Associations between environmental characteristics, high-resolution indoor microbiome, metabolome and allergic and non-allergic rhinitis symptoms for junior high school students

Xi Fu; Bingqian Du; Yi Meng; Yanling Li; Xunhua Zhu; Zheyuan Ou; Mei Zhang; Huarong Wen; Aminnuddin Ma'pol; Jamal Hisham Hashim; Zailina Hashim; Gunilla Wieslander; Qingmei Chen; Jun Jiang; Juan Wang; Dan Norbäck; Yun Xia; Qingsong Chen; Yu Sun

doi:10.1039/D2EM00480A

Associations between environmental characteristics, high-resolution indoor microbiome, metabolome and allergic and non-allergic rhinitis symptoms for junior high school students†

Xi Fu,‡*^a Bingqian Du,‡^a Yi Meng,^bcd Yanling Li,^bcd Xunhua Zhu,^bcd Zheyuan Ou,^bcd Mei Zhang,^bcd Huarong Wen,^e Aminnuddin Ma'pol,^f Jamal Hisham Hashim,^g Zailina Hashim,^h Gunilla Wieslander,ⁱ Qingmei Chen,^bcd Jun Jiang,^bcd Juan Wang,ⁱ Dan Norbäck,ⁱ Yun Xia,^a Qingsong Chen^a and Yu Sun

*^bcd

Author affiliations

* Corresponding authors

^a Guangdong Provincial Engineering Research Center of Public Health Detection and Assessment, School of Public Health, Guangdong Pharmaceutical University, Guangzhou, PR China
E-mail: fuxi@gdpu.edu.cn

^b Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou, Guangdong, PR China
E-mail: sunyu@scau.edu.cn

^c Key Laboratory of Zoonosis of Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou, Guangdong, PR China

^d Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, Guangdong, China

^e Baling Health Center, Dangyang, Hubei, PR China

^f Gombak District Health Office, Ministry of Health, Batu Caves, Selangor Darul Ehsan, Malaysia

^g Universiti Selangor, Shah Alam, Malaysia

^h Department of Environmental and Occupational Health, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, UPM, Serdang, Selangor, Malaysia

ⁱ Occupational and Environmental Medicine, Department of Medical Science, University Hospital, Uppsala University, 75237 Uppsala, Sweden

Abstract

Rhinitis is one of the most prevalent chronic diseases globally. Microbiome exposure affects the occurrence of rhinitis. However, previous studies did not differentiate allergic rhinitis (AR) and non-allergic rhinitis (NAR) in the microbial association analysis. In this study, we investigate 347 students in 8 junior high schools, Terengganu, Malaysia, who were categorized as healthy (70.9%), AR (13.8%) and NAR (15.3%) based on a self-administered questionnaire and skin prick tests of pollen, pet, mould and house dust mite allergens. Classroom microbial and metabolite exposure in vacuumed dust was characterized by PacBio long-read amplicon sequencing, quantitative PCR and LC-MS-based untargeted metabolomics. Our findings indicate a similar microbial association pattern between AR and NAR. The richness in Gammaproteobacteria was negatively associated with AR and NAR symptoms, whereas total fungal richness was positively associated with AR and NAR symptoms (p < 0.05). Brasilonema bromeliae and Aeromonas enteropelogenes were negatively associated with AR and NAR, and Deinococcus was positively associated with AR and NAR (p < 0.01). Pipecolic acid was protectively associated with AR and NAR symptoms (OR = 0.06 and 0.13, p = 0.009 and 0.045). A neural network analysis showed that B. bromeliae was co-occurring with pipecolic acid, suggesting that the protective role of this species may be mediated by releasing pipecolic acid. Indoor relative humidity and the weight of vacuum dust were associated with AR and NAR, respectively (p < 0.05), but the health effects were mediated by two protective bacterial species, Aliinostoc morphoplasticum and Ilumatobacter fluminis. Overall, our study reported a similar microbial association pattern between AR and NAR and also revealed the complex interactions between microbial species, environmental characteristics, and rhinitis symptoms.

This article is part of the themed collection: Environmental exposure and impacts

Environmental Science: Processes & Impacts

Associations between environmental characteristics, high-resolution indoor microbiome, metabolome and allergic and non-allergic rhinitis symptoms for junior high school students†

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Associations between environmental characteristics, high-resolution indoor microbiome, metabolome and allergic and non-allergic rhinitis symptoms for junior high school students

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