Gender difference in the relationship between serum uric acid reduction and improvement in body fat distribution after laparoscopic sleeve gastrectomy in Chinese obese patients: a 6-month follow-up

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Abstract

Background

Hyperuricemia is related to obesity and fat accumulation. This study aimed to observe the effects of laparoscopic sleeve gastrectomy (LSG) on serum uric acid (sUA) level and body fat distribution in obese patients. The relationships between post-LSG improvement in sUA levels and body fat distribution changes, as well as their sex-related differences, were also explored.

Methods

In total, 128 obese patients (48 men; 80 women) who underwent LSG were enrolled. Anthropometric indicators, glucose and lipid metabolic indicators, and sUA levels were measured pre-LSG and 6 months post-LSG. The body compositions were measured via dual-energy X-ray absorptiometry. The patients were divided into normal-sUA (NUA) and high-sUA (HUA) groups based on preoperative sUA levels.

Results

Compared with the NUA group, the reduction of sUA levels 6 months post-LSG was more significant in the HUA group. In addition, sUA reduction in the female HUA group was more significant than that of the male HUA group ( P < 0.01). Changes in serum uric acid levels (ΔsUA) in the male HUA group was positively correlated with changes in body weight, body mass index, neck circumference, and hip circumference ( r = 0.618, 0.653, 0.716, and 0.501, respectively; P < 0.05 in all cases). It was also positively correlated with changes in fat mass in the gynoid region, android region, and legs, ( r = 0.675, 0.551, and 0.712, respectively; P < 0.05 in all cases), and negatively correlated with changes in total testosterone (ΔTT) ( r = − 0.517; P = 0.040). Furthermore, ΔTT in this group was closely associated with the improved sex-related fat distribution. The ΔsUA in the female HUA group was positively correlated with changes in fasting serum C peptide and ΔLNIR ( r = 0.449 and 0.449, respectively; P < 0.05 in both cases). In addition, it was also positively correlated with changes in visceral adipose tissue (VAT) fat mass, VAT fat volume, and VAT fat area ( r = 0.749, 0.749, and 0.747, respectively; P < 0.01 in all cases).

Conclusions

sUA levels of obese patients with hyperuricemia improved 6 months after LSG. Reduction of sUA after LSG was correlated with improved body fat distribution, and the relationships also displayed sex-based differences. Uric acid might be an important metabolic regulator associated with fat distribution and sex hormones.

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Most cited references 27

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Metabolic syndrome, diabetes, and hyperuricemia.

Changgui Li, Yu-Chia Hsieh, King-Jen Chang (2013)

To explore the causal relationship between metabolic syndrome, type 2 diabetes and hyperuricemia. The prevalence of hyperuricemia in male adults with metabolic syndrome was increased and a large difference in prevalence of metabolic syndrome also existed in those with hyperuricemia compared with normouricemia. Even in those with normouricemia, higher serum uric acid levels were associated with metabolic syndrome. Serum uric acid was an independent risk factor for incident diabetes, and evidence showed that the patients with both gout and type 2 diabetes exhibited a mutual inter-dependent effect on higher incidences. Furthermore, obese patients often demonstrated insulin resistance and adipose tissue macrophage with low-grade inflammation, which is suggested to be the major contributor. Although alcohol intake is considered a risk for developing hyperuricemia, moderate alcohol intake showed a lower risk for developing type 2 diabetes and insulin resistance. Hyperinsulinemia reduces renal excretion of uric acid on the proximal tubular of the kidney leading to hyperuricemia, which has deleterious effects on endothelial function and on nitric oxide bioavailability, thus causing hyperinsulinemia. We found evidence to suggest that insulin resistance plays a potentially key role in the causal relationship between metabolic syndrome, type 2 diabetes and hyperuricemia. Furthermore, it is likely that hyperuricemia and insulin resistance share a bidirectional causal effect.

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Hyperuricemia as a Mediator of the Proinflammatory Endocrine Imbalance in the Adipose Tissue in a Murine Model of the Metabolic Syndrome

William Baldwin, Steven McRae, George Marek … (2011)

OBJECTIVE Hyperuricemia is strongly associated with obesity and metabolic syndrome and can predict visceral obesity and insulin resistance. Previously, we showed that soluble uric acid directly stimulated the redox-dependent proinflammatory signaling in adipocytes. In this study we demonstrate the role of hyperuricemia in the production of key adipokines. RESEARCH DESIGN AND METHODS We used mouse 3T3-L1 adipocytes, human primary adipocytes, and a mouse model of metabolic syndrome and hyperuricemia. RESULTS Uric acid induced in vitro an increase in the production (mRNA and secreted protein) of monocyte chemotactic protein-1 (MCP-1), an adipokine playing an essential role in inducing the proinflammatory state in adipocytes in obesity. In addition, uric acid caused a decrease in the production of adiponectin, an adipocyte-specific insulin sensitizer and anti-inflammatory agent. Uric acid–induced increase in MCP-1 production was blocked by scavenging superoxide or by inhibiting NADPH oxidase and by stimulating peroxisome-proliferator–activated receptor-γ with rosiglitazone. Downregulation of the adiponectin production was prevented by rosiglitazone but not by antioxidants. In obese mice with metabolic syndrome, we observed hyperuricemia. Lowering uric acid in these mice by inhibiting xanthine oxidoreductase with allopurinol could improve the proinflammatory endocrine imbalance in the adipose tissue by reducing production of MCP-1 and increasing production of adiponectin. In addition, lowering uric acid in obese mice decreased macrophage infiltration in the adipose tissue and reduced insulin resistance. CONCLUSIONS Hyperuricemia might be partially responsible for the proinflammatory endocrine imbalance in the adipose tissue, which is an underlying mechanism of the low-grade inflammation and insulin resistance in subjects with the metabolic syndrome.

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Effect of insulin on renal sodium and uric acid handling in essential hypertension.

S. Bianchi, Vittorio Sironi, S Frascerra … (1996)

In normal subjects, insulin decreases the urinary excretion of sodium, potassium, and uric acid. We tested whether these renal effects of insulin are altered in insulin resistant hypertension. In 37 patients with essential hypertension, we measured the changes in urinary excretion of sodium, potassium, and uric acid in response to physiological euglycemic hyperinsulinemia (by using the insulin clamp technique at an insulin infusion rate of 6 pmol/min/kg). Glucose disposal rate averaged 26.6 +/- 1.5 mumol/min/kg, i.e., 20% lower than in normotensive controls (33.1 +/- 2.1 mumol/min/kg, P = .015) In the basal state, fasting plasma uric acid concentrations were higher in men than women (P < .001), were positively related to body mass index (r = 0.38, P = .02), waist/hip ratio (r = 0.35, P < .05), and serum triglyceride levels (r = 0.59, P = .0001), and negatively related to HDL cholesterol concentrations (r = -0.59, P = .0001) and glucose disposal rate (r = 0.42, P < .01). Uric acid clearance, on the other hand, was inversely related to body mass index (r = 0.41, P = .01), plasma uric acid (r = 0.65, P < .0001) and triglyceride concentrations (r = 0.39, P < .02), and directly related to HDL cholesterol levels (r = 0.52, P < .001). During insulin infusion, blood pressure, plasma uric acid and sodium concentration, and creatinine clearance did not change. In contrast, hyperinsulinemia caused a significant decrease in the urinary excretion of uric acid (2.67 +/- 0.12 to 1.86 +/- .14 mumol/min/1.73 m2, P = .0001), sodium (184 +/- 12 to 137 +/- 14 mumol/min/1.73 m2, P = .0001), and potassium (81 +/- 7 to 48 +/- 4 mumol/ min/1.73 m2, P = .0001). Both in absolute terms (clearance and fractional excretion rates) and percentagewise, these changes were similar to those found in normotensive subjects. Insulin-induced changes in urate excretion were coupled (r = 0.55, P < .0001) to the respective changes in sodium excretion. In hypertensive patients, higher uric acid levels and lower renal urate clearance rates cluster with insulin resistance and dyslipidemia. Despite insulin resistance of glucose metabolism, acute physiological hyperinsulinemia causes normal antinatriuresis, antikaliuresis, and antiuricosuria in these patients.

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Author and article information

Contributors

Shen Qu: qushencn@hotmail.com

Journal

Journal ID (nlm-ta): Lipids Health Dis

Journal ID (iso-abbrev): Lipids Health Dis

Title: Lipids in Health and Disease

Publisher: BioMed Central (London )

ISSN (Electronic): 1476-511X

Publication date (Electronic): 20 December 2018

Publication date PMC-release: 20 December 2018

Publication date Collection: 2018

Volume: 17

Electronic Location Identifier: 288

Affiliations

[1 ]ISNI 0000000123704535, GRID grid.24516.34, Department of Endocrinology and Metabolism, Shanghai Tenth People’s Hospital, , Tongji University School of Medicine, ; No.301 Middle Yanchang Road, Shanghai, 200072 China

[2 ]ISNI 0000 0004 0527 0050, GRID grid.412538.9, National Metabolic Management Center (Shanghai 10th People’s Hospital), ; Shanghai, 200072 China

[3 ]ISNI 0000000123704535, GRID grid.24516.34, Department of Endocrinology and Metabolism, YangPu Hospital, , Tongji University School of Medicine, ; Shanghai, 200090 China

Article

Publisher ID: 934

DOI: 10.1186/s12944-018-0934-y

PMC ID: 6302487

PubMed ID: 30572901

SO-VID: a960b745-139d-4583-bfac-fa12db97b968

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 17 July 2018

Date accepted : 28 November 2018

Funding

Funded by: Scientific Research Fund of Shanghai Shenkang

Award ID: SHDC12012303

Award Recipient : Shen Qu

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ScienceOpen disciplines: Biochemistry

Keywords: serum uric acid,body fat distribution,gender difference,obesity,laparoscopic sleeve gastrectomy

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ScienceOpen disciplines: Biochemistry

Keywords: serum uric acid, body fat distribution, gender difference, obesity,laparoscopic sleeve gastrectomy

Gender difference in the relationship between serum uric acid reduction and improvement in body fat distribution after laparoscopic sleeve gastrectomy in Chinese obese patients: a 6-month follow-up

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GLUT4 biology

Most cited references 27

Metabolic syndrome, diabetes, and hyperuricemia.

Hyperuricemia as a Mediator of the Proinflammatory Endocrine Imbalance in the Adipose Tissue in a Murine Model of the Metabolic Syndrome

Effect of insulin on renal sodium and uric acid handling in essential hypertension.

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