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Published in: BMC Surgery 1/2024

Open Access 01-12-2024 | Bariatric Surgery | Research

Energy expenditure related biomarkers following bariatric surgery: a prospective six-month cohort study

Authors: Mahsa Hatami, Mohammad Hassan Javanbakht, Neda Haghighat, Zahra Sohrabi, Rahman Yavar, Abdolreza Pazouki, Gholamreza Mohammadi Farsani

Published in: BMC Surgery | Issue 1/2024

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Abstract

Background

Mitochondria dysfunction is one of the major causes of insulin resistance, and other countless complications of obesity. PGC-1α, and UCP-2 play key roles in energy expenditure regulation in the mitochondrial thermogenesis. However, the effects of bariatric surgery on the level of PGC-1α and UCP-2 and their relationships are unclear.

Objective

This study aimed to investigate the effect of bariatric surgery on key pathways in energy, and to assess the potential predictive role of body composition and metabolic parameters in this regard.

Settings

Hazrat-e Rasool General Hospital, Center of Excellence of International Federation for Surgery of Obesity.

Methods

This prospective cohort study was carried out on 45 patients with morbid obesity who underwent Roux-en-Y gastric bypass surgery. The patients have evaluated three-time points at baseline, three, and six months after the surgery. Body composition components, the levels of PGC-1α, UCP-2, and metabolic parameters were measured three times during this study.

Results

Significant changes in TWL%, EBMIL%, and metabolic lab tests were observed at three- and six months post-surgery (P < 0.001). The PGC-1α and UCP-2 had a significant increase three and then six-month post-operation compared with the baseline (P < 0.001). Moreover, multivariate linear regression analysis identified that the changing trend of PGC-1α was associated with insulin, uric Acid, HOMA-IR, fat mass and trunk fat mass. UCP-2 was associated with TSH, AST, fat mass and FFM.

Conclusions

Bariatric surgery has been shown to have a positive effect on UCP-2 and PGC-1α levels, as well as body composition and metabolic parameters. As a result, it is believed that bariatric surgery could improve thermogenesis and energy expenditure by enhancing mitochondrial biogenesis and function. However, further studies are needed to fully understand the precise mechanisms and possible causal relationship.
Literature
1.
go back to reference Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56 e5.CrossRefPubMed Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56 e5.CrossRefPubMed
2.
go back to reference Crémieux P-Y, Ledoux S, Clerici C, Cremieux F, Buessing M. The impact of bariatric surgery on comorbidities and medication use among obese patients. Obes Surg. 2010;20:861–70.CrossRefPubMed Crémieux P-Y, Ledoux S, Clerici C, Cremieux F, Buessing M. The impact of bariatric surgery on comorbidities and medication use among obese patients. Obes Surg. 2010;20:861–70.CrossRefPubMed
3.
go back to reference Arterburn DE, Telem DA, Kushner RF, Courcoulas AP. Benefits and risks of bariatric surgery in adults: a review. JAMA. 2020;324(9):879–87.CrossRefPubMed Arterburn DE, Telem DA, Kushner RF, Courcoulas AP. Benefits and risks of bariatric surgery in adults: a review. JAMA. 2020;324(9):879–87.CrossRefPubMed
4.
go back to reference Bège T, Duconseil P, Lasbleiz A, Dutour A. Benefits of bariatric surgery on weight loss, development of comorbidities and mortality. Rev Prat. 2022;72(2):164–7.PubMed Bège T, Duconseil P, Lasbleiz A, Dutour A. Benefits of bariatric surgery on weight loss, development of comorbidities and mortality. Rev Prat. 2022;72(2):164–7.PubMed
5.
go back to reference Lin Z, Qu S. Legend of weight loss: a crosstalk between the bariatric surgery and the brain. Obes Surg. 2020;30(5):1988–2002.CrossRefPubMed Lin Z, Qu S. Legend of weight loss: a crosstalk between the bariatric surgery and the brain. Obes Surg. 2020;30(5):1988–2002.CrossRefPubMed
6.
go back to reference Lempesis IG, van Meijel RL, Manolopoulos KN, Goossens GH. Oxygenation of adipose tissue: A human perspective. Acta Physiol. 2020;228(1):e13298.CrossRef Lempesis IG, van Meijel RL, Manolopoulos KN, Goossens GH. Oxygenation of adipose tissue: A human perspective. Acta Physiol. 2020;228(1):e13298.CrossRef
7.
go back to reference Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB. Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol. 2016;7:30.CrossRef Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB. Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol. 2016;7:30.CrossRef
8.
go back to reference Gureev AP, Shaforostova EA, Popov VN. Regulation of mitochondrial biogenesis as a way for active longevity: interaction between the Nrf2 and PGC-1α signaling pathways. Front Genet. 2019;10:435.CrossRefPubMedPubMedCentral Gureev AP, Shaforostova EA, Popov VN. Regulation of mitochondrial biogenesis as a way for active longevity: interaction between the Nrf2 and PGC-1α signaling pathways. Front Genet. 2019;10:435.CrossRefPubMedPubMedCentral
10.
go back to reference de Oliveira Bristot VJ, de Bem Alves AC, Cardoso LR, da Luz SD, Aguiar AS Jr. The role of PGC-1α/UCP2 signaling in the beneficial effects of physical exercise on the brain. Front Neurosci. 2019;13:292.CrossRefPubMedPubMedCentral de Oliveira Bristot VJ, de Bem Alves AC, Cardoso LR, da Luz SD, Aguiar AS Jr. The role of PGC-1α/UCP2 signaling in the beneficial effects of physical exercise on the brain. Front Neurosci. 2019;13:292.CrossRefPubMedPubMedCentral
11.
go back to reference Hosseini SRA, Fathi M, Ziaaldini MM, Hejazi K. The effect of eight weeks of aerobic exercise with moderate and high intensities on serum irisin and PGC-1α protein levels in obese male Wistar rats. J Shahrekord Univ Med Sci. 2021;23(1):14–9.CrossRef Hosseini SRA, Fathi M, Ziaaldini MM, Hejazi K. The effect of eight weeks of aerobic exercise with moderate and high intensities on serum irisin and PGC-1α protein levels in obese male Wistar rats. J Shahrekord Univ Med Sci. 2021;23(1):14–9.CrossRef
12.
go back to reference Lee YC, Lee YH, Chuang PN, Kuo CS, Lu CW, Yang KC. The utility of visceral fat level measured by bioelectrical impedance analysis in predicting metabolic syndrome. Obes Res Clin Pract. 2020;14(6):519–23.CrossRefPubMed Lee YC, Lee YH, Chuang PN, Kuo CS, Lu CW, Yang KC. The utility of visceral fat level measured by bioelectrical impedance analysis in predicting metabolic syndrome. Obes Res Clin Pract. 2020;14(6):519–23.CrossRefPubMed
13.
go back to reference Dixon JB, McPhail T, O’Brien PE. Minimal reporting requirements for weight loss: current methods not ideal. Obes Surg. 2005;15(7):1034–9.CrossRefPubMed Dixon JB, McPhail T, O’Brien PE. Minimal reporting requirements for weight loss: current methods not ideal. Obes Surg. 2005;15(7):1034–9.CrossRefPubMed
14.
go back to reference Maïmoun L, Lefebvre P, Aouinti S, Picot M-C, Mariano-Goulart D, Nocca D. Acute and longer-term body composition changes after bariatric surgery. Surg Obes Relat Dis. 2019;15(11):1965–73.CrossRefPubMed Maïmoun L, Lefebvre P, Aouinti S, Picot M-C, Mariano-Goulart D, Nocca D. Acute and longer-term body composition changes after bariatric surgery. Surg Obes Relat Dis. 2019;15(11):1965–73.CrossRefPubMed
15.
go back to reference Sivakumar J, Chen Q, Sutherland TR, Read M, Ward S, Chong L, et al. Body Composition Differences Between Excess Weight Loss≥ 50% and< 50% at 12 Months Following Bariatric Surgery. Obes Surg. 2022;32(8):2556–66.CrossRefPubMedPubMedCentral Sivakumar J, Chen Q, Sutherland TR, Read M, Ward S, Chong L, et al. Body Composition Differences Between Excess Weight Loss≥ 50% and< 50% at 12 Months Following Bariatric Surgery. Obes Surg. 2022;32(8):2556–66.CrossRefPubMedPubMedCentral
16.
go back to reference Peng Y, Rideout DA, Rakita SS, Gower WR, You M, Murr MM. Does LKB1 mediate activation of hepatic AMP-protein kinase (AMPK) and sirtuin1 (SIRT1) after Roux-en-Y gastric bypass in obese rats? J Gastrointest Surg. 2010;14:221–8.CrossRefPubMed Peng Y, Rideout DA, Rakita SS, Gower WR, You M, Murr MM. Does LKB1 mediate activation of hepatic AMP-protein kinase (AMPK) and sirtuin1 (SIRT1) after Roux-en-Y gastric bypass in obese rats? J Gastrointest Surg. 2010;14:221–8.CrossRefPubMed
17.
go back to reference Liu Y, Sheng C, Feng W, Sun F, Zhang J, Chen Y, et al. A multi-center study on glucometabolic response to bariatric surgery for different subtypes of obesity. Front Endocrinol. 2022;13:989202.CrossRef Liu Y, Sheng C, Feng W, Sun F, Zhang J, Chen Y, et al. A multi-center study on glucometabolic response to bariatric surgery for different subtypes of obesity. Front Endocrinol. 2022;13:989202.CrossRef
18.
go back to reference Azulai S, Grinbaum R, Beglaibter N, Eldar SM, Rubin M, Carmi S, et al. Bariatric surgery affects plasma levels of alanine aminotransferase independent of weight loss: a registry-based study. J Clin Med. 2021;10(12):2724.CrossRefPubMedPubMedCentral Azulai S, Grinbaum R, Beglaibter N, Eldar SM, Rubin M, Carmi S, et al. Bariatric surgery affects plasma levels of alanine aminotransferase independent of weight loss: a registry-based study. J Clin Med. 2021;10(12):2724.CrossRefPubMedPubMedCentral
19.
go back to reference Talavera-Urquijo E, Beisani M, Balibrea JM, Alverdy JC. Is bariatric surgery resolving NAFLD via microbiota-mediated bile acid ratio reversal? A comprehensive review. Surg Obes Relat Dis. 2020;16(9):1361–9.CrossRefPubMed Talavera-Urquijo E, Beisani M, Balibrea JM, Alverdy JC. Is bariatric surgery resolving NAFLD via microbiota-mediated bile acid ratio reversal? A comprehensive review. Surg Obes Relat Dis. 2020;16(9):1361–9.CrossRefPubMed
20.
go back to reference Myronovych A, Kirby M, Ryan KK, Zhang W, Jha P, Setchell KD, et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity. 2014;22(2):390–400.CrossRefPubMed Myronovych A, Kirby M, Ryan KK, Zhang W, Jha P, Setchell KD, et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity. 2014;22(2):390–400.CrossRefPubMed
21.
go back to reference Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A, Karns R, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014;509(7499):183–8.CrossRefPubMedPubMedCentral Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A, Karns R, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014;509(7499):183–8.CrossRefPubMedPubMedCentral
22.
23.
go back to reference Kobayashi M, Deguchi Y, Nozaki Y, Higami Y. Contribution of pgc-1α to obesity-and caloric restriction-related physiological changes in white adipose tissue. Int J Mol Sci. 2021;22(11):6025.CrossRefPubMedPubMedCentral Kobayashi M, Deguchi Y, Nozaki Y, Higami Y. Contribution of pgc-1α to obesity-and caloric restriction-related physiological changes in white adipose tissue. Int J Mol Sci. 2021;22(11):6025.CrossRefPubMedPubMedCentral
24.
go back to reference Inutsuka A, Yamanaka A. The physiological role of orexin/hypocretin neurons in the regulation of sleep/wakefulness and neuroendocrine functions. Front Endocrinol. 2013;4:18.CrossRef Inutsuka A, Yamanaka A. The physiological role of orexin/hypocretin neurons in the regulation of sleep/wakefulness and neuroendocrine functions. Front Endocrinol. 2013;4:18.CrossRef
25.
go back to reference Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92(6):829–39.CrossRefPubMed Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92(6):829–39.CrossRefPubMed
26.
go back to reference Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.CrossRefPubMed Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.CrossRefPubMed
27.
go back to reference Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 1990;4(6):1023–34.CrossRefPubMed Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 1990;4(6):1023–34.CrossRefPubMed
28.
go back to reference Scarpulla RC. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem. 2006;97(4):673–83.CrossRefPubMed Scarpulla RC. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem. 2006;97(4):673–83.CrossRefPubMed
30.
go back to reference Huss J, Kopp R, Kelly D. PGC-1α coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and-γ. J Biol Chem. 2002;277:40265–74.CrossRefPubMed Huss J, Kopp R, Kelly D. PGC-1α coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and-γ. J Biol Chem. 2002;277:40265–74.CrossRefPubMed
31.
go back to reference Mootha V, Handschin C, Arlow D, Xie X, St P, Sihag S. Erralpha and gabpa/b specify pgC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA. 2004;101:6570–5 Ι0Ι (17).6570-5.CrossRefPubMedPubMedCentral Mootha V, Handschin C, Arlow D, Xie X, St P, Sihag S. Erralpha and gabpa/b specify pgC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA. 2004;101:6570–5 Ι0Ι (17).6570-5.CrossRefPubMedPubMedCentral
32.
go back to reference Mahadik SR, Lele RD, Saranath D, Seth A, Parikh V. Uncoupling protein-2 (UCP2) gene expression in subcutaneous and omental adipose tissue of Asian Indians: relationship to adiponectin and parameters of metabolic syndrome. Adipocyte. 2012;1(2):101–7.CrossRefPubMedPubMedCentral Mahadik SR, Lele RD, Saranath D, Seth A, Parikh V. Uncoupling protein-2 (UCP2) gene expression in subcutaneous and omental adipose tissue of Asian Indians: relationship to adiponectin and parameters of metabolic syndrome. Adipocyte. 2012;1(2):101–7.CrossRefPubMedPubMedCentral
33.
go back to reference Pecqueur C, Bui T, Gelly C, Hauchard J, Barbot C, Bouillaud F, et al. Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization. FASEB J. 2008;22(1):9–18.CrossRefPubMed Pecqueur C, Bui T, Gelly C, Hauchard J, Barbot C, Bouillaud F, et al. Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization. FASEB J. 2008;22(1):9–18.CrossRefPubMed
34.
go back to reference Krauss S, Zhang C-Y, Lowell BB. The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol. 2005;6(3):248–61.CrossRefPubMed Krauss S, Zhang C-Y, Lowell BB. The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol. 2005;6(3):248–61.CrossRefPubMed
35.
go back to reference Pi J, Collins S. Reactive oxygen species and uncoupling protein 2 in pancreatic β-cell function. Diabetes Obes Metab. 2010;12:141–8.CrossRefPubMed Pi J, Collins S. Reactive oxygen species and uncoupling protein 2 in pancreatic β-cell function. Diabetes Obes Metab. 2010;12:141–8.CrossRefPubMed
36.
go back to reference Pagel-Langenickel I, Bao J, Joseph JJ, Schwartz DR, Mantell BS, Xu X, et al. PGC-1α integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J Biol Chem. 2008;283(33):22464–72.CrossRefPubMedPubMedCentral Pagel-Langenickel I, Bao J, Joseph JJ, Schwartz DR, Mantell BS, Xu X, et al. PGC-1α integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J Biol Chem. 2008;283(33):22464–72.CrossRefPubMedPubMedCentral
37.
go back to reference Aykota MR, Atabey M. Effect of sleeve gastrectomy on thyroid-stimulating hormone levels in morbidly obese patients with normal thyroid function. Eur Rev Med Pharmacol Sci. 2021;25(1):233–40.PubMed Aykota MR, Atabey M. Effect of sleeve gastrectomy on thyroid-stimulating hormone levels in morbidly obese patients with normal thyroid function. Eur Rev Med Pharmacol Sci. 2021;25(1):233–40.PubMed
Metadata
Title
Energy expenditure related biomarkers following bariatric surgery: a prospective six-month cohort study
Authors
Mahsa Hatami
Mohammad Hassan Javanbakht
Neda Haghighat
Zahra Sohrabi
Rahman Yavar
Abdolreza Pazouki
Gholamreza Mohammadi Farsani
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2024
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/s12893-024-02421-3

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