Weight change/body composition.

A 2014 systematic review by Neville et al., based on 37 prospective studies and eight retrospective studies, assessed the relationship between breastfeeding and changes in postpartum weight or body composition in mothers ≤2 years postpartum [17]. Most studies found little or no association between breastfeeding and either change in postpartum weight or maternal body composition.

In 2015, a systematic review conducted by Chowdury et al. [15] updated the review on postpartum weight change by Neville et al. [17] with five additional studies. The authors concluded that there were no clear associations between breastfeeding and postpartum weight change, with factors such as age, gestational weight gain and pre-pregnancy weight possibly confounding these relationships.

Type 2 diabetes.

In a 2014 review and meta-analysis based on six cohort studies, the longest duration of lifetime lactation was associated with a 32% reduction in relative risk of type 2 diabetes compared with the shortest duration [16]. This finding was in line with a later review of the same primary studies [15] and an earlier systematic review [18].

MS.

MS is a cluster of conditions which can increase the risk for diabetes and CVD. Table 1 describes studies with MS as the outcome. Five studies examined the association between breastfeeding and MS [12,22–24,31]. Studies adhered to the National Cholesterol Education Program Adult Treatment Panel III criteria [38] to define MS, which is based on the presence of three of more of the following risk determinants: abdominal obesity, elevated triglyceride levels, reduced high-density lipoprotein cholesterol levels, elevated blood pressure, and elevated fasting glucose levels [38]. The findings from the three cross-sectional studies, conducted among women of different age categories, were mixed [22–24]. One study from the US found a significant protective association of both lactation history and lifetime lactation duration with MS in a dose-response manner in middle-aged, parous premenopausal women from various ethnic backgrounds [22]. Another US study reported a significant association between lactation history and the prevalence of MS in parous women aged ≥20 years. However, this association was no longer significant after additional adjustment for BMI [23]. The third study did not find any association between lactation history and the prevalence of the MS in postmenopausal Korean women [24].

Both prospective studies found significant protective effects of lifetime lactation duration on incident MS [12,31]. One study following Iranian women over 9 years observed a significant association between 13–23 months lifetime lactation duration and higher incidence of MS compared with ≥24 months [31]. The other study showed that lifetime lactation duration of 6–9 and >9 months was significantly associated with a lower incidence of MS compared with 0–1 month lactation, among American women of reproductive age followed over a 20-year period [12].

Metabolic risk factors.

Table 2 provides a summary of studies with metabolic risk factors as the outcomes. Five studies (three cross-sectional/retrospective, two prospective) assessed the relation between breastfeeding and metabolic risk factors [25,26,32,33,36]. All three cross-sectional/retrospective studies reported a protective association of breastfeeding with metabolic risk factors [25,26,36]. One study involving Portuguese mothers who were examined at 4 years postpartum, showed that women who breastfed their child for >26 weeks were less likely to be obese and have and an adverse metabolic profile. However, there was no association between breastfeeding and excessive weight associated with a healthy metabolic profile [25]. Another cross-sectional/retrospective study found that lifetime lactation duration is associated in a dose-response fashion with a more favorable cardiovascular risk profile, including lipids, in a large sample of Norwegian mothers later in life [26]. Similarly, the third cross-sectional/retrospective study found a dose-response relationship between lifetime lactation duration and hyperlipidemia in a large sample of US mothers [36].

The findings from relatively small prospective studies were mixed [32,33]. One US prospective study examining 3-year changes in metabolic risk factors from pre-pregnancy to post-weaning showed that breastfeeding is associated with a more favorable metabolic risk profile in the postpartum period [32]. In contrast, the other US prospective study did not find any association between lactation duration and metabolic risk at 3 years postpartum after adjusting for pre-pregnancy BMI [33].

Hypertension.

Table 3 describes studies with hypertension as the outcome. Seven studies examined the association between breastfeeding and hypertension [7,8,26–28,36,37]. Breastfeeding was associated with lower odds of hypertension in all four cross-sectional/retrospective studies [26–28,36]. Both lactation history and duration were associated with reduced odds of hypertension in middle-aged and older Chinese mothers [27]. Similarly, in a large sample of Australian women aged ≥45 years, lactation history was protective compared to parous women who never breastfed or nulliparous women [28]. Lifetime lactation duration of >6 months, or >3 months/child, was significantly associated with lower odds of hypertension, in women aged 45–64 years compared with parous women who did not breastfeed. The odds of hypertension decreased with longer breastfeeding durations and were mostly not significant in women ≥64 years. In another cross-sectional/retrospective study from Norway, while there were no clear associations in mothers ≥50 years, mothers aged <50 years who had never lactated had higher odds of hypertension than those who had lactated ≥24 months in their lifetime [26]. In contrast, lifetime lactation duration was significantly associated with lower odds of hypertension in postmenopausal US women ≥50 years [36].

Breastfeeding also appeared to be protective in two large prospective studies [7,8]. In a US cohort of parous women, those who did not breastfeed were more likely to develop hypertension compared with those who breastfed their first child for ≥12 months or exclusively breastfed their first child for ≥6 months [7]. Lactation history, lifetime lactation duration between 1–18 months and average lactation duration between 1–9 months were also protective among a large cohort of premenopausal Korean women followed for six years [8]. In a large cluster RCT from Belarus, despite greater breastfeeding duration and exclusivity achieved among breastfeeding mothers randomized to a breastfeeding promotion intervention compared to usual care, there was no significant difference in blood pressure between mothers receiving the intervention and those allocated to the usual care group. However, this was not an RCT of breastfeeding per se but of factors aimed at promoting breastfeeding behaviour. In addition, a marginally significant association was found between lactation duration and lower blood pressure at 11.5 years postpartum in observational analyses in the same sample regardless of treatment allocation [37].

Inflammatory markers and adipokines.

Table 4 provides a summary of studies with inflammatory markers, adipokines and subclinical cardiovascular disease as the outcomes. Only two papers from the same sample were identified [33,34]. In one paper, two inflammatory markers: C-reactive protein (CRP), commonly associated with cardiovascular health outcomes [39], and interleukin-6, a proinflammatory cytokine that induces the hepatic production of CRP [40], were examined, but neither was significantly related to lactation duration at 3 years postpartum among 175 women with fasting blood samples after adjusting for pre-pregnancy BMI [33]. The other paper [34] examined adipokines, which are cytokines secreted by adipose tissue that are involved in inflammatory responses and associated with metabolic disease risk [41]. At 3 years postpartum, longer lactation duration was associated with higher levels of ghrelin and peptide YY, both involved in appetite regulation and associated with reduced risk of metabolic disease [34].

Subclinical cardiovascular disease.

Early physiologic changes in vascular health such as calcified atherosclerotic plaques and increases in carotid adventitial diameter can be detected and identify patients at increased risk of future cardiovascular events [42–44]. Two cross-sectional/retrospective studies from the US assessed the relationship between breastfeeding and subclinical cardiovascular disease [29,30]. Both studies have found non-breastfeeding mothers to be at increased risk of vascular changes associated with subsequent cardiovascular disease. Among premenopausal women assessed 4 to 12 years after delivery, mothers who never breastfed had larger carotid artery lumen and adventitial diameters, which are indicative of poorer cardiovascular health status, compared with mothers who breastfed all of their children for at least 3 months [29]. In another study involving an older sample of women between 45 to 58 years of age, the association between lactation and an increased adventitial diameter was not significant after adjustment for confounders. However, aortic calcification remained significantly associated with lactation duration [30]. McClure et al. [29] suggest that differences in the significance of findings between breastfeeding and adventitial diameter could be due to the younger age group and shorter time since pregnancy in their study.

Cardiovascular disease.

Table 5 describes studies with cardiovascular disease as the outcome. A few studies investigated the relationship between breastfeeding and cardiovascular disease, and found protective effects of breastfeeding [13,36]. One US study examined both the self-reported prevalence and incidence (confirmed by physician adjudication of medical records) of cardiovascular disease in a large sample of parous, postmenopausal women [36]. In that study, increasing lifetime lactation duration was significantly associated with a lower prevalence of cardiovascular disease, compared with never breastfeeding. In particular, women who breastfed ≥13 months in their lifetime and women aged 50–59 years who had breastfed ≥7 months, were less likely to have prevalent cardiovascular disease. Although women aged 60–69 years with 13–23 months of lifetime lactation had lower odds of prevalent cardiovascular disease than similar-aged women who had never breastfed, there were no significant associations observed in women aged 70–79 years [36].

In that same study, lifetime lactation duration was not associated with incident cardiovascular disease in the overall sample followed for 7.9 years [36]. However, compared to similar-aged women who never breastfed, significant cardiovascular benefits were seen in women in the younger age group, but not in the older age groups. In another large US study involving middle-aged and elderly women, women with a lifetime lactation duration ≥12 months had a reduced risk of incident myocardial infarction (confirmed by physician review of medical records) compared with parous women who had never breastfed [13]. A stronger inverse association was observed for women with ≥23 months of lifetime lactation and for those with a birth in the last 30 years.

Two prospective studies assessed the association between breastfeeding and cardiovascular disease mortality ascertained from death registries [14,35]. Among a large sample of Chinese non-smoking textile workers followed between 1989 and 2000, lactation duration was not significantly associated with mortality from ischaemic or haemorrhagic stroke [35]. However, compared to parous women who never breastfed, women who breastfed appeared to have a lower risk of mortality from ischaemic heart disease. In another study from Norway, mothers aged <65 years that never breastfed had nearly three times the risk of death from cardiovascular disease over 15 years compared with mothers with a lifetime lactation duration ≥24 months [14]. There was evidence for a U-shaped association with women who breastfed 7–12 months having almost half the risk of women who breastfed ≥24 months in their lifetime. There were no significant associations in women 65 years and over.

Overall pattern of associations.

The pattern of associations across different outcomes is summarized in Table 6. Overall, 19 studies (10 cross-sectional/retrospective, 9 prospective) reported significant protective effects of breastfeeding, nine studies (3 cross-sectional/retrospective, 5 prospective, 1 cluster RCT) reported non-significant findings and none reported detrimental effects of breastfeeding. Ten out of thirteen associations reported in cross-sectional/retrospective studies suggested that breastfeeding was associated with significant cardiovascular benefits. Although the evidence was less convincing, nine out of fifteen associations reported in prospective studies also indicated beneficial effects of breastfeeding. Out of all cardiovascular risk factors and outcomes considered, the evidence for significant protective effects of breastfeeding was most convincing for hypertension, although the evidence was mainly based on cross-sectional/retrospective studies. Three-quarters of high quality studies [7, 12, 13, 14, 22, 26, 28, 29, 30, 32, 34, 36] and 80% of medium quality studies [8, 27, 31, 35] reported significant protective effects of breastfeeding.

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Table 6. Summary of expected direction of associations^a between breastfeeding and cardiovascular risk factors/outcomes.

https://doi.org/10.1371/journal.pone.0187923.t006

Age, time since last birth and menopause.

Findings from one cross-sectional/retrospective study [26] and a few prospective studies [14,28,36] suggest that the benefits from breastfeeding may diminish with age. In a large cross-sectional Norwegian study, significant associations between lifetime lactation duration and cardiovascular risk factors were observed in parous women <50 years. However, there were no clear associations in women >50 years [26]. Among three prospective studies, there were unclear associations with hypertension [28], the incidence of cardiovascular disease [36], or cardiovascular disease mortality [14] in women >60 [36] or >65 years of age [14,28]. Time since last birth may also have an effect on the association between breastfeeding and cardiovascular outcomes [13,26,36]. Among Norwegian mothers <50 years, the association between lifetime lactation duration and hypertension was attenuated after adjustment for time since last birth, while the association with metabolic risk factors remained similar [26]. In a large prospective cohort study, there was a stronger association between breastfeeding and incident myocardial infarction for women who gave birth in last the 30 years compared to women who had not [13]. Menopausal status may also influence the risk of cardiovascular disease. Among a large cohort of postmenopausal women, increasing lifetime lactation duration was associated with a lower prevalence of hypertension, diabetes, hyperlipidemia and cardiovascular disease [36]. There was also a significant association between breastfeeding and the incidence of cardiovascular disease among women between 50–59 years of age, but not among women >60 years [36]. Whether older age, increasing time since last birth and menopause attenuate the association between breastfeeding and cardiovascular risk factors and outcomes requires further investigation.