Jun; Huang, Yunchao; Yang, Kaiyun; Wu, Guoping; Wei, Fusheng; Shi, Jianxin; Sapkota, Amy R.; Lan, Qing.

In: Environmental and Molecular Mutagenesis, 01.01.2019.

Research output: Contribution to journalArticle

Hosgood, HD, Mongodin, EF, Wan, Y, Hua, X, Rothman, N, Hu, W, Vermeulen, R, Seow, WJ, Rohan, TE, Xu, J, Li, J, He, J, Huang, Y, Yang, K, Wu, G, Wei, F, Shi, J, Sapkota, AR & Lan, Q 2019, 'The Respiratory Tract Microbiome and Its Relationship to Lung Cancer and Environmental Exposures Found in Rural China', Environmental and Molecular Mutagenesis. https://doi.org/10.1002/em.22291
Hosgood, Howard D. ; Mongodin, Emmanuel F. ; Wan, Yunhu ; Hua, Xing ; Rothman, Nathaniel ; Hu, Wei ; Vermeulen, Roel ; Seow, Wei Jie ; Rohan, Thomas E. ; Xu, Jun ; Li, Jihua ; He, Jun ; Huang, Yunchao ; Yang, Kaiyun ; Wu, Guoping ; Wei, Fusheng ; Shi, Jianxin ; Sapkota, Amy R. ; Lan, Qing. / The Respiratory Tract Microbiome and Its Relationship to Lung Cancer and Environmental Exposures Found in Rural China. In: Environmental and Molecular Mutagenesis. 2019.
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AU - Mongodin, Emmanuel F.

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AU - Hua, Xing

AU - Rothman, Nathaniel

AU - Hu, Wei

AU - Vermeulen, Roel

AU - Seow, Wei Jie

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AU - He, Jun

AU - Huang, Yunchao

AU - Yang, Kaiyun

AU - Wu, Guoping

AU - Wei, Fusheng

AU - Shi, Jianxin

AU - Sapkota, Amy R.

AU - Lan, Qing

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N2 - We previously reported that bacterial diversity in sputum samples from never-smoking women in rural China varied by lung cancer status and household air pollution (HAP) exposure type. Here, we expand on our associations between environmental exposures and respiratory tract microbiota with an additional 90 never-smoking women from Xuanwei, China. DNA from sputum samples of cases (n = 45) and controls (n = 45) was extracted using a multistep enzymatic and physical lysis, followed by a standardized clean up. V1–V2 regions of 16S rRNA genes were Polymerase chain reaction (PCR) amplified. Purified amplicons were sequenced by 454 FLX Titanium pyrosequencing and high-quality sequences were evaluated for diversity and taxonomic membership. In our population of never-smokers, increased risk of lung cancer was associated with lower alpha diversity compared to higher alpha diversity (Shannon: OR high = 1.00 [reference], OR medium = 3.84 [1.02–14.48], OR low = 3.78 [1.03–13.82]; observed species: OR high = 1.00 [reference], OR medium = 2.37 [0.67–8.48], OR low = 2.01 [0.58–6.97]; Phylogenetic Diversity (PD) whole tree: OR high = 1.00 [reference], OR medium = 3.04 [0.85–10.92], OR low = 2.53 [0.72–8.96]), as well as a decreased relative abundance of Fusobacteria (OR high = 1.00 [reference], OR medium = 1.24 [0.42–3.66], OR low = 2.01 [0.63–6.44], p trend = 0.03). Increasing alpha diversity was associated with smoky coal use compared to clean fuel use among all subjects (observed species, P = 0.001; PD whole tree, P = 0.006; Shannon, P = 0.0002), as well as cases (observed species, P = 0.02; PD whole tree, P = 0.03; Shannon, P = 0.03) and controls (observed species, P = 0.01; PD whole tree, P = 0.05; Shannon, P = 0.002). Increased diversity was also associated with presence of livestock (observed species, P = 0.02; PD whole tree, P = 0.02; Shannon, P = 0.03) in the home for cases. Our study is the first to report that decreased microbial diversity is associated with risk of lung cancer. Larger studies are necessary to elucidate the direct and indirect effects attributed to the disease-specific, HAP-specific, and animal-specific associations. Environ. Mol. Mutagen. 2019.

AB - We previously reported that bacterial diversity in sputum samples from never-smoking women in rural China varied by lung cancer status and household air pollution (HAP) exposure type. Here, we expand on our associations between environmental exposures and respiratory tract microbiota with an additional 90 never-smoking women from Xuanwei, China. DNA from sputum samples of cases (n = 45) and controls (n = 45) was extracted using a multistep enzymatic and physical lysis, followed by a standardized clean up. V1–V2 regions of 16S rRNA genes were Polymerase chain reaction (PCR) amplified. Purified amplicons were sequenced by 454 FLX Titanium pyrosequencing and high-quality sequences were evaluated for diversity and taxonomic membership. In our population of never-smokers, increased risk of lung cancer was associated with lower alpha diversity compared to higher alpha diversity (Shannon: OR high = 1.00 [reference], OR medium = 3.84 [1.02–14.48], OR low = 3.78 [1.03–13.82]; observed species: OR high = 1.00 [reference], OR medium = 2.37 [0.67–8.48], OR low = 2.01 [0.58–6.97]; Phylogenetic Diversity (PD) whole tree: OR high = 1.00 [reference], OR medium = 3.04 [0.85–10.92], OR low = 2.53 [0.72–8.96]), as well as a decreased relative abundance of Fusobacteria (OR high = 1.00 [reference], OR medium = 1.24 [0.42–3.66], OR low = 2.01 [0.63–6.44], p trend = 0.03). Increasing alpha diversity was associated with smoky coal use compared to clean fuel use among all subjects (observed species, P = 0.001; PD whole tree, P = 0.006; Shannon, P = 0.0002), as well as cases (observed species, P = 0.02; PD whole tree, P = 0.03; Shannon, P = 0.03) and controls (observed species, P = 0.01; PD whole tree, P = 0.05; Shannon, P = 0.002). Increased diversity was also associated with presence of livestock (observed species, P = 0.02; PD whole tree, P = 0.02; Shannon, P = 0.03) in the home for cases. Our study is the first to report that decreased microbial diversity is associated with risk of lung cancer. Larger studies are necessary to elucidate the direct and indirect effects attributed to the disease-specific, HAP-specific, and animal-specific associations. Environ. Mol. Mutagen. 2019.

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