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In Utero Exposure to Alcohol and Puberty in Boys: a Pregnancy Cohort Study

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In Utero Exposure to Alcohol and Puberty in Boys: a Pregnancy Cohort Study Downloaded from http://bmjopen.bmj.com/ on November 16, 2015 - Published by group.bmj.com Open Access Research In utero exposure to alcohol and puberty in boys: a pregnancy cohort study Linn Berger Håkonsen,1 Mette Louise Brath-Lund,2 Marie Louise Hounsgaard,2 Jørn Olsen,1 Andreas Ernst,1 Ane Marie Thulstrup,2 Bodil Hammer Bech,1 Cecilia Høst Ramlau-Hansen1 To cite: Håkonsen LB, Brath- ABSTRACT Strengths and limitations of this study Lund ML, Hounsgaard ML, Objectives: Epidemiological studies have raised et al. In utero exposure to concerns about the reproductive consequences of in alcohol and puberty in boys: a Strengths utero exposure to alcohol. Maternal lifestyle factors pregnancy cohort study. BMJ ▪ Large pregnancy cohort with a rather high par- Open 2014;4:e004467. have been associated with altered pubertal ticipation rate (55%). doi:10.1136/bmjopen-2013- development, but the impact of prenatal alcohol ▪ Prospectively collected data on maternal alcohol 004467 exposure on male puberty is unknown. Thus, the consumption. objective was to explore whether prenatal alcohol ▪ Data with a large exposure contrast. exposure alters pubertal development in boys. ▸ Prepublication history for ▪ Ability to study dose–response effects. this paper is available online. Setting: Follow-up of a Danish pregnancy cohort. ▪ ‘State-of-the-art’ statistical methods. To view these files please Participants: Sons (N=2522) of women who were Limitations visit the journal online enrolled in a Danish pregnancy cohort between 1984 ▪ Self-reported data on pubertal development. (http://dx.doi.org/10.1136/ and 1987. ▪ Lack of valid indicators of pubertal development bmjopen-2013-004467). Primary and secondary outcome measures: in boys. Indicators of pubertal development, assessed by age at ▪ A relatively large amount of missing data on the Received 18 November 2013 first nocturnal emission, voice break, acne and regular indicators of pubertal development. Revised 5 May 2014 ▪ Accepted 13 May 2014 shaving. Risk of uncontrolled or residual confounding. Results: We found a tendency towards a later age at first nocturnal emission and voice break following in 56 utero exposure to binge drinking. Boys exposed to ≥5 countries and is, thus, one of the major binge drinking episodes during pregnancy experienced modifiable risk factors possibly affecting fetal their first nocturnal emission 7.3 months (95% CI growth. −2.8 to 17.4) later and voice break 4.9 months (95% Interest in male reproductive conse- CI −0.6 to 10.4) later than the unexposed boys. quences of prenatal exposure to alcohol has Results for average weekly alcohol consumption were grown recently, as focus on causes of subfe- in the same direction, but differences were smaller and cundity has intensified worldwide. In boys, not statistically significant. one study reported an association between Conclusions: We found no strong support for the prenatal alcohol exposure and cryptorchid- hypothesis that in utero exposure to weekly alcohol ism,7 a congenital malformation that may consumption is a risk factor for altered pubertal development, but a tendency towards delayed pubertal predispose to impaired semen quality, development among boys exposed to binge drinking whereas other studies have shown inconsist- 8–10 during fetal life was observed. Longitudinal studies, ent results. In adult life, indications of with data collected as children go through puberty, are reduced semen quality among exposed men needed to explore this further. have been reported.11 A few studies have investigated the associ- ation between maternal alcohol consumption during pregnancy and pubertal development 1Department of Public Health, INTRODUCTION in girls. One of these observed a later age of Section for Epidemiology, Alcohol consumption during pregnancy has menarche in a small group of heavily Aarhus University, Aarhus C, 12 Denmark been associated with adverse pregnancy out- exposed girls, but two recent studies did 2 12 3 fi 13 14 et al14 Department of Occupational comes and child morbidity. Although not support this nding. Shrestha Medicine, Danish Ramazzini controversy still exists regarding the safety of also assessed binge drinking episodes during Center, Aarhus University low-level consumption4 and specific timing pregnancy, but found no effects on the Hospital, Aarhus C, Denmark of exposure, women are advised to abstain timing of menarche, either of binge drinking Correspondence to from alcohol when planning to conceive and or of weekly alcohol consumption. Linn Berger Håkonsen; throughout pregnancy. Yet, alcohol consump- In boys, studies on risk factors for altered [email protected] tion is common during pregnancy in many pubertal development are sparse. It is well Håkonsen LB, Brath-Lund ML, Hounsgaard ML, et al. BMJ Open 2014;4:e004467. doi:10.1136/bmjopen-2013-004467 1 Downloaded from http://bmjopen.bmj.com/ on November 16, 2015 - Published by group.bmj.com Open Access established that variability in onset of puberty depends to provide the age in years and months at which the on genetic factors, ethnicity and nutritional conditions,15 event first occurred. We converted the month into a frac- but in utero exposures may also have an early ‘program- tion of a year and added years to create a continuous ming’ role. It has been indicated that male pubertal outcome variable for each of the four events. development may be accelerated following in utero – exposure to cigarette smoking16 18 and maternal Covariates obesity.19 Potential confounders were identified a priori: maternal This study aims to explore whether prenatal alcohol age in years (continuous), maternal pre-pregnancy body exposure alters pubertal development in boys. mass index (BMI; <18.5, 18.5–24.9 and >24.9 kg/m2), maternal smoking during pregnancy (smoker, former smoker (stopped before pregnancy) and non-smoker), METHODS maternal chronic diseases (diabetes mellitus, epilepsy, This study is based on data from the pregnancy cohort arthrosis, heart disease, cancer, psychiatric disorders, ‘ ’20 Healthy habits for two established between 1984 and allergy or other chronic diseases combined into one vari- 1987 in the municipalities of Aalborg and Odense, able: present vs not present), municipality of residence Denmark. The cohort included 11 980 pregnant women at the time of delivery (urban areas vs rural areas), (87% of all invited), who at a routine visit to the family socioeconomic status based on the highest midwife around the 36th gestational week, completed a ranking of job description or academic background questionnaire concerning lifestyle, demographic and between parents at the time of pregnancy (white-collar health-related characteristics before and during preg- workers, blue-collar workers and unemployed or stu- nancy, including questions on consumption of alcoholic dents) and cohabitation status of the parents at birth beverages during pregnancy. These women were all (mother living with the father of the child vs mother not Danish citizens and since only 1% of Danish women living with the father of the child). aged 20–34 years were immigrants or descendants from – immigrants during 1984 1987, the participants were Statistical analyses 21 most likely Caucasians. Of the 11 980 pregnant Missing information women, 11 144 delivered live born singletons. Of these, The number (%) of participants who gave information 5716 were boys. In 2005, 5142 men (between 18 and on age for the four outcome variables were: acne 1804 21 years of age) who were alive and living in Denmark (64%), voice break 1696 (60%), regular shaving 2128 fi were identi ed in the Danish Civil Registration System (76%) and first nocturnal emission 924 (33%). About and invited to complete an internet-based questionnaire. three-quarter of these only provided age in years. A total of 2810 (55%) men responded. Information on maternal average weekly alcohol con- sumption was complete and there were only four (0.1%) Exposure assessment missing values on binge drinking. Furthermore, the level In the questionnaire completed by the pregnant women of missing values in covariates varied from 0% to 6.9% around the 36th gestational week, they were asked about (table 1). Unexposed boys had more missing values in their average weekly intake of beer, wine and spirits the pubertal events compared with boys exposed to while being pregnant. One drink was defined as one alcohol during pregnancy. However, differences were bottle of beer (0.33 L), one glass of wine or one glass of rather small. spirits. We calculated the weekly intake of these alcoholic Since complete case analysis can lead to biased esti- beverages for each woman. The average maternal mates and limited power, we addressed the missing data alcohol intake during pregnancy was categorised into problem by using multiple imputations, which often four groups: 0, 0.5–1.5, 2–4 or >4 drinks/week. yield unbiased and more precise estimates if data are Furthermore, the women were asked how many times missing at random.22 23 Briefly, the multiple imputations they had consumed eight or more alcoholic drinks on a model is an approach that creates several (m>1) differ- single occasion (defined as binge drinking) while being ent imputed datasets based on other known paticipant pregnant with the following predetermined response cat- characteristics from the whole dataset. The m complete egories: 0, 1–4, 5–9, 10–19 or >20 times. We formed datasets are then analysed and the results are combined three groups according to the number of binge drinking using the so-called Rubin’s
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