Skip to main content
Download PDF

Lactation duration and lifetime progression to metabolic syndrome in women according to their history of gestational diabetes: a prospective longitudinal community-based cohort study

Journal of Translational Medicine volume 21, Article number: 177 (2023) Cite this article

Abstract

Background

Despite the many signs of progress in pharmacotherapies, metabolic syndrome (MetS) is one of the main public-health burdens worldwide. Our study aimed to compare the effect of breastfeeding (BF) in women with and without gestational diabetes mellitus (GDM) on MetS incidence.

Methods

Of females who participated in the Tehran Lipid and glucose study, women who met our inclusion criteria were selected. The Cox proportional hazards regression model, with adjustment of potential confounders, was done to evaluate the relationship between duration of BF and incident of MetS in women with a GDM history compared to non-GDM.

Results

Out of 1176 women, there were 1001 non-GDM and 175 GDM. The median follow-up was 16.3 (11.9, 19.3) years. Results of the adjusted model illustrated that the total BF duration was negatively associated with MetS incidence risk (hazard ratio (HR) 0.98, 95% CI 0.98–0.99) in total participants indicating that per one-month increase of BF duration, the hazard of MetS reduced by 2%. The HR of MetS in Comparison between GDM and non-GDM women demonstrated significantly more reduced MetS incidence with a longer duration of exclusive BF (HR 0.93, 95% CI 0.88–0.98).

Conclusions

Our findings illustrated the protective effect of BF, especially exclusive BF, on MetS incidence risk. BF is more effective in reducing the risk of MetS among women with a history of GDM than among women without such a history.

Introduction

Metabolic syndrome (MetS) is a group of risk factors that enhance the chance of increasing some diseases, especially heart disease. MetS is now considered a "developmental origin of health and disease", which, on the one hand, can have its origins in early life; on the other hand, early interventions can have the potential impact on preventing MetS [1]. Precise identification of influential factors in preventing and controlling the increasing incidence and prevalence of MetS is crucial [1]. As mentioned, using professional factors or interventional programming to prevent or treat MetS is needed and beneficial.

The World Health Organization (WHO) feeding recommendation is that infants at six months of age receive exclusive breastfeeding (BF) without receiving complementary foods, and then BF should be accompanied by complementary foods [2]. BF duration per se is a critical period in women's reproductive process, and it has many benefits for both mother and child. Thereby, BF can improve health across two generations. There is a piece of solid evidence on the advantages of BF for children later in life. However, the effects of BF on the mother's health have usually been overlooked [3]. BF may result in the improvement of the physical and emotional health situations of the mother during her lifetime. The beneficial mental and physical effects of BF are divided into two groups: early and late effects [4]. Reduced adiposity, weight, stress, and anxiety are examples of early effects [5,6,7]. Furthermore, reducing some noncommunicable diseases (NCDs) such as cardiovascular diseases (CVDs), rheumatoid arthritis, and Alzheimer's are instances of late effects of BF on women's health [8,9,10].

Today, what should be more considered is finding prolonged beneficial effects of BF for mothers. Still, relatively few studies have been done to assess the effect of BF on women's health during their lifetimes [11]. A recent meta-analysis (2020) reported inconclusive results regarding the association between the duration of BF and MetS [12]. Moreover, the association between BF and MetS may be influenced by mothers' histories of gestational diabetes mellitus (GDM). GDM is stated as "diabetes diagnosed in the second or third trimester of pregnancy that is not clearly overt diabetes" [13] and occurs in nearly 13% of births in 2019 [14].

On the one hand, studies illustrated a higher thyroid hormone level in women with a history of GDM with a longer BF duration may have a potential beneficiary effect on their cardiometabolic status through a reduction in weight gain [15]. On the other hand, lactation due to various maternal and fetal morbidities secondary to GDM may cause postponed lactogenesis and the infants' poor sucking type [16, 17]. So further research should be performed to evaluate the beneficial roles of BF duration, for instance, as a preventive factor, on diseases such as MetS [12].

To address these gaps, we aimed to explore the effects of BF and its duration on women according to their history of GDM in a group of women using a longitudinal prospective community-based method with nearly two decades of follow-up.

Methods

Research design and subjects

The present study subjects were selected using the baseline information of the 11,100 Tehran lipid and glucose study (TLGS) female participants. The TLGS is an ongoing prospective study initiated in 1998 to determine the prevalence and incidence of NCDs risk factors. Details of TLGS have been published elsewhere [18]. To perform the current study, prospectively, women were followed who were nulliparous and without metabolic disease at recruitment. Of the 11,100 female participants in the TLGS study, there were 7680 of childbearing age (18–35 years). Of these were excluded women who did not give birth during the study period (N = 784). As well, women that were diagnosed with MetS before their first pregnancy (N = 41), parous women at baseline  (N = 431), those that had a multiple birth pregnancy (N = 11), and those without BF (N = 663) or follow-up data (N = 302) were excluded. Furthermore, since we aimed to report the incidence of MetS during women's lifetimes after BF duration, we excluded those who experienced MetS before their first BF duration (N = 12) (Fig. 1), leaving a sample of N = 1176 for analysis.

Fig. 1
figure 1

Study flowchart. TLGS, Tehran lipid & glucose study; GDM, gestational diabetes Mellitus; MetS, Metabolic syndrome; BF, breastfeeding

Full size image

Measurements

All participants' data were gathered and measured at exams almost every three years. Face-to-face interviews were performed to collect socio-demographic variables and data on several risk factors for NCDs and reproductive histories by trained staff.

For all participants, standardized procedures and calibrated equipment were used to measure weight and height with minimal clothing, without shoes in a standing position. Calculating the body mass index (BMI) was done by dividing weight in kilograms by height in meters squared (kg/m2). Hip circumference was measured via an unstretched measuring tape to the nearest 0.1 cm. Waist circumference (WC) was measured centrally between the lower rib margin and the iliac crest at the side of the umbilicus at the end of a gentle expiration. Blood pressure (BP) was measured twice in the right arm after a 15-min rest in a sitting position and was evaluated according to the mean of the two measurements. Physical activity was assessed by the modifiable activity questionnaire. The participants were questioned about the physical activities they had engaged in over the previous 12 months. So that participants with fewer than 600 metabolic equivalent task minutes per week were categorized as a low physical activity group [19, 20]. Blood samples were gathered after a 12- to 14-h overnight fasting (between 7:00 and 9:00 a.m.). Other details for laboratory measurements were published elsewhere [18].

Definitions

Exposures

The duration of BF has been reported by the response of the samples in months. The total cumulative BF duration for each subject was calculated by collecting all BF months. The duration of BF (as an exposure variable) was calculated in multiparous women who had previously BF and developed MetS in their next pregnancy based on the total duration of BF before the event of MetS. Participants reported exclusive BF duration and the duration of continuing BF accompanied by complementary foods, named partial BF, by answering two questions separately. According to the world health organization (WHO) definition, at first, after delivery, infants, until (maximum) six months of age, receive exclusive BF without receiving complementary foods. Also in Iran, the definition of exclusive BF is only giving breast milk to the infant till the end of 6 months after birth, minus giving any solid food or other liquid, even water, except for vitamin drops or syrups, mineral supplements, and medications prescribed by the doctor [21, 22]. Then partial BF contains BF should be accompanied by complementary foods gradually [23].

GDM was defined as any degree of glucose intolerance with beginning or first recognition during pregnancy [24]. Participants reported a history of GDM. The sensitivity and specificity of self-reported GDM have been revealed to be 100% and 92%, respectively [11].

Outcome

MetS was defined according to the Joint Interim Statement [25], as the presence of any three out of the five following risk factors: (1) Abdominal obesity: WC ≥ 90 cm, accordingly population- and country-specific cutoffs for Iranians [26], (2) fasting plasma glucose (FPG) ≥ 100 mg/dL or drug treatment, (3) Fasting triglycerides (TG) ≥ 150 mg/dL or drug treatment; (4) Fasting high-density lipoprotein cholesterol (HDL-C) < 50 mg/dL in women or drug treatment and (5) Elevated blood pressure (BP) defined as systolic blood pressure (SBP) ≥ 130 mm Hg, diastolic blood pressure (DBP) ≥ 85 mmHg or antihypertensive drug treatment.

Statistical methods

Continuous variables were checked for normality based on the one-sample Kolmogorov–Smirnov test. They were presented as mean (standard deviation) if they had a normal distribution or median with an interquartile range (IQR25–75) for variables with skewed distribution. Categorical variables were presented as numbers and percentages. Demographic and clinical characteristics of women were compared according to GDM/or MetS status using the student t-test or chi-square test for continuous or categorical data, respectively. The Mann–Whitney test was applied to compare variables with skewed distribution.

Data collection for this investigation began in January 1999 and ran until March 2022, with follow-up periods of three years. There has been data collection for a cumulative median follow-up of 16.3 years (interquartile range: 11.9–19.3). We applied the Cox regression model to assess the hazard ratios (HRs) and 95% confidence intervals (CIs) for BF (exclusive, partial, and total) association with MetS in participants. Initially, all risk factors were included in the univariate model. Next, variables, which were found to be significant in the univariate model (P < 0.2), were also included in the multivariate model. The survival time was considered the interval between the age at the entrance and the age (in years) when MetS was detected for the first time or in the last follow-up. Women, who did not develop MetS by the end of the follow-ups, were considered lost to follow-up or censored.

Both unadjusted and adjusted Cox regression models were applied. Confounding factors, including age, BMI, family history of diabetes mellitus (DM) at baseline, physical activity, education, and parity were entered into the multivariate Cox model (physical activity, education, and parity were considered time-dependent covariates in the model).

Interaction analysis was applied to explore if the effect of BF (exclusive, partial, and total) on the hazard of the MetS is affected by GDM status. For this purpose, an interaction term of these two (BF and GDM) was entered in the Cox regression model, and HRs as well as their 95% confidence intervals, were estimated.

As a sensitivity analysis, to eliminate the effect of menopause status during follow-up, menopausal women were excluded, and the association of BF with MetS was reassessed.

Statistical analysis was performed using the software package STATA (version 13; STATA Inc., College Station, TX, USA); the significance level was set at p < 0.05.

Results

Of 1176 eligible participants, 175 (14.9%) women had a history of GDM, and 1001 (85.1%) women without a history of GDM were recruited. The median and interquartile range of follow-up time for the current analysis were 16.3 (11.9, 19.3) years. During the follow-up, 88 (50.3%) women from the GDM group and 377 (37.3%) women from the non-GDM group developed MetS. The characteristics of women according to GDM and MetS status were presented in Tables 1 and 2, respectively. Based on the potential variables in Tables 1 and 2, we considered age, BMI, family history of DM, physical activity, education, parity, and smoking in the univariate model. Among them, only the variable "smoking" with a p-value greater than 0.2 did not enter the multivariate Cox model. Among the components of MetS, women with a history of GDM had higher values of WC, FPG, and TG than non-GDM women (Table 1). All components of the MetS were significantly higher in women who were incident the MetS during the study than in non-suffering women. Lower physical activity was reported by women who were incident MetS than others (33.5% vs. 40.0%) (Table 2).

Table 1 Baseline characteristics of participants according to GDM history
Full size table
Table 2 Baseline characteristics of participants according to MetS status
Full size table

Table 3 summarizes the results of the Cox regression analysis regarding the association between the BF and the hazard of MetS. There are three models reported in Table 3. To eliminate the influence of collinearity, total, partial, or exclusive BF is independently incorporated into each model. Adjusted Cox regression analysis showed that an increase in total BF per month was related to a 2% decrease in the risk of MetS incidence (HRadj: 0.98, 95% CI: 0.98–0.99, p-value = 0.001). Moreover, a per-month increase in exclusive BF was associated with a 3% lower risk of MetS incidence (HRadj: 0.97, 95% CI: 0.95–0.98, p-value = 0.03).

Table 3 Unadjusted and multivariable-adjusted* Cox regression analysis for the effect of BF on hazards (95% CIs) of incident MetS
Full size table

Table 4 reports the result of the interaction analysis to explore the interaction effect of GDM and BF duration (exclusive, partial, and total) on the incidence of MetS. The only significant interaction effect was revealed with exclusive BF in both unadjusted and adjusted models. The adjusted model showed that an increase in exclusive BF per month in women with a history of GDM decreased the hazard of MetS incidence by 7% compared to non-GDM women (HRadj: 0.93, 95% CI: 0.88–0.98, p-value = 0.01).

Table 4 Interaction analysis for the association between BF*GDM and hazard ratio of MetS
Full size table

The results of subgroup analysis for exploring the effect of BF on the hazard of MetS in those with and without GDM are presented as Additional file 1: Table S1. We found that the hazard ratio per month of BF has a protective effect on MetS in both groups of GDM (total or partial BF), except for exclusive BF, which was not statistically significant in the non-GDM subgroup.

During follow-up, 181 (15.4%) women went through menopause. Additional file 1: Table S2, S3 show the HR (95% CI) of MetS for the effect of BF duration in non-menopausal women. Additional file 1: Table S2 reveals BF duration types in all nonmenopausal participants statistically significantly decreased the risk of MetS incidence (p-value < 0.05). Additional file 1: Table S3 shows that the interaction between BF duration and GDM was significant for BF duration (exclusive, partial, and total).

In non-menopausal women, per month increase in total BF decreased the risk of MetS in GDM women by 2% (HRadj: 0.98, 95% CI: 0.96–0.99, p-value = 0.01); 3% reduction in the risk of MetS was observed for GDM women with increasing one month partial BF (HRadj: 0.97, 95% CI: 0.96–0.99, p-value = 0.02); and was shown in exclusive BF for GDM women was associated with decreasing 9% in hazard of MetS (HRadj: 0.91, 95% CI: 0.85–0.97, p-value = 0.004) compared to non-GDM women.

Discussion

Our findings illustrated that the duration of BF was associated with a lower risk of MetS incidence even after adjusting for potential confounders, including age, BMI, family history of DM at baseline, physical activity, education, and parity. Each month of the BF duration reduced the incidence of MetS by 2%. Furthermore, a longer duration of exclusive BF further reduced the risk of MetS incidence in women, especially in those with a history of GDM (by 7% each month of exclusive BF) after adjusting for potential confounders.

Several studies have reported the beneficial effects of lactation on maternal cardiometabolic blood profiles [12]. A few studies investigate the effect of BF duration on metabolic syndrome compared to women with a history of GDM and non-GDM via a longitudinal study [11]. In agreement with our study, Gunderson et al. reported a stronger protective association for each month of BF with the incidence of the MetS, which was 39–56% for non-GDM women and 44–86% for GDM women [11].

Several mechanisms may partly explain the beneficial effect of BF on the MetS and its components.

The prolactin increase begins during pregnancy, reaches peak concentration level till term, and remains above nonpregnant women's level with pulsatile secretion up to weaning [27]. Previous experimental research on prolactin receptor knockout mice revealed a physiological role in pancreatic islet formation and function for prolactin [28]. The pathogeneses of MetS pertaining to pregnancy and BF may be partially explained by the intricate and interconnected signaling pathways that exist between the brain, gut, and adipose tissue and regulate appetite, energy homeostasis, and fat mass maintenance [29,30,31,32,33,34]. In diabetic rats, the physiological elevation of serum prolactin levels during pregnancy; and postpartum Improves insulin resistance and secretion [35]. Additionally, maternal total energy expenditure increases during milk production by 15–25% [36, 37], resulting in significant postpartum weight loss that improves cardiometabolic status. Despite substantial declines in total body fat mass within 3–6 months postpartum being reported in lactating mothers than in nonlactating [38], studies reported controversial results about lactation affecting body composition and regional fat distribution [38,39,40,41].

A direct association between BF duration with ghrelin and protein-peptide YY has been illustrated [42]. By contrast, an adverse association between ghrelin and the risk of MetS and DM was reported [43]. Ghrelin and protein-peptide YY affect metabolism and appetite regulation; ghrelin plays a crucial role in energy homeostasis and glucose regulation, and signals of protein-peptide YY to the brain lead to diminishing food consumption [44,45,46]. Therefore the possible beneficiary effect of lactation may partly be explained by its effect on ghrelin.

In addition, BF may improve the overall status of mothers through stress reduction. Consequently, it downgrades activation of the hypothalamic–pituitary–adrenal axis and inordinate vagal tones. A significant decline in levels of basal norepinephrine, ACTH, cortisol, and glucose responses to exercise has also been reported in lactating women compared to nonlactating maternal [47].

Previous studies revealed that BF, especially prolonged BF duration, reduces insulin resistance. As a result, each one-year BF duration could be reduced by more than 10% of MetS [48, 49]. It has been shown that suppressing islet menin levels stimulates b-cell proliferation during pregnancy by prolactin to adapt to the dynamic physiological requirements [50]. Notwithstanding their elevated glucose production levels, lower insulin secretion and lower glucose levels were reported in lactating women [51]. Glucose circulating levels have an adverse association with the duration of BF, the effect that remains even many years after stopping BF. It has been shown that serum levels of glucose in women with ≥ 10 years BF are significantly lower than those without lactation [52]; moreover, they reported lower serum triglyceride (0.66 mmol/L vs. 0.91 mmol/L, p = 0.001) and serum cholesterol (4.32 mmol/L vs. 4.78 mmol/L, p = 0.004), as well as a lower waist-to-hip ratio (0.77 vs. 0.81, p = 0.001), in women with prolonged lactation [52]. Although the beneficiary impact of prolonged BF on blood pressure was well documented, The persistence of this effect years after stopping BF is unclear [48, 53, 54].

According to our findings, women with a history of GDM had higher BF duration, exclusive BF, and BF with complementary foods than those without a history of GDM. However, this result contrasts with other studies that reported a shorter period of lactation [55,56,57,58]. They assumed that the shorter duration of lactation in women with a history of GDM might be explained through various maternal and fetal morbidities among them [16] that postpone lactogenesis [17] and/or the infants' poor sucking type. It has been shown that the overall rate of exclusively BF duration (37%) in upper-middle-income countries was lower than in others [59]. The longer duration of lactation in GDM women in the present study may be due to the timely prenatal education and intervention that have been available through universal prenatal programs [60]. Besides, supporting BF in the hospital, by health care providers immediately after delivery and during the postpartum period, and by family and community support to persuade BF in Iran is essential [61]. Notably, this purposeful BF support in GDM women is more important and has several advantages for mothers and their offspring.

The thyroid hormone plays an essential role in body metabolism and is one of the several factors influencing body weight [62]. It has been demonstrated that greater levels of thyroid hormones within the normal range are advantageous for metabolism and weight maintenance [63]. A higher thyroid hormone level has been reported in women with a history of GDM associated with a longer BF duration. Findings of research (2018) on women with a history of GDM illustrated that a longer duration of BF can be associated with greater serum fT3 concentrations and fT3:fT4 ratio of 9–16 years postpartum [15] and fT3 is the form of T3 that is in circulation, and the fT3:fT4 ratio is representative of the transformation from T4 to T3. Therefore, the reduction of the incidence of the syndrome in women with a history of GDM may be partly explained through this association; unfortunately, thyroid assessments were not available for the present study.

We found that the beneficiary effect of BF on MetS is enhanced by exclusive BF, so exclusive BF may be more effective in reducing the risk of MetS than total or partial BF among women with a history of GDM. It has been shown that more weight loss occurs following exclusive BF. Furthermore, it is notable that weight loss increases after continuing at least six months of BF [64]. Moreover, women with exclusive BF at 6–9 weeks postpartum had a lower risk for long-term type 2 diabetes mellitus (52% fewer) than those with the exclusive formula [65]. Besides, prior observational studies revealed that an exclusive and longer BF duration might prevent type 2 diabetes mellitus in women with GDM in the future.

Nonetheless, confirmation of these results depends on conducting studies such as longitudinal studies [66]. In this regard, prolactin plays a key role in explaining the beneficial effects of exclusive BF and longer BF duration on MetS incidence in the future [67].

Limitation and strenght

Our study has several strengths. It was a population-based prospective cohort with approximately two decades of follow-up and several precise measurements of cardio-metabolic risk factors. Also, the accurate measurements and statistical analysis with specific adjustments of influential confounders and conducting an interaction analysis to explore if the effect of BF on MetS is affected by GDM status helped the study reach more powerful results. However, there are several potential limitations that several potential limitations need to be acknowledged. Several confounders, including lifestyle factors and genetic background, have not been addressed in the current study. The history of GDM was self-reported by participants. However, in our country, GDM screening is a routine program conducted as a part of prenatal care. The high sensitivity and specificity of the self-reported assessment of GDM were reported previously. However, another study illustrated the high sensitivity and specificity of GDM through self-report [11]. Our results may be influenced by recall bias secondary to the self-reported duration of BF. Since BF is a crucial period in every woman's life, remembering its duration is reliable even after many years. Although, the results of the research elucidated that maternal recall of BF duration is accurate up to 6 years after birth, and as regards the duration of our follow-ups was three years, it may recall of BF exclusivity is not good at six months after birth [68].

Conclusion

Our findings showed the protective effect of BF on the incidence of the MetS that increased by prolonged lactation. This effect is more pronounced in those with a longer duration of BF. This beneficial effect was more shown in exclusive BF. Furthermore, a much stronger beneficial effect of exclusive BF duration on the risk of MetS incidence was observed in women with a history of GDM compared to non-GDM. Besides our findings revealed that the promotion and support of continued BF is an opportunity to improve the long-term health of women after a GDM-complicated pregnancy. BF may be considered a simple protective factor that diverts the adverse effects of pregnancy on the lifetime cardio-metabolic status of women. Conducting well-designed comprehensive prospective population-based studies is recommended considering lifestyle and genetic parameters.

Availability of data and materials

The data sets produced through the current study are not publicly available but are available from the corresponding author on reasonable request.

Abbreviations

Mets:

Metabolic syndrome

GDM:

Gestational diabetes mellitus

BF:

Breastfeeding

HR:

Hazard ratio

CI:

Confidence interval

WHO:

World health organization

NCD:

Non communicable disease

CVD:

Cardiovascular disease

FPG:

Fasting plasma glucose

TG:

Triglycerides

SBP:

Systolic blood pressure

DBP:

Diastolic blood pressure

HDL-C:

High-density lipoprotein cholesterol

References

  1. Hsu C-N, Hou C-Y, Hsu W-H, Tain Y-L. Early-life origins of metabolic syndrome: mechanisms and preventive aspects. Int J Mol Sci. 2021;22 (21):11872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. World Health Organization. Complementary feeding: report of the global consultation, and summary of guiding principles for complementary feeding of the breastfed child. 2003.

  3. Spiro A. The public health benefits of breastfeeding. SAGE PUBLICATIONS LTD 1 OLIVERS YARD, 55 CITY ROAD, LONDON EC1Y 1SP, ENGLAND; 2017. p. 307–8.

  4. Bosch OJ. Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin. Horm Behav. 2011;59 (2):202–12.

    Article  CAS  PubMed  Google Scholar 

  5. Krause KM, Lovelady CA, Peterson BL, Chowdhury N, Østbye T. Effect of breast-feeding on weight retention at 3 and 6 months postpartum: data from the North Carolina WIC Programme. Public Health Nutr. 2010;13 (12):2019–26.

    Article  PubMed  Google Scholar 

  6. McClure CK, Catov J, Ness R, Schwarz EB. Maternal visceral adiposity by consistency of lactation. Matern Child Health J. 2012;16 (2):316–21.

    Article  PubMed  Google Scholar 

  7. Neelon SEB, Stroo M, Mayhew M, Maselko J, Hoyo C. Correlation between maternal and infant cortisol varies by breastfeeding status. Infant Behav Dev. 2015;40:252–8.

    Article  Google Scholar 

  8. Chen H, Wang J, Zhou W, Yin H, Wang M. Breastfeeding and risk of rheumatoid arthritis: a systematic review and metaanalysis. J Rheumatol. 2015;42 (9):1563–9.

    Article  PubMed  Google Scholar 

  9. Fox M, Berzuini C, Knapp LA. Maternal breastfeeding history and Alzheimer’s disease risk. J Alzheimers Dis. 2013;37 (4):809–21.

    Article  CAS  PubMed  Google Scholar 

  10. Gunderson EP, Quesenberry CP Jr, Ning X, Jacobs DR Jr, Gross M, Goff DC Jr, et al. Lactation duration and midlife atherosclerosis. Obstet Gynecol. 2015;126 (2):381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gunderson EP, Jacobs DR Jr, Chiang V, Lewis CE, Feng J, Quesenberry CP Jr, et al. Duration of lactation and incidence of the metabolic syndrome in women of reproductive age according to gestational diabetes mellitus status: a 20-Year prospective study in CARDIA (Coronary Artery Risk Development in Young Adults). Diabetes. 2010;59 (2):495–504.

    Article  CAS  PubMed  Google Scholar 

  12. Tørris C, Bjørnnes AK. Duration of lactation and maternal risk of metabolic syndrome: a systematic review and meta-analysis. Nutrients. 2020;12 (9):2718.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Care D. Classification and diagnosis of diabetes. Diabetes Care. 2016;39 (1):S13–22.

    Google Scholar 

  14. Atlas D. IDF diabetes atlas. International Diabetes Federation (9th editio) http://www.idf.org/about-diabetes/facts-figures. 2019.

  15. Panuganti PL, Hinkle SN, Rawal S, Grunnet LG, Lin Y, Liu A, et al. Lactation duration and long-term thyroid function: A study among women with gestational diabetes. Nutrients. 2018;10 (7):938.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Fallon A, Dunne F. Breastfeeding practices that support women with diabetes to breastfeed. Diabetes Res Clin Pract. 2015;110 (1):10–7.

    Article  PubMed  Google Scholar 

  17. Matias SL, Dewey KG, Quesenberry CP Jr, Gunderson EP. Maternal prepregnancy obesity and insulin treatment during pregnancy are independently associated with delayed lactogenesis in women with recent gestational diabetes mellitus. Am J Clin Nutr. 2014;99 (1):115–21.

    Article  CAS  PubMed  Google Scholar 

  18. Azizi F, Zadeh-Vakili A, Takyar M. Review of rationale, design, and initial findings: Tehran Lipid and Glucose Study. Int J Endocrinol Metab. 2018;16 (4):8.

    Google Scholar 

  19. Ainsworth BE, Jacobs DR Jr, Leon AS. Validity and reliability of self-reported physical activity status: the Lipid Research Clinics questionnaire. Med Sci Sports Exerc. 1993;25 (1):92–8.

    Article  CAS  PubMed  Google Scholar 

  20. Momenan AA, Delshad M, Sarbazi N, Rezaei-Ghaleh N, Ghanbarian A, Azizi F. Reliability and validity of the Modifiable Activity Questionnaire (MAQ) in an Iranian urban adult population. Arch Iran Med. 2012;15 (5):279–82.

    PubMed  Google Scholar 

  21. Taheri Z, Bakouei F. The relationship between mothers’ empowerment in breastfeeding with exclusive breast feeding in infants. J Babol Univ Med Sci. 2019;21 (1):85–92.

    Google Scholar 

  22. Muchacha M, Mtetwa E. Social and economic barriers to exclusive breast feeding in rural Zimbabwe. Int J MCH AIDS. 2015;3 (1):16.

    PubMed  PubMed Central  Google Scholar 

  23. WHO. Complementary feeding: report of the global consultation, and summary of guiding principles for complementary feeding of the breastfed child. 2003.

  24. Association AD. Classification and diagnosis of diabetes: Standards of Medical Care in Diabetes—2020. Diabetes Care. 2020;43 (1):S14–31.

    Article  Google Scholar 

  25. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation. 2009;120 (16):1640–5.

    Article  CAS  PubMed  Google Scholar 

  26. AZIZI F, Khalili D, Aghajani H, Esteghamati A, Hosseinpanah F, DELAVARI A, et al. Appropriate waist circumference cut-off points among Iranian adults: the first report of the Iranian National Committee of Obesity. 2010.

  27. Ramos-Román M. Prolactin and lactation as modifiers of diabetes risk in gestational diabetes. Horm Metab Res. 2011;43 (09):593–600.

    Article  PubMed  Google Scholar 

  28. Freemark M, Avril I, Fleenor D, Driscoll P, Petro A, Opara E, et al. Targeted deletion of the PRL receptor: effects on islet development, insulin production, and glucose tolerance. Endocrinology. 2002;143 (4):1378–85.

    Article  CAS  PubMed  Google Scholar 

  29. de Farias LD, de Freitas DF, Machado AS, Crespo TS, Santos SHS. Angiotensin- (1–7), adipokines and inflammation. Metabolism. 2019;95:36–45.

    Article  Google Scholar 

  30. Blüher M, Mantzoros CS. From leptin to other adipokines in health and disease: facts and expectations at the beginning of the 21st century. Metabolism. 2015;64 (1):131–45.

    Article  PubMed  Google Scholar 

  31. Deng Y, Scherer PE. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N Y Acad Sci. 2010;1212 (1):E1–19.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. The lancet. 2005;365 (9468):1415–28.

    Article  CAS  Google Scholar 

  33. Laclaustra M, Corella D, Ordovas JM. Metabolic syndrome pathophysiology: the role of adipose tissue. Nutr Metab Cardiovasc Dis. 2007;17 (2):125–39.

    Article  CAS  PubMed  Google Scholar 

  34. Rask-Madsen C, Kahn CR. Tissue–specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler Thromb Vasc Biol. 2012;32 (9):2052–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Park S, Kim DS, Daily JW, Kim SH. Serum prolactin concentrations determine whether they improve or impair β-cell function and insulin sensitivity in diabetic rats. Diabetes Metab Res Rev. 2011;27 (6):564–74.

    Article  CAS  PubMed  Google Scholar 

  36. Dewey KG. Energy and protein requirements during lactation. Annu Rev Nutr. 1997;17:19.

    Article  CAS  PubMed  Google Scholar 

  37. Butte NF, Hopkinson JM, Mehta N, Moon JK, Smith EOB. Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. Am J Clin Nutr. 1999;69 (2):299–307.

    Article  CAS  PubMed  Google Scholar 

  38. Butte NF, Hopkinson JM. Body composition changes during lactation are highly variable among women. J Nutr. 1998;128 (2):381S-S385.

    Article  CAS  PubMed  Google Scholar 

  39. Sohlström A, Forsum E. Changes in adipose tissue volume and distribution during reproduction in Swedish women as assessed by magnetic resonance imaging. Am J Clin Nutr. 1995;61 (2):287–95.

    Article  PubMed  Google Scholar 

  40. Sadurskis A, Kabir N, Wager J, Forsum E. Energy metabolism, body composition, and milk production in healthy Swedish women during lactation. Am J Clin Nutr. 1988;48 (1):44–9.

    Article  CAS  PubMed  Google Scholar 

  41. Brewer MM, Bates MR, Vannoy LP. Postpartum changes in maternal weight and body fat depots in lactating vs nonlactating women. Am J Clin Nutr. 1989;49 (2):259–65.

    Article  CAS  PubMed  Google Scholar 

  42. Stuebe AM, Mantzoros C, Kleinman K, Gillman MW, Rifas-Shiman S, Gunderson EP, et al. Duration of lactation and maternal adipokines at 3 years postpartum. Diabetes. 2011;60 (4):1277–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ukkola O, Pöykkö S, Päivänsalo M, Kesäniemi YA. Interactions between ghrelin, leptin and IGF-I affect metabolic syndrome and early atherosclerosis. Ann Med. 2008;40 (6):465–73.

    Article  CAS  PubMed  Google Scholar 

  44. Kizaki T, Maegawa T, Sakurai T, Ogasawara J-E, Ookawara T, Oh-ishi S, et al. Voluntary exercise attenuates obesity-associated inflammation through ghrelin expressed in macrophages. Biochem Biophys Res Commun. 2011;413 (3):454–9.

    Article  CAS  PubMed  Google Scholar 

  45. Holzer P, Reichmann F, Farzi A, Neuropeptide Y. peptide YY and pancreatic polypeptide in the gut–brain axis. Neuropeptides. 2012;46 (6):261–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. McGowan B, Bloom S. Peptide YY and appetite control. Curr Opin Pharmacol. 2004;4 (6):583–8.

    Article  CAS  PubMed  Google Scholar 

  47. Altemus M, Deuster PA, Galliven E, Carter C, Gold PW. Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. J Clin Endocrinol Metab. 1995;80 (10):2954–9.

    CAS  PubMed  Google Scholar 

  48. Ciampo LAD, Ciampo IRLD. Breastfeeding and the Benefits of Lactation for Women’s Health. Rev Bras Ginecol Obstet. 2018;40:354–9.

    Article  PubMed  Google Scholar 

  49. Choi SR, Kim YM, Cho MS, Kim SH, Shim YS. Association between duration of breast feeding and metabolic syndrome: The Korean National Health and Nutrition Examination Surveys. J Womens Health. 2017;26 (4):361–7.

    Article  Google Scholar 

  50. Karnik SK, Chen H, McLean GW, Heit JJ, Gu X, Zhang AY, et al. Menin controls growth of pancreatic ß-cells in pregnant mice and promotes gestational diabetes mellitus. Science. 2007;318 (5851):806–9.

    Article  CAS  PubMed  Google Scholar 

  51. Gunderson EP, Lewis CE, Lin Y, Sorel M, Gross M, Sidney S, et al. Lactation duration and progression to diabetes in women across the childbearing years: the 30-year CARDIA study. JAMA Intern Med. 2018;178 (3):328–37.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Tørris C, Thune I, Emaus A, Finstad SE, Bye A, Furberg A-S, et al. Duration of lactation, maternal metabolic profile, and body composition in the Norwegian EBBA I-study. Breastfeed Med. 2013;8 (1):8–15.

    Article  PubMed  Google Scholar 

  53. Ebina S, Kashiwakura I. Influence of breastfeeding on maternal blood pressure at one month postpartum. Int J Women’s Health. 2012;4:333–9.

    Google Scholar 

  54. Zhang B-Z, Zhang H-Y, Liu H-H, Li H-J, Wang J-S. Breastfeeding and maternal hypertension and diabetes: a population-based cross-sectional study. Breastfeed Med. 2015;10 (3):163–7.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Nommsen-Rivers LA, Chantry CJ, Dewey KG. Early breastfeeding outcomes in gestational diabetic primiparas delivering term infants. FASEB J. 2010;24:914.

    Article  Google Scholar 

  56. Doughty K, Reeves K, Ronnenberg A, Qian J, Sibeko L. Breastfeeding intentions and practices among women in the US with gestational diabetes mellitus. FASEB J. 2015;29:581–9.

    Article  Google Scholar 

  57. Finkelstein S, Keely E, Feig D, Tu X, Yasseen A III, Walker M. Breastfeeding in women with diabetes: lower rates despite greater rewards, A population-based study. Diabetic Med. 2013;30 (9):1094–101.

    Article  CAS  PubMed  Google Scholar 

  58. Nguyen PTH, Pham NM, Chu KT, Van Duong D, Van Do D. Gestational diabetes and breastfeeding outcomes: a systematic review. Asia Pac J Public Health. 2019;31 (3):183–98.

    Article  PubMed  Google Scholar 

  59. Victora CG, Bahl R, Barros AJ, França GV, Horton S, Krasevec J, et al. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet. 2016;387 (10017):475–90.

    Article  PubMed  Google Scholar 

  60. You H, Lei A, Xiang J, Wang Y, Luo B, Hu J. Effects of breastfeeding education based on the self-efficacy theory on women with gestational diabetes mellitus: A CONSORT-compliant randomized controlled trial. Medicine. 2020;99:16.

    Article  Google Scholar 

  61. Ghasemi V, Simbar M, Banaei M, SaeiGhareNaz M, Jahani Z, Nazem H. The effect of interventions on breastfeeding self-efficacy by using Bandura’s theory in Iranian mothers: a systematic review. Int J Pediatr. 2019;7 (8):9939–54.

    Google Scholar 

  62. Chang TI, Nam JY, Shin SK, Kang EW. Low triiodothyronine syndrome and long-term cardiovascular outcome in incident peritoneal dialysis patients. Clin J Am Soc Nephrol. 2015;10 (6):975–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu G, Liang L, Bray GA, Qi L, Hu FB, Rood J, et al. Thyroid hormones and changes in body weight and metabolic parameters in response to weight loss diets: the POUNDS LOST trial. Int J Obes. 2017;41 (6):878–86.

    Article  CAS  Google Scholar 

  64. Dewey KG, Heinig MJ, Nommsen LA. Maternal weight-loss patterns during prolonged lactation. Am J Clin Nutr. 1993;58 (2):162–6.

    Article  CAS  PubMed  Google Scholar 

  65. Gunderson EP, Hurston SR, Ning X, Lo JC, Crites Y, Walton D, et al. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med. 2015;163 (12):889–98.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Tanase-Nakao K, Arata N, Kawasaki M, Yasuhi I, Sone H, Mori R, et al. Potential protective effect of lactation against incidence of type 2 diabetes mellitus in women with previous gestational diabetes mellitus: a systematic review and meta-analysis. Diabetes Metab Res Rev. 2017;33 (4): e2875.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Retnakaran R, Ye C, Kramer CK, Connelly PW, Hanley AJ, Sermer M, et al. Maternal serum prolactin and prediction of postpartum β-cell function and risk of prediabetes/diabetes. Diabetes Care. 2016;39 (7):1250–8.

    Article  CAS  PubMed  Google Scholar 

  68. Bland RM, Rollins NC, Solarsh G, Van den Broeck J, Coovadia HM. Maternal recall of exclusive breast feeding duration. Arch Dis Child. 2003;88 (9):778–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to all the participants of this research for the considerable time and effort given to the present study.

Thanks are also owing to the research staff at the TLGS Unit and the Research Endocrine Laboratory personnel.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Reproductive Endocrinology Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Maryam Farahmand, Maryam Rahmati & Fahimeh Ramezani Tehrani

  2. Endocrine Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Fereidoun Azizi

Authors
  1. Maryam Farahmand
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maryam Rahmati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fereidoun Azizi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fahimeh Ramezani Tehrani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MF contributed to the study design and execution, literature review, data analysis, manuscript drafting, and critical discussion. MR contributed to the study design, data analysis, and manuscript drafting. FA contributed to the study design and manuscript drafting. FRT contributed to the study design and execution, data analysis, manuscript drafting, and critical discussion. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fahimeh Ramezani Tehrani.

Ethics declarations

Ethics approval and consent to participate

The Research Institute for Endocrine Sciences ethics committee approved the study (IR.SBMU.ENDOCRINE.REC.1401.046). Written informed consent was obtained from all subjects before the initiation of the study.

Consent for publication

Consent to publish has been received from all participants of the study.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

Unadjusted and multivariable-adjusted* Cox regression analysis for the effect of BF on hazards (95% CIs) of incident MetS in GDM and non-GDM groups. Table S2. The Cox regression model explores BF's effect on the hazard of MetS incidence for non-menopausal women. Table S3. Cox regression model with interaction effect of BF*GDM on a hazard ratio of MetS for non-menopausal women.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farahmand, M., Rahmati, M., Azizi, F. et al. Lactation duration and lifetime progression to metabolic syndrome in women according to their history of gestational diabetes: a prospective longitudinal community-based cohort study. J Transl Med 21, 177 (2023). https://doi.org/10.1186/s12967-023-04005-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12967-023-04005-w

Keywords

Journal of Translational Medicine

ISSN: 1479-5876

Contact us