Preschool children and their mothers are more exposed to paternal smoking at home than school children and their mothers

Preschool children and their mothers are more exposed to paternal smoking at home than school children and their mothers

Clinica Chimica Acta 411 (2010) 72–76 Contents lists available at ScienceDirect Clinica Chimica Acta j o u r n a l h o m e p a g e : w w w. e l s ev...

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Clinica Chimica Acta 411 (2010) 72–76

Contents lists available at ScienceDirect

Clinica Chimica Acta j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c l i n c h i m

Preschool children and their mothers are more exposed to paternal smoking at home than school children and their mothers Moon-Woo Seong a,e, Jin Soo Moon b, Jong Hee Hwang b, Hye-Jung Ryu a, Soo Jin Kang a, Sun-Young Kong a, Tae Hyun Um c, Jae-Gahb Park d, Jin Soo Lee e, Do-Hoon Lee a,⁎ a

Department of Laboratory Medicine, National Cancer Center Hospital, Goyang, Republic of Korea Department of Pediatrics, Inje University Ilsan Paik Hospital, Goyang, Republic of Korea Department of Laboratory Medicine, Inje University Ilsan Paik Hospital, Goyang, Republic of Korea d Cancer Research Institute and Cancer Research Center, Seoul National University, Seoul, Republic of Korea e Lung Cancer Branch, National Cancer Center Research Institute, Goyang, Republic of Korea b c

a r t i c l e

i n f o

Article history: Received 25 June 2009 Received in revised form 3 October 2009 Accepted 5 October 2009 Available online 12 October 2009 Keywords: Smoking Passive smoking Smoking biomarker

a b s t r a c t Background: Exposure to secondhand smoke (SHS) is a major risk to human health, and the home is the greatest single source of SHS in children. Here, the authors assessed SHS exposure of children and mothers by paternal smoking at home, and investigated how different this exposure is according to smoking location and children's age. Methods: Two hundred-five families were enrolled in this study as trios of fathers, mothers, and children. Nicotine concentrations in hair were measured using liquid chromatography–tandem mass spectrometry to determine long-term exposure to SHS. Results: Differences between the smoker group and nonsmoker group in nicotine levels were statistically significant in both children and their mothers. However, difference between the indoor-smoker group and outdoor-smoker group was marginally significant in children and was not significant in their mothers. In the indoor-smoker group, preschool children and their mothers had nicotine concentrations about twice as high as school children and their mothers, respectively. In the outdoor-smoker group, however, differences between two age groups in nicotine levels were significant in preschool children, but not their mothers. Conclusion: These findings indicate that paternal smoking at home leads to significant exposure to SHS in their children and spouses, which is not completely prevented by smoking outside. Especially, preschool children and their mothers appear to be most at risk for SHS exposure among nonsmoking household members. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Secondhand smoke (SHS) is a major risk to human health given that it has immediate adverse effects on the cardiovascular system, and is known to cause lung cancer and respiratory symptoms [1,2]. Among various environmental sites of tobacco exposure, the home is the dominant site for children and women [3–5]. When smoking takes place in the home, an individual's exposure can be influenced by several factors including physical proximity to the smoking father and house ventilation [4,6]. Nonsmoking household members in a family, therefore, can have differential exposure levels to SHS. Previous studies on exposure to SHS by smoking family members demonstrated that children may be more susceptible to SHS exposure than their ⁎ Corresponding author. Department of Laboratory Medicine, National Cancer Center, 809 Madu-1-dong, Ilsandong-gu, Goyang, Kyeonggi 410-769, Republic of Korea. Tel.: +82 31 920 1734; fax: +82 31 920 1339. E-mail address: [email protected] (D.-H. Lee). 0009-8981/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.cca.2009.10.006

mothers and that younger children may be more at risk than older children [7–9]. These studies, however, did not distinguish between SHS exposure risks and smoking location (i.e. indoor vs. outdoor). When considering the home as an SHS exposure site, it is important to know where the smoking occurs [10]. Family members might be differently exposed to SHS depending on whether the father smoked inside or outside the home. Our previous study on fetal exposure to paternal smoking also suggested that an unborn fetus would be significantly exposed to paternal smoking if the father smoked inside the home, but fetal exposure in an outside-smoker group was not significantly different from that in the nonsmoker group [11]. Therefore, smoking location has to be considered in studies on SHS exposure at home. Hair nicotine measurements have several advantages when assessing SHS exposure since hair can be collected easily, and since nicotine levels in hair represent long-term exposure (up to months), and quantitatively correlates with exposure. Moreover, it is known that levels of nicotine in hair are comparable to other biomarkers for

NS

< 0.001⁎ NS⁎⁎

NS 0.053 Outdoor vs. indoor

These P values were obtained by ⁎ the comparison to the nonsmoker group with the smoker group concerned, or ⁎⁎ comparison to the preschool group with the school group concerned.

29.70 (20.36–35.90) 29.70 (15.64–42.50) 31.60 (15.20–37.40) 41.45 (46.93) 41.95 (44.05) 40.45 (51.27) <0.001⁎ 0.002⁎⁎ 2.21 (1.59–3.07) 2.99 (2.09–4.28) 1.20 (0.77–1.86) 0.53 (0.39–0.85) 0.85 (0.45–1.42) 0.26 (0.15–0.53) 1.06 (1.17) 1.31 (1.23) 0.56 (0.89) <0.001⁎ 0.006⁎⁎ 3.07 (2.32–4.06) 3.81 (2.77–5.23) 1.99 (1.38–2.88) 1.01 (0.75–1.42) 1.46 (0.95–2.21) 0.74 (0.48–1.01) 60 40 20 Indoor Preschool School

1.58 (1.50) 1.95 (1.69) 0.83 (0.50)

< 0.001⁎ NS⁎⁎ 17.80 (13.40–25.60) 17.80 (12.40–25.60) 16.40 (9.21–74.40) 28.64 (27.61) 26.08 (24.27) 34.73 (34.67) <0.001⁎ NS⁎⁎ 2.06 (1.45–2.93) 2.29 (1.57–3.35) 1.61 (0.93–2.79) 0.52 (0.38–0.91) 0.56 (0.42–0.91) 0.30 (0.16–1.06) 0.98 (1.18) 1.01 (1.19) 0.90 (1.20) <0.001⁎ 0.049⁎⁎ 2.23 (1.68–2.94) 2.58 (1.88–3.53) 1.57 (1.00–2.45) 0.72 (0.58–0.92) 0.86 (0.62–1.15) 0.59 (0.26–0.83) 1.01 (0.81) 1.15 (0.87) 0.68 (0.54) 44 31 13 Outdoor Preschool School

20.36 (17.20–25.78) 19.60 (15.60–25.78) 20.68 (16.40–34.20) 33.44 (38.05) 32.56 (35.41) 35.31 (43.55) 1.83 (1.37–2.44) 2.25 (1.66–3.04) 1.19 (0.83–1.69) 0.43 (0.37–0.61) 0.54 (0.42–0.86) 0.26 (0.16–0.43) 0.90 (1.11) 1.04 (1.15) 0.61 (0.94) <0.001⁎ 0.002⁎⁎ 2.27 (1.76–2.93) 2.71 (2.06–3.55) 1.57 (1.15–2.13) 0.76 (0.64–0.95) 0.94 (0.70–1.20) 0.59 (0.34–0.83) 1.24 (1.31) 1.44 (1.38) 0.83 (1.05)

1.00 0.22 (0.18–0.34) 0.28 (0.19–0.36) 0.20 (0.11–0.51) 0.41 (0.50) 0.40 (0.44) 0.42 (0.65) 0.004⁎⁎ 1.00 0.31 (0.26–0.41) 0.39 (0.29–0.48) 0.23 (0.15–0.30) 0.48 (0.48) 0.52 (0.47) 0.35 (0.49)

GMR (95% CI) Median (95% CI)

<0.001⁎ 0.006⁎⁎

NS⁎⁎ 1.33 (1.01–1.81) 1.48 (1.01–1.81) 0.90 (0.46–2.76) NS⁎⁎

P value GMR (95% CI) Mean (SD)

Median (95% CI) Mother

Mean (SD)

Children

P value

80 60 20

125 85 40 Smoker father Preschool School

We calculated medians and confidence intervals, and geometric mean ratios and confidence intervals as well as means because hair nicotine concentrations were skewed. The Mann–Whitney test was used to compare groups for hair nicotine levels. Spearman rank correlation coefficients (r) were calculated for correlation between nicotine levels at the family level. Regression analysis was used to

No smoker Preschool School

2.3. Statistical analysis

N

Nicotine and cotinine levels of hair samples were determined using a blinded study (with respect to smoking status of the study subjects) and the liquid chromatography–tandem mass spectrometry (LC–MS/MS) method previously described [13]. One milligram of hair samples was finely cut, washed for 1 h with 2 ml dichloromethane, and then digested for 90 min with 0.9 ml of 1 mol/l NaOH at 60 °C. The digested samples were mixed with internal standards of nicotine and cotinine, and extracted with 2 ml of diethyl ether. Next, extracts were evaporated for 40 min at 50 °C, redissolved in 50 μL of mobile phase (methanol–water; 80:20, v/v), and injected (10 µl) into the LC–MS/ MS system. The high-pressure liquid chromatography (HPLC) unit used was an HP 1100 (Agilent, Santa Clara, CA), and the tandem mass spectrometer used was an API 4000 (Applied Biosystems/MDS Sciex, Foster City CA) equipped with an atmospheric pressure chemical ionization (APCI) interface.

Study groups

2.2. Measurement of hair nicotine and cotinine

Table 1 Means, medians and geometric mean ratios (GMR) of nicotine concentrations (ng/mg hair) in each study group.

We identified trios of potential subjects consisting of children and both parents at the pediatric clinic of Inje University Ilsan Paik Hospital, Korea from January 2007 to December 2008. Informed consent was obtained from mothers or fathers, and candidates were asked to complete a questionnaire that detailed the smoking histories of family members. In the present study, we selected 253 candidate families with children <13 y. About 2–3 mg of hair was collected from the back of the scalp of each family member. After excluding mothers who smoked or had regular exposure to SHS at places other than home, a total of 205 families entered the final analysis. Based on current self-reported smoking status, each family was classified into the nonsmoker group or smoker group. Of the 205 families enrolled, 80 had no smoking members including the father, and 125 had a father who smoked. The average number of cigarettes that fathers smoked in a day was 13.4, and average number of cigarettes that they smoked at home was 3.6. About half of smoking fathers smoked three or more days per week at home. The smoker group was subdivided into an outdoor-smoker group (44 families) and an indoor-smoker group (60 families) according to whether the smoking father smoked only outside the home or not. Smoking place was indeterminate for the other 21 smoker families. Each family was subsequently classified into preschool group or school group according to whether they had preschool children or school children. The nonsmoker group was comprised of 60 preschool families and 20 school families, and the smoker group was comprised of 85 preschool families and 40 school families. The median age of preschool children in the nonsmoker, outdoor-smoker, and indoorsmoker group were 3.5, 2.9, and 3.0 y, respectively. The median age of school children included in the nonsmoker, outdoor-smoker, and indoor-smoker group were 9.2, 8.8, and 10.2 y, respectively.

Father

2.1. Subject characteristics

2.87 (4.97) 2.96 (5.32) 2.61 (3.87)

2. Materials and methods

Mean (SD)

Median (95% CI)

P value

the assessment of exposure to SHS [10,12]. We assessed SHS exposure of children and mothers by paternal smoking at home, and investigated how different this exposure is according to smoking location and children's age.

73 < 0.001⁎ NS⁎⁎

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identify factors associated with children's exposure to SHS. Factors of interest were children's age, smoking location at home, paternal or maternal nicotine concentrations, and the number of cigarettes that a father smoked at home or all day long. A P < 0.05 was considered significant. These statistical analyses were performed using SPSS ver. 12.0 software. 3. Results The mean values (±SD) of paternal, maternal, and children's nicotine concentrations in the smoker group were 33.44 (±38.05), 0.90 (±1.11), and 1.24 (±1.31) (ng/mg hair), respectively; while in the nonsmoker group they were 2.87 (±4.97), 0.41 (±0.50), and 0.48 (±0.48), respectively (Table 1). The median values (95% confidence interval) of paternal, maternal, and children's nicotine concentrations in the smoker group were 20.36 (17.20–25.78), 0.43 (0.37–0.61), and 0.76 (0.64–0.95), respectively; while in the nonsmoker group they were 1.33 (1.01–1.81), 0.22 (0.18–0.34), and 0.31 (0.26–0.41), respectively (Table 1). Maternal and children's nicotine levels in the smoker group were 1.83 times (geometric mean ratio [GMR], 1.83), and 2.27 times (GMR, 2.27) higher than those in the nonsmoker group, respectively, and these differences were statistically significant when using the Mann–Whitney test (P < 0.001) (Table 1, Fig. 1). The mean values (±SD) of paternal, maternal, and children's nicotine concentrations in the outdoor-smoker group were 28.64 (±27.61), 0.98 (±1.18), and 1.01 (±0.81), respectively; while in the indoor-smoker group they were 41.45 (±46.93), 1.06 (±1.17), and 1.58 (± 1.50), respectively (Table 1). The median values (95% confidence intervals) of paternal, maternal, and children's nicotine concentrations in the outdoor-smoker group were 17.80 (13.40– 25.60), 0.52 (0.38–0.91), and 0.72 (0.58–0.92), respectively; while in the indoor-smoker group were 29.70 (20.36–35.90), 0.53 (0.39–0.85), and 1.01 (0.75–1.42), respectively (Table 1). Fathers who smoked outside the home showed lower nicotine levels than fathers who smoked inside the home, but this difference was not statistically significant (P = 0.118). Maternal exposure showed no difference according to smoking place of their spouse. However, children's

exposure in the indoor-smoker group was higher than that in the outdoor-smoker group, and it was marginally significant (P = 0.053). In the smoker group, mean nicotine concentrations of preschool children and school children were 1.44 (±1.38) and 0.83 (±1.05), and median nicotine concentrations of preschool children and school children were 0.94 (0.70–1.20) and 0.59 (0.34–0.83). Preschool children had nicotine concentrations about twice as high as school children and this difference was significant (GMR, 2.71 vs. 1.57; P = 0.002) (Tables 1 and 2). Similar difference was observed in the outdoor-smoker group (GMR, 2.58 vs. 1.57; P = 0.049) and indoor-smoker group (GMR, 3.81 vs. 1.99; P = 0.006), respectively. Maternal nicotine concentrations in preschool group also were higher than those in school group (GMR, 2.25 vs. 1.19; P = 0.006). This difference, however, was significant in the indoor-smoker group (GMR, 2.99 vs. 1.20; P = 0.002) and not significant in the outdoor-smoker group (GMR, 2.29 vs. 1.61; P = 0.335). In addition, preschool children had higher nicotine concentrations than their mothers (median, 0.94 vs. 0.54; P = 0.004) and school children had higher nicotine concentrations than their mothers (median, 0.59 vs. 0.26; P = 0.008). Among nonsmoking members, preschool children showed the highest nicotine concentration, and mothers of school children showed the lowest (Fig. 2). The number of cigarettes that a father consumed in a day was poorly related to paternal hair nicotine, children's hair nicotine or their spouse's hair nicotine (r = 0.13, P = 0.15; r = 0.03, P = 0.74; and r = 0.07, P = 0.45, respectively). Similar correlation was observed in the indoor-smoker group alone as well as total smoker group. However, paternal hair nicotine itself showed even better correlation with children's hair nicotine or their spouse's hair nicotine (r = 0.50, P < 0.001 and r = 0.26, P < 0.001, respectively). Using multiple regression analysis, the most potent predictors for children's exposure were their age and the location at home which paternal smoking takes place (adjusted-R2, 24.2%). The regression model to use both paternal and maternal nicotine concentrations in addition to these 2 predictors was not much better than the one to use only these 2 predictors (adjusted-R2, 26.6%), although paternal or maternal nicotine concentrations quantitatively correlate with children's nicotine concentrations. It is noteworthy that this result might

Fig. 1. Nicotine concentrations (ng/mg hair) of children, mothers, and fathers by paternal smoking place. Nonsmoker group, outdoor-smoker group, and indoor-smoker group as shown from left to right, respectively, in each panel. Shown are comparative box plots of nicotine concentrations in each group. Y-axes from each part of the graph are scaled to accurately to display the distribution of nicotine concentrations in each group. The vertical line indicates the range of concentrations observed within each group, the box indicates the 25th and 75th percentile, and the middle line indicates the median in each group.

M.-W. Seong et al. / Clinica Chimica Acta 411 (2010) 72–76 Table 2 Comparison of nicotine concentrations in the smoker group, outdoor-smoker group, and indoor-smoker group. Study Groups

Smoker

Children vs. mothers < 0.001⁎ Preschool children vs. school children 0.002 Preschool children vs. mothers of preschool children 0.004 School children vs. mothers of school children 0.008 Mothers of preschool children vs. mothers of school 0.006 children

Outdoor Indoor NS 0.049 NS NS NS

0.003 0.006 0.044 0.002 0.002

⁎ Values are expressed as P values.

arise from high correlation between smoking place and paternal nicotine concentrations. To assess the age as a predictor of SHS exposure, we additionally compared sib-pairs in the indoor-smoker group. The indoor-smoker group had 8 families with 2 siblings, and median age of younger sibling and older sibling were 4.2 y (range 1– 10 y) and 7.0 y (range 3–12 y), respectively. Younger siblings had 2.07 times (GMR, 2.07; 95% CI, 1.08–3.96; P = 0.03) higher nicotine levels than older siblings, supporting the hypothesis that age can be an important predictor of SHS exposure. 4. Discussion The results of this study indicate that when their father smokes in the home, preschool children are more susceptible to SHS than other nonsmoking household members, followed by their mothers and school children, and mothers of school children. This study also demonstrates that outdoor-smoking may reduce SHS exposure to some extent, but cannot completely prevent it. Groner et al. reported that children of nonsmoking mothers had higher hair cotinine levels than their mothers [14]. Wipfli et al. suggested that children <5 y who live with smokers had hair nicotine concentrations that were nearly twice as high as children ≥5 y living with smokers [9]. However, they did not distinguish outdoor-smoking from indoor-smoking. Nonsmoking household members may be

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differently exposed to SHS depending on whether the father smoked inside or outside the home. Our study shows that this tendency may be of no significance, especially when considering the outdoorsmoker group alone. Therefore, smoking location, as well as age, has to be considered in research concerning exposure to SHS. The highest exposure in preschool children can be partly explained on the basis of greater respiratory exposure, deposition, and absorption of inhaled SHS in younger children than in adults as proposed by Groner et al. [14]. However, this interpretation cannot explain why mothers of preschool children have higher hair nicotine concentrations than mothers of school children. An explanation for the difference between the two groups of mothers as well as the two groups of children is how active the subgroup concerned is at attempting to avoid exposure. Younger children are more dependent on their parents and less likely to actively avoid exposure to SHS than older children [15]. Moreover, mothers with younger children are possibly more restricted in activity than mothers with older children because younger children need more care than older children. Therefore, it is thought that the difference in exposure levels between the two groups of children is reproduced in their mothers as well. Although hair nicotine levels of children and women in the outdoor-smoker group were lower than those with an indoorsmoking father, they were still twice as high as levels of nicotine in the hair of those with a father who does not smoke (GMR, 2.23 and 2.06, respectively). Therefore, outdoor-smoking alone is not enough to prevent unwanted exposure to SHS, and a home smoking ban is necessary to prevent it completely. These results are consistent with those from previous studies [16,17]. Nicotine content in hair may vary with growth rate or anatomical location of hair as well as the extent of exposure [18]. We collected hair samples from the back of the scalp and used entire hair shaft to reduce variability in sample collection and preparation process. In addition, gender may affect nicotine content in hair. In our study, the girls and boys were evenly distributed among groups—105 vs. 100 in total, 36 vs. 28 in the nonsmoker group, 22 vs. 22 in the outdoorsmoker group, and 28 vs. 32 in the indoor-smoker group, respectively. Exposure to SHS is related to various factors such as physical proximity to smoker, house ventilation, and duration of exposure, as well as the number of cigarettes that the father smokes at home in a day [6,19]. In addition, the reliability of parental reports is also a considerable factor in assessing SHS exposure at home. Although parental reporting based on questionnaires is a simple tool for the assessment of exposure, it is controversial as to whether this tool is reliable, especially in the quantitative assessment of exposure [20– 22]. Our results also demonstrate that parental reporting alone may seriously mislead the evaluation of SHS exposure as in our settings, and objective measures such as smoking biomarkers is warranted. The findings of this study are limited in the following aspects. First, exposure to SHS and nicotine levels can be better correlated when hair nicotine levels are adjusted for melanin levels because hair pigmentation influences nicotine incorporation into hair [4,18]. Further analyses of melanin content are necessary to consider the influence of hair pigmentation. Second, our analysis did not simultaneously consider sociodemographic characteristics such as annual income and educational status, which can influence smoking behavior and exposure to SHS [4]. In summary, our findings indicate that paternal smoking at home leads to significant exposure to SHS in their children and spouses, and preschool children are most susceptible to SHS exposure among nonsmoking household members. Also, we have shown that outdoorsmoking is not enough to completely prevent this exposure. Acknowledgement

Fig. 2. Nicotine concentrations (ng/mg hair) of nonsmoking household members in the indoor-smoker group. The box plots from left to right denote preschool children, school children, mothers of preschool children, and mothers of school children, respectively.

This work was supported by research grants from the National Cancer Center (N0610010), Korea.

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