Early Life Exposures

Parental smoking during pregnancy and the risk

of gestational diabetes in the daughter

Wei Bao,1,2 Karin B Michels,3,4,5 Deirdre K Tobias,6,7 Shanshan Li,1

Jorge E Chavarro,3,4,7 Audrey J Gaskins,7 Allan A Vaag,8

Frank B Hu3,4,7 and Cuilin Zhang1*

1Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child

Health and Human Development, Rockville, MD, USA, 2Department of Epidemiology, University of Iowa

College of Public Health, Iowa City, IA, USA, 3Department of Epidemiology, Harvard T.H. Chan School of

Public Health, Boston, MA, USA, 4Channing Division of Network Medicine, 5Department of Obstetrics,

Gynecology and Reproductive Biology, 6Division of Preventive Medicine, Brigham and Women’s

Hospital and Harvard Medical School, Boston, MA, USA, 7Department of Nutrition, Harvard T.H. Chan

School of Public Health, Boston, MA, USA and 8Department of Endocrinology, Rigshospitalet,

Copenhagen, Denmark

*Corresponding author. Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy

Shriver National Institute of Child Health and Human Development, National Institutes of Health, 6100 Executive Blvd,

Rockville, MD 20852, USA. E-mail: [email protected]

The abstract of this study was included in poster presentation at the American Heart Association’s EPI/Lifestyle2015

Scientific Sessions (March 3–6, 2015, Baltimore, MD).

Accepted 19 November 2015

Abstract

Background: Fetal exposure to parental smoking may have long-term impact on the de-

velopment of disease in adulthood. We examined the association of parental smoking

during pregnancy with risk of gestational diabetes mellitus (GDM) in the daughter.

Methods: We included 15 665 singleton pregnancies from 10 152 women in the Nurses’

Health Study II cohort whose mothers participated in the Nurses’ Mothers’ Cohort Study.

Data on maternal and paternal smoking during pregnancy and associated covariates

were recalled by the mothers. GDM diagnosis was self-reported by the daughters

and was validated by medical record review in a previous study. We used log-binomial

models with generalized estimating equations to estimate relative risks (RRs) and 95%

confidence intervals (CIs).

Results: We observed a positive association between maternal heavy smoking during

pregnancy and risk of GDM in the daughter. The multivariable-adjusted RRs (95% CIs) of

GDM among women whose mothers did not smoke during pregnancy, continued smoking

1–14, 15–24, and�25 cigarettes/day were 1.00 (reference), 1.05 (0.81–1.35), 1.27 (0.95–1.70) and 1.98 (1.18–3.30), respectively (P for trend¼0.01). Further adjustment for the women’s perinatal variables, adult-life characteristics and body mass index during various periods

of life modestly attenuated the association. No association was observed between pater-

nal smoking during the pregnancy period and risk of GDM in the daughter.

Published by Oxford University Press on behalf of International Epidemiological Association 2016.

This work is written by US Government employees and is in the public domain in the US. 160

International Journal of Epidemiology, 2016, 160–169

doi: 10.1093/ije/dyv334

Advance Access Publication Date: 9 January 2016

Original article

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Conclusions: Maternal heavy smoking (�25 cigarettes/day) during pregnancy was associ- ated with higher risk of gestational diabetes in the daughter. Further studies are warranted

to confirm our findings and to elucidate the underlying mechanisms.

Key words: Gestational diabetes mellitus, maternal smoking during pregnancy

Introduction

The developmental origins of health and disease hypothesis,

or ‘Barker hypothesis’,1 continues to fuel research interest in

examining the health consequences of in utero exposures.

Maternal smoking during pregnancy represents a common

deleterious fetal exposure in many populations.2–4 The

short-term effects of maternal smoking during pregnancy on

multiple adverse pregnancy and perinatal outcomes, includ-

ing fetal growth restriction and low birthweight, have long

been recognized and established.5 Maternal smoking during

pregnancy has also been associated with an increased risk of

obesity during childhood and adulthood in some, although

not all, studies.6–10 There is limited evidence regarding the

long-term impact of fetal exposure to maternal smoking on

the risk of chronic disease in adulthood, which emerges as a

new focus of research interests.11

Gestational diabetes mellitus (GDM) is a common preg-

nancy complication characterized by glucose intolerance,

with onset or first recognition during pregnancy.12 GDM is

not only associated with short-term adverse perinatal out-

comes,13 but also related to long-term metabolic risk in both

mothers and their children.12,14,15 Thus, it is crucial to iden-

tify modifiable risk factors that may contribute to the preven-

tion of GDM in current and subsequent generations.

Animal studies have suggested that fetal exposure to maternal

smoking may lead to impaired glucose metabolism by alter-

ing pancreatic islet development and inducing beta cell apop-

tosis.16,17 In addition, epidemiological studies, although still

limited, suggest that maternal smoking during pregnancy

may increase the risk of diabetes in adulthood.18,19 However

the association, in particular the dose-response relation, be-

tween fetal exposure to maternal smoking and risk of GDM

is not well established. Moreover, no previous study has

examined the association between fetal exposure to paternal

smoking, a major source of maternal passive smoking, and

subsequent risk of GDM. In this study, we aimed to examine

the dose-response relation of maternal and/or paternal smok-

ing during pregnancy with risk of GDM in the daughter.

Methods

Study population

The Nurses’ Health Study II (NHSII) is an ongoing prospect-

ive cohort study of 116 430 female nurses aged 24–44 years

at study inception in 1989. The participants receive a biennial

questionnaire regarding lifestyle behaviours, anthropometric

variables and disease outcomes. In 2001, mothers of the

NHSII participants were invited to complete a questionnaire

regarding their nurse daughter. Details about the Nurses’

Mothers’ Cohort Study have been described elsewhere.20 We

included NHSII participants in the current analyses if they re-

ported at least one singleton pregnancy lasting greater than 6

months between 1989 and 2001 and their mothers partici-

pated in the Nurses’ Mothers’ Cohort Study and reported

data on pregnancy and perinatal variables associated with

the nurse daughter. The NHSII participants were excluded if

they had been adopted, were missing information on mater-

nal smoking or had type 2 diabetes reported in 1989 or be-

fore GDM. Figure 1 depicts the flowchart of study

participants. This study has been approved by the Partners

Human Research Committee (Boston, MA), with partici-

pants’ consent implied by the return of the completed

questionnaires.

Assessment of parental smoking

We used information on parental smoking during pregnancy

from the 2001 Nurses’ Mothers’ Cohort Study question-

naire.21 The mothers reported whether they ever smoked

cigarettes during pregnancy with the nurse daughter, the

number of cigarettes (i.e. 1–14, 15–24, 25–34 or� 35) they

Key Messages

• This study examined the association of parental smoking during pregnancy with risk of gestational diabetes in the

daughter among 15 665 singleton pregnancies from 10 152 women in the Nurses’ Health Study II cohort whose moth-

ers participated in the Nurses’ Mothers’ Cohort Study.

• We demonstrated that maternal heavy smoking (�25 cigarettes/day) during pregnancy was associated with higher risk of gestational diabetes in the daughter. We did not observe an association between paternal smoking during

pregnancy and risk of gestational diabetes in the daughter.

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smoked daily during pregnancy, whether they quit smoking

during pregnancy, and if so, in which trimester. In a separ-

ate validation study, the validity of recalled maternal smok-

ing during pregnancy was found to be high in the National

Collaborative Perinatal Project (sensitivity¼0.86, specifi- city¼0.94).22 We categorized maternal smoking as: never smoked; quit smoking in first trimester of pregnancy; con-

tinued smoking 1–14 cigarettes/day during pregnancy; con-

tinued smoking 15–24 cigarettes/day during pregnancy; and

continued smoking 25 or more cigarettes/day during preg-

nancy. We also asked the mothers whether the nurse’s father

ever smoked during pregnancy and the number of cigarettes

he smoked. We categorized paternal smoking as: never

smoked; smoked 1–14 cigarettes/day during pregnancy;

smoked 15–24 cigarettes/day during pregnancy; and

smoked 25 or more cigarettes/day during pregnancy.

Previous studies based on the same cohort as the current

analysis have found maternal smoking during pregnancy be

associated with an increased risk of overweight and obesity

in the daughter across adolescence and adult life.7

Ascertainment of gestational diabetes

The NHSII participants (i.e. the daughters) reported preva-

lent GDM in 1989 and incident GDM on each biennial

questionnaire through 2001. GDM was not ascertained

after the 2001 questionnaire in the NHSII cohort, because

the majority of NHSII participants had passed reproduct-

ive age by then. In a previous validation study among a

subgroup of the NHSII cohort, 94% of GDM self-reports

were confirmed by medical records.23 In a random sample

of parous women without GDM, 83% reported a glucose

screening test during pregnancy and 100% reported fre-

quent prenatal urine screenings, suggesting a high level of

GDM surveillance in this cohort.23

Covariates assessment

Covariates for maternal, paternal and perinatal characteris-

tics were obtained from the Nurses’ Mothers’ Cohort Study.

The 2001 Nurses’ Mothers’ Cohort Study questionnaire re-

quested data on the daughter’s gestational age at birth, birth-

weight and breastfeeding status, maternal and paternal age

at birth of the daughter, educational level, occupation and

home ownership at the time of the daughter’s birth, maternal

height, maternal pre-pregnancy weight, weight gain during

pregnancy (< 10, 10–14, 15–19, 20–29, 30–40, > 40

pounds; to convert pounds into kilograms, multiply pounds

by the conversion factor 0.453592.), paternal weight, pater-

nal height, maternal consumption of alcoholic beverages dur-

ing pregnancy, and the occurrence of maternal pregnancy

Nurses’ Health Study II cohort (n = 116 430)

Inclusion criteria: pregnancy ≥ 6 months 1989-2001 (NHSII)

(n = 10 862)

Exclusion criteria: • Nurses were adopted (NMS): n = 34 • Missing data on parental smoking (NMS): n = 643 • T2DM at baseline or before GDM (NHSII): n = 6 • Missing main questionnaire (NHSII): n = 33 • Missing data on the daughters’ smoking status

(NHSII): n = 76

Analytical population (n = 10 152)

Mothers participated in the Nurses’ Mothers’ Cohort Study

(n = 35 794)

Figure 1. The flowchart of study participants. Exclusion criteria are not mutually exclusive and individual reasons may not total the number of

excluded participants. GDM denotes gestational diabetes mellitus; NHSII, Nurses’ Health Study II; NMS, Nurses’ Mothers’ Cohort Study; T2DM, type

2 diabetes mellitus.

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complications (gestational diabetes and preeclampsia) during

the pregnancy of the daughter.

Covariates related to the daughters’ characteristics were

obtained from the NHSII questionnaires. The 1989 NHSII

questionnaire assessed the daughters’ age, height, race/ethni-

city and family history of diabetes at baseline. The daugh-

ters’ weight at 18 years old and current weight, parity, and

smoking status (including the number of cigarettes per day)

were self-reported from the 1989 NHSII questionnaire and

were updated with data from each biennial questionnaire

cycle. Self-reported weight was highly correlated with meas-

ured weight (r¼0.97) in a previous validation study.24

Body mass index (BMI) was computed as weight in kilo-

grams divided by height in metres squared. Dietary intake

was collected every 4 years since 1991 using a previously

validated semi-quantitative food frequency question-

naire.25–27 To assess the overall diet quality of the partici-

pants, we derived a diet score, the Alternate Healthy Eating

Index 2010 (AHEI-2010) for each participant, as previously

described.28 The overall AHEI-2010 ranged from 0 to 110

points, with a higher score indicating a better diet quality.

Physical activity was ascertained in 1989, 1991, 1997 and

2001 by frequency of engaging in common recreational

activities, from which metabolic equivalent (MET)-hours

per week were derived. The questionnaire-based estimates

of total physical activity correlated well with detailed activ-

ity diaries in a previous validation study (r¼0.56).29

Cumulative average of physical activity, total energy intake

and AHEI-2010 score were calculated for each individual at

each time period throughout the follow up, to reduce

within-subject variation and represent long-term habitual

diet and physical activity.30

Statistical analysis

We used log-binomial models with generalized estimating

equations to estimate the relative risks (RRs) and 95% confi-

dence intervals (CIs) of GDM for maternal and paternal

smoking, separately and jointly. Generalized estimating equa-

tions allowed us to account for correlations among repeated

observations (pregnancies) contributed by a single participant

(i.e. the nurse daughter). In the multivariable regression mod-

els, we adjusted for: age and race/ethnicity of the daughters

(Model 1); and additionally for maternal and paternal vari-

ables including maternal and paternal age at time of daugh-

ter’s birth, maternal pre-pregnancy BMI, paternal BMI,

maternal weight gain during pregnancy, maternal pregnancy

complications (gestational diabetes, preeclampsia) and mater-

nal alcohol consumption during pregnancy (Model 2); for the

daughters’ perinatal variables including gestational age at

birth, birthweight, and breastfeeding status (Model 3); for

the daughters’ adult life variables including parity, family

history of diabetes, cigarette smoking, total energy intake,

overall diet quality (i.e. Alternate Healthy Eating Index) and

physical activity (Model 4); for the daughters’ BMI at 18

years old (Model 5); and for the daughters’ pre-pregnancy

BMI (Model 6). We mutually adjusted for maternal and pa-

ternal smoking during pregnancy in all these models. Wald

tests were used to assess the differences between maternal

and paternal associations. The daughters’ BMI and other

adult life covariates were updated during the follow-up.

When categorizing each categorical covariate, we created a

category for missing data. We considered Model 3–Model 6

as sensitivity analyses, because the daughter’s perinatal vari-

ables, adult-life variables and adulthood BMI in these models

are potential intermediates or explanatory variables for the

associations of maternal and paternal smoking during preg-

nancy with the risk of GDM. Tests for linear trend were per-

formed across the categories of the number of cigarettes

smoked for mothers who continued to smoke throughout

pregnancy, with non-smoking during pregnancy as the refer-

ence group (for maternal smoking, the test for trend excluded

the category of mothers who quit smoking during preg-

nancy). Statistical analyses were performed using the SAS

statistical software version 9.2 (SAS Institute Inc., Cary, NC)

and the Stata statistical software version 14.0 (StataCorp LP,

College Station, TX).

Results

We included 15 665 singleton pregnancies from 10 152

women in the Nurses’ Health Study II cohort whose mothers

participated in the Nurses’ Mothers’ Cohort Study. Of them,

736 GDM pregnancies were documented. Characteristics of

mothers, fathers and daughters are shown in Table 1 accord-

ing to maternal smoking status during pregnancy. Mothers

who smoked more frequently during pregnancy were more

likely to consume alcoholic beverages during the pregnancy.

The biological fathers of the daughters whose mothers

smoked during pregnancy were also more likely to smoke

during the pregnancy. Women who were exposed to frequent

maternal smoking during pregnancy had a lower birthweight,

were less likely to be breastfed and were heavier and more

likely to smoke in adulthood.

We observed a dose-response relation between in utero

exposure to maternal smoking and risk of GDM (Table 2).

After adjustment for the daughter’s age, race/ethnicity and

maternal and paternal variables, the RRs (95% CIs) of GDM

among women whose mothers did not smoke during preg-

nancy or continued smoking 1–14, 15–24 or � 25 cigarettes/ day were 1.00 (reference), 1.05 (0.81–1.35), 1.27

(0.95–1.70) and 1.98 (1.18–3.30), respectively (P for

trend¼0.02). Further adjustment for the daughter’s perinatal variables and adult life variables, including pre-pregnancy

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BMI, only slightly changed the association. No association

was observed between paternal smoking during pregnancy

and the risk of GDM (Table 3). Wald tests showed suggestive

statistical evidence that the maternal smoking associations

may differ from the paternal smoking associations with

GDM risk (P¼0.10). We further examined the joint effect of both maternal and paternal smoking during pregnancy on

the risk of GDM. Women whose mother or both parents

smoked during pregnancy � 15 cigarettes/day had a higher risk of GDM (RR 1.43, 95% CI 1.11–1.85), compared with

women whose parents did not smoke during pregnancy or

smoked < 15 cigarettes/day (Supplementary Figure 1, avail-

able as Supplementary data at IJE online).

In an analysis on the joint effect of maternal smoking

during pregnancy and the participants’ smoking during

adulthood, we found that the women who smoked < 15

cigarettes/day and whose mothers smoked � 15 cigarettes/ day during pregnancy had an RR (95% CI) of 1.28 (1.00–

1.64) for GDM, compared with neither the mothers nor

the participants smoking � 15 cigarettes/day (Figure 2). We also performed a stratified analysis according to the

daughters’ own smoking status. Among the daughters who

never smoked, the adjusted RRs (95% CIs) of GDM were

1.30 (0.79–2.13), 0.94 (0.67–1.32), 1.13 (0.77–1.65) and

2.15 (1.19–3.88) for the daughters whose mothers smoked

but quit smoking in the first trimester, continued smoking

Table 1. Age-standardized maternal, paternal, and the daughter’s characteristics by maternal smoking status during pregnancya

Maternal cigarette smoking during pregnancy

Non-smoker Quit smoking in

the first trimester

Continued smoking

1–14 cigarettes/day

Continued

smoking 15–24

cigarettes/day

Continued smoking

�25 cigarettes/day

Number of participants 7478 373 1369 793 139

Maternal characteristics

Age at daughter’s birth (years) 26.68 (4.83) 25.33 (4.34) 26.39 (4.75) 26.23 (4.66) 26.90 (4.65)

Prepregnancy BMI (kg/m2) 21.41 (2.60) 21.00 (2.26) 20.88 (2.46) 21.09 (2.70) 21.24 (2.61)

Attended college (%) 40.21 47.11 43.04 40.89 46.57

Ever consumed alcoholic beverages

during pregnancy (%)

25.03 44.82 60.43 63.59 63.68

Pregnancy complicationsb (%) 4.03 4.26 3.90 3.84 3.44

Paternal characteristics

Age at daughter’s birth (years) 28.70 (4.78) 27.85 (4.68) 28.59 (4.67) 28.57 (4.64) 29.63 (4.52)

BMI at daughter’s birth (kg/m2) 23.80 (2.81) 23.86 (3.08) 23.78 (2.80) 23.72 (2.83) 23.40 (2.75)

Attended college (%) 45.90 54.68 51.51 48.45 57.90

Ever smoked during pregnancy (%) 44.61 71.72 73.86 78.26 74.26

Characteristics of the daughter in early life

Gestational age at birth (weeks) 39.42 (2.26) 39.55 (2.32) 39.32 (2.40) 39.12 (2.54) 39.25 (2.54)

Birthweight (g) 3358.28 (493.41) 3291.89 (491.44) 3176.63 (498.50) 3070.21 (514.39) 3056.42 (523.58)

Caucasian (%) 95.05 95.42 96.03 95.84 95.86

Breastfed during infancy (%) 43.46 47.81 32.07 34.65 23.07

Characteristics of the daughter

during adulthoodc

Age in 1989 (years) 30.62 (3.42) 30.57 (3.27) 30.85 (3.42) 30.33 (3.31) 30.40 (3.29)

BMI (kg/m2) 22.81 (3.93) 23.01 (4.01) 22.87 (3.64) 23.32 (4.13) 23.64 (4.66)

Nulliparous (%) 7.68 7.50 6.02 8.21 5.81

Family history of diabetes (%) 10.08 8.51 8.60 7.55 7.88

Current smoking (%) 6.54 11.06 10.86 11.36 10.95

Alcohol intake (g/day) 2.55 (4.67) 3.15 (4.79) 3.42 (5.74) 3.30 (5.66) 3.33 (6.12)

Physical activity (MET-h/week) 25.88 (36.49) 26.26 (38.56) 27.59 (37.17) 28.19 (44.22) 28.31 (34.78)

Total energy intake (kcal/day) 1882.42 (545.50) 1837.95 (522.48) 1871.40 (549.03) 1850.16 (540.46) 1873.85 (559.33)

AHEI-2010d 47.42 (10.67) 48.72 (10.70) 48.38 (11.09) 48.08 (10.56) 47.85 (10.75)

AHEI-2010 indicates Alternate Healthy Eating Index 2010; BMI, body mass index; MET, metabolic equivalent. aValues are means (standard deviations) for continuous variables and percentages for categorical variables and are standardized to age distribution of the

NHSII participants (i.e. the daughters). bMaternal pregnancy complications included gestational diabetes and preeclampsia. cAdulthood characteristics are provided for 1989, except diet information (i.e. total energy intake, alcohol intake and the derived alternate healthy eating

index) which was first collected in the Nurses’ Health Study II cohort in 1991. dAHEI-2010 was derived for each participant, as previously describe,28 to assess the overall diet quality of the participants.

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