Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2021 Nov;23(11):7201-7213.
doi: 10.1111/1462-2920.15791. Epub 2021 Oct 16.

Early life feeding accelerates gut microbiome maturation and suppresses acute post-weaning stress in piglets

R Choudhury  1 , A Middelkoop  2 , J Boekhorst  1 , W J J Gerrits  3 , B Kemp  2 , J E Bolhuis  2 , M Kleerebezem  1
Affiliations

Early life feeding accelerates gut microbiome maturation and suppresses acute post-weaning stress in piglets

R Choudhury et al. Environ Microbiol. 2021 Nov.

Abstract

Early life microbiome perturbations can have important effects on host development, physiology and behaviour. In this longitudinal study, we evaluated the impact of early feeding on gut microbiome colonization in neonatal piglets. Early-fed (EF) piglets had access to a customized fibrous diet from 2 days after birth until weaning in addition to mother's milk, whereas control piglets suckled mother's milk only. Rectal swabs were collected at multiple time points until 6 weeks of age to investigate microbiota development using 16S rRNA gene profiling. The dynamic pre-weaning microbiota colonization was followed by a relatively stable post-weaning microbiota, represented by Prevotella, Roseburia, Faecalibacterium, Ruminococcus, Megasphaera, Catenibacterium and Subdoligranulum. EF piglets showed an accelerated microbiota maturation, characterized by increased microbial diversity, pre-weaning emergence of post-weaning-associated microbes and a more rapid decline of typical pre-weaning microbes. Furthermore, the individual eating behaviour scores of piglets quantitatively correlated with their accelerated microbiome. Importantly, EF piglets displayed a smoother relative weight gain and tended to reach a higher relative weight gain, in addition to reduced diarrhoea scores in the first week post-weaning. Overall, these findings demonstrate the beneficial impact of early feeding on microbiota development as well as pig health and performance during the weaning transition.

PubMed Disclaimer

Figures

Fig. 1
Fig. 1
Age‐associated intestinal microbiota dynamics pre‐ and post‐weaning. A. Alpha diversity (Chao1 bias corrected) displays shifting diversity over time. B. Redundancy analysis of age at genus level (explained variation = 28.22%, P = 0.002) with associated microbial groups at different ages. Triangles are centroids of all samples of a specific time point. The age‐related microbial groups visualized (black arrows) have minimum 35% fit on horizontal axis with a response score ≥0.7 in the biplot (obtained by projecting the taxa points perpendicular to the axes). C. Heat map showing normalized relative abundance (see M&M) of the discriminative bacterial genera identified in redundancy analysis of age. Significant differences between time points were assessed by Student t‐test or Mann–Whitney U test (***P < 0.001).
Fig. 2
Fig. 2
Microbiota colonization development in early‐fed (EF) and control (CON) group. A. Eating behaviour (total eating seconds per week; n = 10 piglets) in EF litters over time pre‐weaning. B. Alpha diversity (Chao1 bias corrected) displays diversity differences between the two groups from 15 days onwards. C. Comparison of squared Bray–Curtis index (distance between different samples with their day +14 time point in individual piglets) between two groups. D. Principal component analysis of microbiota in all ages (PC1 = 42.4%, PC2 = 12.3%), shown for the CON and EF group separately. The ellipses drawn around each time point represent 66% quantile of the approximated 2D‐Normal density distribution function. Large triangles are centroids of all samples of a specific time point. E. Principal response curve (PRC) analysis presenting changes in microbiota composition (genus level) across time for EF (red) and CON (green) group. The horizontal axis represents time and the vertical axis denotes PRC score values. Microbial response scores are shown on the right in a one‐dimensional plot. The combination of PRC score values and microbial response scores offers a quantitative interpretation and direction of change at different time points. The effect of treatment (including its interaction with time) was significant according to the Monte Carlo permutation test (P = 0.002). Significant differences between groups were assessed by Student t‐test or Mann–Whitney U test (**P < 0.01; ***P < 0.001).
Fig. 3
Fig. 3
Accelerated microbiota maturation in early‐fed (EF) group illustrated by emergence of post‐weaning associated microbial groups in pre‐weaning period. A. Redundancy analysis of treatment at day 28 (PC1 = 24.1%, PC2 = 19.7%; P = 0.002) with associated microbial groups in EF and CON groups (response score ≥0.65 on horizontal axis). B. Changes in relative abundance of Prevotella 9 in EF and CON groups at pre‐ and post‐weaning time points. C. Heat map of normalized relative abundance for representative individual genera at different ages showing appearance of post‐weaning associated microbial groups and rapid loss of pre‐weaning associated microbes, simultaneously. Significant differences between groups were assessed by Student t‐test or Mann–Whitney U test (**P < 0.01; ***P < 0.001).
Fig. 4
Fig. 4
Spearman correlation between eating scores of individual animals (n = 10 EF piglets) and squared Bray–Curtis distance to their day +14 ‘matured’ time point. The last 2 days eating behaviour before each corresponding time point (three time‐points: day 15, day 21 and day 28) was employed (r = −0.77, P < 0.0001).
Fig. 5
Fig. 5
Comparison of relative weight gain between the groups (n = 32 per group) during the weaning transition (till 5 days post‐weaning). Statistical comparisons between the groups were assessed by Student t‐test or Mann–Whitney U test in GraphPad Software 8.1.1. The coefficient of variation (CV%) is indicated in black boxes below the labels.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Adeleye, O.O. , Guy, J.H. , and Edwards, S.A. (2014) Exploratory behaviour and performance of piglets fed novel flavoured creep in two housing systems. Anim Feed Sci Technol 191: 91–97.
    1. Alain, B.P.E. , Chae, J.P. , Balolong, M.P. , Bum Kim, H. , and Kang, D.K. (2014) Assessment of fecal bacterial diversity among healthy piglets during the weaning transition. J Gen Appl Microbiol 60: 140–146. - PubMed
    1. Albertsen, M. , Karst, S.M. , Ziegler, A.S. , Kirkegaard, R.H. , and Nielsen, P.H. (2015) Back to basics – the influence of DNA extraction and primer choice on phylogenetic analysis of activated sludge communities. PLoS One 10: e0132783. - PMC - PubMed
    1. Bruininx, E.M.A.M. , Binnendijk, G.P. , Schrama, J.W. , Den Hartog, L.A. , Everts, H. , and Beynen, A.C. (2002) Effect of creep feed consumption on individual feed intake characteristics and performance of group‐housed weanling pigs. J Anim Sci 80: 1413–1418. - PubMed
    1. Chen, L. , Xu, Y. , Chen, X. , Fang, C. , Zhao, L. , and Chen, F. (2017) The maturing development of gut microbiota in commercial piglets during the weaning transition. Front Microbiol 8: 1–13. - PMC - PubMed

Publication types

Substances