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Indoor Microbiome, Environmental Characteristics and Asthma Among Junior High School Students in Johor Bahru, Malaysia T Environment International 138 (2020) 105664 Contents lists available at ScienceDirect Environment International journal homepage: www.elsevier.com/locate/envint Indoor microbiome, environmental characteristics and asthma among junior high school students in Johor Bahru, Malaysia T Xi Fua,b, Dan Norbäckc, Qianqian Yuanb,d,e, Yanling Lib,d,e, Xunhua Zhub,d,e, Jamal Hisham Hashimf,g, Zailina Hashimh, Faridah Alii, Yi-Wu Zhengj, Xu-Xin Laij, ⁎ Michael Dho Spangfortj, Yiqun Dengb,d,e, Yu Sunb,d,e, a Department of Occupational and Environmental Health, School of Public Health, Sun Yat-sen University, Guangzhou, PR China b Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou, Guangdong 510642, PR China c Occupational and Environmental Medicine, Dept. of Medical Science, University Hospital, Uppsala University, 75237 Uppsala, Sweden d Key Laboratory of Zoonosis of Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou, Guangdong 510642, PR China e Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, Guangdong 510642, China f United Nations University-International Institute for Global Health, Kuala Lumpur, Malaysia g Department of Community Health, National University of Malaysia, Kuala Lumpur, Malaysia h Department of Environmental and Occupational Health, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, UPM, Serdang, Selangor, Malaysia i Primary Care Unit, Johor State Health Department, Johor Bahru, Malaysia j Asia Pacific Research, ALK-Abello A/S, Guangzhou, China ARTICLE INFO ABSTRACT Handling editor: Da Chen Indoor microbial diversity and composition are suggested to affect the prevalence and severity of asthma by Keywords: previous home microbiome studies, but no microbiome-health association study has been conducted in a school Bacteria environment, especially in tropical countries. In this study, we collected floor dust and environmental char- Fungi acteristics from 21 classrooms, and health data related to asthma symptoms from 309 students, in junior high Microbial community schools in Johor Bahru, Malaysia. The bacterial and fungal composition was characterized by sequencing 16s Absolute quantity rRNA gene and internal transcribed spacer (ITS) region, and the absolute microbial concentration was quantified Wheezing by qPCR. In total, 326 bacterial and 255 fungal genera were characterized. Five bacterial (Sphingobium, Breathlessness Rhodomicrobium, Shimwellia, Solirubrobacter, Pleurocapsa) and two fungal (Torulaspora and Leptosphaeriaceae) Adolescence taxa were protective for asthma severity. Two bacterial taxa, Izhakiella and Robinsoniella, were positively as- Dampness/visible mold Malaysia sociated with asthma severity. Several protective bacterial taxa including Rhodomicrobium, Shimwellia and Johor Bahru Sphingobium have been reported as protective microbes in previous studies, whereas other taxa were first time Tropics reported. Environmental characteristics, such as age of building, size of textile curtain per room volume, oc- Junior high school currence of cockroaches, concentration of house dust mite allergens transferred from homes by the occupants, were involved in shaping the overall microbial community but not asthma-associated taxa; whereas visible dampness and mold, which did not change the overall microbial community for floor dust, was negatively associated with the concentration of protective bacteria Rhodomicrobium (β = −2.86, p = 0.021) of asthma. The result indicates complex interactions between microbes, environmental characteristics and asthma symp- toms. Overall, this is the first indoor microbiome study to characterize the asthma-associated microbes and their environmental determinant in the tropical area, promoting the understanding of microbial exposure and re- spiratory health in this region. 1. Introduction characteristics have been suggested to be associated with asthma pre- valence and severity, including parental asthma, preterm delivery and Asthma prevalence has been rising globally in the past few decades low birth weight, tobacco smoking, respiratory syncytial virus infec- (Eder et al., 2006). Many personal and environmental and tion, exposure to air/traffic pollution and indoor mold (de Benedictis ⁎ Corresponding author at: Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou, Guangdong 510642, PR China. E-mail address: [email protected] (Y. Sun). https://doi.org/10.1016/j.envint.2020.105664 Received 11 December 2019; Received in revised form 12 March 2020; Accepted 12 March 2020 Available online 19 March 2020 0160-4120/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). X. Fu, et al. Environment International 138 (2020) 105664 and Bush, 2017; Castro-Rodriguez et al., 2016). However, many of sequencing, and thus only dust samples of 21 classes could be se- these risk factors fail to explain the increasing trend of asthma epi- quenced. The numbers of success and failed samples in each school demics. For example, smoking is a strong risk factor for asthma, but the were listed in Table S1. Health data were collected by self-reported prevalence of smoking is significantly reduced in the past thirty years questionnaires from 15 randomly selected students in each class. The (Ng et al., 2014). Recent studies suggested that the changing of lifestyle ethical permission was approved by the Medical Research and Ethics and microbial exposure during the industrialization and urbanization Committee of the National University of Malaysia, and all participants process are associated with the increasing prevalence of asthma gave their informed consent. symptoms (Bello et al., 2018). Nowadays, more people live in the city than the rural area, and they spend most of the time in the indoor 2.1. Assessment of health data environment (Klepeis et al., 2001), thus it is necessary to identify the beneficial and risk exposure in various indoor environments. Progress Questions about doctor-diagnosed asthma and current asthma were in culture-independent microbiome studies reveals the association be- obtained from the European Community Respiratory Health Study tween indoor microbial exposure and human respiratory health in the (ECRHS). The questions included asthma symptoms and related in- home environment. It was reported that high bacterial richness in formation during last 12 months, including wheeze, breathlessness homes of the traditional farm area protected against childhood asthma during wheeze, feeling of chest tightness, shortness of breath during compared with urban families (Ege et al., 2011). Similarly, a high di- rest, shortness of breath during exercise, woken by attack of shortness versity of fungal exposure is protective for childhood asthma develop- of breath, ever had asthma, attack of asthma, and current asthma ment (Dannemiller et al., 2014). There are also studies suggest that the medication use. asthma prevalence is related to the abundance of specific taxa rather A validated asthma score, including eight items, were calculated to than microbial richness (Kirjavainen et al., 2019). For example, two measure asthma severity (Pekkanen et al., 2005) were calculated, and microbiome studies used absolute quantification approaches identified then re-defined as 0, 1, 2, > =3. Questions about current smoking and only one protective or risk microbe for asthma symptoms (Pekkanen parental asthma/allergy were also included. Details about the questions et al., 2018; Dannemiller et al., 2016), and one study in the United were described in a previous study (Norback et al., 2014). States using relative abundance from 16s rRNA identified a few hun- dreds of potentially associated microbes for inner-city children 2.2. Dust sampling and building inspection (O'Connor et al., 2018). Thus, although there are still some dis- crepancies among studies, the association between indoor microbial The detailed dust sampling procedure was reported in a previous exposure and asthma development in the home environment is gen- publication (Norback et al., 2014). Floor dust in the classroom was erally established. collected by a 400 W vacuum cleaner with a dust sampler (ALK Abello, In contrast to the extensive researches in the private home en- Copenhagen, Denmark) through a Millipore filter (pore size 6 µm). The vironment, no study has been conducted in public indoor environments, filter is made of cellulose acetate, which retains 74% of particles of such as schools. Thus, the health effect of microbial assemblage in these 0.3–0.5 mm, 81% of particles of 0.5–1.0 mm, 95% of particles of indoor areas is unclear. Also, these microbiome studies in the home 1–10 mm and 100% of larger particles (> 10 mm). Three dust samples environment are mainly focused on childhood asthma (Ege et al., 2011; were collected at the same time for each classroom. The total vacuum Dannemiller et al., 2014; O'Connor et al., 2018), and the health effect of sampling procedure for each sample lasted 4 min, 2 min on the floor indoor microbial exposure to other age groups, such as adolescents and and 2 min on other surfaces above the floor like chairs and desks. The adults, is not clear. In addition, current home microbiome health as- floor
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