Science of the Total Environment 524–525 (2015) 347–353

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

BTEX in indoor air of waterpipe cafés: Levels and factors influencing their concentrations Sadegh Hazrati a, Roohollah Rostami b, Mehdi Fazlzadeh a,⁎ a b

Department of Environmental Health Engineering, School of Public Health, Ardabil University of Medical Sciences, Ardabil, Iran Department of Environmental Health Engineering, School of Public Health, Semnan University of Medical Sciences, Semnan, Iran

H I G H L I G H T S • • • •

Benzene mean concentration of 4.96 mg/m3 was high compared to OEL-TWA and OEL-STEL The expected cancer risk of 4314 × 10− 6 was obtained for benzene long-term exposure Total hazard index for BTEX long-term exposure was considerably high (HI = 63.23) Fruit flavored tobacco lead to higher BTEX concentrations than regular tobacco

a r t i c l e

i n f o

Article history: Received 19 October 2014 Received in revised form 4 April 2015 Accepted 10 April 2015 Available online xxxx Editor: Lidia Morawska Keywords: Air quality Benzene Ghalyun Risk assessment EST

a b s t r a c t BTEX (benzene, toluene, ethylbenzene and xylene) concentrations, factors affecting their levels, and the exposure risks related to these compounds were studied in waterpipe (Ghalyun/Hookah) cafés of Ardabil city in Islamic Republic of Iran. 81 waterpipe cafés from different districts of Ardabil city were selected and their ambient air was monitored for BTEX compounds. Air samples were taken from standing breathing zone of employees, ~150 cm above the ground level, and were analyzed using GC-FID. In each case, the types of smoked tobacco (regular, fruit flavored), types of ventilation systems (natural/artificial), and the floor level at which the café was located were investigated. A high mean concentration of 4.96 ± 2.63 mg/m3 corresponding to long term exposure to benzene-related cancer risk of 4314 × 10−6 was estimated. The levels of the remaining compounds were lower than the national guideline limits, but their hazard quotients (HQ) for long term exposure to ethylbenzene (1.15) and xylene (17.32) exceeded the HQ unit value. Total hazard indices (HI) of 63.23 were obtained for non-cancer risks. Type of the smoked tobacco was the most important factor influencing BTEX concentrations in the cafés. BTEX concentrations in indoor ambient air of Ardabil waterpipe cafés were noticeably high, and therefore may pose important risks for human health on both short and long term exposures. © 2015 Elsevier B.V. All rights reserved.

1. Introduction There are growing concerns about indoor air pollution; since concentrations of indoor air pollutants are known to be frequently higher than outdoor (Guo et al., 2004; Toor et al., 2014). Furthermore, people normally spend more than 80% of their time in indoor environments (Klepeis et al., 2001) leading to intake of toxic substances, mainly via inhalation and dust ingestion pathways in contaminated atmosphere (Harrad et al., 2006). Volatile Organic Compounds (VOCs) are important atmospheric and indoor ambient air pollutants. VOCs evaporate readily at room

⁎ Corresponding author at: Department of Environmental Health Engineering, School of Public Health, Ardabil University of Medical Sciences, Ardabil, Iran. E-mail address: [email protected] (M. Fazlzadeh).

http://dx.doi.org/10.1016/j.scitotenv.2015.04.031 0048-9697/© 2015 Elsevier B.V. All rights reserved.

temperature and inhalation pathway becomes the most important route of exposure for these substances. Benzene, toluene, ethylbenzene, and xylene, known as BTEX, are environmentally important VOCs. They are released in the atmosphere from both artificial and natural sources (Caselli et al., 2010; Davil et al., 2013; Fazlzadeh et al., 2012; Liu et al., 2009; Sturaro et al., 2010). BTEX compounds are known to have important impact on human health including cancer and may induce neurological disorders and symptoms such as weakness, loss of appetite, fatigue, confusion, and nausea (Hoskins, 2011). Benzene is the most toxic chemical within the BTEX family and long-term exposure to benzene may increase incidence of leukemia and aplastic anemia in human (Baker et al., 1985; Mehlman, 1990; Niri et al., 2009; Wong, 1995). International Agency for Research on Cancer (IARC) has classified benzene as an intense carcinogenic agent and ethylbenzene as a suspected carcinogenic compound (IARC, 1999).

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Sources for BTEX in indoor environments include infiltration of outdoor air pollution, smoking, paints, adhesives, and other VOC emitting materials utilized in building interiors (Singh et al., 1992; WHO, 2000). Among the most visited public indoor environments, waterpipe cafés pose potential risks for elevated BTEX concentrations especially in East Mediterranean countries. Waterpipe tobacco smoking (WTS), also known in different countries as Ghalyun, Hookah, Narghile, Shisha, Sheesha, and Hubbly-bubbly smoking, is a common practice (especially among youth, college students, and young professionals) taking place in dedicated cafés. The WTS involves the passage of charcoal-heated air over flavored/raw tobacco to become smoke (Maziak et al., 2015). The smoke is bubbled through a bowl of water and then inhaled through a mouthpiece connected by a hose to the upper part of the bowl (Knishkowy and Amitai, 2005). WTS has recently gained extensive popularity worldwide and its prevalence especially among young population is increasing (Akl et al., 2011). The epidemiologic studies conducted in 44 countries reported the prevalence rate of WTS to range from less than 1 to 11.5% (Agaku et al., 2014). Other reports estimated WTS rates of up to 15% within different age groups surpassing the rate of cigarette smoking in some instances (Moh'd Al‐Mulla et al., 2008). Unlike cigarette smoking that is either stable or declining possibly due to applied global tobacco control policy, WTS shows a rising trend in many parts of the world (Agaku et al., 2014; CfD, 2013; Czoli et al., 2013; McKelvey et al., 2013; Warren et al., 2009). The important factors contributing to global spread of WTS and its rising trend are likely the introduction of flavored waterpipe tobacco, social nature of WTS (i.e., treating it as a central element of social and family gatherings), and lack of the waterpipe-specific control policies and regulations (Maziak et al., 2015). A major concern about the waterpipe is the toxic constituents of the tobacco smoke released and exposure to its second hand smoke (Dillon and Chase, 2010; Schubert et al., 2014). High concentrations of benzene (271 ± 8 μg/session) have been reported for the main stream of waterpipe; up to 6.2 times higher than the cigarette smoke (Schubert et al., 2014). Based on the available evidences, WTS is significantly associated with lung cancer, respiratory illness, low birth weight and periodontal diseases (Akl et al., 2010). Among the studied patients, regular and occasional water-pipe smokers were significantly younger when developing oral cancer, as compared to nonsmokers (Al-Amad et al., 2014). A positive correlation was reported between waterpipe smoking and respiratory symptoms. Comparing to non-smokers, pulmonary functional test values were reported significantly lower in smokers (Boskabady et al., 2014). Iran parliament passed a prohibition law on smoking (e.g., WTS) in public indoor environments in 2007 (IPRC, 2006). However, this regulation is not yet fully effective because of social considerations. There are a range of recommended occupational exposure limits set for BTEXs in indoor environments (Table 1). However, WHO does not provide acceptable concentration for general population exposure to benzene because of its carcinogenic hazard (WHO, 2010). During WTS sessions, the breath of 25 waterpipe tobacco smokers from 12 regular restaurants in Iran demonstrated high concentrations for BTEX compounds (Samarghandi et al., 2014). Owing to growing concern on increasing use of waterpipe in Iran, BTEX concentration and their

influencing factors in waterpipe cafés were investigated in the present work. 2. Material and methods 2.1. Selection of sampling locations Waterpipe cafés were studied for their indoor air pollution in Ardabil city, capital of Ardabil province in North West of Islamic Republic of Iran. All the cafés serving waterpipe in catchment areas of Ardebil urban health centers were listed and 81 out of 236 cafés were selected using systematic random sampling method and monitored for BTEX compounds. 2.2. Air sampling process Air samples were taken using the procedure described in the NIOSH Manual of Analytical Method no 1501 (NIOSH, 2003). SKC personal sampling pumps equipped with an adjustable low flow holders were used for air sampling. Flow rates were calibrated using a soap bubble flow meter. Air sampling was performed at the flow rate of 0.2 l/min and continued for 50 min to collect a total air volume of 10 l. Charcoal sorbent tubes (SKC) were used as sampling media. After completion of the sampling period, they were transported to the laboratory according to the manufacturer guideline. They were stored at − 20 °C and analyzed within 72 h (Rezazadeh Azari et al., 2011). Air samples were taken from standing breathing zone of employees, ~150 cm above the ground level. All the samples were taken in the afternoon (from 2 to 7 pm). Six more 10 liter-samples (4 from fruit flavored and 2 from regular tobacco waterpipes) were taken directly from the smoke main stream, by attaching the charcoal tube inlet into the mouthpiece of the waterpipes. 2.3. Sample preparation and analysis BTEX compounds were extracted from charcoal tubes by 2 ml of carbon disulfide (CS2). The vials containing CS2 and charcoal were gently shaken for 20 min. The solvent was transferred into GC vials and BTEX compounds were quantified by a GC (Agilent 7890A) equipped with FID detector using a capillary column (30 m, TRB-1 ms). Aliquots of 1 μl were taken from the vial and injected into a capillary column. Injector and detector temperatures were set at 250 and 300 °C, respectively. Oven temperature was programmed at 40 °C for 10 min and then 10 °C/min to 230 °C (NIOSH, 2003; Rezazadeh Azari et al., 2011). 2.4. QC & QA measures In order to control breakthrough of sorbent tubes front and back sections of the tubes were analyzed separately and none of the target compounds was detected in the back sections. Recovery of analytical method was tested by injecting 10 μg of target compounds into fresh charcoal tubes. They were subjected to similar extraction and analysis methods as the field samples. On average recovery of 92% (87–102%) was achieved for BTEX compounds. Method and field blanks (8 for

Table 1 Guidelines for BTEX levels in indoor air (HSE, 2011; MHMEI, 2012; Niosh, 2012; OSHA, 2014). Time weighted average (TWA); mg/m3

Benzene Toluene Ethylbenzene Xylene

Short-term exposure limit (STEL); mg/m3

HSE (U.K.)

MHMEI (Iran)

NIOSH

ACGIH(2007)

HSE (U.K.)

MHMEI (Iran)

NIOSH

ACGIH(2007)

3.25 191 441 220

1.6 75 87 434

0.32 375 435 435

1.6 75 87 434

– 384 552 441

8 – – 651

3.75 560 545 655

8 – – 651

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2.5. Statistical analysis

20

15

10

5

0

Other variables including; the floor level in which the cafés were located (i.e., basement/ground floor), types of ventilation systems (natural and artificial), types of the tobacco smoked (i.e., regular or fruit flavored), and employees' general information were collected using a self-designed questionnaire. Levels of BTEX in indoor air were compared with occupational exposure limit levels. Data obtained were analyzed by t-test and nonparametric tests using SPSS version 16 and the confidence level was set at 95%. Path analysis was performed using Amos 21 in order to identify the factors that significantly affect the BTEX concentrations. Finally, a risk assessment was evaluated from the measured BTEX concentrations by using Eqs. (1) to (5) (Majumdar et al., 2011), and tabulated in Table 2.

E ¼ C  IRa  EDa=BWa

ð1Þ

EY ¼ C  IRa  EDa  ðD=7Þ  ðWk=52Þ=BWa

ð2Þ

EL ¼ E  ðD=7Þ  ðWk=52Þ  ðYE=YLÞ

ð3Þ

Risk ¼ EL ðmg=kg  dÞ  SF ðmg=kg  dÞ

ð4Þ

HQ ¼ EY =R fD

ð5Þ

where, E: daily exposure (mg/kg·d), EY: yearly average daily dose received (mg/kg·d), EL: effective life time exposure (mg/kg·d), HQ: hazard quotient, and RfD; reference dose (mg/m3). Table 2 Details of risk assessment parameters (EPA, 2005).

Concentration of the pollutant (C) Inhalation rate, adult (IRa) Exposure duration, adult (EDa) Body weight, adult (BWa) Days per week exposure (D) Weeks of exposure (WK) Years of exposure (YE) Years in lifetime (YL) Slope factor or carcinogenic potency slope (SF) Reference dose (RfD)

25

mg/m3

field and 5 for method) were taken and subjected to the same preparation and analytical procedures. Concentration of target compounds were found to be within 5% of the values quantified for the samples and no correction was made for blank values. Concentrations of target compounds in blank samples ranged from 0.00 (nd; not detected) to 0.041, nd-0.064, nd-0.105, and nd-0.126 mg/m3 for benzene, toluene, ethylbenzene, and xylene, respectively. GC detector was calibrated running five calibration standard solutions with different BTEX concentrations ranging from 0.01 to 50 ppm. R2 values of 0.992, 0.981, 0.980, and 0.983 were obtained for benzene, ethylbenzene, toluene, and xylene calibration curves, respectively. One of the calibration solutions was run along each batch of samples and external standard method was used for BTEX quantification.

349

Value

Unit

– 0.83 8 70 6 48 30 70 Benzene = 0.029 (Guo et al., 2004) Benzene = 0.00855 Toluene = 1.4 Ethylbenzene = 0.286 Xylene = 0.029

mg/m3 m3/h h/d kg d Week Y Y (mg/kg·d) (mg/kg·d)

RfD = RfC (inhalation reference concentration mg/m3) × 20 (assumed adult inhalation rate m3/d) × 1/BWa (kg); based on RfCs for USEPA, IRIS (benzene = 0.03 mg/m3, toluene = 5 mg/m3, ethylbenzene = 1 mg/m3, xylenes = 0.1 mg/m3) (USEPA, 2007).

Benzene

Toluene

Ethylbenzene

Xylene

Fig. 1. Standard Box-plot with average values for BTEX concentration in indoor air of waterpipe cafés.

3. Results Average concentration of benzene (4.96 ± 2.63 mg/m3) in indoor air of the waterpipe cafés exceeded the occupational exposure limit recommended by national and international organizations (Table 1). However, average concentrations of toluene (4.86 ± 2.98 mg/m3), ethylbenzene (4.38 ± 2.88 mg/m3) and xylenes (6.69 ± 5.77 mg/m3) were lower than the occupational exposure limits (Fig. 1 and Table 3). BTEX concentrations in ambient indoor air of the cafés serving fruit flavored tobacco were significantly higher than those of serving regular tobacco (p-value b 0.01). In order to get more detailed information on BTEX generated by different tobaccos, we directly analyzed the smoke produced by two types of tobacco through attaching the charcoal tube inlets to the waterpipe mouthpiece. These examinations also confirmed a higher content of BTEX in fruit flavored as compared to the regular tobacco smoke (10.2 ± 1.2 vs. 1.9 ± 0.23 mg/m3) (Fig. 2). BTEX concentrations quantified in main stream smokes were generally higher than the corresponding BTEX concentrations of indoor air. However, toluene (1.1 ± 0.26 vs. 2.9 ± 0.29 mg/m3) and ethylbenzene (1.8 ± 0.04 vs. 1.9 ± 0.22 mg/m3) concentrations in indoor air of the cafés serving regular tobacco were higher than those of quantified in main stream of regular tobacco smoke; suggesting other possible sources of indoor air pollution for these VOCs. Distribution of cafés based on the type of smoked tobacco, the ventilation systems, and the level in which the cafés were located is shown in Fig. 3. In 79% of the cafés fruit flavored tobacco was served and 84.4% of these cafés were in basements. Anyway, none of the cafés that served regular tobacco were located in basements. The BTEX concentrations in cafés where fruit flavored tobacco was smoked, equipped with artificial (mechanical) ventilation system were not statistically different from those using natural ventilation system (p-value N0.05); implying that the mechanical ventilation systems were not effective in diluting emitted BTEX into the indoor ambient air

Table 3 Summary of BTEX concentrations in indoor air of waterpipe cafés. Contaminant

Minimum (mg/m3)

Maximum (mg/m3)

Average ± std deviation (mg/m3)

Benzene Toluene Ethylbenzene Xylene

0.37 0.48 0.45 0.01

11.64 15.82 13.82 24.76

4.96 ± 2.63 4.86 ± 2.97 4.38 ± 2.88 6.69 ± 5.77

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18

Concentration ( mg/m3)

16

Fruit flavored Regular

Fruit flavored* Regular*

14 12 10 8 6 4 2 0

Benzene

Toluene

Ethylbenzene

Xylene

Fig. 2. Average concentration of BTEX in indoor air and waterpipe main stream (marked by asterisks). Fig. 4. BTEX concentration in waterpipe cafés according to type of tobacco and ventilation system.

(Fig. 4). BTEX concentrations in the cafés located in basements were significantly higher than the cafés which were located on ground floor (p-value b 0.01) (Fig. 5). Application of path-analysis revealed the type of tobacco served as the most influential factor governing BTEX concentration in café indoor microenvironments. The modulus standardized effect sizes (MSES) were 0.44, 0.28, and 0.22 for tobacco, floor in which they were located, and the ventilation systems, respectively. According to the effect sizes,

the location of the café inside the building (floor level) was the next factor affecting the BTEX concentrations in indoor air. Risk assessment analysis revealed high cancer risk for benzene and high hazard quotient for benzene, ethylbenzene, and xylene. The highest cancer risk and HQ values were observed in the cafés serving fruit flavored tobacco (Table 4).

Fig. 3. Distribution of the waterpipe cafés based on tobacco type, ventilation system, and the floor they were located.

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Concentration (mg/m3)

12.00

Benzene

Toluene

Ethylbenzene

Xylene

10.00 8.00 6.00 4.00 2.00 0.00 Ground

Basement

Ground

Fruit flavored

Regular

Fig. 5. BTEX concentration in waterpipe cafés according to type of smoked tobacco and the floor level.

4. Discussion 4.1. BTEX concentrations in the café indoor environments Although the air sampling campaign in our study last for 50 min, the average concentrations measured for this time span were assumed to represent the pollutant levels for a working shift. BTEX concentrations in the selected waterpipe cafés were quite high. The mean benzene concentration (4.96 ± 2.63 mg/m3) was much higher than the TWA exposure limits recommended by national and international organizations (Table 1). It was also higher than the STEL values recommended by NIOSH; implying unsafe condition for employees as well as the customers spending a short period of time (i.e., ≥15 min) in the cafés, even if they do not practice waterpipe smoking. Several studies monitoring BTEX concentrations in atmospheric ambient air reported quite low levels of these compounds. Ambient air concentration of 63 ppb (0.2 mg/m3) was reported for atmospheric benzene in Tehran, Iran (Fazlzadeh Davil et al., 2012) and up to 23.8 ppb (0.076 mg/m3) for Adelaide, Australia (Hinwood et al., 2007). In case of indoor air pollution, significantly increasing concentration of target pollutants was observed due to waterpipe smoking, for instance benzene concentration increased from 0.11 (for non-smoking room) to 15 μg/m3 during a 4 h WTS session. It is notable that the growth rate of the total VOC level (from 730 to 1800 μg/m3) was significantly lower than the rate observed for benzene concentrations (Fromme et al., 2009). The only study monitoring BTEX compounds in the breath of waterpipe smokers in Hamadan (Iran) found quite similar levels for benzene (i.e., 4.8 mg/m3). However, TEX levels were much higher than those found in our work (Samarghandi et al., 2014). Typical outdoor BTEX concentrations are much lower than the levels found in cafés' indoor ambient air, therefore, the penetration of atmospheric pollution to indoor environments is not relevant in our case; but waterpipe cafés themselves might be important sources of VOC emission into the atmospheric ambient air at the local scale.

Table 4 Cancer risk and hazard quotient (HQ) related to BTEX concentration in waterpipe cafés. Risk

HQ

Total Benzene Toluene Ethylbenzene Xylene

4314 × 10 – – –

Fruit −6

Regular −6

5087 × 10 – – –

1401 × 10 – – –

Total −6

Fruit

Regular

43.50 51.30 14.13 0.26 0.29 0.16 1.15 1.32 0.49 17.32 21.30 2.33

The unit HQ and cancer risk values respectively are: HQ b 1; cancer risk b1 × 10−6.

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4.2. Sources and factors influencing BTEX concentrations Among the different variables of possible impact on indoor air quality, the type of smoked tobacco, the floor at which the café was located, and the operating mechanical general ventilation were studied. The tobaccos used in preparation of waterpipe are presumably the main sources of BTEX emission for the indoor ambient air of the cafés (Markowicz et al., 2014). Different types and amount of pollutants are emitted by WTS as compared to cigarette smoke. Greater exposure to benzene and high molecular weight PAH, but less exposure to nitrosamines, 1,3-butadiene, acrolein, acrylonitrile, propylene oxide, ethylene oxide, and low molecular weight PAHs were reported for waterpipe smoking as compared to cigarette smoking (Jacob et al., 2013). Different emission rates of air pollutants from different tobacco smokes were also observed in previous studies (Baker and Proctor, 1990; Eissenberg and Shihadeh, 2009). Emission factors of 630, 1020, 157, 467 and 104 ng/mg were reported respectively for benzene, toluene, ethylbenzene, m-p-xylene, and o-xylene for cigarette tobacco (Daisey et al., 1997). The type of smoked tobacco was found to be the most influencing factor for BTEX concentration in this study (MSES of 0.44). Significantly higher BTEX concentrations found in indoor air of the cafés serving fruit flavored tobacco (relative to regular tobacco) agreed well with the results obtained from direct measurement of BTEX concentrations in main stream of the waterpipes. Such differences were also observed in CO concentrations of fruit flavored comparing to regular tobacco serving cafés in our previous work (Fazlzadeh et al., in press). This suggests fruit flavored tobacco as a main source of BTEX emission in waterpipe cafés. Path analysis revealed the floor in which the café was located as the second important factor affecting BTEX concentrations (MSES of 0.28 vs. 0.44). This factor is related to the significantly lower concentrations of BTEX found in fruit flavored tobacco serving cafés located on ground floor vs. those located in the basement. Although the effect of the ventilation system on BTEX concentrations was not significant in the cafés involving a similar tobacco usage, it appeared that the location of the cafés greatly influenced the natural ventilation rates. Basements usually are confined places with no perforated walls and very restricted natural ventilation. It was reported a good natural ventilation to provide adequate air exchange rates in houses (Staepels et al., 2013). However, the basements are more favored by owners of the waterpipe cafés, especially in city center where rent fees for ground floor settings are quite expensive. 4.3. Risk assessment Although the average concentrations of toluene, ethylbenzene and xylenes were lower than the national occupational exposure limits, however, most of the cafés run for 12 h per day and 7 days per week. Under this condition, the exposure risks of employees could not be negligible. Risk assessment results using the parameters presented in Table 2 showed ethylbenzene (HQ = 1.15) and xylenes (HQ = 17.32) to have high hazard potential to human health. HQ values larger than 1 represent unacceptable exposure conditions with high chronic noncancer risks for the target organs (McKenzie et al., 2012; Salvi, 2014). The HQ values for individual target pollutants (except toluene) were N1 and the hazard index (HI) for all BTEX compounds (sum of the individual HQs) is estimated at 62.23, which corresponds to an unacceptably high risk. Thus, much increase in indoor air exchange rate is required to decrease BTEX concentration to a safe and healthy level. The overall cancer risk obtained for benzene (4314 × 10− 6) exceeded the acceptable risk value of 1 × 10−6 (Guo et al., 2004; Kelly and Cardon, 1991; USEPA, 2007) implying a significant risk for the employees of such cafés. Comparing to regular tobacco serving cafés, the cancer risk of those serving fruit flavored tobacco is much higher (i.e., 5087 × 10− 6 vs. 1401 × 10− 6). It is important to note that there might be other carcinogenic compounds such as PAHs, naphthylamines,

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and aldehydes in indoor air of waterpipe serving cafés (Schubert et al., 2011; Sepetdjian et al., 2008; Shihadeh and Saleh, 2005) that were not included in our risk assessment process. High concentrations of BTEX found in main stream of flavored tobacco smoke implies that the large number of young people who usually favor smoking fruit flavored waterpipe is at high risk of adverse health effects. A very recent study reported a significant increase in smokers' urinary S-phenylmercapturic acid, a metabolite of benzene, after a waterpipe smoking event (Kassem et al., 2014). 5. Conclusion Benzene concentrations in the indoor air of selected waterpipe cafés are considerably higher than the OEL-TWA level for occupational exposure recommended by the Iran Ministry of Health. Long term exposure to the measured BTEX concentrations could significantly increase the cancer risk and chronic non-cancer hazards for café workers. Tobacco smoke is the main source of indoor BTEX concentrations in the waterpipe cafés. Moreover, people smoking fruit flavored waterpipe tobacco are more prone to be exposed to higher concentrations of BTEX compounds and consequently are at increased risk of cancer and chronic non-cancer hazards. Poorly designed general ventilation systems operated in majority of cafés located on basements were unable to reduce BTEX concentration to safe levels. Consequently, the basements are not recommended for running waterpipe cafés. More detailed studies are recommended to characterize indoor air quality and to elucidate other variables influencing indoor air pollution of waterpipe cafés. Acknowledgments The authors are grateful for the financial support of Ardabil University of Medical Sciences for this project (grant number 91397). Prof. JeanFrançois Gal, University Nice Sophia Antipolis, France, is gratefully acknowledged for his corrections and suggestions. References Agaku, I.T., Filippidis, F.T., Vardavas, C.I., Odukoya, O.O., Awopegba, A.J., Ayo-Yusuf, O.A., Connolly, G.N., 2014. Poly-tobacco use among adults in 44 countries during 2008–2012: evidence for an integrative and comprehensive approach in tobacco control. Drug Alcohol Depend. 139, 60–70. Akl, E.A., Gaddam, S., Gunukula, S.K., Honeine, R., Jaoude, P.A., Irani, J., 2010. The effects of waterpipe tobacco smoking on health outcomes: a systematic review. Int. J. Epidemiol. 39, 834–857. Akl, E.A., Gunukula, S.K., Aleem, S., Obeid, R., Jaoude, P.A., Honeine, R., Irani, J., 2011. The prevalence of waterpipe tobacco smoking among the general and specific populations: a systematic review. BMC Public Health 11, 244. Al-Amad, S., Awad, M., Nimri, O., 2014. Oi0221 water-pipe smoking is significantly associated with earlier development of oral cancer. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 117, e383. Baker, R.R., Proctor, C.J., 1990. The origins and properties of environmental tobacco smoke. Environ. Int. 16, 231–245. Baker, E.L., Smith, T.J., Landrigan, P.J., 1985. The neurotoxicity of industrial solvents: a review of the literature. Am. J. Ind. Med. 8, 207–217. Boskabady, M.H., Farhang, L., Mahmoodinia, M., Boskabady, M., Heydari, G.R., 2014. Prevalence of water pipe smoking in the city of Mashhad (north east of Iran) and its effect on respiratory symptoms and pulmonary function tests. Lung India Off. Organ Indian Chest Soc. 31, 237. Caselli, M., de Gennaro, G., Marzocca, A., Trizio, L., Tutino, M., 2010. Assessment of the impact of the vehicular traffic on BTEX concentration in ring roads in urban areas of Bari (Italy). Chemosphere 81, 306–311. CDC (Centers for Disease Control and Prevention), Prevention, 2013. Tobacco product use among middle and high school students—United States, 2011 and 2012. Morb. Mortal. Wkly Rep. 62, 893–897. Czoli, C.D., Leatherdale, S.T., Rynard, V., 2013. Bidi and hookah use among Canadian youth: findings from the 2010 Canadian youth smoking survey. Prev. Chronic Dis. 10. Daisey, J., Mahanama, K., Hodgson, A., 1997. Toxic volatile organic compounds in simulated environmental tobacco smoke: emission factors for exposure assessment. J. Expo. Anal. Environ. Epidemiol. 8, 313–334. Davil, M.F., Naddafi, K., Rostami, R., Zarei, A., Feizizadeh, M., 2013. A mathematical model for predicting 24-h variations of BTEX concentrations in ambient air of Tehran. Int. J. Environ. Health Eng. 2, 4. Dillon, K.A., Chase, R.A., 2010. Secondhand smoke exposure, awareness, and prevention among African-born women. Am. J. Prev. Med. 39, S37–43.

Eissenberg, T., Shihadeh, A., 2009. Waterpipe tobacco and cigarette smoking: direct comparison of toxicant exposure. Am. J. Prev. Med. 37, 518–523. EPA, 2005. Reference Doses for Petroleum Mixtures. EPA, Seattle, Washington. Fazlzadeh Davil, M., Rostami, R., Zarei, A., Feizizadeh, M., Mahdavi, M., Mohammadi, A., Eekandari, D., 2012. A survey of 24 hour variations of BTEX concentration in the ambient air of Tehran. J. Babol Univ. Med. Sci. (JBUMS) 14, 50–55. Fazlzadeh, M., Rostami, R., Hazrati, S., Rastgu, A., 2015. Concentrations of carbon monoxide in indoor and outdoor air of Ghalyun cafés. Atmos. Pollut. Res. (in press). Fromme, H., Dietrich, S., Heitmann, D., Dressel, H., Diemer, J., Schulz, T., Jorres, R.A., Berlin, K., Volkel, W., 2009. Indoor air contamination during a waterpipe (narghile) smoking session. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 47, 1636–1641. Guo, H., Lee, S.C., Chan, L.Y., Li, W.M., 2004. Risk assessment of exposure to volatile organic compounds in different indoor environments. Environ. Res. 94, 57–66. 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. Hinwood, A.L., Rodriguez, C., Runnion, T., Farrar, D., Murray, F., Horton, A., Glass, D., Sheppeard, V., Edwards, J.W., Denison, L., Whitworth, T., Eiser, C., Bulsara, M., Gillett, R.W., Powell, J., Lawson, S., Weeks, I., Galbally, I., 2007. Risk factors for increased BTEX exposure in four Australian cities. Chemosphere 66, 533–541. Hoskins, J.A., 2011. Health effects due to indoor air pollution. Survival and Sustainability. Springer, pp. 665–676. HSE, 2011. Eh40/2005 Workplace Exposure Limits. Health and Safety Executive, London. IARC, 1999. Monographs on the evaluation of carcinogenic risks to humans vol 71(II), pp. 401–432 (Lyon). Islamic Parliament Research Center (IPRC), 2006. Comprehensive national law on controlling smoking. Available at: http://rc.majlis.ir/fa/law/show/97817 ([in Farsi], Accessed on 30/03/2015). Jacob, P., Raddaha, A.H.A., Dempsey, D., Havel, C., Peng, M., Yu, L., Benowitz, N.L., 2013. Comparison of nicotine and carcinogen exposure with water pipe and cigarette smoking. Cancer Epidemiol. Biomarkers Prev. 22, 765–772. Kassem, N.O., Kassem, N.O., Jackson, S.R., Liles, S., Daffa, R.M., Zarth, A.T., Younis, M.A., Carmella, S.G., Hofstetter, C.R., Chatfield, D.A., 2014. Benzene uptake in hookah smokers and non-smokers attending hookah social events: regulatory implications. Cancer Epidemiol. Biomarkers Prev. 23, 2793–2809. Kelly, K., Cardon, N., 1991. The myth of 10-6 as a definition of acceptable risk. 84th Annual Meeting and Exhibition of the Air and Waste Management Association. Vancouver, B.C., Canada. Klepeis, N.E., Nelson, W.C., Ott, W.R., Robinson, J.P., Tsang, A.M., Switzer, P., Behar, J.V., Hern, S.C., Engelmann, W.H., 2001. The national human activity pattern survey (NHAPS): a resource for assessing exposure to environmental pollutants. J. Expo. Anal. Environ. Epidemiol. 11, 231–252. Knishkowy, B., Amitai, Y., 2005. Water-pipe (narghile) smoking: an emerging health risk behavior. Pediatrics 116, e113–e119. Liu, J., Mu, Y., Zhang, Y., Zhang, Z., Wang, X., Liu, Y., Sun, Z., 2009. Atmospheric levels of BTEX compounds during the 2008 Olympic Games in the urban area of Beijing. Sci. Total Environ. 408, 109–116. Majumdar, D., Mukherjeea, A., Sen, S., 2011. BTEX in ambient air of a metropolitan city. J. Environ. Prot. 2, 11. 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. Maziak, W., Taleb, Z.B., Bahelah, R., Islam, F., Jaber, R., Auf, R., Salloum, R.G., 2015. The global epidemiology of waterpipe smoking. Tob. Control 24, i3–i12. McKelvey, K.L., Wilcox, M.L., Madhivanan, P., Mzayek, F., Khader, Y.S., Maziak, W., 2013. Time trends of cigarette and waterpipe smoking among a cohort of school children in Irbid, Jordan, 2008–11. Eur. J. Public Health 23, 862–867. McKenzie, L.M., Witter, R.Z., Newman, L.S., Adgate, J.L., 2012. Human health risk assessment of air emissions from development of unconventional natural gas resources. Sci. Total Environ. 424, 79–87. Mehlman, M.A., 1990. Dangerous properties of petroleum-refining products: carcinogenicity of motor fuels (gasoline). Teratog. Carcinog. Mutagen. 10, 399–408. MHMEI, 2012. Occupational Exposure Limits. Center EOH, Tehran. Moh'd Al-Mulla, A., Abdou Helmy, S., Al-Lawati, J., Al Nasser, S., Ali Abdel Rahman, S., Almutawa, A., Abi Saab, B., Al-Bedah, A.M., Al-Rabeah, A.M., Ali Bahaj, A., 2008. Prevalence of tobacco use among students aged 13–15 years in Health Ministers' Council/Gulf Cooperation Council Member States, 2001–2004. J. School Health 78, 337–343. NIOSH, 2003. NIOSH Manual of Analytical Methods (NMAM). fourth ed. Hydrocarbons, Aromatic vol. 1501. Centers for Disease Control and Prevention, 1600 Clifton Rd. Atlanta, GA 30329-4027, USA. Niosh, 2012. NIOSH Pocket Guide to Chemical Hazards. Books Express Publishing, 1600 Clifton Rd. Atlanta, GA 30333, USA. Niri, V., Mathers, J., Musteata, M., Lem, S., Pawliszyn, J., 2009. Monitoring BTEX and aldehydes in car exhaust from a gasoline engine during the use of different chemical cleaners by solid phase microextraction-gas chromatography. Water Air Soil Pollut. 204, 205–213. OSHA, 2014. Occupational Exposure Limits. Occupational Safety & Health Administration, 200 Constitution Ave., NW, Washington, DC 20210. Rezazadeh Azari, M., Naghavi Konjin, Z., Zayeri, F., Salehpour, S., Seyedi, M., 2011. Occupational exposure of petroleum depot workers to BTEX compounds. Int. J. Occup. Environ. Med. 3. Salvi, S., 2014. Tobacco smoking and environmental risk factors for chronic obstructive pulmonary disease. Clin. Chest Med. 35, 17–27.

S. Hazrati et al. / Science of the Total Environment 524–525 (2015) 347–353 Samarghandi, M., Mehralipour, J., Shabanlo, A., Rahimpoor, R., 2014. The evaluation of personal exposure to BTEX compounds in the traditional restaurants in Hamadan in 2013. Sci. J. Hamadan Univ. Med. Sci. 21, 231–239. Schubert, J., Hahn, J., Dettbarn, G., Seidel, A., Luch, A., Schulz, T.G., 2011. Mainstream smoke of the waterpipe: does this environmental matrix reveal as significant source of toxic compounds? Toxicol. Lett. 205, 279–284. Schubert, J., Müller, F.D., Schmidt, R., Luch, A., Schulz, T.G., 2014. Waterpipe smoke: source of toxic and carcinogenic VOCs, phenols and heavy metals? Arch. Toxicol. 1–11. Sepetdjian, E., Shihadeh, A., Saliba, N.A., 2008. Measurement of 16 polycyclic aromatic hydrocarbons in narghile waterpipe tobacco smoke. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 46, 1582–1590. Shihadeh, A., Saleh, R., 2005. Polycyclic aromatic hydrocarbons, carbon monoxide, “tar”, and nicotine in the mainstream smoke aerosol of the narghile water pipe. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 43, 655–661. Singh, H.B., Salas, L., Viezee, W., Sitton, B., Ferek, R., 1992. Measurement of volatile organic chemicals at selected sites in California. Atmos. Environ. Part A Gen. Top. 26, 2929–2946. Staepels, L., Verbeeck, G., Roels, S., Van Gelder, L., Bauwens, G., 2013. Do ventilation systems accomplish the necessary indoor air quality in low energy houses. Clima vol. 2013, p. 11th.

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Sturaro, A., Rella, R., Parvoli, G., Ferrara, D., 2010. Long-term phenol, cresols and BTEX monitoring in urban air. Environ. Monit. Assess. 164, 93–100. Toor, R., Yee, C., Peart, T., Serrano, J., Buka, I., Wong, J., Johansson, A., De Leon-Rosales, S.P., Osornio, A., Castro, M., 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. USEPA (United States Environmental Protection Agency), 2007. Reference concentration for chronic inhalation exposure. Available at: http://www.epa.gov/iris. Warren, C.W., Lea, V., Lee, J., Jones, N.R., Asma, S., McKenna, M., 2009. Change in tobacco use among 13–15 year olds between 1999 and 2008: findings from the global youth tobacco survey. Glob. Health Promot. 16, 38–90. WHO, 2000. Air quality guidelines for Europe. second ed. WHO Regional Publications, European Series no. 91. WHO, Copenhagen. WHO, 2010. Who Guidelines for Indoor Air Quality: Selected Pollutants. WHO. Wong, O., 1995. Risk of acute myeloid leukaemia and multiple myeloma in workers exposed to benzene. Occup. Environ. Med. 52, 380–384.