The goal of this review is to summarize the epidemiologic evidence on maternal behaviors and preterm birth, evaluate the quality and strength of the evidence, and make specific recommendations regarding research methods that are likely to be productive in future studies. Epidemiologic research on the etiology of preterm birth has expanded considerably in the 15 years since the last comprehensive review.1 Although overviews and commentaries have appeared, including a recent report from the Institute of Medicine,2 to our knowledge there has been no comprehensive presentation and evaluation of the epidemiologic literature on behavioral risk factors for preterm birth since the early 1990s.
Clinicians and public health practitioners recognize that early delivery has a profound impact on infant morbidity and mortality.3 However, despite extensive investigation, we have made little progress in identifying modifiable behavioral causes of preterm birth. The risk of preterm birth appears to be rising modestly but steadily over time.4 Part of the increase is attributable to increased use of assisted reproductive technology leading to more multiple births (at notably higher risk of preterm delivery). Risks are also increasing among singleton births, in part due to medical intervention.5
The operational definition of preterm birth is birth prior to the completion of 37 weeks' gestation. However, gestational age estimates are subject to error, with varying reliance on last menstrual period dates, ultrasound at different times in gestation, and algorithms for combining information from the 2 sources. Multiple approaches have been used to subdivide preterm birth, including clinical presentation (preterm labor, preterm rupture of chorioamniotic membranes, medical indication for early delivery), etiologic pathway (eg, infection/inflammation, vascular compromise, presence of specific complications), and severity of prematurity (based on number of weeks' gestation). The proportion of studies considering subsets of preterm births appears to be increasing, yet with little consistency with regard to which subsets are considered and precisely how they are defined.
Etiologic influences may act at different times in relation to pregnancy: prior to the onset of pregnancy (through maternal genetic or lifestyle influences), early in pregnancy during placentation, and close to the time of delivery. Since behaviors often vary over time, judgment is required regarding the appropriate time(s) for measurement. Beyond the general concerns with accurate assessment of behaviors, there are special concerns with the potential for reverse causality if symptoms associated with future preterm delivery result in behavioral changes, or if previous adverse pregnancy outcomes affect behaviors in the subsequent pregnancies. Isolating specific behaviors from closely correlated ones is always a challenge in epidemiology, with socioeconomic deprivation strongly associated with an array of potentially harmful behaviors. Self-reported exposures are susceptible to response biases from social desirability, which may be particularly strong in relation to pregnancy and vulnerable to reporting biases when exposures are recalled after the outcome of pregnancy is known.
In contrast to the limited success in identifying strong behavioral influences on preterm birth, there are clear social patterns, with markedly increased risk among African-Americans compared with non-Hispanic Whites.4 Elevated risk is less consistently observed for other minorities in the United States, particularly Mexican-Americans,6,7 but generally found among Puerto Ricans and Filipinos.8 Women who are less educated or poorer often manifest elevated risk of preterm birth, though not with the same strength or consistency as is found for racial disparities.1,9 As increasing proportions of preterm birth are due to medical indications,5 which depend in part on intensity of medical care, women who have insufficient medical care may experience a lower risk of preterm birth due to induction, once other influences on risk are taken into account.
Several biologic markers of impending preterm birth have been identified that are predictive in the days or weeks before delivery. These are not true causes in the sense that manipulating the marker would not prevent the outcome, but they are informative and potentially useful in allowing clinical interventions to postpone delivery or to help prepare the fetus for postnatal life through the use of antenatal steroids.10 Fetal fibronectin has been shown to be highly predictive of impending very early preterm birth when measured at 22–24 weeks' gestation.11 Rises in corticotrophin-releasing hormone and cortisol also precede preterm birth.12
With the continued, accelerating pursuit of the behavioral causes of preterm birth through epidemiologic inquiry, it is timely to take stock and identify the more promising methods and risk factors that should be pursued, as well as those that have stagnated and appear to be unworthy of continued effort without fundamentally new approaches. Although social and biologic processes associated with behaviors are recognized, they have not been fully integrated into the epidemiologic studies thus far. Despite the logistical challenges of conducting randomized behavioral intervention trials, such research needs to be considered when the observational studies are sufficiently promising.
We conducted PubMed literature searches to locate all relevant articles. A highly sensitive search strategy was used to retrieve literature comprehensively back to 1992 (a 15-year period, approximately the date at which the previous comprehensive review1 left off) through January 2008. We used the following key words: “obstetric labor, premature”; “premature birth”; “infant, premature”; “pregnancy outcome”; “pregnancy complications”; “preterm”; “premature”; and “prematurity.” Similarly, a broad search strategy was used for each behavior of interest. For example, “smoking or smoker or smokers or tobacco” was used to retrieve all smoking literature. We then combined the outcome retrieval set with the behavior retrieval set using the Boolean AND operator. Retrieval was limited to English language articles. References were cross-checked for completeness using review articles. One of the authors (P.M.) reviewed each article for inclusion, the requirement being an assessment of a dichotomous outcome of preterm birth, rather than a continuous gestational age outcome. For topics in which the literature was sparse, we calculated relative risks from available data; otherwise, we omitted the few articles that did not provide relative risks.
The following key features of the methods and results were tabulated: geographic source of the population, study design, outcome definition(s), method of measurement of gestational age, exposure ascertainment methods, specific definition and timing of exposure, and the resulting risk ratio (RR) or odds ratio (OR) for each index of exposure with 95% confidence intervals (CIs). We considered preterm birth in the aggregate (all births <37 weeks' gestation) and subsets of preterm birth defined by clinical presentation, severity, complications, or maternal attributes (eg, parity), as information was available.
Within each behavioral category, the literature was first divided into groups with comparable reported outcomes, allowing some flexibility (eg, <37-week and <38-week endpoints were combined), exposure levels (eg, 1–9 cigarettes and 1–10 cigarettes), and reference levels (eg, no caffeine and <10 mg caffeine per day). Preterm births were subdivided based on severity and clinical presentation (spontaneous, medically indicated) where sufficient numbers of studies provided such information. After generating subgroups of literature based on shared outcome definitions and shared exposure assignment, for those with sufficient numbers of studies, we stratified by several methodologic features of the studies: method of gestational age assessment, prenatal or postpartum exposure assessment, clinic versus population source, and geographic location of study. Summary estimates were generated from subgroups containing at least 3 studies sharing these common measures. Estimates were calculated with both random effects and fixed effects methods using R software (www.r-project.org); results of random effects analysis are presented here. Individual studies that did not present 95% CIs for the relative risk estimates were excluded from summary estimates.
From the summary estimates, forest plot figures were generated to present the results. All tabulated studies are included in the eAppendix (http://links.lww.com/EDE/A371). In behavioral categories where the literature was too sparse to generate any summary estimates, the relevant literature is described in the text and the full list of identified articles has been included in the electronic appendix.
Tobacco is by far the most extensively evaluated behavior-related influence on preterm birth, with 58 relevant studies identified (eFigure 1, http://links.lww.com/EDE/A371). This literature allows for summary estimates to address dose-response gradients, some indicators of study quality, and potential effect-modifiers of the smoking/preterm birth relationship (Fig. 1).13–43 There is evidence of increased risk even in the lowest dose range (for >0–10 cigarettes per day, RR = 1.2 [95% CI = 1.1–1.3]) with a modest increase for the higher dose groups but still with summary ORs of <1.5 and imprecision in the highest dose ranges. Both medically indicated and spontaneous preterm births were associated with smoking, but the latter more strongly (relative risks of 1.5 vs. 1.2 for 10+ cigarettes per day). No meaningful differences were found for prenatal versus postpartum assessment, clinic versus population-based studies, or European versus North American studies. Method of gestational age assessment, grouped for simplicity into those that were and were not “cleaned” by considering information in addition to the date of the last menstrual period (LMP) (using ultrasound or birth-weight), showed no evidence for enhanced associations with refinement. Consideration of earlier preterm birth, <32 or <33 weeks' gestation, yielded somewhat stronger associations than were found for preterm births in the aggregate. Despite the precision resulting from the large number of studies, there is little variation in the summary estimates, ranging only from 1.0 to 1.5, so that “stronger” means only relative risks of ∼1.4–1.5 and “weaker” denotes relative risks of ∼1.1–1.2.
Smokeless tobacco has been evaluated to a very limited extent (eFigure 2, http://links.lww.com/EDE/A371) due to the relative rarity of exposure among women, at least in western countries. The 2 studies that addressed this issue found stronger associations with preterm birth than have been found for active smoking.35,44 Because smokeless tobacco exposes the women to nicotine but not the combustion products of tobacco, it seems unlikely that smokeless tobacco could be more harmful than smoking.
Environmental tobacco smoke exposure has been examined over the last 15 years, with 9 pertinent publications (eFigure 2). Exposure indicators vary widely across studies, including self-reported hours per day of exposure, number of smokers in the household, smoke exposure at work, and urinary or hair cotinine. In the aggregate, the studies suggest an association comparable in magnitude to that observed for active smoking—RRs of 1.2–1.4, with little impact of refinements to gestational age assessment and a slightly stronger association for population-based versus clinic-based studies (Fig. 2).21,29,43,45–50 The comparability of relative risks for active and passive smoking, despite markedly differing doses, raises questions about potential biases, perhaps confounding or publication bias.
Alcohol has been evaluated in 25 epidemiologic studies (eFigure 3, http://links.lww.com/EDE/A371), with most studies indicating no association with preterm birth (Fig. 3)14,16,17,22,39,42,51–65 The exposure categories vary markedly across studies, depending on the overall distribution of alcohol use in the study population. Comparing studies that provided relative risks for doses of >0–6 drinks per week and 7 or more drinks per week (less than daily vs. at least daily, on average) identified a modestly increased risk in the higher dose group. Otherwise, population source, timing of ascertainment, and study location all generated null findings for the association between alcohol and preterm birth.
There have been few studies of marijuana use and preterm birth (6 identified) (eFigure 4, http://links.lww.com/EDE/A371), generating imprecise evidence of a modest increase in risk of preterm birth (summary RR = 1.4 [0.8–2.3]).39,58,66–68 Studies of cocaine (eFigure 4) yielded slightly stronger associations based on self-report (summary RR = 1.8 [1.2–2.7] based on 7 studies)22,39,66,67,69–71 or urine screening (1.6 [0.9–2.6], based on 4 studies).66,71–73 Studies that identified cocaine use through self-report or urine screening were likely to isolate the heaviest users, with accompanying adverse social conditions and associated behaviors. Studies that used more sensitive biomarkers found little or no support for an association. Other drugs, including opiates and mixed drug use, yielded RR estimates around 2.0 (eFigure 4), with insufficient homogeneity in methods to generate summary estimates. Isolating the biologic effects of illicit drugs from their social and behavioral context poses a serious challenge, in addition to the potential for incomplete and selective identification of exposure based on suspicion followed by query or measurement of biomarkers, rather than systematic assessment of drug use among all women.74
The potential effect of caffeine on preterm birth has been examined in 9 studies (eFigure 5, http://links.lww.com/EDE/A371), all based on self-reported exposure. The absolute levels of caffeine that were considered vary depending on the study population's range, making it difficult to generate summary estimates that address absolute dose level (Fig. 4).14,15,48,58,75–79 There is no support for an adverse effect at lower doses and some suggestion of an increased risk associated with 3 or more cups of coffee per day (RR = 1.2 [1.0–1.5]) as well as among the studies based on clinic populations (RR = 1.2 [1.0–1.4]). Overall, these studies offer very little support for an association between caffeine and preterm birth.
Although several studies of leisure time physical activity (6 identified) suggest a fairly strong reduction in risk of preterm birth (eFigure 6, http://links.lww.com/EDE/A371), it is difficult to combine results across studies given the markedly differing definitions of “physically active.” Nonetheless, the summary relative risk is very close to the null (RR = 0.9 [0.7–1.1]) (Fig. 5)80–83 and driven closer to the null due to one large, negative study.82 Isolating direct effects of the physical activity from the social conditions that create the opportunity to be active (having leisure time, having access to places for exercise) and the behavioral determinants (being free of medical contraindications, feeling motivated to exercise) is challenging in observational studies.
Only 3 studies were identified that evaluated sex ual activity in relation to preterm birth (eFigure 7, http://links.lww.com/EDE/A371) with divergent findings. One reported a strong positive association,84 one a strong inverse association,85 and one with results close to the null.86 Isolating sexual behavior from the determinants of sexual behavior, as would be done in a hypothetical randomized trial, is very difficult, given that sustained sexual activity requires the presence of a partner, absence of medical contraindications, and the desire to engage in this behavior, all of which may be associated with preterm birth through other pathways.
A sizable number of studies (27 identified) (eFigure 8, http://links.lww.com/EDE/A371) have evaluated the relationship between employment (vs. unemployment) and many aspects of work in relation to the risk of preterm birth. Employment per se was not associated with preterm birth, with slightly increased risks in studies with more refined gestational age assessment and those with prenatal assessment (Fig. 5).18,48,57,87–108 Focusing on specific aspects of work, we found little indication that jobs involving standing, lifting, or shift work were associated with preterm birth, whereas those requiring night work (RR = 1.3 [0.8–2.2]) and physically strenuous work (RR = 1.3 [1.1–1.6]) were weakly associated with increased risk.
The volume of epidemiologic research on behavioral influences on preterm birth is substantial, but shows little progress in reaching firm conclusions regarding causal effects. Tobacco smoking is consistently associated with a modest increased risk of preterm birth, and it appears that the association is stronger for higher number of cigarettes per day and earlier preterm birth, consistent with a causal interpretation. Environmental tobacco smoke, though studied less extensively, tends to yield associations of a similar magnitude despite the markedly lower exposure levels than for active smoking; these results are thus of questionable etiologic significance. A range of addictive behaviors, notably higher levels of alcohol, cocaine, and other illicit drugs (behaviors that are among the least socially acceptable), appear to be associated with preterm birth. Two plausible explanations are that a range of pharmacologically active agents are all capable of causing preterm birth or that all these associations are confounded by behaviors correlated with the use of these substances (poor nutrition, sexually transmitted infections) or by adverse socioeconomic conditions more generally. Studies that measure a range of exposures with accuracy, a major challenge for stigmatized behaviors, and that consider not just the agent of interest but the most plausible confounders, would help to isolate any independent causal influence of these behaviors. By contrast, caffeine appears to be unrelated to preterm birth.
Some (but not all) studies of recreational physical activity have suggested a substantially reduced risk of preterm birth, plausibly related to a direct physiological effect as well as to confounding by the social circumstances that promote physical activity and other favorable health behaviors that may accompany it. A more careful evaluation of the underlying proclivity and opportunity for physical activity is essential to allow observational studies to come closer to simulating a randomized trial. Measurement of activity is notoriously difficult and requires some form of objective assessment in addition to self-report.
Employment and preterm birth show only sporadic associations, with the most support for an association between jobs requiring physical exertion or night work and increased risk of preterm birth. Even though work-related physical demands point in the opposite direction as recreational physical activity, the same possibilities remain: an adverse physiologic effect or confounding by the social and behavioral correlates of holding physically demanding jobs.
The constellation of findings and the failure to show much progress with the marked expansion in the volume of research in the last 15 years calls for a radical rethinking of the value of further research on the etiologic influence of these behaviors on preterm birth. Had the large number of reasonably well-designed observational studies yielded a strong signal, a case could be made for proceeding with large behavioral intervention trials. However, except for the modest impact of smoking (with the attributable fraction lower than in the past, due to the success in smoking cessation efforts), no strong signal has been found. For every one of the more promising directions, additional studies of similar quality using traditional methods will yield only small increments to the collective picture, with a slightly narrower confidence interval on the summary estimate. Instead, we need to tackle the real limiting factors: (1) the antecedents of the behaviors, (2) the measurement of the behaviors, (3) and the biologic events that result from the behaviors.
To address the causal impact of the behaviors of concern, we need a better understanding of the social context and determinants of those behaviors. This applies to stigmatized behaviors such as cocaine use or heavy alcohol consumption, to health-motivated behaviors such as recreational physical activity, and to the life circumstances that result in jobs with varying physical demands. To the extent that we must rely on observational studies, those studies need to approximate randomized trials in attempting to isolate the individuals whose self-assignment to exposure groups is sufficiently free of major confounding to contribute to causal inference. As illustrated so dramatically by our inability to isolate postmenopausal estrogen use from associated risks for cardiovascular disease, this is a major challenge but one that can be addressed. Where the social disparities associated with the behavior are profound, (eg, cocaine use, physically demanding jobs), there is a need to restrict the study population to women who are broadly comparable in education and income. Where the medical course of the pregnancy may affect engagement in the behavior, (eg, contraindications to physical activity or continued sexual activity), those women must be excluded to generate a more valid estimate of the independent, causal effect of the behavior. Conventional approaches to measuring and adjusting for confounders are pertinent, but a more systematic, careful dissection of the proclivity to engage in the behavior should be undertaken, isolating those who faced a more random choice or at least one that is free of profound distortion by other obvious determinants of preterm birth. Propensity scores109 may be useful in refining the estimate of the causal impact, but the setting and structure of the study need to be selected with this problem in mind. Measuring these sources of confounding and demonstrating the impact of their removal through restriction or control would enhance our confidence in the causal relevance of what remains.
Past research clearly shows that even sophisticated approaches to the study of behaviors and preterm birth do not yield strong or consistent evidence of associations. These approaches include carefully designed interviews and standardized instruments, with appropriate attention to data quality. Within the range of available studies, there is little basis for confidence that modest refinements (more carefully worded questions, better-trained interviewers) would yield much benefit. It is of course possible that there truly is no impact of the behavior on preterm birth, but there is such extensive opportunity for measurement error for these behaviors (eg, caffeine, alcohol, physical activity, work demands) that it remains possible that the measured relative risks of 1.0 to 1.5 would be substantially higher if misclassification were markedly reduced. Where suitable technologies exist, such as monitoring of physical activity or biomarkers reflective of exposures over the time course of interest, new studies will at minimum yield informative findings that can shape our understanding of the causal impact of the behavior and thus encourage or discourage further investigation. While refinements to questionnaire-based methods could in theory yield radically different exposure assignment, the more likely direction is in qualitatively different technologies, such as hair nicotine or cocaine metabolites or prospectively applied instruments to measure physical activity. Perinatal epidemiologists need to watch for breakthroughs in exposure measurement that could move the field forward.
The lack of biologic specificity inherent in the clinical entity of preterm birth is well appreciated,2 with subsets of cases resulting from different etiologic pathways even though the specific pathways have yet to be clearly defined. Moreover, the appropriate axes for division may have to be addressed on an exposure-by-exposure basis, ie, the subset of cases plausibly affected by tobacco or by alcohol. This might be manifested either by a subset of preterm births that are more strongly associated with the exposure or with an effect-measure modifier defining a group in which the impact of the exposure is enhanced. The literature provides some clues, suggesting, for example, a greater impact of smoking on earlier preterm birth and spontaneous as compared with medically indicated preterm birth. Where feasible, division of cases along those conventional lines is encouraged, although doing so requires very large studies.
A more promising avenue for elucidating the potential causal impact of behaviors on preterm birth is through evaluation of near-term biologic consequences that affect the pathways thought to contribute to preterm birth. While the mechanisms resulting in preterm birth are incompletely understood, there is a strong justification to focus on a subset of biologic responses that are most likely to be relevant, including inflammation, vascular compromise, and neuroendocrine changes. In each of those pathways (and other suspected ones, including oxidative stress and hypoxia), there are biologic markers of response that could help to strengthen and clarify the link between behaviors and clinical outcomes. For example, a great deal is known about the impact of physical activity on cardiovascular health in the nonpregnant state. These markers of effect through lipid profile, blood pressure, and inflammatory markers are pertinent to pregnancy as well. It would be feasible to carry out observational studies that monitor physical activity over shorter periods of time (and thus permit precise assessment of activity), combined with short-term biologic response in the form of altered inflammatory markers or lipids.
The feasibility of randomized trials requires postulating the relevant impact of the behavior of concern, being able to manipulate the behavior (which can be a major logistical or ethical challenge), and examining the near-term biologic consequences. It would be daunting to modify behavior throughout pregnancy to assess impact on clinical outcomes such as preterm birth, whereas short-term manipulation of behavior to study proximal biologic changes is not out of reach. While such evidence constitutes only one link in the chain from behavior to preterm birth, the tightness of the question and clarity of the answer would help to encourage or discourage further efforts. Such results could also help to pinpoint the subset of preterm births most deserving of attention in relation to the behavior.
For many of the behaviors of concern, conventional epidemiologic approaches have been applied with little in the way of conclusive data other than the small effect of smoking on preterm birth. The absence of clear associations for other intensively studied behaviors offers some guidance for clinical and public health application, but they do little to help in designing more ambitious efforts to prevent preterm birth. Prevention requires identification of clear etiologic relationships, and reaching that level of certainty calls for a markedly different approach to the examination of the antecedents of the behaviors of interest, novel approaches to assessment, and examination of near-term biologic consequences of the behaviors of concern, focusing on pathways thought to result in preterm birth.
We thank Stephanie Engel and Anna Maria Siega-Riz for their helpful review of an earlier draft.
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