1 PM2.5 as a marker of exposure to tobacco smoke and other sources of 2 particulate matter in , 3

4 Christopher A. Loffredo,1 Yitao Tang,1 Mohamed Momen,2 Kepher Makambi,1 5 Ghada Nasr Radwan,3 Aisha Aboul-Foutoh2 6 7

8 1 Georgetown University, Washington DC, USA

9 2 Ain Shams University, Cairo, Egypt

10 3 Cairo University, Cairo, Egypt 11 12 13 Send correspondence to: 14 Dr. Christopher Loffedo, Georgetown University, 3970 Reservoir Rd NW, 15 Washington DC 20057, 202-687-3758 (phone) 202-687-0313 (fax), 16 [email protected] 17 18 Authors’ emails: 19 Christopher A. Loffredo [email protected] 20 Yitao Tang [email protected] 21 Mohamed Momen [email protected] 22 Kepher Makambi [email protected] 23 Ghada Nasr Radwan [email protected] 24 Aisha Aboul-Foutoh [email protected] 25 26 27 28 29

30 31 PM2.5 and waterpipe smoking in Egypt

32 ABSTRACT

33 Setting: Cairo and Giza governorates of Egypt

34 Objective: Particulate matter under 2.5 microns in diameter (PM2.5) arises

35 from diverse sources, including tobacco smoke from cigarettes and

36 waterpipes, and is recognized as a cause of acute and chronic morbidity and

37 mortality. Our study aimed to measure PM2.5 in workplaces with different

38 intensities of smoking and varying levels of smoking restrictions

39 Design: We conducted an air sampling study to measure PM2.5 levels in a

40 convenience sample of indoor and outdoor venues in 2005-6.

41 Results: 3,295 individual measurements were collected at 96 venues with a

42 calibrated SidePak instrument. Compared to indoor venues where tobacco

3 43 smoking was banned (PM2.5 levels of 72-81ug/m ), places offering waterpipes

44 to patrons of cafes (478 ug/m3) and tents (612 ug/m3) had much

45 higher concentrations, as did venues such as public buildings with poor

46 enforcement of smoking restrictions (range: 171-704 ug/m3). Both the number

47 of waterpipe smokers and the number of cigarette smokers observed at each

48 venue contributed significantly to the overall burden of PM2.5.

49 Conclusion: Such data will support smoke-free policies and programs aimed

50 at reducing environmental tobacco exposure specifically and improving air

51 quality generally, and will provide a baseline for monitoring the impact of

52 tobacco control policies.

53 Key words: particulate matter, indoor air quality, smoking

2 PM2.5 and waterpipe smoking in Egypt

54 BACKGROUND

55 Atmospheric particulate matter with diameter <= 2.5 microns (PM2.5) is

56 generated from anthropogenic sources such as vehicle exhaust and tobacco

57 smoke and is composed of diverse compounds and elements including

58 organic matter, sulfate, ammonium, nitrate, and various metals (e.g. Cu, Cr,

59 Mn, As, Pb and Zn).1,2 The main route of human exposure results in

60 absorption into the bloodstream through the respiratory tract. Studies show

61 that variations in the level of PM2.5 in air is associated with changes in the

62 incidence of all-cause mortality3,4 and with cause-specific hospital

5 6 63 admissions, especially for cardiovascular and respiratory diseases. PM2.5 is a

64 major component of both cigarette smoke and environmental tobacco smoke

65 (ETS), both of which are associated with cancer and other chronic diseases.

66 The U.S. Environmental Protection Agency cited over 80 epidemiologic

67 studies in creating an initial particulate air pollution standard in 1997 to protect

68 public health and more recently updated the current standards to 12 μg/m3 as

3 69 the average annual level of PM2.5 exposure, with 35 μg/m as the upper limit for

70 24-hour exposure.7,8

71

72 Although PM2.5 levels have been well characterized in relation to cigarette

73 smoking, relatively little is known about the contribution of waterpipe (or

74 hookah) smoking to PM2.5, particularly in countries in North Africa and the

75 Middle East, where waterpipe smoking represents a major form of tobacco

76 use.9 Exposure to ETS from waterpipes, which are typically smoked in social

77 settings including cafes, bars, and restaurants, may be a particular concern

78 for workers in such establishments, who often have low levels of protection

3 PM2.5 and waterpipe smoking in Egypt

79 due to inadequate smoking regulations in some countries.10-16 Indeed, the

80 World Health Organization’s Framework Convention on Tobacco Control calls

81 on governments to “protect all persons from exposure to tobacco smoke,”

82 rather than just specific populations such as children or pregnant women. This

83 protection should be extended, according to Article 8, “in indoor workplaces,

84 public transport, indoor public places and…other public places.”17

85

86 Limited laboratory-based testing suggests that the levels of particulate matter

87 released from waterpipes under controlled conditions are comparable to those

88 from cigarettes; in one such experimental protocol, a waterpipe smoking

89 session of 30 minutes generated PM emissions similar in magnitude to a 90 91 single cigarette smoked for 10 minutes.18 In contrast, there is scant data

92 reporting measurements of PM2.5 under natural exposure conditions of

93 waterpipe smoking, and the contribution of such emissions to the overall

94 societal burden of PM2.5 has yet to be established. Therefore, the purpose of

95 our study was to measure PM2.5 in a sample of workplaces in Cairo, Egypt,

96 characterized by different intensities of waterpipe smoking and varying levels

97 of indoor smoking restrictions. Such data will support more effective smoke-

98 free policies and programs aimed at reducing ETS exposure and will provide

99 a baseline for monitoring the impact of tobacco control policies.

100

101

4 PM2.5 and waterpipe smoking in Egypt

102 METHODS

103 This study was approved by the Institutional Review Boards of the University

104 of Maryland, Ain Shams University, and the Ministry of Health in Egypt.

105 Venues sampled

106 A convenience sample of hospitality settings (waterpipe cafes, restaurants,

107 and Ramadan tents) was selected for PM2.5 monitoring between October 12,

108 2005 and January 31, 2006, in the Cairo and Giza governorates of Egypt.

109 Waterpipe cafes are establishments offering food, drinks, and waterpipes to

110 patrons, while Ramadan tents are similar places where people gather in the

111 evenings after daily fasting during the month of Ramadan. PM2.5 levels were

112 also examined during the same time period for a cross section of other public

113 places with varying degrees of indoor air restrictions: Cairo International

114 Airport, a municipal court building, a faculty office building at Ain Shams

115 University, and governmental offices (where tobacco smoking is officially

116 restricted but not well enforced); in transport vehicles such as buses and taxis

117 (where tobacco smoking is restricted but enforcement is at the driver’s

118 discretion); in the open air of the center of a semi-rural village within Giza

119 governorate; and sidewalks along major streets as well as in the center of the

120 crosswalk. A mosque and our Cairo study office (Egyptian Smoking

121 Prevention Research Initiative, or ESPRI) were also included in the air

122 sampling protocol, as they were among the only places in the regions where

123 tobacco smoking was absolutely not allowed. The hospitality settings were

124 sampled between 6 PM and 3 AM, and in all other settings the sampling was

125 carried out between 8 AM and 2 PM.

126

5 PM2.5 and waterpipe smoking in Egypt

127

128 Measurements

129 Each sampling site was tested for a minimum of 60 minutes. A TSI SidePak

130 AM510 Personal Aerosol Monitor (TSI, Inc., St. Paul, MN) was used to

131 sample and record the levels of suspended particles in the air. Sampling was

132 performed discreetly in order to avoid disturbing the occupants’ normal

133 behavior; for this reason the device was concealed within a backpack, with

134 the inlet tube protruding just far enough to allow air sampling. The SidePak

135 uses a built-in sampling pump to draw air through the device where the

136 particulate matter in the air scatters the light from a laser to assess the real-

137 time concentration of particles smaller than 2.5µm in micrograms per cubic

138 meter, or PM2.5. The SidePak was calibrated against a laser photometer, which

139 had been previously calibrated and used in similar studies. In addition, the

140 SidePak was zero-calibrated prior to each use by attaching a HEPA filter

141 according to the manufacturer’s specifications. For each indoor venue, the

142 first and last minute of data were removed from the statistical analysis

143 because they are strongly influenced by outdoor and entryway air. The

144 remaining data points were averaged to provide a mean PM2.5 concentration

145 within the venue. After air monitoring, the SidePak was immediately

146 connected to a PC, and the data were downloaded using TrakPro software

147 version 3.40. Observational data were entered into an Excel spreadsheet.

148

149 For the hospitality venues only, several additional variables were measured.

150 The number of patrons and the number of burning cigarettes and waterpipes

151 observed were recorded every 15 minutes during the visit. These

6 PM2.5 and waterpipe smoking in Egypt

152 observations were averaged over the time inside the venue to determine the

153 average number of people on the premises and the average number of

154 burning cigarettes and waterpipes. A sonic measure (Zircon Corporation,

155 Campbell, CA) was used to measure room dimensions and hence the volume

156 of each of the hospitality venues. When using the sonic measure to calculate

157 room dimensions was not possible, room measurements were made through

158 visual estimation.

159

160 For estimation of occupational exposure to PM2.5 in the hospitality settings, an

161 8 hour time weighted average was calculated. To derive the 8 hour time

162 weighted average from more than one sample of a shorter period, the

163 following equation was used: {(C1 x T1) + (C2 x T2) ... + (Cn x Tn)} / 8, where

164 C is the exposure level, T is the time for that exposure, and n is the last of the

165 sequential sampling periods.

166

167 Statistical analysis

168 PM2.5 measurements were log2-transformed so that their frequency distribution

169 achieved a normal distribution. We examined the differences in means of

170 PM2.5 levels in different venues by using ANOVA. Dunnett's t-test was used to

171 compare the means between venues, using the ESPRI office as the common

172 comparison venue. Duncan’s multiple range test was used to stratify venues

173 into statistically similar groupings of PM2.5 levels. The contribution of cigarettes

174 and waterpipes to each venue’s mean PM2.5 was tested by two-way ANOVA;

175 we also evaluated the interaction term between these two factors. Finally,

176 quadratic terms for cigarettes and waterpipes were introduced to account for

7 PM2.5 and waterpipe smoking in Egypt

177 any non-linear effects. SAS version 9.3 (Cary, North Carolina, USA) was used

178 for the statistical analysis.

179

180

8 PM2.5 and waterpipe smoking in Egypt

181 RESULTS

182 All venues

183 A total of 3,295 measurements were analyzed in this study (Table 1),

184 including 25 at Cairo International Airport, 42 in court buildings, 780 in cafes,

185 240 in restaurants, 449 in Ramadan tents, and 21 in a mosque, among a total

186 of 14 categories of venues. The municipal court, with air measurements taken

187 in the public waiting area and inside the court itself, had the highest mean

3 188 level of PM2.5 (704.3 µg/m ), followed by the Ramadan tents (612.5) and cafes

189 (478.4); in comparison, the smoke-free ESPRI offices and mosque had the

190 lowest levels (72 and 81, respectively). Venues where smoking is nominally

191 restricted but not well enforced, such as the airport, government offices, and

192 public transport vehicles, were intermediate in the measured PM2.5 levels.

193 Outdoor air measurements were relatively high (range 236-401 µg/m3),

194 reflecting the diverse sources of particulate matter in the urban environment.

195 The overall one-way ANOVA F-test on these log2-transformed raw readings

196 was highly significant (F=150, P<0.0001), suggesting a strong relationship

197 between the specific type of venue and PM2.5 levels. Comparing venues using

198 Dunnett's t-test showed that the mean levels of every venue except the

199 mosque were significantly higher than in the control venue (ESPRI office),

200 where a no smoking policy was strictly enforced.

201

202 Duncan’s multiple range test indicated the following groupings of venues

203 according to similarities in their PM2.5 levels (from highest to lowest

204 concentrations): (1) the court building, Ramadan tents, and cafes; (2) traffic

205 and transportation vehicles; (3) restaurants, university buildings,

9 PM2.5 and waterpipe smoking in Egypt

206 governmental offices, and sidewalks; (4) airport and ambient air; (5) the rural

207 village center; and (6) the mosque and the ESPRI office.

208

209 A two-way ANOVA model examining the impacts of cigarettes and waterpipes

210 showed that both types of tobacco smoking contributed significantly (F=88.58,

211 P<0.0001, and F=12.99, P<0.001, respectively) to the PM2.5 levels in the

212 combined group of Ramadan tents and cafes (data not shown). The quadratic

213 term for cigarette smoking improved the fit of the model to our data,

214 suggesting a non-linear acceleration in PM2.5 levels with increasing numbers of

215 cigarettes in a venue.

216

217 Hospitality settings

218 PM2.5 levels were measured in 25 hospitality settings (15 waterpipe cafes, 5

219 Ramadan tents and 5 restaurants). Tobacco smoking was observed in all of

220 them, with waterpipes predominating: the mean number of burning waterpipes

221 was 19 in the cafes and 16 in the tents, compared to an average of 8 burning

222 cigarettes in the cafes and 7 in the tents (data not shown). None of the

223 restaurants had smoking patrons present during sampling. Most of the

224 waterpipe cafes (11 of 15) were outdoor establishments and the remainder

225 were indoor establishments. All tents and restaurants were enclosed indoor

226 spaces, each with a roof and walls. No waterpipe smoking was observed in

227 the airport, court, university, and governmental buildings, although cigarette

228 smoking was observed in each of those venues. No smoking of any kind was

229 seen in the mosque or the ESPRI office.

230

10 PM2.5 and waterpipe smoking in Egypt

231 The average size of the sampled restaurants (128 m3 ) was smaller than that

232 of cafes and tents (235 m3 and 2878 m3 respectively). The average number of

233 patrons present during sampling in restaurants was 12 in comparison to an

234 average of 39 in the cafes and 42 in the Ramadan tents. The mean PM2.5

235 levels in open air waterpipe cafes was 478 µg/m3, ranging from 100 to 1313

236 (as shown in Table 1). However, the average PM2.5 level in Ramadan tents

237 was significantly higher - 613 µg/m3 ranging from 111 to 1723. The 8-hr time

238 weighted average of PM2.5 exposure level was significantly higher in Ramadan

239 tents when compared to cafes (141.6 µg/m3 versus 56.5 µg/m3, respectively).

3 240 Regarding the restaurants, the mean PM2.5 level was 213 µg/m (range: 105 to

3 241 865 µg/m ). Figure 1 shows the average levels of PM2.5 in each of the

242 selected venues.

243

244

11 PM2.5 and waterpipe smoking in Egypt

245 DISCUSSION 246 247 The results of this study demonstrate that venues that allowed tobacco

248 smoking, either explicitly (cafes and Ramadan tents) or by poor enforcement

249 of indoor smoking restrictions (courts and other governmental buildings) had

250 on average much higher PM2.5 levels compared to smoke-free venues (the

251 mosque and ESPRI office) and places where no smoking was observed

252 during the study (restaurants). Although both types of smokers were observed

253 during the sampling sessions, waterpipe smoking predominated over cigarette

254 smoking in the cafes and Ramadan tents. According to the indoor Air Quality

255 Index, which was established by the EPA, the indoor air quality as measured

7 256 by PM2.5 in these venues is considered very unhealthy. Our study also

257 suggests that PM2.5 levels were generally higher in venues in which waterpipe

258 smoking was observed compared to those in which only cigarette smoking

259 was observed, e.g. in transport vehicles and governmental offices, where it

260 would not be convenient for a smoker to bring his or her own waterpipe.

261

262 The findings of this study are generally consistent with previous studies.

263 Recent studies from the Middle East region that used comparable study

264 designs to ours have documented similarly elevated levels of one to two

265 orders of magnitude in venues such as waterpipe cafes compared to those

266 where tobacco smoking was banned.16, 19, 20 In contrast, other studies have

267 reported differences between venues that were slightly smaller than those in

268 our study. For example, recent air monitoring in seven cities in the U.S. found

269 PM2.5 to be 82% lower in smoke-free hospitality settings compared to venues

270 where smoking was permitted.21 Another study found a similar 90% decline in

12 PM2.5 and waterpipe smoking in Egypt

271 PM2.5 levels in 8 hospitality venues in Delaware after smoking was prohibited

272 there by a state law.22 One reason why our study may have observed smaller

273 differences between smoke-free and non-smoke-free sites is the larger size of

274 the sampled rooms and lower active smoker densities in our study, which

275 would tend to dilute the PM2.5 concentration. Even in municipalities in which

276 cigarette smoking in cafes, bars, and restaurants has been banned, regulatory

277 loopholes have resulted in a flourishing trend of waterpipe smoking in such

278 venues, e.g. Baltimore and New York City, where investigators have recently

279 measured unacceptably high levels of PM2.5, CO, and other pollutants

280 released from waterpipes.23,24

281

282 Several previous studies have assessed improvements in health associated

283 with indoor smoking bans. For example, one study found that respiratory

284 health improved rapidly in a sample of bartenders after a statewide smoke-

285 free workplace law was implemented in California,10 and another study

286 reported a 40% reduction in acute myocardial infarctions admitted to a

287 regional hospital during the first 6 months that a local smoke-free ordinance

288 was in effect.25 While our study did not assess health effects, it does provide a

289 robust baseline measure of PM2.5 exposure levels experienced by local

290 hospitality workers and patrons, against which future reductions in exposure

291 can be compared when their worksites become smoke-free.

292

293 PM2.5 measurements have been shown to correlate well with levels of ETS

26 294 from cigarette smoking. However, PM2.5 is only one aspect of overall air

295 quality. Other factors such as meteorologic variables and pollutants such as

13 PM2.5 and waterpipe smoking in Egypt

296 NO3, SO4, O3, NO2, and CO must also be taken into account.4,27 In addition,

297 the fact that we observed elevated levels of PM2.5 at indoor venues where

298 smoking is prohibited suggests that other sources, including the transport of

299 outdoor pollution due to factory emissions and vehicle exhaust,28-30 may have

300 contributed to the overall exposure burden. Biomass fuels for cooking,

301 heating, and lighting have also been reported to result in elevated particulate

302 levels.31-33

303

304 This study is subject to several limitations. The venues selected for air

305 measurements were a convenience sample and may not be representative of

306 all venues in Cairo and Giza. However, these venues were selected on the

307 basis of offering a wide range in terms of physical size, smoking restrictions,

308 indoor versus outdoor settings, and waterpipe availability. In addition, ETS is

309 not the only source of indoor particulate matter. While PM2.5 monitoring is not

310 specific for ETS, it is highly sensitive to it, as evidenced by the sharp elevation

311 in PM2.5 levels upon entering venues where smoking is present. Ambient

312 particle concentrations and traffic are additional sources of indoor particle

313 levels; however, PM2.5 levels were significantly higher in cafes and tents than

314 in outdoor air. In contrast to the instruments available at the time of the study,

315 current technology is capable of measuring smaller size particles, e.g. PM1.0 or

316 smaller, which may better reflect the exposures originating from cigarettes

317 and waterpipes.

318

14 PM2.5 and waterpipe smoking in Egypt

319 CONCLUSIONS

320 In summary, we sought to characterize levels of PM2.5 in diverse indoor and

321 outdoor venues in the Cairo metropolitan area. We took advantage of the

322 presence of waterpipe smoking in some venues to further explore the

323 contribution of this source of ETS to that of cigarette smoking, for which much

324 more information is available in the literature. The results suggest strongly

325 that waterpipe smoking can be a major contributor to both ETS and poor air

326 quality. Ongoing tobacco control efforts in such places need to address the

327 double burden of both types of tobacco smoking in planning for the

328 implementation and evaluation of strategies to reduce ETS exposure.

329

330

15 PM2.5 and waterpipe smoking in Egypt

331 COMPETING INTERESTS

332 The authors declare that they have no competing interests.

333 ACKNOWLEDGMENTS

334 The authors offer profound thanks to the late Dr. Mostafa Kamel Mohamed of

335 Ain Shams University, not only for conceiving and designing this study but

336 also for his leadership on tobacco control efforts in Egypt and the entire

337 region. This work was supported by grant number R01TW05944 from the

338 Fogarty International Center, U.S. National Institutes of Health and by grant

339 number 1000-024-388 from the program of Research for International

340 Tobacco Control of the International Development Research Centre. All of the

341 authors participated in writing the manuscript. Data collection was carried out

342 by MM; data analysis was performed by KM & YT; the fieldwork was

343 supervised by AAF; and study design was provided by CAL.

344

345 346

347

348

349

16 PM2.5 and waterpipe smoking in Egypt

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20 PM2.5 and waterpipe smoking in Egypt

3 453 Table 1. PM2.5 levels (µg/m ) in the sampled venues in Cairo and Giza, Egypt. 454 Venue (N) Number Mean STD Median IQR Maximum Minimum of air samples Hospitality settings Restaurants (5) 240 297.9 183.9 231 216 865 105 Cafes (15) 780 478.4 225.2 444 292 1313 100 Ramadan tents (5) 449 612.6 385.7 590 531 1723 111 Public venues Airport (1) 25 171.5 41.1 178 35 240 80 University buildings (1) 16 223.0 13.4 219 28 244 207 Courts (2) 42 704.3 316.6 743 488 1297 80 Transport vehicles (8) 200 346.4 217.0 320 149 1330 72 Government offices 112 321.4 345.8 204 109 1176 76 (3) Open air venues Ambient air (22) 485 236.8 134.4 209 222 730 47 Village center (1) 93 102.5 25.0 96 27 236 68 Sidewalks (3) 92 253.2 144.1 240 145 1003 74 Crosswalks (28) 631 401.3 260.0 366 367 1399 41 Smoking-restricted venues Mosque (1) 21 81.1 7.2 80 9 96 72 ESPRI office (1) 109 72.1 9.8 70 13 106 55 455 STD=standard deviation; IQR=Intequartile range

456

21 PM2.5 and waterpipe smoking in Egypt

Figure 1. PM2.5 levels at various sampling sites in Cairo, Egypt, 2005-6

1400

1200

1000

3 800 /m

Ug 600

400

200

0

ESPRI

Café 9 Café Café 1 Café 2 Café 3 Café 4 Café 5 Café 6 Café 7 Café 8 Café

Tent 1 Tent 1 Tent 3 Tent 4 Tent 5 Tent

Airport

Café 10 Café 11 Café 12 Café 13 Café 14 Café 15 Café

Court 1 Court 2 Court

Office 1 Office 2 Office 3 Office 4 Office Mosque

22