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Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications
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Contents lists available at ScienceDirect
Paediatric Respiratory Reviews
Mini-Symposium: Interventions to Prevent Respiratory Disease
Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications Mary-ann Wagijo 1, Aziz Sheikh 2,3, Liesbeth Duijts 1,4,5, Jasper V. Been 1,2,3,* 1
Division of Neonatology, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB, Rotterdam, The Netherlands Centre of Medical Informatics, Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK 3 School for Public Health and Primary Care (CAPHRI), Maastricht University, PO Box 616, 6200MD Maastricht, The Netherlands 4 Department of Paediatrics, division of Respiratory Medicine, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB Rotterdam, The Netherlands 5 Department of Epidemiology, Erasmus University Medical Centre, PO Box 2060, 3000CB, Rotterdam, The Netherlands 2
EDUCATIONAL AIMS THE READER WILL BE ABLE TO DISCUSS: Aspects of the relationship of tobacco smoking during pregnancy and second-hand smoke exposure with preterm birth and its complications The effectiveness of interventions aimed at preventing tobacco smoking and its harmful effects during pregnancy The effectiveness of interventions to reduce pre- and postnatal smoke exposure in relation to preterm birth and its complications
A R T I C L E I N F O
S U M M A R Y
Keywords: Premature birth Infant Tobacco use Smoking Pregnancy Prevention Smoking cessation Smoke-free policy
Tobacco smoking and smoke exposure during pregnancy are associated with a range of adverse health outcomes, including preterm birth. Also, children born preterm have a higher risk of complications including bronchopulmonary dysplasia and asthma when their mothers smoked during pregnancy. Smoking cessation in early pregnancy can help reduce the adverse impact on offspring health. Counselling interventions are effective in promoting smoking cessation and reducing the incidence of preterm birth. Peer support and incentive-based approaches are likely to be of additional benefit, whereas the effectiveness of pharmacological interventions, including nicotine replacement therapy, has not definitely been established. Smoke-free legislation can help reduce smoke exposure as well as maternal smoking rates at a population level, and is associated with a reduction in preterm birth. Helping future mothers to stop smoking and protect their children from second hand smoke exposure must be a key priority for health care workers and policy makers alike. ß 2015 Elsevier Ltd. All rights reserved.
INTRODUCTION Tobacco smoking and second-hand smoke (SHS) exposure during pregnancy are associated with a considerable burden of
* Corresponding author. Division of Neonatology, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB Rotterdam, The Netherlands; Tel.: +31 10 7036077; fax: +31 10 7036542. E-mail addresses: [email protected] (M.-a. Wagijo), [email protected] (A. Sheikh), [email protected] (L. Duijts), [email protected] (J.V. Been).
adverse perinatal and child health outcomes [1,2]. Among these is preterm birth, currently the leading cause of death in children worldwide and responsible for considerable morbidity among survivors [3,4]. This review will first map out the global burden of mortality and morbidity resulting from tobacco smoking and preterm birth. We will then outline how smoking and SHS exposure are linked to preterm birth and its complications, with particular attention to complications affecting the lungs. Finally we will highlight various approaches to reduce the impact of tobacco smoking and SHS exposure on preterm birth and its complications.
http://dx.doi.org/10.1016/j.prrv.2015.09.002 1526-0542/ß 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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Global burden of tobacco smoking and SHS exposure Prevalence and consequences of smoking Every year, approximately six million people die because of tobacco use, making it the primary preventable cause of mortality worldwide [5,6]. Tobacco use is causally linked to many diseases, including different types of cancer, cardiovascular diseases and chronic obstructive pulmonary disease (COPD) [1,6]. Between 1980 and 2012, the worldwide smoking prevalence decreased from 41% to 31% among men and from 11% to 6% among women [5]. However due to population growth the absolute number of daily smokers increased from 721 million to 967 million during that period [5]. Important variation exists in smoking prevalence across countries with, for example, very high prevalence among men in Russia and Indonesia (both >50%) and among women in Greece and Bulgaria (both >25%) [5]. Prevalence and consequences of SHS exposure Tobacco is not only harmful to the health of its users; it also affects the health of non-smokers through exposure to SHS [1]. SHS exposure was estimated to have caused 603 000 deaths and 10.9 million disability adjusted life years (DALYs) worldwide in 2004 [7]. SHS exposure is highest in children (40%), compared to men (33%) and women (35%) [7]. Over 25% of the lives and over 60% of the health life years estimated to be lost due to SHS exposure each year are among children [7]. This is likely an underestimation of tobacco’s true impact on early-life health as it is solely based on the well-recognised impact of SHS on respiratory tract infections and asthma in childhood [8]. Many children are however in addition affected by antenatal smoke exposure, either via active maternal smoking or maternal SHS exposure, putting them at risk of a range of adverse perinatal and long-term outcomes [1,2,6]. Smoking and SHS exposure during pregnancy The prevalence of antenatal smoke exposure varies by country according to its social, cultural, and ethnic background. In highincome countries, an estimated 10-20% of women smoke during pregnancy, with high percentages in the United Kingdom (14-20%) and the United States (US; 15-18%) [9]. Smoking during pregnancy is much less common in low- and middle-income countries, with an overall prevalence of 1.3% (range 0-15%) estimated from 20012012 Demographic and Health Survey data from 54 countries [10]. Of concern, however, is that in some of these countries up to 75% of pregnant women are exposed to SHS [11]. Multiple epidemiologic studies and meta-analyses have demonstrated maternal smoking during pregnancy to be associated with severe adverse pregnancy outcomes, including: stillbirth [12], congenital anomalies [13], low birth weight [1], preterm birth [14], and neonatal mortality [1]. Children whose mothers smoked during pregnancy are furthermore at increased risk of sudden infant death syndrome (SIDS) [15], respiratory tract infections [16], recurrent wheezing [17], asthma [18], overweight and obesity [19], cognitive delay [20], and behavioural problems [20]. There is increasing evidence that maternal smoking also increases the offspring’s risk of taking up smoking themselves later on [21]. Although SHS exposure during pregnancy is generally less strongly associated with adverse paediatric health outcomes than is active smoking, it has been linked to increased risks of low birth weight and childhood asthma [22,23]. Epidemiology of preterm birth and its complications Incidence of preterm birth In 2010, an estimated 14.9 million babies were born preterm worldwide [8]. Over 60% of all preterm births were
in Sub-Saharan Africa and South Asia [8]. Although in developed countries the overall preterm birth rate is relatively low at 8.6% compared to the global rate of 11.1%, the US ranks among the top 10 countries contributing to the global number of preterm births, with 12.0% of babies being born preterm [8]. Preterm birth is thus a global public health problem, which is likely to escalate given that only three out of 184 countries experienced a reduction in preterm birth rate between 1990 and 2010 [8]. Mortality attributable to preterm birth Annually, approximately one million deaths are directly attributable to preterm birth [4,24]. Although low- and middleincome countries contribute the majority of preterm-birth related deaths, several high-income countries are among those with the highest percentage of deaths being directly attributable to preterm birth [4]. Variation is influenced by many factors including the level of care available and provided, ethnic and socioeconomic background of the population, and ethical considerations regarding resuscitation of babies born at the edge of viability, and end-oflife decisions. Complications of preterm birth When healthy, the uterus provides the optimal environment for the developing fetus. Preterm birth however removes a baby from this environment during a critical phase of development, putting it at risk of many adverse outcomes [3]. For almost all outcomes the risk is highly gestational age-dependent, with the highest prevalence seen among the most preterm infants. Common pathological processes underlying preterm birth, including intrauterine inflammation and infection, preeclampsia, and intrauterine growth restriction, have distinct adverse effects on specific organs, further modulating these risks. Respiratory complications The introduction of antenatal corticosteroids and postnatal surfactant therapy has allowed for increased survival after preterm birth and thereby for respiratory complications to shift towards much more immature babies. Respiratory distress remains a common early sign of very preterm birth. Despite a general shift away from aggressive ventilator strategies, an important proportion of extremely preterm infants go on to develop chronic lung disease of prematurity, bronchopulmonary dysplasia (BPD). BPD likely represents the severe end of a spectrum of prematurity-related respiratory complications, and is associated with sustained airway obstruction and wheezing symptoms [25]. Especially during the first years, children born preterm are at increased risk of re-hospitalisation, often due to respiratory problems and in particular bronchiolitis [26]. Prematurity-associated respiratory problems may extend well into later life [3], with increased risks for childhood asthma [27,28], and chronic obstructive pulmonary disease (COPD) [29]. Even children born near-term are increasingly recognised to be at risk for adverse pulmonary outcomes and as a group are the primary contributors to the overall burden of prematurity-associated respiratory problems [27]. Other complications Common severe non-respiratory neonatal complications following preterm birth include: sepsis, necrotising enterocolitis (NEC), intraventricular haemmorrhage (IVH), periventricular leukomalacia (PVL), and retinopathy of prematurity (ROP). In the long term, developmental impairments, including motor disturbances and cognitive and communicative deficits, and behavioural problems are commonly seen.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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Maternal tobacco smoking and SHS exposure and the risk of preterm birth Maternal smoking and preterm birth The association between maternal smoking during pregnancy and preterm birth has been assessed in numerous studies. To the best of our knowledge the most recent meta-analysis on the topic was published in 2000 [14]. Data from 20 prospective studies where preterm birth rates were reported according to at least two levels of maternal smoking were combined. Maternal smoking during pregnancy was associated with a 1.27 (95%CI 1.21-1.33) times increased risk for preterm birth. There was evidence of a dose-response association, with risk for light smokers (0-10 cigarettes/day) being lower than for moderate and heavy smokers. Numerous large studies have been conducted since this metaanalysis, almost invariably confirming the association between maternal smoking and preterm birth, including various studies demonstrating evidence of a dose-response effect [30–34]. Findings from some of these studies suggest that smoking differentially affects very preterm as opposed to moderately preterm birth. An analysis of over 1 million singleton births in Missouri furthermore demonstrated that the risk was increased for both spontaneous and indicated preterm birth [30]. It is important to note that the vast majority of studies adjusted for possible confounders including pregnancy-related disorders, maternal age, socioeconomic status and lifestyle factors. Maternal smoking is commonly self-reported and not biochemically validated, which is important as underreporting of maternal smoking from self-report is well recognised [1]. Underreporting leads to contamination of the control group with smokers, resulting in likely underestimation of the true association between maternal smoking and preterm birth. Maternal smoking and preterm birth: underlying mechanisms The potential mechanisms underlying the link between maternal smoking and preterm birth have recently been reviewed [35]. Overall the mechanisms remain poorly understood and are likely to be multifactorial. Many cases of preterm delivery associated with maternal smoking are mediated via intrauterine growth restriction, necessitating early delivery for fetal concerns. Smoking increases levels of carbon monoxide, which readily passes the placenta, displacing oxygen from haemoglobin and decreasing its ability to release oxygen to the tissues [35]. Nicotine has been shown to decrease uterine blood flow, and human data are indicative of increased resistance and microscopic changes in placental vasculature among smokers [35]. Whereas these mechanisms are likely involved in the association of maternal smoking with intrauterine growth restriction, others appear to underlie its association with spontaneous preterm delivery. Smoking predisposes to intrauterine infection, cervical insufficiency, and preterm prelabour rupture of membranes, all key causes of spontaneous preterm delivery [31,36]. Oxidative stress and reduced anti-oxidant capacity, reduced progesterone levels, and increased oxytocin sensitivity and prostaglandin production may in addition promote uterine contractility and induce preterm labour in smokers [31,35]. Maternal SHS exposure and preterm birth Two meta-analyses have addressed the association between maternal SHS exposure during pregnancy and preterm birth [22,37]. Leonardi-Bee et al. combined data from studies assessing the association between ‘any record of maternal contact’ with SHS and preterm birth among non-smoking women [22]. SHS exposure was associated with preterm birth in retrospective studies (nine studies; OR 1.18 (95%CI 1.03-1.35), but not in prospective studies (eight studies; p = 0.24, OR not reported) and one case-control
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study (OR 0.92 (95%CI 0.65-1.31)). In a separate meta-analysis, Salmasi et al. combined data from studies where SHS exposure was either self-reported or biochemically validated and where active smokers were either excluded or controlled for in the analyses [37]. There was no significant association between maternal SHS exposure and preterm birth in meta-analyses of unadjusted or adjusted effect estimates (unadjusted: 18 studies, OR 1.20 (95%CI 0.99-1.46); adjusted: seven studies, OR 1.07 (95%CI 0.93-1.22)). Individual studies published since also showed mixed evidence, although a rather strong association for very preterm versus moderate preterm birth was observed in one study [38]. Maternal tobacco smoking, SHS exposure, and complications following preterm birth Respiratory complications The adverse impact of antenatal smoke exposure on lung development and adverse respiratory outcomes, in particular wheezing and asthma, is well recognised [18]. Antenatal smoke exposure disrupts lung development in mice, resulting in a pathological picture closely resembling human BPD [39]. Observed airway smooth muscle layer thickening, collagen deposition, and increased numbers of house dust mite-induced goblet cells may all contribute to airway remodeling and hyper-responsiveness [40]. Nicotine-mediated reductions in placental blood flow, fetal oxygen and nutrient supply, fetal breathing movements and changes in alveolar type II cell metabolism may explain abnormal growth and maturation of the airways and lungs and subsequent development of respiratory diseases [41–43]. Last, antenatal smoke exposure seems to alter expression of susceptibility genes for respiratory diseases via reduction of histone deacetylase activity and changes in methylation patterns [44]. Maternal smoking has been associated with the development of BPD in a case-control study of Italian very-low-birth-weight (VLBW) infants: OR 2.21 (95%CI: 1.03-4.76) [45]. This association was confirmed in a large population-based Canadian cohort of very preterm infants (OR 1.16 (95%CI 1.02-1.33)) [46], as well as a German cohort of preterm VLBW infants (OR 1.34 (95%CI 1.011.79)). [47] At follow up, home SHS exposure was associated with increased need for inhaled corticosteroids in US children with BPD (86% vs. 76% in exposed vs. non-exposed, p = 0.05) [48]. Hair nicotine levels furthermore predicted activity limitation and hospitalisation among those requiring respiratory support [49]. SHS exposure is associated with respiratory complications beyond BPD among children born preterm (Figure 1). Home SHS exposure was independently associated with wheezing in very preterm and VLBW infants [50,51], and with the need for acute care for respiratory problems during the first year of life [52]. A significant interaction between preterm birth and maternal smoking was demonstrated in another prospective birth cohort, maternal smoking during pregnancy
antenatal SHS exposure ?
fetus newborn
?
preterm birth
BPD
child
wheezing / asthma
postnatal SHS exposure
Figure 1. Impact of tobacco smoke exposure on preterm birth and its respiratory complications. Blue arrows indicate positive associations, red arrows indicate positive interactions. BPD = bronchopulmonary dysplasia.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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with children born preterm to smoking mothers having the highest risk of recurrent wheezing (OR 4.0 (95%CI 1.9-8.6) vs. children born at term to non-smoking mothers) [53]. Other complications Several studies suggest that the negative impact of antenatal tobacco smoke exposure among children born preterm may not be confined to the lung. The largest cohort study on the topic to date demonstrated an independent 1.17 (95%CI 1.04-1.32) times increased risk of developing a composite outcome of death or major morbidity among preterm babies whose mothers smoked [46]. Specific adverse outcomes associated with maternal smoking included BPD, and severe IVH or PVL [46]. The study did not confirm the increased risk of ROP seen in another, smaller cohort [46,47]. Maternal smoking was furthermore identified as a major risk factor for NEC in a recent case control study [54], although the association did not reach statistical significance in two recent cohort studies [46,47]. Overall, given the low number of studies and their inconsistent findings, as well as the lack of mechanistic studies on the topic, no firm conclusions can be made regarding the impact of maternal tobacco smoking on extrapulmonary complications of preterm birth. Smoking cessation and preterm birth risk Results from observational studies indicate that stopping smoking before or early in pregnancy has the potential to
normalise preterm birth risk. In an elegant study, Cnattingius and colleagues evaluated pregnancy outcomes in almost 250 000 women who delivered two consecutive singleton infants [55]. The risks of very and moderately preterm birth were increased in the second versus the first pregnancy in initially non-smoking women who took up smoking before the second pregnancy, whereas the risk normalised in women who smoked during the first pregnancy but stopped before the second. Both associations were dose-dependent, the risk differences being more pronounced with increasing number of cigarettes smoked. Several studies have since confirmed that the risks of preterm birth and other adverse pregnancy outcomes after stopping smoking before or early in pregnancy indeed decrease to those observed among nonsmoking women, while the risks remained elevated in women who continued smoking [31,34,56–58]. This indicates that interventions to support smoking cessation either pre-conception or in the first trimester have significant potential to reduce preterm birth. Pregnancy may be a major ‘teachable moment’ to promote a healthy lifestyle given mothers’ concern about fetal health and their regular contact with health care providers. It is imperative that these providers identify smokers who are either pregnant or planning to become pregnant as early as possible, to ensure that effective interventions for smoking cessation can be offered [59]. Below we discuss the effectiveness of interventions to promote smoking cessation during pregnancy and to reduce SHS exposure among pregnant women and their offspring (see also Table 1).
Table 1 Best evidence on interventions to reduce maternal smoking and pre- and postnatal SHS exposure Type of intervention
Study design
Individual and family based – smoking cessation Preconception counselling Systematic review [60]
Psychosocial interventions
Systematic review [61]
Incentive-based interventions
RCT [62]
Nicotine replacement therapy
Systematic review [63]
Other pharmacological interventions Physical activity (adjunct to counselling) Relapse prevention
Systematic review [63]
*
RCT [65] Systematic review [66]
Individual and family based – harm reduction Vitamin C / E supplementation in RCT [67] pregnant smokers RCT (secondary analysis) [68] Individual and family based – SHS exposure reduction SHS reduction during pregnancy Systematic review [69] SHS reduction after NICU discharge Policy-based interventions Smoke-free legislation
Systematic review [79]
Tobacco taxation
Quasi-experimental study [85]
RCT [71]
Main findings
Impact on preterm birth and related complications
Only three studies identified, including two observational studies; some evidence that quit advice may reduce smoking rates and promote relapse during pregnancy Counselling interventions are effective in reducing smoking rates up to 17 months postpartum, especially when combined with other strategies. Peer support programs are also effective. Health education alone had no effect on smoking cessation during pregnancy. Financial incentives increase smoking cessation during pregnancy. No significant effect on smoking rates among pregnant women. No studies available
NA
Counselling interventions reduce preterm birth
No significant effect on preterm birth No significant effect on preterm birth NA
No significant effect on smoking cessation during pregnancy No significant effect of behavioral interventions on smoking relapse during pregnancy or at postpartum follow-up
No significant effect on preterm birth
Vitamin C 500 mg /day
Better respiratory outcomes among offspring of smokers Reduction in preterm birth and placental abruption among smokers
Vitamin C 1000 mg /day + vitamin E 400 IU
NA
Five RCTs all showed some effect on SHS exposure but overall evidence of low quality Motivational interviewing reduces SHS exposure at home, but only on short-term
Reduction in preterm birth before 34 weeks in one RCT of multifaceted intervention No significant effect on respiratory outcomes after NICU discharge
Smoke-free legislation known to be associated with reduced SHS exposure and reduced smoking during pregnancy Tobacco tax increase associated with reductions in maternal smoking among white mothers with low education and black mothers
Reduction in preterm birth after smoke-free legislation Tobacco tax increase associated with small reduction in preterm birth among white mothers with low education and black mothers
* several very small studies are available but not reported here. RCT: randomized controlled trial; NA: Not Assessed; SHS: second-hand smoke; NICU: neonatal intensive care unit.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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Opportunities for prevention: individual-level and family-based interventions Preconceptional smoking cessation A recent systematic review of preconception counselling strategies identified only three studies that focused on smoking [60]. Overall the results were mixed, with some evidence of a reduction in smoking and maintenance of cessation with quit advice, with or without counselling. Pregnancy outcomes were not reported. Interpretation is complicated by the observational study design of two studies and differences in intervention strategy. Smoking cessation during pregnancy – psychosocial interventions Much more data is available for interventions to promote smoking cessation during pregnancy. Eighty-six trials were included in a recent Cochrane review on the efficacy of psychosocial interventions [61]. Among these, counselling interventions increased smoking abstinence in late pregnancy as compared to usual care (27 studies; risk ratio (RR) 1.44 (95%CI 1.19-1.75)) or to less intensive interventions (16 studies; RR 1.35 (95%CI 1.00-1.82)) in meta-analyses. Of note, reduced smoking rates were sustained up to 17 months post-partum. The effect was generally larger when counselling was combined with other strategies such as providing feedback via biochemical measures of cessation or fetal health indicators: two studies, RR 4.39 (95%CI 1.89-10.21). Most importantly, counselling interventions significantly reduced the risks of preterm delivery (14 studies, RR 0.82 (95%CI: 0.70-0.96)) and delivering a low-birth-weight baby. Another effective approach identified in this review included social support provided by peers (5 studies, RR 1.49 (95%CI 1.012.19)). Health education had no significant impact on smoking cessation during pregnancy. Smoking cessation during pregnancy – incentive-based interventions Incentive based interventions were deemed promising by the Cochrane review on psychosocial interventions, but only a few small trials were identified [61]. Recently, a large randomised controlled trial (RCT) investigated the effectiveness of offering shopping vouchers of incremental value for sustained, biochemically validated cessation at repeated health visits [62]. The intervention was highly effective in achieving sustained smoking cessation at the end of pregnancy versus routine care: RR 2.63 (95%CI 1.73-4.01). No significant impact on pregnancy complications including preterm birth was observed, but the trial was not powered to assess these outcomes. Smoking cessation during pregnancy – pharmacological interventions Six trials of pharmacological interventions were identified in a recent Cochrane review [63]. All trials evaluated nicotine replacement therapy (NRT), which in meta-analysis was not more effective than control in achieving smoking cessation during pregnancy: RR 1.33 (95%CI 0.93-1.91). NRT also did not affect the risk of preterm delivery, prematurity-related adverse outcomes (i.e. need for mechanical ventilation, IVH, NEC), or serious side-effects. The review authors argue that NRT is likely to be more effective at higher doses and suggest the need for further trials evaluating this. Although guidelines in a number of countries support the use of NRT when psychosocial interventions are not effective, the World Health Organization (WHO) refrains from making a recommendation on this issue [59]. Interestingly, two-year follow-up data of a large RCT recently demonstrated a larger proportion of infants born to mothers in the NRT arm as compared to controls to have unimpaired development: OR 1.40 (95%CI 1.05-1.86) [64]. This supports the need for additional research in this area, with particular attention to offspring follow-up.
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No trials during pregnancy have been conducted to assess the safety or effectiveness of other pharmacological agents used routinely in the treatment of nicotine-dependence in adults and their use is not therefore at present recommended [59,63]. Smoking cessation during pregnancy – other interventions Physical activity as an adjunct to behavioural therapy was recently evaluated in an RCT. No effect on smoking cessation during pregnancy or birth outcomes, including preterm birth, was observed [65]. Relapse prevention In a recent systematic review and meta-analysis, behavioural interventions were not significantly effective in preventing smoking relapse by the end of pregnancy or at longest postpartum follow-up [66]. Harm reduction interventions Evidence from animal studies showing that vitamin C may reverse the negative impact of nicotine on fetal lung development informed a recent RCT of vitamin C supplementation (500 mg/d) to pregnant mothers who declined to quit smoking [67]. Babies randomised to vitamin C had significantly better lung function measures, and less wheezing during the first year of life. The authors acknowledge that the primary goal should be for pregnant women to quit smoking, but conclude that vitamin C may be ‘an inexpensive and simple approach’ to reduce some of the adverse effects on offspring respiratory outcomes associated with smoking. Although the aforementioned trial found no impact of vitamin C on preterm birth [67], a recent secondary analysis of an RCT of combined vitamin C (1000 mg) and E (400 IU) supplementation during pregnancy found a reduction in preterm birth (RR 0.76 (95%CI 0.58-0.99)) and placental abruption in treated versus untreated smokers [68]. This effect was not observed among nonsmokers. Clearly, more research is needed to explore the potential and scope for vitamin supplementation in pregnant smokers to reduce preterm birth and adverse pulmonary outcomes in their babies. Reduction of SHS exposure during pregnancy The WHO recommends that besides noting active smoking, health care workers should also explore patterns of SHS exposure during pregnancy [59]. Evidence on the effectiveness of interventions to reduce SHS exposure among non-smoking pregnant women is however scarce, as shown by a recent systematic review which identified five RCTs of different interventions [69]. Each showed evidence of benefit in terms of reduction in SHS. A reduction in birth before 34 weeks gestation was furthermore seen after a multifaceted counselling intervention in one of the trials [70]. The review authors however felt that weaknesses in study design precluded firm conclusions to be made and declared the need for more rigorous studies [69]. Reduction of SHS exposure after preterm birth Given the clear associations between postnatal SHS exposure and respiratory symptoms among children born preterm, there is a need for effective interventions to reduce this exposure. We are however aware of only one RCT specifically aimed at reducing SHS exposure among infants born preterm after discharge from the neonatal unit [71]. Motivational interviewing to address smoking and SHS resulted in a short-term increase in the number of children being protected by home smoking bans and a reduction in infant contact with smokers. Neither however persisted until end of the study (i.e. eight months post-discharge), and the intervention had no significant impact on respiratory symptoms.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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Transferrable lessons may be drawn from studies assessing the effectiveness of interventions to reduce SHS exposure in infants and children, irrespective of preterm birth status. Such studies have recently been systematically reviewed, showing mixed results overall [72]. In 14 out of the 57 studies a significant reduction in child SHS exposure was achieved. Many effective studies used counselling or motivational interviewing techniques, however so did many studies with negative results. Generalisation is therefore difficult and interventions to reduce childhood SHS exposure likely need to be tailored to specific settings and populations, including infants and children born preterm. Opportunities for prevention: population-level interventions Governmental policies have significant potential to reduce smoking and SHS exposure. The WHO recommends countries worldwide to implement a package of comprehensive tobacco control measures to reduce the considerable harm caused by smoking and SHS exposure [6]. Evidence is now increasing that such policies also benefit perinatal and child health, including via reducing preterm birth. Smoke-free legislation Smoke-free public environments enforced through legislation are effective in reducing SHS exposure [73]. Studies in several countries have furthermore demonstrated significant reductions in maternal smoking during pregnancy following the introduction of smoke-free laws [74–78]. Consistent with these reductions in maternal smoking and SHS exposure and their link with preterm birth, implementation of smoke-free legislation was associated with a 10.4% (95%CI 2.0-18.8) reduction in preterm births in a recent meta-analysis which included over 1.3 million births [79]. A subsequent Canadian study confirmed the finding [80]. Smoke-free legislation has furthermore been associated with reductions in stillbirth, neonatal mortality, very-small-for-gestational-age births, and hospital attendance for childhood asthma and respiratory tract infections [79,81,82]. Tobacco taxation Another promising policy intervention is tobacco taxation. Studies have demonstrated a dose-dependent association between increased taxation and reductions in smoking during pregnancy [77,83–86]. In a recent US multi-state analysis this was associated with significant reductions in preterm birth among black mothers, and among white mothers with low educational levels [85]. This suggests that tobacco taxation may help reduce inequalities in maternal smoking, and accordingly, preterm birth incidence [84,85]. Implications for practice and future research needs Maternal smoking is associated with a clinically relevant increased risk of preterm birth, and smoking cessation in early pregnancy can reduce this risk. Individual-level psychosocial interventions are of proven benefit and should ideally be offered to all smoking pregnant women. Peer support and financial incentives may be of additional value, whereas the effectiveness of NRT has not definitely been established. Although stopping smoking before conception is theoretically preferable, more research is needed to identify the effectiveness of interventions at this stage. Overall, given the small absolute reductions in smoking prevalence with most individual-level interventions, there remains a need to explore additional interventions, including simple harm reduction approaches such as vitamin C/E supplementation. There is a need for rigorous studies to evaluate interventions to reduce SHS exposure during pregnancy and after birth, particularly among those born preterm. From a policy perspective there is
evidence that smoke-free legislation and tobacco taxes can help reduce adverse pregnancy outcomes, including preterm birth, supporting WHO recommendations to implement these policies on a global scale [6]. There is a great need to address the lack of studies evaluating the effectiveness of individual-level and policylevel interventions in low- and middle income countries, given the substantial contribution of these countries to the global burden of smoking, SHS exposure, and preterm birth. CONCLUSIONS Smoking in pregnancy is associated with a range of adverse pregnancy outcomes, including preterm birth, and may continue to affect children’s health throughout their life course. The significant burden associated with smoking and SHS exposure during pregnancy and childhood is entirely preventable. Helping future mothers to stop smoking and protect their children from SHS exposure must be a key priority for health care workers and policy makers alike. CONFLICT OF INTEREST The authors have no conflicts of interest to disclose. FUNDING JVB is supported by fellowship grants from the Netherlands Lung Foundation and the Erasmus University Medical Centre. The sponsors had no involvement in the collection, analysis, and interpretation of data, or in the writing of the manuscript.
PRACTICE POINTS Tobacco smoking and smoke exposure during pregnancy are associated with a range of adverse health outcomes in offspring, including preterm birth Emerging evidence suggests that smoking during pregnancy is associated with increased risk of complications following preterm birth Postnatal smoke exposure among children born preterm is associated with increased risk of respiratory complications, including asthma Counselling interventions promote smoking cessation during pregnancy and reduce the risk of preterm birth Peer support and incentive-based interventions are likely to be of additional benefit to promote smoking cessation during pregnancy Smoke-free legislation is associated with a reduction in preterm birth, likely mediated via reductions in smoking and smoke exposure during pregnancy
RESEARCH DIRECTIONS Effectiveness of preconception smoking cessation strategies Effectiveness of incentive-based interventions to reduce smoking during pregnancy in different settings Effectiveness of interventions aimed at reducing smoke exposure among children born preterm Effectiveness of interventions in low- and middle income countries to reduce smoking during pregnancy and preand postnatal smoke exposure
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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Contents lists available at ScienceDirect
Paediatric Respiratory Reviews
Mini-Symposium: Interventions to Prevent Respiratory Disease
Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications Mary-ann Wagijo 1, Aziz Sheikh 2,3, Liesbeth Duijts 1,4,5, Jasper V. Been 1,2,3,* 1
Division of Neonatology, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB, Rotterdam, The Netherlands Centre of Medical Informatics, Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK 3 School for Public Health and Primary Care (CAPHRI), Maastricht University, PO Box 616, 6200MD Maastricht, The Netherlands 4 Department of Paediatrics, division of Respiratory Medicine, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB Rotterdam, The Netherlands 5 Department of Epidemiology, Erasmus University Medical Centre, PO Box 2060, 3000CB, Rotterdam, The Netherlands 2
EDUCATIONAL AIMS THE READER WILL BE ABLE TO DISCUSS: Aspects of the relationship of tobacco smoking during pregnancy and second-hand smoke exposure with preterm birth and its complications The effectiveness of interventions aimed at preventing tobacco smoking and its harmful effects during pregnancy The effectiveness of interventions to reduce pre- and postnatal smoke exposure in relation to preterm birth and its complications
A R T I C L E I N F O
S U M M A R Y
Keywords: Premature birth Infant Tobacco use Smoking Pregnancy Prevention Smoking cessation Smoke-free policy
Tobacco smoking and smoke exposure during pregnancy are associated with a range of adverse health outcomes, including preterm birth. Also, children born preterm have a higher risk of complications including bronchopulmonary dysplasia and asthma when their mothers smoked during pregnancy. Smoking cessation in early pregnancy can help reduce the adverse impact on offspring health. Counselling interventions are effective in promoting smoking cessation and reducing the incidence of preterm birth. Peer support and incentive-based approaches are likely to be of additional benefit, whereas the effectiveness of pharmacological interventions, including nicotine replacement therapy, has not definitely been established. Smoke-free legislation can help reduce smoke exposure as well as maternal smoking rates at a population level, and is associated with a reduction in preterm birth. Helping future mothers to stop smoking and protect their children from second hand smoke exposure must be a key priority for health care workers and policy makers alike. ß 2015 Elsevier Ltd. All rights reserved.
INTRODUCTION Tobacco smoking and second-hand smoke (SHS) exposure during pregnancy are associated with a considerable burden of
* Corresponding author. Division of Neonatology, Erasmus University Medical Centre – Sophia Children’s Hospital, PO Box 2060, 3000CB Rotterdam, The Netherlands; Tel.: +31 10 7036077; fax: +31 10 7036542. E-mail addresses: [email protected] (M.-a. Wagijo), [email protected] (A. Sheikh), [email protected] (L. Duijts), [email protected] (J.V. Been).
adverse perinatal and child health outcomes [1,2]. Among these is preterm birth, currently the leading cause of death in children worldwide and responsible for considerable morbidity among survivors [3,4]. This review will first map out the global burden of mortality and morbidity resulting from tobacco smoking and preterm birth. We will then outline how smoking and SHS exposure are linked to preterm birth and its complications, with particular attention to complications affecting the lungs. Finally we will highlight various approaches to reduce the impact of tobacco smoking and SHS exposure on preterm birth and its complications.
http://dx.doi.org/10.1016/j.prrv.2015.09.002 1526-0542/ß 2015 Elsevier Ltd. All rights reserved.
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Global burden of tobacco smoking and SHS exposure Prevalence and consequences of smoking Every year, approximately six million people die because of tobacco use, making it the primary preventable cause of mortality worldwide [5,6]. Tobacco use is causally linked to many diseases, including different types of cancer, cardiovascular diseases and chronic obstructive pulmonary disease (COPD) [1,6]. Between 1980 and 2012, the worldwide smoking prevalence decreased from 41% to 31% among men and from 11% to 6% among women [5]. However due to population growth the absolute number of daily smokers increased from 721 million to 967 million during that period [5]. Important variation exists in smoking prevalence across countries with, for example, very high prevalence among men in Russia and Indonesia (both >50%) and among women in Greece and Bulgaria (both >25%) [5]. Prevalence and consequences of SHS exposure Tobacco is not only harmful to the health of its users; it also affects the health of non-smokers through exposure to SHS [1]. SHS exposure was estimated to have caused 603 000 deaths and 10.9 million disability adjusted life years (DALYs) worldwide in 2004 [7]. SHS exposure is highest in children (40%), compared to men (33%) and women (35%) [7]. Over 25% of the lives and over 60% of the health life years estimated to be lost due to SHS exposure each year are among children [7]. This is likely an underestimation of tobacco’s true impact on early-life health as it is solely based on the well-recognised impact of SHS on respiratory tract infections and asthma in childhood [8]. Many children are however in addition affected by antenatal smoke exposure, either via active maternal smoking or maternal SHS exposure, putting them at risk of a range of adverse perinatal and long-term outcomes [1,2,6]. Smoking and SHS exposure during pregnancy The prevalence of antenatal smoke exposure varies by country according to its social, cultural, and ethnic background. In highincome countries, an estimated 10-20% of women smoke during pregnancy, with high percentages in the United Kingdom (14-20%) and the United States (US; 15-18%) [9]. Smoking during pregnancy is much less common in low- and middle-income countries, with an overall prevalence of 1.3% (range 0-15%) estimated from 20012012 Demographic and Health Survey data from 54 countries [10]. Of concern, however, is that in some of these countries up to 75% of pregnant women are exposed to SHS [11]. Multiple epidemiologic studies and meta-analyses have demonstrated maternal smoking during pregnancy to be associated with severe adverse pregnancy outcomes, including: stillbirth [12], congenital anomalies [13], low birth weight [1], preterm birth [14], and neonatal mortality [1]. Children whose mothers smoked during pregnancy are furthermore at increased risk of sudden infant death syndrome (SIDS) [15], respiratory tract infections [16], recurrent wheezing [17], asthma [18], overweight and obesity [19], cognitive delay [20], and behavioural problems [20]. There is increasing evidence that maternal smoking also increases the offspring’s risk of taking up smoking themselves later on [21]. Although SHS exposure during pregnancy is generally less strongly associated with adverse paediatric health outcomes than is active smoking, it has been linked to increased risks of low birth weight and childhood asthma [22,23]. Epidemiology of preterm birth and its complications Incidence of preterm birth In 2010, an estimated 14.9 million babies were born preterm worldwide [8]. Over 60% of all preterm births were
in Sub-Saharan Africa and South Asia [8]. Although in developed countries the overall preterm birth rate is relatively low at 8.6% compared to the global rate of 11.1%, the US ranks among the top 10 countries contributing to the global number of preterm births, with 12.0% of babies being born preterm [8]. Preterm birth is thus a global public health problem, which is likely to escalate given that only three out of 184 countries experienced a reduction in preterm birth rate between 1990 and 2010 [8]. Mortality attributable to preterm birth Annually, approximately one million deaths are directly attributable to preterm birth [4,24]. Although low- and middleincome countries contribute the majority of preterm-birth related deaths, several high-income countries are among those with the highest percentage of deaths being directly attributable to preterm birth [4]. Variation is influenced by many factors including the level of care available and provided, ethnic and socioeconomic background of the population, and ethical considerations regarding resuscitation of babies born at the edge of viability, and end-oflife decisions. Complications of preterm birth When healthy, the uterus provides the optimal environment for the developing fetus. Preterm birth however removes a baby from this environment during a critical phase of development, putting it at risk of many adverse outcomes [3]. For almost all outcomes the risk is highly gestational age-dependent, with the highest prevalence seen among the most preterm infants. Common pathological processes underlying preterm birth, including intrauterine inflammation and infection, preeclampsia, and intrauterine growth restriction, have distinct adverse effects on specific organs, further modulating these risks. Respiratory complications The introduction of antenatal corticosteroids and postnatal surfactant therapy has allowed for increased survival after preterm birth and thereby for respiratory complications to shift towards much more immature babies. Respiratory distress remains a common early sign of very preterm birth. Despite a general shift away from aggressive ventilator strategies, an important proportion of extremely preterm infants go on to develop chronic lung disease of prematurity, bronchopulmonary dysplasia (BPD). BPD likely represents the severe end of a spectrum of prematurity-related respiratory complications, and is associated with sustained airway obstruction and wheezing symptoms [25]. Especially during the first years, children born preterm are at increased risk of re-hospitalisation, often due to respiratory problems and in particular bronchiolitis [26]. Prematurity-associated respiratory problems may extend well into later life [3], with increased risks for childhood asthma [27,28], and chronic obstructive pulmonary disease (COPD) [29]. Even children born near-term are increasingly recognised to be at risk for adverse pulmonary outcomes and as a group are the primary contributors to the overall burden of prematurity-associated respiratory problems [27]. Other complications Common severe non-respiratory neonatal complications following preterm birth include: sepsis, necrotising enterocolitis (NEC), intraventricular haemmorrhage (IVH), periventricular leukomalacia (PVL), and retinopathy of prematurity (ROP). In the long term, developmental impairments, including motor disturbances and cognitive and communicative deficits, and behavioural problems are commonly seen.
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Maternal tobacco smoking and SHS exposure and the risk of preterm birth Maternal smoking and preterm birth The association between maternal smoking during pregnancy and preterm birth has been assessed in numerous studies. To the best of our knowledge the most recent meta-analysis on the topic was published in 2000 [14]. Data from 20 prospective studies where preterm birth rates were reported according to at least two levels of maternal smoking were combined. Maternal smoking during pregnancy was associated with a 1.27 (95%CI 1.21-1.33) times increased risk for preterm birth. There was evidence of a dose-response association, with risk for light smokers (0-10 cigarettes/day) being lower than for moderate and heavy smokers. Numerous large studies have been conducted since this metaanalysis, almost invariably confirming the association between maternal smoking and preterm birth, including various studies demonstrating evidence of a dose-response effect [30–34]. Findings from some of these studies suggest that smoking differentially affects very preterm as opposed to moderately preterm birth. An analysis of over 1 million singleton births in Missouri furthermore demonstrated that the risk was increased for both spontaneous and indicated preterm birth [30]. It is important to note that the vast majority of studies adjusted for possible confounders including pregnancy-related disorders, maternal age, socioeconomic status and lifestyle factors. Maternal smoking is commonly self-reported and not biochemically validated, which is important as underreporting of maternal smoking from self-report is well recognised [1]. Underreporting leads to contamination of the control group with smokers, resulting in likely underestimation of the true association between maternal smoking and preterm birth. Maternal smoking and preterm birth: underlying mechanisms The potential mechanisms underlying the link between maternal smoking and preterm birth have recently been reviewed [35]. Overall the mechanisms remain poorly understood and are likely to be multifactorial. Many cases of preterm delivery associated with maternal smoking are mediated via intrauterine growth restriction, necessitating early delivery for fetal concerns. Smoking increases levels of carbon monoxide, which readily passes the placenta, displacing oxygen from haemoglobin and decreasing its ability to release oxygen to the tissues [35]. Nicotine has been shown to decrease uterine blood flow, and human data are indicative of increased resistance and microscopic changes in placental vasculature among smokers [35]. Whereas these mechanisms are likely involved in the association of maternal smoking with intrauterine growth restriction, others appear to underlie its association with spontaneous preterm delivery. Smoking predisposes to intrauterine infection, cervical insufficiency, and preterm prelabour rupture of membranes, all key causes of spontaneous preterm delivery [31,36]. Oxidative stress and reduced anti-oxidant capacity, reduced progesterone levels, and increased oxytocin sensitivity and prostaglandin production may in addition promote uterine contractility and induce preterm labour in smokers [31,35]. Maternal SHS exposure and preterm birth Two meta-analyses have addressed the association between maternal SHS exposure during pregnancy and preterm birth [22,37]. Leonardi-Bee et al. combined data from studies assessing the association between ‘any record of maternal contact’ with SHS and preterm birth among non-smoking women [22]. SHS exposure was associated with preterm birth in retrospective studies (nine studies; OR 1.18 (95%CI 1.03-1.35), but not in prospective studies (eight studies; p = 0.24, OR not reported) and one case-control
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study (OR 0.92 (95%CI 0.65-1.31)). In a separate meta-analysis, Salmasi et al. combined data from studies where SHS exposure was either self-reported or biochemically validated and where active smokers were either excluded or controlled for in the analyses [37]. There was no significant association between maternal SHS exposure and preterm birth in meta-analyses of unadjusted or adjusted effect estimates (unadjusted: 18 studies, OR 1.20 (95%CI 0.99-1.46); adjusted: seven studies, OR 1.07 (95%CI 0.93-1.22)). Individual studies published since also showed mixed evidence, although a rather strong association for very preterm versus moderate preterm birth was observed in one study [38]. Maternal tobacco smoking, SHS exposure, and complications following preterm birth Respiratory complications The adverse impact of antenatal smoke exposure on lung development and adverse respiratory outcomes, in particular wheezing and asthma, is well recognised [18]. Antenatal smoke exposure disrupts lung development in mice, resulting in a pathological picture closely resembling human BPD [39]. Observed airway smooth muscle layer thickening, collagen deposition, and increased numbers of house dust mite-induced goblet cells may all contribute to airway remodeling and hyper-responsiveness [40]. Nicotine-mediated reductions in placental blood flow, fetal oxygen and nutrient supply, fetal breathing movements and changes in alveolar type II cell metabolism may explain abnormal growth and maturation of the airways and lungs and subsequent development of respiratory diseases [41–43]. Last, antenatal smoke exposure seems to alter expression of susceptibility genes for respiratory diseases via reduction of histone deacetylase activity and changes in methylation patterns [44]. Maternal smoking has been associated with the development of BPD in a case-control study of Italian very-low-birth-weight (VLBW) infants: OR 2.21 (95%CI: 1.03-4.76) [45]. This association was confirmed in a large population-based Canadian cohort of very preterm infants (OR 1.16 (95%CI 1.02-1.33)) [46], as well as a German cohort of preterm VLBW infants (OR 1.34 (95%CI 1.011.79)). [47] At follow up, home SHS exposure was associated with increased need for inhaled corticosteroids in US children with BPD (86% vs. 76% in exposed vs. non-exposed, p = 0.05) [48]. Hair nicotine levels furthermore predicted activity limitation and hospitalisation among those requiring respiratory support [49]. SHS exposure is associated with respiratory complications beyond BPD among children born preterm (Figure 1). Home SHS exposure was independently associated with wheezing in very preterm and VLBW infants [50,51], and with the need for acute care for respiratory problems during the first year of life [52]. A significant interaction between preterm birth and maternal smoking was demonstrated in another prospective birth cohort, maternal smoking during pregnancy
antenatal SHS exposure ?
fetus newborn
?
preterm birth
BPD
child
wheezing / asthma
postnatal SHS exposure
Figure 1. Impact of tobacco smoke exposure on preterm birth and its respiratory complications. Blue arrows indicate positive associations, red arrows indicate positive interactions. BPD = bronchopulmonary dysplasia.
Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002
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with children born preterm to smoking mothers having the highest risk of recurrent wheezing (OR 4.0 (95%CI 1.9-8.6) vs. children born at term to non-smoking mothers) [53]. Other complications Several studies suggest that the negative impact of antenatal tobacco smoke exposure among children born preterm may not be confined to the lung. The largest cohort study on the topic to date demonstrated an independent 1.17 (95%CI 1.04-1.32) times increased risk of developing a composite outcome of death or major morbidity among preterm babies whose mothers smoked [46]. Specific adverse outcomes associated with maternal smoking included BPD, and severe IVH or PVL [46]. The study did not confirm the increased risk of ROP seen in another, smaller cohort [46,47]. Maternal smoking was furthermore identified as a major risk factor for NEC in a recent case control study [54], although the association did not reach statistical significance in two recent cohort studies [46,47]. Overall, given the low number of studies and their inconsistent findings, as well as the lack of mechanistic studies on the topic, no firm conclusions can be made regarding the impact of maternal tobacco smoking on extrapulmonary complications of preterm birth. Smoking cessation and preterm birth risk Results from observational studies indicate that stopping smoking before or early in pregnancy has the potential to
normalise preterm birth risk. In an elegant study, Cnattingius and colleagues evaluated pregnancy outcomes in almost 250 000 women who delivered two consecutive singleton infants [55]. The risks of very and moderately preterm birth were increased in the second versus the first pregnancy in initially non-smoking women who took up smoking before the second pregnancy, whereas the risk normalised in women who smoked during the first pregnancy but stopped before the second. Both associations were dose-dependent, the risk differences being more pronounced with increasing number of cigarettes smoked. Several studies have since confirmed that the risks of preterm birth and other adverse pregnancy outcomes after stopping smoking before or early in pregnancy indeed decrease to those observed among nonsmoking women, while the risks remained elevated in women who continued smoking [31,34,56–58]. This indicates that interventions to support smoking cessation either pre-conception or in the first trimester have significant potential to reduce preterm birth. Pregnancy may be a major ‘teachable moment’ to promote a healthy lifestyle given mothers’ concern about fetal health and their regular contact with health care providers. It is imperative that these providers identify smokers who are either pregnant or planning to become pregnant as early as possible, to ensure that effective interventions for smoking cessation can be offered [59]. Below we discuss the effectiveness of interventions to promote smoking cessation during pregnancy and to reduce SHS exposure among pregnant women and their offspring (see also Table 1).
Table 1 Best evidence on interventions to reduce maternal smoking and pre- and postnatal SHS exposure Type of intervention
Study design
Individual and family based – smoking cessation Preconception counselling Systematic review [60]
Psychosocial interventions
Systematic review [61]
Incentive-based interventions
RCT [62]
Nicotine replacement therapy
Systematic review [63]
Other pharmacological interventions Physical activity (adjunct to counselling) Relapse prevention
Systematic review [63]
*
RCT [65] Systematic review [66]
Individual and family based – harm reduction Vitamin C / E supplementation in RCT [67] pregnant smokers RCT (secondary analysis) [68] Individual and family based – SHS exposure reduction SHS reduction during pregnancy Systematic review [69] SHS reduction after NICU discharge Policy-based interventions Smoke-free legislation
Systematic review [79]
Tobacco taxation
Quasi-experimental study [85]
RCT [71]
Main findings
Impact on preterm birth and related complications
Only three studies identified, including two observational studies; some evidence that quit advice may reduce smoking rates and promote relapse during pregnancy Counselling interventions are effective in reducing smoking rates up to 17 months postpartum, especially when combined with other strategies. Peer support programs are also effective. Health education alone had no effect on smoking cessation during pregnancy. Financial incentives increase smoking cessation during pregnancy. No significant effect on smoking rates among pregnant women. No studies available
NA
Counselling interventions reduce preterm birth
No significant effect on preterm birth No significant effect on preterm birth NA
No significant effect on smoking cessation during pregnancy No significant effect of behavioral interventions on smoking relapse during pregnancy or at postpartum follow-up
No significant effect on preterm birth
Vitamin C 500 mg /day
Better respiratory outcomes among offspring of smokers Reduction in preterm birth and placental abruption among smokers
Vitamin C 1000 mg /day + vitamin E 400 IU
NA
Five RCTs all showed some effect on SHS exposure but overall evidence of low quality Motivational interviewing reduces SHS exposure at home, but only on short-term
Reduction in preterm birth before 34 weeks in one RCT of multifaceted intervention No significant effect on respiratory outcomes after NICU discharge
Smoke-free legislation known to be associated with reduced SHS exposure and reduced smoking during pregnancy Tobacco tax increase associated with reductions in maternal smoking among white mothers with low education and black mothers
Reduction in preterm birth after smoke-free legislation Tobacco tax increase associated with small reduction in preterm birth among white mothers with low education and black mothers
* several very small studies are available but not reported here. RCT: randomized controlled trial; NA: Not Assessed; SHS: second-hand smoke; NICU: neonatal intensive care unit.
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Opportunities for prevention: individual-level and family-based interventions Preconceptional smoking cessation A recent systematic review of preconception counselling strategies identified only three studies that focused on smoking [60]. Overall the results were mixed, with some evidence of a reduction in smoking and maintenance of cessation with quit advice, with or without counselling. Pregnancy outcomes were not reported. Interpretation is complicated by the observational study design of two studies and differences in intervention strategy. Smoking cessation during pregnancy – psychosocial interventions Much more data is available for interventions to promote smoking cessation during pregnancy. Eighty-six trials were included in a recent Cochrane review on the efficacy of psychosocial interventions [61]. Among these, counselling interventions increased smoking abstinence in late pregnancy as compared to usual care (27 studies; risk ratio (RR) 1.44 (95%CI 1.19-1.75)) or to less intensive interventions (16 studies; RR 1.35 (95%CI 1.00-1.82)) in meta-analyses. Of note, reduced smoking rates were sustained up to 17 months post-partum. The effect was generally larger when counselling was combined with other strategies such as providing feedback via biochemical measures of cessation or fetal health indicators: two studies, RR 4.39 (95%CI 1.89-10.21). Most importantly, counselling interventions significantly reduced the risks of preterm delivery (14 studies, RR 0.82 (95%CI: 0.70-0.96)) and delivering a low-birth-weight baby. Another effective approach identified in this review included social support provided by peers (5 studies, RR 1.49 (95%CI 1.012.19)). Health education had no significant impact on smoking cessation during pregnancy. Smoking cessation during pregnancy – incentive-based interventions Incentive based interventions were deemed promising by the Cochrane review on psychosocial interventions, but only a few small trials were identified [61]. Recently, a large randomised controlled trial (RCT) investigated the effectiveness of offering shopping vouchers of incremental value for sustained, biochemically validated cessation at repeated health visits [62]. The intervention was highly effective in achieving sustained smoking cessation at the end of pregnancy versus routine care: RR 2.63 (95%CI 1.73-4.01). No significant impact on pregnancy complications including preterm birth was observed, but the trial was not powered to assess these outcomes. Smoking cessation during pregnancy – pharmacological interventions Six trials of pharmacological interventions were identified in a recent Cochrane review [63]. All trials evaluated nicotine replacement therapy (NRT), which in meta-analysis was not more effective than control in achieving smoking cessation during pregnancy: RR 1.33 (95%CI 0.93-1.91). NRT also did not affect the risk of preterm delivery, prematurity-related adverse outcomes (i.e. need for mechanical ventilation, IVH, NEC), or serious side-effects. The review authors argue that NRT is likely to be more effective at higher doses and suggest the need for further trials evaluating this. Although guidelines in a number of countries support the use of NRT when psychosocial interventions are not effective, the World Health Organization (WHO) refrains from making a recommendation on this issue [59]. Interestingly, two-year follow-up data of a large RCT recently demonstrated a larger proportion of infants born to mothers in the NRT arm as compared to controls to have unimpaired development: OR 1.40 (95%CI 1.05-1.86) [64]. This supports the need for additional research in this area, with particular attention to offspring follow-up.
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No trials during pregnancy have been conducted to assess the safety or effectiveness of other pharmacological agents used routinely in the treatment of nicotine-dependence in adults and their use is not therefore at present recommended [59,63]. Smoking cessation during pregnancy – other interventions Physical activity as an adjunct to behavioural therapy was recently evaluated in an RCT. No effect on smoking cessation during pregnancy or birth outcomes, including preterm birth, was observed [65]. Relapse prevention In a recent systematic review and meta-analysis, behavioural interventions were not significantly effective in preventing smoking relapse by the end of pregnancy or at longest postpartum follow-up [66]. Harm reduction interventions Evidence from animal studies showing that vitamin C may reverse the negative impact of nicotine on fetal lung development informed a recent RCT of vitamin C supplementation (500 mg/d) to pregnant mothers who declined to quit smoking [67]. Babies randomised to vitamin C had significantly better lung function measures, and less wheezing during the first year of life. The authors acknowledge that the primary goal should be for pregnant women to quit smoking, but conclude that vitamin C may be ‘an inexpensive and simple approach’ to reduce some of the adverse effects on offspring respiratory outcomes associated with smoking. Although the aforementioned trial found no impact of vitamin C on preterm birth [67], a recent secondary analysis of an RCT of combined vitamin C (1000 mg) and E (400 IU) supplementation during pregnancy found a reduction in preterm birth (RR 0.76 (95%CI 0.58-0.99)) and placental abruption in treated versus untreated smokers [68]. This effect was not observed among nonsmokers. Clearly, more research is needed to explore the potential and scope for vitamin supplementation in pregnant smokers to reduce preterm birth and adverse pulmonary outcomes in their babies. Reduction of SHS exposure during pregnancy The WHO recommends that besides noting active smoking, health care workers should also explore patterns of SHS exposure during pregnancy [59]. Evidence on the effectiveness of interventions to reduce SHS exposure among non-smoking pregnant women is however scarce, as shown by a recent systematic review which identified five RCTs of different interventions [69]. Each showed evidence of benefit in terms of reduction in SHS. A reduction in birth before 34 weeks gestation was furthermore seen after a multifaceted counselling intervention in one of the trials [70]. The review authors however felt that weaknesses in study design precluded firm conclusions to be made and declared the need for more rigorous studies [69]. Reduction of SHS exposure after preterm birth Given the clear associations between postnatal SHS exposure and respiratory symptoms among children born preterm, there is a need for effective interventions to reduce this exposure. We are however aware of only one RCT specifically aimed at reducing SHS exposure among infants born preterm after discharge from the neonatal unit [71]. Motivational interviewing to address smoking and SHS resulted in a short-term increase in the number of children being protected by home smoking bans and a reduction in infant contact with smokers. Neither however persisted until end of the study (i.e. eight months post-discharge), and the intervention had no significant impact on respiratory symptoms.
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Transferrable lessons may be drawn from studies assessing the effectiveness of interventions to reduce SHS exposure in infants and children, irrespective of preterm birth status. Such studies have recently been systematically reviewed, showing mixed results overall [72]. In 14 out of the 57 studies a significant reduction in child SHS exposure was achieved. Many effective studies used counselling or motivational interviewing techniques, however so did many studies with negative results. Generalisation is therefore difficult and interventions to reduce childhood SHS exposure likely need to be tailored to specific settings and populations, including infants and children born preterm. Opportunities for prevention: population-level interventions Governmental policies have significant potential to reduce smoking and SHS exposure. The WHO recommends countries worldwide to implement a package of comprehensive tobacco control measures to reduce the considerable harm caused by smoking and SHS exposure [6]. Evidence is now increasing that such policies also benefit perinatal and child health, including via reducing preterm birth. Smoke-free legislation Smoke-free public environments enforced through legislation are effective in reducing SHS exposure [73]. Studies in several countries have furthermore demonstrated significant reductions in maternal smoking during pregnancy following the introduction of smoke-free laws [74–78]. Consistent with these reductions in maternal smoking and SHS exposure and their link with preterm birth, implementation of smoke-free legislation was associated with a 10.4% (95%CI 2.0-18.8) reduction in preterm births in a recent meta-analysis which included over 1.3 million births [79]. A subsequent Canadian study confirmed the finding [80]. Smoke-free legislation has furthermore been associated with reductions in stillbirth, neonatal mortality, very-small-for-gestational-age births, and hospital attendance for childhood asthma and respiratory tract infections [79,81,82]. Tobacco taxation Another promising policy intervention is tobacco taxation. Studies have demonstrated a dose-dependent association between increased taxation and reductions in smoking during pregnancy [77,83–86]. In a recent US multi-state analysis this was associated with significant reductions in preterm birth among black mothers, and among white mothers with low educational levels [85]. This suggests that tobacco taxation may help reduce inequalities in maternal smoking, and accordingly, preterm birth incidence [84,85]. Implications for practice and future research needs Maternal smoking is associated with a clinically relevant increased risk of preterm birth, and smoking cessation in early pregnancy can reduce this risk. Individual-level psychosocial interventions are of proven benefit and should ideally be offered to all smoking pregnant women. Peer support and financial incentives may be of additional value, whereas the effectiveness of NRT has not definitely been established. Although stopping smoking before conception is theoretically preferable, more research is needed to identify the effectiveness of interventions at this stage. Overall, given the small absolute reductions in smoking prevalence with most individual-level interventions, there remains a need to explore additional interventions, including simple harm reduction approaches such as vitamin C/E supplementation. There is a need for rigorous studies to evaluate interventions to reduce SHS exposure during pregnancy and after birth, particularly among those born preterm. From a policy perspective there is
evidence that smoke-free legislation and tobacco taxes can help reduce adverse pregnancy outcomes, including preterm birth, supporting WHO recommendations to implement these policies on a global scale [6]. There is a great need to address the lack of studies evaluating the effectiveness of individual-level and policylevel interventions in low- and middle income countries, given the substantial contribution of these countries to the global burden of smoking, SHS exposure, and preterm birth. CONCLUSIONS Smoking in pregnancy is associated with a range of adverse pregnancy outcomes, including preterm birth, and may continue to affect children’s health throughout their life course. The significant burden associated with smoking and SHS exposure during pregnancy and childhood is entirely preventable. Helping future mothers to stop smoking and protect their children from SHS exposure must be a key priority for health care workers and policy makers alike. CONFLICT OF INTEREST The authors have no conflicts of interest to disclose. FUNDING JVB is supported by fellowship grants from the Netherlands Lung Foundation and the Erasmus University Medical Centre. The sponsors had no involvement in the collection, analysis, and interpretation of data, or in the writing of the manuscript.
PRACTICE POINTS Tobacco smoking and smoke exposure during pregnancy are associated with a range of adverse health outcomes in offspring, including preterm birth Emerging evidence suggests that smoking during pregnancy is associated with increased risk of complications following preterm birth Postnatal smoke exposure among children born preterm is associated with increased risk of respiratory complications, including asthma Counselling interventions promote smoking cessation during pregnancy and reduce the risk of preterm birth Peer support and incentive-based interventions are likely to be of additional benefit to promote smoking cessation during pregnancy Smoke-free legislation is associated with a reduction in preterm birth, likely mediated via reductions in smoking and smoke exposure during pregnancy
RESEARCH DIRECTIONS Effectiveness of preconception smoking cessation strategies Effectiveness of incentive-based interventions to reduce smoking during pregnancy in different settings Effectiveness of interventions aimed at reducing smoke exposure among children born preterm Effectiveness of interventions in low- and middle income countries to reduce smoking during pregnancy and preand postnatal smoke exposure
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Please cite this article in press as: M- Wagijo, et al. Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications. Paediatr. Respir. Rev. (2015), http://dx.doi.org/10.1016/j.prrv.2015.09.002