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Prenatal Active or Passive Tobacco Smoke Exposure and the Risk of Preterm Delivery or Low Birth Weight

Windham, Gayle C1; Hopkins, Barbara1; Fenster, Laura1; Swan, Shanna H2

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From the 1Reproductive Epidemiology Section, Department of Health Services, Oakland, California, and the 2University of Missouri, Columbus, Missouri.

Submitted June 21, 1999; final version accepted January 4, 2000.

Address correspondence to: Gayle C. Windham, Reproductive Epidemiology Section, Department of Health Services, 1515 Clay Street, Suite 1700, Oakland, California, 94612.

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We examined the association of exposure to environmental tobacco smoke with birth weight and gestational age in a large, prospective study. We also compared these endpoints between infants of active maternal smokers and those of non-smoking, non-ETS exposed women. Pregnant women were interviewed by telephone during the first trimester, and pregnancy outcome was determined for 99%. Among the 4,454 singleton live births that could be linked to their birth certificate, we confirmed increased risks of low birth weight and small for gestational age with heavier maternal smoking (>10 cigarettes/day), as well as noting an increased risk for “very preterm” birth (<35 weeks). These associations were generally stronger among infants of older (≥30 years) than those of younger mothers, as well as among non-whites. High environmental tobacco smoke exposure (≥7 hours/day in non-smokers) was moderately associated with low birth weight (adjusted odds ratio (AOR) 1.8, 95% confidence limits (95% CL) = 0.82, 4.1), preterm birth (AOR 1.6, 95% CL = 0.87, 2.9), and most strongly with very preterm birth (AOR 2.4, 95% CL = 1.0, 5.3). These associations were generally greater among non-whites than whites. The data support earlier studies suggesting that prenatal environmental tobacco smoke exposure, in addition to maternal smoking, affects infant health.

Maternal active smoking has been associated with a number of adverse developmental and reproductive endpoints. 1–4 Infants of women who smoke during pregnancy are estimated to have twice the risk of low birth weight or an average weight decrement of 150–200 gm at birth, compared with those of non-smokers. The decrement in birth weight appears to be due primarily to intra-uterine growth retardation, and to a lesser extent to preterm birth. 5–9 Because of these relations, exposure to environmental tobacco smoke (ETS) has been of increasing concern. 10,11 Persons exposed to environmental tobacco smoke are subjected to most of the same constituents as those contained in mainstream smoke, but the pattern and amounts of exposure differ. 12 Studies of environmental tobacco smoke exposure tend to show a decrement in mean birth weight of a small magnitude and suggest a slight increase in the risk of low birth weight. 11,13–26 Many studies, however, were based on only crude measures of ETS exposure, such as paternal smoking. Fewer studies have examined ETS exposure and preterm birth, some of which found moderately increased risks. 13,22,27

Some studies of maternal smoking or ETS exposure have shown greater effects in older women. 27–29 Furthermore, a few studies have indicated that blacks have higher levels of cotinine, a nicotine metabolite, than do whites at the same reported smoking level, suggesting possible differences in metabolism. 30–32 Age and race may thus modify effects of tobacco smoke exposure.

This report has several objectives. The primary one is to examine the association of ETS exposure (or passive smoking) with birth weight and gestational age in a prospective study conducted during the first trimester of pregnancy, with ETS exposure reported at home and work. Our second objective is to estimate the effects of active smoking using a non-smoke-exposed comparison group, instead of including possibly ETS-exposed women in the comparison as is done in most studies of active smoking. Another objective is to examine these associations among demographic sub-groups defined by maternal age and race.

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Subjects and Methods

Study methods have been published elsewhere, 33 but are described briefly below.

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Subject Recruitment and Endpoints

Pregnant women were recruited during 1990–1991 from a large pre-paid health plan (Kaiser Permanente Medical Care Program) in three regions of California at the time they called to make their first prenatal appointment. A prospective study design was used to obtain information on exposures early in pregnancy to avoid problems of reporting bias. Eligibility criteria included age 18 years or older, 12 weeks gestation or less and English or Spanish speaking. Telephone interviews were completed within a few weeks of initial contact for 5,342 women; 18% of the total refused, about 10% were ineligible and 3% could not be re-contacted. The median gestational age at interview was 8 weeks.

Pregnancy outcomes were ascertained primarily from computerized hospital admission files as well as by abstraction of medical records for pregnancy losses. Less than 1% of outcomes could not be determined. We limited this analysis of birth weight and preterm delivery to singleton live births. Birth weight was abstracted from the birth certificate for 4,454 births, which excludes 103 (2.3%) that could not be linked. We calculated gestational age using the date of birth as reported on the birth certificate and the 1st day of the last menstrual period as ascertained at interview preferentially, to maintain dating used throughout the interview. These were compared with gestational age as reported on the birth certificate, and in 48 births we substituted the certificate gestational age to correct an improbable calculated gestational age.

We defined low birth weight (LBW) as weight less than 2,500 gm. We examined the usual classification of preterm delivery as less than 37 weeks’ gestation, as well as an earlier cut-off at less than 35 weeks (“very preterm”) to identify infants at even higher risk of neonatal morbidity and mortality. 34 We defined small for gestational age (SGA) as birth weight less than the 10th percentile for gestational week. For this purpose, we calculated a standard from the weight distribution of the over 2 million singleton births that occurred in California during years comparable with this study (1990–93) separately for males and females, for each gestational week from 24–44.

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Exposure Assessment

The interview asked about a number of topics including demographics (eg age, race, education); reproductive history; job characteristics; physical and psychosocial stress; and water, tobacco, caffeine, and alcohol consumption. Most of the consumption questions (including amount smoked) were asked about two time periods: the week before interview (referred to here as “during” the first trimester of pregnancy) and the week at last menstrual period (“before” pregnancy). The smoking status of the infant’s father was also ascertained for the same two time periods. The number of hours per day that non-smoking respondents were near other people smoking both at home and at work, since the last menstrual period, was also asked. We summed these two variables to estimate total daily ETS exposure. These ETS variables were examined only among women who reported not smoking both before and during pregnancy. Thus, women who reported smoking at one of the time intervals, but not the other, were excluded (N = 351) to avoid potential misclassification. (Infants of these women did not generally appear at increased risk for any adverse outcome.) We created a categorical variable with six levels of smoke exposure (excluding an additional four women missing one of the smoking variables) as follows:

Among non-smokers:

1. No smoke exposure (reference): none or <0.5 hours ETS exposure/day

2. Moderate ETS: 0.5–6.5 hours ETS/day

3. High ETS: ≥7 hours ETS/day

Among smokers irrespective of ETS exposure:

4. Low smoking: <5 cigarettes/day at interview

5. Moderate smoking: 5–10 cigarettes/day at interview

6. Heavy smoking: >10 cigarettes/day at interview

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Statistical Analysis

We calculated crude rates for the four categorical endpoints as well as rate ratios and adjusted odds ratios and their 95% confidence limits (95% CL) by smoke exposure, relative to non-exposed. We assessed a variety of potential confounders, identified from the literature and univariate analyses, in logistic regression models (ie the “full” model) for each endpoint. These included: maternal age, pre-pregnancy body mass index (BMI = weight/height 2), parity and prior pregnancy loss, race, education, marital status, employment status (and hours worked), stressful life events and social support (assessed using modifications of standard instruments), 35 and caffeinated and alcoholic beverage consumption during the first trimester. We used the change in estimate method 36 to identify covariates whose exclusion from the full models changed the adjusted odds ratio for high environmental tobacco smoke or heavy smoking by 10% or more, to create a “reduced” model. The variables that met this criterion were pregnancy history for all endpoints, race for small for gestational age, stressful life events for preterm delivery, and BMI and education for very preterm delivery. We included all five in the reduced models used to calculate the adjusted odds ratios (AOR) presented, unless otherwise indicated. Potential effect modifiers of a priori interest from previous smoking studies were maternal age and race, assessed by stratification and separate models.

We determined mean birth weight for each exposure category, and we calculated the difference from the non-tobacco-exposed group. We used multivariate regression models to control for all the variables in the full model noted above. In addition we added gestational age to some models to examine effects on weight, controlling for the influence of age at delivery.

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The mothers of these live births were on average 27.8 years old, with most (90%) under 35 years. About two thirds of the women were white, one quarter were nulliparous, and most were married (83.4%). Over three quarters of the women worked during the first trimester and 60% had some education past the high school level (Table 1). In this cohort of women receiving prenatal care at a health maintenance organization, 3.2% of infants had low birth weight, 6.9% were small for gestational age, and 6.1% were born preterm, 40% of which were very preterm (or 2.4% of total). Of those with low birth weight, 65% were born preterm.

Table 1
Table 1
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About two thirds of the women reported no smoke exposure, 18% were non-smokers with some ETS exposure (or 21% of non-smokers reported ETS), and about 11% smoked during the first trimester. As shown in Table 1, reported exposure to any form of tobacco smoke decreased with increasing age and education. Asians were the least likely to report any smoke exposure whereas blacks were most likely to report exposure, particularly to ETS. Women who were not married were more likely to be exposed to either form of tobacco smoke, and women who worked were more likely to be exposed to ETS. Consumers of alcohol or caffeinated beverages were more likely to smoke, but they were not more likely to report ETS exposure.

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Mean Birth Weight

Infants of active smokers had reductions in crude mean birth weight on the order of 100–200 gm, with a dose response trend. These weight decrements were greater in the adjusted models (Table 2). Adding gestational age to the model still yielded large decrements in weight for all smoking categories. Mean birth weight varied little by ETS exposure (Table 2). When we examined home and work ETS exposures separately, we found a slight weight decrement with high exposure at home, but the confidence intervals were wide. Examining an even higher ETS exposure level, infants of the 28 women reporting 12 hours or more per day had a weight decrement of −128 gm (SE 101) or −88 gm (SE 103) when adjusted. Had we used paternal smoking status as the ETS exposure variable, the adjusted difference in mean birth weight would be about −32 gm (95% CL = −81, 18).

Table 2
Table 2
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Stratifying by race, infants of Asians and Pacific Islanders who reported high ETS exposure (≥7 hours/day) had crude birth weight reductions of up to 500 gm. Infants of exposed blacks had about a 100 gm reduction, Hispanics had little reduction and exposed whites had somewhat increased weights, compared with unexposed women of the same race. (A weight reduction of about 100 gm was seen among white infants at the higher ETS exposure level of ≥12 hours/day.) Because of small numbers in some of these categories, we compared whites with all other races. The non-whites had much greater absolute and relative crude weight decrements than whites with both high ETS exposure and heavier smoking (Table 3). Including gestational age in the models reduced the magnitude of the weight decrements more for non-whites than for whites. Stratifying by maternal age revealed a greater weight reduction with heavier smoking among older women (Table 3), which was magnified at an even greater smoking level (>20 cigarettes/day, data not shown). This age modification was not as apparent with high ETS exposure (Table 3).

Table 3
Table 3
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Low Birth Weight, Preterm Delivery and Small for Gestational Age

Increasing amount smoked was associated with an increased risk in low birth weight and small for gestational age; infants of heavy smokers had adjusted risks 2.6–4.5 times those of unexposed women (Table 4). The risk of preterm birth was not greatly increased by smoking, but the risk of very preterm birth was more than doubled among heavier smokers.

Table 4
Table 4
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High ETS exposure was associated with an increased risk of LBW on the order of that of low-moderate smoking, which was changed little by adjustment (Table 4). The adjusted odds ratio for any ETS exposure (≥1 hr/day) and LBW was 1.1 (95% CL = 0.71, 1.7). The increased risk from high ETS exposure appeared more strongly related to preterm delivery, particularly very preterm, than to growth retardation (Table 4). The adjusted odds ratio for any ETS exposure and preterm delivery was 1.2 (95% CL = 0.90, 1.7). For both low birth weight and preterm birth, risks were somewhat greater with ETS exposure at home rather than work.

Stratifying by race (Table 5) indicated that the risk of LBW from high ETS exposure was much greater in non-whites than in whites. This finding was not consistent for active smoking, but when we examined individual race categories, we found that blacks and Hispanics who were heavier smokers had crude rates of LBW that were six times those of non-exposed based on very small numbers. There was a pattern of excess risk of preterm and very preterm birth with both high ETS exposure and heavy smoking in non-whites (Table 5).

Table 5
Table 5
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Stratifying by maternal age (Table 5) indicated little age modification of the association of SGA with heavier active smoking. The risks of LBW associated with active smoking were greater among older women, but there was little difference in the association with high ETS exposure by age. The associations of preterm and very preterm birth with both active and passive smoke exposure tended to be greater in older women.

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Our strong finding of a decrement in birth weight with active smoking is consistent with the literature and was not affected materially by the exclusion of ETS-exposed women from the comparison group. Earlier findings regarding ETS and mean birth weight have varied, with some studies reporting decrements of 30–100 gm and others showing little effect. 10,11 ETS exposure has been defined in a variety of ways in these studies and effects may be missed if high exposure is not examined, as suggested here. It is highly likely that the proportion of ETS-exposed women that were highly exposed was greater in studies conducted earlier and in areas such as Europe and Asia where smoking is more pervasive than in California. 15,17–19,21–22,24–26

Offering further validation of our data, we confirmed the consistent findings of an excess risk of low birth weight, and particularly small for gestational age, with heavier smoking. 1–4 While smoking is thought to be more strongly associated with SGA, there is sufficient evidence to indicate it is moderately associated with preterm delivery. 8,9,34,37–39 In support of our finding of a doubled rate of very preterm birth (<35 weeks) among heavy smokers, other studies have reported a greater association of smoking with delivery before 33 weeks gestation than with moderate preterm delivery (33–36 weeks). 37,38

High ETS exposure was moderately related to low birth weight and particularly to very preterm birth, but not to small for gestational age. Other studies of ETS exposure and low birth weight or small for gestational age have found varying results from no effect up to about a doubling of risk. 10,11,13,14,16,17,19,20,23,25 A meta-analysis of studies published by 1995 reported pooled adjusted odds ratios from 1.1–1.4 for these endpoints. 11 Studies of preterm delivery and ETS exposure are fewer and several have found moderate associations, but none has examined earlier preterm births. 13,22,27

An effect of ETS on very preterm delivery that is of a similar magnitude as that of heavy smoking appears inconsistent. Non-smokers exposed to ETS generally have levels of cotinine, a metabolite of nicotine, that are 1–2 levels of magnitude lower than active smokers, suggesting that effects of ETS exposure should be correspondingly lower than those of active smoking. This theory presupposes a linear relationship, however, which may not be appropriate. 10,15,18 Furthermore, ETS is composed of hundreds of compounds contained in exhaled mainstream, as well as sidestream, smoke of which others besides nicotine are probable toxicants of interest (eg carbon monoxide, cadmium, polycyclic aromatic hydrocarbons). 10 These compounds are not all present in the same relative ratio as nicotine in mainstream versus sidestream smoke, 12 nor in aged ETS, so that a linear trend of effects by cotinine level might not be expected. ETS was not associated with SGA, as smoking is, but SGA has a different etiology than preterm delivery. A recent study of breast cancer similarly found an odds ratio for passive smoking that was of the same magnitude as that for active smoking. 40

The associations we found with high ETS exposure appeared limited to non-whites for the most part, which was not explained by a differential exposure distribution within this high category. There was generally a similar pattern of race-modification for heavy smoke exposure, but the number of non-whites in this group was small and estimates less stable. A previous U.S. study 19 reported that ETS and LBW were more strongly associated in non-whites than in whites. Several other studies 31,41–43 found few racial differences in the effects of active smoking on low birth weight or small for gestational age, but mean birth weight does not appear to have been examined in this way. There is some evidence that blacks metabolize nicotine differently than whites. 30–32 Data on other specific ethnic groups is not readily available, so our preliminary data suggesting some differential effects by ethnicity (including Hispanics and Asians) is of interest.

Our finding of generally greater effects of heavy smoking among older mothers did not appear to be explained by a differential distribution of smoking within this high category and is supported by several other studies. 28,29,44 Such an effect may be due to cumulative exposure over years or perhaps to diminished reserves to compensate for the toxic effects of smoking among older mothers. A recent U.S. study 27 found some age modification of ETS exposure with both LBW and preterm delivery in a low income population, but two other studies did not and we found it only for preterm birth. 18,45

Although our ascertainment of ETS exposure was more detailed than in many previous studies, it was based on self-report of hours exposed and did not include exposure outside home or work. The associations of low birth weight and preterm birth with high ETS exposure were not dependent on the cutpoint selected, as similar increases in risk were seen at 5 or more hours/day. Decreases in mean birth weight, however, were not observed until ETS exposure levels were much greater, highlighting possible difficulties in across-study comparisons of self-reported exposure. Another limitation was that exposure was assessed during the first trimester of pregnancy. Many pregnant women have already changed their smoking habits by this time, 46 but in an interview we conducted during the third trimester (or post-natally) on a sub-set of this sample, about one third of first-trimester smokers did not report any smoking in the last 3 months of pregnancy; some of this may reflect retrospective reporting errors. Nevertheless, the associations we found based on first trimester smoking may be underestimated (eg a conservative bias) if quitting later decreases risk. It is unlikely that many women started smoking later in pregnancy, so associations with ETS exposure examined among non-smokers should not be greatly affected. We did not ask about ETS exposure in the third trimester re-interview and there is little other data on the consistency of ETS exposure during pregnancy, so some misclassification may exist.

Another possible source of error is misclassification of outcome. We did not have information from medical records to verify gestational age. As several authors 47,48 have recommended updating fetal growth curves and California has an unusual racial distribution (more Hispanic births), we calculated a new standard for California. The weight-for-age cutpoints were similar to, but consistently slightly higher than, recent U.S. and Canadian standards. 47,48 This HMO-based population had generally low risks of the adverse outcomes examined, perhaps due to early, routine prenatal care and/or lack of extreme socioeconomic disadvantages, which limited the power for sub-group analyses at higher smoke exposure levels. Although we were able to examine many potential confounders, including some on stress, exertion, and socioeconomic factors, residual confounding may influence the results. We had no data on history of other diseases, particularly sexually transmitted diseases, which may play a role in preterm delivery, or on the specific causes of preterm birth.

The strengths of this study are many, including the prospective design, nearly complete follow-up of all pregnancy outcomes, and a population with equal access to medical care that should decrease possible confounding effects of socio-demographic variables on exposure status.

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We thank Kirsten Waller for her work in assigning gestational age and final pregnancy outcome. Financial support from the Packard Family Foundation allowed completion of data collection. We also acknowledge the contributions of the Kaiser clinics involved in patient recruitment and investigators at Kaiser Division of Research, including Catherine Schaefer and Robert Hiatt.

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Science of the Total Environment
Associations among genetic susceptibility, DNA damage, and pregnancy outcomes of expectant mothers exposed to environmental tobacco smoke
Wu, FY; Wu, HDI; Yang, HL; Kuo, HW; Ying, JC; Lin, CJ; Yang, CC; Lin, LY; Chiu, TH; Lai, JS
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International Journal of Environmental Research and Public Health
Maternal Smoking, GSTM1 and GSTT1 Polymorphism and Susceptibility to Adverse Pregnancy Outcomes
Grazuleviciene, R; Danileviciute, A; Nadisauskiene, R; Vencloviene, J
International Journal of Environmental Research and Public Health, 6(3): 1282-1297.
Scandinavian Journal of Work Environment & Health
Effects of environmental tobacco smoke on the respiratory health of children
Jaakkola, JJK; Jaakkola, MS
Scandinavian Journal of Work Environment & Health, 28(): 71-83.

Effects of long-term passive smoking on the diameter of glomeruli in rats: Histopathological evaluation
Dundar, M; Kocak, I; Culhaci, N
Nephrology, 9(2): 53-57.

Maternal/newborn GSTT1 null genotype contributes to risk of preterm, low birthweight infants
Nukui, T; Day, RD; Sims, CS; Ness, RB; Romkes, M
Pharmacogenetics, 14(9): 569-576.

Environmental Health Perspectives
Origins and evolution of children's environmental health
Lanphear, BP
Environmental Health Perspectives, (): 24-32.

Archives of Pediatrics & Adolescent Medicine
Effect of gestational and passive smoke exposure on ear infections in children
Lieu, JEC; Feinstein, AR
Archives of Pediatrics & Adolescent Medicine, 156(2): 147-154.

Pediatric Nephrology
Nephron number and blood pressure in rat offspring with maternal high-protein diet
Zimanyi, MA; Bertram, JF; Black, MJ
Pediatric Nephrology, 17(): 1000-1004.
Archives of Disease in Childhood
Adverse health effects of prenatal and postnatal tobacco smoke exposure on children
Hofhuis, W; de Jongste, JC; Merkus, PJFM
Archives of Disease in Childhood, 88(): 1086-1090.

Annals of Epidemiology
CYP1A1 gene polymorphisms in modifying the association between passive smoking and primary dysmenorrhea
Li, N; Liu, H; Chen, CZ; Yang, F; Li, ZP; Fang, Z; Wang, LH; Hu, YH; Chen, DF
Annals of Epidemiology, 17(): 882-888.
American Journal of Epidemiology
Adverse birth outcomes associated with maternal smoking and polymorphisms in the N-nitrosamine-metabolizing enzyme genes NQO1 and CYP2E1
Sasaki, S; Sata, F; Katoh, S; Saijo, Y; Nakajima, S; Washino, N; Konishi, K; Ban, S; Ishizuka, M; Kishi, R
American Journal of Epidemiology, 167(6): 719-726.
Environmental Health Perspectives
Association between Local Traffic-Generated Air Pollution and Preeclampsia and Preterm Delivery in the South Coast Air Basin of California
Wu, J; Ren, CZ; Delfino, RJ; Chung, J; Wilhelm, M; Ritz, B
Environmental Health Perspectives, 117(): 1773-1779.
Acta Obstetricia Et Gynecologica Scandinavica
Environmental tobacco smoke exposure and perinatal outcomes: a systematic review and meta-analyses
Salmasi, G; Grady, R; Jones, J; McDonald, SD
Acta Obstetricia Et Gynecologica Scandinavica, 89(4): 423-441.
American Journal of Respiratory and Critical Care Medicine
Environmental epigenetics and asthma - Current concepts and call for studies
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American Journal of Respiratory and Critical Care Medicine, 177(6): 567-573.
Ginekologia Polska
The influence of social and health factors including pregnancy weight gain rate and pre-pregnancy body mass on low birth weight of the infant
Wlodzimierz, B; Hanna, M
Ginekologia Polska, 79(6): 415-421.

Journal of Pharmaceutical and Biomedical Analysis
Nicotine exposure can be detected in cerebrospinal fluid of active and passive smokers
Malkawi, AH; Al-Ghananeem, AM; de Leon, J; Crooks, PA
Journal of Pharmaceutical and Biomedical Analysis, 49(1): 129-132.
Fetal Diagnosis and Therapy
Should We Customize Fetal Growth Standards?
Figueras, F; Gardosi, J
Fetal Diagnosis and Therapy, 25(3): 297-303.
Obstetrics and Gynecology
An Integrated Intervention to Reduce Intimate Partner Violence in Pregnancy A Randomized Controlled Trial
Kiely, M; El-Mohandes, AAE; El-Khorazaty, MN; Gantz, MG
Obstetrics and Gynecology, 115(2): 273-283.

European Journal of Obstetrics Gynecology and Reproductive Biology
Smoking and female fecundity: the effect and importance of study design
Wilks, DJ; Hay, AWM
European Journal of Obstetrics Gynecology and Reproductive Biology, 112(2): 127-135.
American Journal of Health Promotion
Self exposure to secondhand smoke among prenatal smokers, abstainers, and nonsmokers
Dunn, CL; Pirie, PL; Hellerstedt, WL
American Journal of Health Promotion, 18(4): 296-299.

American Journal of Epidemiology
Age at menarche in relation to maternal use of tobacco, alcohol, coffee, and tea during pregnancy
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Journal of Allergy and Clinical Immunology
Preterm delivery and asthma: A systematic review and meta-analysis
Jaakkola, JJK; Ahmed, P; Ieromnimon, A; Goepfert, P; Laiou, E; Quansah, R; Jaakkola, MS
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Paediatric and Perinatal Epidemiology
Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study
Jaddoe, VWV; Troe, EJWM; Hofman, A; Mackenbach, JP; Moll, HA; Steegers, EAP; Witteman, JCM
Paediatric and Perinatal Epidemiology, 22(2): 162-171.

Drug and Alcohol Dependence
The effect of maternal betel quid exposure during pregnancy on adverse birth outcomes among aborigines in Taiwan
Yang, MS; Lee, CH; Chang, SJ; Chung, TC; Tsai, EM; Ko, AMJ; Ko, YC
Drug and Alcohol Dependence, 95(): 134-139.
Reproductive Toxicology
Cytochrome P450IA1 polymorphisms along with PM10 exposure contribute to the risk of birth weight reduction
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Reproductive Toxicology, 24(): 281-288.
European Journal of Epidemiology
Passive smoking, cytochrome P450 gene polymorphisms and dysmenorrhea
Lei, L; Ye, LN; Liu, H; Chen, CZ; Fang, Z; Wang, LH; Hu, YH; Chen, DF
European Journal of Epidemiology, 23(7): 475-481.
International Archives of Occupational and Environmental Health
Different effects of PM10 exposure on preterm birth by gestational period estimated from time-dependent survival analyses
Suh, YJ; Kim, H; Seo, JH; Park, H; Kim, YJ; Hong, YC; Ha, EH
International Archives of Occupational and Environmental Health, 82(5): 613-621.
Neurotoxicology and Teratology
Developmental effects of exposure to environmental tobacco smoke and material hardship among inner-city children
Rauh, VA; Whyatt, RM; Garfinkel, R; Andrews, H; Hoepner, L; Reyes, A; Diaz, D; Camann, D; Perera, FP
Neurotoxicology and Teratology, 26(3): 373-385.

European Journal of Obstetrics Gynecology and Reproductive Biology
Risk factors for low birth weight: a review
de Bernabe, JV; Soriano, T; Albaladejo, R; Juarranz, M; Calle, ME; Martinez, D; Dominguez-Rojas, V
European Journal of Obstetrics Gynecology and Reproductive Biology, 116(1): 3-15.
Early Human Development
Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: prospective evidence from a Dutch birth cohort
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Environmental Health Perspectives
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Savitz, DA
Environmental Health Perspectives, 115(): A528-A529.
American Journal of Physiology-Endocrinology and Metabolism
Fetal growth restriction triggered by polycyclic aromatic hydrocarbons is associated with altered placental vasculature and AhR-dependent changes in cell death
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American Journal of Physiology-Endocrinology and Metabolism, 295(2): E519-E530.
Archives of Disease in Childhood-Fetal and Neonatal Edition
Environmental tobacco smoke and fetal health: systematic review and meta-analysis
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Bjog-An International Journal of Obstetrics and Gynaecology
Low birthweight and preterm birth rates 1 year before and after the Irish workplace smoking ban
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Bjog-An International Journal of Obstetrics and Gynaecology, 116(): 1782-1787.
Annals of Epidemiology
Maternal exposure to biomass smoke and reduced birth weight in Zimbabwe
Mishra, V; Dai, XL; Smith, KR; Mika, L
Annals of Epidemiology, 14(): 740-747.
Reproductive Toxicology
Passive smoking, Cyp1A1 gene polymorphism and dysmenorrhea
Liu, H; Yang, F; Li, ZP; Chen, CZ; Fang, Z; Wang, LH; Hu, YH; Chen, DF
Reproductive Toxicology, 24(1): 114-119.
American Journal of Physiology-Regulatory Integrative and Comparative Physiology
Cigarette exposure induces changes in maternal vascular function in a pregnant mouse model
Gandley, RE; Jeyabalan, A; Desai, K; McGonigal, S; Rohland, J; DeLoia, JA
American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 298(5): R1249-R1256.
Molecular Human Reproduction
Maternal smoking during pregnancy and genetic polymorphisms in the Ah receptor, CYP1A1 and GSTM1 affect infant birth size in Japanese subjects
Sasaki, S; Kondo, T; Sata, F; Saijo, Y; Katoh, S; Nakajima, S; Ishizuka, M; Fujita, S; Kishi, R
Molecular Human Reproduction, 12(2): 77-83.
Paediatric and Perinatal Epidemiology
Prenatal polychlorinated biphenyl exposures in eastern Slovakia modify effects of social factors on birthweight
Sonneborn, D; Park, HY; Petrik, J; Kocan, A; Palkovicova, L; Trnovec, T; Nguyen, D; Hertz-Picciotto, I
Paediatric and Perinatal Epidemiology, 22(3): 202-213.
Paediatric and Perinatal Epidemiology
Trait anxiety in pregnant women predicts offspring birth outcomes
Hosseini, SM; Biglan, MW; Larkby, C; Brooks, MM; Gorin, MB; Day, NL
Paediatric and Perinatal Epidemiology, 23(6): 557-566.
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Teratology, 65(3): 106-115.
Environmental Health Perspectives
Association between gaseous ambient air pollutants and adverse pregnancy outcomes in Vancouver, Canada
Liu, SL; Krewski, D; Shi, YL; Chen, Y; Burnett, RT
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Acta Paediatrica
Exposure to tobacco smoke and infant crying
Reijneveld, SA; Lanting, CI; Crone, MR; Van Wouwe, JP
Acta Paediatrica, 94(2): 217-221.
Swiss Medical Weekly
Association between maternal smoking and low birth weight in Switzerland: the EDEN study
Chiolero, A; Bovet, P; Paccaud, F
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Journal of Maternal-Fetal & Neonatal Medicine
Factors that influence the timing of spontaneous labor at term
Fogleman, KA; Herring, AH; Kaczor, D; Pusek, SN; Jo, H; Thorp, JM
Journal of Maternal-Fetal & Neonatal Medicine, 20(): 813-817.

European Journal of Obstetrics Gynecology and Reproductive Biology
Association of smoking during pregnancy and fetal growth restriction: Subgroups of higher susceptibility
Figueras, F; Meler, E; Eixarch, E; Francis, A; Coll, O; Gratacos, E; Gardosi, J
European Journal of Obstetrics Gynecology and Reproductive Biology, 138(2): 171-175.
Paediatric and Perinatal Epidemiology
Population-attributable risk of low birthweight related to PM10 pollution in seven Korean cities
Seo, JH; Leem, JH; Ha, EH; Kim, OJ; Kim, BM; Lee, JY; Park, HS; Kim, HC; Hong, YC; Kim, YJ
Paediatric and Perinatal Epidemiology, 24(2): 140-148.
Nursing Clinics of North America
Reduction of primary and secondary smoke exposure for low-income black pregnant women
Pletsch, PK
Nursing Clinics of North America, 37(2): 315-+.
PII S0029-6465(01)00011-1
European Respiratory Journal
Impact of smoke-free workplace legislation on exposures and health: possibilities for prevention
Jaakkola, MS; Jaakkola, JJK
European Respiratory Journal, 28(2): 397-408.
Development and Psychopathology
Prenatal drug exposure effects on subsequent vulnerability to drug abuse
Glantz, MD; Chambers, JC
Development and Psychopathology, 18(3): 893-922.
Journal of Epidemiology
Is maternal smoking during early pregnancy a risk factor for all low birth weight infants?
Suzuki, K; Tanaka, T; Kondo, N; Minai, J; Sato, M; Yamagata, Z
Journal of Epidemiology, 18(3): 89-96.
Annals of Agricultural and Environmental Medicine
Maternal Passive Smoking During Pregnancy and Neonatal Health
Wdowiak, A; Wiktor, H; Wdowiak, L
Annals of Agricultural and Environmental Medicine, 16(2): 309-312.

European Journal of Pediatrics
Smoking and smoking cessation during early pregnancy and its effect on adverse pregnancy outcomes and fetal growth
Vardavas, CI; Chatzi, L; Patelarou, E; Plana, E; Sarri, K; Kafatos, A; Koutis, AD; Kogevinas, M
European Journal of Pediatrics, 169(6): 741-748.
International Journal of Environmental Health Research
Cooking smoke and tobacco smoke as risk factors for stillbirth
Mishra, V; Retherford, RD; Smith, KR
International Journal of Environmental Health Research, 15(6): 397-410.
American Journal of Epidemiology
Passive smoking, metabolic gene polymorphisms, and infant birth weight in a prospective cohort study of Chinese women
Wu, T; Hu, YH; Chen, CZ; Yang, F; Li, ZP; Fang, Z; Wang, LH; Chen, DF
American Journal of Epidemiology, 166(3): 313-322.
Community Dentistry and Oral Epidemiology
Parental smoking behavior and caries experience in preschool children
Leroy, R; Hoppenbrouwers, K; Jara, A; Declerck, D
Community Dentistry and Oral Epidemiology, 36(3): 249-257.
Journal of Toxicology and Environmental Health-Part B-Critical Reviews
Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants
Wigle, DT; Arbuckle, TE; Turner, MC; Berube, A; Yang, QY; Liu, SL; Krewski, D
Journal of Toxicology and Environmental Health-Part B-Critical Reviews, 11(): 373-517.
Technical Report-Secondhand and Prenatal Tobacco Smoke Exposure
Best, D
Pediatrics, 124(5): E1017-E1044.
Plos Medicine
Protecting children from environmental toxins - Toxicity testing of pesticides and industrial chemicals is a crucial step
Lanphear, BP; Vorhees, CV; Bellinger, DC
Plos Medicine, 2(3): 203-208.
ARTN e61
Paediatric and Perinatal Epidemiology
Preterm delivery and exposure to active and passive smoking during pregnancy: a case-control study from Italy
Fantuzzi, G; Aggazzotti, G; Righi, E; Facchinetti, F; Bertucci, E; Kanitz, S; Barbone, F; Sansebastiano, G; Battaglia, MA; Leoni, V; Fabiani, L; Triassi, M; Sciacca, S
Paediatric and Perinatal Epidemiology, 21(3): 194-200.

American Journal of Preventive Medicine
Environmental Tobacco Smoke Avoidance Among Pregnant African-American Nonsmokers
Blake, SM; Murray, KD; El-Khorazaty, MN; Gantz, MG; Kiely, M; Best, D; Joseph, JG; El-Mohandes, AAE
American Journal of Preventive Medicine, 36(3): 225-234.
Environmental Health Perspectives
Effect of environmental tobacco smoke on levels of urinary hormone markers
Chen, CZ; Wang, XB; Wang, LH; Yang, F; Tang, GF; Xing, HX; Ryan, L; Lasley, B; Overstreet, JW; Stanford, JB; Xu, XP
Environmental Health Perspectives, 113(4): 412-417.
Pediatrics International
Smoking trends before, during, and after pregnancy among women and their spouses
Kaneko, A; Kaneita, Y; Yokoyama, E; Miyake, T; Harano, S; Suzuki, K; Ibuka, E; Tamaki, T; Nakajima, H; Chida, T
Pediatrics International, 50(3): 367-375.
Romanian Biotechnological Letters
Epigenetics in relation to environmental pollution, nutrition and pathogenesis
Lucian, G; Liliana, B; Irina, R; Monica, M; Ardelean, A; Cotoraci, C; Barbacar, N
Romanian Biotechnological Letters, 14(6): 4769-4778.

American Journal of Medicine
Smoking and the risk of psoriasis in women: Nurses' health study II
Setty, AR; Curhan, G; Choi, HK
American Journal of Medicine, 120(): 953-959.
Mutation Research-Genetic Toxicology and Environmental Mutagenesis
GSTM1 polymorphism along with PM10 exposure contributes to the risk of preterm delivery
Suh, YJ; Ha, EH; Park, H; Kim, YJ; Kim, H; Hong, YC
Mutation Research-Genetic Toxicology and Environmental Mutagenesis, 656(): 62-67.
American Journal of Public Health
Maternal Weathering and Risk of Preterm Delivery
Holzman, C; Eyster, J; Kleyn, M; Messer, LC; Kaufman, JS; Laraia, BA; O'Campo, P; Burke, JG; Culhane, J; Elo, IT
American Journal of Public Health, 99(): 1864-1871.
Yonsei Medical Journal
Self-Reported Exposure to Second-Hand Smoke and Positive Urinary Cotinine in Pregnant Nonsmokers
Paek, YJ; Kang, JB; Myung, SK; Lee, DH; Seong, MW; Seo, HG; Cho, JJ; Song, HJ; Park, KH; Kim, CH; Ko, JA
Yonsei Medical Journal, 50(3): 345-351.
Reproductive Toxicology
Prenatal exposure to environmental tobacco smoke alters gene expression in the developing murine hippocampus
Mukhopadhyay, P; Horn, KH; Greene, RM; Pisano, MM
Reproductive Toxicology, 29(2): 164-175.
Scandinavian Journal of Work Environment & Health
Effects of exposure to environmental tobacco smoke on reproductive health
Lindbohm, ML; Sallmen, M; Taskinen, H
Scandinavian Journal of Work Environment & Health, 28(): 84-96.

Public Health
Impact of reproductive experience on women's smoking behaviour in Japanese nurses
Maeno, T; Ohta, A; Hayashi, K; Kobayashi, Y; Mizunuma, H; Nakai, S; Ohashi, Y; Suzuki, S
Public Health, 119(9): 816-824.

Journal of Pediatrics
Maternal Smoking during Pregnancy and Regional Brain Volumes in Preterm Infants
Ekblad, M; Korkeila, J; Parkkola, R; Lapinleimu, H; Haataja, L; Lehtonen, L
Journal of Pediatrics, 156(2): 185-U40.
American Journal of Perinatology
Impact of prenatal tobacco smoke exposure, as measured by midgestation serum cotinine levels, on fetal biometry and umbilical flow velocity waveforms
Kalinka, J; Hanke, W; Sobala, W
American Journal of Perinatology, 22(1): 41-47.
Paediatric and Perinatal Epidemiology
Smoking during pregnancy and preterm birth according to obstetric history: French national perinatal surveys
Nabet, C; Ancel, PY; Burguet, A; Kaminski, M
Paediatric and Perinatal Epidemiology, 19(2): 88-96.

American Journal of Health Behavior
Are fewer women smoking during pregnancy?
Okah, FA; Cai, JW; Dew, PC; Hoff, GL
American Journal of Health Behavior, 29(5): 456-461.

Respiratory Medicine
In utero and childhood exposure to parental tobacco smoke, and allergies in schoolchildren
Raherison, C; Penard-Morand, C; Moreau, D; Caillaud, D; Charpin, D; Kopfersmitt, C; Lavaud, F; Taytard, A; Annesi-Maesano, I
Respiratory Medicine, 101(1): 107-117.
British Medical Journal
Impact of a stepwise introduction of smoke-free legislation on the rate of preterm births: analysis of routinely collected birth data
Cox, B; Martens, E; Nemery, B; Vangronsveld, J; Nawrot, TS
British Medical Journal, 346(): -.
ARTN f441
Particle and Fibre Toxicology
Placental DNA hypomethylation in association with particulate air pollution in early life
Janssen, BG; Godderis, L; Pieters, N; Poels, K; Kicinski, M; Cuypers, A; Fierens, F; Penders, J; Plusquin, M; Gyselaers, W; Nawrot, TS
Particle and Fibre Toxicology, 10(): -.
Environmental Research
Household air pollution and stillbirths in India: Analysis of the DLHS-II National Survey
Lakshmi, PVM; Virdi, NK; Sharma, A; Tripathy, JP; Smith, KR; Bates, MN; Kumar, R
Environmental Research, 121(): 17-22.
Bmc Pregnancy and Childbirth
Active and passive maternal smoking during pregnancy and birth outcomes: the Kyushu Okinawa Maternal and Child Health Study
Miyake, Y; Tanaka, K; Arakawa, M
Bmc Pregnancy and Childbirth, 13(): -.
ARTN 157
Bjog-An International Journal of Obstetrics and Gynaecology
Sequential screening for psychosocial and behavioural risk during pregnancy in a population of urban African Americans
Kiely, M; Gantz, MG; El-Khorazaty, MN; El-Mohandes, AAE
Bjog-An International Journal of Obstetrics and Gynaecology, 120(): 1395-1402.
Paediatric and Perinatal Epidemiology
Maternal Smoking During Pregnancy and Failure of the Georgia First Grade Criterion-Referenced Competency Test
Feng, J; Kramer, MR; Dever, BV; Dunlop, AL; Williams, B; Jain, L
Paediatric and Perinatal Epidemiology, 27(3): 275-282.
Maternal Smoking and Birth Weight: Interaction With Parity and Mother's Own In Utero Exposure to Smoking
Misra, DP; Astone, N; Lynch, CD
Epidemiology, 16(3): 288-293.
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Prenatal Ultrasound Scanning and the Risk of Schizophrenia and Other Psychoses
Stålberg, K; Haglund, B; Axelsson, O; Cnattingius, S; Hultman, CM; Kieler, H
Epidemiology, 18(5): 577-582.
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Obstetrics & Gynecology
Term-Gestation Low Birth Weight and Health-Compromising Behaviors During Pregnancy
Okah, FA; Cai, J; Hoff, GL
Obstetrics & Gynecology, 105(3): 543-550.
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Journal of Occupational and Environmental Medicine
Effects of the GSTM1 and GSTT1 Polymorphisms on the Relationship Between Maternal Exposure to Environmental Tobacco Smoke and Neonatal Birth Weight
Hong, Y; Lee, K; Son, B; Ha, E; Moon, H; Ha, M
Journal of Occupational and Environmental Medicine, 45(5): 492-498.

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maternal smoking; passive smoking; environmental tobacco smoke; low birth weight; preterm delivery; birth weight; small for gestational age

© 2000 Lippincott Williams & Wilkins, Inc.

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