Reverting to a Healthy Diet during Lactation Normalizes Maternal Milk Lipid Content of Diet‐Induced Obese Rats and Prevents Early Alterations in the Plasma Lipidome of the Offspring

Abstract

This study aims to assess in rats whether normalizing maternal diet during lactation prevents the harmful effects of western diet (WD) consumption during the whole perinatal period on the lipidomic profile in maternal milk and offspring plasma. Methods and Results: Control dams (CON-dams), fed with standard diet (SD); WD-dams, fed with WD prior and during gestation and lactation; and reversion dams (REV-dams), fed as WD-dams but moved to SD during lactation are followed. Lipidomic analysis is performed in milk and plasma samples from pups. Milk of WD-dams presents a different triacylglycerol composition and free fatty acid (FA) profile compared to CON-dams, including an increased ratio of pro-inflammatory to anti-inflammatory long-chain polyunsaturated FA. Such alterations, which are also present in the plasma of their offspring, are widely reversed in the milk of REV-dams and the plasma of their pups. This is related with the recovery of control adiponectin expression levels in the mammary gland, and the presence of decreased expression of pro-inflammatory factors. Conclusion: Implementing a healthy diet during lactation prevents early alterations in the plasma lipidome of pups associated to the maternal intake of an obesogenic diet, which may be related to the normalization of milk lipid content and the inflammatory state in the mammary gland.

Influence of Maternal Metabolic Status and Diet during the Perinatal Period on the Metabolic Programming by Leptin Ingested during the Suckling Period in Rats

“…This was tentatively related to the intake of higher amounts of leptin from maternal milk during the suckling period (due to greater maternal adiposity) in the absence of alterations in maternal diet. Taken together, these results would be in accordance with a greater influence of maternal diet on milk composition and on offspring metabolic programming, rather than maternal obesity per se, as previously proposed [ 9 , 10 ].…”

“…In this regard, we have previously shown that implementation of a healthy diet during lactation in diet-induced obese dams attenuates detrimental programming effects in their offspring observed at an early age [ 9 ]. This was associated with the normalization of milk composition [ 9 , 10 ]. Here, in the same cohort studied at early age [ 9 ], it is also highlighted that maternal intake of an obesogenic diet before and during gestation and lactation has detrimental effects on the phenotype of the adult offspring, and that these effects are magnified by exposure to WD conditions after weaning.…”

“…It could be speculated that changes in milk composition in WD-dams could interfere with leptin action during this critical period of development. Of note, the implementation of a healthy diet during lactation was shown to reverse most of the alterations in milk composition [ 9 , 10 ]. This could explain the improvement of the metabolic programming of the offspring, and in turn the recovery of the beneficial effects of oral leptin during the suckling period, which were observed particularly in males.…”

“…A scheme of the experimental design described below is detailed in Figure 1 . As previously described [ 9 , 10 ], virgin female Wistar rats were housed under controlled conditions (22 °C, a 12 h light–dark period and free access to food and water) and divided into two groups: dams fed with a standard chow diet (SD; 3.3 kcal·g − 1 , with 72.4% from carbohydrates, 8.4% calories from fat and 19.3% from protein; Safe, Augy, France) ( n = 8) or with a high-fat and high-sucrose diet (western diet, WD; 4.7 kcal·g − 1 , with 43.0% from carbohydrates, 40.0% calories from fat and 17.0% from proteins; Research Diets, New Brunswick, NJ, USA) ( n = 19) one month before being mated with male rats. During gestation, rats continued to be fed with the same diets.…”

“…Of note, maternal intake of a westernized diet throughout gestation and lactation, without suffering from obesity previously to gestation, has been described as being sufficient to trigger metabolic disorders in the offspring [ 6 , 7 , 8 ]. In addition, we have recently shown that implementing a healthy diet during lactation in diet-induced obese rats attenuates the detrimental impact of Western diet (WD) consumption before and during gestation on phenotypic traits and circulating parameters of the offspring at weaning [ 9 , 10 ], although the longer-term effects are not known.…”