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Low-fat dairy consumption improves intestinal immune function more than high-fat dairy in a diet-induced swine model of insulin resistance

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A Correction to this article was published on 11 October 2023

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Abstract

Purpose

To understand the effects of consuming high-fat and low-fat dairy products on postprandial cardiometabolic risk factors and intestinal immune function, we used an established low birthweight (LBW) swine model of diet-induced insulin resistance.

Methods

LBW piglets were randomized to consume one of the 3 experimental high fat diets and were fed for a total of 7 weeks: (1) Control high fat (LBW–CHF), (2) CHF diet supplemented with 3 servings of high-fat dairy (LBW–HFDairy) and (3) CHF diet supplemented with 3 servings of low-fat dairy (LBW–LFDairy). As comparison groups, normal birthweight (NBW) piglets were fed a CHF (NBW–CHF) or standard pig grower diet (NBW–Chow). At 11 weeks of age, all piglets underwent an established modified oral glucose and fat tolerance test. At 12 weeks of age, piglets were euthanized and ex vivo cytokine production by cells isolated from mesenteric lymph node (MLN) stimulated with mitogens was assessed.

Results

Dairy consumption did not modulate postprandial plasma lipid, inflammatory markers and glucose concentrations. A lower production of IL-2 and TNF-α after pokeweed mitogen (PWM) stimulation was observed in LBW–CHF vs NBW–Chow (P < 0.05), suggesting impaired MLN T cell function. While feeding high-fat dairy had minimal effects, feeding low-fat dairy significantly improved the production of IL-2 and TNF-α after PWM stimulation (P < 0.05).

Conclusions

Irrespective of fat content, dairy had a neutral effect on postprandial cardiometabolic risk factors. Low-fat dairy products improved intestinal T cell function to a greater extent than high-fat dairy in this swine model of obesity and insulin resistance.

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Abbreviations

APC:

Antigen presenting cell

AUC:

Area under curve

CHF:

Control high-fat diet

CI:

Confidence interval

CV:

Coefficient of variation

CVD:

Cardiovascular disease

ELISA:

Enzyme-linked immunosorbent assay

FSC:

Forward scatter

GALT:

Gut-associated lymphoid tissue

HFDairy:

High-fat dairy diet

IEC:

Intestinal epithelial cells

IFN-γ:

Interferon-gamma

IL:

Interleukin

LBW:

Low birthweight

LDL-C:

Low-density lipoprotein cholesterol

LFDairy:

Low-fat dairy diet

LPS:

Lipopolysaccharide

MFI:

Median florescence intensity

MFGM:

Milk fat globular membrane

MHC:

Major histocompatibility complex

MLN:

Mesenteric lymph node

MOGTT:

Modified oral glucose and fat tolerance test

NBW:

Normal birthweight

PBMC:

Peripheral blood mononuclear cell

PBS:

Phosphate-buffered saline

PC:

Phosphatidylcholine

PMA-I:

Phorbol 12-myristate 13-acetate plus ionomycin

PP:

Peyer's patches

PWM:

Pokeweed mitogen

SEM:

Standard error of the mean

SM:

Sphingomyelin

S–MCFA:

Short–medium chain fatty acid

SRTC:

Swine research technology centre

SSC:

Side scatter

TC:

Total cholesterol

TG:

Triglycerides

Th:

T helper cell

TLR-4:

Toll-like receptor 4

TNF-α:

Tumor necrosis factor-alpha

Treg:

T regulatory cell

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Acknowledgements

This study was supported by grants from Dairy Farmers of Canada (RES0042193) and the Natural Sciences and Engineering Research Council of Canada Discovery Grants to both CR and SDP. YS is a recipient of a Ph.D. scholarship from China Scholarship Council (201807980001).

Funding

Dairy Farmers of Canada (Grant No. RES0042193), Natural Sciences and Engineering Research Council of Canada (Grant No. RES0038933).

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Authors and Affiliations

  1. Division of Human Nutrition, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada

    Yongbo She, Kun Wang, Alexander Makarowski, Rabban Mangat, Benjamin P. Willing, Spencer D. Proctor & Caroline Richard

  2. Metabolic and Cardiovascular Diseases Laboratory, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada

    Yongbo She, Kun Wang, Alexander Makarowski, Rabban Mangat, Spencer D. Proctor & Caroline Richard

  3. Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB, Canada

    Sue Tsai

  4. Division of Human Nutrition, Department of Agricultural, Food and Nutritional Science, Faculty of Agricultural, Life and Environmental Science, 4-002G Li Ka Shing (LKS) Centre for Health Research Innovation, University of Alberta, Edmonton, AB, T6G 2E, Canada

    Caroline Richard

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Contributions

CR and SDP designed and obtained funding for this study. ST and BPW provided expertise on immunology and animal model. YS, AM, RM and KW conducted research and analyzed data. YS performed the statistical analysis and wrote the manuscript under the supervision of CR and SDP. CR has primary responsibility for final content. All authors have read and approved the final manuscript.

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Correspondence to Caroline Richard.

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She, Y., Wang, K., Makarowski, A. et al. Low-fat dairy consumption improves intestinal immune function more than high-fat dairy in a diet-induced swine model of insulin resistance. Eur J Nutr 62, 699–711 (2023). https://doi.org/10.1007/s00394-022-03013-8

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