Hostname: page-component-5d59c44645-jb2ch Total loading time: 0 Render date: 2024-03-03T03:09:39.245Z Has data issue: false hasContentIssue false

Association between plasma and dietary trace elements and obesity in a rural Chinese population

Published online by Cambridge University Press:  13 July 2023

Yufu Lu
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Qiumei Liu
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Chuwu Huang
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Xu Tang
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Yanfei Wei
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Xiaoting Mo
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Shenxiang Huang
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Yinxia Lin
Affiliation:
School of Public Health, Guangxi Medical University, Shuangyong Road No.22, Nanning 530021, Guangxi, People’s Republic of China
Tingyu Luo
Affiliation:
School of Public Health, Guilin Medical University, 20 Lequn Road, Guilin, Guangxi, People’s Republic of China
Ruoyu Gou
Affiliation:
School of Public Health, Guilin Medical University, 20 Lequn Road, Guilin, Guangxi, People’s Republic of China
Zhiyong Zhang
Affiliation:
Guangxi Key Laboratory of Environmental Exposomics and Entire Lifecycle Health, Guilin Medical University, Guilin, Guangxi, People’s Republic of China
Jian Qin*
Affiliation:
Key Laboratory of Longevity and Aging-related Diseases of Chinese Ministry of Education, Guangxi Medical University, Nanning 530021, People’s Republic of China Guangxi Colleges and Universities Key Laboratory of Prevention and Control of Highly Prevalent Diseases, School of Public Health, Guangxi Medical University, Nanning 530021, People’s Republic of China Guangxi Key Laboratory of Environment and Health Research, Guangxi Medical University, Nanning 530021, People’s Republic of China
Jiansheng Cai
Affiliation:
School of Public Health, Guilin Medical University, 20 Lequn Road, Guilin, Guangxi, People’s Republic of China Guangxi Key Laboratory of Tumor Immunology and Microenvironmental Regulation, Guilin Medical University, Guilin, Guangxi, People’s Republic of China
*
*Corresponding author: Jian Qin, email qinjian@gxmu.edu.cn

Abstract

Trace elements may play an important role in obesity. This study aimed to assess the plasma and dietary intake levels of four trace elements, Mn, Cu, Zn and Se in a rural Chinese population, and analyse the relationship between trace elements and obesity. A cross-sectional study involving 2587 participants was conducted. Logistic regression models were used to analyse the association between trace elements and obesity; restricted cubic spline (RCS) models were used to assess the dose–response relationship between trace elements and obesity; the weighted quantile sum (WQS) model was used to examine the potential interaction of four plasma trace elements on obesity. Logistic regression analysis showed that plasma Se concentrations in the fourth quartile (Q4) exhibited a lower risk of developing obesity than the first quartile (Q1) (central obesity: OR = 0·634, P = 0·002; general obesity: OR = 0·525, P = 0·005). Plasma Zn concentration in the third quartile (Q3) showed a lower risk of developing obesity in general obesity compared with the first quartile (Q1) (OR = 0·625, P = 0·036). In general obesity, the risk of morbidity was 1·727 and 1·923 times higher for the second and third (Q2, Q3) quartiles of dietary Mn intake than for Q1, respectively. RCS indicated an inverse U-shaped correlation between plasma Se and obesity. WQS revealed the combined effects of four trace elements were negatively associated with central obesity. Plasma Zn and Se were negatively associated with obesity, and dietary Mn was positively associated with obesity. The combined action of the four plasma trace elements had a negative effect on obesity.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work

References

Bendor, CD, Bardugo, A, Pinhas-Hamiel, O, et al. (2020) Cardiovascular morbidity, diabetes and cancer risk among children and adolescents with severe obesity. Cardiovasc Diabetol 19, 79.Google Scholar
Santamaría-Ulloa, C, Chinnock, A & Montero-López, M (2022) Association between obesity and mortality in the Costa Rican elderly: a cohort study. BMC Public Health 22, 1007.Google Scholar
Stanaway, JD, Afshin, A, Gakidou, E, et al. (2018) Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392, 19231994.Google Scholar
Mohammadifard, N, Humphries, KH, Gotay, C, et al. (2019) Trace minerals intake: risks and benefits for cardiovascular health. Crit Rev Food Sci Nutr 59, 13341346.Google Scholar
Li, L & Yang, X (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid Med Cell Longevity 2018, 7580707.Google Scholar
Basu, A, Alman, AC & Snell-Bergeon, JK (2022) Associations of dietary antioxidants with glycated hemoglobin and insulin sensitivity in adults with and without type 1 diabetes. J Diabetes Res 2022, 4747573.Google Scholar
Wong, MMH, Chan, KY & Lo, K (2022) Manganese exposure and metabolic syndrome: a systematic review and meta-analysis. Nutrients 14, 825.Google Scholar
Monteiro, CA, Moura, EC, Conde, WL, et al. (2004) Socioeconomic status and obesity in adult populations of developing countries: a review. Bull World Health Organ 82, 940946.Google Scholar
Monteiro, CA, Conde, WL & Popkin, BM (2007) Income-specific trends in obesity in Brazil: 1975–2003. Am J Public Health 97, 18081812.Google Scholar
Skalnaya, MG, Skalny, AV, Grabeklis, AR, et al. (2018) Hair trace elements in overweight and obese adults in association with metabolic parameters. Biol Trace Elem Res 186, 1220.Google Scholar
Tinkov, AA, Bogdański, P, Skrypnik, D, et al. (2021) Trace element and mineral levels in serum, hair, and urine of obese women in relation to body composition, blood pressure, lipid profile, and insulin resistance. Biomolecules 11, 689.Google Scholar
Major, GC, Doucet, E, Jacqmain, M, et al. (2008) Multivitamin and dietary supplements, body weight and appetite: results from a cross-sectional and a randomised double-blind placebo-controlled study. Br J Nutr 99, 11571167.Google Scholar
Błażewicz, A, Klatka, M, Astel, A, et al. (2013) Differences in trace metal concentrations (Co, Cu, Fe, Mn, Zn, Cd, And Ni) in whole blood, plasma, and urine of obese and nonobese children. Biol Trace Elem Res 155, 190200.Google Scholar
Yerlikaya, FH, Toker, A & Arıbaş, A (2013) Serum trace elements in obese women with or without diabetes. Indian J Med Res 137, 339345.Google Scholar
Tinkov, AA, Ajsuvakova, OP, Filippini, T, et al. (2020) Selenium and selenoproteins in adipose tissue physiology and obesity. Biomolecules 10, 658.Google Scholar
Chooi, YC, Ding, C & Magkos, F (2019) The epidemiology of obesity. Metab Clin Exp 92, 610.Google Scholar
Du, P, Wang, HJ, Zhang, B, et al. (2017) Prevalence of abdominal obesity among Chinese adults in 2011. J Epidemiol 27, 282286.Google Scholar
Zhang, J, Liu, Q, Xu, M, et al. (2022) Associations between plasma metals and cognitive function in people aged 60 and above. Biol Trace Elem Res 200, 31263137.Google Scholar
Feng, X, Li, L, Huang, L, et al. (2021) Associations between serum multiple metals exposures and metabolic syndrome: a longitudinal cohort study. Biol Trace Elem Res 199, 24442455.Google Scholar
Berger, MM, Shenkin, A, Schweinlin, A, et al. (2022) ESPEN micronutrient guideline. Clin Nutr 41, 13571424.Google Scholar
Gać, P, Czerwińska, K, Macek, P, et al. (2021) The importance of selenium and zinc deficiency in cardiovascular disorders. Environ Toxicol Pharmacol 82, 103553.Google Scholar
Liu, X, Wang, X, Lin, S, et al. (2015) Reproducibility and validity of a food frequency questionnaire for assessing dietary consumption via the dietary pattern method in a Chinese rural population. PLoS One 10, e0134627.Google Scholar
Barak, F, Falahi, E, Keshteli, AH, et al. (2015) Red meat intake, insulin resistance, and markers of endothelial function among Iranian women. Mol Nutr Food Res 59, 315322.Google Scholar
Esfahani, FH, Asghari, G, Mirmiran, P, et al. (2010) Reproducibility and relative validity of food group intake in a food frequency questionnaire developed for the Tehran Lipid and Glucose Study. J Epidemiol 20, 150158.Google Scholar
Mu, L, Liu, J, Zhou, G, et al. (2021) Obesity prevalence and risks among Chinese adults: findings from the China PEACE million persons project, 2014–2018. Circ Cardiovasc Quality Outcome 14, e007292.Google Scholar
Hu, L, Ma, L, Xia, X, et al. (2022) Efficacy of bariatric surgery in the treatment of women with obesity and polycystic ovary syndrome. J Clin Endocrinol Metab 107, e3217e3229.Google Scholar
Li, P, Ji, G, Li, W, et al. (2020) The relationship between BMI, body composition, and fat mass distribution in Rou-en-Y gastric bypass patients. Obes Surg 30, 13851391.Google Scholar
Bellavia, A, James-Todd, T & Williams, PL (2019) Approaches for incorporating environmental mixtures as mediators in mediation analysis. Environ Int 123, 368374.Google Scholar
Wheeler, DC, Rustom, S, Carli, M, et al. (2021) Assessment of grouped weighted quantile sum regression for modeling chemical mixtures and cancer risk. Int J Environ Res Public Health 18, 504.Google Scholar
Czarnota, J, Gennings, C, Colt, JS, et al. (2015) Analysis of environmental chemical mixtures and non-Hodgkin lymphoma risk in the NCI-SEER NHL study. Environ Health Perspect 123, 965970.Google Scholar
Czarnota, J, Gennings, C & Wheeler, DC (2015) Assessment of weighted quantile sum regression for modeling chemical mixtures and cancer risk. Cancer Inf 14, 159171.Google Scholar
Nadaska, G, Lesny, J & Michalik, I (2010) Environmental aspect of manganese chemistry. Chemistry 116. http://heja.szif.hu/ENV/ENV-100702-A/env100702a.pdf Google Scholar
Martins, AC, Krum, BN, Queirós, L, et al. (2020) Manganese in the diet: bioaccessibility, adequate intake, and neurotoxicological effects. J Agric Food Chem 68, 1289312903.Google Scholar
Lv, WH, Zhao, T, Pantopoulos, K, et al. (2022) Manganese-induced oxidative stress contributes to intestinal lipid deposition via the deacetylation of PPARγ at K339 by SIRT1. Antioxid Redox Signaling 37, 417436.Google Scholar
Ma, Z, Wang, C, Liu, C, et al. (2020) Manganese induces autophagy dysregulation: the role of S-nitrosylation in regulating autophagy related proteins in vivo and in vitro . Sci Total Environ 698, 134294.Google Scholar
Zhang, Z, Yan, J, Bowman, AB, et al. (2020) Dysregulation of TFEB contributes to manganese-induced autophagic failure and mitochondrial dysfunction in astrocytes. Autophagy 16, 15061523.Google Scholar
Zhou, B, Su, X, Su, D, et al. (2016) Dietary intake of manganese and the risk of the metabolic syndrome in a Chinese population. Br J Nutr 116, 853863.Google Scholar
Rotter, I, Kosik-Bogacka, D, Dołęgowska, B, et al. (2015) Relationship between the concentrations of heavy metals and bioelements in aging men with metabolic syndrome. Int J Environ Res Public Health 12, 39443961.Google Scholar
Fan, Y, Zhang, C & Bu, J (2017) Relationship between selected serum metallic elements and obesity in children and adolescent in the U.S. Nutrients 9, 104.Google Scholar
Tao, C, Huang, Y, Huang, X, et al. (2022) Association between blood manganese levels and visceral adipose tissue in the United States: a population-based study. Nutrients 14, 4770.Google Scholar
Pérez-Torres, I, Castrejón-Téllez, V, Soto, ME, et al. (2021) Plant natural antioxidants, and obesity. Int J Mol Sci 22, 1786.Google Scholar
Liu, H, Guo, H, Jian, Z, et al. (2020) Copper induces oxidative stress and apoptosis in the mouse liver. Oxid Med Cell Longevity 2020, 1359164.Google Scholar
Gu, K, Li, X, Xiang, W, et al. (2020) The relationship between serum copper and overweight/obesity: a meta-analysis. Biol Trace Elem Res 194, 336347.Google Scholar
Ge, W, Liu, W & Liu, G (2020) The relationships between serum copper levels and overweight/total obesity and central obesity in children and adolescents aged 6–18 years. J Trace Elements Med Biol: Organ Soc Minerals Trace Elements (GMS) 61, 126557.Google Scholar
Vazquez-Moreno, M, Sandoval-Castillo, M, Rios-Lugo, MJ, et al. (2022) Overweight and obesity are positively associated with serum copper levels in Mexican schoolchildren. Biol Trace Element Res 201, 27442749.Google Scholar
Yang, H, Liu, CN, Wolf, RM, et al. (2019) Obesity is associated with copper elevation in serum and tissues. Metallomics: Integrated Biometal Sci 11, 13631371.Google Scholar
Piacenza, F, Giacconi, R, Costarelli, L, et al. (2021) Age, sex, and BMI influence on copper, zinc, and their major serum carrier proteins in a large European population including nonagenarian offspring from MARK-AGE study. J Gerontol Ser A, Biol Sci Med Sci 76, 20972106.Google Scholar
Koppel, DJ, Adams, MS, King, CK, et al. (2019) Preliminary study of cellular metal accumulation in two Antarctic marine microalgae - implications for mixture interactivity and dietary risk. Environ Pollut 252, 15821592.Google Scholar
Zavala, G, Long, KZ, García, OP, et al. (2013) Specific micronutrient concentrations are associated with inflammatory cytokines in a rural population of Mexican women with a high prevalence of obesity. Br J Nutr 109, 686694.Google Scholar
Cayir, Y, Cayir, A, Turan, MI, et al. (2014) Antioxidant status in blood of obese children: the relation between trace elements, paraoxonase, and arylesterase values. Biol Trace Elem Res 160, 155160.Google Scholar
Xiao, XH, Wang, YD, Qi, XY, et al. (2018) Zinc alpha2 glycoprotein protects against obesity-induced hepatic steatosis. Int J Obes 42, 14181430.Google Scholar
Liu, M, Zhu, H, Dai, Y, et al. (2018) Zinc-α2-glycoprotein is associated with obesity in Chinese people and HFD-induced obese mice. Front Physiol 9, 62.Google Scholar
Hernández-Mendoza, H, Martínez-Navarro, I, Hernández-Ochoa, E, et al. (2022) Serum zinc levels are associated with obesity and low-density lipoprotein cholesterol in Mexican adults. J Trace Elements Med Biol: Organ Soc Minerals Trace Elements (GMS) 73, 127002.Google Scholar
Jiang, S, Ma, X, Li, M, Yan, S, Zhao, H, Pan, Y, et al. (2020) Association between dietary mineral nutrient intake, body mass index, and waist circumference in U.S. adults using quantile regression analysis NHANES 2007–2014. Peer J 8, e9127.Google Scholar
Tinkov, AA, Skalnaya, MG, Ajsuvakova, OP, et al. (2021) Selenium, zinc, chromium, and vanadium levels in serum, hair, and urine samples of obese adults assessed by inductively coupled plasma mass spectrometry. Biol Trace Elem Res 199, 490499.Google Scholar
Kerkadi, A, Alkudsi, DS, Hamad, S, et al. (2021) The association between zinc and copper circulating levels and cardiometabolic risk factors in adults: a study of Qatar Biobank Data. Nutrients 13, 2729.Google Scholar
Ju, L, Wei, X, Yu, D, et al. (2022) Dietary micronutrient status and relation between micronutrient intakes and overweight and obesity among non-pregnant and non-lactating women aged 18–49 in China. Nutrients 14, 1895.Google Scholar
Burk, RF & Hill, KE (2015) Regulation of selenium metabolism and transport. Annu Rev Nutr 35, 109134.Google Scholar
Duntas, LH & Benvenga, S (2015) Selenium: an element for life. Endocrine 48, 756775.Google Scholar
Abo El-Magd, NF, Barbosa, PO, Nick, J, et al. (2022) As selenite, prevents adipogenesis by modulating selenoproteins gene expression and oxidative stress-related genes. Nutrition 93, 111424.Google Scholar
Hossain, A, Skalicky, M, Brestic, M, et al. (2021) Selenium biofortification: roles, mechanisms, responses and prospects. Molecule 26, 881.Google Scholar
Wang, X, Wu, B, Sun, G, et al. (2022) Dietary selenomethionine attenuates obesity by enhancing beiging process in white adipose tissue. J Nutr Biochem 113, 109230.Google Scholar
Błażewicz, A, Klatka, M, Astel, A, et al. (2015) Serum and urinary selenium levels in obese children: a cross-sectional study. J Trace Elements Med Biol: Organ Soc Minerals Trace Elements (GMS) 29, 116122.Google Scholar
Zhong, Q, Lin, R & Nong, Q (2018) Adiposity and serum selenium in U.S. Adults. Nutrients 10 Google Scholar
Fontenelle, LC, Cardoso de Araújo, DS, da Cunha Soares, T, et al. (2022) Nutritional status of selenium in overweight and obesity: a systematic review and meta-analysis. Clin Nutr 41, 862884.Google Scholar
Artacho-Cordón, F, León, J, Sáenz, JM, et al. (2016) Contribution of persistent organic pollutant exposure to the adipose tissue oxidative microenvironment in an adult cohort: a multipollutant approach. Environ Sci Technol 50, 1352913538.Google Scholar