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ORIGINAL RESEARCH – QUANTITATIVE Tobacco use in the third trimester of pregnancy and its relationship to birth weight. A prospective study in Spain Rafael Vila Candel a,b, *, Francisco J. Soriano-Vidal b,c , Enrique Hevilla Cucarella b,d , Enrique Castro-Sa ´nchez e , Jose ´M. Martin-Moreno f,a a Department of Obstetrics and Gynecology, Hospital Universitario de la Ribera, Crta. Corbera km 1, 46.600 Valencia, Spain b Department of Nursing, Universidad Cato ´lica de Valencia, C/ Jesu ´s, 10, 46.007 Valencia, Spain b c Department of Obstetrics and Gynecology, Hospital Luis Alcanyis, Avda. Ausias March, 46.800 Xativa, Spain c d Department of Public Health, Conselleria de Sanitat de Valencia, C/ Micer Masco ´, 31, 46010 Valencia, Spain d e National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infection and Antimicrobial Resistance at Imperial College London, Du Cane Road, London W12 0NN, United Kingdom e f Department of Preventive Medicine and Public Health, Universitat de Valencia, Avda. Blasco Iban ˜ez, 15, 46.010 Valencia, Spain f 1. Introduction Optimal foetal growth is dependant on a variety of physiological and pathological determinants. 1 Amongst the physiological factors, pre-gestational body mass index (BMI) is directly related to birth weight, with higher BMI associated with higher birth weight. 2 On the contrary, the misuse of toxic substances during pregnancy, including tobacco, can lead tofoetalgrowthretardation andlowbirth weight. 3,4 Nicotine reduces the blood flow to the placenta, whilst carbon monoxide present in smoke reduces oxygenation of the fetus. 5 Different authors have analysed tobacco use during pregnancy using different methods including self-reported questionnaires, measurements of nicotine concentration in urine or expired carbon monoxide. 6–8 In Europe, the prevalence of tobacco use during pregnancy is approximately 20%. 9 In Spain, figures are higher and Women and Birth 28 (2015) e134–e139 A R T I C L E I N F O Article history: Received 8 January 2015 Received in revised form 4 June 2015 Accepted 22 June 2015 Keywords: Pregnancy Tobacco Birth weight BMI Cessation A B S T R A C T Background: Few studies have been carried out in Spain examining the use of tobacco amongst expectant mothers and its effect on birth weight. Aims: To observe the proportion of expectant mothers who smoke during their pregnancy, and the impact of tobacco consumption on maternal and birth weight. We also aimed to identify the trimester of pregnancy in which tobacco use produced the greatest reduction in birth weight. Methods: Prospective observational study in Spain. A random sampling strategy was used to select health centres and participant women. A total of 137 individuals were enrolled in the study. Exposure to tobacco was measured through a self-reported questionnaire. Regressions were performed to obtain a predictive model for birth weight related to smoking. Findings: Overall, 35% of study participants were smokers during the pre-gestational period (27% in the first trimester, 21.9% in the second and 21.2% in the third). 38.7% of smoking cessation attempts took place in the third-trimester. Pregnant women who smoked up to the third trimester had a higher risk of giving birth to a baby under 3000 g, compared to non-smokers (OR = 5.94, CI 95%: 1.94–18.16). Each additional unit of tobacco consumed daily in the 3rd trimester led to a 32 g reduction in birth weight. Conclusion: An important proportion of pregnant women in Spain smoke during pregnancy. Pregnant women exposed to tobacco have newborns with lower birth weight. Smoking during the 3rd trimester of pregnancy is associated with the greatest risk of lower birth weight. ß 2015 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved. *Corresponding author at: Department of Obstetric and Gynecology, Hospital Universitario de la Ribera, Crta. Corbera km 1, 46.600 Alzira, Valencia, Spain. Tel.: +34 962458100. E-mail addresses: [email protected], [email protected] (R. Vila Candel), [email protected] (F.J. Soriano-Vidal), [email protected] (E. Hevilla Cucarella), [email protected] (E. Castro-Sa ´nchez), [email protected] (J.M. Martin-Moreno). a Director, Programme Management World Health Organization, Europe. b Tel.: +34 963637412. c Tel.: +34 962218100. d Tel.: +34 963869210. e Tel.: +44 203 3132732. f Tel.: +34 963864100. Contents lists available at ScienceDirect Women and Birth jo u rn al h om ep age: w ww.els evier.c o m/lo c ate/wo mb i http://dx.doi.org/10.1016/j.wombi.2015.06.003 1871-5192/ß 2015 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.
around 30–43% of expectant mothers are smokers at the start of their pregnancy. 6 Although about 40% of them quit in the first trimester, 10 about 13–25% continue smoking up to delivery. 11 Spanish studies, however, are affected by methodological weaknesses. For example, the majority of studies assessed tobacco use through self-reported instruments, which may facilitate socially desirable responses and thus underestimate smoking status by 11–26%. 6,10 However, the combined effect of BMI and tobacco on birth weight remains unclear 12 and few studies on tobacco prevalence have examined the effect of quitting smoking in the thirdtrimester of pregnancy and birth weight. Some authors have suggested that early cessation of smoking in pregnancy has a greater impact on birth weight improvement 13,14 with a relatively small impact if quitting takes place during the third-trimester of pregnancy. 15 However, other researchers have claimed that thirdtrimester maternal cigarette consumption had the strongest association with birth weight, regardless of pre-pregnancy consumption levels. 16 Our study evaluated the association of prenatal exposure to maternal smoking with birth weight in different stages of pregnancy. Additionally, we aimed to identify the trimester of pregnancy in which tobacco use produced the greatest reduction in neonatal birth weight. 2. Subjects and methods 2.1. Design Prospective observational study. Participating expectant mothers were classified into two groups according to their use of tobacco during gestation. A sample of 159 women was obtained from April 2011 to March 2012. A two-stage sampling approach was used. In the first stage, we selected health centres in Carlet and Benimodo (Spain) from all primary care centres of La Ribera health district using simple random probability sampling (probability = 2/13). In the second stage, we selected pregnant women using a similar probability sampling with systematic monitoring of the number of pregnancies per year on each health centre (N 0 ). The ratio’s value (k) for the calculated sample size (n) was 2 (k = N 0 /n). We estimated that for 180 pregnant women per year attending the health centres, a minimum sample of 123 women was required (95% confidence interval (95% CI), 5% precision error). The attending midwives recruited the women at clinic and obtained their informed consent to participate. Overall, one of every two pregnant women was selected until the required sample size was obtained. The inclusion criteria were: a maternal age of 18–36 years, first prenatal visit between 5 and 12 weeks of gestation, and single foetus with no malformations. Exclusion criteria included: patient declined to participate in the study, language barrier, and expectant mothers with pathologies that significantly modified foetal growth, such as pre-gestational diabetes, essential hypertension prior to pregnancy, maternal infection or other chronic maternal pathologies. 2.2. Ethics The Committee of Ethics and Research of the University Hospital of La Ribera (UHLR) approved the study proposal in January 2011 (#11-415). Written informed consent was obtained from all women. The participants were free to decline their participation and withdraw from the research at any time. 2.3. Study variables The questionnaire was purposely designed with agreement from the research team. Birth weight was considered the dependent variable, and was recorded in the delivery room following the clamping and separation of the umbilical cord, using a digital scale (SECA 1 , Vogel & Halke GmbH & Co, Hamburg, Germany), to an accuracy of 10 g. The independent variables included socio-demographic characteristics (maternal age, country of origin, marital status, educational level, occupational state), anthropometric measurements (pre-gestational BMI, as calculated from self-reported body weight at 2–3 months prior to pregnancy and recorded at the first prenatal visit; absolute gestational weight gain; and difference between final weight on the day of delivery and pre-gestational weight), and obstetric-neonatal features (newborn gender and gestational age at birth expressed in days of gestation from the end of the mother’s last menstrual cycle). Women selected for inclusion in our study provided an estimate of their pre-pregnancy day cigarette consumption. Self-reported average tobacco consumption was used to estimate pre-gestational tobacco misuse. Equally, women were asked to report the mean number of cigarettes consumed per day in the 7 days prior to the enrolment in the study, and again for each trimester on appointment with the midwife. Data collection also included the frequency of smoking cessation attempts and relapses during pregnancy and for a period of 30 days postpartum. 2.4. Statistical analysis An analysis of the dependent variables was carried out for each of the categories of pre-gestational BMI, using descriptive methods. Afterwards, the normality of the distribution of continuous variables was examined using the Kolmogorov– Smirnov test. Statistical significance was set at the 0.05 level. Bivariate correlation analyses using Pearson correlation coefficient were initially used to explore factors associated with neonatal birth. The comparison of multiple averages was carried out using analysis of variance tests (ANOVA), after assessment of the homogeneity and normality of the data with the Levene test. The magnitude of the effect of first-hand exposure to tobacco on categorised birth weight was estimated using multiple logistic regression, with birth weight (<3000 g or >3000 g) as the outcome measure and adjusted for pre-gestational maternal BMI (WHO categories: underweight (UW) <18.5 kg/m 2 , normal weight (NW) 18.5–24.9 kg/m 2 , overweight (OW) 25.0–29.9 kg/m 2 , obese (OB) >30 kg/m 2 ) 17 as explanatory variable. Additional explanatory variables included gestational age at birth (days). To analyse the relationship between birth weight (dependent variable) and tobacco use by the expectant mother (independent variable), an adjusted multiple linear regression model was applied using a stepwise method for variables shown to have an effect on birth weight. Smoking indicators examined included the number of cigarettes consumed per day before pregnancy, at the time of registration into the study (first trimester), and in the second and third trimester. Partial correlation coefficients represent the strength of the linear relationship between each independent variable and birth weight, after controlling for other predictors in the regression model. The data was analysed using SPSS Statistics version 22. 3. Results Out of a total of 159 expectant mothers initially included in the study, we excluded 22 cases (10 cases of spontaneous miscarriage in the first trimester, 1 case of foetal malformation in the second trimester, 2 cases of loss to follow-up during the pregnancy, and 9 cases of gestational diabetes). Therefore, the final sample included 137 expectant mothers. R. Vila Candel et al. / Women and Birth 28 (2015) e134–e139 e135
Table 1 provides a detailed description of maternal and neonatal characteristics. Smokers were 30–34 years old, less educated, married, employees and more frequently within normal weight than non-smokers at each corresponding point during gestation. The neonatal birth weight of smoking mothers was 235 g lower than non-smokers (p = 0.006). Table 2 presents tobacco statuses. Regarding pre-pregnancy tobacco use, 64.2% (88) did not smoke, 35.8% (49) did, and 0.8% (1) quit prior to becoming pregnant. At the beginning of pregnancy, the proportion of smokers was 35%, of whom 14.6% were underweight, 68.8% were normal weight and 26.7% were overweight. None of the mothers smoking prior to pregnancy were obese. In terms of smoking cessation during pregnancy, cessation rates increased progressively during the three trimesters (8%, 13.1% and 13.9% respectively). We did not find any expectant mothers who relapsed during pregnancy or during 30 days of postpartum. Underweight smokers accounted for the largest proportion of those who stopped smoking (44.5%) when compared to women who either had normal weight (12.6%) or were overweight (10%). Additionally, underweight smokers achieved a greater reduction in the average number of cigarettes smoked compared to women who had normal weight (4.3 fewer daily cigarettes compared to 1.0). Overweight smokers, on the contrary, had increased their daily average consumption by 3.1 cigarettes by the end of their pregnancies. The results of the bivariate analysis on tobacco status and birth weight for different trimesters of gestation, according to categorised pre-gestational maternal BMI are displayed in Table 3. Maternal smoking was associated with birth weight only at NW pre-gestational BMI. Of the smoking indicators examined, cigarette consumption was significantly and negatively correlated with birth weight before pregnancy (R = 0.243, p = 0.018), as well as the second (R = 0.276, p = 0.007) and third trimester (R = 0.304, p = 0.003). Birth weight in newborns from nonsmoking mothers was significantly higher when compared with smoking participants (3297.8 g [95% CI: 3187.6–3408.0] compared to 3070.1 g [95% CI: 2910.4–3229.8], p = 0.018). Likewise, expectant mothers who did not smoke in the second and third trimesters had babies with higher birth weight than mothers who were smokers during those periods (3284.3 g [95% CI: 3179.8–3388.9] vs 2990.6 g [95% CI: 2816.7–3164.5] for the second trimester and 3289.0 g [3185.5–3392.6] compared to 2960.2 g [95% CI: 2789.8– 3130.6] for the third), with statistically significant differences (p = 0.007 and p = 0.003, respectively). Table 4 describes the risk of having a newborn with a weight below 3000 g, according to smoking behaviour during pregnancy, and adjusted for pre-gestational maternal BMI and gestational age at birth. Expectant mothers exposed to tobacco during the third trimester were at greater risk of having a lower neonatal weight than their non-smoking counterparts (OR: 5.94 [CI 95%: 1.94– 18.16]). The results of the multiple regression analyses (Table 5 and Fig. 1) suggest that of the smoking variables examined, maternal third trimester cigarette consumption was the strongest predictor of birth weight after adjusting for gestational age and pregestational maternal BMI (partial R = 0.253, p = 0.003). For each additional cigarette per day smoked in the third-trimester, there was an estimated reduction in birth weight of 32 g (CI 95%: 53.08, 11.04). Additional direct independent contributors to birth Table 1 Distribution of socio-demographic, obstetrics and neonatal variables, categorised according to tobacco use during pregnancy. Variables Smoking status p-Value Non-smokers (n = 89. 65%) Smokers (n = 48. 35%) Final no. % Final no. % Maternal age (years) <25 9 10.1 12 25.0 0.036 a 26–29 24 27.0 12 25.0 30–34 38 42.7 21 43.8 >35 18 20.2 3 6.3 Marital status Married 80 89.9 32 66.7 0.001 a Single 9 10.1 16 33.3 Country of origin Spain 78 87.6 39 81.3 0.312 a Other 11 12.4 9 18.8 Education Up to primary 29 32.6 25 52.1 0.033 a Up to secondary 34 38.2 17 35.4 University degree 26 29.2 6 12.5 Occupational state I 6 6.7 4 8.3 0.045 a II 57 64.1 26 54.2 III 0 0.0 1 2.1 IV 13 14.6 4 8.3 V 13 14.6 13 27.1 PRE-GEST BMI (kg/m 2 ) <=18.5 2 2.2 7 14.6 0.021 a 18.6–24.9 62 69.7 33 68.8 25.0–29.9 22 24.7 8 16.7 30.0+ 3 3.4 0 0.0 Newborn gender Male 48 53.9 23 47.9 0.501 a Female 41 46.1 25 52.1 Parity 0 43 48.3 29 60.4 0.176 a >=1 46 51.7 19 39.6 Birth weight (g) >=3000 69 77.5 26 54.2 0.005 a <3000 20 22.5 22 45.8 I: self-employed, managerial or higher professions; II: employees; III: student; IV: stay at home mothers; V: unemployed. PRE-GEST BMI: pre-gestational Body Mass Index. a p-Value: obtained through Chi-square test of different categories of variables. Table 2 Distribution of obstetrics and neonatal variables, categorised according to tobacco use during pregnancy. Smoking status Non-smokers (n = 89. 65%) Smokers (n = 48. 35%) Mean (CI 95%) Mean (CI 95%) Birth weight (g) 3339 (3236.7–3441.2) 3104 (2976.2–3231.7) 0.006 a Gestational age 278.6 (276.9–280.3) 278.1 (275.1–281.0) 0.742 a Gestational weight gain (kg) 14.0 (13.0–15.1) 15.2 (14.0–16.4) 0.178 a Pre-pregnancy smoker (cig/day) 0 14.5 (12.2–16.9) Cigarettes per day 1T 0 5.0 (3.8–6.2) <0.001 b Cigarettes per day 2T 0 4.58 (3.2–5.9) <0.001 b Cigarettes per day 3T 0 4.3 (3.0–5.6) <0.001 b 1T: first trimester; 2T: second trimester; 3T: third trimester. a p-Value: obtained through ANOVA (factor: smoker). b p-Value: obtained through Student t-test for averages related to pre-gestational smoking status. R. 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weight after adjusting for gestational age (partial R = 0.404, p < 0.001) included maternal BMI (partial R = 0.281, p = 0.006). The final model included 3 variables and explained 27% of the variability in newborn birth weight. 4. Discussion Our prospective observational study included 137 expectant mothers in Spain, who were classified into groups according to their gestational tobacco use. In our results, pre-gestational maternal BMI is positively related to birth weight, independently of all other parameters examined, and in agreement with other studies. 2,3,18 In the Spanish health care system, midwives are the main point of contact for women during pregnancy. National guidelines indicate that midwives should ask about women’s smoking status at the first antenatal appointment (usually between 8 and 12 weeks), and provide smoking cessation advice and referral if warranted. However, there is still a paucity of data regarding the impact of smoking cessation advice on smoking status. The proportion of smokers decreased progressively from the first to the third trimester, which is also consistent with previous studies. 6,7,10,11,13,19 In our study, we observed statistically significant differences between cigarette consumption and maternal age, educational level and occupational state. 20 Our data suggest that, taking into consideration already known factors that influence on birth weight, a linear relation persists between self-reported consumption of cigarettes in the third trimester and neonatal birth weight, as previously reported. 17 However, other studies have postulated safe levels of tobacco consumption. 15,21,22 The observable effect of maternal smoking Table 3 Association between smoking status during pregnancy and birth weight, according to maternal pre-gestational BMI (kg/m 2 ; n = 137). PRE-GEST BMI Mean cig/day Birth weight (g) n (%) R p-Value (CI 95%) Mean (CI 95%) <=18.5 kg/m 2 (n = 9) PRE-PREG non-smoker 0 3065.0 (333.1–5796.8) 2 (22.2) 0.034 0.93 a PRE-PREG smoker 10.7 (4.5–16.7) 3095.3 (2702.0–3487.9) 7 (77.8) Non-smoker 1T 0 3104.1 (2796.7–3411.5) 6 (66.6) 0.062 0.874 a Smoker 1T 4.3 (2.9–8.7) 3056.6 (1542.0–4571.2) 3 (33.3) Non-smoker 2T 0 3104.1 (2796.7–3411.5) 6 (66.6) 0.062 0.874 a Smoker 2T 7.3 (3.0–9.6) 3056.6 (1542.0–4571.2) 3 (33.3) Non-smoker 3T 0 3104.1 (2796.7–3411.5) 6 (66.6) 0.062 0.874 a Smoker 3T 5.0 (4.5–7.9) 3056.6 (1542.0–4571.2) 3 (33.3) 18.6–24.9 kg/m 2 (n = 95) PRE-PREG non-smoker 0 3297.8 (3187.6–3408.0) 61 (64.3) 0.243 0.018 a PRE-PREG smoker 5.5 (3.7–7.3) 3070.1 (2910.4–3229.8) 33 (34.7) Non-smoker 1T 0 3265.6 (3158.6–3372.6) 68 (71.6) 0.174 0.091 a Smoker 1T 7.3 (3.4–9.2) 3092.2 (2910.5–3273.9) 27 (28.4) Non-smoker 2T 0 3284.3 (3179.8–3388.9) 73 (76.8) 0.276 0.007 a Smoker 2T 7.7 (4.2–8.5) 2990.6 (2816.7–3164.5) 22 (23.2) Non-smoker 3T 0 3289.0 (3185.5–3392.6) 74 (77.9) 0.304 0.003 a Smoker 3T 4.5 (3.4–9.4) 2960.2 (2789.8–3130.6) 21 (22.1) 25.0–29.9 kg/m 2 (n = 30) PRE-PREG non-smoker 0 3380.2 (3134–3625.9) 22 (73.3) 0.121 0.523 a PRE-PREG smoker 3.1 (0.7–5.5) 3243.1 (2941.4–3544.7) 8 (26.7) Non-smoker 1T 0 3386.5 (3151.9–3621.0) 23 (76.6) 0.156 0.411 a Smoker 1T 4.4 (2.2–7.4) 3202.8 (2860.8–3544.8) 7 (23.3) Non-smoker 2T 0 3388.8 (3174.3–3603.2) 25 (83.3) 0.202 0.284 a Smoker 2T 5.4 (1.1–8.3) 3118.0 (2601.5–3634.5) 5 (16.7) Non-smoker 3T 0 3388.8 (3174.3–3603.2) 25 (83.3) 0.202 0.284 a Smoker 3T 6.2 (1.6–8.2) 3118.0 (2601.5–3634.5) 5 (16.7) >30.0 kg/m 2 (n = 3) PRE-PREG non-smoker 0 4166.6 (2781.0–5552.2) 3 (100.0) PRE-GEST BMI: pre-gestational Body Mass Index; PRE-PREG: pre-pregnancy; 1T: first trimester; 2T: second trimester; 3T: third trimester; CI 95%: confidence interval 95%; R: Pearson’s correlation; p-value: obtained through ANOVA. Table 4 Logistical regression between smoking status during pregnancy and categorised birth weight. Variables Birth weight (<3000, 3000 g) Gross OR (IC 95%) p-Value Adjusted OR * (CI 95%) p-Value PRE-PREG smoker 2.77 (1.30–5.87) 0.008 3.77 (1.42–9.99) 0.007 Cigarettes/day 1T 3.00 (1.36–6.61) 0.007 4.90 (1.70–14.14) 0.003 Cigarettes/day 2T 4.29 (1.83–10.03) 0.001 5.34 (1.79–15.92) 0.003 Cigarettes/day 3T 4.70 (1.98–11.15) <0.001 5.94 (1.94–18.16) 0.002 PRE-PREG: pre-pregnancy; 1T: first trimester; 2T: second trimester; 3T: third trimester. * OR adjusted for: pre-gestational BMI (normal weight category) and gestational age at birth (days). Table 5 Multivariate linear regression analysis predicting birth weight. Independent variable Coefficient Partial R Partial R 2 p-Value Constant 3079.464 Gestational age (days) 20.673 0.404 0.186 <0.001 3rd trimester cigarettes/days 32.061 0.253 0.232 0.003 Pre-gestational BMI 27.387 0.236 0.269 0.006 BMI: body mass index. R. Vila Candel et al. / Women and Birth 28 (2015) e134–e139 e137
later in pregnancy suggests that every additional cigarette consumed per day in the third-trimester results in a reduction of approximately 32 g in the birth weight of the newborn. Such effect appears to be greater than the previously reported by Bernstein et al., 16 Mathai et al. 23 or England et al. 15 who noted between 12 and 27 g. Overall, our results propose a total weight reduction of 137.6 g (32 g/cigarette 4.3 cigarettes/day), within the range determined by other authors 20,24,25 reporting a weight fall between 114 and 170 g amongst smokers. The greater percigarette influence on birth weight in our data can be explained by the continuous linear relationship we observed. Thus, we disagree with the notion of a minimum secure level on cigarette consumption rather than a continuous effect. A valid estimation of the risks associated with tobacco exposure would depend on accurate measurements. However, some individuals may be more reluctant than others to disclose their smoking status and exposure to tobacco. This can be particularly true for pregnant women, for whom smoking may be regarded as socially unacceptable. Thus, estimates based on self-reported information are likely to underestimate the real proportion of tobacco use. Exposure to tobacco can be analysed by measuring smoke components in the air, self-reported indicators of exposure through interviews or measuring smoke components concentrations with biomarkers. 26 The first approach is suboptimal as monitors can only be used for short periods of time, which are unlikely to be reflective of overall exposure. In terms of selfreported smoking behaviours, a recent meta-analysis 27 suggested that in most studies it could be an acceptable methodology for estimating tobacco consumption, if validated with biochemical measurements. However, the authors excluded studies which included pregnant women. Other authors have concluded that validation with biomarkers should also be considered in studies with students and intervention studies. 28,29 Despite these advantages, self-reported questionnaires present various concerns related to their validity as tools for data collection, a lack of validation and standardisation as well as misclassification of exposure amongst the most serious drawbacks. These may originate from participants’ failure to accurately recall exposure, lack of knowledge, intentional false reporting, biased recall, or memory failure. 28 Bias may be more common whenever social desirability is greater. 11 Furthermore, the quantity of inhaled and absorbed smoking products varies with the manner of smoking, which may be difficult to express and quantify in a questionnaire. 25 Underreporting was found in 4–12% of pregnant women who demonstrated values inconsistent with their self-report. 26 Other investigators have identified a poor correlation of selfreported maternal cigarette consumption with biomarkers like urinary cotinine. They have reported an inversely proportional relationship of urinary nicotine to birth weight. 15,30 Some methodological considerations should be noted with regard to our study. First, our results rely on the validity of responses to the self-reported questionnaire. Consequently, the smoking rate we observed may effectively be an underestimation of the true proportion, due to the potential for socially desirable responses offered by our participants. The factors most closely related to concealing an individual’s smoking status have to do with the timing and the quantity of tobacco consumed. 9,12,31,32 We acknowledge that in optimal circumstances, midwives caring for participants may not be the ideal recruiters of individuals onto a study. As an additional limitation in our study, we had a reduced number of participants within the underweight and obese categories, although this was due to the nature of the sampling. The strengths of our study are the use of probability sampling in the selection of the study population. In addition, we were able to draw a valid sample size representative of the total population of expectant mothers in our setting. Unlike other studies, our sample was categorised by pre-gestational maternal BMI, an important independent factor in determining birth weight. Different studies have tried to determine the relationship between cigarette smoking amongst expectant mothers and birth weight. Although the studies have produced heterogeneous results, most observe an increased risk of lower birth weight amongst smokers. 1,19–21 However, the studies are limited by the difficulty in quantifying maternal exposure precisely and in adjusting for the multiplicity of confounding factors that can affect birth weight. 32,33 In conclusion, our results on the association of active smoking during pregnancy with birth weight indicate that smoking in pregnancy increased the risk of having lower weight newborns (<3000 g), and that this risk is most pronounced for women who smoke during their third trimester, reinforcing the need to encourage and support women to avoid smoking during Fig. 1. The relationship between third-trimester cigarette consumption and newborn birth weight is illustrated at the sample means for gestational age (days) and body mass index. The effect of each added cigarette consumed in the third trimester on newborn birth weight is approximately 32 g. R. Vila Candel et al. / Women and Birth 28 (2015) e134–e139 e138
pregnancy. Pregnancy offers a strategic opportunity for health professionals to promote smoking cessation and motivate women to give up tobacco use. Such opportunity to encourage smoking cessation interventions should be specially seized by midwives, as first point of contact for women during their pregnancy. Ethical approval The present study was carried out in accordance with the basic principles for all medical research, the Helsinki Declaration. The Committee of Ethics and Research of the University Hospital of La Ribera (UHLR) approved the study proposal in January 2011 (#11-415). Acknowledgements and disclosures The authors would like to thank all study participants. We also acknowledge the managers of the University Hospital of La Ribera for their support during our research. We would like to thank Meggan Harris, Professor of Preventive Medicine and Public Health at Universitat de Vale `ncia (Spain) for the translation of this paper and feedback. The authors have no conflicts of interest to disclose. References 1. Mercer BM, Merlino AA, Milluzzi CJ, Moore JJ. Small fetal size before 20 weeks’ gestation: associations with maternal tobacco use, early preterm birth, and low birthweight. Am J Obstet Gynecol 2008;198(6):673.e1–e. discussion e7-8. 2. Simas TA, Liao X, Garrison A, Sullivan GM, Howard AE, Hardy JR. Impact of updated Institute of Medicine guidelines on prepregnancy body mass index categorization: gestational weight gain recommendations, and needed counseling. J Womens Health (Larchmt) 2011;20(6):837–44. 3. Nohr EA, Vaeth M, Baker JL, Sorensen TI, Olsen J, Rasmussen KM. Pregnancy outcomes related to gestational weight gain in women defined by their body mass index: parity, height, and smoking status. Am J Clin Nutr 2009;90(5):1288–94. 4. Jaddoe VW, Troe EJ, Hofman A, Mackenbach JP, Moll HA, Steegers EA, et al. Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. Paediatr Perinat Epidemiol 2008;22(2):162–71. 5. Geelhoed JJ, El Marroun H, Verburg BO, van Osch-Gevers L, Hofman A, Huizink AC, et al. Maternal smoking during pregnancy, fetal arterial resistance adaptations and cardiovascular function in childhood. BJOG 2011;118(6):755–62. 6. Mateos-Vilchez PM, Aranda-Regules JM, Diaz-Alonso G, Mesa-Cruz P, Gil-Barcenilla B, Ramos-Montserrat M, et al. Smoking prevalence and associated factors during pregnancy in Andalucia 2007–2012. Rev Esp Salud Publica 2014;88(3):369–81. 7. Russell T, Crawford M, Woodby L. Measurements for active cigarette smoke exposure in prevalence and cessation studies: why simply asking pregnant women isn’t enough. Nicotine Tob Res 2004;6(Suppl. 2):S141–51. 8. Peacock JL, Cook DG, Carey IM, Jarvis MJ, Bryant AE, Anderson HR, et al. Maternal cotinine level during pregnancy and birthweight for gestational age. Int J Epidemiol 1998;27(4):647–56. 9. Vardavas CI, Patelarou E, Chatzi L, Roumeliotaki T, Sarri K, Murphy S, et al. Factors associated with active smoking: quitting, and secondhand smoke exposure among pregnant women in Greece. J Epidemiol 2010;20(5):355–62. 10. Salvador J, Villalbi JR, Nebot M, Borrell C. Exposure to smoking during pregnancy: Barcelona (Spain) 1994–2001. An Pediatr (Barc) 2004;60(2):139–41. 11. Jimenez-Muro A, Samper MP, Marqueta A, Rodriguez G, Nerin I. Prevalence of smoking and second-hand smoke exposure: differences between Spanish and immigrant pregnant women. Gac Sanit 2012;26(2):138–44. 12. Goetzinger KR, Cahill AG, Macones GA, Odibo AO. The relationship between maternal body mass index and tobacco use on small-for-gestational-age infants. Am J Perinatol 2012;29(3):153–8. 13. Iniguez C, Ballester F, Costa O, Murcia M, Souto A, Santa-Marina L, et al. Maternal smoking during pregnancy and fetal biometry: the INMA Mother and Child Cohort Study. Am J Epidemiol 2013;178(7):1067–75. 14. Iniguez C, Ballester F, Amoros R, Murcia M, Plana A, Rebagliato M. Active and passive smoking during pregnancy and ultrasound measures of fetal growth in a cohort of pregnant women. J Epidemiol Community Health 2012;66(6):563–70. 15. England LJ, Kendrick JS, Wilson HG, Merritt RK, Gargiullo PM, Zahniser SC. Effects of smoking reduction during pregnancy on the birth weight of term infants. Am J Epidemiol 2001;154(8):694–701. 16. Bernstein IM, Mongeon JA, Badger GJ, Solomon L, Heil SH, Higgins ST. Maternal smoking and its association with birth weight. Obstet Gynecol 2005;106(5 Pt 1):986–91. 17. Andersen CS, Gamborg M, Sorensen TI, Nohr EA. Weight gain in different periods of pregnancy and offspring’s body mass index at 7 years of age. Int J Pediatr Obes 2010;6(2–2):e179–86. 18. Stein AD, Zybert PA, van de Bor M, Lumey LH. Intrauterine famine exposure and body proportions at birth: the Dutch Hunger Winter. Int J Epidemiol 2004;33(4):831–6. 19. Kharrazi M, DeLorenze GN, Kaufman FL, Eskenazi B, Bernert JT, Graham S, et al. Environmental tobacco smoke and pregnancy outcome. Epidemiology 2004;15(6):660–70. 20. Cano-Serral G, Rodriguez-Sanz M, Borrell C, Perez Mdel M, Salvador J. Socioeconomic inequalities in the provision and uptake of prenatal care. Gac Sanit 2006;20(1):25–30. 21. Ribot B, Isern R, Hernandez-Martinez C, Canals J, Aranda N, Arija V. Effects of tobacco habit: second-hand smoking and smoking cessation during pregnancy on newborn’s health. Med Clin (Barc) 2014;143(2):57–63. 22. Britton GR, James GD, Collier R, Sprague LM, Brinthaupt J. The effects of smoking cessation and a programme intervention on birth and other perinatal outcomes among rural pregnant smokers. Ann Hum Biol 2013;40(3):256–65. 23. Mathai M, Skinner A, Lawton K, Weindling AM. Maternal smoking: urinary cotinine levels and birth-weight. Aust N Z J Obstet Gynaecol 1990;30(1):33–6. 24. Anderka M, Romitti PA, Sun L, Druschel C, Carmichael S, Shaw G, et al. Patterns of tobacco exposure before and during pregnancy. Acta Obstet Gynecol Scand 2010;89(4):505–14. 25. Samper MP, Jimenez-Muro A, Nerin I, Marqueta A, Ventura P, Rodriguez G. Maternal active smoking and newborn body composition. Early Hum Dev 2012;88(3):141–5. 26. Florescu A, Ferrence R, Einarson T, Selby P, Soldin O, Koren G. Methods for quantification of exposure to cigarette smoking and environmental tobacco smoke: focus on developmental toxicology. Ther Drug Monit 2009;31(1):14–30. 27. Patrick DL, Cheadle A, Thompson DC, Diehr P, Koepsell T, Kinne S. The validity of self-reported smoking: a review and meta-analysis. Am J Public Health 1994;84(7):1086–93. 28. Almeida ND, Koren G, Platt RW, Kramer MS. Hair biomarkers as measures of maternal tobacco smoke exposure and predictors of fetal growth. Nicotine Tob Res 2011;13(5):328–35. 29. Spanier AJ, Kahn RS, Xu Y, Hornung R, Lanphear BP. Comparison of biomarkers and parent report of tobacco exposure to predict wheeze. J Pediatr 2011;159(5):776–82. 30. Hoekzema L, Werumeus Buning A, Bonevski B, Wolke L, Wong S, Drinkwater P, et al. Smoking rates and smoking cessation preferences of pregnant women attending antenatal clinics of two large Australian maternity hospitals. Aust N Z J Obstet Gynaecol 2014;54(1):53–8. 31. Myers RE. Promoting healthy behaviors: how do we get the message across? Int J Nurs Stud 2010;47(4):500–12. 32. Mendelsohn C, Gould GS, Oncken C. Management of smoking in pregnant women. Aust Fam Phys 2014;43(1):46–51. 33. Ino T. Maternal smoking during pregnancy and offspring obesity: meta-analysis. Pediatr Int 2010;52(1):94–9. R. Vila Candel et al. / Women and Birth 28 (2015) e134–e139 e139