Maternal consumption of urbanized diet compromises early-life health in association with gut microbiota

Abstract

Urbanization has significantly transformed dietary habits worldwide, contributing to a globally increased burden of non-communicable diseases and altered gut microbiota landscape. However, it is often overlooked that the adverse effects of these dietary changes can be transmitted from the mother to offspring during early developmental stages, subsequently influencing the predisposition to various diseases later in life. This review aims to delineate the detrimental effects of maternal urban-lifestyle diet (urbanized diet) on early-life health and gut microbiota assembly, provide mechanistic insights on how urbanized diet mediates mother-to-offspring transfer of bioactive substances in both intrauterine and extrauterine and thus affects fetal and neonatal development. Moreover, we also further propose a framework for developing microbiome-targeted precision nutrition and diet strategies specifically for pregnant and lactating women. The establishment of such knowledge can help develop proactive preventive measures from the beginning of life, ultimately reducing the long-term risk of disease and improving public health outcomes.

Keywords: Maternal urbanized diet; breast milk; early-life health; gut microbiota; metabolome; transmission.

Figure 1.

Global changes in disease burdens of infants and children with urbanization. (a) Changes in total prevalence (per 100,000) of 104 non-communicable diseases (NCDs) among children under 5 years across 203 countries between 1990 and 2021. (b) Changes in total prevalence (per 100,000) of neonatal disorders among infants under 1 year old across 203 countries between 1990 and 2021.

Figure 2.

Mechanisms by which prenatal urbanized diets affect maternal-fetal crosstalk. Effects of healthy (left) and urbanized (right) prenatal diets on fetal development are illustrated. Urbanized dietary patterns significantly alter gut microbiota composition and metabolic profiles, potentially disrupting the host’s immune and metabolic systems. These microbiota dysbiosis, metabolic abnormalities, and immune dysfunctions resulting from urbanized diets may transmit from the mother to offspring via placental transfer, further adversely affecting offspring health. Human and animal studies were distinguished by using solid and dashed lines, respectively. SCFAs, short-chain fatty acids; TMA, trimethylamine; TMAO, trimethylamine N-oxide; 5-AVAB, 5-aminovaleric acid betaine; IPA, 3-indolepropionic acid; 5-HT, serotonin; LPS, lipopolysaccharides; MMCs, maternal microchimeric cells; GPCRs, G protein-coupled receptors; IgG, immunoglobulin G; AHR, aryl hydrocarbon receptor; IL-22, interleukin-22; ILC3, intestinal group 3 innate lymphoid cells; tnf-a, tumor necrosis factor-alpha; CX3CL1, chemokine C-X3-C motif ligand 1; NK cell, natural killer cell.

Figure 3.

Mechanisms by which urbanized postnatal diets affect the maternal-infant crosstalk. Effects of healthy (left) and urbanized (right) postnatal diets on neonatal development are illustrated. Urbanized diets alter the composition of HMOs, immune cells, microbiome (bacteria, fungi, and viruses), and metabolites in breast milk, which can be transferred to offspring, thus influencing the assembly of the early-life gut microbiome and the development of the immune system. Human and animal studies were distinguished by using solid and dashed lines, respectively. SCFAs, short-chain fatty acids; TMA, trimethylamine; TMAO, trimethylamine N-oxide; HMOs, human milk oligosaccharides; 5-AVAB, 5-aminovaleric acid betaine; ILA, indole-3-lactic acid; 12,13-diHOME, 12,13-dihydroxy-9Z-octadecenoic acid; sIgA, secretory immunoglobulin A; AHR, aryl hydrocarbon receptor; IL-6, interleukin-6; TNF-α, tumor necrosis factor-alpha; NEC, necrotizing enterocolitis.

Figure 4.

A proposed framework for the development of microbiome-directed precision diet. The framework consists of a three-step strategy: 1) identify specific molecules in the blood, or breast milk of mothers to predict the long-term health trajectories of offspring; 2) establish a comprehensive database that captures information on human and gut microbial metabolism and their links to hundreds of diseases and nutritional data, aiming to predict host-diet-microbiome interactions and their metabolic output; 3) predict disease risks in their offspring by measuring pregnant women’s metabolic profiles and customizing dietary and nutrition strategies to modulate key metabolite levels according to each pregnant woman ’s unique gut microbiome composition and function. Continuous optimization of algorithms and databases is essential to improve the ability to predict the host and microbial metabolic output of a defined diet, ultimately maximizing maternal nutritional benefits and enhancing offspring health.