Atmospheric Environment 213 (2019) 311–325 Contents lists available at ScienceDirect Atmospheric Environment journal homepage: www.elsevier.com/locate/atmosenv Do Conocarpus erectus airborne pollen grains exacerbate autumnal T thunderstorm asthma attacks in Ahvaz, Iran? ∗ Hassan Dehdari Rada,b, Mohammad-Ali Assarehzadeganc, Gholamreza Goudarzia,b,d, , Armin Sorooshiane,f, Yaser Tahmasebi Birganib,d, Heidar Malekia,g, Saeed Jahantabh, Esmaeil Idania,i, Ali Akbar Babaeia,b,d, Abdolkazem Neisia,b,d a Air Pollution and Respiratory Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran b Department of Environmental Health Engineering, School of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran c Department of Immunology, Faculty of Medicine, and Immunology Research Center, Iran University of Medical Sciences, Tehran, Iran d Environmental Technologies Research Center (ETRC), Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran e Department of Chemical and Environmental Engineering, University of Arizona, Tucson, AZ, USA f Department of Hydrology and Atmospheric Sciences, University of Arizona, Tucson, AZ, USA g MS of Environmental Engineering, Faculty of Water Sciences Engineering, Shahid Chamran University of Ahvaz, Ahvaz, Iran h Department of Immunology, Faculty of Medicine, Ahvaz Joundishapur University of Medical Sciences, Ahvaz, Iran i Department of Internal Medicine, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran GRAPHICAL ABSTRACT ARTICLE INFO ABSTRACT Keywords: A disastrous outbreak of thunderstorm-induced asthma attacks posed a major public health threat in Ahvaz, Iran Pollen grains in autumn of 2013 (> 15,000 referrals to hospital emergency rooms and pulmonary clinics). City officials Fungal spores claimed that promoting factors included acid rain, particulate matter, ozone, and polycyclic aromatic hydro- Conocarpus erectus carbon compounds (PAHS) could lead to this phenomenon. After these potential causes were rejected by careful Temporal variations research, the next possible cause that this study addresses is a potential link of the asthma attacks to airborne Tree pruning pollen grains and fungal spores. In order to sample these parameters, a Hirst-type volumetric spore sampler was used, which was installed on the rooftop of the sampling site. Sampling was done during two six-month periods to characterize the regional bioaerosol. The first period included the autumn (September 22 to December 20of 2016) and winter seasons (December 21 of 2016 to March 19 of 2017), while the second period included the following autumn (September 23 to December 21 of 2017) and winter seasons (December 22 of 2017 to March 20 of 2018). In both studied periods, airborne weed pollen grains, especially Amaranthaceae sp., were by far the greatest contributor to total airborne pollen grain concentrations (50.45%, 3757 pollen grains/m3 and 52.12%, 2392 pollen grains/m3, respectively). Among fungal spores, Cladosporium had the highest concentrations ∗ Corresponding author. Air Pollution and Respiratory Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran E-mail address: [email protected] (G. Goudarzi). https://doi.org/10.1016/j.atmosenv.2019.06.010 Received 19 December 2018; Received in revised form 31 May 2019; Accepted 3 June 2019 Available online 04 June 2019 1352-2310/ © 2019 Elsevier Ltd. All rights reserved. H. Dehdari Rad, et al. Atmospheric Environment 213 (2019) 311–325 (75.29%, 258677 spores/m3 and 80.33%, 247693 spores/m3, respectively). Findings also showed that con- centrations of airborne pollen grains were higher in autumn seasons (6361 and 4167 pollen grains/m3, re- spectively) in comparison with winter seasons (1085 and 423 pollen grains/m3, respectively), while the con- centrations of fungal spores were enhanced in winter seasons (189216 and 160962 spores/m3, respectively) versus autumn seasons (154377 and 147377 spores/m3, respectively). Fungal spores exhibited a uniform dis- tribution during the entire study period, but airborne pollen grains were significantly higher in autumn seasons. The numbers of referrals associated with thunderstorm asthma attacks decreased drastically after implementing Conocarpus erectus tree pruning activities. We concluded that the autumnal thunderstorm asthma attacks in Ahvaz might be triggered by a combination of bio-allergens (fungal spores and airborne pollen grains such as from Conocarpus erectus) and high levels of air pollutants from industrial activity. The results of this work suggest controlling bio-allergen levels by preventive measures such as tree pruning, weed removal, and emasculating urban green infrastructures before the flowering season. 1. Introduction 2015). According to studies worldwide, pollen allergies affect urban po- Bacteria, viruses, pollen grains, fungal spores and fragments of pulations more than those of rural areas. This can be partly attributed to plants are the most common components of biological aerosols in the urban green infrastructures and their role in producing airborne pollen. atmosphere. Airborne pollen grains are a male biological structure The substantial advantages of urban green infrastructures are (a) pro- playing an important role in the reproductive cycle of the anemophilous viding aesthetic beauty, (b) lowering urban temperatures and miti- (wind-pollinated) plants (Ribeiro et al., 2015; Ring, 2012; Zhai et al., gating the intensity of urban heat island effects, and (c) capturing 2018). Large amounts of pollen grains are released into the atmosphere particulate matter, carbon dioxide, ozone, and other air pollutants. by wind pollination process (transportation of pollen grain from the Nevertheless, they also have some fundamental disadvantages, which anthers to the stigma by wind), especially during flowering seasons. are associated with the pollination of the plants and their subsequent Consequently, airborne pollen grains become a seasonal biogenic con- negative role in producing related respiratory diseases (Cariñanos et al., stituent of atmospheric aerosols (Ribeiro et al., 2017; Sun et al., 2016). 2014; Maya-Manzano et al., 2017; Tseng et al., 2018). Pollen grains are typically divided into three broad categories (tree, High concentrations of aeroallergens from urban green infra- grass, weed) with each category having a distinct temporal distribution structures can lead to respiratory disease outbreaks. One of the most (Fuhrmann et al., 2016). Fungal spores are also an important compo- important respiratory outbreaks is in the form of a thunderstorm nent of biological aerosol in the atmosphere, which frequently can be asthma attack, which can affect a huge number of people. Following the observed at any time of the year (Ezike et al., 2016). In general, the early rainfall during the autumn of 2013, a severe outbreak of re- presence, kind, and concentration of pollen grains and fungal spores in spiratory syndromes occurred in the Khuzestan Province, Iran which the ambient air mainly depend on plant type, the geographical dis- was very severe in Ahvaz. By 20 November 2013, about 20,000 patients tribution of plants, the physiological state of plants, season of the year, had been registered in emergency rooms (ERs) with respiratory symp- meteorological conditions (wind, precipitation, temperature, humidity, toms, of whom 93% received clinical care on an outpatient basis and etc), and topography (Cariñanos and Casares-Porcel, 2011; Duque et al., were discharged with rapid relief of symptoms. The remaining 7% were 2013; Fernández-Rodríguez et al., 2014). hospitalized due to the severity of the disease. These respiratory syn- Pollen grains and fungal spores pose negative impacts on human drome outbreaks also reoccurred in 2014 and 2015 (Idani et al., 2016). health and quality of life owing to their ability to penetrate and deposit There have been various assumptions regarding the autumn re- inside the human respiratory system (Youn et al., 2016). Exposure to spiratory incidents of 2013–2015 in Ahvaz. Since this phenomenon these aeroallergens is associated with the development of allergies. happened concurrently with the first autumnal rain, some govern- Allergic sensitization is a risk factor for the subsequent development of mental organizations such as the Ahvaz Department of Environment allergic rhinitis, asthma attacks, and pollinosis (Caillaud et al., 2015; (DOE) claimed that acidic or contaminated wet deposition was the main Irani et al., 2013; Katz et al., 2018; Weinberger, 2015). The common cause for promoting the respiratory outbreaks during this period. Our symptoms of seasonal pollen allergies that normally affect people are earlier work showed that there was no acidic precipitation during the sneezing, blocked nasal passages, and ocular itching. The intensity of time of respiratory outbreaks in 2013–2015. The average value of the these symptoms vary between individuals and range from mildly an- pH of the rainwater indicates that it can be categorized as neutral noying to severely disruptive. According to European Community Re- rainfall (Naimabadi et al., 2018). Other possible factors in creating this spiratory Health Survey (ECRHS) reports, 30% of the European Union phenomenon that were posed by air quality control specialists include population suffers from chronic allergic diseases (Zuberbier et al., particulate matter (PM), ozone (O3), and polycyclic aromatic hydro- 2014). The World Allergy