The negative relationship between smoking in pregnancy and infant birth weight (BW) is well established. Continued active smoking in pregnancy beyond the first trimester is associated with reduced infant BW [1
], low birth weight (LBW) and pre-term birth [3
], and this relationship is causal and dose dependent [4
]. The influence of maternal smoking on BW is primarily mediated through fetal growth restriction [5
] due to utero-placental vasoconstriction caused by nicotine and carbon monoxide poisoning from products of combustion [7
The link between smoking in pregnancy and social disadvantage is also well recognized [8
]. Prevalence of smoking in Ireland is highest in young girls of childbearing age with a distinct social class gradient [9
], and inequalities in smoking prevalence have increased over time [9
]. These disadvantaged women attend public ante-natal clinics and are at increased risk of having a LBW infant because of high smoking prevalence compounded by disadvantage [12
From a public health perspective, maternal smoking, because of its particularly high prevalence in socially disadvantaged women, is the leading preventable cause of intra-uterine growth retardation in Europe and North America [5
]. Most studies estimate a reduction of 150–300 g in BW in women who continue to smoke compared to non-smoking pregnant women [2
]. BW declines as tobacco exposure increases; however, the relationship between maternal smoking and BW is not linear; steepest declines in BW have occurred at low levels of exposure measured in the third trimester, suggesting that quitting is far more effective than cutting down [16
]. Although not a linear relationship, there is an estimated 27 g reduction in BW for each additional cigarette smoked per day in the third trimester of pregnancy [6
Even in non-smoking women, high exposure to Second-Hand Smoke (SHS) is negatively associated with BW reduction of 25–75 g and up to 110 g in their offspring [17
]. Khazarri et al. [19
] found mean BW declined in a dose dependent manner as cotinine levels increased in non-smoking women, and there was no threshold level below which BW was not reduced [19
A number of studies have shown that women who reported quitting smoking early in pregnancy, i.e., prior to four months (16 weeks) gestation, had infants with mean BWs similar to non smokers [13
]. The mechanism underpinning this effect is primarily via a reduction in Small for Gestational Age (SGA) [5
], and, to a lesser extent, pre-term birth [5
]. Stopping smoking at any time up until 30 weeks has a positive effect on BW, but stopping before 16 weeks has the greatest effect [21
However, many women quit and relapse repeatedly during pregnancy [24
]. An effect of partial, i.e., temporary quitting, may be particularly important for low-income women who are much more likely to continue to smoke during pregnancy [8
] and be heavier smokers. This group of smokers is also more likely to be exposed to SHS particularly in their household environment [25
Knowledge of the effect of partial quitting beyond the first trimester on BW is limited. An older study showed that those who stopped smoking temporarily after 16 weeks had some increase in mean BW [21
]. An observational study [27
] found an estimated gain in BW of 105 g with cutting down by 10 cigarettes per day after the first visit. England et al. concluded, as a result of measuring cotinine levels in the third trimester, that reducing smoking by eight cigarettes per day was necessary to avoid a reduction in BW [28
]. The Generation R prospective cohort study of over 7000 pregnant women in the Netherlands showed a small non-significant beneficial effect for reducing the number of cigarettes from ≥5 per day in early pregnancy to <5 per day without quitting [20
Lumley et al. [29
] have highlighted the need to obtain greater insight into the experiences of women who continue to smoke so that appropriate interventions and supports may be developed for these women. They raise the possibility of including smoking reduction as a goal in a “harm minimization strategy” similar to other substance misuse strategies. This may have particular importance for low-income women for whom quitting may not be an attainable goal.
This study aims to determine how variation in patterns of smoking behavior (smoking patterns), defined as: continuing to smoke, partial quitting or sustained quitting during pregnancy in low-income women, who were all smokers at time of pregnancy, influences infant BW, taking into account household smoking, and other smoking and socio-demographic variables including maternal age, parity and infant factors. A secondary objective was to compare smoking patterns with the average number of cigarettes smoked (CiggsAv) at a particular time point as a measure of smoking exposure. Our null hypothesis stated that there was no difference in BW outcome between those who had quit partially and those who continued to smoke during pregnancy, and that smoking pattern and average number of cigarettes smoked were equivalent measures of smoking exposure.
Our study examined the combined effect of active and passive smoking throughout pregnancy, complete cessation and partial cessation on BW in a group of low-income women, all of whom were smokers at time of pregnancy. It demonstrated a clear inverse gradient between active smoking pattern and baby’s BW, having adjusted for gestational age, gender, household SHS and other covariates. Sustained quitting resulted in significantly increased BW in term infants of both sexes, with greatest effect in newborn females. An intermediate effect on BW was observed for partial quitters, which impacted favorably on female infant BW. Smoking pattern throughout pregnancy had a greater effect on BW than average number of cigarettes smoked. Post-hoc analysis showed that additional home smoking was selectively inversely associated with a reduction in pre-term though not term infant BW.
In keeping with previous research, our study provides further evidence that the negative effects of maternal smoking on BW are at least partly reversible [5
]. Mothers who continued not to smoke from early in pregnancy experienced greatest benefits in terms of increased BW than those who quit later or not at all. Our findings of a modest increase in BW in partial quitters, compared to continued smokers, further support this concept. The findings add to those of Benjamin–Garner and Stotts [37
] in a smaller US study of 225 primarily low-income women, which found a non-significant increase in term infant BW, on cotinine analysis, associated with a reduction from heavy to light smoking exposure during pregnancy.
Our study also showed that smoking pattern throughout pregnancy had a greater effect on BW than average number of cigarettes smoked. Although data completion rates were similar for smoking patterns (88.8%) and CiggsAv (90.5%) in the multivariable models (Table 2
and Table 3
), it is likely that data on CiggsAv are less reliable due to underreporting of the amount smoked and regression to the mean. England et al. did not find a significant association between number of cigarettes smoked at enrolment and BW [28
]. Their study showed a rapid decline in BW in the third trimester from smoking up to eight cigarettes per day, which then leveled off, implying that greatest damage occurred at lowest levels of exposure.
Our study reports a higher mean difference in BW (−350 g) in term infants of continued smokers and sustained quitters in our low-income cohort than previous general population studies of pregnant women (−250–(−150) g) [3
]. The US study in primarily low-income women reported above [37
] also found a higher mean difference (−299 g) in BW in term infants of mothers who continued to smoke and those who quit [37
], reflecting the combined impact of active and SHS compounded by disadvantage. Although SHS exposure has declined in recent years, the decline has been greatest in socioeconomically advantaged households [26
] due to higher smoking rates and a reduced likelihood of having smoke free homes [38
]. Benjamin-Garner and Stotts reported 81% of women having partners who continued to smoke or living in households with other smokers [37
]. It is possible that quitting is particularly important for low-income pregnant women who suffer multiple environmental stresses including passive smoking related to their socio-economic position.
In our study, no effect on gestational age at delivery was noted for stopping smoking. This may be due to the exclusion of a small number of very preterm babies from the analysis; however, it is more likely that the study may be underpowered to show an effect on preterm birth.
Current evidence supports a causal relationship between maternal exposure to household environmental tobacco smoke and a small decrease in BW; Ward, adjusted mean difference 36 g, (95% CI: 5–67 g); Leonardi-Bee 33 g (95% CI: 16–51 g) prospective studies; 40 g (95% CI, 26–54 g), retrospective studies; Salmasi −60 g, (95% CI: −80–(−39) g) [14
]. However, it is considered [19
] that the 200 g reduction in BW attributable to active smoking may be underestimated by approximately 100 g—the effect of SHS. Few studies have examined the effect of home smoking in addition to partner smoking. In the UK Millennium Cohort study, 10% of households surveyed were shared by non-partner adults e.g., grandparents, who were not captured by that study [14
]. The authors of that study acknowledge that the small mean reduction in BW observed of 36 g (95% CI: 5–37 g) from partner smoking is thus an underestimate of the true effect of SHS exposure on BW. It is also possible that partners who smoke may behave differently, i.e., smoke outside in comparison with other household smokers such as grandparents.
Our study, which examined the cumulative effect of all additional household smokers, did not show an overall effect of domestic SHS on reduced BW. The Generation R study [20
] found an effect of passive smoking on BW only in late pregnancy. A selective effect of additional home smoking inversely associated with pre-term infant births (37 weeks) was found although the numbers are small. However, in our study, the influence of household SHS on BW was a post hoc analysis rather than an a priori hypothesis and must be regarded as such in terms of the interpretation of the findings.
However, a cohort study of over 10,000 live singleton births in China, where 49% of men are active smokers, examined the association between passive smoking and pre-term birth. This study showed a 98% increased risk for very pre-term birth <32 weeks (odd ratio (OR) = 1.98, (95% CI: 1.41–2.76 g), p
for trend = 0.0014). The effect increased with increased duration of exposure but was not shown for moderate pre-term births (32–36 weeks) after adjustment for gestational age [41
A recent meta-analysis of 24 observational studies by Cui et al. [42
] reported summary odds ratios (SORs) of preterm birth for women who were sometimes exposed to passive smoking versus women who were never exposed to passive smoking: ever exposed: (SOR = 1.20 g (95% CI = 1.07–1.34 g), I2
= 36.1%); never exposed: (SOR = 1.16 g (95% CI: 1.04–1.30 g), I2
= 4.4%), respectively. The effect was weaker in the cohort (SOR = 1.10 g, (95% CI: 1.00–1.21 g), n
= 16) than in cross-sectional studies (SOR = 1.47 g, (95% CI = 1.23–1.74 g), n
= 5) and higher in Asian populations and studies with more than 100 preterm births. The relationship between passive smoking and pre-term birth needs to be explored in future prospective studies in different populations, and to be examined during different trimesters of pregnancy and by different causes of preterm birth [42
Data on gender-specific associations with BW and smoking during pregnancy and/or Environmental Tobacco Smoke are scarce and somewhat conflicting and compare the effects of the number of cigarettes smoked per day with non-smokers rather than the effects of quitting on BW.
A German Perinatal Study demonstrated a greater negative effect of maternal smoking on mean BW of newborn girls than boys particularly in heavy smokers (>20 cigaretts per day), [43
]. Although a large sample, this study does not distinguish between mothers who smoked for the entire pregnancy and those who stopped early in pregnancy. A disproportionate effect on newborn males has previously been reported in women who smoked more than 10 cigarettes per day (males 8.2% reduction in weight vs. females 4.8%) [44
]. More rapid growth of male foetuses and a different hormonal milieu were suggested as the explanation for the greater effect of cigarette smoking on male foetuses. More recent cross-sectional data from 11,000 newborns from the US National Health and Nutrition Survey (NHANES) found ante-natal smoking to be associated with a greater decrease in BW among infant boys who were also more likely to be admitted to intensive care [45
In our study, the average number of cigarettes smoked did not show a differential effect on male and female BW. However, gender-stratified analysis showed that sustained quitting resulted in significantly increased BW in term infants of both sexes, with the greatest effect in newborn females who are smaller in terms of BW to begin with. Significantly higher BWs were also observed in female infants as a result of partial quitting but not in males. This would suggest a potentially greater impact of quitting on female BW. Gender did not influence BW in pre-term infants.
The strength of the study lies in its longitudinal design, which facilitated follow-up and measurement of smoking status at a number of time points. Acceptance rates to take part in the study were high, with few refusals (8.1%). Response rate at the second visit in late pregnancy was (93.8%). Urinary cotinine levels validated self-reported smoking cessation at V2.
Many previous studies have been unable to distinguish between women who have quit before pregnancy and those who have quit since becoming pregnant. Almost all have focused on comparing the effects of smokers with “non-smokers”, i.e., “never smokers” and “ex-smokers” at baseline. All women in our studies were smokers at the time of pregnancy.
Our study has some limitations worthy of consideration. This was an observational study and has all the hazards of bias and confounding which are often not resolved by multivariable regression analysis. The study did not address certain established confounders such as alcohol intake in pregnancy and the known association with alcohol intake and cigarette smoking. However, Zaren et al. [44
] report that although smokers reported a higher alcohol consumption prior to pregnancy, no difference in consumption during pregnancy was found between smokers and non-smokers and overall consumption was low. In addition, we did not have data on maternal body mass index, although very low maternal weight is seldom encountered in Ireland. Unmeasured dietary components such as Vitamin D intake may also have an influence on BW, particularly in low-income women, who may be nutritionally deficient. Iron deficiency anaemia during the first half of pregnancy increases the risk for preterm birth, LBW, infant mortality, and infant iron deficiency [46
], and taking iron daily during pregnancy is associated with a significant increase in BW and a reduction in the risk of LBW [47
]. Our study did not measure iron intake.
The second visit took place between 28–32 weeks at the beginning of the third trimester in our study. As the main influence of smoking on BW occurs in the third trimester, our estimate of the average number of cigarettes smoked is likely to be an underestimate of the effect of smoking dose on BW, particularly in heavy smokers. In addition, the timing of partial quitting was not determined.
In relation to SHS, our study did not consider workplace exposure. However, it took place after the introduction of the ban on smoking in the workplace, hence the household environment is the most likely source of SHS exposure. Similarly, genetic influences were not examined.