Abstract
Introduction:
Throughout the Eastern Mediterranean region, tobacco is used primarily in 2 forms: cigarette smoking and waterpipe smoking. Despite the fact that tobacco use is considered as a global public health threat, waterpipe smoking is reported to be growing in popularity, particularly among women. The objectives of this study are to determine the prevalence and patterns of cigarette, waterpipe, and passive smoking among pregnant women in Jordan, and to assess their perception of harmful effects of cigarette and waterpipe smoking.
Methods:
A total of 500 pregnant women were randomly recruited from maternity clinics in North and Middle of Jordan and surveyed regarding exposure to waterpipe tobacco and cigarette smoking.
Results:
The results showed that 7.9% of women were current cigarette smokers and 8.7% were current waterpipe smokers. About 82.4% of all women reported that they are exposed to cigarette smoke and 32.8% reported that they are exposed to waterpipe smoke. The most common place where women are exposed to cigarette and waterpipe smoke was their house (50.4% and 48.7%, respectively) followed by public places (31.4% and 21.4%, respectively). In addition, the husband was the main source for exposure to cigarette and waterpipe smoke (48.5% and 42.7%, respectively). Approximately, 74% of women believed that cigarette smoking is addictive, whereas only 55.1% reported that waterpipe smoking leads to addiction.
Conclusions:
Exposure of pregnant women to tobacco smoke is a public health problem in Jordan that requires immediate action.
Introduction
Tobacco smoke contains many toxicants that adversely influence human health. For example, chronic tobacco-smoke exposure causes cancers of the lung, oral cavity, esophagus, stomach, pancreas, liver, kidney, and bone marrow myeloid leukemia (International Agency for Research on Cancer, 2004). Moreover, smoking increases the risk for atherosclerosis and cardiovascular disease (Glantz & Parmley, 1995; Wells, 1994). More than five million deaths each year are attributed to tobacco use (WHO, 2009).
During pregnancy, exposure to tobacco smoke is associated with fetal growth restriction (Kayemba-Kay's et al., 2010; Robinson, Moore, Owens, & McMillen, 2000), spontaneous abortion (Nakamura et al., 2004), preterm delivery (Nabet, Ancel, Burguet, & Kaminski, 2005), and birth defects (Hackshaw, Rodeck, & Boniface, 2011). In addition, children born to smoker mothers are at risk of developing non-Hodgkin lymphoma (Klimentopoulou et al., 2011), cochlear dysfunction (Durante, Ibidi, Lotufo, & Carvallo, 2011), and being overweight or obese (Durmus et al., 2011; Ino, Shibuya, Saito, & Ohtani, 2011). Similar findings were reported using experimental animal models such as mice (Esposito, Horn, Greene, & Pisano, 2008; Ng, Silverstone, Lai, & Zelikoff, 2006). The mechanisms by which tobacco smoking might cause such hazardous health effects include decrease availability of oxygen for the fetus that is caused by nicotine and carbon monoxide (CO; Rogers, 2008) and the production of high amount of free radicals in the bodies of smokers and fetus (Chelchowska, Ambroszkiewicz, Gajewska, Laskowska-Klita, & Leibschang, 2011). These free radicals are remarkably reactive and randomly attack various cellular constituents as in the case of initiation of lipid peroxidation (Frei, Forte, Ames, & Cross, 1991), protein oxidation (Reznick et al., 1992), and DNA damage (Fahn et al., 1998).
Tobacco can be consumed in several different ways including cigarette, cigar, and waterpipe (a.k.a. hookah, narghile, or shisha). The popularity of waterpipe tobacco smoking (WTS) is growing in the eastern Mediterranean and throughout the world including the United States and other western countries, especially among youth (Azab et al., 2010; Eissenberg, Ward, Smith-Simone, & Maziak, 2008; Maziak et al., 2008; Primack et al., 2008; Warren et al., 2009). In Arab countries including Jordan, WTS is reported to be growing in popularity among women, perhaps because it is more socially accepted than cigarette smoking (Nakkash, Khalil, & Afifi, 2011; Rastam, Ward, Eissenberg, & Maziak, 2004). There is also a global misperception that the waterpipe filters the smoke, rendering it less harmful and less addictive than cigarette smoking (Ghafouri et al., 2011; e.g., Kandela, 2000; Kiter, Ucan, Ceylan, & Kilinc, 2000). Pregnant women who share these misperceptions might be at high risk of exposure to waterpipe smoke. For example, a study from Lebanon revealed that women knew little about the harmful constituents in waterpipe smoke and had many misconceptions regarding how waterpipe worked or how it can produce harm (Chaaya, Jabbour, El-Roueiheb, & Chemaitelly, 2004). Though few data addressing waterpipe smoke exposure in pregnant women are available, this study was conducted to determine the prevalence and patterns of cigarette, waterpipe, and passive smoking among pregnant women in Jordan, and to assess their perception of harmful effects of smoking. Results of this study will help to establish the base for interventions that target this population.
Methods
This cross-sectional study was conducted during April to August of 2011. Pregnant women (n = 585, 20–40 years of age) were invited from randomly selected maternity clinics (n = 6). Random selection was carried out based on locations of the clinics in major cities of Jordan, the economic status of the city area, based on data from the Department of Statistics of Jordan, and type of clinic (public vs. private). Participants were approached during their wait for regular pregnancy checkup. They were offered a description of the study and its goals and were asked to participate. Those who agreed (n = 500, 85.5%) were asked to provide written informed consent and to complete a self-administered questionnaire. The study was approved by the institutional review board of the Hashemite University. Those who did not agree to participate in the study were equally distributed among clinics, and among other demographic factors such as age and economic status.
The questionnaire was prepared by the research team, reviewed by several colleagues in the field, and then pilot tested with 50 subjects to examine clarity and comprehensibility. In addition, the participants in the pilot study were asked to give feedback about the questionnaire items, and this feedback informed the final version.
The survey was divided into several parts: (a) general information about women and pregnancy history, including age, income, education, family size etc.; (b) personal smoking information for both cigarettes and waterpipe such as age of initiation and frequency of use; (c) exposure to secondhand smoke, including sources, magnitude, and places of exposure; (d) beliefs and perceptions of the addictiveness of waterpipe and cigarette smoking; and (e) awareness of harmful effects of smoking on fetal health.
Current cigarette smoking was defined as smoking cigarettes in at least one day in the past month and current waterpipe smoking was defined as smoking waterpipe at least once in the past month. Dual smoking was defined as current cigarette smoking and current waterpipe smoking.
Statistical analysis was performed using SPSS® version 17 for windows (SPSS, Inc., Chicago, IL). Demographic data and categorical variables were summarized using frequency tables. The differences in the prevalence rates of cigarette and waterpipe smoking among women according to the sociodemographic and other characteristics were analyzed using Chi-square test (χ2 test). Binary logistic regression analysis was conducted to determine the factors associated with current cigarette and waterpipe smoking. A p value of less than .05 was considered statistically significant.
Results
Sociodemographic Characteristics
This study included a total of 500 pregnant women aged 17 years and above. About 21.1% of women aged 17–24.9 years, 30.8% aged 25–29.9 years, and 48.1% aged ≥30 years. More than two-thirds of women (69.3%) had a bachelor's degree or had received some form of higher education. The majority of women (76.6%) were living in urban areas and 23.4% in rural areas.
Pattern of Cigarette and Waterpipe Smoking
Of the total 500 pregnant women, 38.3% reported that they had ever smoked cigarettes and 35.6% had ever smoked waterpipe. About 17.2% of ever cigarette smokers and 7% of waterpipe smokers initiated smoking before they reached 18 years old. Overall, 7.9% of women were current cigarette smokers and 8.7% were current waterpipe smokers. About 2.8% reported that they currently smoke cigarettes and waterpipe (dual smoking). None of the studied sociodemographic characteristics of women were significantly associated with current cigarette or waterpipe smoking (Table 1). About one quarter (23.5%) of cigarette smokers reported daily smoking. Of the waterpipe smokers, 74.1% reported smoking waterpipe at least once per month but not weekly, 12.9% reported smoking at least once a week but not daily, and 13.0% reported daily waterpipe smoking. Almost all waterpipe smokers reported using the waterpipe once on days that they smoked. Of waterpipe smokers, the majority reported that they usually smoke waterpipe with one of the family members (59.8%) or friends (32.2%). About 58.7% of waterpipe smokers reported smoking in their houses, 20.0% in a coffee shop or a restaurant, and 13.0% in the park.
Table 1.
Current cigarette smoking | p Value | Current waterpipe smoking | p Value | |||
Yes | No | Yes | No | |||
Age (years) | .622 | .119 | ||||
17–24.9 | 6 (6.2) | 91 (93.8) | 14 (13.6) | 89 (86.4) | ||
25–29.9 | 11 (7.4) | 137 (92.6) | 12 (7.9) | 140 (92.1) | ||
≥30 | 21 (9.2) | 207 (90.8) | 16 (6.9) | 217 (93.1) | ||
Level of education | .217 | .200 | ||||
High school or less | 15 (10.2) | 132 (89.8) | 17 (11.1) | 136 (88.9) | ||
Bachelor's degree or more | 23 (6.9) | 310 (93.1) | 26 (7.6) | 316 (92.4) | ||
Income (JD) | .617 | .479 | ||||
<300 | 6 (5.7) | 100 (94.3) | 9 (8.3) | 99 (91.7) | ||
300–500 | 20 (8.6) | 212 (91.4) | 18 (7.5) | 223 (92.5) | ||
>500 | 12 (8.5) | 129 (91.5) | 16 (11.0) | 129 (89.0) | ||
Residency | .070 | .589 | ||||
Urban | 32 (9.1) | 319 (90.9) | 32 (8.8) | 330 (91.2) | ||
Rural | 4 (3.7) | 103 (96.3) | 8 (7.2) | 103 (92.8) | ||
Trimester | .928 | .467 | ||||
First | 7 (8.1) | 79 (91.9) | 10 (11.4) | 78 (88.6) | ||
Second | 9 (8.1) | 102 (91.9) | 10 (8.8) | 103 (91.2) | ||
Third | 20 (7.2) | 259 (92.8) | 21 (7.3) | 268 (92.7) |
Note. JD = Jordanian Dinars.
Factors Associated with Current Cigarette and Waterpipe Smoking
Table 2 shows the multivariate analysis of factors associated with current cigarette smoking and current waterpipe smoking. Level of education and residency were significantly associated with current cigarette smoking. A bachelor's degree or higher level of education was significantly associated with increased odds of current cigarette smoking (OR = 2.27, 95% CI = 1.09–5.22). Compared with women living in urban areas, those who were living in the rural areas were almost three times more likely to be current cigarette smokers (OR = 3.30, 95% CI = 1.12–8.28). On the other hand, age ≥30 years, and monthly income ≤ 500 were significantly associated with increased odds of current waterpipe smoking.
Table 2.
Variable | Current cigarette smoking | Current waterpipe smoking | ||
OR (95% CI) | p Value | OR (95% CI) | p Value | |
Age (years) | ||||
17–24.9 | 1 | 1 | ||
25–29.9 | 0.67 (0.23, 1.99) | .472 | 1.70 (0.68, 4.26) | .258 |
≥30 | 0.72 (0.26, 2.00) | .528 | 2.47 (1.03, 5.92) | .043 |
Level of education | ||||
High school or less | 1 | 1 | ||
Bachelor's degree or more | 2.27 (1.09, 5.22) | .043 | 1.90 (0.85, 4.28) | .120 |
Income (JD) | ||||
<300 | 1.55 (0.47, 5.15) | .472 | 2.77 (1.10, 8.29) | .045 |
300–500 | 1.19 (0.52, 2.73) | .686 | 2.30 (1.04, 5.09) | .041 |
>500 | 1 | 1 | ||
Residency | ||||
Urban | 1 | |||
Rural | 3.30 (1.12, 8.28) | .040 | 1.24 (0.51, 2.98) | .633 |
Pregnancy trimester | ||||
First | 1.07 (0.40, 2.85) | .888 | 0.69 (0.28, 1.66) | .406 |
Second | 0.82 (0.35, 1.90) | .642 | 0.77 (0.34, 1.75) | .532 |
Third | 1 | 1 |
Note. JD = Jordanian Dinars.
Secondhand Smoke
The husband was the main source for exposure to cigarette and waterpipe smoke (48.5% and 42.7% respectively) followed by relatives for cigarette (21.1%) and friends for waterpipe (24.4%). The house was the most common place of exposure to cigarette and waterpipe smoke (50.4% and 48.7%, respectively), followed by public places (31.4% and 21.4%, respectively; Table 3). About 82.4% of all women reported that they were exposed to cigarette smoke and 32.8% reported that they were exposed to waterpipe smoke. Of those who were exposed to cigarette smoke, 78.8% reported daily exposure (40.5% more than 5 times/day, 20.3% between 2 and 5 times/day, 17.8% once/day). Of those who were exposed to waterpipe smoke, 46.3% reported daily exposure (18.2% more than once/day and 28.2% once/day).
Table 3.
Variable | Cigarette smoke (N = 412) | Waterpipe smoke (N = 164) |
Sources of smoke | ||
Husband | 48.5 | 42.7 |
Relatives | 21.1 | 20.7 |
Friends | 13.6 | 24.4 |
Others | 16.8 | 12.2 |
Places of exposure | ||
Home | 50.4 | 48.7 |
Relative's house | 12.5 | 19.5 |
Friend's house | 5.7 | 10.4 |
Public places | 31.4 | 21.4 |
Perception of Harmful Effects of Cigarette and Waterpipe Smoking
The majority of women believe that cigarette smoking is addictive (74.3%) while only 55.1% reported that there is high probability for waterpipe smokers to become addicts. Regarding the direct health effects, about 43.7% of women reported that the waterpipe smokers have high probability to suffer from immediate symptoms of smoking including headache, nausea, vomiting, stomach ache, and coughing, 21.5% reported that cigarette smokers have high probability to suffer from such symptoms. To assess women’s perception regarding harms of cigarette smoking to the health of the fetus, the following question was asked: In your opinion, which of the following statements apply to the effect of exposure to cigarette smoking on fetal health? Women were given the following choices: (a) cigarette smoking does not affect fetal health, (b) cigarette smoking has some negative effects on fetal health, and (c) cigarette smoking has many negative effects on fetal health. To assess women’s perception about the effects of waterpipe smoking on fetal health, the same question was asked, but replacing “cigarette” with “waterpipe.” The results show that comparable percentages of women believed that either waterpipe (80.8%) or cigarette (76.4%) smoking are associated with negative health effects on the fetus.
Discussion
In this study, we examined the prevalence and the pattern of cigarettes and waterpipe smoking among pregnant women in Jordan. The data indicate that approximately 15% of the pregnant women in Jordan smoke tobacco during pregnancy. Higher prevalence rates were reported in some developed and developing countries including France (36%; Lelong, Blondel, & Kaminski, 2011), United Kingdom (27%; Fleming & Blair, 2007), Lebanon (25.7%; Bachir & Chaaya, 2008), and Serbia (37.2%; Krstev, Marinkovic, Simic, Kocev, & Bondy, 2011). In other countries, different estimates were reported: United States (10.2%), Japan (8.9%) (Suzuki et al., 2010), Australia (17.4%; Thrift, Nancarrow, & Bauman, 2011), Tunisia (4%–18.8%; Fakhfakh et al., 2011), Romania (15%; Meghea, Rus, Rus, Summers Holtrop, & Roman, 2010), and Poland (8%; Perz, Gaca, Mniszak, & Wesol, 2006). In this study, about 83% of the sample reported that they were exposed to tobacco smoke from both cigarette and waterpipe (passive smoking). Reports from several countries indicated that rates of secondhand smoke exposure during pregnancy ranged between 17% and 94% (Bloch et al., 2008; Franchini et al., 2008; Kelly et al., 2011; Torres et al., 2011; Yang, Tong, Mao, & Hu, 2010). In previous studies from Jordan, exposure to secondhand cigarette smoke among Jordanian women was about 70% in a sample of patients admitted to a local hospital, using a survey that was developed by the researchers (Zmeili, 1992) while another study indicated that 60% of mothers were exposed to secondhand smoke from other family members at home using both survey instrument and biomarkers of exposure to cigarettes (nicotine and cotinine plasma levels [n = 220, Badran, Salhab, & Al-Jaghbir, 2009]). Recently, using a modified Pregnancy Risk Assessment Monitoring System questionnaire, it was reported that 65% of pregnant women are exposed to cigarette smoke at home (n = 300, Abu-Baker, Haddad, & Savage, 2010). In our study, we included exposures to waterpipe smoking, and we interviewed a relatively larger number of subjects (n = 500), which could explain the relatively higher percentage of exposure to tobacco smoke. Alternatively, the steady increase in tobacco use in Jordan might be responsible for the reported tobacco exposure in this study. Previous studies have also reported some inconsistency in the responses of pregnant women about their tobacco use as opposed to blood nicotine and cotinine levels (Sasaki, Braimoh, Yila, Yoshioka, & Kishi, 2011). In the case of the waterpipe, waterpipe-specific biomarkers of exposures are not available. Identifying these specific markers will be very useful for waterpipe research. Overall, tobacco-smoke exposure in utero, remains a world public health challenge and the need for action against it in Jordan and worldwide is strongly suggested.
Over the last decade, WTS has spread worldwide and is alarmingly common among adolescents and young adults. According to this study, the percentage of pregnant women that use waterpipe during pregnancy in Jordan may be equal to and perhaps slightly higher than those who smoke cigarettes. This prevalence of WTS during pregnancy could be due to the common perception that water in the waterpipe filters the smoke and renders it less harmful and not addictive. The higher percentage of pregnant women who use waterpipe could also be attributed to the lack of waterpipe-specific policy and regulations. Only two studies have examined the effects of waterpipe smoking on fetal health and found that waterpipe smoking during pregnancy is associated with low birth weight (Mirahmadizadeh & Nakhaee, 2008; Tamim, Yunis, Chemaitelly, Alameh, & Nassar, 2008). The literature shows that waterpipe smoke contains similar profile of toxicants to that of cigarette smoking. For example, it contains polycyclic aromatic hydrocarbons and aldehydes that cause cancer and lung diseases (Monzer, Sepetdjian, Saliba, & Shihadeh, 2008; Shihadeh & Saleh, 2005), CO that contributes to cardiovascular disease (El-Nachef & Hammond, 2008; Saleh & Shihadeh, 2008), and nicotine that causes dependence (Blank et al., 2011; Neergaard, Singh, Job, & Montgomery, 2007; Shihadeh, 2003). Moreover, because waterpipe users exhale 50–100 L of smoke with each use episode (e.g., Cobb, Shihadeh, Weaver, & Eissenberg, 2011), secondhand smokers are exposed to high toxicant levels (e.g., Daher et al., 2010). Finally, waterpipe smoking was shown to be more mutagenic than cigarette smoking (Khabour, Alsatari, Azab, Alzoubi, & Sadiq, 2011). Thus, relative to cigarette smoke, waterpipe smoke exposure during pregnancy might be expected to have similar or even more harmful consequences for fetal health. In fact, a study by Nuwayhid, Yamout, Azar, and Kambris (1998) showed that, similar to cigarette smoking, waterpipe smoking during pregnancy is associated with harmful effects to the fetus.
The results showed that smoking among pregnant women in Jordan is associated with level of education, living in the rural areas, age, and monthly income. Previous studies have shown similar risk factors in other populations. For example, waterpipe smoking was found to be associated with age, income, and level of education among Blacks in Minnesota (Dillon & Chase, 2010). Similarly, women’s age was associated with waterpipe smoking in United Arab Emirate population (Mandil, Hussein, Omer, Turki, & Gaber, 2007). Identification of factors that contribute to smoking among pregnant women might help in interventions that target this population.
Findings of the current study emphasize the need for action against maternal tobacco smoke exposure in Jordan. Results of the current study also provide strong evidence for an end to tobacco smoking in all enclosed areas. Jordan has signed The Framework Convention on Tobacco Control treaty and now has a law that prohibits smoking in public enclosed areas. Results reported here show a considerable fraction of pregnant women are exposed to smoke in public places such as restaurants, transportation vehicles, stores, and others. Thus, the implementation and vigorous enforcement of that law that prohibits smoking in public enclosed areas is essential. The results also showed that a Jordanian woman’s husband is the main source of exposure to tobacco smoke. This finding is in accordance with previous reports (Chaaya, Awwad, Campbell, Sibai, & Kaddour, 2003; Lemola & Grob, 2008; Zolnierczuk-Kieliszek, Chemperek, & Koza, 2004). One way to limit this source of exposure is educational programs that emphasize fetal harm, which could occur as a result of both passive and active maternal smoking. These programs should target families (especially husbands) within homes of pregnant women. In summary, maternal exposure to tobacco smoke is a public health problem in Jordan and worldwide that requires immediate action.
Funding
This work was supported from the Deanship of Research at Hashemite University and the U.S. National Institutes of Health (R03-TW008371 and R01-CA120142).
Declaration of Interests
None to declare.
References
- Abu-Baker NN, Haddad L, Savage C. The influence of secondhand smoke exposure on birth outcomes in Jordan. International Journal of Environmental Research and Public Health. 2010;7:616–634. doi: 10.3390/ijerph7020616. doi:10.3390/ijerph7020616. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Azab M, Khabour OF, Alkaraki AK, Eissenberg T, Alzoubi KH, Primack BA. Water pipe tobacco smoking among university students in Jordan. Nicotine & Tobacco Research. 2010;12:606–612. doi: 10.1093/ntr/ntq055. doi:ntq055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bachir R, Chaaya M. Maternal smoking: Determinants and associated morbidity in two areas in Lebanon. Maternal and Child Health Journal. 2008;12:298–307. doi: 10.1007/s10995-007-0242-z. doi:10.1007/s10995-007-0242-z. [DOI] [PubMed] [Google Scholar]
- Badran E, Salhab AS, Al-Jaghbir M. Infant exposure to environmental tobacco smoke: Jordan University hospital-based study. Eastern Mediterranean Health Journal. 2009;15(1):39–46. [PubMed] [Google Scholar]
- Blank MD, Cobb CO, Kilgalen B, Austin J, Weaver MF, Shihadeh A, et al. Acute effects of waterpipe tobacco smoking: A double-blind, placebo-control study. Drug and Alcohol Dependence. 2011;116:102–109. doi: 10.1016/j.drugalcdep.2010.11.026. doi:S0376-8716(11)00023-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bloch M, Althabe F, Onyamboko M, Kaseba-Sata C, Castilla EE, Freire S, et al. Tobacco use and secondhand smoke exposure during pregnancy: An investigative survey of women in 9 developing nations. American Journal of Public Health. 2008;98:1833–1840. doi: 10.2105/AJPH.2007.117887. doi:AJPH.2007.117887. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chaaya M, Awwad J, Campbell OM, Sibai A, Kaddour A. Demographic and psychosocial profile of smoking among pregnant women in Lebanon: Public health implications. Maternal and Child Health Journal. 2003;7:179–186. doi: 10.1023/a:1025136421230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chaaya M, Jabbour S, El-Roueiheb Z, Chemaitelly H. Knowledge, attitudes, and practices of argileh (water pipe or hubble-bubble) and cigarette smoking among pregnant women in Lebanon. Addictive Behaviors. 2004;29:1821–1831. doi: 10.1016/j.addbeh.2004.04.008. doi:S0306460304001376. [DOI] [PubMed] [Google Scholar]
- Chelchowska M, Ambroszkiewicz J, Gajewska J, Laskowska-Klita T, Leibschang J. The effect of tobacco smoking during pregnancy on plasma oxidant and antioxidant status in mother and newborn. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2011;155:132–136. doi: 10.1016/j.ejogrb.2010.12.006. doi:S0301-2115(10)00577-4. [DOI] [PubMed] [Google Scholar]
- Cobb CO, Shihadeh A, Weaver MF, Eissenberg T. Waterpipe tobacco smoking and cigarette smoking: A direct comparison of toxicant exposure and subjective effects. Nicotine & Tobacco Research. 2011;13:78–87. doi: 10.1093/ntr/ntq212. doi: 10.1093/ntr/ntq212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daher N, Saleh R, Jaroudi E, Sheheitli H, Badr T, Sepetdjian E, et al. Comparison of carcinogen, carbon monoxide, and ultrafine particle emissions from narghile waterpipe and cigarette smoking: Sidestream smoke measurements and assessment of second-hand smoke emission factors. Atmospheric Environment. 2010;44:8–14. doi: 10.1016/j.atmosenv.2009.10.004. doi:10.1016/j.atmosenv.2009.10.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dillon KA, Chase RA. Secondhand smoke exposure, awareness, and prevention among African-born women. American Journal of Preventive Medicine. 2010;39(6 Suppl. 1):S37–S43. doi: 10.1016/j.amepre.2010.08.011. doi:S0749-3797(10)00477-0. [DOI] [PubMed] [Google Scholar]
- Durante AS, Ibidi SM, Lotufo JP, Carvallo RM. Maternal smoking during pregnancy: Impact on otoacoustic emissions in neonates. International Journal of Pediatric Otorhinolaryngology. 2011;75:1093–1098. doi: 10.1016/j.ijporl.2011.05.023. doi:S0165-5876(11)00274-6. [DOI] [PubMed] [Google Scholar]
- Durmus B, Kruithof CJ, Gillman MH, Willemsen SP, Hofman A, Raat H, et al. Parental smoking during pregnancy, early growth, and risk of obesity in preschool children: The Generation R Study. American Journal of Clinical Nutrition. 2011;94:164–171. doi: 10.3945/ajcn.110.009225. doi:ajcn.110.009225. [DOI] [PubMed] [Google Scholar]
- Eissenberg T, Ward KD, Smith-Simone S, Maziak W. Waterpipe tobacco smoking on a U.S. College campus: Prevalence and correlates. Journal of Adolescent Health. 2008;42:526–529. doi: 10.1016/j.jadohealth.2007.10.004. doi:S1054-139X(07)00413-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- El-Nachef WN, Hammond SK. Exhaled carbon monoxide with waterpipe use in US students. Journal of the American Medical Association. 2008;299:36–38. doi: 10.1001/jama.2007.6. doi:299/1/36-a. [DOI] [PubMed] [Google Scholar]
- Esposito ER, Horn KH, Greene RM, Pisano MM. An animal model of cigarette smoke-induced in utero growth retardation. Toxicology. 2008;246:193–202. doi: 10.1016/j.tox.2008.01.014. doi:S0300-483X(08)00019-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fahn HJ, Wang LS, Kao SH, Chang SC, Huang MH, Wei YH. Smoking-associated mitochondrial DNA mutations and lipid peroxidation in human lung tissues. American Journal of Respiratory Cell and Molecular Biology. 1998;19:901–909. doi: 10.1165/ajrcmb.19.6.3130. [DOI] [PubMed] [Google Scholar]
- Fakhfakh R, Jellouli M, Klouz A, Ben Hamida M, Lakhal M, Belkahia C, et al. Smoking during pregnancy and postpartum among Tunisian women. Journal of Maternal-Fetal and Neonatal Medicine. 2011;24:859–862. doi: 10.3109/14767058.2010.531317. doi:10.3109/14767058.2010.531317. [DOI] [PubMed] [Google Scholar]
- Fleming P, Blair PS. Sudden Infant Death Syndrome and parental smoking. Early Human Development. 2007;83:721–725. doi: 10.1016/j.earlhumdev.2007.07.011. doi:S0378-3782(07)00129-6. [DOI] [PubMed] [Google Scholar]
- Franchini M, Caruso C, Perico A, Pacifici R, Monleon T, Garcia-Algar O, et al. Assessment of foetal exposure to cigarette smoke after recent implementations of smoke-free policy in Italy. Acta Paediatrica. 2008;97:546–550. doi: 10.1111/j.1651-2227.2008.00762.x. doi:APA762. [DOI] [PubMed] [Google Scholar]
- Frei B, Forte TM, Ames BN, Cross CE. Gas phase oxidants of cigarette smoke induce lipid peroxidation and changes in lipoprotein properties in human blood plasma. Protective effects of ascorbic acid. Biochemical Journal. 1991;277:133–138. doi: 10.1042/bj2770133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghafouri N, Hirsch JD, Heydari G, Morello CM, Kuo GM, Singh RF. Waterpipe smoking among health sciences university students in Iran: Perceptions, practices and patterns of use. BMC Research Notes. 2011;4:496. doi: 10.1186/1756-0500-4-496. doi:1756-0500-4-496. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glantz SA, Parmley WW. Passive smoking and heart disease. Mechanisms and risk. Journal of the American Medical Association. 1995;273:1047–1053. [PubMed] [Google Scholar]
- Hackshaw A, Rodeck C, Boniface S. Maternal smoking in pregnancy and birth defects: A systematic review based on 173 687 malformed cases and 11.7 million controls. Human Reproduction Update. 2011;17:589–604. doi: 10.1093/humupd/dmr022. doi:10.1093/humupd/dmr022. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ino T, Shibuya T, Saito K, Ohtani T. Effects of maternal smoking during pregnancy on body composition in offspring. Pediatric International. 2011;53:851–857. doi: 10.1111/j.1442-200X.2011.03383.x. doi:10.1111/j.1442-200X.2011.03383.x. [DOI] [PubMed] [Google Scholar]
- International Agency for Research on Cancer. Tobacco smoke and involuntary smoking, IARC monographs on the evaluation of carcinogenic risk of chemicals to humans. vol. 83. Lyon, France: Author; 2004. [Google Scholar]
- Kandela P. Nargile smoking keeps Arabs in Wonderland. The Lancet. 2000;356:1175. doi: 10.1016/s0140-6736(05)72871-3. [DOI] [PubMed] [Google Scholar]
- Kayemba-Kay’s S, Ribrault A, Burguet A, Gouyon JB, Riethmuller D, Menget A, et al. Maternal smoking during pregnancy and fetal growth. Effects in preterm infants of gestational age less than 33 weeks. Swiss Medical Weekly. 2010;140:w13139. doi: 10.4414/smw.2010.13139. doi:smw-13139. [DOI] [PubMed] [Google Scholar]
- Kelly PJ, Goudar SS, Chakraborty H, Moore J, Derman R, Kodkany B, et al. Pregnant women and children's exposure to tobacco and solid fuel smoke in southwestern India. Journal of Maternal-Fetal and Neonatal Medicine. 2011;24:973–977. doi: 10.3109/14767058.2010.537411. doi:10.3109/14767058.2010.537411. [DOI] [PubMed] [Google Scholar]
- Khabour OF, Alsatari ES, Azab M, Alzoubi KH, Sadiq MF. Assessment of genotoxicity of waterpipe and cigarette smoking in lymphocytes using the sister-chromatid exchange assay: A comparative study. Environmental and Molecular Mutagenesis. 2011;52:224–228. doi: 10.1002/em.20601. doi:10.1002/em.20601. [DOI] [PubMed] [Google Scholar]
- Kiter G, Ucan ES, Ceylan E, Kilinc O. Water-pipe smoking and pulmonary functions. Respiratory Medicine. 2000;94:891–894. doi: 10.1053/rmed.2000.0859. doi:S0954-6111(00)90859-X. [DOI] [PubMed] [Google Scholar]
- Klimentopoulou A, Antonopoulos CN, Papadopoulou C, Kanavidis P, Tourvas AD, Polychronopoulou S, et al. Maternal smoking during pregnancy and risk for childhood leukemia: A nationwide case-control study in Greece and meta-analysis. Pediatric Blood & Cancer. 2011;58:344–351. doi: 10.1002/pbc.23347. doi:10.1002/pbc.23347. [DOI] [PubMed] [Google Scholar]
- Krstev S, Marinkovic J, Simic S, Kocev N, Bondy SJ. Prevalence and predictors of smoking and quitting during pregnancy in Serbia: Results of a nationally representative survey. International Journal of Public Health. 2011 doi: 10.1007/s00038-011-0301-5. doi:10.1007/s00038-011-0301-5. [DOI] [PubMed] [Google Scholar]
- Lelong N, Blondel B, Kaminski M. [Smoking during pregnancy in France between 1972 to 2003: Results from the national perinatal surveys] Journal de gynecologie, obstetrique et biologie de la reproduction (Paris) 2011;40:42–49. doi: 10.1016/j.jgyn.2010.07.007. doi:S0368-2315(10)00220-6. [DOI] [PubMed] [Google Scholar]
- Lemola S, Grob A. Smoking cessation during pregnancy and relapse after childbirth: The impact of the grandmother's smoking status. Maternal and Child Health Journal. 2008;12:525–533. doi: 10.1007/s10995-007-0258-4. doi:10.1007/s10995-007-0258-4. [DOI] [PubMed] [Google Scholar]
- Mandil A, Hussein A, Omer H, Turki G, Gaber I. Characteristics and risk factors of tobacco consumption among University of Sharjah students, 2005. Eastern Mediterranean Health Journal. 2007;13:1449–1458. doi: 10.26719/2007.13.6.1449. [DOI] [PubMed] [Google Scholar]
- Maziak W, Ali RA, Fouad MF, Rastam S, Wipfli H, Travers MJ, et al. Exposure to secondhand smoke at home and in public places in Syria: A developing country's perspective. Inhalation Toxicology. 2008;20:17–24. doi: 10.1080/08958370701758783. doi:790161371. [DOI] [PubMed] [Google Scholar]
- Meghea CI, Rus D, Rus IA, Summers Holtrop J, Roman L. Smoking during pregnancy and associated risk factors in a sample of Romanian women. European Journal of Public Health. 2010 doi: 10.1093/eurpub/ckq189. doi:10.1093/eurpub/ckq189. [DOI] [PubMed] [Google Scholar]
- Mirahmadizadeh A, Nakhaee N. Prevalence of waterpipe smoking among rural pregnant women in Southern Iran. Medical Principles and Practice. 2008;17:435–439. doi: 10.1159/000151563. doi:000151563. [DOI] [PubMed] [Google Scholar]
- Monzer B, Sepetdjian E, Saliba N, Shihadeh A. Charcoal emissions as a source of CO and carcinogenic PAH in mainstream narghile waterpipe smoke. Food and Chemical Toxicology. 2008;46:2991–2995. doi: 10.1016/j.fct.2008.05.031. doi:S0278-6915(08)00278-0. [DOI] [PubMed] [Google Scholar]
- Nabet C, Ancel PY, Burguet A, Kaminski M. Smoking during pregnancy and preterm birth according to obstetric history: French national perinatal surveys. Paediatric and Perinatal Epidemiology. 2005;19:88–96. doi: 10.1111/j.1365-3016.2005.00639.x. doi:PPE639. [DOI] [PubMed] [Google Scholar]
- Nakamura MU, Alexandre SM, Kuhn dos Santos JF, de Souza E, Sass N, Auritscher Beck AP, et al. Obstetric and perinatal effects of active and/or passive smoking during pregnancy. Sao Paulo Medical Journal. 2004;122:94–98. doi: 10.1590/S1516-31802004000300004. doi:/S1516-31802004000300004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakkash RT, Khalil J, Afifi RA. The rise in narghile (shisha, hookah) waterpipe tobacco smoking: A qualitative study of perceptions of smokers and non smokers. BMC Public Health. 2011;11:315. doi: 10.1186/1471-2458-11-315. doi:1471-2458-11-315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neergaard J, Singh P, Job J, Montgomery S. Waterpipe smoking and nicotine exposure: A review of the current evidence. Nicotine & Tobacco Research. 2007;9:987–994. doi: 10.1080/14622200701591591. doi:783052859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ng SP, Silverstone AE, Lai ZW, Zelikoff JT. Effects of prenatal exposure to cigarette smoke on offspring tumor susceptibility and associated immune mechanisms. Toxicological Sciences. 2006;89:135–144. doi: 10.1093/toxsci/kfj006. doi:kfj006. [DOI] [PubMed] [Google Scholar]
- Nuwayhid IA, Yamout B, Azar G, Kambris MA. Narghile (hubble-bubble) smoking, low birth weight, and other pregnancy outcomes. American Journal of Epidemiology. 1998;148:375–383. doi: 10.1093/oxfordjournals.aje.a009656. [DOI] [PubMed] [Google Scholar]
- Perz S, Gaca M, Mniszak M, Wesol D. [Smoking prevalence during pregnancy and exposition of infants to environmental tobacco smoke] Przegląd Lekarski. 2006;63:1063–1065. [PubMed] [Google Scholar]
- Primack BA, Sidani J, Agarwal AA, Shadel WG, Donny EC, Eissenberg TE. Prevalence of and associations with waterpipe tobacco smoking among U.S. university students. Annals of behavioral medicine. 2008;36:81–86. doi: 10.1007/s12160-008-9047-6. doi:10.1007/s12160-008-9047-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rastam S, Ward KD, Eissenberg T, Maziak W. Estimating the beginning of the waterpipe epidemic in Syria. BMC Public Health. 2004;4:32. doi: 10.1186/1471-2458-4-32. doi:10.1186/1471-2458-4-32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reznick AZ, Cross CE, Hu ML, Suzuki YJ, Khwaja S, Safadi A, et al. Modification of plasma proteins by cigarette smoke as measured by protein carbonyl formation. Biochemistry Journal. 1992;286:607–611. doi: 10.1042/bj2860607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson JS, Moore VM, Owens JA, McMillen IC. Origins of fetal growth restriction. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2000;92:13–19. doi: 10.1016/s0301-2115(00)00421-8. doi:S0301211500004218 [pii] [DOI] [PubMed] [Google Scholar]
- Rogers JM. Tobacco and pregnancy: Overview of exposures and effects. Birth Defects Research Part C: Embryo Today. 2008;84:1–15. doi: 10.1002/bdrc.20119. doi:10.1002/bdrc.20119. [DOI] [PubMed] [Google Scholar]
- Saleh R, Shihadeh A. Elevated toxicant yields with narghile waterpipes smoked using a plastic hose. Food and Chemical Toxicology. 2008;46:1461–1466. doi: 10.1016/j.fct.2007.12.007. doi:S0278-6915(07)00564-9. [DOI] [PubMed] [Google Scholar]
- Sasaki S, Braimoh TS, Yila TA, Yoshioka E, Kishi R. Self-reported tobacco smoke exposure and plasma cotinine levels during pregnancy—A validation study in Northern Japan. Science of the Total Environment. 2011;412–413:114–118. doi: 10.1016/j.scitotenv.2011.10.019. doi:S0048-9697(11)01211-3. [DOI] [PubMed] [Google Scholar]
- Shihadeh A. Investigation of mainstream smoke aerosol of the argileh water pipe. Food and Chemical Toxicology. 2003;41:143–152. doi: 10.1016/s0278-6915(02)00220-x. doi:S027869150200220X. [DOI] [PubMed] [Google Scholar]
- Shihadeh A, Saleh R. Polycyclic aromatic hydrocarbons, carbon monoxide, “tar”, and nicotine in the mainstream smoke aerosol of the narghile water pipe. Food and Chemical Toxicology. 2005;43:655–661. doi: 10.1016/j.fct.2004.12.013. doi:S0278-6915(05)00012-8. [DOI] [PubMed] [Google Scholar]
- Suzuki K, Kondo N, Sato M, Tanaka T, Ando D, Yamagata Z. Gender differences in the association between maternal smoking during pregnancy and childhood growth trajectories: Multilevel analysis. International Journal of Obesity. 2010;35:53–59. doi: 10.1038/ijo.2010.198. doi:ijo2010198. [DOI] [PubMed] [Google Scholar]
- Tamim H, Yunis KA, Chemaitelly H, Alameh M, Nassar AH. Effect of narghile and cigarette smoking on newborn birthweight. BJOG. 2008;115:91–97. doi: 10.1111/j.1471-0528.2007.01568.x. doi:BJO1568. [DOI] [PubMed] [Google Scholar]
- Thrift AP, Nancarrow H, Bauman AE. Maternal smoking during pregnancy among Aboriginal women in New South Wales is linked to social gradient. Australian and New Zealand Journal of Public Health. 2011;35:337–342. doi: 10.1111/j.1753-6405.2011.00728.x. doi:10.1111/j.1753-6405.2011.00728.x. [DOI] [PubMed] [Google Scholar]
- Torres E, Quinones de Monegro Z, French L, Swanson DP, Guido J, Ossip DJ. Tobacco use and exposure to secondhand smoke among pregnant women in the dominican republic: An exploratory look into attitudes, beliefs, perceptions, and practices. Nicotine & Tobacco Research. 2011;13:1220–1227. doi: 10.1093/ntr/ntr193. doi:ntr193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warren CW, Lea V, Lee J, Jones NR, Asma S, McKenna M. Change in tobacco use among 13-15 year olds between 1999 and 2008: Findings from the Global Youth Tobacco Survey. Global Health Promotion. 2009;16(2 Suppl.):38–90. doi: 10.1177/1757975909342192. doi:16/2_suppl/38. [DOI] [PubMed] [Google Scholar]
- Wells AJ. Passive smoking as a cause of heart disease. Journal of the American College of Cardiology. 1994;24:546–554. doi: 10.1016/0735-1097(94)90315-8. doi:0735-1097(94)90315-8. [DOI] [PubMed] [Google Scholar]
- WHO. Tobacco alert specific. Geneva, Switzerland: Author; 2009. The tobacco epidemic. A global public health emergency. Tobacco or health programme on substance abuse; p. 28. [Google Scholar]
- Yang L, Tong EK, Mao Z, Hu TW. Exposure to secondhand smoke and associated factors among non-smoking pregnant women with smoking husbands in Sichuan province, China. Acta Obstetricia et Gynecologica Scandinavica. 2010;89:549–557. doi: 10.3109/00016341003713851. doi:10.3109/00016341003713851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zmeili SM. Cigarette smoking in Jordan in some Jordanian patients. Dirasat. 1992;19B:253–260. [Google Scholar]
- Zolnierczuk-Kieliszek D, Chemperek E, Koza M. Circumstances of tobacco smoking by pregnant women. Annales Universitatis Mariae Curie-Sklodowska Medicine. 2004;59:163–168. [PubMed] [Google Scholar]