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Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes

International Journal of Obesity volume 46, pages 1145–1154 (2022)Cite this article

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Abstract

Background

Exercise is an important strategy in the management of diabetes. Experimental studies have shown that exercise acts, at least in part, by inducing the production of myokines that improve metabolic control and activate brown/beige adipose tissue depots. Combined training (CT) is recommended by the major diabetes guidelines due to its metabolic and cardiovascular benefits, however, its impact on brown/beige adipose tissue activities has never been tested in humans with overweight and type 2 diabetes (T2D). Here, we evaluated the effects of 16-week combined training (CT) program on brown adipose tissue activity; browning and autophagy markers, and serum pro-thermogenic/inflammatory inducers in patients with overweight and T2D.

Methods

Thirty-four patients with overweight and T2D were assigned to either a control group (CG) or a combined training group (CTG) in a randomized and controlled study. Functional/fitness parameters, anthropometry/body composition parameters, blood hormone/biochemical parameters, thermogenic/autophagic gene expression in subcutaneous adipose tissue were evaluated before and at the end of the intervention. In addition, cold-induced 18-Fluoroxyglucose Positron Emission Computed Tomography (18F-FDG PET/CT) was performed in the training group before and after the end of the intervention.

Results

CT increased cervical/supraclavicular brown adipose tissue (BAT) thermogenic activity (p = 0.03) as well as in perirenal adipose tissue (p = 0.02). In addition, CT increased the expression of genes related to thermogenic profile (TMEM26: + 95%, p = 0.04; and EPSTI1: + 26%, p = 0.03) and decreased autophagic genes (ULK1: −15%, p = 0.04; LC3: −5%, p = 0.02; and ATG4: −22%, p < 0.001) in subcutaneous adipose tissue. There were positive correlations between Δ% BAT activity with Δ% of post training energy expenditure cold exposure, HDL-c, IL4, adiponectin, irisin, meteorin-like, and TMEM26 and ZIC1 genes, besides negative correlations with LDL-c, total cholesterol and C-reactive protein.

Conclusion

This is the first evidence of the beneficial actions of CT on adipose tissue thermogenic activity in humans, and it adds important support for the recommendation of CT as a strategy in the management of diabetes.

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Fig. 1: Serum levels of hormones, adipokines, inflammatory and thermogenesis-related markers.
Fig. 2: White adipose tissue expression of thermogenesis-related genes.
Fig. 3: White adipose tissue expression of autophagy-related genes.
Fig. 4: Standard uptake value in PET-CT scans and correlations.
Fig. 5: Calorimetry in PET-CT.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

ILPB thank Luiz Carlos Bonfante (In memoriam). The authors thank the participants; Obesity and Comorbidities Research Center—University of Campinas; Clinics Hospital—University of Campinas; Faculty of Physical Education—University of Campinas; Nuclear Medicine and collaborators team of Clinics Hospital—University of Campinas; Integrated Teaching, Research and Extension Laboratory—School of Physical Education—University of Campinas; Bárbara J. Amorim, Sergio Brunetto, Edna Brunetto, Natália Tobar, Antonio Calixto and Marcela Reymond Simões for your contribution in technical support. Finally we thank the funding agencies, cited mentioned below.

Funding

São Paulo State Research Support Foundation (FAPESP)—São Paulo/Brazil—Regular Research Grants—Process: 2016/08751-3; Coordination for the Improvement of Higher Education Personnel (CAPES) - Brazil—Financing Code 001; National Council for Scientific and Technological Development (CNPQ) – Brazil - Financing Code 303571/2018-7.

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Author notes

  1. These authors contributed equally: Milena Monfort-Pires, Renata Garbellini Duft, Keryma Chaves da Silva Mateus, José Carlos de Lima Júnior.

Authors and Affiliations

  1. Laboratory of Exercise Physiology, School of Physical Education, University of Campinas, Campinas, SP, 13083-970, Brazil

    Ivan Luiz Padilha Bonfante, Renata Garbellini Duft, Keryma Chaves da Silva Mateus, Joice Cristina dos Santos Trombeta, Enrico Antonio Rautenberg Finardi, Diego Trevisan Brunelli, Jéssica Aparecida Barbosa de Lima, Maria Luisa Bellotto, Mara Patricia Traina Chacon-Mikahil & Cláudia Regina Cavaglieri

  2. Federal Institute of Education, Science and Technology of São Paulo, Hortolândia campus, Hortolândia, SP, 13183-091, Brazil

    Ivan Luiz Padilha Bonfante

  3. Laboratory of Cell Signaling, Department of Internal Medicine, University of Campinas, Campinas, SP, 13084-970, Brazil

    Milena Monfort-Pires, José Carlos de Lima Júnior, Joseane Morari, Thiago Matos Ferreira de Araújo & Licio Augusto Velloso

  4. Obesity and Comorbidities Research Center, University of Campinas, Campinas, SP, 13084-970, Brazil

    Milena Monfort-Pires, José Carlos de Lima Júnior, Joseane Morari, Thiago Matos Ferreira de Araújo & Licio Augusto Velloso

  5. Department of Radiology, University of Campinas, Campinas, SP, 13084-970, Brazil

    Celso Darío Ramos

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  1. Ivan Luiz Padilha Bonfante
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Contributions

CRC supervised the study. ILPB, MMP, RGD, KCSM, JCLJ, JCST, EARF, DTB, JM, CDR, MPTCM, LAV, and CRC performed hypothesis, generation, contributed to the design, data analysis, interpretation of results and paper preparation. ILPB, MMP, RGD, KCSM, JCLJ, EARF, DTB, JABL, JM, MLB, TMFA conducted experiments, tests, training sessions, and data analysis. All authors edited and approved the final paper. ILPB is the guarantor of this work and, as such, had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Correspondence to Ivan Luiz Padilha Bonfante or Cláudia Regina Cavaglieri.

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Bonfante, I.L.P., Monfort-Pires, M., Duft, R.G. et al. Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes. Int J Obes 46, 1145–1154 (2022). https://doi.org/10.1038/s41366-022-01086-3

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