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ORIGINAL RESEARCH |
From the Departments of Health Studies, Obstetrics & Gynecology, and Psychiatry, University of Chicago, Chicago, Illinois.
Address reprint requests to: Kate E. Pickett, PhD, University of Chicago, Department of Health Studies, 5841 South Mary-land Ave, MC 2007, Chicago, IL 60637; E-mail: kpickett{at}health.bsd.uchicago.edu.
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ABSTRACT |
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METHODS: We examined changes in absolute smoking status in 1426 women who reportedly smoked during their last pregnancy in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement and fluctuations in amount smoked in 60 pregnant smokers in the Family Health and Development Project.
RESULTS: In the National Health Interview Survey 1991 Pregnancy and Smoking Supplement, a substantial proportion of women exhibited a pattern of repeated cessation and relapse. In multivariable logistic regression models, having more than a high school education was significantly associated with being an intermittent versus a continuous smoker (odds ratio = 1.55, P < .01) and with successful quitting versus continuously smoking or relapsing (odds ratio = 1.74, P < .01). Fluctuations in smoking intensity in the Family Health and Development Project were also substantial and, although 48% quit or reduced their smoking upon learning of their pregnancy, over half changed smoking intensity multiple times.
CONCLUSION: We conclude that smoking during pregnancy is a complex and variable behavior for many women. Simple measures of smoking may lead to under-estimation of the impact of smoking on the fetus, and brief smoking cessation interventions early in pregnancy are likely to be inadequate for many smokers during pregnancy.
The latest evidence from US vital statistics reports suggests that 12.9% of women smoke during pregnancy, although prevalence varies widely by region, ethnicity, age, and socioeconomic status, ranging from 9% to 42% in various subgroups.1 Pregnant women are increasingly aware that smoking may be harmful to their offspring and are under significant social pressure to quit.2 As a result, the stability that characterizes smoking behavior in adulthood in general3,4 may not be characteristic of smoking during pregnancy. Many women stop smoking upon learning they are pregnant.5 Those who do not quit for the duration may quit, reduce, and relapse multiple times during pregnancy, balancing their desire to promote the health of their infant against nicotine dependence, stress, and other pressures that induce smoking. Although there is some evidence of variability in pregnancy smoking,6 the extent and pattern of within person variation is unknown. If there were widespread fluctuations in smoking during pregnancy, this would have substantial implications for both treatment of tobacco use during pregnancy and research into the effects of fetal exposure to cigarette smoke.
Public health and clinical interventions for women who smoke during pregnancy are typically brief, didactic interventions, integrated into an early prenatal care visit.7 Although such interventions can reach a large number of pregnant women, even the most effective "best practices" interventions are successful with, at best, only 20% of women.8 Understanding patterns of cessation, reduction, and relapse over the course of pregnancy may be vital to developing targeted interventions for pregnant women for whom standard interventions are not successful.
Different patterns of timing, duration, and intensity of fetal exposure to cigarette smoke are likely to result in differences in the effect of smoking on fetal outcomes. During pregnancy, different dimensions of fetal growth and development follow different trajectories.9–13 Linear growth rate peaks early in pregnancy, growth in lean body mass peaks in the second trimester, and subcutaneous fat deposition occurs mainly in the third trimester. Brain development, including cell differentiation and the development of neuroregulatory systems, occurs primarily in the second and third trimesters of pregnancy, and it has been suggested that neurobehavioral effects of smoking during pregnancy may occur in this latter part of pregnancy.14 Studies of the effects of stopping or reducing smoking during pregnancy on perinatal outcomes have shown that quitting smoking protects fetal growth,15–17 but timing effects have not been studied systematically.16,18,19 Intensity or heaviness of smoking is related to fetal growth, so reducing the amount smoked during pregnancy can be a harm reduction strategy for women who are unable to quit20; however, quitting smoking has been shown to be more effective than harm reduction strategies in protecting fetal growth and development in the first trimester.21
Evidence is accumulating to suggest that exposure to maternal cigarette smoke during pregnancy may also have subtle and long-term health consequences for offspring. For example, fetal exposure may result in compromised lung growth and function,22 intellectual deficits,23 and increased risk of disruptive behavior disorders.24 In many epidemiologic studies, however, maternal smoking has generally been measured categorically (eg, any smoking versus none) or has been treated as a behavior that is stable throughout pregnancy (eg, average cigarettes per day in pregnancy), and has often been measured retrospectively. Consequently, variations in dosage, timing, and duration have not been systematically examined in relation to these outcomes. Establishing the prevalence and patterns of fluctuations in populations of smokers during pregnancy is an important next step in developing valid, informative methodological approaches for characterizing fetal exposure.
The objective of this study was to determine whether or not, and to what degree, smoking during pregnancy is a fluctuating behavior.
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MATERIALS AND METHODS |
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The National Health Interview Survey is an annual survey of the prevalence of illness and use of health services in a nationally representative sample of US adults.25 Each year, supplemental special interest questions are added to the core interview and, in 1991, the supplement surveyed women aged 18–49 years regarding pregnancy and cigarette smoking. There were 29,239 women, aged 18–49 years in the core survey, and 97% of these women answered the supplemental questions on pregnancy and smoking; 7170 had delivered a live infant in the previous 5 years and provided data on smoking. Twenty percent of women in this subsample (n = 1426) reported any smoking during their last pregnancy.
Women were interviewed once, either in person or by telephone, at varying lengths of time since the index pregnancy. They were asked if they had smoked cigarettes when they became pregnant or at any time during the pregnancy. Women who reported any pregnancy smoking were asked if they ever quit smoking for at least 1 week and in what month of pregnancy that occurred, whether or not they started smoking again, and how long they stayed off cigarettes. These questions were repeated to assess possible second and third quit attempts during pregnancy. Information on smoking intensity was not collected in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement.
The Family Health and Development Project is a clinic-based sample of 96 pregnant women, recruited through Chicago-area prenatal clinics, during the first trimester of pregnancy. The purpose of the study was to examine the effect of fetal exposure to cigarette smoking on infant behavior. Smokers were intentionally over-sampled, and the sample included 60 women (63%) who were smoking at the start of pregnancy; as no nonsmokers started smoking, these 60 women form the analytic sample for this study.
Data on smoking were collected via in-depth, in-person interviews once during each trimester. Women were queried about "average smoking on a typical day during the current trimester" as well as month-by-month smoking behavior during that trimester. Using the month-by-month report of cigarettes smoked per day, we defined smoking intensity categorically, based on self-reported number of daily cigarettes in each month: 0 = not smoking, 1–5 = light smoking, 6–10 = moderate smoking, 10+ heavy smoking.
We compared the sociodemographic characteristics of those who did and did not smoke during pregnancy within the National Health Interview Survey 1991 Pregnancy and Smoking Supplement, using t tests for differences in means of continuous variables and 
2 tests for differences in proportions of categorical variables.
In the National Health Interview Survey 1991 Pregnancy and Smoking Supplement, we calculated changes in absolute smoking status (smoking, quitting, relapse), as well as the average duration of smoking during pregnancy among women who quit and relapsed one or more times. Sampling weights were incorporated into all analyses of the National Health Interview Survey 1991 Pregnancy and Smoking Supplement to account for the complex sampling scheme. Among smokers, we also estimated the relationship of sociodemographic and smoking characteristics to the risk of being a constant versus an intermittent smoker and to the risk of successful quitting versus continuing smoking or relapsing in multivariable logistic regression models.
In the smaller Family Health and Development Project, which we viewed as pilot data in which to explore changes in smoking intensity, our analytic approach was descriptive. We estimated the proportion of women who smoked who would be mistakenly classified as nonsmokers, light, moderate, or heavy smokers, based on a summary measure of month-to-month smoking often used in epidemiologic studies (typical number of cigarettes smoked per day after learning of pregnancy) and similar summary measures aimed at isolating fetal exposure in the first and third trimesters (typical number of cigarettes smoked per day for both first and third trimesters).
All statistical analyses were conducted using Stata Statistical Software 7.0 (StataCorp, College Station, TX).
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RESULTS |
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. Consistent with other studies, women who smoked during pregnancy were statistically significantly more likely to be non-Hispanic whites, to be unmarried, to have low income, and to have less than a high school education. Smokers were less likely to be working outside the home. The clinic-based Family Health and Development Project sample was similar: 90% of the women were non-Hispanic white, 48% were married, 61% had family incomes less than $45,000 in 2001, 30% had education beyond high school, and 70% were working when enrolled in the study. Thus, in both samples, the women who smoked during pregnancy seem typical of the established profile of women who smoke during pregnancy in the United States.
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shows changes in absolute smoking status among women who were smoking cigarettes at the start of their most recent pregnancy in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement. Although nearly 40% of the women reported making a serious quit attempt (ie, not smoking for 1 week or more), close to half of these women started smoking again later in the pregnancy.
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The timing of quit attempts also varied. First quit attempts were most frequent in the first trimester (71%); however, 21% of quit attempts took place later in pregnancy, and 8% of first quit attempts took place in the third trimester.
Table 2 shows the results of two multivariable logistic regression models relating maternal sociodemographic characteristics associated with pregnancy in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement to the risk of being 1) an intermittent versus continuous smoker, and 2) a successful quitter versus a continuous or relapsed smoker. Income, marital status, and working outside the home were not statistically significantly associated with smoking status. Non-Hispanic white women were marginally less likely to be quitters (odds ratio [OR] = 0.72, P = .06). Women with at least a high school education were more likely to be intermittent smokers (OR = 1.55, P < .01) and more likely to be successful quitters (OR = 1.74, P < .01). We also estimated the effect of prepregnancy smoking heaviness on the odds of being an intermittent versus a continuous smoker in pregnancy and found no effect (model not shown).
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Figure 2 shows the allocation of women into different smoking categories (heavy, moderate, light, none) using different summary measures of smoking during pregnancy. If classification of smoking during pregnancy is based on typical number of cigarettes after learning of pregnancy, then the overall prevalence of smoking in the first trimester and the proportion of women in the heavy smoking category during that time are substantially under-estimated. In contrast, the prevalence of smoking in the third trimester and the proportion of women who are smoking heavily at that time are over-estimated by classifying women based on typical day after learning of pregnancy. Thus, in studies of the effects of fetal exposure to cigarettes in which particular trimester effects are hypothesized to be most relevant, classifying smokers by typical day after learning of pregnancy will lead to biased measures of the impact of smoking.
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DISCUSSION |
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An alternative interpretation of our data is that, if women repeatedly quit or reduce smoking and then relapse, they are, in fact, stable smokers. Our interpretation of the smoking patterns we observed as "fluctuations," rather than stability measured with error, derives from the potential significance of even temporary or subtle fluctuations in exposure to cigarette smoke for fetal growth and development. Variations in the timing of quitting or reduction of smoking have important implications for fetal growth,16–18 and evidence is accumulating to support subtle effects of smoking on intelligence quotient, child behavior, long-term health outcomes, etc.23,24 Given these facts, even minor fluctuations in smoking status or intensity may have profound effects, in which case it is the fluctuations that are of etiologic interest rather than long-term persistence or stability of smoking in pregnancy.
Our study has important implications for clinical and public health efforts to get women who smoke during pregnancy to quit or substantially reduce the amount they smoke. Although current clinical practice guidelines for treating tobacco use during pregnancy emphasize the need for extended and repeated screening and treatment,7 the most commonly used interventions are brief, didactic interventions (many using the "Ask, Advise, Assess, Assist, Arrange" model) at the first prenatal visit only. Some pregnant smokers receive even less treatment. Among the women who reported smoking during pregnancy in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement, 30% said they had never been advised to quit by a doctor. Brief clinical interventions are effective with a minority of women who do not spontaneously quit smoking when they learn they are pregnant; however, many women continue to smoke even when they receive these interventions.8 The results of our multivariable analyses suggest that low maternal education may be a barrier to successful quitting during pregnancy or at least be a useful risk marker of intractable smoking. Our data suggest that repeated screening and intervention over the course of pregnancy may be vital to helping women maintain any successful attempts to quit or cut down their smoking.
Our findings also have implications for researchers interested in the effects of fetal exposure to cigarette smoke. Misclassification of smoking status may not matter much for established consequences of fetal exposure to cigarette smoke, such as low birth weight; however, understanding variations in dosage, timing, and duration of fetal exposure to cigarette smoke may be critical to advancing research on subtle or long-term effects of maternal smoking during pregnancy. Measurement error is likely to prove a major methodological difficulty in conducting research in these areas. For example, if a woman quits smoking as soon as she learns she is pregnant, she may report being a nonsmoker during the entire pregnancy, truthfully according to her own perspective. She would be classified in most studies as a nonsmoker or quitter, yet her fetus would be at risk for any adverse outcomes associated with first-trimester exposure. The direction and magnitude of bias caused by the misclassification of smoking during pregnancy will depend on the magnitude of the true effect of exposure on the fetus as well as the degree of misclassification. Under most plausible scenarios, however, misclassification is likely to lead to an under-estimate of the impact of exposure on the fetus.
We conducted various simulations of the effects of misclassifying smoking in epidemiologic studies, using misclassification estimates from the Family Health and Development Project. In one scenario, we assumed that a true association exists between acute heavy exposure in the first trimester and an adverse fetal outcome. In a second scenario, we assumed a true association between chronic heavy exposure in the third trimester and an adverse outcome. Under both scenarios, we calculated the error in the estimated relative risk that would be induced if average number of cigarettes smoked per day after learning of pregnancy was used to classify women as heavy smokers or not. We also assumed that misclassification of exposure was nondifferential with respect to fetal outcome and that smoking was measured without error. In the first scenario, using average cigarettes per day after learning of pregnancy instead of peak exposure in the first trimester would underestimate a true relative risk of 2.00 by 14%, with relative risk estimated to be 1.71. If the true relative risk for the fetal outcome were 4.00, the bias would be a 55% under-estimate, with relative risk estimated as 1.8. In the second scenario, the exposure of interest was average exposure in the third trimester. Using typical day after learning of pregnancy would lead to only minor under-estimation (< 10%) of the true relative risks. Although we do not believe that misclassification will be problematic in studies in which smoking effects are substantial, studies of more subtle effects of exposure may be hampered by misclassification bias.
Although our samples provide consistent evidence of fluctuation in smoking during pregnancy, we note that our findings are based on women’s self-report of smoking. Biochemical validation of cigarette smoking, via assays of cotinine, a by-product of nicotine, is sometimes considered a "gold standard" measurement of smoking. In fact, cotinine levels do not provide a detailed history of exposure; instead, they indicate whether a woman did or did not smoke in the previous 30 hours.27 There is no standard method for mapping cigarettes per day to cotinine levels. As a result, if a woman’s smoking behavior truly fluctuates over time, then cotinine measures will be of limited or no use for validation. For example, a woman might truthfully report that she smoked heavily during the weekend but still have a low cotinine level if assayed midweek. Although self-report of cigarette smoking can be influenced by social desirability factors, the fact that women in both the Family Health and Development Project and the National Health Interview Survey 1991 Pregnancy and Smoking Supplement reported quit attempts and relapses, and ups and downs in amount smoked, suggests that they are not consistently conforming to social pressure to deny smoking. In addition, in the Family Health and Development Project, cotinine was measured once during each trimester to verify absolute smoking status, and nondisclosure rates were low, only 6% of women who reported not smoking had cotinine levels indicating otherwise; however, these cotinine values could not be used to validate women’s reports of month-to-month smoking. Some studies validating absolute smoking status (current smoking versus not) in pregnant women via cotinine measures report similarly low levels of nondisclosure.28,29 It is likely that the accuracy of self-report depends greatly on the context in which it occurs.
Another limitation of our study is that we were able to study changes in smoking status in the nationally representative National Health Interview Survey 1991 Pregnancy and Smoking Supplement but changes in smoking intensity only in the clinic-based Family Health and Development Project sample. Our finding of substantial fluctuation in number of cigarettes smoked throughout pregnancy needs to be confirmed. Smoking patterns in the National Health Interview Survey 1991 Pregnancy and Smoking Supplement reflect the prevalence and patterns of smoking during pregnancy in the late 1980s through 1991 and may have changed since that time; however, the prevalence of smoking during pregnancy during the intervening time period has not declined as much as smoking in the nonpregnant adult population.1 It is also likely that, as social pressures to quit or reduce smoking during pregnancy have increased during the same period, fluctuations in smoking may have increased, as tobacco-dependent women are pulled in opposite directions by behavioral norms and tobacco dependence. Possibly, our estimates of smoking fluctuations based on the National Health Interview Survey 1991 Pregnancy and Smoking Supplement are conservative; certainly our more recent data from the Family Health and Development Project sample confirm that variations in amount smoked throughout pregnancy are substantial in the early 2000s.
In conclusion, our data suggest that smoking during pregnancy fluctuates substantially within individual smokers. This fluctuation may be sufficient to render cross-sectional or average measures of smoking in pregnancy imprecise proxies for fetal exposure. The fluctuations we describe also suggest the need for repeated interventions to promote smoking cessation and harm reduction during pregnancy, targeted at women most likely to keep on trying to quit or reduce.
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Footnotes |
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The authors acknowledge the substantive contribution of Dr. Diane Lauderdale.
Received March 19, 2002. Received in revised form June 13, 2002. Accepted August 1, 2002.
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