Duration of lactation is associated with lower prevalence of the metabolic syndrome in midlife—SWAN, the study of women’s health across the nation

Article Outline

• Abstract
• Materials and Methods
  • The study of women’s health across the nation (SWAN)
  • Lactation history
  • Physical measurements
  • Demographic, dietary, and lifestyle factors
  • Definition of metabolic syndrome
  • Laboratory assays
  • Analytic sample
  • Statistical analysis
• Results
• Comment
• Acknowledgments
• References
• Copyright

Objective

The objective of the study was to evaluate whether lactation duration is associated with lower prevalence of metabolic syndrome (MetSyn) in midlife, parous women.

Study Design

This was a cross-sectional cohort analysis of 2516 parous, midlife women using multivariable logistic regression to determine the independent association of lactation and lactation duration on prevalence of MetSyn.

Results

One thousand six hundred twenty women (64.4%) reported a history of breast-feeding, with average lifetime duration of lactation of 1.16 (± 1.04) years. MetSyn was present in 536 women (21.3%). Adjusting for age, smoking history, parity, ethnicity, socioeconomic status, study site, physical activity, caloric intake, and high school body mass index, women with prior lactation had significantly lower odds of MetSyn (odds ratio [OR] 0.79, 95% confidence interval [CI] 0.63 to 0.99). Furthermore, increasing duration of lactation was similarly associated with lower odds of MetSyn (OR 0.88, 95% CI 0.77 to 0.99).

Conclusion

Duration of lactation is associated with lower prevalence of MetSyn in a dose-response manner in midlife, parous women.

Key words: lactation, metabolic syndrome, parity

The metabolic syndrome (MetSyn) is a clustering of the metabolic abnormalities: insulin resistance, dyslipidemia, hypertension (HTN), and obesity. Women with MetSyn are at increased risk of diabetes mellitus (DM),¹ major cardiovascular events,² and increased all-cause mortality.³ Lifestyle factors including smoking, poor diet and sedentary lifestyle are associated with increased risk of MetSyn.

Lactation creates a metabolic drain that leads to altered energy homeostasis. The studies associating weight loss with lactation, however, have been mixed.⁴, ⁵ Lactation increases high-density lipoprotein (HDL) levels,⁶ decreases triglyceride levels,⁷ and improves insulin sensitivity⁵, ⁸, ⁹ in the postpartum period. Each of these changes represents an improvement in the characteristics of MetSyn. There is evidence that this enhanced metabolic efficiency persists in the immediate post-lactational period.¹⁰ Duration of lactation has also been associated with a decreased incidence of type 2 DM¹¹ and possibly HTN¹² later in life, demonstrating that lactation may confer long-term benefits to the mother.

Although several studies have characterized the effects of lactation on carbohydrate and lipid metabolism, no study, to our knowledge, has examined the association between lactation duration and MetSyn. We performed a cross-sectional analysis of the association between lifetime duration of lactation and the prevalence of MetSyn in a cohort of midlife women who participated in the Study of Women’s Health Across the Nation (SWAN). We hypothesized that duration of lactation is associated with a lower prevalence of MetSyn in midlife women.

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Materials and Methods 

The study of women’s health across the nation (SWAN) 

SWAN is a multisite, multiethnic longitudinal study of 3302 midlife women developed to characterize patterns of health in women as they traverse the menopausal transition. Women enrolled in the SWAN study were recruited from community-based samples at 7 clinical sites At each site a Caucasian sample and a pre-specified non-Caucasian sample were recruited. African American women were recruited at Detroit, MI; Boston, MA; Chicago, IL; and Pittsburgh, PA. Hispanic women were recruited at Newark, NJ. Chinese and Japanese women were recruited at Oakland, CA, and Los Angeles, CA, sites, respectively.

Ethnicity was self-reported based on predefined categories. Women could not self-classify into more than 1 group. Briefly, in 1995-1997, a cross-sectional cohort of 16,065 women aged 40-55 years completed a short screening interview, most often by telephone. The longitudinal SWAN cohort was recruited from women who had completed the screening questionnaire; 50% of eligible women were enrolled in the longitudinal cohort. The study design and recruitment process has been previously described in detail.¹³

Eligibility for the longitudinal SWAN cohort included: (1) age 42-52 years; (2) an intact uterus and at least 1 ovary; (3) at least 1 menstrual period within the past 3 months; and (4) not having taken any reproductive hormones for at least 3 months. Common baseline and annual follow-up protocols were used at all sites; these included interviewer-administered forms, self-administered forms, anthropometry, and phlebotomy. All data collectors were trained and certified by SWAN. For the purposes of this study, the baseline data set was used. For the current study, participants were required to have had at least 1 live birth; 2726 met these criteria.

Written informed consent was obtained from all participants. Staff bilingual in Spanish, Cantonese, and Japanese were available at the relevant sites, and all questionnaires were available in translation.

Lactation history 

Participants answered retrospective questions about number of pregnancies and lactation duration following each live birth. All women who reported a live birth were included. Duration of lactation was coded in months, with less than 1 month of lactation effort coded as zero. Parous women who chose not to breast-feed were coded as zero. After the first year of lactation, the infant receives the majority of its caloric needs from alternate sources. Therefore, for the purposes of this study, for women who breast-fed longer than 1 year/pregnancy each lactation interval was truncated at 1 year.

Physical measurements 

At baseline, 12 hour fasting blood samples were collected. Blood was refrigerated, centrifuged within 2 hours of phlebotomy, aliquoted, frozen, and batched for approximately monthly shipment (Medical Research Laboratories International, Highland Heights, KY). Blood pressure, height, weight, and waist and hip circumference were measured using standardized procedures. For these analyses, body mass index (BMI) was characterized as underweight (less than 18.5 kg/m²), normal (18.5 or greater and less than 25 kg/m²), overweight (25 or greater and less than 30 kg/m²), or obese (30 kg/m² or greater).

Demographic, dietary, and lifestyle factors 

Demographic variables including age, income, education, self-identified race, employment, and socioeconomic status were collected from interviewer- and self-administered questionnaires. Smoking status was dichotomized into current and past/never smokers. Weight at completion of high school was retrospectively self- reported. Socioeconomic status was categorized into 3 levels based on self-report of difficulty in paying for basics (food, shelter, and heat). Daily caloric intake was measured using a modification of the 1995 Block Food Frequency,¹⁴ with the addition of ethnic-specific foods to the questionnaires used at sites enrolling Hispanic, Chinese, and Japanese participants. Ethnicity was categorized as African American, Caucasian, Chinese, Japanese, or Hispanic. Physical activity questions were adapted from the Kaiser Physical Activity Survey, adapted from the Baecke physical activity questionnaire.¹⁵

Definition of metabolic syndrome 

Dichotomous variables were created for each component of the MetSyn based on the National Cholesterol Education Program III criteria¹⁶: (1) abdominal obesity (waist circumference greater than 80 cm for Chinese and Japanese, greater than 88 cm for Caucasians, African Americans, and Hispanics); (2) hypertriglyceridemia (fasting triglycerides 150 mg/dL or greater); (3) low HDL cholesterol less than 50 mg/dL; (4) elevated blood pressure (average systolic blood pressure 130 mm Hg or greater or average diastolic blood pressure 85 mm Hg or greater, or on antihypertensive medication); and (5) impaired fasting glucose (fasting glucose 110 mg/dL or greater and 125 mg/dL or less). Participants were classified as having MetSyn if they satisfied 3 or more of the above criteria.

Laboratory assays 

All lipid and lipoprotein fractions were analyzed on EDTA-treated plasma. Total cholesterol was analyzed by enzymatic methods. HDL cholesterol was isolated using heparin-2M manganese chloride. Serum insulin was measured using radioimmunoassay (Coat-a-Count, Diagnostics Products Corp, Los Angeles, CA) and monitored as part of the monthly quality assurance program by the DM Diagnostic Laboratory at the University of Missouri (Columbia, MO). Glucose was measured using a hexokinase-coupled reaction (Roche Molecular Biochemicals Diagnostics, Indianapolis, IN).

Analytic sample 

Of the total cohort of 2726 parous women, 210 women with missing lactation or MetSyn data were excluded from this analysis. The final analytic sample included 2516 women.

Statistical analysis 

Associations between demographic and clinical characteristics stratified by MetSyn were assessed using Student’s t tests or Kruskall-Wallis tests for continuous variables. χ² or Fisher’s exact tests were used to assess these associations for categorical variables. The association of lifetime duration of lactation with MetSyn was tested using the Wilcoxon rank-sum test. Spearman’s rank correlations were performed between lifetime duration of lactation and current BMI, waist circumference, systolic blood pressure, diastolic blood pressure, and fasting levels of total cholesterol, triglycerides, HDL cholesterol, and glucose.

To evaluate the effect of lactation on the development of MetSyn, 2 logistic regression models were constructed with lactation ever (yes/no) and duration of lactation. Multivariable models included age, physical activity, and daily caloric intake as continuous variables and high school BMI, parity, socioeconomic status, study site, current smoking, and ethnicity as categorical variables. Interaction product terms of lactation history with each covariate were created and tested separately in models that included all main-effects terms. In a similar manner, interaction product terms of duration of lactation with each covariate were created and tested separately in models with all main effects terms. In addition, to determine whether parity affected the association between lactation history and MetSyn, logistic regression models were stratified on parity (1, 2, 3, and 4 or greater) and adjusted for the same covariates above.

To evaluate the independent effect of lactation on each individual component of the MetSyn, 5 additional adjusted logistic regression models were constructed with elevated blood pressure, abdominal obesity, impaired fasting glucose, low HDL, and elevated triglycerides as dependent outcome variables. Each model included the same covariates as the full model (cited in earlier text).

Because the full model could not be adjusted for current BMI because of collinearity with the outcome variable (MetSyn), we performed a sensitivity analysis in which MetSyn without the waist circumference component was our outcome variable. The logistic regression model with lactation (yes/no) as the independent variable was adjusted for all covariates noted above with the addition of current BMI.

All statistical tests used a 2-tailed alpha of 0.05. All analyses were performed using STATA 8.2 (StataCorp LP, College Station, TX).

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Results 

At baseline, the SWAN cohort consisted of 2516 parous women with a mean (SD) age of 46.4 (2.7) years, mean BMI of 28.4 (7.2) kg/m², and a median (interquartile range) parity of 2.0 (1.0) live births per woman. Of these women, 1620 (64.4%) reported a history of lactation. The mean lifetime duration of lactation among women who breast-fed was 1.16 (± 1.04) years.

There were 536 prevalent cases of MetSyn (21.3%). Among those who breast-fed, 297 (18.3%) met the criteria for MetSyn, compared with 239 among those who did not (26.7%) (P < .01). Women who developed MetSyn were more likely to have a higher BMI at time of interview (P < .01) and at completion of high school (P < .01), be African American (P < .01) or Hispanic (P < .01), smoke (P = .02), and be of lower socioeconomic status (P = .04) (Table 1). They breast-fed for shorter periods of time (Wilcoxon rank sum, P <.01).

TABLE 1. Characteristics of cohort stratified by presence or absence of MetSyn

	Absence of MetSyn (n = 1980)	Presence of MetSyn (n = 536)	P value
Lifetime lactation (y)	1.12(0.96)	1.05(0.99)	<.01
Age, y	46.5(2.2)	46.7(2.1)	.48
Daily caloric intake	1852.1(786.5)	1936.3(793.5)	.09
Physical activity	7.8(1.7)	7.2(1.6)	.28
High school BMI	20.6(2.9)	22.4(2.9)	<.01
Current BMI	26.3(7.2)	34.5(6.6)	<.01
Parity, n (%)
Para 1	400(20.1)	114(21.2)	.61
Para 2	842(42.4)	188(34.9)	<.01
Para 3	469(23.6)	125(23.2)	.81
Para 4 or greater	275(13.9)	112(20.7)	<.01
Ethnicity
African American	589(29.8)	195(36.4)	<.01
Caucasian	862(43.6)	219(40.9)	.86
Hispanic	163(8.2)	66(12.3)	<.01
Chinese	168(8.5)	25(4.7)	<.01
Japanese	195(9.9)	30(5.6)	.02
Lowest SES category	170(8.6)	79(14.7)	.04
Current smokers	788(39.8)	249(46.5)	.02

Continuous variables presented as mean (SD) with P values calculated by t tests or Kruskal- Wallis tests, as appropriate.

Categorical variables presented as n (percent) with P values calculated by χ².

SES, socioeconomic status.

Ram. Lactation and its association with metabolic syndrome. Am J Obstet Gynecol 2008.

Spearman’s rank correlations were computed on all women, and found duration of lactation inversely correlated with current BMI (r_s = −0.16, P < .01), waist circumference (r_s = −0.18, P < .01), systolic blood pressure (r_s = −0.17, P < .01), diastolic blood pressure (r_s = −0.09, P < .01), fasting levels of glucose (r_s = −0.09, P < .01), insulin (r_s = −0.15, P < .01), triglycerides (r_s = −0.06, P < .01), total cholesterol (r_s = −0.06, P < .01), and low-density lipoprotein (LDL) cholesterol (r_s = −0.07, P < .01). There was a positive correlation with fasting HDL levels (r_s = 0.07, P < .01). Whereas all of the above correlations were statistically significant, it is worth noting that the strength of these associations was relatively small.

Logistic regression analyses were performed to assess the association of lactation with MetSyn. Parous women who had ever breast-fed had a significantly lower prevalence of MetSyn: unadjusted odds ratio (OR) of 0.62 (95% confidence interval [CI] 0.51, 0.75). This association remained significant in the multivariable model adjusting for age, current smoking, parity, ethnicity, socioeconomic status, study site, physical activity, caloric intake, and high school BMI: OR of 0.77 (95% CI 0.62, 0.96) (Table 2). The model was not adjusted for current BMI because of collinearity with the waist circumference component of our outcome variable (r_s = 0.92, P < .01). We entered MetSyn without the waist circumference component into the multivariable model, and after adjusting for current BMI, the relationship between lactation and this newly defined metabolic cluster remained statistically significant (P = .02). There were no statistically significant interactions of lactation history with any covariate; thus, no interaction terms were included in the final model. Logistic regression analyses were then performed to assess the association of lactation history with each component of the MetSyn. Women who had ever breast-fed were significantly less likely to have impaired fasting glucose (P < .01), elevated blood pressure (P = .048), and abdominal obesity (P < .01).

TABLE 2. Impact of a history of lactation (ever/never) on MetSyn and components of MetSyn, adjusted for multiple covariates

Ram. Lactation and its association with metabolic syndrome. Am J Obstet Gynecol 2008.

Logistic regression analysis found a significant association of duration of lactation with MetSyn: the unadjusted OR for each year of lactation was 0.80 (95% CI, 0.72, 0.91). The multivariable model adjusting for all the aforementioned covariates also found a significant association: the OR per each additional year of lactation was 0.88 (95% CI, 0.77, 0.99) for MetSyn (Table 3). There were no statistically significant interactions of lactation duration with any covariate; thus, no interaction terms were included in the final model. Logistic regression analyses exploring the duration of lactation with each MetSyn component demonstrated significant inverse relationships with elevated blood pressure (P = .04) and abdominal obesity (P < .01)

TABLE 3. Impact of duration of lactation (per year) on MetSyn and components of MetSyn, adjusted for multiple covariates

Ram. Lactation and its association with metabolic syndrome. Am J Obstet Gynecol 2008.

When the multivariable model was stratified by parity (Table 4), a statistically significant inverse relationship between duration of lactation and MetSyn was seen in women who had 1 (OR 0.57; 95% CI, 0.34, 0.95) or 2 (OR 0.69; 95% CI, 0.47, 0.998) successful pregnancies. However, in women who had 4 or more successful pregnancies, this inverse relationship no longer persisted.

TABLE 4. Multivariable logistic regression models assessing the relationship of a history of lactation with prevalence of MetSyn stratified by parity

Ram. Lactation and its association with metabolic syndrome. Am J Obstet Gynecol 2008.

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Comment 

A protective association between a history of lactation and MetSyn has recently been demonstrated.¹⁷ Our study supports and extends these observations to show that the rate of MetSyn is significantly lower with increasing duration of lactation, suggesting a dose-response relationship. However, a threshold appears to be reached between the third and fourth pregnancies, after which any protective effect no longer remains. This finding was unexpected because increasing parity should be associated with increasing duration of lactation. Increasing parity, however, is also associated with increased weight retention and has been independently associated with increased prevalence of MetSyn.¹⁷ We hypothesized therefore that the effects of increasing parity outweigh the benefits of increased duration of lactation between the third and fourth pregnancies.

A history of lactation has been shown to attenuate the adverse changes in LDL cholesterol, and longer duration of breast-feeding (longer than 3 months) has been shown to attenuate the decrements in HDL cholesterol associated with pregnancy up to 16 months after delivery.¹⁸

We also found a statistically significant correlation between a duration of lactation and HDL cholesterol and an inverse correlation with LDL cholesterol. Furthermore, when examining the association of lactation on the individual components of MetSyn, we found that lactation was associated with significantly lower odds of elevated blood pressure, abdominal obesity, and impaired fasting glucose after adjusting for multiple risk factors.

Duration of lactation has been associated with decreased incidence of type 2 DM among parous women.¹⁵ This finding is in agreement with our observation of a statistically significant protective effect of lactation on fasting glucose. Increasing duration of lactation has been shown to protect against the development of HTN in Korean women.¹⁶ We found that duration of lactation had a significant protective effect against development of elevated blood pressure.

The strengths of our study lie in its large sample and comprehensive collection of metabolic and lactation data. Breast-feeding data were collected as a continuous variable, not extrapolated from a categorical collection. Another strength is the multiethnic composition of our cohort that suggests generalizability of our results to other populations.

Our study has a number of limitations. A cross-sectional analysis cannot construct a causal or temporal relationship between the variable of interest and the outcome measure. It is possible that MetSyn preceded lactation. Alternatively, women who are prone to developing MetSyn may have difficulty initiating lactogenesis.

Several studies have suggested that maternal obesity may be associated with decreased breast-feeding initiation and duration.¹⁹, ²⁰, ²¹ However, our multivariable regression model is adjusted for high school BMI. Furthermore, in a post hoc analysis when the model is stratified by high school BMI, the point estimates are similar and protective for the development of MetSyn in each category except the highest (data not shown).

Lactation may protect against obesity, and this may be driving the association with MetSyn. This is difficult to evaluate in our model because of collinearity with our outcome variable. However, in adjusted analyses lactation was significantly associated with several components of the MetSyn in addition to abdominal obesity. Furthermore, when we removed the waist circumference component of MetSyn and reentered it into the multivariable model and adjusted for current BMI, the relationship between history of lactation and this metabolic cluster remained statistically significant.

Women who choose to breast-feed were more likely to choose other healthy behaviors and this healthy lifestyle bias may lead to confounding. We adjusted for markers of a healthy lifestyle, including diet, exercise, and smoking history. After adjusting for these markers, the protective association of lactation on development of MetSyn remained unchanged.

Recall bias may be another limitation of this study; women were asked to provide lactation histories and weight at completion of high school several years after the prevalent outcomes. However, several studies have found both reporting of breast-feeding duration²², ²³ and recall of high school weight²⁴ to be a valid, reliable measure up to 20 years later.

Lactation may prime the metabolic system by making it a more energy-efficient machine, and this metabolic efficiency may persist in the postlactational period. In the immediate postlactational period, fasting plasma free fatty acids both basally and in response to noradrenaline infusion are significantly lower than those observed during lactation or in bottle-feeding and nonpregnant controls.⁸ Similarly, after lactation the response of plasma glycerol to noradrenaline is significantly lower than these same controls.⁸ Each of these changes represents an improvement in metabolic efficiency.

Lactation may decrease visceral adiposity, and indeed we demonstrated a negative association between lactation and abdominal obesity. Central fat accumulation has been postulated to be a physiological basis for reduced postprandial thermogenesis.²⁵ A redistribution of fat from central stores through lactation may lead to improved postprandial thermogenesis and a more efficient metabolism.

Lactation may also decrease the prevalence of MetSyn by improving insulin sensitivity. Unfortunately, most of the data on lactation and carbohydrate metabolism have been collected from gestational diabetics and confined to the immediate postpartum period. Nonetheless, improved glucose tolerance, fasting glucose, and total area under the glucose tolerance curve have been shown in breast-feeding gestational diabetics.⁵ Gestational diabetics who lactate have a higher disposition index, indicating a more efficient pancreatic beta-cell function.⁷ We found a significant inverse correlation between duration of lactation and fasting levels of both glucose and insulin. Longitudinal studies in women with intact carbohydrate metabolism are needed to evaluate whether lactation has a long-term impact on insulin sensitivity.

In conclusion, we have found that duration of lactation is associated with prevalence of MetSyn in parous midlife women in a dose-response manner. This association is most marked after the first and second pregnancies and appears to reach a threshold by the fourth pregnancy. These changes may be mediated by changes in insulin resistance, visceral adiposity, and/or free fatty acid metabolism. Further research is needed to confirm and elaborate on these results. In addition to the pediatric benefits of breast-feeding, these findings of maternal benefit may encourage more women to initiate and maintain breast-feeding behavior.

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Acknowledgments 

We thank the study staff at each site and all the women who participated in SWAN.

Clinical centers included the following: University of Michigan, Ann Arbor, MaryFran Sowers, principal investigator; Massachusetts General Hospital, Boston, MA, Robert Neer, principal investigator 1994-1999; Joel Finkelstein, principal investigator 1999 to present; Rush University, Rush University Medical Center, Chicago, IL, Lynda Powell, principal investigator; University of California, Davis/Kaiser, Ellen Gold, principal investigator; University of California, Los Angeles, Gail Greendale, principal investigator; University of Medicine and Dentistry, New Jersey Medical School, Newark, NJ, Gerson Weiss, principal investigator 1994-2004; Nanette Santoro, principal investigator 2004 to present; and the University of Pittsburgh, Pittsburgh, PA, Karen Matthews, principal investigator.

The National Institutes of Health Program Office included the following: National Institute on Aging, Bethesda, MD, Marcia Ory 1994-2001; Sherry Sherman 1994 to present; National Institute of Nursing Research, Bethesda, MD, program officers.

The central laboratory included the following: University of Michigan, Ann Arbor, Daniel McConnell; Central Ligand Assay Satellite Services.

The coordinating center included the following: New England Research Institutes, Watertown, MA, Sonja McKinlay, principal investigator 1995-2001; University of Pittsburgh, Pittsburgh, PA, Kim Sutton-Tyrrell, principal investigator 2001 to present.

The steering committee included Chris Gallagher, chair, and Susan Johnson, chair.

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