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Maternal Smoking During Pregnancy and Metabolic Syndrome in Their Children
Maternal Smoking During Pregnancy and Metabolic Syndrome in Their Children Nuananong Seal, PhD, RN, Glenn Krakower, PhD, and John Seal, MS ABSTRACT The purpose of this review is to provide the evidence that demonstrates a significant association between prenatal cigarette smoke exposure and the risk for metabolic syndrome (MetS). The PubMed database was searched for papers published from 1995 through 2012 to identify original human studies that related maternal smoking during pregnancy to MetS in their children. The relationships among maternal smoking during pregnancy and their child’s high blood cholesterol levels, high blood pressure, and high waist circumferences are identified. Stronger associations were reported in children with higher body mass index and those who reported smoking as adults. Keywords: children, hyperlipidemia, hypertension, maternal smoking, metabolic syndrome, pregnancy, waist circumferences Ó 2013 Elsevier, Inc. All rights reserved.
C
hildhood obesity is a major public health problem in the United States and worldwide. The prevalence of obesity among US children and adolescents has almost tripled since 1980, with an estimated 12.5 million (approximately 17%) considered obese.1 The prevalence of obesity has increased even in very young children, from 5% in 1980 to 10.4% in 2008 among preschool children (2-5 years old).1 Evidence indicates that maternal smoking during pregnancy is associated with a 50% higher risk of childhood obesity.2 Two recent meta-analyses reported an association between maternal smoking during pregnancy and childhood obesity (body mass index [BMI] 95th percentile), with respective pooled adjusted odds ratios of 1.50; 95% confidence interval (CI): 1.36, 1.65 (based upon 14 studies)2 and 1.64; 95% CI: 1.42, 1.90 (based upon 16 studies).3 A National Toxicology Program Workshop Review reported that maternal smoking also increases the risk of adult-onset diseases, including metabolic syndrome (MetS), type 2 diabetes, and cardiovascular disease (CVD) in the children of women who smoked during pregnancy, after adjustment for confounders that include birth weight, gestational age, www.npjournal.org
socioeconomic status, and maternal factors.4 This suggests that the associations between maternal smoking and increased risks for childhood obesity and other adverse health outcomes may directly result from intrauterine exposure to the chemicals in cigarette smoke.5,6 The prevalence of MetS in US adults was recently estimated as 34%.7 There is increasing concern that children exposed to cigarette smoke in utero may also have increased risk for MetS. The condition is characterized by a clustering of risk factors that include abdominal obesity, high blood pressure (BP), elevated serum glucose levels, and abnormal serum lipid profile.8 MetS is associated with the development of diabetes and CVD, as well as all-cause mortality.8-10 The National Cholesterol Education Program’s Adult Treatment Panel III report (ATP III) has recommended clinical criteria for the diagnosis of adult MetS11 (Table 1). Since there is no consensus over the definition of childhood MetS, adult MetS criteria have been used in pediatric studies. Among the women giving birth in the US, approximately 480,000 women (12%) reported having smoked during pregnancy.12 For that reason it is The Journal for Nurse Practitioners - JNP
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important to better understand the associations between in utero exposure to cigarette smoke and the risk factors for MetS in order to guide future research toward the development of prevention strategies. This article reviews existing evidence from original human studies that demonstrate a significant association between prenatal cigarette smoke exposure and the risk factors for MetS.
come to an agreement. We used standardized data extraction forms to record the following information: last name of the first author, publication year, setting, population, number of participants, exposure assessment, study outcomes, and risk for developing MetS with corresponding 95% CI. Studies that did not meet the inclusion criteria or that met any exclusion criterion were excluded.
METHODS Data Sources and Study Selection
RESULTS
The PubMed database (http://www.ncbi.nlm.nih. gov/pubmed) was searched for papers published from 1995 through 2012 to identify human studies that related maternal smoking during pregnancy to their offspring’s a) high BP, hypercholesterolemia, dyslipidemia, insulin resistance, glycemic control, or metabolic syndrome; and b) high waist circumference (WC) or abdominal obesity after infancy ( 1 year old). The Medical Subject Headings (MeSH) and keyword strategies were used to identify the studies. Search terms and keywords used to identify those studies include but were not limited to the following: maternal smoking, pregnancy, prenatal exposure, abdominal obesity, glucose, insulin resistance, hypertension, metabolic syndrome, syndrome X, and cardiometabolic syndrome. The combination of the terms was also searched using the Boolean operators. Studies were excluded if: They were secondary data or represented an editorial, commentary, or a literature review After adjustment for confounders, they neither detected nor reported associations between maternal smoking during pregnancy and any risk factors for MetS in offspring in their final findings (null) The population consisted of specific subgroups (eg, preterm, very low-birth weight or high-birth weight infants, mothers or infants with health condition or disease) or were based upon twins They were not published in English Data Extraction
Two reviewers independently evaluated all relevant articles and identified eligible studies from the database. During data extraction, differences and disagreements were resolved through discussion to 696
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Of the 255 published articles identified, 9 studies with original data that met the inclusion criteria were selected and included in review (Figure 1). We used the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement13 to determine the quality of data reporting in the papers. The STROBE Statement is a checklist of items that should be addressed in articles reporting on the 3 main study designs of analytical epidemiology, including cohort, case control, and cross-sectional studies (Table 2). Details of the authors, year of publications, study design, setting, populations, age and number of subjects, gender, methods used to assess maternal smoking, findings, and adjustment for confounders are presented in Table 3. The selected studies, published between 2000 and 2012, included a combined 94,311 offspring participants (offspring sample sizes ranged from 328 to 74,023) from different populations (4 studies in Australia and 1 each in Brazil, the Netherlands, Norway, the United Kingdom, and the US). Offspring age ranged from 3 to 47 years. Most studies used a prospective cohort design. Exposure to maternal smoking was assessed by one of the following methods: interview, selfreport survey, or questionnaire. In the offspring of women who smoked during pregnancy, 3 of the 9 studies reported significantly lower levels of high-density lipoprotein (HDL) cholesterol,14-16 4 reported higher systolic BP and hypertension,17-20 and 2 reported higher WC.21,22 Maternal Smoking During Pregnancy and Lower Levels of HDL Cholesterol in Offspring
Three studies support the association between maternal smoking during pregnancy and lower HDL cholesterol levels in their offspring (Table 3). HDL Volume 9, Issue 10, November/December 2013
Table 1. ATP III Clinical Criteria for Metabolic Syndrome Risk Factors
Defining Level
Abdominal obesity, given as waist circumference Men
> 102 cm (> 40 in)
Women
> 88 cm (> 35 in)
Triglycerides
150 mg/dL
HDL cholesterol Men
< 40 mg/dL
Women
< 50 mg/dL
Blood pressure
130/ 85 mm Hg
Fasting glucose
110 mg/dL
Data from the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults.11
cholesterol levels were significantly lower in these children compared with those whose mothers did not smoke during pregnancy, although 1 study found significance only in the female offspring.15 In addition, 1 study reported a significantly positive
association between maternal smoking during pregnancy and the levels of low-density lipoprotein (LDL) cholesterol in offspring, both before and after controlling for offspring current height, smoking habits, and alcohol consumption.16 Potential confounders and factors affecting HDL cholesterol levels in the 3 studies include birth weight, child’s current BMI,13 physical activity, personal smoking, alcohol consumption, and WC.15,16 The studies include females and males, as well as children and adults (8 to 46 years old). Within these studies the sample sizes of the offspring varied from 328 to 3824, and the length of follow-up varied from 8 to 23 years. In each study, information on smoking during pregnancy was collected from the mothers after delivery by using a questionnaire. Cholesterol levels were tested in non-fasting blood samples in all studies. The investigators noted that the minimal variation in the total and HDL cholesterol levels found between fasting and non-fasting methods did not significantly affect the results of these studies.14-16,23,24
Figure 1. Flow diagram showing the number of studies included in and excluded from review.
255 articles identified for full text review.
246 articles excluded because: a) abstract, review, commentary or repeated data articles (n = 84); b) target only obesity, overweight, or include abnormal subgroups (n = 116); and c) do not detect or report associations between maternal smoking during pregnancy and the risk factors for MetS in offspring (n = 37).
18 articles identified for full text review.
9 articles excluded (n = 9) because of incomplete data (ie, no information about setting, no information about the methods used to assess maternal smoking).
9 articles identified and included in review.13-21
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Table 2. STROBE Statement Checklist for Reports Item Title and abstract
Number
Recommendation
1
A. Indicate the study’s design with a commonly used term in the title or the abstract B. Provide in the abstract an informative and balanced summary of what was done and what was found
Introduction Background/ rationale
2
Explain the scientific background and rationale for the investigation being reported
Objectives
3
State specific objectives, including any prespecified hypotheses
Study design
4
Present key elements of study design early in the paper
Setting
5
Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data collection
Participants
6
A. Give the eligibility criteria and the sources and methods of selection of participants. Describe methods of follow-up
Methods
B. For matched studies, give matching criteria and number of exposed and unexposed Variables
7
Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if applicable
Data sources/ measurement
8a
For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe comparability of assessment methods if there is more than 1 group
Bias
9
Describe any efforts to address potential sources of bias
Study size
10
Explain how the study size was determined
Quantitative variables
11
Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and why
Statistical methods
12
A. Describe all statistical methods, including those used to control for confounding B. Describe any methods used to examine subgroups and interactions C. Explain how missing data were addressed D. If applicable, explain how loss to follow-up was addressed E. Describe any sensitivity analyses
Results Participants
13a
A. Report numbers of individuals at each stage of study (eg, numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed) B. Give reasons for non-participation at each stage C. Consider use of a flow diagram
Descriptive data
a
14
A. Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential confounders B. Indicate number of participants with missing data for each variable of interest C. Summarize follow-up time (eg, average and total amount)
Outcome data
15a
Report numbers of outcome events or summary measures over time continued
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Table 2. (continued ) Item Main results
Number
Recommendation
16
A. Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% CI). Make clear which confounders were adjusted for and why they were included B. Report category boundaries when continuous variables were categorized C. If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period
Other analyses
17
Report other analyses done (eg, analyses of subgroups and interactions and sensitivity analyses)
Key results
18
Summarize key results with reference to study objectives
Limitations
19
Discuss limitations of the study, taking into account sources of potential bias or imprecision. Discuss both direction and magnitude of any potential bias
Interpretation
20
Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from similar studies, and other relevant evidence
Generalizability
21
Discuss the generalizability (external validity) of the study results
22
Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on which the present article is based
Discussion
Other information Funding a
Give information separately for exposed and unexposed groups. Data from von Elm et al.13 The STROBE checklist is freely available at http://www.plosmedicine.org/article/info%3Adoi%2F10.1371%2Fjournal.pmed.0040296. Information on the STROBE Initiative is available at http://www.strobe-statement.org.
Maternal Smoking During Pregnancy and Offspring High BP
Of the 9 studies evaluated, 4 reported a significant association between maternal smoking during pregnancy and high BP in offspring17-20 (Table 3). Although the increases were small, children of mothers who smoked showed higher systolic17-20 and diastolic BPs17 than those born to mothers did not smoke during pregnancy. Birth weight is a key confounder for high systolic BP and is independent of maternal smoking during pregnancy.17,19 However, 1 study reported that systolic BP in children of mothers who smoked in pregnancy increased with age, independent of restricted growth.20 In addition, the child’s weight and height at age 5 and parental BMI were all independently associated with the child’s systolic BP.19 Other potential confounders, including the child’s BMI, maternal education, income, race/ ethnicity, breastfeeding, and offspring lifestyle pattern, only minimally influenced effect sizes.19,20 One study indicated that women who quit smoking during pregnancy could prevent the adverse www.npjournal.org
effect on offspring BP.19 All studies used systolic BP of the offspring as primary outcome because of its superior prediction of later BP25 and its correlation with diastolic BP.19 All studies used a prospective cohort design, but 1 study was cross-sectional.18 Information on the exposure to smoking during pregnancy was collected from the mothers after delivery,17,19-20 but 1 study conducted surveys from the offspring along with their mothers at the time of data collection and validated these results with the Medical Birth Registry.18 Among these studies, the sample sizes of the offspring varied from 689 to 74,023, and the length of follow-up varied from 0 to 6 years. Maternal Smoking During Pregnancy and Offspring High WC
Many previous studies have examined the association between maternal smoking during pregnancy and BMI in their offspring,26-27 but little is known about any associations between maternal smoking and WC in the offspring. Longitudinal studies detailing the development of abdominal obesity are rare, and it’s The Journal for Nurse Practitioners - JNP
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Table 3. Summary of Studies that Demonstrate Associations Between Prenatal Smoke Exposure and MetS Risk MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
14
1-22
Authors
Ayer et al, 2011
Design
Prospective study
Setting
Australia
Population
Healthy children (female/male)
Age (years)
8
Sample size
328
Assessment of maternal smoking
Questionnaire
Findings
-0.14 mmol/L 95% CI: -0.36 to -0.08; P ¼ 0.0003
Confounders
Postnatal exposure, gender, breastfeeding duration, physical inactivity, and adiposity
MetS Risk Factor: Low HDL Cholesterol Authors
Horta et al, 201115
Design
Prospective study
Setting
Brazil
Population
Adults (female)
Age (years)
23
Sample size
3824
Assessment of maternal smoking
Interview
Findings
-2.10 to -1.03 mg/dL; P ¼ 0.002
Confounders
Birth weight, body mass index (BMI), waist circumference (WC), lifestyle, self-smoking
1-22
MetS Risk Factor: Low HDL Cholesterol Authors
Jaddoe et al, 200716
1-21a
Design
Prospective cohort study
Setting
Netherlands
Population
Adults (female/male)
Age (years)
32-46
Sample size
350
Assessment of maternal smoking
Questionnaire
Findings
-0.05 mmol/L per 10 years; 95% CI:-0.11 to 0; P < .05
Confounders
Current weight and height, number of cigarettes, and current alcohol consumption are associated with the levels of HDL but not low-density lipoprotein (LDL), birth weight, child current weight, and socioeconomic status (SES) continued
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Table 3. (continued ) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High LDL Cholesterol Authors
Jaddoe et al, 200716
1-21a
Design
Prospective cohort study
Setting
Netherlands
Population
Adults (female/male)
Age (years)
32-46
Sample size
350
Assessment of maternal smoking
Questionnaire
Findings
0.19 mmol/L per 10 years; 95% CI:-0.05 to 0.43
Confounders
Current weight and height, number of cigarettes, birth weight, child current weight, and SES
MetS Risk Factor: High Blood Pressure Authors
Blake et al, 200017
Design
Prospective study
Setting
Australia
Population
Children (female/male)
Age (years)
6
Sample Size
1708
Assessment of maternal smoking
Questionnaire
Findings
With 20 cigarettes smoked: systolic blood pressure 3.4 mmHg higher, 95% CI: -0.5 to 7.4; diastolic blood pressure 2.2 mmHg higher, 95% CI: -1.6 to 6.0
Confounders
Birth weight, child current weight, and SES
1-22
MetS Risk Factor: High Blood Pressure Authors
Cupul-Uicab et al, 201118
Design
Cross-sectional study
Setting
Norway
Population
Pregnant offspring with 17-18 weeks of gestation (female)
Age (years)
14-47
Sample size
74023
Assessment of maternal smoking
Self-report (yes/no) by the offspring
Findings
Systolic blood pressure 1.68 mmHg higher, 95% CI: 1.19 to 2.39
Confounders
Birth weight, BMI, age, education, and self-smoking
1-22
continued
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Table 3. (continued) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High Blood Pressure Authors
Lawlor et al, 200419
Design
Prospective cohort study
Setting
Australia
Population
Healthy children (female/male)
Age (years)
5
Sample size
3864
Assessment of maternal smoking
Interview (yes/no)
Findings
Systolic blood pressure 0.88 mmHg higher, 95% CI: 0.14 to 1.64
Confounders
Age, gender, birth weight, and weight and height at 5 years old, maternal age, education, income
1-22
MetS Risk Factor: High Blood Pressure Authors
Oken et al, 200520
Design
Prospective cohort study
Setting
USA
Population
Children (female/male)
Age (years)
3
Sample size
689
Assessment of maternal smoking
Interview and questionnaire
Findings
Systolic blood pressure 2.4 mmHg higher, 95% CI: -0.01 to 4.9 1.5 mmHg higher, 95% CI: -1.0 to 3.9 after adjustment of child BMI
Confounders
Maternal socioeconomics, gestational age, child age, gender, height
1-22
MetS Risk Factor: High Waist Circumference Authors
Mamun et al, 201221
Design
Prospective cohort study
Setting
Australia
Population
Adults (female/male)
Age (years)
21
Sample Size
2038
Assessment of maternal smoking
Self-report (yes/no)
Findings
WC 2.12 cm higher, 95% CI: 1.02 to 3.22
Confounders
Birth weight, breastfeeding, gender, diet, physical activity, maternal age, education, pre-pregnancy BMI
1-22
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Table 3. (continued ) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High Waist Circumference
a
Authors
Power et al, 201022
Design
Prospective cohort study
Setting
United Kingdom
Population
Adults (female/male)
Age (years)
45
Sample size
8815
Assessment of maternal smoking
Interview
Findings
WC 1.76 cm higher, 95% CI: 1.20 to 2.33
Confounders
Social class, maternal BMI, number of cigarettes smoked, education, birth weight, breastfeeding, diet, physical activity
1-22
No funding source is reported.
even scarcer to discuss it in children. Two of these 9 studies reported that both the male and female offspring of mothers who smoked during pregnancy had greater mean WC (Table 3) compared to those of the mothers who never smoked.21,22 Another study reported a significant positive association between maternal smoking during pregnancy and mean waist-hip ratio (WHR) in offspring at 21 years.21 The authors found no significant differences in either mean WC or WHR between the offspring of the mothers who smoked before or after pregnancy, versus those of the mothers who never smoked.21 In addition, mean WC in the offspring of mothers who quit smoking after the 4th month of pregnancy did not differ from those of the mothers who never smoked.22 Mamun et al21 reported that a majority of the participants were white, with high levels of education and income; unfortunately, no such information about participant characteristics was reported in the other study.22 No significant differences in mean WC between male and female offspring were found.21,22 Potential confounders and mediators included maternal pre-pregnancy BMI and dietary and physical activity patterns in their offspring.21,22 Doseresponse relationships between the number of cigarettes smoked during pregnancy and mean WC in the offspring were demonstrated in these www.npjournal.org
2 prospective cohort studies;21,22 1 followed both the mothers and their offspring till age 21,21 and the other followed the offspring to age 45.22 The sample sizes of the offspring were 2038 and 8815, respectively. Information on smoking during pregnancy was collected from the mothers at the first clinic visit22 and at birth21,22 by using self-report21 and interview22 surveys. DISCUSSION
According to the data from 9 selected studies, the relationships between maternal smoking during pregnancy and the risk of MetS in their offspring (low HDL and high LDL cholesterol levels, high systolic BP, and high WC) were evident. Stronger associations were reported in those offspring with higher BMI and in those who reported smoking in their adult lives.14,16-19,22 Among offspring exposed to maternal cigarette smoke during pregnancy, those with higher BMI are more likely to have lower HDL cholesterol, higher systolic BP, and higher WC.14-22 Some of these individuals demonstrated lower HDL cholesterol levels as early as age 8,14 higher systolic BP from 3 years,20 and higher WC by 21 years.21 Dose-response relationships between maternal smoking during pregnancy (number of cigarette smoked) and risk of MetS in their offspring have been documented in a number of studies.14-19,22 However, The Journal for Nurse Practitioners - JNP
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the information of cigarette smoke exposure in offspring in all 9 studies came from maternal self-report/ survey, which was often under-reported or biased by social pressure, particularly in pregnant women.28 Selfreports has been widely used to assess maternal smoking because it is convenient and inexpensive. Smoking assessment from pregnant women can be more accurate if questions about smoking are in open-ended than yesno questions.28 Objective measures of cigarettes smoked using salivary or urine cotinine may help to validate self-reported smoking status.29 The effects of smoking at different stages of pregnancy on the risk of MetS in offspring remain insufficient. One study indicated increased risk for MetS in the offspring exposed to maternal smoking after 4 months of gestation,22 while several failed to specify any stage of pregnancy. The effects of maternal smoking differentially affected distinct components of MetS in their offspring; for example, high BP in exposed children seems to be more pronounced in younger age, compared to cholesterol levels and WC.17-20 This suggests a distinct lifetime clustering of risks for offspring of mothers who smoked during pregnancy. Offspring lifestyle factors including smoking and alcohol consumption appear to synergistically increase the risk for MetS.14-16,22 The associations between maternal smoking during pregnancy, low HDL cholesterol levels, and high BP in their offspring remain strong after more than 20 years, suggesting that the effect of cigarette smoked exposure is long term. No significant gender and ethnic differences were detected across these 9 studies. CONCLUSIONS AND POLICY IMPLICATIONS
There is clearly a role for nurse practitioners and midwives in addressing health consequences of maternal smoking on their offspring. The importance of the early identification of children at risk for developing MetS must not be underestimated. Nurses need to be trained in interviewing techniques and improving trustworthy interpersonal relationship skill to elicit more accurate maternal smoking assessment. Knowing about the association between maternal smoking and the risk for MetS in children will enable nurses to better assess MetS risk and also provide personalized health care to individuals exposed to cigarette smoke. 704
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Given the extent of harmful cigarette use during pregnancy to the offspring, nurses and midwives are well positioned to deliver appropriate interventions in a broad range of settings such as primary health care, hospital, and antenatal care settings. Nurses and midwives can have a significant impact in reducing the risk of MetS in offspring; for example, they may conduct a routine screening of cigarette use in antenatal and postnatal care settings for early preventive interventions, provide education to pregnant women about potential harmful health effects of cigarette smoke exposure on their child, and make recommendations on policy to control cigarette use in pregnant women. References 1. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA. 2010;303(3):242-249. 2. Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond). 2008;32(2):201-210. 3. Ino T. Maternal smoking during pregnancy and offspring obesity: metaanalysis. Pediatr Inl. 2010;52(1):94-99. 4. Behl M, Rao D, Aagaard K, et al. Evaluation of the association between maternal smoking, childhood obesity, and metabolic disorders: a National Toxicology Program Workshop Review. Environ Health Perspect. 2013;121(2):170-180. 5. Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002;31(2):413-419. 6. Syme C, Abrahamowicz M, Mahboubi A, et al. Prenatal exposure to maternal cigarette smoking and accumulation of intra-abdominal fat during adolescence. Obesity (Silver Spring). 2010;18:1021-1025. 7. Ervin RB. Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003e2006. National Health Statistics Reports no 13. Hyattsville, MD: National Center for Health Statistics; 2009. 8. Grundy SM. Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol. 2008;28(4):629-636. 9. Türkoglu C, Duman BS, Günay D, Cagatay P, Ozcan R, Büyükdevrim AS. Effect of abdominal obesity on insulin resistance and the components of the metabolic syndrome: evidence supporting obesity as the central feature. Obes Surg. 2003;13(5):699-705. 10. Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among U.S. adults. Diabetes Care. 2004;27(10):2444-2449. 11. Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) Final Report. Circulation. 2002;106:3143. 12. Brown HL, Graves CR. Prenatal cigarette and marijuana smoking. Clin Obstetr Gynecol. 2013;56(1):107-113. 13. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61(4):344-349. 14. Ayer JG, Belousova E, Harmer JA, David C, Marks GB, Celermajer DS. Maternal cigarette smoking is associated with reduced high-density lipoprotein cholesterol in healthy 8-year-old children. Europ Heart J. 2011;32(19):2446-2453. 15. Horta BL, Gigante DP, Nazmi A, Silveira VM, Oliveira I, Victora CG. Maternal smoking during pregnancy and risk factors for cardiovascular disease in adulthood. Atherosclerosis. 2011;219(2):815-820. 16. Jaddoe VW, de Ridder MA, van den Elzen AP. Maternal smoking in pregnancy is associated with cholesterol development in the offspring: a 27-year followup study. Atherosclerosis. 2008;196:42-48. 17. Blake KV, Gurrin LC, Evans SF, et al. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev. 2000;57:137-147.
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18. Cupul-Uicab LA, Skjaerven R, Haug K, et al. Exposure to tobacco smoke in utero and subsequent plasma lipids, ApoB, and CRP among adult women in the MoBa cohort. Environ Health Perspect. 2012;120:1532-1537. 19. Lawlor DA, Najman JM, Sterne J, Williams GM, Ebrahim S, Smith GD. Associations of parental, birth, and early life characteristics with systolic blood pressure at 5 years of age: findings from the Mater-University study of pregnancy and its outcomes. Circulation. 2004;110:2417-2423. 20. Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res. 2005;13:2021-2028. 21. Mamun AA, O’Callaghan MJ, Williams GM, Najma JM. Maternal smoking during pregnancy predicts adult offspring cardiovascular risk factors e evidence from a community-based large birth cohort study. PLoS ONE. 2012;7(7):e41106. 22. Power C, Atherton K, Thomas C. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis. 2010;211(2):643-648. 23. Mora S, Rifai N, Buring JE, Ridker PM. Fasting compared with nonfasting lipids and apolipoproteins for predicting incident cardiovascular events. Circulation. 2008;118:993-1001. 24. Sidhu D, Naugler C. Fasting time and lipid levels in a community-based population: a cross-sectional study. Arch Intern Med. 2012;172(22):1707-1710. 25. Gillman MW, Cook NR. Blood pressure measurement in childhood epidemiological studies. Circulation. 1995;92:1049-1057. 26. Chen AM, Pennell ML, Klebanoff MA, Rogan WJ, Longnecker MP. Maternal smoking during pregnancy in relation to child overweight: follow-up to age 8 years. Int J Epidemiol. 2006;35:121-130. 27. Suzuki K, Ando D, Sato M, Tanaka T, Kondo N, et al. The association between maternal smoking during pregnancy and childhood obesity persists to the age of 9-10 years. J Epidemiol. 2009;19:136-142.
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28. Greenaway R, Mogg K, Bradley BP. Attentional bias for smoking-related information in pregnant women: relationships with smoking experience, smoking attitudes and perceived harm to foetus. Addict Behav. 2012;37(9):1025-1028. 29. Llaquet H, Pichini S, Joya X, et al. Biological matrices for the evaluation of exposure to environmental tobacco smoke during prenatal life and childhood. Anal Bioanal Chem. 2010;396:379-399.
Nuananong Seal, PhD, RN, is an assistant professor at the University of Wisconsin in Milwaukee and can be reached at [email protected]. Glenn Krakower, PhD, is director of the General Clinical Research Center/Clinical and Translational Science Institute Core Laboratory in the Medical College of Wisconsin in Milwaukee. John Seal, MS, is a scientific consultant. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/13/$ see front matter © 2013 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2013.07.009
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hildhood obesity is a major public health problem in the United States and worldwide. The prevalence of obesity among US children and adolescents has almost tripled since 1980, with an estimated 12.5 million (approximately 17%) considered obese.1 The prevalence of obesity has increased even in very young children, from 5% in 1980 to 10.4% in 2008 among preschool children (2-5 years old).1 Evidence indicates that maternal smoking during pregnancy is associated with a 50% higher risk of childhood obesity.2 Two recent meta-analyses reported an association between maternal smoking during pregnancy and childhood obesity (body mass index [BMI] 95th percentile), with respective pooled adjusted odds ratios of 1.50; 95% confidence interval (CI): 1.36, 1.65 (based upon 14 studies)2 and 1.64; 95% CI: 1.42, 1.90 (based upon 16 studies).3 A National Toxicology Program Workshop Review reported that maternal smoking also increases the risk of adult-onset diseases, including metabolic syndrome (MetS), type 2 diabetes, and cardiovascular disease (CVD) in the children of women who smoked during pregnancy, after adjustment for confounders that include birth weight, gestational age, www.npjournal.org
socioeconomic status, and maternal factors.4 This suggests that the associations between maternal smoking and increased risks for childhood obesity and other adverse health outcomes may directly result from intrauterine exposure to the chemicals in cigarette smoke.5,6 The prevalence of MetS in US adults was recently estimated as 34%.7 There is increasing concern that children exposed to cigarette smoke in utero may also have increased risk for MetS. The condition is characterized by a clustering of risk factors that include abdominal obesity, high blood pressure (BP), elevated serum glucose levels, and abnormal serum lipid profile.8 MetS is associated with the development of diabetes and CVD, as well as all-cause mortality.8-10 The National Cholesterol Education Program’s Adult Treatment Panel III report (ATP III) has recommended clinical criteria for the diagnosis of adult MetS11 (Table 1). Since there is no consensus over the definition of childhood MetS, adult MetS criteria have been used in pediatric studies. Among the women giving birth in the US, approximately 480,000 women (12%) reported having smoked during pregnancy.12 For that reason it is The Journal for Nurse Practitioners - JNP
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important to better understand the associations between in utero exposure to cigarette smoke and the risk factors for MetS in order to guide future research toward the development of prevention strategies. This article reviews existing evidence from original human studies that demonstrate a significant association between prenatal cigarette smoke exposure and the risk factors for MetS.
come to an agreement. We used standardized data extraction forms to record the following information: last name of the first author, publication year, setting, population, number of participants, exposure assessment, study outcomes, and risk for developing MetS with corresponding 95% CI. Studies that did not meet the inclusion criteria or that met any exclusion criterion were excluded.
METHODS Data Sources and Study Selection
RESULTS
The PubMed database (http://www.ncbi.nlm.nih. gov/pubmed) was searched for papers published from 1995 through 2012 to identify human studies that related maternal smoking during pregnancy to their offspring’s a) high BP, hypercholesterolemia, dyslipidemia, insulin resistance, glycemic control, or metabolic syndrome; and b) high waist circumference (WC) or abdominal obesity after infancy ( 1 year old). The Medical Subject Headings (MeSH) and keyword strategies were used to identify the studies. Search terms and keywords used to identify those studies include but were not limited to the following: maternal smoking, pregnancy, prenatal exposure, abdominal obesity, glucose, insulin resistance, hypertension, metabolic syndrome, syndrome X, and cardiometabolic syndrome. The combination of the terms was also searched using the Boolean operators. Studies were excluded if: They were secondary data or represented an editorial, commentary, or a literature review After adjustment for confounders, they neither detected nor reported associations between maternal smoking during pregnancy and any risk factors for MetS in offspring in their final findings (null) The population consisted of specific subgroups (eg, preterm, very low-birth weight or high-birth weight infants, mothers or infants with health condition or disease) or were based upon twins They were not published in English Data Extraction
Two reviewers independently evaluated all relevant articles and identified eligible studies from the database. During data extraction, differences and disagreements were resolved through discussion to 696
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Of the 255 published articles identified, 9 studies with original data that met the inclusion criteria were selected and included in review (Figure 1). We used the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement13 to determine the quality of data reporting in the papers. The STROBE Statement is a checklist of items that should be addressed in articles reporting on the 3 main study designs of analytical epidemiology, including cohort, case control, and cross-sectional studies (Table 2). Details of the authors, year of publications, study design, setting, populations, age and number of subjects, gender, methods used to assess maternal smoking, findings, and adjustment for confounders are presented in Table 3. The selected studies, published between 2000 and 2012, included a combined 94,311 offspring participants (offspring sample sizes ranged from 328 to 74,023) from different populations (4 studies in Australia and 1 each in Brazil, the Netherlands, Norway, the United Kingdom, and the US). Offspring age ranged from 3 to 47 years. Most studies used a prospective cohort design. Exposure to maternal smoking was assessed by one of the following methods: interview, selfreport survey, or questionnaire. In the offspring of women who smoked during pregnancy, 3 of the 9 studies reported significantly lower levels of high-density lipoprotein (HDL) cholesterol,14-16 4 reported higher systolic BP and hypertension,17-20 and 2 reported higher WC.21,22 Maternal Smoking During Pregnancy and Lower Levels of HDL Cholesterol in Offspring
Three studies support the association between maternal smoking during pregnancy and lower HDL cholesterol levels in their offspring (Table 3). HDL Volume 9, Issue 10, November/December 2013
Table 1. ATP III Clinical Criteria for Metabolic Syndrome Risk Factors
Defining Level
Abdominal obesity, given as waist circumference Men
> 102 cm (> 40 in)
Women
> 88 cm (> 35 in)
Triglycerides
150 mg/dL
HDL cholesterol Men
< 40 mg/dL
Women
< 50 mg/dL
Blood pressure
130/ 85 mm Hg
Fasting glucose
110 mg/dL
Data from the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults.11
cholesterol levels were significantly lower in these children compared with those whose mothers did not smoke during pregnancy, although 1 study found significance only in the female offspring.15 In addition, 1 study reported a significantly positive
association between maternal smoking during pregnancy and the levels of low-density lipoprotein (LDL) cholesterol in offspring, both before and after controlling for offspring current height, smoking habits, and alcohol consumption.16 Potential confounders and factors affecting HDL cholesterol levels in the 3 studies include birth weight, child’s current BMI,13 physical activity, personal smoking, alcohol consumption, and WC.15,16 The studies include females and males, as well as children and adults (8 to 46 years old). Within these studies the sample sizes of the offspring varied from 328 to 3824, and the length of follow-up varied from 8 to 23 years. In each study, information on smoking during pregnancy was collected from the mothers after delivery by using a questionnaire. Cholesterol levels were tested in non-fasting blood samples in all studies. The investigators noted that the minimal variation in the total and HDL cholesterol levels found between fasting and non-fasting methods did not significantly affect the results of these studies.14-16,23,24
Figure 1. Flow diagram showing the number of studies included in and excluded from review.
255 articles identified for full text review.
246 articles excluded because: a) abstract, review, commentary or repeated data articles (n = 84); b) target only obesity, overweight, or include abnormal subgroups (n = 116); and c) do not detect or report associations between maternal smoking during pregnancy and the risk factors for MetS in offspring (n = 37).
18 articles identified for full text review.
9 articles excluded (n = 9) because of incomplete data (ie, no information about setting, no information about the methods used to assess maternal smoking).
9 articles identified and included in review.13-21
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Table 2. STROBE Statement Checklist for Reports Item Title and abstract
Number
Recommendation
1
A. Indicate the study’s design with a commonly used term in the title or the abstract B. Provide in the abstract an informative and balanced summary of what was done and what was found
Introduction Background/ rationale
2
Explain the scientific background and rationale for the investigation being reported
Objectives
3
State specific objectives, including any prespecified hypotheses
Study design
4
Present key elements of study design early in the paper
Setting
5
Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data collection
Participants
6
A. Give the eligibility criteria and the sources and methods of selection of participants. Describe methods of follow-up
Methods
B. For matched studies, give matching criteria and number of exposed and unexposed Variables
7
Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if applicable
Data sources/ measurement
8a
For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe comparability of assessment methods if there is more than 1 group
Bias
9
Describe any efforts to address potential sources of bias
Study size
10
Explain how the study size was determined
Quantitative variables
11
Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and why
Statistical methods
12
A. Describe all statistical methods, including those used to control for confounding B. Describe any methods used to examine subgroups and interactions C. Explain how missing data were addressed D. If applicable, explain how loss to follow-up was addressed E. Describe any sensitivity analyses
Results Participants
13a
A. Report numbers of individuals at each stage of study (eg, numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed) B. Give reasons for non-participation at each stage C. Consider use of a flow diagram
Descriptive data
a
14
A. Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential confounders B. Indicate number of participants with missing data for each variable of interest C. Summarize follow-up time (eg, average and total amount)
Outcome data
15a
Report numbers of outcome events or summary measures over time continued
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Table 2. (continued ) Item Main results
Number
Recommendation
16
A. Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% CI). Make clear which confounders were adjusted for and why they were included B. Report category boundaries when continuous variables were categorized C. If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period
Other analyses
17
Report other analyses done (eg, analyses of subgroups and interactions and sensitivity analyses)
Key results
18
Summarize key results with reference to study objectives
Limitations
19
Discuss limitations of the study, taking into account sources of potential bias or imprecision. Discuss both direction and magnitude of any potential bias
Interpretation
20
Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from similar studies, and other relevant evidence
Generalizability
21
Discuss the generalizability (external validity) of the study results
22
Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on which the present article is based
Discussion
Other information Funding a
Give information separately for exposed and unexposed groups. Data from von Elm et al.13 The STROBE checklist is freely available at http://www.plosmedicine.org/article/info%3Adoi%2F10.1371%2Fjournal.pmed.0040296. Information on the STROBE Initiative is available at http://www.strobe-statement.org.
Maternal Smoking During Pregnancy and Offspring High BP
Of the 9 studies evaluated, 4 reported a significant association between maternal smoking during pregnancy and high BP in offspring17-20 (Table 3). Although the increases were small, children of mothers who smoked showed higher systolic17-20 and diastolic BPs17 than those born to mothers did not smoke during pregnancy. Birth weight is a key confounder for high systolic BP and is independent of maternal smoking during pregnancy.17,19 However, 1 study reported that systolic BP in children of mothers who smoked in pregnancy increased with age, independent of restricted growth.20 In addition, the child’s weight and height at age 5 and parental BMI were all independently associated with the child’s systolic BP.19 Other potential confounders, including the child’s BMI, maternal education, income, race/ ethnicity, breastfeeding, and offspring lifestyle pattern, only minimally influenced effect sizes.19,20 One study indicated that women who quit smoking during pregnancy could prevent the adverse www.npjournal.org
effect on offspring BP.19 All studies used systolic BP of the offspring as primary outcome because of its superior prediction of later BP25 and its correlation with diastolic BP.19 All studies used a prospective cohort design, but 1 study was cross-sectional.18 Information on the exposure to smoking during pregnancy was collected from the mothers after delivery,17,19-20 but 1 study conducted surveys from the offspring along with their mothers at the time of data collection and validated these results with the Medical Birth Registry.18 Among these studies, the sample sizes of the offspring varied from 689 to 74,023, and the length of follow-up varied from 0 to 6 years. Maternal Smoking During Pregnancy and Offspring High WC
Many previous studies have examined the association between maternal smoking during pregnancy and BMI in their offspring,26-27 but little is known about any associations between maternal smoking and WC in the offspring. Longitudinal studies detailing the development of abdominal obesity are rare, and it’s The Journal for Nurse Practitioners - JNP
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Table 3. Summary of Studies that Demonstrate Associations Between Prenatal Smoke Exposure and MetS Risk MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
14
1-22
Authors
Ayer et al, 2011
Design
Prospective study
Setting
Australia
Population
Healthy children (female/male)
Age (years)
8
Sample size
328
Assessment of maternal smoking
Questionnaire
Findings
-0.14 mmol/L 95% CI: -0.36 to -0.08; P ¼ 0.0003
Confounders
Postnatal exposure, gender, breastfeeding duration, physical inactivity, and adiposity
MetS Risk Factor: Low HDL Cholesterol Authors
Horta et al, 201115
Design
Prospective study
Setting
Brazil
Population
Adults (female)
Age (years)
23
Sample size
3824
Assessment of maternal smoking
Interview
Findings
-2.10 to -1.03 mg/dL; P ¼ 0.002
Confounders
Birth weight, body mass index (BMI), waist circumference (WC), lifestyle, self-smoking
1-22
MetS Risk Factor: Low HDL Cholesterol Authors
Jaddoe et al, 200716
1-21a
Design
Prospective cohort study
Setting
Netherlands
Population
Adults (female/male)
Age (years)
32-46
Sample size
350
Assessment of maternal smoking
Questionnaire
Findings
-0.05 mmol/L per 10 years; 95% CI:-0.11 to 0; P < .05
Confounders
Current weight and height, number of cigarettes, and current alcohol consumption are associated with the levels of HDL but not low-density lipoprotein (LDL), birth weight, child current weight, and socioeconomic status (SES) continued
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Table 3. (continued ) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High LDL Cholesterol Authors
Jaddoe et al, 200716
1-21a
Design
Prospective cohort study
Setting
Netherlands
Population
Adults (female/male)
Age (years)
32-46
Sample size
350
Assessment of maternal smoking
Questionnaire
Findings
0.19 mmol/L per 10 years; 95% CI:-0.05 to 0.43
Confounders
Current weight and height, number of cigarettes, birth weight, child current weight, and SES
MetS Risk Factor: High Blood Pressure Authors
Blake et al, 200017
Design
Prospective study
Setting
Australia
Population
Children (female/male)
Age (years)
6
Sample Size
1708
Assessment of maternal smoking
Questionnaire
Findings
With 20 cigarettes smoked: systolic blood pressure 3.4 mmHg higher, 95% CI: -0.5 to 7.4; diastolic blood pressure 2.2 mmHg higher, 95% CI: -1.6 to 6.0
Confounders
Birth weight, child current weight, and SES
1-22
MetS Risk Factor: High Blood Pressure Authors
Cupul-Uicab et al, 201118
Design
Cross-sectional study
Setting
Norway
Population
Pregnant offspring with 17-18 weeks of gestation (female)
Age (years)
14-47
Sample size
74023
Assessment of maternal smoking
Self-report (yes/no) by the offspring
Findings
Systolic blood pressure 1.68 mmHg higher, 95% CI: 1.19 to 2.39
Confounders
Birth weight, BMI, age, education, and self-smoking
1-22
continued
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Table 3. (continued) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High Blood Pressure Authors
Lawlor et al, 200419
Design
Prospective cohort study
Setting
Australia
Population
Healthy children (female/male)
Age (years)
5
Sample size
3864
Assessment of maternal smoking
Interview (yes/no)
Findings
Systolic blood pressure 0.88 mmHg higher, 95% CI: 0.14 to 1.64
Confounders
Age, gender, birth weight, and weight and height at 5 years old, maternal age, education, income
1-22
MetS Risk Factor: High Blood Pressure Authors
Oken et al, 200520
Design
Prospective cohort study
Setting
USA
Population
Children (female/male)
Age (years)
3
Sample size
689
Assessment of maternal smoking
Interview and questionnaire
Findings
Systolic blood pressure 2.4 mmHg higher, 95% CI: -0.01 to 4.9 1.5 mmHg higher, 95% CI: -1.0 to 3.9 after adjustment of child BMI
Confounders
Maternal socioeconomics, gestational age, child age, gender, height
1-22
MetS Risk Factor: High Waist Circumference Authors
Mamun et al, 201221
Design
Prospective cohort study
Setting
Australia
Population
Adults (female/male)
Age (years)
21
Sample Size
2038
Assessment of maternal smoking
Self-report (yes/no)
Findings
WC 2.12 cm higher, 95% CI: 1.02 to 3.22
Confounders
Birth weight, breastfeeding, gender, diet, physical activity, maternal age, education, pre-pregnancy BMI
1-22
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Table 3. (continued ) MetS Risk Factor: Low High-Density Lipoprotein (HDL) Cholesterol
Meet the STROBE Checklist
MetS Risk Factor: High Waist Circumference
a
Authors
Power et al, 201022
Design
Prospective cohort study
Setting
United Kingdom
Population
Adults (female/male)
Age (years)
45
Sample size
8815
Assessment of maternal smoking
Interview
Findings
WC 1.76 cm higher, 95% CI: 1.20 to 2.33
Confounders
Social class, maternal BMI, number of cigarettes smoked, education, birth weight, breastfeeding, diet, physical activity
1-22
No funding source is reported.
even scarcer to discuss it in children. Two of these 9 studies reported that both the male and female offspring of mothers who smoked during pregnancy had greater mean WC (Table 3) compared to those of the mothers who never smoked.21,22 Another study reported a significant positive association between maternal smoking during pregnancy and mean waist-hip ratio (WHR) in offspring at 21 years.21 The authors found no significant differences in either mean WC or WHR between the offspring of the mothers who smoked before or after pregnancy, versus those of the mothers who never smoked.21 In addition, mean WC in the offspring of mothers who quit smoking after the 4th month of pregnancy did not differ from those of the mothers who never smoked.22 Mamun et al21 reported that a majority of the participants were white, with high levels of education and income; unfortunately, no such information about participant characteristics was reported in the other study.22 No significant differences in mean WC between male and female offspring were found.21,22 Potential confounders and mediators included maternal pre-pregnancy BMI and dietary and physical activity patterns in their offspring.21,22 Doseresponse relationships between the number of cigarettes smoked during pregnancy and mean WC in the offspring were demonstrated in these www.npjournal.org
2 prospective cohort studies;21,22 1 followed both the mothers and their offspring till age 21,21 and the other followed the offspring to age 45.22 The sample sizes of the offspring were 2038 and 8815, respectively. Information on smoking during pregnancy was collected from the mothers at the first clinic visit22 and at birth21,22 by using self-report21 and interview22 surveys. DISCUSSION
According to the data from 9 selected studies, the relationships between maternal smoking during pregnancy and the risk of MetS in their offspring (low HDL and high LDL cholesterol levels, high systolic BP, and high WC) were evident. Stronger associations were reported in those offspring with higher BMI and in those who reported smoking in their adult lives.14,16-19,22 Among offspring exposed to maternal cigarette smoke during pregnancy, those with higher BMI are more likely to have lower HDL cholesterol, higher systolic BP, and higher WC.14-22 Some of these individuals demonstrated lower HDL cholesterol levels as early as age 8,14 higher systolic BP from 3 years,20 and higher WC by 21 years.21 Dose-response relationships between maternal smoking during pregnancy (number of cigarette smoked) and risk of MetS in their offspring have been documented in a number of studies.14-19,22 However, The Journal for Nurse Practitioners - JNP
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the information of cigarette smoke exposure in offspring in all 9 studies came from maternal self-report/ survey, which was often under-reported or biased by social pressure, particularly in pregnant women.28 Selfreports has been widely used to assess maternal smoking because it is convenient and inexpensive. Smoking assessment from pregnant women can be more accurate if questions about smoking are in open-ended than yesno questions.28 Objective measures of cigarettes smoked using salivary or urine cotinine may help to validate self-reported smoking status.29 The effects of smoking at different stages of pregnancy on the risk of MetS in offspring remain insufficient. One study indicated increased risk for MetS in the offspring exposed to maternal smoking after 4 months of gestation,22 while several failed to specify any stage of pregnancy. The effects of maternal smoking differentially affected distinct components of MetS in their offspring; for example, high BP in exposed children seems to be more pronounced in younger age, compared to cholesterol levels and WC.17-20 This suggests a distinct lifetime clustering of risks for offspring of mothers who smoked during pregnancy. Offspring lifestyle factors including smoking and alcohol consumption appear to synergistically increase the risk for MetS.14-16,22 The associations between maternal smoking during pregnancy, low HDL cholesterol levels, and high BP in their offspring remain strong after more than 20 years, suggesting that the effect of cigarette smoked exposure is long term. No significant gender and ethnic differences were detected across these 9 studies. CONCLUSIONS AND POLICY IMPLICATIONS
There is clearly a role for nurse practitioners and midwives in addressing health consequences of maternal smoking on their offspring. The importance of the early identification of children at risk for developing MetS must not be underestimated. Nurses need to be trained in interviewing techniques and improving trustworthy interpersonal relationship skill to elicit more accurate maternal smoking assessment. Knowing about the association between maternal smoking and the risk for MetS in children will enable nurses to better assess MetS risk and also provide personalized health care to individuals exposed to cigarette smoke. 704
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Given the extent of harmful cigarette use during pregnancy to the offspring, nurses and midwives are well positioned to deliver appropriate interventions in a broad range of settings such as primary health care, hospital, and antenatal care settings. Nurses and midwives can have a significant impact in reducing the risk of MetS in offspring; for example, they may conduct a routine screening of cigarette use in antenatal and postnatal care settings for early preventive interventions, provide education to pregnant women about potential harmful health effects of cigarette smoke exposure on their child, and make recommendations on policy to control cigarette use in pregnant women. References 1. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA. 2010;303(3):242-249. 2. Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond). 2008;32(2):201-210. 3. Ino T. Maternal smoking during pregnancy and offspring obesity: metaanalysis. Pediatr Inl. 2010;52(1):94-99. 4. Behl M, Rao D, Aagaard K, et al. Evaluation of the association between maternal smoking, childhood obesity, and metabolic disorders: a National Toxicology Program Workshop Review. Environ Health Perspect. 2013;121(2):170-180. 5. Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002;31(2):413-419. 6. Syme C, Abrahamowicz M, Mahboubi A, et al. Prenatal exposure to maternal cigarette smoking and accumulation of intra-abdominal fat during adolescence. Obesity (Silver Spring). 2010;18:1021-1025. 7. Ervin RB. Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003e2006. National Health Statistics Reports no 13. Hyattsville, MD: National Center for Health Statistics; 2009. 8. Grundy SM. Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol. 2008;28(4):629-636. 9. Türkoglu C, Duman BS, Günay D, Cagatay P, Ozcan R, Büyükdevrim AS. Effect of abdominal obesity on insulin resistance and the components of the metabolic syndrome: evidence supporting obesity as the central feature. Obes Surg. 2003;13(5):699-705. 10. Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among U.S. adults. Diabetes Care. 2004;27(10):2444-2449. 11. Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) Final Report. Circulation. 2002;106:3143. 12. Brown HL, Graves CR. Prenatal cigarette and marijuana smoking. Clin Obstetr Gynecol. 2013;56(1):107-113. 13. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61(4):344-349. 14. Ayer JG, Belousova E, Harmer JA, David C, Marks GB, Celermajer DS. Maternal cigarette smoking is associated with reduced high-density lipoprotein cholesterol in healthy 8-year-old children. Europ Heart J. 2011;32(19):2446-2453. 15. Horta BL, Gigante DP, Nazmi A, Silveira VM, Oliveira I, Victora CG. Maternal smoking during pregnancy and risk factors for cardiovascular disease in adulthood. Atherosclerosis. 2011;219(2):815-820. 16. Jaddoe VW, de Ridder MA, van den Elzen AP. Maternal smoking in pregnancy is associated with cholesterol development in the offspring: a 27-year followup study. Atherosclerosis. 2008;196:42-48. 17. Blake KV, Gurrin LC, Evans SF, et al. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev. 2000;57:137-147.
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18. Cupul-Uicab LA, Skjaerven R, Haug K, et al. Exposure to tobacco smoke in utero and subsequent plasma lipids, ApoB, and CRP among adult women in the MoBa cohort. Environ Health Perspect. 2012;120:1532-1537. 19. Lawlor DA, Najman JM, Sterne J, Williams GM, Ebrahim S, Smith GD. Associations of parental, birth, and early life characteristics with systolic blood pressure at 5 years of age: findings from the Mater-University study of pregnancy and its outcomes. Circulation. 2004;110:2417-2423. 20. Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res. 2005;13:2021-2028. 21. Mamun AA, O’Callaghan MJ, Williams GM, Najma JM. Maternal smoking during pregnancy predicts adult offspring cardiovascular risk factors e evidence from a community-based large birth cohort study. PLoS ONE. 2012;7(7):e41106. 22. Power C, Atherton K, Thomas C. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis. 2010;211(2):643-648. 23. Mora S, Rifai N, Buring JE, Ridker PM. Fasting compared with nonfasting lipids and apolipoproteins for predicting incident cardiovascular events. Circulation. 2008;118:993-1001. 24. Sidhu D, Naugler C. Fasting time and lipid levels in a community-based population: a cross-sectional study. Arch Intern Med. 2012;172(22):1707-1710. 25. Gillman MW, Cook NR. Blood pressure measurement in childhood epidemiological studies. Circulation. 1995;92:1049-1057. 26. Chen AM, Pennell ML, Klebanoff MA, Rogan WJ, Longnecker MP. Maternal smoking during pregnancy in relation to child overweight: follow-up to age 8 years. Int J Epidemiol. 2006;35:121-130. 27. Suzuki K, Ando D, Sato M, Tanaka T, Kondo N, et al. The association between maternal smoking during pregnancy and childhood obesity persists to the age of 9-10 years. J Epidemiol. 2009;19:136-142.
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28. Greenaway R, Mogg K, Bradley BP. Attentional bias for smoking-related information in pregnant women: relationships with smoking experience, smoking attitudes and perceived harm to foetus. Addict Behav. 2012;37(9):1025-1028. 29. Llaquet H, Pichini S, Joya X, et al. Biological matrices for the evaluation of exposure to environmental tobacco smoke during prenatal life and childhood. Anal Bioanal Chem. 2010;396:379-399.
Nuananong Seal, PhD, RN, is an assistant professor at the University of Wisconsin in Milwaukee and can be reached at [email protected]. Glenn Krakower, PhD, is director of the General Clinical Research Center/Clinical and Translational Science Institute Core Laboratory in the Medical College of Wisconsin in Milwaukee. John Seal, MS, is a scientific consultant. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/13/$ see front matter © 2013 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2013.07.009
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