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Volume 16
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10.3390/nu16203554
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Article

Regular Exercise Training Induces More Changes on Intestinal Glucose Uptake from Blood and Microbiota Composition in Leaner Compared to Heavier Individuals in Monozygotic Twins Discordant for BMI

by
Martin S. Lietzén
1,*,
Maria Angela Guzzardi
2,
Ronja Ojala
1,
Jaakko Hentilä
1,
Marja A. Heiskanen
3,4,
Sanna M. Honkala
1,
Riikka Lautamäki
5,
Eliisa Löyttyniemi
6,
Anna K. Kirjavainen
7,
Johan Rajander
8,
Tarja Malm
9,
Leo Lahti
10,
Juha O. Rinne
1,11,
Kirsi H. Pietiläinen
12,13,
Patricia Iozzo
2 and
Jarna C. Hannukainen
1
1
Turku PET Centre, University of Turku, 20521 Turku, Finland
2
Institute of Clinical Physiology, National Research Council, 56124 Pisa, Italy
3
Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, 20521 Turku, Finland
4
Centre for Population Health Research, University of Turku and Turku University Hospital, 20520 Turku, Finland
5
Heart Centre, Turku University Hospital, 20521 Turku, Finland
6
Department of Biostatistics, University of Turku, 20520 Turku, Finland
7
Turku PET Centre, Radiopharmaceutical Chemistry Laboratory, University of Turku, 20521 Turku, Finland
8
Turku PET Centre, Accelerator Laboratory, Åbo Akademi University, 20500 Turku, Finland
9
A.I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, 70211 Kuopio, Finland
10
Department of Computing, University of Turku, 20521 Turku, Finland
11
Turku PET Centre, Turku University Hospital, 20520 Turku, Finland
12
Obesity Research Unit, Research Program for Clinical and Molecular Metabolism, Faculty of Medicine, University of Helsinki, 00014 Helsinki, Finland
13
Abdominal Center, Obesity Center, Endocrinology, University of Helsinki and Helsinki University Central Hospital, 00014 Helsinki, Finland
 
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Nutrients 2024, 16(20), 3554; https://doi.org/10.3390/nu16203554
Submission received: 22 September 2024 / Revised: 16 October 2024 / Accepted: 18 October 2024 / Published: 20 October 2024
(This article belongs to the Special Issue Physical Exercise and Nutrition on the Gastrointestinal Pathophysiology)
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Abstract

Background/Objectives: Obesity impairs intestinal glucose uptake (GU) (intestinal uptake of circulating glucose from blood) and alters gut microbiome. Exercise improves intestinal insulin-stimulated GU and alters microbiome. Genetics influence the risk of obesity and gut microbiome. However, the role of genetics on the effects of exercise on intestinal GU and microbiome is unclear. Methods: Twelve monozygotic twin pairs discordant for BMI (age 40.4 ± 4.5 years, BMI heavier 36.7 ± 6.0, leaner 29.1 ± 5.7, 8 female pairs) performed a six-month-long training intervention. Small intestine and colonic insulin-stimulated GU was studied using [18F]FDG-PET and microbiota from fecal samples with 16s rRNA. Results: Ten pairs completed the intervention. At baseline, heavier twins had lower small intestine and colonic GU (p < 0.05). Response to exercise differed between twins (p = 0.05), with leaner twins increasing colonic GU. Alpha and beta diversity did not differ at baseline. During the intervention, beta diversity changed significantly, most prominently at the mid-point (p < 0.01). Beta diversity changes were only significant in the leaner twins when the twin groups were analyzed separately. Exercise was associated with changes at the phylum level, mainly at the mid-point (pFDR < 0.05); at the genus level, several microbes increased, such as Lactobacillus and Sellimonas (pFDR < 0.05). In type 1 analyses, many genera changes were associated with exercise, and fewer, such as Lactobacillus, were also associated with dietary sugar consumption (p < 0.05). Conclusions: Obesity impairs insulin-stimulated intestinal GU independent of genetics. Though both twin groups exhibited some microbiota changes, most changes in insulin-stimulated colon GU and microbiota were significant in the leaner twins.
Keywords: physical exercise; gut microbiota; insulin sensitivity; intestine physical exercise; gut microbiota; insulin sensitivity; intestine

Share and Cite

MDPI and ACS Style

Lietzén, M.S.; Guzzardi, M.A.; Ojala, R.; Hentilä, J.; Heiskanen, M.A.; Honkala, S.M.; Lautamäki, R.; Löyttyniemi, E.; Kirjavainen, A.K.; Rajander, J.; et al. Regular Exercise Training Induces More Changes on Intestinal Glucose Uptake from Blood and Microbiota Composition in Leaner Compared to Heavier Individuals in Monozygotic Twins Discordant for BMI. Nutrients 2024, 16, 3554. https://doi.org/10.3390/nu16203554

AMA Style

Lietzén MS, Guzzardi MA, Ojala R, Hentilä J, Heiskanen MA, Honkala SM, Lautamäki R, Löyttyniemi E, Kirjavainen AK, Rajander J, et al. Regular Exercise Training Induces More Changes on Intestinal Glucose Uptake from Blood and Microbiota Composition in Leaner Compared to Heavier Individuals in Monozygotic Twins Discordant for BMI. Nutrients. 2024; 16(20):3554. https://doi.org/10.3390/nu16203554

Chicago/Turabian Style

Lietzén, Martin S., Maria Angela Guzzardi, Ronja Ojala, Jaakko Hentilä, Marja A. Heiskanen, Sanna M. Honkala, Riikka Lautamäki, Eliisa Löyttyniemi, Anna K. Kirjavainen, Johan Rajander, and et al. 2024. "Regular Exercise Training Induces More Changes on Intestinal Glucose Uptake from Blood and Microbiota Composition in Leaner Compared to Heavier Individuals in Monozygotic Twins Discordant for BMI" Nutrients 16, no. 20: 3554. https://doi.org/10.3390/nu16203554

APA Style

Lietzén, M. S., Guzzardi, M. A., Ojala, R., Hentilä, J., Heiskanen, M. A., Honkala, S. M., Lautamäki, R., Löyttyniemi, E., Kirjavainen, A. K., Rajander, J., Malm, T., Lahti, L., Rinne, J. O., Pietiläinen, K. H., Iozzo, P., & Hannukainen, J. C. (2024). Regular Exercise Training Induces More Changes on Intestinal Glucose Uptake from Blood and Microbiota Composition in Leaner Compared to Heavier Individuals in Monozygotic Twins Discordant for BMI. Nutrients, 16(20), 3554. https://doi.org/10.3390/nu16203554

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