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Published in: BMC Endocrine Disorders 1/2020

Open Access 01-12-2020 | Research article

Association of total bilirubin and indirect bilirubin content with metabolic syndrome among Kazakhs in Xinjiang

Authors: Hao Hao, Heng Guo, Ru-lin Ma, Yi-zhong Yan, Yun-hua Hu, Jiao-long Ma, Xiang-hui Zhang, Xin-ping Wang, Kui Wang, La-ti Mu, Yan-peng Song, Jing-yu Zhang, Jia He, Shu-xia Guo

Published in: BMC Endocrine Disorders | Issue 1/2020

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Abstract

Background

Some studies have shown that a high level of bilirubin is a protective factor against metabolic syndrome (MS), while a high level of transaminase is a risk factor for MS. However, the existing results are inconsistent and few cohort studies have been published.

Methods

Using an ambispective cohort study, 565 Kazakhs from Xinjiang, China were selected as the study subjects. The baseline serum bilirubin and transaminase levels of the subjects were divided into quartiles and the relationship between these values and the incidence of MS was analyzed. The definition of MS was based on the Joint Interim Statement (JIS) diagnostic criteria.

Results

The average follow-up time for the subjects was 5.72 years. The cumulative incidence of MS was 36.11% (204 of the 565 subjects), and the incidence density was 63.10/1000 person-years. Multivariate Cox regression analysis showed that the levels of total bilirubin (TBIL) and indirect bilirubin (IBIL) were negatively correlated with the occurrence of MS, Compared to the lowest quartile level (Q1), the hazard ratios of MS the TBIL levels at the Q2-Q4 quartiles were: 0.47 (0.31–0.71), 0.53 (0.35–0.79), and 0.48 (0.32–0.72), respectively, while IBIL levels at the Q2-Q4 quartiles showed an MS hazard ratio of 0.48 (0.32–0.72), 0.54(0.36–0.81), and 0.52 (0.35–0.77), respectively, all at a 95% confidence level. However, no relationship was found between transaminase levels and the incidence of MS.

Conclusion

Serum TBIL and IBIL levels were negatively correlated with the incidence of MS in a Kazakh population in China.
Literature
1.
go back to reference Mendrick DL, Diehl AM, Topor LS, et al. Metabolic syndrome and associated diseases: from the bench to the clinic. Toxicol Sci. 2018;162(1):36–42.PubMedCrossRef Mendrick DL, Diehl AM, Topor LS, et al. Metabolic syndrome and associated diseases: from the bench to the clinic. Toxicol Sci. 2018;162(1):36–42.PubMedCrossRef
2.
go back to reference Vona R, Gambardella L, Cittadini C, et al. Biomarkers of oxidative stress in metabolic syndrome and associated diseases. Oxidative Med Cell Longev. 2019;2019:8267234.CrossRef Vona R, Gambardella L, Cittadini C, et al. Biomarkers of oxidative stress in metabolic syndrome and associated diseases. Oxidative Med Cell Longev. 2019;2019:8267234.CrossRef
3.
go back to reference Mccracken E, Monaghan M, Sreenivasan S. Pathophysiology of the metabolic syndrome. Clin Dermatol. 2018;36(1):14–20.PubMedCrossRef Mccracken E, Monaghan M, Sreenivasan S. Pathophysiology of the metabolic syndrome. Clin Dermatol. 2018;36(1):14–20.PubMedCrossRef
4.
go back to reference Cheriyath P, Gorrepati VS, Peters I, et al. High Total Bilirubin as a Protective Factor for Diabetes Mellitus: An Analysis of NHANES Data From 1999–2006. J Clin Med Res. 2010;2(5):201–6.PubMedPubMedCentral Cheriyath P, Gorrepati VS, Peters I, et al. High Total Bilirubin as a Protective Factor for Diabetes Mellitus: An Analysis of NHANES Data From 1999–2006. J Clin Med Res. 2010;2(5):201–6.PubMedPubMedCentral
5.
go back to reference Wagner KH, Wallner M, Molzer C, et al. Looking to the horizon: the role of bilirubin in the development and prevention of age-related chronic diseases. Clin Sci (Lond). 2015;129(1):1–25.CrossRef Wagner KH, Wallner M, Molzer C, et al. Looking to the horizon: the role of bilirubin in the development and prevention of age-related chronic diseases. Clin Sci (Lond). 2015;129(1):1–25.CrossRef
7.
go back to reference Shiraishi M, Tanaka M, Okada H, et al. Potential impact of the joint association of total bilirubin and gamma-glutamyltransferase with metabolic syndrome. Diabetol Metab Syndr. 2019;11:12.PubMedPubMedCentralCrossRef Shiraishi M, Tanaka M, Okada H, et al. Potential impact of the joint association of total bilirubin and gamma-glutamyltransferase with metabolic syndrome. Diabetol Metab Syndr. 2019;11:12.PubMedPubMedCentralCrossRef
8.
go back to reference Schindhelm RK, Dekker JM, Nijpels G, et al. Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn study. Atherosclerosis. 2007;191(2):391–6.PubMedCrossRef Schindhelm RK, Dekker JM, Nijpels G, et al. Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn study. Atherosclerosis. 2007;191(2):391–6.PubMedCrossRef
9.
go back to reference Lee SH, Cho DY, Joo NS, et al. The relationship of alanine aminotransferase to metabolic syndrome in a Korean population. Turk J Gastroenterol. 2018;29(1):52–60.PubMedPubMedCentralCrossRef Lee SH, Cho DY, Joo NS, et al. The relationship of alanine aminotransferase to metabolic syndrome in a Korean population. Turk J Gastroenterol. 2018;29(1):52–60.PubMedPubMedCentralCrossRef
10.
go back to reference Pei D, Hsia TL, Chao TT, et al. Gamma-glutamyl transpeptidase in men and alanine aminotransferase in women are the most suitable parameters among liver function tests for the prediction of metabolic syndrome in nonviral hepatitis and nonfatty liver in the elderly. Saudi J Gastroenterol. 2015;21(3):158–64.PubMedPubMedCentralCrossRef Pei D, Hsia TL, Chao TT, et al. Gamma-glutamyl transpeptidase in men and alanine aminotransferase in women are the most suitable parameters among liver function tests for the prediction of metabolic syndrome in nonviral hepatitis and nonfatty liver in the elderly. Saudi J Gastroenterol. 2015;21(3):158–64.PubMedPubMedCentralCrossRef
11.
go back to reference Zhang XH, Zhang M, He J, et al. Comparison of anthropometric and Atherogenic indices as screening tools of metabolic syndrome in the Kazakh adult population in Xinjiang. Int J Environ Res Public Health. 2016;13(4):428.PubMedPubMedCentralCrossRef Zhang XH, Zhang M, He J, et al. Comparison of anthropometric and Atherogenic indices as screening tools of metabolic syndrome in the Kazakh adult population in Xinjiang. Int J Environ Res Public Health. 2016;13(4):428.PubMedPubMedCentralCrossRef
12.
go back to reference Guo SX, Zhang XH, Zhang JY, et al. Visceral adiposity and anthropometric indicators as screening tools of metabolic syndrome among low income rural adults in Xinjiang. Sci Rep. 2016;6:36091.PubMedPubMedCentralCrossRef Guo SX, Zhang XH, Zhang JY, et al. Visceral adiposity and anthropometric indicators as screening tools of metabolic syndrome among low income rural adults in Xinjiang. Sci Rep. 2016;6:36091.PubMedPubMedCentralCrossRef
13.
go back to reference Heng G, Rulin M, Jingyu Z, Dongsheng R, Shangzhi X, Feng S, Shuxia G. Comparison and analysis of epidemic characteristics of metabolic syndrome between Kazakh and Han ethnic groups in Xinjiang. Chin J Hypertension. 2011;19(06):538–43. Heng G, Rulin M, Jingyu Z, Dongsheng R, Shangzhi X, Feng S, Shuxia G. Comparison and analysis of epidemic characteristics of metabolic syndrome between Kazakh and Han ethnic groups in Xinjiang. Chin J Hypertension. 2011;19(06):538–43.
14.
go back to reference Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; National Heart, Lung, and Blood Institute; American Heart Association; world heart federation; international atherosclerosis society; and International Association for the Study of obesity. Circulation. 2009;120(16):1640–5.PubMedCrossRef Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; National Heart, Lung, and Blood Institute; American Heart Association; world heart federation; international atherosclerosis society; and International Association for the Study of obesity. Circulation. 2009;120(16):1640–5.PubMedCrossRef
15.
go back to reference Sun H, Liu Q, Wang X, et al. The longitudinal increments of serum alanine aminotransferase increased the incidence risk of metabolic syndrome: a large cohort population in China. Clin Chim Acta. 2019;488:242–7.PubMedCrossRef Sun H, Liu Q, Wang X, et al. The longitudinal increments of serum alanine aminotransferase increased the incidence risk of metabolic syndrome: a large cohort population in China. Clin Chim Acta. 2019;488:242–7.PubMedCrossRef
16.
go back to reference Hwang JH, Kam S, Shin JY, et al. Incidence of metabolic syndrome and relative importance of five components as a predictor of metabolic syndrome: 5-year follow-up study in Korea. J Korean Med Sci. 2013;28(12):1768–73.PubMedPubMedCentralCrossRef Hwang JH, Kam S, Shin JY, et al. Incidence of metabolic syndrome and relative importance of five components as a predictor of metabolic syndrome: 5-year follow-up study in Korea. J Korean Med Sci. 2013;28(12):1768–73.PubMedPubMedCentralCrossRef
18.
go back to reference Bulmer AC, Verkade HJ, Wagner KH. Bilirubin and beyond: a review of lipid status in Gilbert's syndrome and its relevance to cardiovascular disease protection. Prog Lipid Res. 2013;52(2):193–205.PubMedCrossRef Bulmer AC, Verkade HJ, Wagner KH. Bilirubin and beyond: a review of lipid status in Gilbert's syndrome and its relevance to cardiovascular disease protection. Prog Lipid Res. 2013;52(2):193–205.PubMedCrossRef
19.
go back to reference Boon AC, Bulmer AC, Coombes JS, Fassett RG. Circulating bilirubin and defense against kidney disease and cardiovascular mortality: mechanisms contributing to protection in clinical investigations. Am J Physiol Renal Physiol. 2014;307(2):123–36.CrossRef Boon AC, Bulmer AC, Coombes JS, Fassett RG. Circulating bilirubin and defense against kidney disease and cardiovascular mortality: mechanisms contributing to protection in clinical investigations. Am J Physiol Renal Physiol. 2014;307(2):123–36.CrossRef
20.
go back to reference Gazzin S, Vitek L, Watchko J, et al. A novel perspective on the biology of bilirubin in health and disease. Trends Mol Med. 2016;22(9):758–68.PubMedCrossRef Gazzin S, Vitek L, Watchko J, et al. A novel perspective on the biology of bilirubin in health and disease. Trends Mol Med. 2016;22(9):758–68.PubMedCrossRef
21.
go back to reference Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J Biol Chem. 1994;269(24):16712–9.PubMed Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J Biol Chem. 1994;269(24):16712–9.PubMed
22.
go back to reference Wu TW, Fung KP, Yang CC. Unconjugated bilirubin inhibits the oxidation of human low density lipoprotein better than Trolox. Life Sci. 1994;54(25):477–P481.CrossRef Wu TW, Fung KP, Yang CC. Unconjugated bilirubin inhibits the oxidation of human low density lipoprotein better than Trolox. Life Sci. 1994;54(25):477–P481.CrossRef
23.
go back to reference Peng YF, Xie LQ, Xiang Y, et al. Serum bilirubin and their association with C-reactive protein in patients with migraine. J Clin Lab Anal. 2016;30(6):982–5.PubMedPubMedCentralCrossRef Peng YF, Xie LQ, Xiang Y, et al. Serum bilirubin and their association with C-reactive protein in patients with migraine. J Clin Lab Anal. 2016;30(6):982–5.PubMedPubMedCentralCrossRef
24.
go back to reference Zhao X, Li L, Li X, et al. The relationship between serum bilirubin and inflammatory bowel disease. Mediat Inflamm. 2019;2019:5256460. Zhao X, Li L, Li X, et al. The relationship between serum bilirubin and inflammatory bowel disease. Mediat Inflamm. 2019;2019:5256460.
25.
go back to reference Mazzone GL, Rigato I, Ostrow JD, et al. Bilirubin inhibits the TNFalpha-related induction of three endothelial adhesion molecules. Biochem Biophys Res Commun. 2009;386(2):338–44.PubMedCrossRef Mazzone GL, Rigato I, Ostrow JD, et al. Bilirubin inhibits the TNFalpha-related induction of three endothelial adhesion molecules. Biochem Biophys Res Commun. 2009;386(2):338–44.PubMedCrossRef
26.
go back to reference Takei R, Inoue T, Sonoda N, et al. Bilirubin reduces visceral obesity and insulin resistance by suppression of inflammatory cytokines. PLoS One. 2019;14(10):e223302. Takei R, Inoue T, Sonoda N, et al. Bilirubin reduces visceral obesity and insulin resistance by suppression of inflammatory cytokines. PLoS One. 2019;14(10):e223302.
27.
go back to reference Dong H, Huang H, Yun X, et al. Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinology. 2014;155(3):818–28.PubMedPubMedCentralCrossRef Dong H, Huang H, Yun X, et al. Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinology. 2014;155(3):818–28.PubMedPubMedCentralCrossRef
28.
go back to reference Huang SS, Chan WL, Leu HB, et al. Serum bilirubin levels predict future development of metabolic syndrome in healthy middle-aged nonsmoking men. Am J Med. 2015;128(10):1135–8.CrossRef Huang SS, Chan WL, Leu HB, et al. Serum bilirubin levels predict future development of metabolic syndrome in healthy middle-aged nonsmoking men. Am J Med. 2015;128(10):1135–8.CrossRef
29.
go back to reference Kawamoto R, Kikuchi A, Akase T, et al. Total bilirubin independently predicts incident metabolic syndrome among community-dwelling women. Diabetes Metab Syndr. 2019;13(2):1329–34.PubMedCrossRef Kawamoto R, Kikuchi A, Akase T, et al. Total bilirubin independently predicts incident metabolic syndrome among community-dwelling women. Diabetes Metab Syndr. 2019;13(2):1329–34.PubMedCrossRef
30.
go back to reference Oda E, Aizawa Y. Total bilirubin is inversely associated with metabolic syndrome but not a risk factor for metabolic syndrome in Japanese men and women. Acta Diabetol. 2013;50(3):417–22.PubMedCrossRef Oda E, Aizawa Y. Total bilirubin is inversely associated with metabolic syndrome but not a risk factor for metabolic syndrome in Japanese men and women. Acta Diabetol. 2013;50(3):417–22.PubMedCrossRef
31.
go back to reference Li XH, Lin HY, Guan LY, et al. Direct bilirubin levels and risk of metabolic syndrome in healthy Chinese men. Biomed Res Int. 2017;2017:9621615.PubMedPubMedCentral Li XH, Lin HY, Guan LY, et al. Direct bilirubin levels and risk of metabolic syndrome in healthy Chinese men. Biomed Res Int. 2017;2017:9621615.PubMedPubMedCentral
32.
go back to reference Maruhashi T, Soga J, Fujimura N, et al. Hyperbilirubinemia, augmentation of endothelial function, and decrease in oxidative stress in Gilbert syndrome. Circulation. 2012;126(5):598–603.PubMedCrossRef Maruhashi T, Soga J, Fujimura N, et al. Hyperbilirubinemia, augmentation of endothelial function, and decrease in oxidative stress in Gilbert syndrome. Circulation. 2012;126(5):598–603.PubMedCrossRef
33.
go back to reference Sundararaghavan VL, Binepal S, Stec DE, et al. Bilirubin, a new therapeutic for kidney transplant? Transplant Rev (Orlando). 2018;32(4):234–40.PubMedCentralCrossRef Sundararaghavan VL, Binepal S, Stec DE, et al. Bilirubin, a new therapeutic for kidney transplant? Transplant Rev (Orlando). 2018;32(4):234–40.PubMedCentralCrossRef
34.
go back to reference Zhou JA, Jiang M, Yang X, et al. Unconjugated bilirubin ameliorates the inflammation and digestive protease increase in TNBS-induced colitis. Mol Med Rep. 2017;16(2):1779–84.PubMedPubMedCentralCrossRef Zhou JA, Jiang M, Yang X, et al. Unconjugated bilirubin ameliorates the inflammation and digestive protease increase in TNBS-induced colitis. Mol Med Rep. 2017;16(2):1779–84.PubMedPubMedCentralCrossRef
35.
go back to reference Boon AC, Hawkins CL, Coombes JS, et al. Bilirubin scavenges chloramines and inhibits myeloperoxidase-induced protein/lipid oxidation in physiologically relevant hyperbilirubinemic serum. Free Radic Biol Med. 2015;86:259–68.PubMedCrossRef Boon AC, Hawkins CL, Coombes JS, et al. Bilirubin scavenges chloramines and inhibits myeloperoxidase-induced protein/lipid oxidation in physiologically relevant hyperbilirubinemic serum. Free Radic Biol Med. 2015;86:259–68.PubMedCrossRef
36.
go back to reference McCarty MF. “Iatrogenic Gilbert syndrome”--a strategy for reducing vascular and cancer risk by increasing plasma unconjugated bilirubin. Med Hypotheses. 2007;69(5):974–94.PubMedCrossRef McCarty MF. “Iatrogenic Gilbert syndrome”--a strategy for reducing vascular and cancer risk by increasing plasma unconjugated bilirubin. Med Hypotheses. 2007;69(5):974–94.PubMedCrossRef
37.
go back to reference Lin JP, Vitek L, Schwertner HA. Serum bilirubin and genes controlling bilirubin concentrations as biomarkers for cardiovascular disease. Clin Chem. 2010;56(10):1535–43.PubMedCrossRef Lin JP, Vitek L, Schwertner HA. Serum bilirubin and genes controlling bilirubin concentrations as biomarkers for cardiovascular disease. Clin Chem. 2010;56(10):1535–43.PubMedCrossRef
Metadata
Title
Association of total bilirubin and indirect bilirubin content with metabolic syndrome among Kazakhs in Xinjiang
Authors
Hao Hao
Heng Guo
Ru-lin Ma
Yi-zhong Yan
Yun-hua Hu
Jiao-long Ma
Xiang-hui Zhang
Xin-ping Wang
Kui Wang
La-ti Mu
Yan-peng Song
Jing-yu Zhang
Jia He
Shu-xia Guo
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2020
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-020-00563-y

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