Tobacco smoking during pregnancy remains perhaps the most important modifiable influence on adverse pregnancy outcome. Smoking during pregnancy results in restricted fetal growth, with approximately a 200-gm reduction in average birth weight for heavy smokers. 1–3 In addition, smoking has been reported to result in a modest increased risk in preterm birth among smokers, with relative risks on the order of 1.2 to 1.6. 4,5 Although adverse pregnancy outcomes are more common among African-Americans than among whites, 6 smoking during pregnancy is generally less frequent among African-Americans, as has been found in North Carolina. 7,8
Given the evidence of overall lower smoking during pregnancy among African-Americans, further evaluation of their patterns of use in regard to dose, brand, and modifications of use during pregnancy is of interest. There is some evidence that metabolism of nicotine differs by race, 9,10 generating higher cotinine levels for a given amount of smoking among African-Americans, which could cause the dose-response relation of smoking and pregnancy outcome among African-Americans and whites to differ. African-American smokers tend to prefer mentholated cigarettes, 11–13 which have distinctive chemical constituents, with more than half of African-American smokers preferring such brands vs approximately one-quarter of white smokers. 11,12 Furthermore, the suggestion of behavioral differences in how the cigarette is smoked by African-Americans and whites also encourages examination of tobacco-related risks among racial groups. 13–15 Data collected for the Pregnancy, Infection, and Nutrition Study allow such an evaluation, with detailed information on tobacco use obtained in a large population of African-American and white women.
Subjects and Methods
We conducted the Pregnancy, Infection, and Nutrition Study at prenatal care clinics affiliated with University of North Carolina Hospitals and at Wake County Human Services and the Wake Area Health Education Center. As described in detail elsewhere, 16 we recruited women for a prospective cohort study, with enrollment at 24–29 weeks’ gestation. We asked women to provide blood, urine, and genital tract specimens and participate in a telephone interview in the subsequent 2 weeks to collect information on a number of potential determinants of preterm birth, including education and income; use of tobacco, alcohol, and illicit drugs; symptoms of infection during pregnancy; physical exertion; and employment. Given the clinic locations, patients resided in Raleigh, Durham, Chapel Hill, Burlington, and surrounding smaller communities in central North Carolina.
Recruitment began in August 1995, and the analyses presented here include women whose last menstrual periods (LMPs) were between January 31, 1995 and October 26, 1999. During that period, we identified 5,011 women as eligible, having come to the participating clinic before 30 weeks’ gestation, with a singleton pregnancy, access to a telephone, able to communicate in English, and planning to continue care and deliver at a study hospital. Among those eligible, we recruited 3,029 (60%), defined as willing to provide genital tract specimens; approximately 29% were lost as a result of patient refusal, 5% because of inability to make contact at the time of the clinic visit, 5% because of physician refusal, and 1% for other reasons. Among the recruited women, 2,752 (91%) completed the telephone interview with a mean gestational age of 26 weeks at the time of interview, and 127 were excluded from this analysis because of missing or implausible smoking information. This analysis was limited to women who reported race as African-American or white, resulting in the exclusion of 169 women who reported other races. Of the remaining 2,456 women, 309 (13%) delivered before completing 37 weeks’ gestation, 2,109 (86%) delivered at term, and 38 (<2%) were lost to follow-up before delivery status could be determined, leaving 2,418 for analysis. We analyzed patterns of participation in detail 16 and found that those recruited were generally similar to those eligible, particularly with respect to risk of adverse pregnancy outcome.
We obtained detailed information about tobacco use in the telephone interview. We asked women to report for each month of pregnancy the exact brand of cigarette they smoked most often and the number of cigarettes smoked per day. To specify the brand in sufficient detail to classify it according to the Federal Trade Commission report on tar, nicotine, and carbon monoxide for domestic cigarettes, 17 we asked about the cigarette brand, length of the cigarette, and whether it was menthol or nonmenthol and in a hard or soft pack. From this information, we derived a month-by-month index of smoking behavior starting with the month before the woman became pregnant and continuing through the date of interview. With the Federal Trade Commission report, 17 we were able to calculate average exposure to tar, nicotine, and carbon monoxide on a daily basis for each woman who smoked. As found by others, 18 the measures of intensity of smoking were very highly correlated. During months 1–6 of pregnancy, the number of cigarettes per day had a Pearson correlation coefficient of 0.95 with total nicotine per day and 0.97 with total carbon monoxide per day. Nicotine and carbon monoxide had a correlation of 0.99 with one another. Thus, we only present data on total number of cigarettes rather than nicotine or carbon monoxide.
We re-interviewed preterm cases and a randomly selected sample of the cohort after delivery. We examined smoking behavior from the time of interview to the end of pregnancy among those women and found that smoking behavior changed so little subsequent to the interview during pregnancy that we conducted the analysis on the entire cohort and analyzed smoking behavior during the first 6 months of pregnancy only. The correlation coefficients between number of cigarettes smoked per day in months 1–3, 4–6, 1–6, 6, 7, and 8 (the last three restricted to preterm cases and controls who were re-interviewed) ranged from 0.79 to 0.98, effectively precluding analyses to examine the effects of smoking in specific time windows of pregnancy. The time window chosen for analysis, months 1–6, had correlation coefficients of 0.85 to 0.98 with cigarettes per day in the other intervals.
Urine was collected for all women at the clinic visit in which women were recruited, between 24 and 29 weeks’ gestation and again shortly after delivery for preterm cases and a random sample of the cohort who constituted the controls. Assays of cotinine were conducted for all available preterm cases and controls, and a selected number of other women in the cohort who had been designated for special interest because of participation in another study. Urine samples were analyzed using immunoassay kits from STC Technologies (Portage, MI), with results in the form of dichotomous findings of >50 or >500 ng/ml. We were thus able to group the women into categories of <50, 50–<500, and 500+ ng/ml.
We compared lifetime never-smokers with women who smoked but not during pregnancy and with women who smoked during pregnancy. Because the number of never-smokers was sufficient to form a stable reference category, and there is some possibility of former smokers misrepresenting their current smoking status (denying smoking during pregnancy), “never-smokers” constituted the reference group for the analyses. We examined risk of preterm and small-for-gestational-age (SGA) births in relation to the number of cigarettes smoked per day (1–9, 10–19, 20+), menthol/nonmenthol brand, and cotinine at 24–29 weeks’ gestation and postpartum.
We estimated gestational age on the basis of an algorithm that combined LMP with ultrasound dating. If both were available and the two agreed within 14 days, we used LMP to assign gestational age, whereas if the disparity was more than 14 days, we relied on ultrasound. If a reliable LMP date was not available, we used the earliest available ultrasound. For this cohort, 79% of women had both LMP dates and ultrasound, 12% ultrasound only, and 9% LMP only. Most of the ultrasounds were taken before the 20th week of gestation (89%). When both were available, we assigned gestational age on the basis of LMP in 86% and ultrasound in 14%. We defined preterm birth as delivery before the completion of 37 weeks’ gestation, subdivided on the basis of severity (<37 weeks and <34 weeks) and on clinical presentation as interpreted by study obstetricians [preterm labor, preterm premature rupture of amniotic membranes (PROM) with membrane rupture 4 or more hours before onset of labor, and medically indicated]. We measured fetal growth restriction by identifying those infants below the 10th percentile of birth weight for gestational age, race, gender, and parity, using national norms. 19
We examined indices of tobacco exposure in relation to birth outcomes by calculating crude and adjusted risk ratios for the full cohort and odds ratios for the nested case-control sample. We derived adjusted risk ratios by log-linear modeling, with adjustment as needed for confounding factors. We began with a list of known and suspected determinants of pregnancy outcome, including clinic site (Wake County institutions, or University of North Carolina Hospital), race, marital status, maternal age, height, prepregnancy body mass index, education, poverty status, parity, bacterial vaginosis, alcohol use, and illicit drug use. By first conducting log linear analyses with each potential confounder in the model for preterm or SGA outcomes, we examined only those factors associated with risk ratios of <0.8 or >1.2. For those variables, we adjusted as needed for individual covariates that changed the association between the smoking measure and pregnancy outcome by 10% or more. Variables included in the analysis using that criterion are noted in the table footnotes. We also conducted race-specific analyses of African-Americans and whites.
Results
Among the 2,418 women in the study with smoking and pregnancy outcome data, 1,487 (62%) never smoked, 252 (10%) smoked before but not during pregnancy, and 679 (28%) smoked at some time during the pregnancy. Among the women who smoked at some time during months 1–6 of pregnancy, light smokers predominated, with 390 (57% of smokers) smoking fewer than 10 cigarettes per day, 199 (29% of smokers) smoking 10–19 cigarettes per day, and only 90 (13% of smokers) smoking 20 or more cigarettes per day. Heavy smoking was even rarer among African-American than among white smokers, with 1% and 12% of smokers, respectively, smoking 20 or more cigarettes per day. Thus, smoking was common among women in this cohort, but heavy smoking was rare. Brand preference for menthol and nonmenthol was nearly evenly divided among all women in the cohort who smoked (47% menthol and 53% nonmenthol), but notably uneven by race. Among African-American smokers, 95% smoked menthol cigarettes, whereas among white women, 26% smoked menthols.
Smoking before pregnancy was not related to preterm or SGA births (Table 1). Smoking during pregnancy showed small and inconsistent associations with preterm birth, with limited evidence for a dose-response gradient. Only the postpartum cotinine measure suggested that women with the highest levels were at increased risk for preterm birth. In contrast, risk of fetal growth restriction was much more strongly and consistently associated with indices of tobacco use, with a positive dose-response gradient and relative risks of 1.6–2.4 in the highest exposure categories.
;)
Table 1: Adjusted Relative Risks (RR) for Preterm Birth and Small for Gestational Age (SGA) Births in Relation to Smoking in Months 1–6 of Pregnancy: Pregnancy, Infection, and Nutrition Study, 1995–1999
Stratification by race (Table 2) suggested somewhat stronger associations, overall, for whites compared with African-Americans, but the statistical support for such an interaction was limited on the basis of comparing models with and without dose by race interaction terms. Among white women, smoking during pregnancy was weakly related to preterm birth but without evidence for a dose-response gradient. The magnitude of association with fetal growth restriction was substantial, reaching a risk ratio of 2.9 (95% confidence interval = 1.6–5.2) in the highest category. Further stratification of white smokers by menthol/nonmenthol brand preference resulted in limited study size, but gave some indication of stronger associations among nonmenthol smokers. Too few African-Americans smoked nonmenthol cigarettes for us to examine associations with pregnancy outcome. High levels of cotinine were associated with preterm birth among both whites and African-Americans, more strongly for the postpartum than the 24–29-week urine measure. African-Americans were notably lighter smokers than whites on average, with too few for us to analyze risks associated with 20 or more cigarettes per day. Strength and consistency of association between indicators of smoking and preterm birth as well as SGA births appeared to be similar for African-Americans as for whites, once the lower doses among African-Americans were taken into account.
Table 2: Adjusted Relative Risks for Preterm Birth and Small-for-Gestational-Age (SGA) Births in Relation to Smoking in Months 1–6 of Pregnancy
Division of preterm birth by clinical presentation into idiopathic preterm labor (N = 94, 34% of preterm births), preterm PROM (N = 50, 18% of preterm births), and medical indication (N = 112, 40% of preterm births) (Table 3) yielded a clear suggestion of stronger associations for preterm PROM, despite imprecision. Both self-reported quantity and cotinine measures yielded the strongest associations with preterm PROM. Only the postpartum cotinine measure was associated to any extent with preterm birth because of preterm labor or medical indications.
Table 3: Relative Risks (RR) for Preterm Birth Subtypes in Relation to Smoking in Months 1–6 of Pregnancy
Discussion
The results of this study support the generally accepted notion that smoking is weakly associated with preterm birth, although unevenly across measures of tobacco use and without clear dose-response gradients. This finding is consistent with a number of other studies. 20–32 Some reports, however, suggest that a stronger association is present, 33–35 and others suggest no association at all. 36–40 Given random error and some evidence that the impact of smoking may vary in relation to maternal age, 22 caffeine consumption, 30 body weight, 31 and parity, 32 results would be expected to differ on the basis of the composition of the population under study. The literature suggests relative risks of around 1.2–1.5 for smoking 10–20 cigarettes per day and a relative risk of 1.5–2.0 for 20 or more cigarettes per day, with our study findings at the lower end of that range. Some studies suggest that there is substantial confounding of the smoking-preterm birth association, 41 but there was minimal confounding identified in our data, and the scarcity of other strong risk factors for preterm birth makes it unlikely that adjustment would have a major impact on the results.
The evaluation of preterm birth subtypes defined by clinical presentation offered a clear suggestion of a stronger association for preterm birth due to preterm PROM. This pattern has been reported in other studies, 42,43 although the differential by clinical presentation was less striking than what we found. Results for preterm labor have been mixed, with some indication of a fairly strong association 35 and other evidence consistent with our lack of association. 29 The value and feasibility of separating preterm birth by subtype is uncertain, 44 such that failure to find differences in risk may not be important. When such differences are found, however, only random error or some causal pattern could explain it.
The notably stronger association we observed between smoking and fetal growth restriction as compared with preterm birth is also consistent with prior literature. Relative risks on the order of 1.5–3.0 have been found by most other investigators who have examined the issue, with clear dose-response gradients in relation to the amount smoked. 22,27,29,31,38,39,45–49 The many studies of low birth weight show results that are similar to those for measures of fetal growth restriction 20,26,28,39,50 but represent some blending of reduced fetal growth and early deliveries.
Most studies that have considered smoking in detail have addressed the number of cigarettes smoked per day as a measure of dose, with consistent evidence for a dose-response gradient for both preterm birth and fetal growth restriction. Given that women smokers in particular are often light smokers, tobacco use should not be analyzed as “present” or “absent” in relation to pregnancy outcome, but rather divided at least into nonsmokers, light smokers, and heavy smokers. Efforts to estimate dose of the hypothesized toxic constituents of tobacco smoke in relation to pregnancy outcome to refine the exposure measure have been limited. Secker-Walker et al51 examined exhaled carbon monoxide measured at the first prenatal care visit and found that the gradient in risk of low birth weight deliveries was quite similar for number of cigarettes per day as for measured carbon monoxide level. The measures of association between cotinine assay results and pregnancy outcome in our study tended to be stronger than those based on self-reported smoking, despite the short time period reflected by the biological measures. Cotinine measured after delivery was more strongly associated with adverse outcome than was smoking at the clinic visit at 24–29 weeks’ gestation. Given that the former is outside the time window for etiology, this pattern is surprising. Perhaps those women who managed to maintain their cotinine levels through the period before, during, and shortly after delivery (by going outside the hospital to smoke) were the most addicted, heaviest smokers in the earlier periods as well.
The primary racial differences we observed reflect the differing smoking patterns of African-American compared with white women, not indicating that a given tobacco dose results in differential effects across racial groups. Beyond the number of cigarettes per day, some account must be taken of the differing brand preferences, with African-American women strongly preferring menthol cigarettes. Because of the virtual absence of high-dose or nonmenthol African-American smokers, our ability to address effect modification of smoking effects by race was limited. The Alameda County study of low birth weight also found similar relative risks in white and black smokers. 52 In a study of low-income North Carolina women, smoking was related to risk of low birth weight in both groups, but the associations were stronger among whites compared with blacks at each dose level. 7 In a study of births at Yale-New Haven Hospital, the risk of SGA births was 2.0 for whites who smoked and 1.5 for blacks who smoked, compared with their nonsmoking counterparts. 27 Corresponding race-specific relative risks for smoking in a population in Los Angeles were 2.5 and 2.2 for African-Americans and whites, respectively. 53 A recent report from Atlanta indicated rather striking differences in dose-specific relative risks of fetal growth restriction by race, with adjusted relative risks of 3.8 and 2.4 for white and African-American smokers of less than one pack per day, and 4.9 and 2.5 for smokers of 1–2 packs per day, respectively. 46 Although one early report suggested stronger effects of smoking in blacks compared with whites, 54 nearly all the subsequent studies point in the opposite direction, providing rather consistent evidence that African-American smokers experience less of an increased risk from smoking than whites.
Beyond the limitations in precision and ability to identify subtypes of preterm births already noted, the challenge of accurately estimating gestational age must also be considered in the interpretation of results. Errors in assignment would affect both preterm birth and fetal growth restriction. Despite using the best available clinical data in a consistent manner, errors in gestational age assessment are almost certain to be present. 55,56 To the extent that those errors result from confusion about the date of the LMP or from erroneous reporting, the potential for those factors to be related to smoking must be considered. Accuracy of reported smoking may also be questioned, with perhaps a modest incentive to misrepresent smoking habits because of social pressure or errors in recall. We examined urinary cotinine on a sample of women in the study and found sizable correlations (0.6–0.7) with number of cigarettes smoked per day, confirming the overall accuracy of self-report. When we compared self-reported smoking with assay results, only 5 of the 301 self-reported nonsmokers (<2%) tested positive for cotinine at delivery.
The selectivity of our population tempers generalization of our findings, particularly given that we had a population of relatively high-risk white women and relatively low-risk African-American women. The choice of clinics helped to define racial groups of similar risk, and we recruited African-American women somewhat less successfully than white women. 16 Nonetheless, among eligible women who did not enroll, racial differences were similar to those for women who did enroll, with relative risks on the order of 1.3 for African-Americans compared with whites among women who did and did not enroll. Extrapolation of our findings to broader populations is a matter of judgment and depends on the distribution of social, behavioral, and medical factors that affect pregnancy outcome and may well affect vulnerability to tobacco.
Our results confirm the well-established effect of tobacco smoking during pregnancy on fetal growth and very small effect on preterm birth. The incremental value of biomarkers of exposure was demonstrated, despite the short time period that they reflect. Although the evidence suggests similar effects for a given tobacco dose among African-Americans and whites, in light of the notably lower prevalence and dose of smoking among African-Americans, tobacco use clearly does not contribute to the excess risk of adverse pregnancy outcomes among African-American women compared with whites, and may well tend to reduce the magnitude of the racial differences in adverse pregnancy outcomes.
We thank the project manager, Jude F. Williams, and the clinic site coordinators, Barbara Eucker and Anne Carter. We also thank the staffs of the obstetrics clinics, particularly Peter Morris, Ida Dawson, Cathi Weatherly-Jones, Juan Granados, Thad McDonald, and Sara Caviness, and the many obstetrical care providers in these clinics who assisted in the collection of specimens.
References
1. Butler NR, Goldstein H, Ross EM. Cigarette
smoking in
pregnancy: its influence on birth weight and perinatal mortality. Br Med J 1972; 2: 127–130.
2. Landesman-Dwyer S, Emanuel I.
Smoking during
pregnancy. Teratology 1980; 19: 119–126.
3. Institute of Medicine. Preventing Low Birth Weight. Committee to Study the Prevention of Low Birth Weight. Washington, DC: National Academy Press, 1985.
4. Savitz DA, Pastore LM. Causes of prematurity. In: McCormick MC, Siegel JE, eds. Prenatal Care: Effectiveness and Implementation. Cambridge, UK: Cambridge University Press, 1999; 63–104.
5. Berkowitz GS, Papiernik E. Epidemiology of preterm birth. Epidemiol Rev 1993; 15: 414–443.
6. Shiono PH, Klebanoff MA. Ethnic differences in preterm and very preterm delivery. Am J Public Health 1986; 76: 1317–1321.
7. Barnett E. Race differences in the impact of maternal cigarette
smoking on infant birth weight. CHES Studies. A Special Report Series by the State Center for Health and Environmental Statistics, No. 79. Raleigh: North Carolina Department of Environment, Health, and Natural Resources, 1994.
8. Buescher PA.
Smoking in
pregnancy in North Carolina. NC Med J 1997; 58: 356–360.
9. Caraballo RS, Giovino GA, Pechacek TF, Mowery PD, Richter PA, Strauss WJ, Sharp DJ, Eriksen MP, Pirkle JL, Maurer KR. Racial and ethnic differences in serum cotinine levels of cigarette smokers: Third National Health and Nutrition Examination Survey, 1988–1991. JAMA 1998: 280: 135–139.
10. Pérez-Stable EJ, Herrera B, Jacob P III, Benowitz NL. Nicotine metabolism and intake in black and white smokers. JAMA 1998; 280: 152–156.
11. Sidney S, Tekawa I, Friedman GD. Mentholated cigarette use among multiphasic examinees, 1979–86. Am J Public Health 1989; 79: 1415–1416.
12. Kabat GC, Morabia A, Wynder EL. Comparison of
smoking habits of blacks and whites in a case-control study. Am J Public Health 1991; 81: 1483–1486.
13. Ahijevych K, Wewers ME. Factors associated with nicotine dependence among African American women cigarette smokers. Res Nurs Health 1993; 16: 283–292.
14. Caskey NH, Jarvik ME, McCarthy WJ, Rosenblatt MR, Gross TM, Carpenter CL. Rapid
smoking of menthol and nonmenthol cigarettes by black and white smokers. Pharmacol Biochem Behav 1993; 46: 259–263.
15. Ahijevych K, Parsley LA. Smoke constituent exposure and stage of change in black and white women cigarette smokers. Addict Behav 1999; 24: 115–120.
16. Savitz DA, Dole N, Williams J, Thorp JM, McDonald T, Carter AC, Eucker B. Study design and determinants of participation in an epidemiologic study of preterm delivery. Paediatr Perinat Epidemiol 1999; 13: 114–125.
17. Federal Trade Commission. Report of “tar,” nicotine, and carbon monoxide of the smoke of 1249 varieties of domestic cigarettes for the year 1995 (online). Available:
http://www.ftc.gov/opa/1998/9801/tandn97-2.htm (January 15, 1998).
18. Anderson HR, Bland JM, Peacock JL. The effects of
smoking on fetal growth: evidence for a threshold, the importance of brand of cigarette, and interaction with alcohol and caffeine consumption. In: Poswillo D, Alberman E, eds. Effects of
Smoking on the Fetus, Neonate, and Child. Oxford, UK: Oxford University Press, 1992; 89–107.
19. Zhang J, Bowes WA Jr. Birth-weight-for-gestational-age patterns by race, sex, and parity in the United States population. Obstet Gynecol 1995; 86: 200–208.
20. Meyer MB, Jonas BS, Tonascia JA. Perinatal events associated with maternal
smoking during
pregnancy. Am J Epidemiol 1976; 103: 464–476.
21. Shiono PH, Kiebanoff MA, Rhoads GG.
Smoking and drinking during
pregnancy. JAMA 1986; 255: 82–84.
22. Wen SW, Goldenberg RL, Cutter GR, Hoffman JJ, Cliver SP, Davis RO, Dubard MB.
Smoking, maternal age, fetal growth, and gestational age at delivery. Am J Obstet Gynecol 1990; 162: 53–58.
23. De Hass I, Harlow BL, Cramer DW, Frigoletto FD. Spontaneous preterm birth: a case-control study. Am J Obstet Gynecol 1991; 165: 1290–1296.
24. Kramer MS, McLean FH, Eason EL, Usher RH. Maternal nutrition and spontaneous preterm birth. Am J Epidemiol 1992; 136: 574–583.
25. McDonald AD, Armstrong BG, Sloan M. Cigarette, alcohol, and coffee consumption and prematurity. Am J Public Health 1992; 82: 87–90.
26. Li CQ, Windsor RA, Perkins L, Goldenberg RL, Lowe JB. The impact on infant birth weight and gestational age of cotinine-validated
smoking reduction during
pregnancy. JAMA 1993; 269: 1519–1524.
27. Zhang H, Bracken MB. Tree-based risk factor analysis of preterm delivery and small-for-gestational-age birth. Am J Epidemiol 1995; 141: 70–78.
28. Eskenazi B, Prehn AW, Christianson RE. Passive and active maternal
smoking as measured by serum cotinine: the effect on birthweight. Am J Public Health 1995; 85: 395–398.
29. Lang JM, Lieberman E, Cohen A. A comparison of risk factors for preterm labor and term small-for-gestational-age birth. Epidemiology 1996; 7: 369–376.
30. Wisborg K, Henriksen TB, Hedegaard M, Secher NJ.
Smoking during
pregnancy and preterm birth. Br J Obstet Gynaecol 1996; 103: 800–805.
31. Hellerstedt WL, Himes JH, Story M, Edwards LE. The effects of cigarette
smoking and gestational weight change on birth outcomes in obese and normal-weight women. Am J Public Health 1997; 87: 591–596.
32. Cnattingius S, Granath F, Petersson G, Harlow BL. The influence of gestational age and
smoking habits on the risk of subsequent preterm deliveries. N Engl J Med 1999; 341: 943–948.
33. Fedrick J, Anderson ABM. Factors associated with spontaneous pre-term birth. Br J Obstet Gynaecol 1976; 83: 342–350.
34. Hartikainen-Sorri A, Sorri M. Occupational and socio-medical factors in preterm birth. Obstet Gynecol 1989; 74: 13–16.
35. Heffner LJ, Sherman CB, Speizer FE, Weiss ST. Clinical and environmental predictors of preterm labor. Obstet Gynecol 1993; 81: 750–757.
36. Berkowitz GS. An epidemiologic study of preterm delivery. Am J Epidemiol 1981; 113: 81–92.
37. Abrams B, Newman V, Key T, Parker J. Maternal weight gain and preterm delivery. Obstet Gynecol 1989; 74: 577–583.
38. Nordentoft M, Lou HC, Hansen D, Nim J, Pryds O, Rubin P, Hemmingsen R. Intrauterine growth retardation and premature delivery: the influence of maternal
smoking and psychosocial factors. Am J Public Health 1996; 86: 347–354.
39. Horta BL, Victora CG, Menezes AM, Halperin R, Barros FC. Low birthweight, preterm births and intrauterine growth retardation in relation to maternal
smoking. Paediatr Perinat Epidemiol 1997; 11: 140–151.
40. Goldenberg RL, Iams JD, Mercer BM, Meis PJ, Moawad AH, Copper RL, Das A, Thom E, Johnson F, McNellis D, Miodovnik M, Van Dorsten JP, Caritis SN, Thurnau GR, Bottoms SF. The preterm prediction study: the value of new
vs standard risk factors in predicting early and all spontaneous preterm births. Am J Public Health 1998; 88: 233–238.
41. Berkowitz GS, Holford TR, Berkowitz RL. Effects of cigarette
smoking, alcohol, coffee and tea consumption on preterm delivery. Sci Hum Dev 1982; 7: 239–250.
42. Williams MA, Mittendorf R, Stubblefield PG, Lieberman E, Schoenbaum SC, Monson RR. Cigarettes, coffee, and preterm premature rupture of the membranes. Am J Epidemiol 1992; 135: 895–903.
43. Berkowitz GS, Blackmore-Prince C, Lapinski RH, Savitz DA. Risk factors for preterm birth subtypes. Epidemiology 1998; 9: 279–285.
44. Klebanoff MA, Shiono PH. Top down, bottom up, and inside out: reflections on preterm birth. Paediatr Perinat Epidemiol 1995; 9: 125–129.
45. Abrams B, Newman V. Small-for-gestational-age birth: maternal predictors and comparison with risk factors of spontaneous preterm delivery in the same cohort. Am J Obstet Gynecol 1991; 164: 785–790.
46. McDonald AD, Armstrong BG, Sloan M. Cigarette, alcohol, and coffee consumption and prematurity. Am J Public Health 1992; 82: 87–90.
47. Cnattingius S, Forman MR, Berendes HW, Graubard BI, Isotalo L. Effect of age, parity and
smoking on
pregnancy outcome: a population-based study. Am J Obstet Gynecol 1993; 168: 16–21.
48. Lieberman E, Gremy I, Lang JM, Cohen AP. Low birthweight at term and the timing of fetal exposure to maternal
smoking. Am J Public Health 1994; 84: 1127–1131.
49. Sprauve ME, Lindsay MK, Drews-Botsch CD, Graves W. Racial patterns in the effects of
tobacco use on fetal growth. Am J Obstet Gynecol 1999; 181: S22–S27.
50. Kullander S, Källén B. A prospective study of
smoking and
pregnancy. Acta Obstet Gynecol Scand 1971; 50: 83–94.
51. Secker-Walker RH, Vacek PM, Flynn BS, Mead PB.
Smoking in
pregnancy, exhaled carbon monoxide, and birth weight. Obstet Gynecol 1997; 89: 648–653.
52. Alameda County Low Birth Weight Study Group. Cigarette
smoking and the risk of low birth weight: a comparison in black and white women. Epidemiology 1990; 1: 201–205.
53. Castro LC, Azen C, Hobel CJ, Platt LD. Maternal
tobacco use and substance abuse: reported prevalence rates and associations with the delivery of small for gestational age neonates. Obstet Gynecol 1993; 81: 396–401.
54. Lubs M-LE. Racial differences in maternal
smoking effects on the newborn infant. Am J Obstet Gynecol 1973; 115: 66–76.
55. Kramer MS, McLean FH, Boyd ME, Usher RH. The validity of gestational age estimation by menstrual dating in term, preterm, and postterm gestations. JAMA 1988; 250: 3306–3308.
56. Gjessing HK, Skjærven R, Wilcox AJ. Errors in gestational age: evidence of bleeding early in
pregnancy. Am J Public Health 1999; 89: 213–218.
