Maternal Smoking in Pregnancy and Externalizing Behavior in 18-Month-Old Children: Results From a Population-Based Prospective Study KIM STENE-LARSEN, M.SC., ANNE I.H. BORGE, PH.D.,
AND
MARGARETE E. VOLLRATH, PH.D.
ABSTRACT Objective: The relation between prenatal smoking and child behavioral problems has been investigated in children of school age and older, but prospective studies in younger children are lacking. Using the population-based prospective Norwegian Mother and Child Cohort Study, we examined the risk for externalizing behaviors among 18-month-old children after exposure to maternal smoking during pregnancy. Method: Participants were 22,545 mothers and their 18-month-old children. Mothers reported their smoking habits at the 17th week of gestation and their child’s externalizing behavior at 18 months of age by means of standardized questionnaires. Data were analyzed using logistic regression, with scores of externalizing behavior above the 88.6th percentile as the dependent variable and self-reported smoking as the independent variable. We examined the child’s sex as a possible moderator. Results: We documented a threshold effect of smoking 10 cigarettes or more per day during pregnancy on subsequent externalizing behaviors among 18-month-old children, even after adjusting for relevant confounders (odds ratio 1.32, 95% confidence interval 1.03Y1.70). The child’s sex did not moderate these effects (odds ratio 0.98, 95% confidence interval 0.83Y1.16). Conclusions: Maternal smoking during pregnancy increases offspring’s subsequent risk for externalizing behavior problems at 18 months of age. The pattern of risk does not differ between boys and girls. Our findings suggest a population attributable risk of 17.5% (i.e., the proportion of externalizing cases that could potentially be avoided if prenatal smoking was eliminated or reduced to fewer than 10 cigarettes per day). J. Am. Acad. Child. Adolesc. Psychiatry, 2009;48(3):283Y289. Key Words: maternal smoking, pregnancy, externalizing behavior, sex differences, Child Behavior Checklist.
The risks associated with smoking are now well known. Despite this knowledge, many women who smoke continue to do so during pregnancy.1 Because nicotine crosses the placenta, smoking has the potential to harm the fetus in several ways.2 Babies born to women who Accepted November 1, 2008. Mr. Stene-Larsen and Dr. Vollrath are with the Norwegian Institute of Public Health, Department of Psychosomatics and Health Behavior; Dr. Borge is with the Psychological Institute, University of Oslo. The Norwegian Mother and Child Cohort Study is supported by the Norwegian Ministry of Health, NIH/NIEHS (grant no N01-ES-85433), NIH/ NINDS (grant no.1 UO1 NS 047537-01), and the Norwegian Research Council/FUGE (grant no. 151918/S10). The authors thank Mr. Eivind Ystrøm for guidance on the item-response theoretical analysis. Correspondence to Kim Stene-Larsen, M.Sc., Division of Mental Health, Norwegian Institute of Public Health, Postbox 4404, Nydalen, 0403 Oslo, Norway; e-mail:
[email protected]. 0890-8567/09/00-0283Ó2009 by the American Academy of Child and Adolescent Psychiatry. DOI: 10.1097/CHI.0b013e318195bcfb
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smoke during pregnancy have higher odds for lower birth weight and below-average head circumference and are more likely to die of sudden infant death syndrome.3Y5 Recent findings also suggest that prenatal nicotine exposure alters the fetal brain permanently.6Y9 Because prenatal nicotine exposure may alter the fetal brain, it may also affect the child’s later development and behavior. Several studies have shown a link between maternal smoking during pregnancy and externalizing behavior in the child. For instance, in a prospective study conducted in children aged 3 and 5 years, researchers found an association between maternal smoking in pregnancy and later externalizing behaviors, such as aggression and hyperactivity as measured using the Child Behavior Checklist (CBCL).10 Other investigations have examined the link between maternal smoking in pregnancy and other behaviors associated with the externalizing spectrum in both children and adults. For example, maternal smoking in pregnancy has been linked to behavioral
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outcomes such as toddler negativity, psychiatric symptoms, attention-deficit/hyperactivity disorder, disruptive/ aggressive behavior, and adult criminal behavior.11Y16 Little is known about the age at which behavioral problems of children exposed to maternal smoking in pregnancy first appear. An answer to this question is important because it will contribute to our understanding of the trajectories between early exposure and later behavior, which again could have clinical implications with respect to early treatment of children at risk. The few existing studies suggest that signs of externalizing behaviors may appear early. Danish researchers investigated 1,355 children aged 3.5 years in a follow-up study and found that children who were exposed to more than 10 cigarettes daily in utero had a 60% increased risk for developing behaviors such as hyperactivity, inattention, impulsivity, and hostile aggression.17 Other researchers have also found increased risk for physical aggression18,19 and disruptive behaviors20 in toddlers that have been exposed to maternal smoking in pregnancy. The findings of some studies suggested that the effects of maternal smoking during pregnancy on externalizing behavior may be specific for boys. A review article concluded thatVdespite diverging evidenceVmost studies showed a higher risk for boys.21 However, some recent studies found that the effects of prenatal smoking with respect to externalizing behavior are equal for girls and boys.10,22,23 However, several methodological shortcomings limit the generalizability of these findings. Many studies focused on older children and adults,24Y26 thereby leaving ample room for confounding effects of other risk factors occurring after the child’s birth. One of the studies that examined children younger than 2 years included only 92 cases, which reduced its generalizability.27 Other studies10 did not adjust for important confounding variables when analyzing sex-specific effects of maternal smoking during pregnancy. Such confounders having an impact on child externalizing behavior are the child’s sex,23 low birth weight,22 preterm delivery,24 mother’s level of education,26 mother’s alcohol use during pregnancy,25 being a single parent,28 mother’s current smoking,29 and mother’s mood.30,31 Recent findings also point to the importance of testing whether certain variables moderate the effect of maternal smoking in pregnancy on child externalizing behavior. Both maternal antisocial behavior18 and the mothers’ socioeconomic status32 have been found to in-
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teract with the effects of maternal smoking. To obtain a complete picture of the effects of maternal smoking in pregnancy on child externalizing behavior, both confounding factors and possible moderating variables must be targeted. The present study investigated in a large prospective population study whether maternal smoking in pregnancy increases the risk for externalizing behavior in 18-month-old children, while controlling for other well-known risk factors. Moreover, the study investigated whether the effect of smoking on externalizing behavior was moderated by the child’s sex, the mother’s mood, or the mother’s level of education. METHOD Study Design and Participants The data collection was conducted as part of the Norwegian Mother and Child Cohort Study (www.fhi.no/morogbarn) at the Norwegian Institute of Public Health. The target population of the Norwegian Mother and Child Cohort Study study is all women who give birth in Norway. Recruitment started in 1999 and will continue until the end of 2008. The sampling frame comprises all pregnant woman attending routine ultrasound examinations, which are performed at gestation weeks 17 to 18. The participation rate at first assessment is 42.7%.33 The assessment points are at the 17th and 30th gestation weeks and at child age of 18 months. Mothers responded to mailed questionnaires at each assessment, with response rates of 95%, 92%, and 77%, respectively.33 In addition, the present study used data from the Medical Birth Registry of Norway, which contains information about all births in Norway.34 For the present study, information was available from 24,901 mothers who had completed the questionnaires at all three assessment points. Because of missing data in one or more of the central variables, such as smoking or child externalizing problems, 2,356 mothers had to be excluded. Thus, the final sample included 22,545 mothers and their child (51% boys and 49% girls), for which complete information at all three assessments was available. Measures Externalizing behavior was assessed at child age 18 months by means of 8 items from the CBCL for ages 1.5 to 5 years (CBCL/ 1.5Y5).35 The items used were as follows: "Doesn’t seem to feel guilty after misbehaving," "Punishment doesn’t change his/her behavior," "Defiant," "Hits others," "Doesn’t get along with other children," "Can’t sit still, restless or hyperactive," "Can’t concentrate, can’t pay attention for long," and "Quickly shifts from one activity to another." The items were chosen to represent the CBCL 1.5Y5 Externalizing subscales of oppositional behavior (items 1Y3), aggressive behavior (items 4Y5), and overly active behavior (items 6Y8). The use of selected items was necessary because of the questionnaire space restrictions that are typical for large interdisciplinary epidemiological studies. Item selection aimed at representing each subscale with 2 to 3 items that were both clinically and theoretically relevant for externalizing behavior and based on a consensus among specialists in clinical and developmental psychology.
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Mothers were asked to report the extent to which they agreed with the eight behavioral statements on a three-point Likert scale with the answer format not true (1), somewhat or sometimes true (2), and very true or often true (3). Items were summed up to a scale ranging from 8 to 23. The internal consistency of the scale was relatively low (Cronbach ! = .57) and could not be improved by eliminating single items. Therefore, we investigated whether the scale had higher local reliability at certain points on the scale. An item response theoretical36,37 analysis revealed that the scale had high local reliability at and above 1 SD of the mean. In other words, the scale was good in discriminating the children with the highest scores from the rest. In view of the skewed distribution of the scale, and to identify children with clinically significant scores, we dichotomized the externalizing scale in the range where the reliability was highest (in effect at the 88.6th percentile). Although this cutoff point is arbitrary, our analysis showed that varying the cutoff points or using a continuous score did not yield substantially different results. Maternal smoking in pregnancy was assessed by means of the questionnaire administered at the 17th week of gestation. Mothers were asked to report whether they smoked at all, if they smoked occasionally, or if they smoked daily, andVif soVto report the number of cigarettes that they smoked each day. In addition, the mothers were asked to report how many cigarettes they smoked each week. To reduce the number of missing values, data from the questionnaire were cross-checked with the information on smoking that mothers reported to a midwife during a face to face interview when hospitalized to give birth; this information was collected from the Medical Birth Registry of Norway. Because the number of cigarettes showed an uneven distribution, with a clear clustering of mothers smoking either zero or less than 10 cigarettes (the typical pack size in Norway), we constructed a smoking variable with three categories: 0 cigarettes, 1 to 9 cigarettes, and 10 or more cigarettes. This categorization of maternal smoking during pregnancy has been used previously.17 Occasional smokers were categorized as either smoking 1 to 9 cigarettes per day or more than 10 cigarettes per day, depending on the total number of cigarettes they reported to smoke each week. Mothers’ current smoking was assessed when the child was 18 months old by means of a question inquiring whether they smoked at all, if they smoked occasionally, or if they smoked daily andVif soVto report the number of cigarettes that they smoked each day. We defined mothers’ current smoking as a variable with three categories: 0 cigarettes, 1 to 9 cigarettes, and 10 or more cigarettes. Because information on weekly smoking was lacking in this questionnaire, the occasional smokers (n = 1,598) were excluded from this variable. Mothers’ alcohol use during pregnancy was assessed at the 30th week of gestation. Mothers reported how often they drank alcohol during three distinct periods of pregnancy, from 0 to 12 weeks of gestation, 13 to 24 weeks of gestation, and after the 25th week of gestation. There were seven answer categories: never drank alcohol, drank alcohol less than once per month, drank alcohol one to three times per month, drank alcohol once per week, drank alcohol two to three times per week, drank alcohol four to five times per week, and drank alcohol six to seven times each week. Mothers’ mood was measured when the child was 18 months old using a short version of the Hopkins Symptom Checklist (SCL). The short version of the checklist used, the SCL-8, is a self-administered instrument designed to measure psychological distress, particularly anxiousness and depressiveness. The developers of this short version chose the eight items by means of a regression analysis of all items from the depression and anxiety subscales in a Norwegian study.38 A
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typical item of the SCL-8 is "worrying too much about things." Each item has four response categories ranging from not at all to severe. In the present study, the internal consistency of the SCL-8 was ! = .85. Mothers’ highest level of education was measured in the 17th week of gestation and was defined as a 4-point categorical variable that included years of education, including college and university studies. The categories were as follows: fewer than 10 years of education, 10 to 12 years of education, 13 to 15 years of education, and more than 15 years of education. Marital/partner status was assessed when the child was 18 months old. Response categories were as follows: married, having a common law partner, single, separated/divorced, and widowed. We categorized as single parents mothers who reported their marital/partner status as single, separated/divorced, or widowed. Information regarding the child’s birth weight, sex, and preterm status was retrieved from the Medical Birth Registry of Norway. In accordance with the guidelines of the World Health Organization,39 we defined low birth weight as weight at birth of less than 2,500 g (5.5 lb) and preterm status as birth before gestation week 37 (Table 1). Statistical Analysis To investigate the relation between maternal smoking in pregnancy and externalizing behavior in the 18-month-old children, logistic regression analyses were performed in the full sample. The interaction effects of smoking with child’s sex, mother’s mood, and mother’s level of education on externalizing behavior were examined separately by means of entering interaction terms40 into three TABLE 1 Main Characteristics of the Study Participants (N = 22,545) Characteristics n % Mother’s education, y Less than 10 10Y12 13Y15 More than 15 Single parent Maternal mood (mean, SD) Smoking in pregnancy, per day 0 cigarettes 1Y9 cigarettes 10Y41 cigarettes Current smoking, per day 0 cigarettes 1Y9 cigarettes 10Y41 cigarettes Child’s sex Boys Girls Externalizing behavior Boys with scores Q 88.6th percentile Girls with scores Q 88.6th percentile Birth weight, e2,500 g Gestational age, e37 wk
813 8,157 9,238 3,823 797
3.7 37.0 41.9 17.4 3.6 (10.2, 2.9)
19,510 2,101 848
86.9 9.4 3.8
18,031 2,838 1,676
80.0 12.6 7.4
11,543 10,999
51.2 48.8
1,450 1,126 722 1,164
12.6 10.3 3.2 5.2
Note: Sample size varies depending on the number of participants answering the specific question.
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separate logistic regression analyses. All analyses were adjusted for relevant confounders. RESULTS
We found that 86.9% of the mothers did not smoke during pregnancy, 9.4% smoked 1 to 9 cigarettes daily, and 3.8% smoked more than 10 cigarettes daily. In line with earlier findings, the present study found a significant sex difference in the distribution of the externalizing behaviors (x = 413.9, p = .000), with boys being overrepresented among those with the highest scores of the scale.41 The logistic regression analyses in the total sample (Table 2) also showed a noticeable significant effect of maternal smoking during pregnancy on externalizing behavior in the 18-month-old children. Smoking fewer than 10 cigarettes daily during pregnancy did not increase the child’s risk for externalizing behavior. However, smoking 10 cigarettes or more daily increased the risk for extreme scores on the externalizing scale by 32%Vafter adjusting for important confounders. We did not find any interaction effects of smoking and child’s sex on TABLE 2 Logistic Regression Analysis of Maternal Smoking in Pregnancy and Externalizing Behavior in Children, Adjusted for Relevant Confounders 95% Odds Confidence Variables Ratio Interval Maternal prenatal smoking (reference = none) 1Y9 cigarettes per day 1.12 10Y41 cigarettes per day 1.32* Mother’s current smoking (reference = none) 1Y9 cigarettes per day 0.98 10Y41 cigarettes per day 1.15 Child’s sex (reference = female) 1.26*** Mother’s depressed mood (per unit 1.10*** increase in the Hopkins Symptom ChecklistY8) Alcohol use in pregnancy (reference = none) Week 0Y12 1.05 Week 13Y24 0.82* Week 25+ 1.05 Level of educationa (reference e 10 y) 0.84*** Single parent 0.85 Gestational week, e37 wk 1.15 Birth weight, e2,500 g 0.93 a
0.94Y1.35 1.03Y1.70 0.84Y1.15 0.94Y1.42 1.15Y1.38 1.09Y1.12
0.98Y1.13 0.68Y0.98 0.89Y1.24 0.79Y0.89 0.66Y1.08 0.90Y1.48 0.68Y1.29
Levels of education are less than 10 years, 10 to 12 years, 13 to 15 years, and more than 15 years. *p < .05; **p < .01; ***p < .001.
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externalizing behavior (odds ratio [OR] 0.98, 95% confidence interval [CI] 0.83Y1.16). Nor did we find any effects of the interaction between smoking and mothers’ mood on externalizing behavior (OR 0.99, 95% CI 0.97Y1.01) nor of smoking and level of education on externalizing behavior (OR 0.93, 95% CI 0.83Y1.05). To calculate the population attributable risk percent,42 we first calculated the population attributable risk by subtracting the incidence of externalizing behavior among those unexposed to smoking in pregnancy from the incidence of externalizing behavior in the total population. We then divided this number by the incidence of externalizing behavior in the total population and multiplied this by 100. The population attributable risk percent calculation revealed that 17.5% of the externalizing cases could be avoided if smoking was eliminated or reduced to smoking fewer than 10 cigarettes per day. DISCUSSION
The main goal of this study was to explore whether an association between maternal smoking in pregnancy and externalizing behavior can be documented in children as young as 18 months old. A further goal of this study was to examine whether maternal smoking in pregnancy constitutes a general or sex-specific risk. Indeed, we could show that maternal smoking in pregnancy increased the risk for externalizing behavior in 18-month-old children after adjusting for important confounders. Smoking showed a threshold effect, predicting externalizing behavior only if the mothers had smoked at least 10 cigarettes daily during pregnancy. This effect was not moderated by the child’s sex, mothers’ mood, or mothers’ level of education. Our findings are important because they are based on the largest population-based prospective study ever on the effects of maternal smoking during pregnancy on later behavior problems. Extending the findings of earlier studies with toddlers and children,10,13,26,43 we could show for the first time in such a large prospective cohort study that behavioral deviations after maternal smoking in pregnancy can be observed in children younger than 2 years. These findings lend support to previous studies on maternal smoking in pregnancy and externalizing behaviors in children younger than 2 years.18,19 Our findings also lend support to the minority of studies that found that maternal smoking in pregnancy was associated with increased risk for both boys and girls.10,13,43
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The finding that exposure to maternal smoking in pregnancy increased the risk for externalizing problems in both girls and boys is at odds with findings from most studies in the field.21 However, it is possible that the excellent statistical power resulting from our large sample size was crucial for this finding. As pointed out by the authors of several review articles on this topic,21,26 most of the studies on maternal smoking and later externalizing behaviors had low statistical power. This may have led to a bias in past research in direction of only discovering the risk in boys because the behavior in question is much more frequent in boys.23 The discrepancy in sex differences between studies may also stem from the developmental period in which the externalizing behavior was measured. Longitudinal studies of sex-specific trajectories in externalizing behavior after prenatal smoke exposure may help to answer this question. It is also important to note that the construct of externalizing behavior changes with age. Externalizing behavior in infants and toddlers has a different manifestation from externalizing behavior in older children and adults. In this study, we did not find that the mother’s level of education or her mood moderated the effect of maternal smoking in pregnancy on child externalizing behavior. These results contradict earlier findings.18,32 In Norway, the negative impact of low education and low income on health may be reduced by the existence of excellent social services provided by the government. The stress normally associated with low education and low income in other countries may therefore have a weaker impact on the mother’s mental health and behavior in our material. Another possibility is that the mothers in our sample represent a selected group with more than average psychological resources. Still, the variation we found with respect to negative mood and education should have allowed us to detect effects on externalizing behavior. With regard to the threshold effect setting in at 10 cigarettes smoked per day, earlier studies diverge, some finding a dose-response relation and some finding a threshold effect similar to the one documented by this study.10,13,15 The reason for this divergence may be related to differences in the intake of nicotine and other compounds among various cigarette brands preferred by women in different countries and samples because these can be large.44,45 These brand differences influence the number of cigarettes smoked and the amount of
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nicotine absorbed in the mother’s lungs, which, in turn, may influence the degree of fetal exposure. Therefore, comparison of nicotine intake across different studies is exceedingly difficult, as is the interpretation of doseresponse or threshold effects. It has also been documented that mother’s degree of smoking fluctuates to a great degree during pregnancy.46 This constitutes a general problem related to correctly classifying women as either mild or heavy smokers because the mother may change groups several times during pregnancy. The effects of misclassifying the mothers may be either to underestimate or to overestimate the effects of smoking on child externalizing behavior. Obtaining a good measure of maternal smoking in pregnancy is difficult. Individual differences in nicotine metabolism47 and brand differences44 further complicate the picture, and these aspects should therefore be taken in consideration when interpreting the results. The mechanisms by which smoking may affect later behavioral problems were discussed in a review article on the topic.48 One of these mechanisms is that the mother’s smoking causes a restriction of blood flow to the placenta and hence reduces the amount of oxygenrich blood available for the fetus. Lack of oxygen-rich blood is suspected to impair the child’s neurodevelopment, which may, over time, dispose the child to later behavioral disorders. Another mechanism discussed pertains to direct interactions of nicotine with the child’s acetylcholine receptors in the brain, a specific receptor system that is present early in fetal development. This interaction may lead to permanent changes in receptor levels in the brain and possibly make the child more prone to developing behavioral problems. Moreover, researchers discussed the harmful effects of carbon monoxide (another compound in cigarettes) on fetal neurodevelopment. A major difficulty consists, however, in separating out the effects of nicotine exposure from those of genetic and other environmental factors. On the one hand, externalizing behavior is heritable,49 but on the other hand, it is related to a higher propensity to smoke.50 Thus, the effects of maternal externalizing behavior problems may be transmitted both genetically and environmentally through maternal smoking. In our study, we did not have the possibility to separate the environmental effects from the genetic, but other researchers have found that maternal smoking during pregnancy
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had an independent effect on later externalizing behavior when studying twins with externalizing behavior.49 This finding suggests that maternal smoking does have harmful effects on the fetus in its own right. A further limitation results from our use of a short version of the CBCL (CBCL/1.5Y5) externalizing scale to assess the child’s behavior. The short scale is not as comprehensive as desirable. However, our findings produced substantial ORs, the sizes of which were in line with those found in earlier studies10,13 Also, mothers may have systematically underreported their amount of smoking because smoking during pregnancy is considered irresponsible behavior by health personnel in Norway. This may have caused weaker associations between maternal smoking during pregnancy and later externalizing behavior in the children. Another limitation results from using mothers as the only source of information on their child’s behavior. In general, parental reports on their child’s behavior need to be interpreted with caution, because they may partly reflect the parents’ own characteristics. Despite these limitations, there are important aspects of our study that lend credibility to our results. The sheer size of our sample gave us enough statistical power to examine interaction effects while taking into account a range of confounders. Moreover, the study is truly prospective, and the assessment of both the predictors and the outcomes occurred concurrently with the variables in question. Finally, information on important confounders such as birth weight, prematurity, and other medical variables relied on objective data collected by health personnel. Although we do not know how many of the children showing early signs of behavioral problems after maternal smoking during pregnancy will develop persistent problems in later childhood, early identification could be important. It could give health personnel the opportunity to intervene at an early stage in development and to increase the chances of successful treatment.28 Although we found a threshold effect for smoking rather than a dose-response effect, there is no reason to Ballow[ mothers to smoke a little, rather than not at all. First of all, smoking has so many negative effects on the unborn child’s health that every cigarette that can be avoided should be avoided. Moreover, on a population basis, eliminating smoking entirely has the potential to reduce the prevalence of externalizing behaviors among toddlers by 17.5%, which is a substantial number. Increased
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effort to reduce smoking during pregnancy could have considerable preventive effects on the development of externalizing behaviors in children and would probably save society a great deal of money spent on treatment. To conclude, our findings have several implications for future research. The finding that the effect of prenatal smoking on externalizing behavior is evident in children as young as 18 months old opens up the possibility to investigate the developmental pathway of externalizing behavior in this group of children. A central issue will be the extent to which these behaviors persist into school age, adolescence, and adulthood. Moreover, factors from the child’s environment that contribute to either improvement or deterioration of these behavior problems ought to be identified. Future research could also investigate whether children exposed to maternal smoking during pregnancy with extreme scores on externalizing behavior differ from children with extreme scores on externalizing behavior not exposed to maternal smoking during pregnancy. Disclosure: The authors report no conflicts of interest. REFERENCES 1. Ebrahim S, Floyd L, Merrit R, Decoufle P, Holtzman D. Trends in pregnancy-related smoking rates in the United States, 1987Y1996. JAMA. 2000;283:361Y366. 2. Nekhayeva IA, Nanovskaya TN, Pentel PR, Keyler DE, Hankins GDV, Ahmed MS. Effects of nicotine-specific antibodies, Nic311 and NicIgG, on the transfer of nicotine across the placenta. Biochem Pharmacol. 2005;70:1664Y1672. 3. Horne RSC, Franco P, Adamson TM, Groswasser J, Kahn A. Influences of maternal cigarette smoking on infant arousability. Early Hum Dev. 2004;79:49Y58. 4. Kallen K. Maternal smoking during pregnancy and infant head circumference at birth. Early Hum Dev. 2000;58:197Y204. 5. Secker-Walker RH, Vacek PM. Relationships between cigarette smoking during pregnancy, gestational age, maternal weight gain, and infant birthweight. Addict Behav. 2003;28:55Y66. 6. Abdel-Rahman A, Dechkovskaia AM, Sutton SM et al. Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrallary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty. Toxicology. 2005;209:245Y261. 7. Falck L, Nordberg A, Seiger Å, Kjældgaard A, Hellstrøm-Lindahl E. Smoking during early pregnancy affects the expression pattern of both nicotine and muscarinic acetylcholine receptors in human first trimester brainstem and cerebellum. Neuroscience. 2005;132:389Y397. 8. Hasan SV, Simakagornboon N, Mackinnon Y, Gozal D. Prenatal cigarette smoke exposure selectively alters protein kinase c and nitric oxide synthase expression within the neonatal rat brainstem. Neurosci Lett. 2001;301:135Y138. 9. Jankunen S, Tuominen RK, Piepponen TP, Aktee L. Nicotine and epibatidine alter differently nomifensine-elevated dopamine output in the rat dorsal and ventral striatum. Eur J Pharmacol. 2005;511:143Y150. 10. Ho¨o¨k B, Cederblad M, Berg R. Prenatal and postnatal maternal smoking as risk factors for preschool children’s mental health. Acta Paediatr. 2006;95:671Y677.
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MATERNAL SMOKING AND CHILD BEHAVIOR 11. Brennan P. Tobacco consumption during pregnancy and its impact on psychosocial child development. Encyclopedia on Early Childhood Development (Online) Revised Edition. In: Trembley RE, Barr RG, Peters R, eds. 2005. Accessed April 15, 2008. 12. Brook JS, Brook DW, Whiteman M. The influence of maternal smoking during pregnancy on toddler‘s negativity. Arch Pediatr Adolesc Med. 2000;154:381Y385. 13. Indredavik MS, Brubakk AM, Romundstad P, Vik T. Prenatal smoking exposure and psychiatric symptoms in adolescence. Acta Paediatr. 2006;96:377Y382. 14. Nigg JT, Breslau N. Prenatal smoking exposure, low birth weight, and disruptive behavior disorders. J Am Acad Child Adolesc Psychiatry. 2007;46:362Y369. 15. Schmitz M, Denardin D, Silva TL et al. Smoking during pregnancy and attention-deficit/hyperactivity disorder, predominantly inattentive type: a case-control study. J Am Acad Child Adolesc Psychiatry. 2006;45: 1338Y1345. 16. Wakschlag LS, Pickett KE, Kasza KE, Loeber R. Is prenatal smoking associated with a developmental pattern of conduct problems in young boys? J Am Acad Child Adolesc Psychiatry. 2006;45:461Y467. 17. Linnet KM, Obel C, Bonde E et al. Cigarette smoking during pregnancy and hyperactive-distractible preschooler’s: a follow-up study. Acta Paediatr. 2007;95:694Y700. 18. Huijbregts SC, Seguin JR, Zoccolillo M, Boivin M, Tremblay RE. Maternal prenatal smoking, parental antisocial behavior, and early childhood physical aggression. Dev Psychopathol. 2008;20:437Y453. 19. Tremblay RE, Nagin DS, Seguin JR et al. Physical aggression during early childhood: trajectories and predictors. Pediatrics. 2004;114: e43Ye50. 20. Wakschlag LS, Leventhal BL, Pine DS, Pickett KE, Carter AS. Elucidating early mechanisms of developmental psychopathology: the case of prenatal smoking and disruptive behaviour. Child Dev. 2006;77:893Y906. 21. Wakschlag LS, Pickett KE, Cook E, Benowitz NL, Leventhal BL. Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. Am J Public Health. 2002;92:966Y974. 22. Mick E, Biederman J, Prince J, Fischer MJ, Faraone SV. Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr. 2002;23:16Y22. 23. Moffitt TE, Caspi A, Rutter M, Silva PA. Sex Differences in Antisocial Behavior: Conduct Disorder, Delinquency and Violence in the Dunedin Longitudinal Study. Cambridge: Cambridge University Press; 2001. 24. Bhutta AT, Cleves MA, Casey PH, Gradock MM, Anand KJS. Cognitive and behavioral outcomes of school-aged children who were born preterm. JAMA. 2002;288:728Y737. 25. Eckard MJ, File SE, Gessa GL et al. Effects of moderate alcohol consumption on the central nervous system. J Child Psychol Psychiatry. 1998;47:313Y337. 26. Linnet KM, Dalsgaard S, Obel C et al. Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry. 2003;160: 1028Y1040. 27. Cummings EM, Davies PT. Maternal depression and child development. J Child Psychol Psychiatry. 1994;35:73Y122. 28. Webster-Stratton C. Preventing conduct problems in head start children: strengthening parenting competencies. J Consult Clin Psychol. 1998; 66:715Y730. 29. Williams GM, O’Callaghan M, Najman JM et al. Maternal cigarette smoking and child psychiatric morbidity: a longitudinal study. Pediatrics. 1998;102:e11. 30. Cummings EM, Davies PT. Maternal depression and child development. J Child Psychol Psychiatry. 1994;35:73Y122. 31. Maughan B, Taylor A, Caspi A, Moffitt TE. Prenatal smoking and early
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