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Bioaerosols in the waterpipe cafés: genera, levels, and factors influencing their concentrations

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Abstract

This study was conducted in order to assess the exposure to bacterial and fungal bioaerosols in the air of waterpipe cafés (AWPCs), in the hose of waterpipe (HWP), and in the water bowl of the waterpipe (WBWP) and to investigate the factors influence increasing the contamination levels in waterpipe cafés in Ardabil. From all the 50 cafés studied, the samples were taken from air and from water contained in water bowl and hose for bacterial and fungal analyses. The results demonstrated that the mean numbers of bacteria and fungi in the indoor air of café, hose, and water bowl were 33.90 ± 14.86 and 25.24 ± 1.99 CFU/m3, 72.16 ± 29.55 and 72.78 ± 42.45 CFU/plate, 53.7 ± 25.46 and 25.26 ± 13.94 CFU/ml, respectively. The predominant bacterial genera in waterpipe cafés were Pseudomonas and Bacillus in air, Staphylococcus and Pseudomonas in the hose, and Staphylococcus and Pseudomonas in the water bowl, respectively. The predominant fungal species in waterpipe cafés were Penicillium and Cladosporium in air, yeast and Fusarium in the hose, and Paecilomyces and yeast in the water bowl, respectively. The results of statistical analysis showed that there was a significant relationship between the mean concentrations of bacterial aerosol and qualitative variables such as type of heating system, materials of wall and ceiling, traditional restaurants, interior supermarkets, moisturized walls, the number of people, area of cafés, and temperature. But there was no significant relationship between these variables and the mean concentration of fungal aerosols. The results also showed that the levels of bioaerosols were high in the air, hose, and water bowl of the waterpipe. Therefore, cafés can be a potential source for the transmission of pathogenic agents and increase the risk of respiratory diseases among waterpipe smoking individuals.

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References

  • Akl EA, Gaddam S, Gunukula SK, Honeine R, Jaoude PA, Irani J (2010) The effects of waterpipe tobacco smoking on health outcomes: a systematic review. Int J Epidemiol 39:834–857

    Article  Google Scholar 

  • Akl EA, Jawad M, Lam WY, Obeid R, Irani J (2013) Motives, beliefs and attitudes towards waterpipe tobacco smoking: a systematic review. Harm Reduct J 10:12

    Article  Google Scholar 

  • Alaidarous M, Alanazi M, Abdel-Hadi A (2017) Isolation, identification, and antimicrobial susceptibility of bacteria associated with Waterpipe contaminants in selected area of Saudi Arabia BioMed research international 2017

  • Arzanlo M, Fazlzadeh M, Hazrati S (2017) Types and concentration of fungal bio-aerosols in hospital indoor air of Imam Khomeini and Alavi hospital in Ardabil city during 2016. Iran Occup Health 14:84–95

    Google Scholar 

  • Baghani AN, Rostami R, Arfaeinia H, Hazrati S, Fazlzadeh M, Delikhoon MJE (2018) BTEX in indoor air of beauty salons: Risk assessment, levels and factors influencing their concentrations. 159:102–108

  • Bibars ARM, Obeidat SR, Khader Y, Mahasneh AM, Khabour OF (2015) The effect of waterpipe smoking on periodontal health. Oral Health Prev Dent 13

  • Chen Q, Hildemann LM (2009) The effects of human activities on exposure to particulate matter and bioaerosols in residential homes. Environ Sci Technol 43:4641–4646

    Article  CAS  Google Scholar 

  • Dehghani M, Sorooshian A, Ghorbani M, Fazlzadeh M, Miri M, Badiee P, Parvizi A, Ansari M, Baghani AN, Delikhoon M (2018a) Seasonal variation in culturable bioaerosols in a wastewater treatment plant. Aerosol Air Qual Res 18:2826–2839

    Article  CAS  Google Scholar 

  • Dehghani M, Sorooshian A, Nazmara S, Baghani AN, Delikhoon M (2018b) Concentration and type of bioaerosols before and after conventional disinfection and sterilization procedures inside hospital operating rooms. Ecotoxicol Environ Saf 164:277–282

    Article  CAS  Google Scholar 

  • EPA (2006) Alternate 1 in 3 sampling and returns hipping schedule. [Online]. Available from:http://www.epa.gov/ttn/amtic/files/ambient/pm25/2006altspec.pdf

  • Faridi S et al (2017) Bioaerosol exposure and circulating biomarkers in a panel of elderly subjects and healthy young adults. Sci Total Environ 593:380–389

    Article  CAS  Google Scholar 

  • Fazlzadeh M, Rostami R, Hazrati S, Rastgu A (2015) Concentrations of carbon monoxide in indoor and outdoor air of Ghalyun cafes. Atmos Pollut Res 6:550–555

    Article  CAS  Google Scholar 

  • Fröhlich-Nowoisky J, Kampf CJ, Weber B, Huffman JA, Pöhlker C, Andreae MO, Lang-Yona N, Burrows SM, Gunthe SS, Elbert W, Su H, Hoor P, Thines E, Hoffmann T, Després VR, Pöschl U (2016) Bioaerosols in the earth system: climate, health, and ecosystem interactions. Atmos Res 182:346–376

    Article  CAS  Google Scholar 

  • Fromme H, Schober W (2017) Die Wasserpfeife (Shisha)–Innenraumluftqualität, human-biomonitoring und Gesundheitseffekte The waterpipe (shisha)–indoor air quality, human biomonitoring, and health effects. Pneumologe 14:250–264

    Article  Google Scholar 

  • Ghafouri N, Hirsch JD, Heydari G, Morello CM, Kuo GM, Singh RF (2011) Waterpipe smoking among health sciences university students in Iran: perceptions, practices and patterns of use. BMC Res Notes 4:496

    Article  Google Scholar 

  • Grekin ER, Ayna D (2012) Waterpipe smoking among college students in the United States: a review of the literature. J Am Coll Heal 60:244–249

    Article  Google Scholar 

  • Gόrny RL, Dutkiewicz J, Krysinska-Traczyk E (1999) Size distribution of bacterial and fungal bioaerosols in indoor air. Ann Agric Environ Med 6:105–113

    Google Scholar 

  • Harrad S, Hazrati S, Ibarra C (2006) Concentrations of polychlorinated biphenyls in indoor air and polybrominated diphenyl ethers in indoor air and dust in Birmingham, United Kingdom: implications for human exposure. Environ Sci Technol 40:4633–4638

    Article  CAS  Google Scholar 

  • Hassanvand MS et al (2015) Characterization of PAHs and metals in indoor/outdoor PM10/PM2. 5/PM1 in a retirement home and a school dormitory. Sci Total Environ 527:100–110

    Article  CAS  Google Scholar 

  • Hazrati S, Rostami R, Fazlzadeh M (2015) BTEX in indoor air of waterpipe cafés: levels and factors influencing their concentrations. Sci Total Environ 524:347–353

    Article  CAS  Google Scholar 

  • Hazrati S, Rostami R, Farjaminezhad M, Fazlzadeh M (2016) Preliminary assessment of BTEX concentrations in indoor air of residential buildings and atmospheric ambient air in Ardabil, Iran. Atmos Environ 132:91–97

    Article  CAS  Google Scholar 

  • Heo KJ, Lim CE, Kim HB, Lee BU (2017) Effects of human activities on concentrations of culturable bioaerosols in indoor air environments. J Aerosol Sci 104:58–65

    Article  CAS  Google Scholar 

  • Heydari G, Taghizdeh F, Fazlzadeh M, Jafari AJ, Asadgol Z, Mehrizi EA, Moradi M, Arfaeinia H (2019) Levels and health risk assessments of particulate matters (PM 2.5 and PM 10) in indoor/outdoor air of waterpipe cafés in Tehran, Iran. Environ Sci Pollut Res 26:7205–7215

    Article  CAS  Google Scholar 

  • Hsu Y-C, Kung P-Y, Wu T-N, Shen Y-H (2012) Characterization of indoor-air bioaerosols in Southern Taiwan. Aerosol Air Qual Res 12:651–661

    Article  CAS  Google Scholar 

  • Jackson D, Aveyard P (2008) Waterpipe smoking in students: prevalence, risk factors, symptoms of addiction, and smoke intake. Evidence from one British university. BMC Public Health 8:174

    Article  Google Scholar 

  • Jawad M, Lee JT, Millett C (2015) Waterpipe tobacco smoking prevalence and correlates in 25 Eastern Mediterranean and Eastern European countries: cross-sectional analysis of the Global Youth Tobacco Survey. Nicotine Tob Res 18:395–402

    Article  Google Scholar 

  • Jo W-K, Seo Y-J (2005) Indoor and outdoor bioaerosol levels at recreation facilities, elementary schools, and homes. Chemosphere 61:1570–1579

    Article  CAS  Google Scholar 

  • Karra S, Katsivela E (2007) Microorganisms in bioaerosol emissions from wastewater treatment plants during summer at a Mediterranean site. Water Res 41:1355–1365

    Article  CAS  Google Scholar 

  • Kim KY, Kim YS, Kim D (2010) Distribution characteristics of airborne bacteria and fungi in the general hospitals of Korea. Ind Health 48:236–243

    Article  Google Scholar 

  • Kim K-H, Kabir E, Jahan SA (2017) Airborne bioaerosols and their impact on human health. J Environ Sci

  • Lee J-H, Jo W-K (2006) Characteristics of indoor and outdoor bioaerosols at Korean high-rise apartment buildings. Environ Res 101:11–17

    Article  CAS  Google Scholar 

  • Markowicz P, Löndahl J, Wierzbicka A, Suleiman R, Shihadeh A, Larsson L (2014) A study on particles and some microbial markers in waterpipe tobacco smoke. Sci Total Environ 499:107–113

    Article  CAS  Google Scholar 

  • Masadeh MM, Hussein EI, Alzoubi KH, Khabour O, Shakhatreh MAK, Gharaibeh M (2015) Identification, characterization and antibiotic resistance of bacterial isolates obtained from waterpipe device hoses. Int J Environ Res Public Health 12:5108–5115

    Article  CAS  Google Scholar 

  • Masjedi MR, Taghizadeh F, Hamzehali S, Ghaffari S, Fazlzadeh M, Jafari AJ, Niazi S, Mehrizi EA, Moradi M, Pasalari H, Arfaeinia H (2019) Air pollutants associated with smoking in indoor/outdoor of waterpipe cafés in Tehran, Iran: concentrations, affecting factors and health risk assessment. Sci Rep 9:3110

    Article  CAS  Google Scholar 

  • Maziak W, Ward K, Soweid RA, Eissenberg T (2004) Tobacco smoking using a waterpipe: a re-emerging strain in a global epidemic. Tob Control 13:327–333

    Article  CAS  Google Scholar 

  • Maziak W, Taleb ZB, Bahelah R, Islam F, Jaber R, Auf R, Salloum RG (2014) The global epidemiology of waterpipe smoking tobacco control:tobaccocontrol-2014-051903

  • PK Menon, Sajit A, Rehman O, Tamali S, John S (2015) A pilot study on microbial flora of water contained in shisha water pipes and their identification by MALDI-TOF MS. In: Proceedings of the 7th annual scientific meeting of Gulf Medical University, 4th & 5th November, 2015. pp 12–16

  • Mentese S, Yousefirad A, Arısoy M, Güllü G (2012) Seasonal and spatial variations of bioaerosols in indoor urban environments, Ankara, Turkey. Indoor Built Environ 21:797–810

  • Nazaroff WW (2016) Teaching indoor environmental quality. Indoor Air 26:515–516

    Article  Google Scholar 

  • Niazi S, Hassanvand MS, Mahvi AH, Nabizadeh R, Alimohammadi M, Nabavi S, Faridi S, Dehghani A, Hoseini M, Moradi-Joo M, Mokamel A, Kashani H, Yarali N, Yunesian M (2015) Assessment of bioaerosol contamination (bacteria and fungi) in the largest urban wastewater treatment plant in the Middle East. Environ Sci Pollut Res 22:16014–16021

    Article  CAS  Google Scholar 

  • Nikaeen M, Hatamzadeh M, Hasanzadeh A, Sahami E, Joodan I (2009) Bioaerosol emissions arising during application of municipal solid-waste compost. Aerobiologia 25:1–6

    Article  Google Scholar 

  • Perrino C, Marcovecchio F (2016) A new method for assessing the contribution of primary biological atmospheric particles to the mass concentration of the atmospheric aerosol. Environ Int 87:108–115

    Article  CAS  Google Scholar 

  • Priyamvada H, Priyanka C, Singh RK, Akila M, Ravikrishna R, Gunthe SS (2018) Assessment of PM and bioaerosols at diverse indoor environments in a southern tropical Indian region. Build Environ 137:215–225

    Article  Google Scholar 

  • Rostami R, Naddafi K, Aghamohamadi A (2009) Survey of peanut fungal contamination and its relationship with ambient conditions in the Bazar of Zanjan. J Environ Health Sci Eng 6:295–300

    Google Scholar 

  • Rostami R, Zarei A, Saranjam B, Ghaffari HR, Hazrati S, Poureshg Y, Fazlzadeh M (2019) Exposure and risk assessment of PAHs in indoor air of waterpipe cafés in Ardebil, Iran Building and Environment

  • Ruzer LS, Harley NH (2012) Aerosols handbook: measurement, dosimetry, and health effects. CRC press

  • Sabahy A, Divsalar K, Bahreinifar S, Marzban M, Nakhaee N (2011) Waterpipe tobacco use among Iranian university students: correlates and perceived reasons for use. Int J Tuberc Lung Dis 15:844–847

    Article  Google Scholar 

  • Safizadeh H, Moradi M, Rad MR, Nakhaee N (2014) Bacterial contamination of different components of the waterpipe. Int J Tuberc Lung Dis 18:988–991

    Article  CAS  Google Scholar 

  • Shchipkova A, Nagaraja H, Kumar P (2010) Subgingival microbial profiles of smokers with periodontitis. J Dent Res 89:1247–1253

    Article  CAS  Google Scholar 

  • Smith SY, Curbow B, Stillman FA (2007) Harm perception of nicotine products in college freshmen. Nicotine Tob Res 9:977–982

    Article  Google Scholar 

  • Suzuki K, Nakamura A, Fujieda A, Nakase K, Katayama N (2012) Pulmonary infection caused by Exophiala dermatitidis in a patient with multiple myeloma: a case report and a review of the literature. Med Mycol Case Rep 1:95–98. https://doi.org/10.1016/j.mmcr.2012.10.002

    Article  Google Scholar 

  • Toor R et al (2014) Children summer exposure to environmental tobacco smoke. Results from the first phase of a larger seasonal exposure study. Am J Respir Crit Care Med 189:A4103

    Google Scholar 

  • Walser SM, Gerstner DG, Brenner B, Bünger J, Eikmann T, Janssen B, Kolb S, Kolk A, Nowak D, Raulf M, Sagunski H, Sedlmaier N, Suchenwirth R, Wiesmüller G, Wollin KM, Tesseraux I, Herr CEW (2015) Evaluation of exposure–response relationships for health effects of microbial bioaerosols–a systematic review. Int J Hyg Environ Health 218:577–589

    Article  Google Scholar 

  • Wang Y-F, Wang C-H, Hsu K-L (2010) Size and seasonal distributions of airborne bioaerosols in commuting trains. Atmos Environ 44:4331–4338

    Article  CAS  Google Scholar 

  • Warnakulasuriya S (2011) Waterpipe smoking, oral cancer and other oral health effects. Evid Based Dent 12:44–45

    Article  Google Scholar 

  • WHO (2010) WHO guidelines for indoor air quality: selected pollutants

Download references

Acknowledgments

The authors are grateful for the technical support from the laboratory of environmental health engineering in Tehran University of Medical Sciences.

Funding

This research work was financially supported by the Social Determinants of Health Research Center (Grant number: ARUMS.SDHRC.1397.05).

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Authors and Affiliations

  1. Department of Environmental Health Engineering, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Kazem Naddafi, Ramin Nabizadeh, Abbas Norouzian Baghani & Mehdi Fazlzadeh

  2. Center for Air Pollution Research (CAPR), Institute for Environmental Research (IER), Tehran University of Medical Sciences, Tehran, Iran

    Kazem Naddafi & Ramin Nabizadeh

  3. Social Determinants of Health Research Center, Ardabil University of Medical Sciences, Ardabil, Iran

    Mehdi Fazlzadeh

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  1. Kazem Naddafi
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  2. Ramin Nabizadeh
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Correspondence to Mehdi Fazlzadeh.

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Naddafi, K., Nabizadeh, R., Baghani, A.N. et al. Bioaerosols in the waterpipe cafés: genera, levels, and factors influencing their concentrations. Environ Sci Pollut Res 26, 20297–20307 (2019). https://doi.org/10.1007/s11356-019-05413-6

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