Indoor metabolites and chemicals outperform microbiome in classifying childhood asthma and allergic rhinitis

Yu Sun; Hao Tang; Shuang Du; Yang Chen; Zheyuan Ou; Mei Zhang; Zhuoru Chen; Zhiwei Tang; Dongjun Zhang; Tianyi Chen; Yanyi Xu; Jiufeng Li; Dan Norback; Jamal Hisham Hashim; Zailina Hashim; Jie Shao; Xi Fu; Zhuohui Zhao

Eco-Environment & Health (Dec 2023)

Indoor metabolites and chemicals outperform microbiome in classifying childhood asthma and allergic rhinitis

Yu Sun,
Hao Tang,
Shuang Du,
Yang Chen,
Zheyuan Ou,
Mei Zhang,
Zhuoru Chen,
Zhiwei Tang,
Dongjun Zhang,
Tianyi Chen,
Yanyi Xu,
Jiufeng Li,
Dan Norback,
Jamal Hisham Hashim,
Zailina Hashim,
Jie Shao,
Xi Fu,
Zhuohui Zhao

Affiliations

Yu Sun: Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
Hao Tang: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Shuang Du: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Yang Chen: Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
Zheyuan Ou: Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
Mei Zhang: Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
Zhuoru Chen: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Zhiwei Tang: Department of Pediatrics, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Dongjun Zhang: Department of Pediatrics, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Tianyi Chen: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Yanyi Xu: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Jiufeng Li: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China
Dan Norback: Department of Medical Sciences, Uppsala University, Uppsala SE-751, Sweden
Jamal Hisham Hashim: Department of Environmental Health, Faculty of Health Sciences, Universiti Selangor, Shah Alam 40000, Malaysia
Zailina Hashim: Department of Environmental and Occupational Health, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, UPM, Serdang 43400, Malaysia
Jie Shao: Department of Pediatrics, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; Corresponding authors.
Xi Fu: Guangdong Provincial Engineering Research Center of Public Health Detection and Assessment, School of Public Health, Guangdong Pharmaceutical University, Guangzhou 510006, China; Corresponding authors.
Zhuohui Zhao: Department of Environmental Health, School of Public Health, Fudan University, NHC Key Laboratory of Health Technology Assessment (Fudan University), Shanghai 200032, China; Key Laboratory of Public Health Safety of the Ministry of Education, Shanghai Typhoon Institute/CMA, Shanghai Key Laboratory of Meteorology and Health, Shanghai 200030, China; IRDR International Center of Excellence on Risk Interconnectivity and Governance on Weather/Climate Extremes Impact and Public Health, Fudan University, Shanghai 200438, China; WMO/IGAC MAP-AQ Asian Office Shanghai, Fudan University, Shanghai 200438, China; Corresponding authors.

Journal volume & issue: Vol. 2, no. 4
pp. 208 – 218

Abstract

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Indoor microorganisms impact asthma and allergic rhinitis (AR), but the associated microbial taxa often vary extensively due to climate and geographical variations. To provide more consistent environmental assessments, new perspectives on microbial exposure for asthma and AR are needed. Home dust from 97 cases (32 asthma alone, 37 AR alone, 28 comorbidity) and 52 age- and gender-matched controls in Shanghai, China, were analyzed using high-throughput shotgun metagenomic sequencing and liquid chromatography-mass spectrometry. Homes of healthy children were enriched with environmental microbes, including Paracoccus, Pseudomonas, and Psychrobacter, and metabolites like keto acids, indoles, pyridines, and flavonoids (astragalin, hesperidin) (False Discovery Rate < 0.05). A neural network co-occurrence probability analysis revealed that environmental microorganisms were involved in producing these keto acids, indoles, and pyridines. Conversely, homes of diseased children were enriched with mycotoxins and synthetic chemicals, including herbicides, insecticides, and food/cosmetic additives. Using a random forest model, characteristic metabolites and microorganisms in Shanghai homes were used to classify high and low prevalence of asthma/AR in an independent dataset in Malaysian schools (N = 1290). Indoor metabolites achieved an average accuracy of 74.9% and 77.1% in differentiating schools with high and low prevalence of asthma and AR, respectively, whereas indoor microorganisms only achieved 51.0% and 59.5%, respectively. These results suggest that indoor metabolites and chemicals rather than indoor microbiome are potentially superior environmental indicators for childhood asthma and AR. This study extends the traditional risk assessment focusing on allergens or air pollutants in childhood asthma and AR, thereby revealing potential novel intervention strategies for these diseases.

Published in Eco-Environment & Health

ISSN: 2772-9850 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General): Ecology; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.sciencedirect.com/journal/eco-environment-and-health

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