Abstract
Background:
This study aimed to evaluate the association of the lifelong duration of breast feeding with metabolic syndrome (MetS) and its components in Korean parous women aged 19–50 years.
Materials and Methods:
A total of 4724 participants from the Korean National Health and Nutritional Survey were included. Subjects were divided into four groups according to the duration of breast feeding: ≤5, 6–11, 12–23, or ≥24 months groups. The adjusted odds ratios (ORs) of MetS and its components were assessed according to the duration of breast feeding.
Results:
Women who breastfed for 6–11 months had an OR of 0.67 (95% confidence interval [CI], 0.54–0.86) for elevated blood pressure (BP) compared with those who breastfed for ≤5 months after adjustment for possible confounders in a multivariable logistic regression analyses. Women who breastfed for 12–23 months were associated with an OR of 0.68 (95% CI, 0.54–0.86) for elevated BP, an OR of 0.78 (95% CI, 0.62–0.97) for elevated glucose, and an OR of 0.73 (95% CI, 0.56–0.95) for MetS compared with those who breastfed for ≤5 months in a multivariable logistic regression analyses. Women who breastfed for ≥24 months had an OR of 0.62 (95% CI, 0.52–0.84) for elevated glucose, an OR of 0.76 (95% CI, 0.60–0.96) for elevated triglycerides, and an OR of 0.70 (95% CI, 0.53–0.92) for MetS compared with those who breastfed for ≤5 months in a multivariable logistic regression analyses.
Conclusions:
Our results suggest that lifelong breast feeding for ≥12 months may be associated with lower risk for MetS.
Introduction
M
Breast feeding is not only the optimal nutrition for the first 6 months of life but also related to various medical benefits for the child and the mother. 7 It had been demonstrated that breast feeding is associated with weight loss, increased HDL-C, decreased TG, decreased incidence of T2DM, and a lower prevalence of hypertension (HTN). 8 –10 However, there are few studies evaluating the association of breast feeding with MetS, although previous studies reported that breast feeding is associated with components of MetS.
In the current population-based and cross-sectional study, we aimed to assess the association of a lifelong duration of breast feeding with MetS and its components in Korean parous women aged 19–50 years using a nationally representative survey. We also evaluated whether a longer duration of breast feeding is associated with MetS.
Materials and Methods
Subjects
Data from the Korean National Health and Nutrition Examination Survey (KNHANES) 2010–2013 were analyzed in this study. KNHANES is a cross-sectional, nationally representative survey that was designed using a multistage and stratified sampling method. The survey is composed of three parts: a health interview survey, a health examination survey, and a nutritional survey. It is conducted by the Division of Chronic Disease Surveillance, Korea Centre for Disease Control and Prevention annually.
11
Additional details about the study design and method are provided elsewhere.
12
Of the total randomly selected 33,552 participants in the KNHANES 2010–2013, 7387 subjects were women aged 19–50 years. Currently pregnant women were excluded (n = 73). Women with no history of labor were excluded (n = 1709). Subjects who had incomplete analytic data were excluded (n = 881). Finally, 4724 Korean women were included in this study. The database is available to the public at the KNHANES website (
Measurements
The anthropometric assessment was conducted by a trained expert using standard methods. In brief, height and body weight were measured to the nearest 0.1 cm and 0.1 kg, respectively. Body mass index (BMI) was calculated as the weight (kg)/square of height (m2). Waist circumference was assessed at the area between the lower rib margin and iliac crest to the nearest 0.1 cm. Systolic and diastolic blood pressure (SBP and DBP, mmHg) were measured three times on the right upper arm using a calibrated sphygmomanometer with an appropriately sized cuff. Every measurement was taken 2 minutes apart. Then, the mean of the last two values was used for analysis. Blood samples were collected from the antecubital vein after fasting ≥10 hours. Serum concentrations of total cholesterol (T-C, mg/dL), HDL-C (mg/dL), TG (mg/dL), low-density lipoprotein cholesterol (LDL-C, mg/dL), and fasting glucose (mg/dL) were measured using an automatic analyzer, Hitachi 7600 (Hitachi, Tokyo, Japan). In women with TG levels ≤400 mg/dL, LDL cholesterol was determined with the Friedewald formula: LDL-C (mg/dL) = T-C (mg/dL) − HDL-C (mg/dL) − [TG (mg/dL)/5]. 13 Glycated hemoglobin or the hemoglobin A1c (HbA1c, %) level was determined using high-performance liquid chromatography-723G7 (Tosho, Tokyo, Japan).
Data collection of general characteristics
The data regarding general characteristics of the participants were obtained from the KNHANES. Household income, education, and marriage status were included as socio-demographic characteristics. Household income was reported in quartiles and was categorized into two groups: lowest quartile or ≥second quartile. Education level was divided into two categories: ≤elementary school or ≥elementary school. Status of marriage was divided into two categories: yes or no. The lifestyle characteristics included smoking, alcohol drinking, and physical activity. Smoking was categorized into three groups: current, former, or never. Former smoking was defined as ≥5 packs in one's lifetime. Alcohol drinkers were divided into two groups: <2/week or ≥2/week alcoholic beverages consumed in the previous year. Physical activity was categorized into two groups: exercise or no exercise. Exercise was defined as intense physical activity for 20 minutes for ≥3 days/week, moderate physical activity for 30 minutes for ≥5 days/week, or walking for 30 minutes for ≥5 days/week. An assessment of gynecological history, lifestyle, and socio-demographic characteristics were included in the general characteristics. The gynecological characteristics included age at menarche, menopause, parity, and use of oral contraceptives (OCS). Age at menarche was defined as the age of the first menstrual period. This information was determined from a self-reported question: “At what age did your first menstrual period begin?” Subjects were divided into two categories according to the age at menarche: normal (12–16 years) or early (<12 years) or late (≥16 years) age at menarche. Menopause was categorized into two groups: yes or no. Parity, which was defined as the number of times a woman has given birth, was divided into three groups: 1, 2, 3, or ≥4 parity in a lifetime. Use of OCS was also categorized into two groups: consumption of OCS ≥1 month in a lifetime or not. HTN, dyslipidemia, and diabetes were also included as characteristics of past medical history. Hypertension was defined as SBP ≥140 mmHg, DBP ≥90 mmHg, or current administration of anti-hypertensive medicine. Dyslipidemia was also assessed by a self-reported answer to a question (yes or no) or administration of medicine for the treatment of dyslipidemia. T2DM, which does not include T1DM, was defined by fulfilling at least one of the following four criteria: (i) self-report using a questionnaire: yes or no, (ii) current use of medication for T2DM, (iii) current administration of insulin for managing T2DM, or (iv) fasting glucose ≥126 mg/dL during the national survey.
Definition of duration of breast feeding and MetS
The duration of breast feeding was defined as the total period of breast feeding in a woman's life. This information was obtained from an open-ended question: “How long did you feed your children with breast milk?” Participants were divided into four groups according to the duration of breast feeding: ≤5, 6–11, 12–23, or ≥24 months groups.
MetS was defined according to NECP-ATP III. 14 The diagnosis of MetS in this study was constituted as the presence of ≥3 of the following five criteria: (i) central obesity (WC >80 cm) using the International Obesity Task Force criteria for Asian-Pacific populations to determine waist circumference, 15 (ii) SBP ≥130 mmHg, DBP ≥85 mmHg, or treated with anti-hypertensive medication, (iii) fasting glucose ≥100 mg/dL or previously diagnosed with T2DM, (iv) HDL-C <50 mg/dL in women or medication use, (v) TG ≥150 mg/dL or medication use.
Statistical analyses
All analyses were conducted using SPSS software for Windows (SPSS version 22.0, IBM SPSS, Inc., Chicago, IL). The mean ± standard error are presented for normally distributed variables, while percentages (%) are presented for categorical variables. The differences were analyzed using an analysis of variance for normally distributed variables and analyzed using a chi-square test for categorical variables. An analysis of covariance (ANCOVA) was used to evaluate the association between the duration of breast feeding and the components of MetS after adjustment for possible confounders, such as age, BMI, household income, educational level, marriage status, smoking status, alcohol drinking, physical activity, age at menarche, menopause, parity, and use of ICS according to the duration of breast feeding. To investigate the odds ratios (ORs) of duration of breast feeding for MetS and its components, a stepwise multivariable logistic regression test was conducted after controlling for the previously described confounders, and the ORs and 95% confidence intervals (95% CIs) was determined. The ORs for MetS and its components were determined with the <5 months breast feeding group as the reference. The test for trends across groups according to duration of breast feeding was assessed for each group as a continuous variable in the multivariate logistic regression models. All significances were analyzed using a two-tailed method, and a p value <0.05 was considered statistically significant.
Results
Clinical characteristics of the study population
The mean age of the study participants was 39.79 years (Table 1). The clinical characteristics of the study population are shown in Table 1. The participants with a longer duration of breast feeding tended to have increased age (p = 0.001), BMI (p < 0.001), WC (p < 0.001), SBP (p < 0.001), and DBP (p < 0.001). They were more likely to be individuals with a lower educational status (p < 0.001), married (p < 0.001), physically active (p < 0.001), individuals who experienced menopause (p = 0.029), and multiparous ≥3 in their lifetime (p < 0.001), and were less likely to be alcohol drinkers (p = 0.032), current smokers (p < 0.001), and users of OCS (p = 0.030).
Age, BMI, WC, SBP, DBP, HbA1c, T-C, HDL-C, TG, and LDL-C are presented as the mean ± SE. House income, education, marriage, alcohol drinker, current smoker, physical activity, age at menarche, menopause, parity, use of oral contraceptives, hypertension, dyslipidemia, and diabetes are shown as percentages of total subjects. Statistical significance was determined using a one-way analysis of variance for continuous variables and a chi-square test for categorical variables (p < 0.05).
BMI, body mass index; DBP, diastolic blood pressure; HbA1c, glycated hemoglobin A1c; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; OCS, oral contraceptives; SE, standard error; SBP, systolic blood pressure; T2DM, type 2 diabetes mellitus; T-C, total cholesterol; TG, triglyceride; WC, waist circumference.
Adjusted association between the duration of breast feeding and components of MetS
We evaluated the associations between the duration of breast feeding and components of MetS using ANCOVA after adjustment for possible confounding factors, including age, BMI, household income, educational level, marriage status, smoking status, alcohol drinking, physical activity, age at menarche, menopause, parity, and use of OCS (Table 2). The adjusted association between the duration of breast feeding and components of MetS are shown in Table 2. There was a significantly inverse association between duration of breast feeding and SBP (p < 0.001 for trend) and DBP (p = 0.004 for trend). SBP was significantly lower in women who breastfed for 12–23 months than in women who breastfed for ≤5 months (p < 0.001). Additionally, DBP was significantly lower in women who breastfed for 6–11 and 12–23 months than in women who breastfed for ≤5 months (p = 0.025 and p = 0.025, respectively). There were no statistically significant linear associations of the duration of breast feeding with WC, glucose, HDL-C, and TG.
All values are presented as the mean ± SE. Statistical significance was determined using an analysis of covariance after adjusted for age, BMI, household income, educational level, marriage status, smoking status, alcohol drinking, physical activity, age at menarche, menopause, parity, and use of oral contraceptives according to the duration of breast feeding.
Adjusted ORs (95% CIs) of MetS and its components according to the duration of breast feeding
The prevalence of MetS was 12.6% among the total 4724 women (Table 3). The prevalence of MetS according to the duration of breast feeding was 13.8% among women who breastfed for ≤5 months, 11.0% among women who breastfed for 6–11 months, 11.2% among women who breastfed for 12–23 months, and 13.3% among women who breastfed for ≥24 months (p = 0.107). The ORs of MetS and its components according to the duration of breast feeding was assessed using a stepwise multivariable logistic regression analysis after adjustment for possible confounding factors, including age, BMI, household income, educational level, marriage status, smoking status, alcohol drinking, physical activity, age at menarche, menopause, parity, and use of OCS. Table 3 shows the adjusted ORs of MetS and its components according to duration of breast feeding. The women who breastfed for 6–11 months were found to have a 33% decreased OR of elevated blood pressure (BP) (95% CI, 0.51–0.89) compared with women who breastfed for ≤5 months. The women who breastfed for 12–23 months exhibited a 32% decreased OR of elevated BP (95% CI, 0.54–0.86) and a 22% decreased OR of elevated glucose (95% CI, 0.62–0.97) than women who breastfed for ≤5 months. The women who breastfed for 12–23 months were found to have a 27% decreased OR of MetS compared with women who breastfed for ≤5 months. The women who breastfed for ≥24 months were found to have a 38% decreased OR of elevated glucose (95% CI, 0.52–0.84), a 24% decreased OR of elevated TG (95% CI, 0.60–0.96), and a 30% decreased OR of MetS (95% CI, 0.53–0.91) compared with women who breastfed for ≤5 months. Significantly inverse associations were observed between the duration of breast feeding and elevated BP (p = 0.015 for trend), elevated glucose (p < 0.001 for trend), elevated TG (p = 0.023 for trend), and MetS (p = 0.003 for trend).
The odds ratio for MetS was adjusted for age, BMI, household income, educational level, marriage status, smoking status, alcohol drinking, physical activity, age at menarche, menopause, parity, and use of oral contraceptives according to the duration of breast feeding. Elevated WC was defined as >80 cm. Elevated BP was defined as SBP ≥130 mmHg, DBP ≥85 mmHg, or medication for hypertension. Elevated glucose was defined as glucose ≥100 mg/dL or medication for diabetes. Reduced HDL-C was defined as HDL-C <50 mg/dL or medication for dyslipidemia. Elevated TG was defined as TG ≥150 mg/dL or medication for dyslipidemia.
Discussion
In this population-based cross-sectional study, Korean young and middle-aged parous women who breastfed for 12–23 months had lower ORs of developing MetS than those who breastfed ≤5 months, and this was associated with decreased ORs of elevated BP and elevated glucose. In addition, women who breastfed for ≥24 months exhibited lower ORs of MetS than women who breastfed ≤5 months, and this was associated with decreased ORs of elevated glucose and elevated TG.
In normal physiology, breast feeding provides specific and innate immunologic factors and nutrients to the infants. To support this, mothers need ∼500 kcal of energy per day for breast feeding, 16 which is delivered from the fatty tissue that they accumulated during pregnancy. Change in this physiology is related to adverse maternal health outcomes. Breast feeding is associated with a protective effect on maternal metabolic diseases. Most previous studies reported that breast feeding is associated with a decreased risk of components of MetS, such as obesity, 17 hypertension, 18 and diabetes. 19,20 Breast feeding was also associated with MetS. In the Coronary Artery Risk Development in Young Adults (CARDIA) study, breast feeding was associated with a lower incidence of MetS among women years after weaning and after adjustment for possible confounder. 21 In CARDIA study, relative hazard range as risk reduction associated with longer breast feeding was 0.14–0.56 (p = 0.03) in gestational diabetes mother (GDM) group and non-GDM groups and was 0.44–0.61 (p = 0.03) in non-GDM group after adjusted for possible confounders. In the SWAN (Study of Women's health Across the Nation) study, women who breastfed their children exhibited a lower risk of MetS than those who had never breastfed. 22 In their study, women with long breast feeding had significantly decreased ORs for MetS (ORs; 0.79, 95% CI, 0.63–0.99) compared to those who never breastfed. However, there are inconsistent findings. A recent Iran study showed that breast feeding was not protective in the development of MetS. In this study, Korean young and middle-aged women who breastfed for 12–23 months were associated with a lower risk of MetS, and women who breastfed for ≥24 months had a lower risk of MetS than those who breastfed for 12–23 months. Our results support the hypothesis that breast feeding plays a protective role in the development of MetS.
A longer duration of breast feeding is associated with a lower risk of MetS and its components. In a study of the Danish National Birth Cohort, a longer duration and greater intensity of breast feeding was associated with reduced postpartum weight retention. 23 A longer duration of breast feeding was associated with a reduced risk of T2DM after controlling for confounders. 24 In the Women's Health Initiative observational study, an increased duration of breast feeding was associated with a lower prevalence of hypertension, diabetes, hyperlipidemia, and cardiovascular disease. 25 However, inconsistent findings were observed between a longer duration and metabolic risk. In a prospective study by Stuebe et al., a dose–response relationship was not observed between breast feeding duration and metabolic risk during a 3-year follow-up period. 26 Actually, the underlying mechanism of the association between a longer duration of breast feeding and metabolic risk is not fully understood. One possible explanation is that breast feeding, a normal physiologic form of energy expenditure, may influence persistent, protective maternal health outcomes. This explanation is supported by animal models. In mice, maternal BP and visceral adiposity at 2 months postpartum were significantly higher in nonlactating mice than that in lactating mice. 27 Another explanation is that breast feeding may be associated with maternal health through stress reactivity. Women who breastfed have reduced hypothalamus-pituitary-adrenal axis activation and greater vagal tones. 28 The levels of basal norepinephrine and ACTH, cortisol, and glucose responses to exercise were significantly decreased in lactating women than those in nonlactating women. 28 Additionally, lactating women who were aggressive exhibited lower SBP than formula-feeding or never-pregnant women who were nonaggressive. 29 In this study, breast feeding for 12–23 months was associated with decreased risks of elevated BP, elevated glucose, and MetS. Breast feeding for ≥24 months was associated with lower risks of elevated glucose and elevated TG. These findings were in agreement with previous reports and hypotheses explaining the relationship between breast feeding and MetS.
Unexpectedly, we found that the association of breast feeding with elevated BP was attenuated with an increasing duration of breast feeding among the group of women who breastfed for ≥24 months. This may be related with parity. Increased parity is associated with a longer duration of breast feeding in this study. Parity is associated with a greater left ventricular mass. 30 Additionally, there is a 40% increase in blood volume during pregnancy with no increase in SBP; this is related to a simultaneous reduction in peripheral vascular resistance. 31 Childbearing may have long-lasting effects on the cardiovascular system. A series of studies that evaluated the association between childbearing and the prevalence of hypertension in later life reported that childbearing was associated with decreased SBP or DBP. 32,33 Gunderson et al. 32 reported that the first childbearing was associated with a decrease in BP. In a recent Australian study, parity was associated with a lower risk of high BP, and women who had given birth had significantly lower adjusted ORs for high BP than nulliparous women. 33 However, increased parity may have adverse health outcomes later in life. 34,35 There is some evidence indicating that parity has nonlinear associations with hypertension 36 and diabetes. 37 Parity ≥4 was significantly associated with increased adjusted ORs for hypertension in the Trabzon Hypertension Study. 34 A recent U.S. population-based study demonstrated a nonlinear association between parity and the carotid distensibility coefficient, which is a risk factor for cardiovascular diseases, and women who had two live births had significantly lower distensibility than women who were primiparous or multiparous ≥3. 36 In our study, women who breastfed ≥24 months were more likely to be multiparous ≥3 in their lifetime than those who breastfed ≤5, 6–11 or 12–23 months. This may be related to the attenuated association between duration of breast feeding for ≥24 months and elevated BP. However, parity was adjusted as one of the confounders in multivariate logistic regression analyses in this study. There may be the underlying mechanism of between longer duration for ≥24 months and elevated BP. Further studies are needed.
This study has potential limitations. First, this study was conducted with a cross-sectional design, and causality between breast feeding and MetS cannot be identified. Second, the intensity of breast feeding could not be used for the analyses. Third, this study was based on the individuals' memory for duration of breast feeding, which is related to the possibility of information bias. However, breastfeeding is a major concern for women raising children, and recall of breastfeeding is considered to be reliable over many years. Fourth, our results could not be analyzed in relation to pregnancy-related problems, such as gestational hypertension, and gestational diabetes, that may be related to MetS in later life. 38 Finally, it is desirable that mediation analyses could be performed to evaluate which components of MetS are related to longer duration of breast feeding in this study.
Conclusion
A nationally representative, population-based cross-sectional study found that Korean young and middle-aged parous women with lifelong breast feeding for ≥12 months were at a lower risk of MetS than those with lifelong breast feeding for ≤5 months. Breast feeding for 12–23 months was associated with lower risks of elevated BP and elevated glucose. Women who breastfed ≥24 months exhibited a decreased risk of MetS than those who breastfed for 12–23 months. Breast feeding for ≥24 months was associated with lower risks of elevated glucose and elevated TG, whereas the relationship between breast feeding ≥24 months and elevated BP was not statistically significant. Our results suggest that lifelong breast feeding for ≥12 months may be associated with lower risk for MetS in parous women.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
