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The association between urine elements and fasting glucose levels in a community-based elderly people in Beijing

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Abstract

Epidemiological studies have demonstrated that various kinds of urinary element concentrations were different between healthy, prediabetes, and diabetes patients. Meanwhile, many studies have explored the relationship between element concentration and fasting blood glucose (FBG), but the association between joint exposure to co-existing elements and FBG level has not been well understood. The study explored the associations of joint exposure to co-existing urinary elements with FBG level in a cross-sectional design. 275 retired elderly people were recruited from Beijing, China. The questionnaire survey was conducted, and biological samples were collected. The generalized linear model (GLM) and two-phase Bayesian kernel machine regression (BKMR) model were used to perform in-depth association analysis between urinary elements and FBG. The GLM analysis showed that Zn, Sr, and Cd were significantly correlated with the FBG level, under control potential confounding factors. The BKMR analysis demonstrated 8 elements (Zn, Se, Fe, Cr, Ni, Cd, Mn, and Al) had a higher influence on FBG (posterior inclusion probabilities > 0.1). Further intensive analyses result of the BKMR model indicated that the overall estimated exposure of 8 elements was positively correlated with the FBG level and was statistically significant when all creatinine-adjusted element concentrations were at their 65th percentile. Meanwhile, the BKMR analysis showed that Cd and Zn had a statistically significant association with FBG levels when other co-existing elements were controlled at different levels (25th, 50th, or 75th percentile), respectively. The results of the GLM and BKMR model were inconsistent. The BKMR model could flexibly calculate the joint exposure to co-existing elements, evaluate the possible interaction effects and nonlinear correlations. The meaningful conclusions were found that it was difficult to get by traditional methods. This study will provide methodological reference and experimental evidence for the association between joint exposure to co-existing elements and FBG in elderly people.

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References

  • American Diabetes A (2018) Classification and diagnosis of diabetes: standards of medical care in diabetes-2018. Diabetes Care 41:S13-S27

  • Anetor JI, Uche CZ, Ayita EB, Adedapo SK, Adeleye JO, Anetor GO, SK. A, (2016) Cadmium level, glycemic control, and indices of renal function in treated type II diabetics: implications for polluted environments. Front Public Health 4:114

    Article  Google Scholar 

  • Bellavia A, Chiu YH, Brown FM, Minguez-Alarcon L, Ford JB, Keller M, Petrozza J, Williams PL, Ye X, Calafat AM, Hauser R, James-Todd T, Team ES (2019) Urinary concentrations of parabens mixture and pregnancy glucose levels among women from a fertility clinic. Environ Res 168:389-396

  • Bjorklund G, Dadar M, Pivina L, Dosa MD, Semenova Y, Aaseth J (2019) The role of zinc and copper in insulin resistance and diabetes mellitus. Curr Med Chem 27:6643–6657

    Article  CAS  Google Scholar 

  • Bobb JF, Valeri L, Claus Henn B, Christiani DC, Wright RO, Mazumdar M, Godleski JJ, Coull BA (2015) Bayesian kernel machine regression for estimating the health effects of multi-pollutant mixtures. Biostatistics 16:493–508

    Article  Google Scholar 

  • Bobb JF, Claus Henn B, Valeri L, Coull BA (2018) Statistical software for analyzing the health effects of multiple concurrent exposures via Bayesian kernel machine regression. Environ Health 17:67

    Article  Google Scholar 

  • Bonaventura P, Benedetti G, Albarede F, Miossec P (2015) Zinc and its role in immunity and inflammation. Autoimmun Rev 14(4):277–285

    Article  CAS  Google Scholar 

  • Brodzka R, Trzcinka-Ochocka M, Janasik B (2013) Multi-element analysis of urine using dynamic reaction cell inductively coupled plasma mass spectrometry (ICP-DRC-MS) - a practical application. Int J Occup Med Environ Health 26:302–312

    Article  Google Scholar 

  • Chen H, Tan C (2012) Prediction of type-2 diabetes based on several element levels in blood and chemometrics. Biol Trace Elem Res 147:67–74

    Article  CAS  Google Scholar 

  • Cruz KJC, de Oliveira ARS, Morais JBS, Severo JS, Mendes PMV, de Sousa Melo SR, de Sousa GS, Marreiro DDN (2018) Zinc and insulin resistance: biochemical and molecular aspects. Biol Trace Elem Res 186(2):407–412

    Article  CAS  Google Scholar 

  • Das S, Dewanjee S, Dua TK, Joardar S, Chakraborty P, Bhowmick S, Saha A, Bhattacharjee S, De Feo V (2019) Carnosic acid attenuates cadmium induced nephrotoxicity by inhibiting oxidative stress, Promoting Nrf2/HO-1 signalling and impairing TGF-β1/Smad/Collagen IV signalling. Molecules 24:4176

    Article  CAS  Google Scholar 

  • De Souza BA, Graves DT, de Melo Loureiro AP, Junior CR, Corbi SCT, Frizzera F, Scarel-Caminaga RM, Camara NO, Andriankaja OM, Hiyane MI, Orrico SRP (2016) Diabetes and increased lipid peroxidation are associated with systemic inflammation even in well-controlled patients. J Diabetes Complications 30(8):1593–1599

    Article  Google Scholar 

  • Dubey P, Thakur V, Chattopadhyay M (2020) Role of minerals and trace elements in diabetes and insulin resistance. Nutrients 12:1864

    Article  CAS  Google Scholar 

  • Edwards J, Ackerman C (2016) A review of diabetes mellitus and exposure to the environmental toxicant cadmium with an emphasis on likely mechanisms of action. Curr Diabetes Rev 12:252–258

    Article  CAS  Google Scholar 

  • Feng W, Cui X, Liu B, Liu C, Xiao Y, Lu W, Guo H, He M, Zhang X, Yuan J, Chen W, Wu T (2015) Association of urinary metal profiles with altered glucose levels and diabetes risk: a population-based study in China. PLoS One 10(4):e0123742

  • Fiore M, Barone R, Copat C, Grasso A, Cristaldi A, Rizzo R, Ferrante M (2020) Metal and essential element levels in hair and association with autism severity. J Trace Elem Med Biol 57, 126409.

  • Fukunaka A, Y. F (2018) Role of zinc homeostasis in the pathogenesis of diabetes and obesity. Int J Mol Sci 19:476

  • Ge X, Yang A, Huang S, Luo X, Hou Q, Huang L, Zhou Y, Li D, Lv Y, Li L, Cheng H, Chen X, Zan G, Tan Y, Liu C, Xiao L, Zou Y, Yang X (2021) Sex-specific associations of plasma metals and metal mixtures with glucose metabolism: an occupational population-based study in China. Sci Total Environ 760:143906

  • Goulle JP, Mahieu L, Castermant J, Neveu N, Bonneau L, Laine G, Bouige D, Lacroix C (2005) Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair. Reference Values Forensic Sci Int 153(1):39–44

    Article  CAS  Google Scholar 

  • Guo FF, Hu ZY, Li BY, Qin LQ, Fu C, Yu H, Zhang ZL (2019) Evaluation of the association between urinary cadmium levels below threshold limits and the risk of diabetes mellitus: a dose-response meta-analysis. Environ Sci Pollut Res Int 26:19272–19281

    Article  CAS  Google Scholar 

  • Guo H, Callaway JB, Ting JP (2015) Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 21:677–687

    Article  CAS  Google Scholar 

  • Hang H, Yuan S, Yang Q, Yuan D, Liu Q (2014) Multiplex bead array assay of plasma cytokines in type 2 diabetes mellitus with diabetic retinopathy. Mol vis 20:1137–1145

    CAS  Google Scholar 

  • Hansen AF, Simic A, Asvold BO, Romundstad PR, Midthjell K, Syversen T, Flaten TP (2017) Trace elements in early phase type 2 diabetes mellitus-A population-based study (The HUNT study in Norway). J Trace Elem Med Biol 40:46–53

    Article  CAS  Google Scholar 

  • Heitland P, Koster HD (2006) Biomonitoring of 30 trace elements in urine of children and adults by ICP-MS. Clin Chim Acta 365(1–2):310–318

    Article  CAS  Google Scholar 

  • Henning RJ (2018) Type-2 diabetes mellitus and cardiovascular disease. Future Cardiol 14:491–509

    Article  CAS  Google Scholar 

  • Hoffman NJ, Penque BA, Habegger KM, Sealls W, Tackett L, Elmendorf JS (2014) Chromium enhances insulin responsiveness via AMPK. J Nutr Biochem 25:565–572

    Article  CAS  Google Scholar 

  • Hojyo S, T. F (2016) Roles of zinc signaling in the immune system. J Immunol Res 2016:6762343

  • Ibs KH, Rink L (2003) Zinc-altered immune function. J Nutr 133(5 Suppl 1):1452S-1456S

    Article  CAS  Google Scholar 

  • Igbokwe IO, Igwenagu E, Igbokwe NA (2019) Aluminium toxicosis: a review of toxic actions and effects. Interdiscip Toxicol 12(2):45–70

    Article  CAS  Google Scholar 

  • Ivanenko NB, Ivanenko AA, Solovyev ND, Zeimal AE, Navolotskii DV, Drobyshev EJ (2013) Biomonitoring of 20 trace elements in blood and urine of occupationally exposed workers by sector field inductively coupled plasma mass spectrometry. Talanta 116:764–769

    Article  CAS  Google Scholar 

  • Iyama T, Takata T, Yamada K, Mae Y, Taniguchi S, Ida A, Ogawa M, Yamamoto M, Hamada S, Fukuda S, Kanda T, Sugihara T, Isomoto H, Urano Y (2020) A novel method for assessing the renal biopsy specimens using an activatable fluorescent probe. Sci Rep 10:12094

    Article  CAS  Google Scholar 

  • Jaacks LM, Siegel KR, Gujral UP, Narayan KM (2016) Type 2 diabetes: a 21st century epidemic, Best Pract Res Clin Endocrinol Metab, pp. 331–343

  • Jarup L (2002) Cadmium overload and toxicity. Nephrol Dial Transplant 17(Suppl 2):35–39

    Article  CAS  Google Scholar 

  • Kanoni S et al (2011) Total zinc intake may modify the glucose-raising effect of a zinc transporter (SLC30A8) variant: a 14-cohort meta-analysis. Diabetes 60(9):2407–2416

    Article  CAS  Google Scholar 

  • Kim MK, Kim G, Jang EH, Kwon HS, Baek KH, Oh KW, Lee JH, Yoon KH, Lee WC, Lee KW, Son HY, Kang MI (2010) Altered calcium homeostasis is correlated with the presence of metabolic syndrome and diabetes in middle-aged and elderly Korean subjects: the Chungju metabolic disease cohort study (CMC study). Atherosclerosis 212:674–681

    Article  CAS  Google Scholar 

  • Kohler LN, Foote J, Kelley CP, Florea A, Shelly C, Chow HS, Hsu P, Batai K, Ellis N, Saboda K, Lance P, ET. J, (2018) Selenium and type 2 diabetes: systematic review. Nutrients 10:1924

    Article  CAS  Google Scholar 

  • Li L, X. Y (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid Med Cell Longev 2018:7580707

  • Li XT, Yu PF, Gao Y, Guo WH, Wang J, Liu X, Gu AH, Ji GX, Dong Q, Wang BS, Cao Y, Zhu BL, Xiao H (2017) Association between plasma metal levels and diabetes risk: a case-control study in China. Biomed Environ Sci 30:482–491

    CAS  Google Scholar 

  • Liu B, Feng W, Wang J, Li Y, Han X, Hu H, Guo H, Zhang X, He M (2016) Association of urinary metals levels with type 2 diabetes risk in coke oven workers. Environ Pollut 210:1–8

    Article  CAS  Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214

    Article  CAS  Google Scholar 

  • Liu J, Li Q, Yang Y, Ma L (2020) Iron metabolism and type 2 diabetes mellitus: a meta-analysis and systematic review. J Diabetes Investig 11:946–955

    Article  CAS  Google Scholar 

  • Liu M, Liu SW, Wang LJ, Bai YM, Zeng XY, Guo HB, Liu YN, Jiang YY, Dong WL, He GX, Zhou MG, Yu SC (2019) Burden of diabetes, hyperglycaemia in China from to 2016: findings from the 1990 to 2016, global burden of disease study. Diabetes Metab 45:286–293

    Article  CAS  Google Scholar 

  • Lv Y, Wei Y, Zhou J, Xue K, Guo Y, Liu Y, Ju A, Wu B, Zhao F, Chen C, Xiong J, Li C, Gu H, Cao Z, Ji JS, Shi X (2021) Human biomonitoring of toxic and essential metals in younger elderly, octogenarians, nonagenarians and centenarians: analysis of the Healthy Ageing and Biomarkers Cohort Study (HABCS) in China. Environ Int 156:106717

  • Menke A, Guallar E, Cowie CC (2016) Metals in urine and diabetes in U.S. Adults. Diabetes 65(1):164–171

  • Molnar J, Garamvolgyi Z, Herold M, Adanyi N, Somogyi A, Rigo J Jr (2008) Serum selenium concentrations correlate significantly with inflammatory biomarker high-sensitive CRP levels in Hungarian gestational diabetic and healthy pregnant women at mid-pregnancy. Biol Trace Elem Res 121:16–22

    Article  CAS  Google Scholar 

  • Morais JBS, Severo JS, Beserra JB, de Oiveira ARS, Cruz KJC, de Sousa Melo SR, do Nascimento GVR, de Macedo GFS, do Nascimento Marreiro D, (2019) Association between cortisol, insulin resistance and zinc in obesity: a mini-review. Biol Trace Elem Res 191(2):323–330

    Article  CAS  Google Scholar 

  • Norouzi S, Adulcikas J, Sohal SS, Myers S (2018) Zinc stimulates glucose oxidation and glycemic control by modulating the insulin signaling pathway in human and mouse skeletal muscle cell lines. PLoS One 13, e0191727

  • Prozialeck WC, Edwards JR (2010) Early biomarkers of cadmium exposure and nephrotoxicity. Biometals 23:793–809

    Article  CAS  Google Scholar 

  • Ranasinghe P, Pigera S, Galappatthy P, Katulanda P, Constantine GR (2015) Zinc and diabetes mellitus: understanding molecular mechanisms and clinical implications. Daru 23:44

    Article  CAS  Google Scholar 

  • Rezaei M, Blaszczyk M, Tinkov AA, Binkowski LJ, Mansouri B, Skalny A, Azadi N, Dosa MD, Bjorklund G (2021) Relationship between gestational diabetes and serum trace element levels in pregnant women from Eastern Iran: a multivariate approach. Environ Sci Pollut Res Int 28:45230–45239

    Article  CAS  Google Scholar 

  • Roels H, Bernard A, Buchet JP, Goret A, Lauwerys R, Chettle DR, Harvey TC, Haddad IA (1979) Critical concentration of cadmium in renal cortex and urine. Lancet 1:221

    Article  CAS  Google Scholar 

  • Sanjeevi N, Freeland-Graves J, Beretvas SN, Sachdev PK (2018) Trace element status in type 2 diabetes: a meta-analysis. J Clin Diagn Res 12(5):OE01-OE08

  • Summersgill H, England H, Lopez-Castejon G, Lawrence CB, Luheshi NM, Pahle J, Mendes P, Brough D (2014) Zinc depletion regulates the processing and secretion of IL-1beta. Cell Death Dis 5:e1040

  • Tinkov AA, Filippini T, Ajsuvakova OP, Aaseth J, Gluhcheva YG, Ivanova JM, Bjorklund G, Skalnaya MG, Gatiatulina ER, Popova EV, Nemereshina ON, Vinceti M, Skalny AV (2017) The role of cadmium in obesity and diabetes. Sci Total Environ 601–602:741–755

    Article  CAS  Google Scholar 

  • Valeri L, Mazumdar MM, Bobb JF, Claus Henn B, Rodrigues E, Sharif OIA, Kile ML, Quamruzzaman Q, Afroz S, Golam M, Amarasiriwardena C, Bellinger DC, Christiani DC, Coull BA, Wright RO (2017) The joint effect of prenatal exposure to metal mixtures on neurodevelopmental outcomes at 20–40 months of age: evidence from rural bangladesh. Environ Health Perspect 125:067015

  • Velmurugan G, Swaminathan K, Veerasekar G, Purnell JQ, Mohanraj S, Dhivakar M, Avula AK, Cherian M, Palaniswami NG, Alexander T, Pradeep T (2018) Metals in urine in relation to the prevalence of pre-diabetes, diabetes and atherosclerosis in rural India. Occup Environ Med 75:661–667

    Article  Google Scholar 

  • Vincent JB (2019) Effects of chromium supplementation on body composition, human and animal health, and insulin and glucose metabolism. Curr Opin Clin Nutr Metab Care 22(6):483–489

    Article  CAS  Google Scholar 

  • Wang L, Gao P, Zhang M, Huang Z, Zhang D, Deng Q, Li Y, Zhao Z, Qin X, Jin D, Zhou M, Tang X, Hu Y, Wang L (2017) Prevalence and ethnic pattern of diabetes and prediabetes in China in 2013. JAMA 317:2515–2523

    Article  Google Scholar 

  • Wang X, Karvonen-Gutierrez CA, Herman WH, Mukherjee B, Harlow SD, Park SK (2020a) Urinary metals and incident diabetes in midlife women: Study of Women's Health Across the Nation (SWAN). BMJ Open Diabetes Res Care 8(1), e001233

  • Wang X, Mukherjee B, Karvonen-Gutierrez CA, Herman WH, Batterman S, Harlow SD, Park SK (2020b) Urinary metal mixtures and longitudinal changes in glucose homeostasis: the study of women's health across the nation (SWAN). Environ Int 145, 106109

  • WHO (2021) Diabetes. World Health Organization (WHO)Web, World Health Organization (WHO)Web

  • Williams R (2021) IDF Diabetes Atlas 9th Edition. International Diabetes Federation (IDF)Web

  • Wu M, Song J, Zhu C, Wang Y, Yin X, Huang G, Zhao K, Zhu J, Duan Z, Su L (2017) Association between cadmium exposure and diabetes mellitus risk: a prisma-compliant systematic review and meta-analysis. Oncotarget 8:113129–113141

    Article  Google Scholar 

  • Xu J, Zhou Q, Liu G, Tan Y, L. C, (2013) Analysis of serum and urinal copper and zinc in Chinese northeast population with the prediabetes or diabetes with and without complications. Oxid Med Cell Longev 2013:1–11

    Article  CAS  Google Scholar 

  • Yao X, Liu R, Li X, Li Y, Zhang Z, Huang S, Ge Y, Chen X, Yang X (2021) Zinc, selenium and chromium co-supplementation improves insulin resistance by preventing hepatic endoplasmic reticulum stress in diet-induced gestational diabetes rats. J Nutr Biochem 96:108810

  • Yin RV, Phung OJ (2015) Effect of chromium supplementation on glycated hemoglobin and fasting plasma glucose in patients with diabetes mellitus. Nutr J 14:14

    Article  CAS  Google Scholar 

  • Yuan Y et al (2018) Associations of multiple plasma metals with incident type 2 diabetes in Chinese adults: the Dongfeng-Tongji Cohort. Environ Pollut 237:917–925

    Article  CAS  Google Scholar 

  • Zhang K, Han Y, Zhao Q, Zhan T, Li Y, Sun W, Li S, Sun D, Si X, Yu X, Qin Y, Tang C, Zhang J (2020) Targeted metabolomics analysis reveals that dietary supranutritional selenium regulates sugar and acylcarnitine metabolism homeostasis in pig liver. J Nutr 150:704–711

    Article  Google Scholar 

  • Zheng Y, Zhang C, Weisskopf MG, Williams PL, Claus Henn B, Parsons PJ, Palmer CD, Buck Louis GM, James-Todd T (2020) Evaluating associations between early pregnancy trace elements mixture and 2nd trimester gestational glucose levels: a comparison of three statistical approaches. Int J Hyg Environ Health 224, 113446

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Acknowledgements

The authors gratefully acknowledge assistants from all persons involved in the project.

Funding

This study was supported by the China Medical Board (Grant No. 15–230).

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Liu Liu, Ang Li, Chunyu Xu, Feng Han, Zhe Liu, and Qin Wang performed the data collection. Liu Liu, Chunyu Xu, and Qin Wang analyzed the biological samples. Liu Liu, Ang Li, and Dongqun Xu analyzed the data and wrote the paper. Liu Liu, Ang Li, Zhe Liu, Donggang Xu, Qun Xu, and Dongqun Xu reviewed and edited the manuscript. Dongqun Xu was the corresponding author of this paper. Donggang Xu was also the co-corresponding author of this paper.

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Correspondence to Dongqun Xu or Donggang Xu.

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Participants provided written informed consent and this study was approved by the Ethics Committee of the Institute of Basic Medical Sciences, Peking Union Medical College (Beijing, China).

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Liu, L., Li, A., Xu, Q. et al. The association between urine elements and fasting glucose levels in a community-based elderly people in Beijing. Environ Sci Pollut Res 29, 30102–30113 (2022). https://doi.org/10.1007/s11356-021-17948-8

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