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Characteristics of Airborne Bacterial Communities in Indoor and Outdoor Environments During Continuous Haze Events in Beijing I

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Characteristics of Airborne Bacterial Communities in Indoor and Outdoor Environments During Continuous Haze Events in Beijing I Environment International 139 (2020) 105721 Contents lists available at ScienceDirect Environment International journal homepage: www.elsevier.com/locate/envint Characteristics of airborne bacterial communities in indoor and outdoor T environments during continuous haze events in Beijing: Implications for health care Jianguo Guoa,b, Yi Xiongc, Changhua Shia,b, Ce Liud, Hongwei Lia,b, Hua Qiane, Zongke Sunf, ⁎ Chuan Qina,b, a NHC Key Laboratory of Human Disease Comparative Medicine (The Institute of Laboratory Animal Sciences, CAMS&PUMC), Beijing 100021, China b Key Laboratory of Human Diseases Animal Model, State Administration of Traditional Chinese Medicine, Beijing 100021, China c Department of Food Science and Engineering, School of Chemistry and Chemical Engineering, Harbin Institute of Technology, Harbin 150001, China d Department of Infectious Disease, Beijing Chuiyangliu Hospital, Affiliated with Tsinghua University, Beijing 100022, China e School of Energy and Environment, Southeast University, Nanjing 211189, China f National Institute of Environmental Health, China CDC, Beijing 100021, China ARTICLE INFO ABSTRACT Handling editor: Adrian Covaci There is solid evidence that haze pollution threatens human health owing to the abiotic pollutants it contains. Keywords: However, the characteristics of airborne bacterial communities in indoor and outdoor environments exhibiting Airborne bacterial community haze occurrence are still unknown. Thus, we examined variations in both indoor and outdoor airborne bacterial Haze events communities in Beijing from December 9–27, 2016, a period which included three haze events. The outdoor Indoor environment airborne bacterial communities were clustered into two main groups (Groups I and II), and they shifted between Outdoor environment two typical bacterial communities regardless of the haze event. The Chao1, Shannon, and phylogenetic diversity Respiratory disease indexes and abundance of dominant classes changed significantly, as did airborne bacterial community type. The Pneumonia indoor airborne bacterial community closely tracked the outdoor bacterial community type, forming two ob- vious groups supported by Adonis analysis, changes in dominant classes, and bacterial diversity compared to the outdoor group. Furthermore, we found that the airborne bacterial community type could affect the morbidity of respiratory diseases. Daily pneumonia cases were significantly higher in Group I(p = 0.035), whereas daily amygdalitis cases were significantly higher in Group II(p = 0.025). Interestingly, the enriched classes in the indoor environment were quite different from those in the typical airborne bacterial community environment, except for Clostridia, which had significantly higher abundance in both indoor environments. In conclusion, we found that the two indoor and outdoor airborne bacterial community types changed independently of haze events, and the special airborne bacterial community type was closely related to the incidence of pneumonia in the heavy haze season. 1. Introduction NOx, CO, VOCs, PM10, and PM2.5 emissions were reduced by 20–40% in 2020 (Guo et al. 2018). Many other measures have been implemented The annual concentrations of PM2.5 have increased by 48% in China to reduce the level of air pollution. However, there is still a long way to and an increasing trend was observed in 87.9% of the country ac- go. The level of air pollution in China is substantially higher than that in cording to data from 1999 to 2016 (Zhao et al. 2019). High PM2.5 levels developed countries, and its threat to public health has attracted a large were mainly located in the Beijing-Tianjin-Hebei region in North China, amount of attention, particularly in relation to haze events (Guan et al. East China, and the Henan province (Lin et al. 2014). The annual PM2.5 2016). 3 concentrations in >10% of this area have been > 35 μg/m since 2003 Haze pollution, and especially fine particulate matter (PM2.5), can (Zhaoet al. 2019). A total of 83% of the population lives in areas where increase mortality from heart disease (Pope et al. 2009; Pope et al. 3 the annual PM2.5 level exceeds 35 μg/m (Liu et al. 2016). A coal cap 2004), stroke, respiratory disease (Zhang and Cao 2015), and lung policy was implemented in the Beijing-Tianjin-Hebei region, and SO2, cancer (Lepeule et al. 2012; Pope et al. 2011), and can shorten ⁎ Corresponding author at: Pan Jia Yuan Nan Li No. 5, Chao Yang District, Beijing 100021, China. E-mail address: [email protected] (C. Qin). https://doi.org/10.1016/j.envint.2020.105721 Received 1 November 2019; Received in revised form 2 April 2020; Accepted 3 April 2020 Available online 16 April 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/). J. Guo, et al. Environment International 139 (2020) 105721 ) )a( )b( 3 200 PM2.5 PM10 150 100 50 Concentration (ug/m 0 Jul-16 Oct-16 Apr-16 Jun-16 Jan-17 Mar-17 Feb-17 Nov-16 Dec-16 Aug-16 Sep-16 May-16 (c) TC1 TP2 TC3 TP4 TC5 TP6 TC7 3 g/m μ and PM10 Concentration of PM2.5 12/9a12/9p 12/10a12/10p12/11a12/11p12/12a12/12p12/13a12/13p12/14a12/14p12/15a12/15p12/16a12/16p12/17a12/17p12/18a12/18p12/19a12/19p12/20a12/20p12/21a12/21p12/22a12/22p12/23a12/23p12/24a12/24p12/25a12/25p12/26a12/26p12/27a12/27p Fig. 1. Sampling details. (a) Distribution of sampling sites. The room (307, 311, 315) represents the indoor environment, and balcony (Y) represents the outdoor environment. (b) Mean concentrations of PM2.5 and PM10 for each month between April 2016 and March 2017. (c) Concentrations of PM2.5 and PM10 at each sampling interval between December 9 and 27, 2016. TC: time interval < 75 μg/m3; TP: time interval > 75 μg/m3 (note: time intervals were numbered in chronological order). lifespans. Data from six low- and middle-income countries showed that outdoors (Kembel et al. 2012). Our knowledge of indoor microbial 3 each 10 μg/m increase of PM2.5 corresponded to a 0.72 increase in communities has greatly increased in recent years owing to the devel- overall disability scores based on the World Health Organization Dis- opment of high-throughput sequencing technology. This technology has ability Assessment Schedule (Lin et al. 2017). PM2.5 exposure caused shown that the indoor microbial community is affected by building 4.2 million deaths (7.6% of total global deaths) and 103.1 million factors, which govern the entry behavior of outdoor microorganisms, as disability-adjusted life-years (DALYs) (4.2% of global DALYs) in 2015 well as by occupants, who release human-associated microorganisms (Cohen et al. 2017). Premature mortalities attributed to PM2.5 in China and re-suspend microbes residing on floors and surfaces (Leung and Lee amounted to 1.37 million in 2013 (Liuet al. 2016). 2016). Therefore, both the outdoor environment and occupants act as Airborne microorganisms are crucial components of the atmo- major sources of indoor microorganisms (Adams et al. 2015; Hospodsky sphere, with bacterial cells exceeding 1 × 104 m−3 (Burrows et al. et al. 2012; Leung and Lee 2016; Stephens et al. 2015). 2009), and they can threaten human health by disseminating allergens In Beijing, severe haze pollution occurs frequently in winter, when and pathogens (Griffin 2007). Many researchers have investigated pathogenic bacteria and fungi are more abundant (Duet al. 2018). Al- structural variation in the airborne bacterial community during haze though microbial composition varies between settings, bacteria are events (Du et al. 2018; Sun et al. 2018; Yan et al. 2018; Zhen et al. generally the most abundant microbes (approximately 80%), followed 2017). However, comparisons of the airborne bacterial community on by fungi (Zhai et al. 2018). Therefore, in this study, we investigated haze and non-haze days have yielded inconsistent results. Fan et al. variations in airborne bacterial communities in indoor and outdoor screened several dominant genera in PM2.5 on heavy or severe pollution environments in Beijing from December 9–27, 2016, a period which days (Fan et al. 2019), and Sun et al. found that the dominant genera included three haze cycles. In addition, we explored the reason for the varied under different concentrations of PM including Rhizobium, Pro- shift in the bacterial community and the relationship between bacterial pionibacterium and Comamonadaceae (Abd Aziz et al. 2018; Sunet al. community structure and respiratory disease. Our results have im- 2018), while no correlation between dominant genera and pollution portant implications for health care during haze events. levels was observed in other studies (Duet al. 2018; Wei et al. 2016; Xu et al. 2017b; Yanet al. 2018). These inconsistent results may be largely 2. Material and methods due to the limited numbers of samples and lack of continuous sampling (Dong et al. 2016; Duet al. 2018), as data on unsampled days might 2.1. Exposure experiment help explain the correlation between airborne bacterial communities and air pollution. Therefore, a better understanding of the dynamic In this study, we sampled the indoor and outdoor environments on variation in airborne bacterial communities throughout the haze pro- the third floor of a three-story building at approximately 10 mabove cess is important for human health risk evaluation. the ground (116°26′35.86″E, 39°52′22.30″N). We selected four sam- Indoor airborne microorganisms are also an important considera- pling sites: one in each of three different student dormitories (307, 311, tion in human health risk evaluations during haze events, because hu- and 315), and one on a balcony (Y) (Fig. 1a). The balcony was open to mans spend most of their time indoors (up to 90% in industrialized the outdoor air, with no barriers. The samples collected from 307, 311, countries [(Hoppe and Martinac 1998; Klepeis et al. 2001)]).
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