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. 2023 Sep 26:10:1242301.
doi: 10.3389/fnut.2023.1242301. eCollection 2023.

Metabolite profiling of peripheral blood plasma in pigs in early postnatal life fed whole bovine, caprine or ovine milk

Affiliations

Metabolite profiling of peripheral blood plasma in pigs in early postnatal life fed whole bovine, caprine or ovine milk

Ankita Jena et al. Front Nutr. .

Abstract

Ruminants' milk is commonly used for supplying nutrients to infants when breast milk is unavailable or limited. Previous studies have highlighted the differences between ruminants' milk composition, digestion, absorption, and fermentation. However, whether consuming different ruminants' milk impact the appearance of the circulatory blood metabolites in the early postnatal life is not well understood. The analysis conducted here aimed to determine the effect of feeding exclusively whole milk from bovine, caprine or ovine species to pigs, approximately 7 days-old for 15 days, on circulatory blood plasma metabolites. Relative intensities of plasma metabolites were detected using a liquid chromatography-mass spectrometry based metabolomic approach. Seven polar and 83 non-polar (lipids) metabolites in plasma were significantly different (false discovery rate < 0.05) between milk treatments. These included polar metabolites involved in amino acid metabolism and lipids belonging to phosphatidylcholine, lysophosphatidylcholine, sphingomyelin, and triglycerides. Compared to the caprine or bovine milk group, the relative intensities of polar metabolites and unsaturated triglycerides were higher in the peripheral circulation of the ovine milk group. In contrast, relative intensities of saturated triglycerides and phosphatidylcholine were higher in the bovine milk group compared to the ovine or caprine milk group. In addition, correlations were identified between amino acid and lipid intake and their appearance in peripheral blood circulation. The results highlighted that consuming different ruminants' milk influences the plasma appearance of metabolites, especially lipids, that may contribute to early postnatal life development in pigs.

Keywords: early life; infant; lipids; metabolomics; nutrition; pigs; plasma; ruminant milk.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer CB declared a past co-authorship with the author RD to the handling editor.

Figures

Figure 1
Figure 1
(A) Score plot of principal component analysis showing lipid relative intensity differences between bovine, caprine and ovine milk. The first two principal components are plotted. Percentages of variation explained by each principal components (PC) are indicated along the axes. (B) Heatmap showing hierarchical clustering [method, Ward] of top 30 significantly different lipids between bovine (aqua), caprine (yellow), and ovine (purple) milk samples. Heatmap colour indicates normalised (Z score) peak intensity of lipids. The intensity of the red colour denotes the number of standard deviations above the mean (higher relative intensity), and the intensity of green colour denotes the number of standard deviations below the mean (lower relative intensity). TG, triglyceride.
Figure 2
Figure 2
Partial least squares discriminant analysis (PLS-DA) of metabolites relative intensity differences in plasma of pigs fed bovine, caprine, or ovine milk treatment. (A) Score plot and (B) permutation plot of polar metabolites. (C) Score plot and (D) permutation plot of non-polar metabolites. Permutation plots involve 100 permutation tests showing no overfitting of the PLS-DA model, confirming the robustness of the model. The criteria for evaluating whether there is overfitting of the PLS-DA model is that Q2 and R2 values of the permutated Y model to the left were lower than the Q2 and R2 value of the original model to the far right. The first two principal components are plotted. Percentages of variation explained by each principal component are indicated along the axes. PC, principal component.
Figure 3
Figure 3
Heatmap showing relative intensities of significantly different. (A) polar metabolites and (B) lipids (top 30 significant lipids) in plasma of pigs fed bovine, caprine, or ovine milk treatment. Heatmap colour indicates normalised (Z score) peak intensity of metabolites. The intensity of the red colour denotes the number of standard deviations above the mean (higher relative intensity), and the intensity of the green colour denotes the number of standard deviations below the mean (lower relative intensity).
Figure 4
Figure 4
Correlation plot showing Spearman correlations between milk amino acid intake in the last meal (mg) and plasma amino acid concentrations (μmol/L) of pigs fed bovine, caprine, or ovine milk treatment. The colour of the ellipse indicates the type of correlation, i.e., blue indicates positive correlation and red indicates negative correlation. The ellipse shape indicates the magnitude of the correlation, i.e., the stronger the correlation, the flatter the ellipse. Only significant correlations (p < 0.05) are shown. The legend at the bottom of each correlation plot shows the correlation coefficients with their corresponding colours. The vertical axis represents amino acid intakes (preceded with the letter m), and the horizontal axis represents plasma amino acid concentrations.
Figure 5
Figure 5
Correlation plot showing Spearman correlations between milk lipid intakes (mg) and plasma lipid relative intensities of pigs fed bovine, caprine, or ovine milk treatment. The colour of the ellipse indicates the type of correlation, i.e., blue indicates positive correlation and red indicates negative correlation. The ellipse shape indicates the magnitude of the correlation, i.e., the stronger the correlation, the flatter the ellipse. Only significant correlations (p < 0.05) are shown. The legend at the bottom of each correlation plot shows the correlation coefficients with their corresponding colours. The vertical axis represents milk lipid intakes (preceded with the letter m), and the horizontal axis represents plasma lipid relative intensities.

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