Timing of complementary feeding is associated with gut microbiota diversity and composition and short chain fatty acid concentrations over the first year of life

Abstract

Background: Early introduction of complementary foods has been associated with various immune disorders, oxidative stress, and obesity in childhood. The gut microbiota and the short chain fatty acids (SCFAs) they produce are postulated to be on the causal pathway. The objective of this study was to determine if early complementary feeding (i.e. consumption of solids or non-water/formula liquids at or before 3 months) is prospectively associated with infant gut microbiota composition, diversity and SCFAs at 3 and 12 months of age in the Nurture birth cohort. Results: Mother-infant dyads in the early complementary feeding group (n = 18) had similar baseline characteristics to those in the later feeding group (n = 49). We assessed differential abundance of microbial taxa (measured by 16S rRNA gene sequencing of the V4 region) by timing of complementary feeding using beta-binomial regression models (considering a two-sided FDR corrected p-value of < 0.05 as significant), and we fittted linear regression models to assess the association between early complementary feeding and SCFA concentrations (quantified using gas chromatography). After multivariable adjustment for breastfeeding, delivery method, birth weight, and gestational age, there were 13 differentially abundant microbial amplicon sequence variants (ASVs) by timing of introduction to complementary foods at 3 months and 20 ASVs at 12 months. Infants introduced to complementary foods early (vs. later) had higher concentrations of the SCFA butyric acid (mean difference = 0.65, 95% CI: 0.27, 1.04, p < 0.01) and total SCFAs (mean difference = 38.8, 95% CI: 7.83, 69.7) at 12 months. Bilophila wadsworthia and Lachnospiraceae Roseburia were associated with early (vs. later) complementary feeding and with higher butyric acid concentrations at 3 and 12 months, respectively. Conclusions: Our findings are consistent with the hypothesis that early (vs. later) introduction to complementary foods is associated with altered gut microbiota composition and butyric acid concentrations measured in stool until at least 1 year of age. Further research is needed to determine if these changes mediate future development of metabolic and immune conditions.

Gut-Brain Axis in the Early Postnatal Years of Life: A Developmental Perspective

“…For instance, exclusively breastfed infants had relatively more acetate in their stools as compared to non-breastfed infants (Bridgman et al, 2017), likely due to the fermentation of oligosaccharides present in human breast-milk by members of the Bifidobacterium genus (Azad et al, 2016). The introduction of solid food results in the establishment of different microbial colonizers, which change the SCFA profile in the fecal sample (Differding et al, 2020). However, direct and indirect effects of SCFA production in the early postnatal period on GBA and subsequent consequences for the development of the brain and behaviors are poorly understood.…”

Evolving Technologies in Gastrointestinal Microbiome Era and Their Potential Clinical Applications

“…After birth, according to the findings of Koenig et al [ 27 ], there were apparent chaotic shifts of microbiome from that endowed with genes facilitating lactate utilization and plant polysaccharide metabolism mediated by milk-based diet to increase in Bacteroidetes initiated by introduction of solid food that prepares the infant gut for adult diet. However, in the findings of Differding et al [ 28 ], the early introduction of infants to complementary food was associated with altered gut microbiota composition and butyric acid concentration, which have been previously identified as precursors to oxidative stress, immune disorder and obesity in childhood.…”

Early Nutrition and Risk of Type 1 Diabetes: The Role of Gut Microbiota

“…However, Bifidobacteria , together with Bacteroides , remain among the prevalent species found in children's microbiota even after the introduction of complementary feeding ( 146 ). A recent study showed that the early introduction (<3 months) of complementary food is associated with an altered microbial composition with a higher diversity and an accelerated maturation pattern ( 149 ). Increased fecal excretion of butyrate and other SCFAs is associated with both local and systemic effects.…”

“…Instead, the greater abundance of Akkermansia Muciniphila promotes an early growth of adult associated bacteria, impairing the growth of taxa typical of the developmental phase. Finally, the early introduction of food results in an increased concentration of fecal butyrate ( 149 ).…”