Skip to main content
Top
Published in: BMC Public Health 1/2024

Open Access 01-12-2024 | Research

Association between multiple-heavy-metal exposures and systemic immune inflammation in a middle-aged and elderly Chinese general population

Authors: Linhai Zhao, Yanfei Wei, Qiumei Liu, Jiansheng Cai, Xiaoting Mo, Xu Tang, Xuexiu Wang, Lidong Qin, Yujian Liang, Jiejing Cao, Chuwu Huang, Yufu Lu, Tiantian Zhang, Lei Luo, Jiahui Rong, Songju Wu, Wenjia Jin, Qinyi Guan, Kaisheng Teng, You Li, Jian Qin, Zhiyong Zhang

Published in: BMC Public Health | Issue 1/2024

Login to get access

Abstract

Background

Exposure to heavy metals alone or in combination can promote systemic inflammation. The aim of this study was to investigate potential associations between multiple plasma heavy metals and markers of systemic immune inflammation.

Methods

Using a cross-sectional study, routine blood tests were performed on 3355 participants in Guangxi, China. Eight heavy metal elements in plasma were determined by inductively coupled plasma mass spectrometry. Immunoinflammatory markers were calculated based on peripheral blood WBC and its subtype counts. A generalised linear regression model was used to analyse the association of each metal with the immunoinflammatory markers, and the association of the metal mixtures with the immunoinflammatory markers was further assessed using weighted quantile sum (WQS) regression.

Results

In the single-metal model, plasma metal Fe (log10) was significantly negatively correlated with the levels of immune-inflammatory markers SII, NLR and PLR, and plasma metal Cu (log10) was significantly positively correlated with the levels of immune-inflammatory markers SII and PLR. In addition, plasma metal Mn (log10 conversion) was positively correlated with the levels of immune inflammatory markers NLR and PLR. The above associations remained after multiple corrections. In the mixed-metal model, after WQS regression analysis, plasma metal Cu was found to have the greatest weight in the positive effects of metal mixtures on SII and PLR, while plasma metals Mn and Fe had the greatest weight in the positive effects of metal mixtures on NLR and LMR, respectively. In addition, blood Fe had the greatest weight in the negative effects of the metal mixtures for SII, PLR and NLR.

Conclusion

Plasma metals Cu and Mn were positively correlated with immunoinflammatory markers SII, NLR and PLR. While plasma metal Fe was negatively correlated with immunoinflammatory markers SII, NLR, and PLR.
Appendix
Available only for authorised users
Literature
1.
go back to reference Zhang Y, Huo X, Lu X, Zeng Z, Faas MM, Xu X. Exposure to multiple heavy metals associate with aberrant immune homeostasis and inflammatory activation in preschool children. Chemosphere. 2020;257:127257.PubMedCrossRef Zhang Y, Huo X, Lu X, Zeng Z, Faas MM, Xu X. Exposure to multiple heavy metals associate with aberrant immune homeostasis and inflammatory activation in preschool children. Chemosphere. 2020;257:127257.PubMedCrossRef
2.
go back to reference Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, Holgate ST, Jönsson LS, Latulippe ME, Marcos A, et al. A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr. 2013;109(Suppl 1):S1-34.PubMedCrossRef Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, Holgate ST, Jönsson LS, Latulippe ME, Marcos A, et al. A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr. 2013;109(Suppl 1):S1-34.PubMedCrossRef
3.
go back to reference Twig G, Afek A, Shamiss A, Derazne E, Tzur D, Gordon B, Tirosh A. White blood cells count and incidence of type 2 diabetes in young men. Diabetes Care. 2013;36(2):276–82.PubMedPubMedCentralCrossRef Twig G, Afek A, Shamiss A, Derazne E, Tzur D, Gordon B, Tirosh A. White blood cells count and incidence of type 2 diabetes in young men. Diabetes Care. 2013;36(2):276–82.PubMedPubMedCentralCrossRef
4.
go back to reference Koupenova M, Clancy L, Corkrey HA, Freedman JE. Circulating platelets as mediators of immunity, inflammation, and thrombosis. Circ Res. 2018;122(2):337–51.PubMedPubMedCentralCrossRef Koupenova M, Clancy L, Corkrey HA, Freedman JE. Circulating platelets as mediators of immunity, inflammation, and thrombosis. Circ Res. 2018;122(2):337–51.PubMedPubMedCentralCrossRef
5.
go back to reference Scapini P, Cassatella MA. Social networking of human neutrophils within the immune system. Blood. 2014;124(5):710–9.PubMedCrossRef Scapini P, Cassatella MA. Social networking of human neutrophils within the immune system. Blood. 2014;124(5):710–9.PubMedCrossRef
6.
go back to reference Morrison L, Laukkanen JA, Ronkainen K, Kurl S, Kauhanen J, Toriola AT. Inflammatory biomarker score and cancer: A population-based prospective cohort study. BMC Cancer. 2016;16:80.PubMedPubMedCentralCrossRef Morrison L, Laukkanen JA, Ronkainen K, Kurl S, Kauhanen J, Toriola AT. Inflammatory biomarker score and cancer: A population-based prospective cohort study. BMC Cancer. 2016;16:80.PubMedPubMedCentralCrossRef
7.
go back to reference Bonaccio M, Di Castelnuovo A, Pounis G, De Curtis A, Costanzo S, Persichillo M, Cerletti C, Donati MB, de Gaetano G, Iacoviello L. A score of low-grade inflammation and risk of mortality: prospective findings from the Moli-sani study. Haematologica. 2016;101(11):1434–41.PubMedPubMedCentralCrossRef Bonaccio M, Di Castelnuovo A, Pounis G, De Curtis A, Costanzo S, Persichillo M, Cerletti C, Donati MB, de Gaetano G, Iacoviello L. A score of low-grade inflammation and risk of mortality: prospective findings from the Moli-sani study. Haematologica. 2016;101(11):1434–41.PubMedPubMedCentralCrossRef
8.
go back to reference Nøst TH, Alcala K, Urbarova I, Byrne KS, Guida F, Sandanger TM, Johansson M. Systemic inflammation markers and cancer incidence in the UK Biobank. Eur J Epidemiol. 2021;36(8):841–8.PubMedPubMedCentralCrossRef Nøst TH, Alcala K, Urbarova I, Byrne KS, Guida F, Sandanger TM, Johansson M. Systemic inflammation markers and cancer incidence in the UK Biobank. Eur J Epidemiol. 2021;36(8):841–8.PubMedPubMedCentralCrossRef
9.
10.
go back to reference Zhao J, Li A, Mei Y, Zhou Q, Li Y, Li K, Xu Q. The association of arsenic exposure with hypertension and blood pressure: A systematic review and dose-response meta-analysis. Environ Pollut. 2021;289:117914.PubMedCrossRef Zhao J, Li A, Mei Y, Zhou Q, Li Y, Li K, Xu Q. The association of arsenic exposure with hypertension and blood pressure: A systematic review and dose-response meta-analysis. Environ Pollut. 2021;289:117914.PubMedCrossRef
11.
go back to reference Bonaventura P, Benedetti G, Albarède F, Miossec P. Zinc and its role in immunity and inflammation. Autoimmun Rev. 2015;14(4):277–85.PubMedCrossRef Bonaventura P, Benedetti G, Albarède F, Miossec P. Zinc and its role in immunity and inflammation. Autoimmun Rev. 2015;14(4):277–85.PubMedCrossRef
12.
go back to reference Guo H, Liu H, Jian Z, Cui H, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L, et al. Immunotoxicity of nickel: Pathological and toxicological effects. Ecotoxicol Environ Saf. 2020;203:111006.PubMedCrossRef Guo H, Liu H, Jian Z, Cui H, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L, et al. Immunotoxicity of nickel: Pathological and toxicological effects. Ecotoxicol Environ Saf. 2020;203:111006.PubMedCrossRef
13.
go back to reference Guo H, Deng H, Cui H, Peng X, Fang J, Zuo Z, Deng J, Wang X, Wu B, Chen K. Nickel chloride (NiCl2)-caused inflammatory responses via activation of NF-κB pathway and reduction of anti-inflammatory mediator expression in the kidney. Oncotarget. 2015;6(30):28607–20.PubMedPubMedCentralCrossRef Guo H, Deng H, Cui H, Peng X, Fang J, Zuo Z, Deng J, Wang X, Wu B, Chen K. Nickel chloride (NiCl2)-caused inflammatory responses via activation of NF-κB pathway and reduction of anti-inflammatory mediator expression in the kidney. Oncotarget. 2015;6(30):28607–20.PubMedPubMedCentralCrossRef
14.
go back to reference Chwalba A, Maksym B, Dobrakowski M, Kasperczyk S, Pawlas N, Birkner E, Kasperczyk A. The effect of occupational chronic lead exposure on the complete blood count and the levels of selected hematopoietic cytokines. Toxicol Appl Pharmacol. 2018;355:174–9.PubMedCrossRef Chwalba A, Maksym B, Dobrakowski M, Kasperczyk S, Pawlas N, Birkner E, Kasperczyk A. The effect of occupational chronic lead exposure on the complete blood count and the levels of selected hematopoietic cytokines. Toxicol Appl Pharmacol. 2018;355:174–9.PubMedCrossRef
15.
go back to reference Xiong L, Fan C, Song J, Wan Y, Lin X, Su Z, Qiu J, Wu W, He Z, Wu Y, et al. Associations of long-term cadmium exposure with peripheral white blood cell subtype counts and indices in residents of cadmium-polluted areas. Chemosphere. 2022;308(Pt 1):135946.PubMedCrossRef Xiong L, Fan C, Song J, Wan Y, Lin X, Su Z, Qiu J, Wu W, He Z, Wu Y, et al. Associations of long-term cadmium exposure with peripheral white blood cell subtype counts and indices in residents of cadmium-polluted areas. Chemosphere. 2022;308(Pt 1):135946.PubMedCrossRef
16.
go back to reference Xiao X, Yeoh BS, Vijay-Kumar M. Lipocalin 2: an emerging player in iron homeostasis and inflammation. Annu Rev Nutr. 2017;37:103–30.PubMedCrossRef Xiao X, Yeoh BS, Vijay-Kumar M. Lipocalin 2: an emerging player in iron homeostasis and inflammation. Annu Rev Nutr. 2017;37:103–30.PubMedCrossRef
17.
go back to reference Miah MR, Ijomone OM, Okoh COA, Ijomone OK, Akingbade GT, Ke T, Krum B, da Cunha Martins A, Akinyemi A Jr, Aranoff N, et al. The effects of manganese overexposure on brain health. Neurochem Int. 2020;135:104688.PubMedPubMedCentralCrossRef Miah MR, Ijomone OM, Okoh COA, Ijomone OK, Akingbade GT, Ke T, Krum B, da Cunha Martins A, Akinyemi A Jr, Aranoff N, et al. The effects of manganese overexposure on brain health. Neurochem Int. 2020;135:104688.PubMedPubMedCentralCrossRef
18.
go back to reference Zhang J, Zhao Y, Wang S, Li G, Xu K. CREBH alleviates mitochondrial oxidative stress through SIRT3 mediating deacetylation of MnSOD and suppression of Nlrp3 inflammasome in NASH. Free Radic Biol Med. 2022;190:28–41.PubMedCrossRef Zhang J, Zhao Y, Wang S, Li G, Xu K. CREBH alleviates mitochondrial oxidative stress through SIRT3 mediating deacetylation of MnSOD and suppression of Nlrp3 inflammasome in NASH. Free Radic Biol Med. 2022;190:28–41.PubMedCrossRef
19.
go back to reference Zhong Q, Zhou W, Lin J, Sun W, Qin Y, Li X, Xu H. Independent and combined associations of blood manganese, cadmium and lead exposures with the systemic immune-inflammation index in adults. Toxics. 2023;11(8):659.PubMedPubMedCentralCrossRef Zhong Q, Zhou W, Lin J, Sun W, Qin Y, Li X, Xu H. Independent and combined associations of blood manganese, cadmium and lead exposures with the systemic immune-inflammation index in adults. Toxics. 2023;11(8):659.PubMedPubMedCentralCrossRef
20.
go back to reference Luo T, Chen S, Cai J, Liu Q, Gou R, Mo X, Tang X, He K, Xiao S, Wei Y, et al. Association between combined exposure to plasma heavy metals and dyslipidemia in a chinese population. Lipids Health Dis. 2022;21(1):131.PubMedPubMedCentralCrossRef Luo T, Chen S, Cai J, Liu Q, Gou R, Mo X, Tang X, He K, Xiao S, Wei Y, et al. Association between combined exposure to plasma heavy metals and dyslipidemia in a chinese population. Lipids Health Dis. 2022;21(1):131.PubMedPubMedCentralCrossRef
21.
go back to reference Zhang J, Liu Q, Xu M, Cai J, Wei Y, Lin Y, Mo X, Huang S, Liu S, Mo C, et al. Associations between plasma metals and cognitive function in people aged 60 and above. Biol Trace Elem Res. 2022;200(7):3126–37.PubMedCrossRef Zhang J, Liu Q, Xu M, Cai J, Wei Y, Lin Y, Mo X, Huang S, Liu S, Mo C, et al. Associations between plasma metals and cognitive function in people aged 60 and above. Biol Trace Elem Res. 2022;200(7):3126–37.PubMedCrossRef
22.
go back to reference Cai J, Li Y, Liu S, Liu Q, Min X, Zhang J, Wei Y, Mo X, Lin Y, Tang X, et al. Associations between multiple heavy metals exposure and glycated hemoglobin in a Chinese population. Chemosphere. 2022;287(Pt 2):132159.PubMedCrossRef Cai J, Li Y, Liu S, Liu Q, Min X, Zhang J, Wei Y, Mo X, Lin Y, Tang X, et al. Associations between multiple heavy metals exposure and glycated hemoglobin in a Chinese population. Chemosphere. 2022;287(Pt 2):132159.PubMedCrossRef
23.
go back to reference Feng X, Li L, Huang L, Zhang H, Mo Z, Yang X. Associations between serum multiple metals exposures and metabolic syndrome: a longitudinal cohort study. Biol Trace Elem Res. 2021;199(7):2444–55.PubMedCrossRef Feng X, Li L, Huang L, Zhang H, Mo Z, Yang X. Associations between serum multiple metals exposures and metabolic syndrome: a longitudinal cohort study. Biol Trace Elem Res. 2021;199(7):2444–55.PubMedCrossRef
24.
go back to reference Zhang H, Yan J, Niu J, Wang H, Li X. Association between lead and cadmium co-exposure and systemic immune inflammation in residents living near a mining and smelting area in NW China. Chemosphere. 2022;287(Pt 3):132190.PubMedCrossRef Zhang H, Yan J, Niu J, Wang H, Li X. Association between lead and cadmium co-exposure and systemic immune inflammation in residents living near a mining and smelting area in NW China. Chemosphere. 2022;287(Pt 3):132190.PubMedCrossRef
25.
go back to reference Xu M, Chen R, Liu L, Liu X, Hou J, Liao J, Zhang P, Huang J, Lu L, Chen L, et al. Systemic immune-inflammation index and incident cardiovascular diseases among middle-aged and elderly Chinese adults: The Dongfeng-Tongji cohort study. Atherosclerosis. 2021;323:20–9.PubMedCrossRef Xu M, Chen R, Liu L, Liu X, Hou J, Liao J, Zhang P, Huang J, Lu L, Chen L, et al. Systemic immune-inflammation index and incident cardiovascular diseases among middle-aged and elderly Chinese adults: The Dongfeng-Tongji cohort study. Atherosclerosis. 2021;323:20–9.PubMedCrossRef
26.
go back to reference WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet (London, England). 2004;363(9403):157–63.CrossRef WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet (London, England). 2004;363(9403):157–63.CrossRef
27.
go back to reference Wang T, Xu Y, Xu M, Wang W, Bi Y, Lu J, Dai M, Zhang D, Ding L, Xu B, et al. Awareness, treatment and control of cardiometabolic disorders in Chinese adults with diabetes: a national representative population study. Cardiovasc Diabetol. 2015;14:28.PubMedPubMedCentralCrossRef Wang T, Xu Y, Xu M, Wang W, Bi Y, Lu J, Dai M, Zhang D, Ding L, Xu B, et al. Awareness, treatment and control of cardiometabolic disorders in Chinese adults with diabetes: a national representative population study. Cardiovasc Diabetol. 2015;14:28.PubMedPubMedCentralCrossRef
28.
go back to reference Mo X, Cai J, Lin Y, Liu Q, Xu M, Zhang J, Liu S, Wei C, Wei Y, Huang S, et al. Correlation between urinary contents of some metals and fasting plasma glucose levels: A cross-sectional study in China. Ecotoxicol Environ Saf. 2021;228:112976.PubMedCrossRef Mo X, Cai J, Lin Y, Liu Q, Xu M, Zhang J, Liu S, Wei C, Wei Y, Huang S, et al. Correlation between urinary contents of some metals and fasting plasma glucose levels: A cross-sectional study in China. Ecotoxicol Environ Saf. 2021;228:112976.PubMedCrossRef
30.
go back to reference Brown M, Worrell C, Pariante CM. Inflammation and early life stress: An updated review of childhood trauma and inflammatory markers in adulthood. Pharmacol Biochem Behav. 2021;211:173291.PubMedCrossRef Brown M, Worrell C, Pariante CM. Inflammation and early life stress: An updated review of childhood trauma and inflammatory markers in adulthood. Pharmacol Biochem Behav. 2021;211:173291.PubMedCrossRef
31.
go back to reference Sun M, Wang L, Guo Y, Yan S, Li J, Wang X, Li X, Li B. The association among inflammatory diet, glycohemoglobin, and cognitive function impairment in the elderly: based on the NHANES 2011–2014. J Alzheimers Dis. 2022;87(4):1713–23.PubMedCrossRef Sun M, Wang L, Guo Y, Yan S, Li J, Wang X, Li X, Li B. The association among inflammatory diet, glycohemoglobin, and cognitive function impairment in the elderly: based on the NHANES 2011–2014. J Alzheimers Dis. 2022;87(4):1713–23.PubMedCrossRef
32.
go back to reference Wolkowicz P, White CR, Anantharamaiah GM. Apolipoprotein mimetic peptides: an emerging therapy against diabetic inflammation and dyslipidemia. Biomolecules. 2021;11(5):627.PubMedPubMedCentralCrossRef Wolkowicz P, White CR, Anantharamaiah GM. Apolipoprotein mimetic peptides: an emerging therapy against diabetic inflammation and dyslipidemia. Biomolecules. 2021;11(5):627.PubMedPubMedCentralCrossRef
33.
go back to reference Bao S, Xia W, Xu S, Li Y, Lu B, Wu C, Liao J, Liu H, Sun X, Zhou A. Multiple metal exposure and platelet counts during pregnancy: A repeated measure study. Environ Int. 2020;136:105491.PubMedCrossRef Bao S, Xia W, Xu S, Li Y, Lu B, Wu C, Liao J, Liu H, Sun X, Zhou A. Multiple metal exposure and platelet counts during pregnancy: A repeated measure study. Environ Int. 2020;136:105491.PubMedCrossRef
34.
go back to reference Luo JC, Hsu KH, Shen WS. Inflammatory responses and oxidative stress from metal fume exposure in automobile welders. J Occup Environ Med. 2009;51(1):95–103.PubMedCrossRef Luo JC, Hsu KH, Shen WS. Inflammatory responses and oxidative stress from metal fume exposure in automobile welders. J Occup Environ Med. 2009;51(1):95–103.PubMedCrossRef
35.
go back to reference Galaris D, Barbouti A, Pantopoulos K. Iron homeostasis and oxidative stress: An intimate relationship. Biochim Biophys Acta Mol Cell Res. 2019;1866(12):118535.PubMedCrossRef Galaris D, Barbouti A, Pantopoulos K. Iron homeostasis and oxidative stress: An intimate relationship. Biochim Biophys Acta Mol Cell Res. 2019;1866(12):118535.PubMedCrossRef
36.
go back to reference Carocci A, Catalano A, Sinicropi MS, Genchi G. Oxidative stress and neurodegeneration: the involvement of iron. Biometals. 2018;31(5):715–35.PubMedCrossRef Carocci A, Catalano A, Sinicropi MS, Genchi G. Oxidative stress and neurodegeneration: the involvement of iron. Biometals. 2018;31(5):715–35.PubMedCrossRef
37.
go back to reference Deng L, He S, Guo N, Tian W, Zhang W, Luo L. Molecular mechanisms of ferroptosis and relevance to inflammation. Inflamm Res. 2023;72(2):281–99.PubMedCrossRef Deng L, He S, Guo N, Tian W, Zhang W, Luo L. Molecular mechanisms of ferroptosis and relevance to inflammation. Inflamm Res. 2023;72(2):281–99.PubMedCrossRef
38.
39.
go back to reference Arnhold J, Furtmüller PG, Obinger C. Redox properties of myeloperoxidase. Redox Rep. 2003;8(4):179–86.PubMedCrossRef Arnhold J, Furtmüller PG, Obinger C. Redox properties of myeloperoxidase. Redox Rep. 2003;8(4):179–86.PubMedCrossRef
40.
go back to reference Pfeifhofer-Obermair C, Tymoszuk P, Nairz M, Schroll A, Klais G, Demetz E, Engl S, Brigo N, Weiss G. Regulation of Th1 T Cell Differentiation by Iron via Upregulation of T Cell Immunoglobulin and Mucin Containing Protein-3 (TIM-3). Front Immunol. 2021;12:637809.PubMedPubMedCentralCrossRef Pfeifhofer-Obermair C, Tymoszuk P, Nairz M, Schroll A, Klais G, Demetz E, Engl S, Brigo N, Weiss G. Regulation of Th1 T Cell Differentiation by Iron via Upregulation of T Cell Immunoglobulin and Mucin Containing Protein-3 (TIM-3). Front Immunol. 2021;12:637809.PubMedPubMedCentralCrossRef
41.
go back to reference Zhang Y, Meng Y, Chen M, Baral K, Fu Y, Yang Y, Cao L, Zhao M. Correlation between the systemic immune-inflammation indicator (SII) and serum ferritin in US adults: a cross-sectional study based on NHANES 2015–2018. Ann Med. 2023;55(2):2275148.PubMedPubMedCentralCrossRef Zhang Y, Meng Y, Chen M, Baral K, Fu Y, Yang Y, Cao L, Zhao M. Correlation between the systemic immune-inflammation indicator (SII) and serum ferritin in US adults: a cross-sectional study based on NHANES 2015–2018. Ann Med. 2023;55(2):2275148.PubMedPubMedCentralCrossRef
42.
go back to reference Cheng X, Wei Y, Wang R, Jia C, Zhang Z, An J, Li W, Zhang J, He M. Associations of essential trace elements with epigenetic aging indicators and the potential mediating role of inflammation. Redox Biol. 2023;67:102910.PubMedPubMedCentralCrossRef Cheng X, Wei Y, Wang R, Jia C, Zhang Z, An J, Li W, Zhang J, He M. Associations of essential trace elements with epigenetic aging indicators and the potential mediating role of inflammation. Redox Biol. 2023;67:102910.PubMedPubMedCentralCrossRef
43.
go back to reference Zhou S, Zhang F, Chen F, Li P, He Y, Wu J, Dong L, Wang C, Wang X, Zhang W, et al. Micronutrient Level Is Negatively Correlated with the Neutrophil-Lymphocyte Ratio in Patients with Severe COVID-19. Int J Clin Pract. 2022;2022:6498794.PubMedPubMedCentralCrossRef Zhou S, Zhang F, Chen F, Li P, He Y, Wu J, Dong L, Wang C, Wang X, Zhang W, et al. Micronutrient Level Is Negatively Correlated with the Neutrophil-Lymphocyte Ratio in Patients with Severe COVID-19. Int J Clin Pract. 2022;2022:6498794.PubMedPubMedCentralCrossRef
44.
go back to reference Tuuminen T, Sorsa M, Tornudd M, Poussa T, Antila E, Jaakkola K. The association between high sensitivity C-reactive protein and micronutrient levels: A cross-sectional analysis based on a laboratory database. Clinical nutrition ESPEN. 2019;33:283–9.PubMedCrossRef Tuuminen T, Sorsa M, Tornudd M, Poussa T, Antila E, Jaakkola K. The association between high sensitivity C-reactive protein and micronutrient levels: A cross-sectional analysis based on a laboratory database. Clinical nutrition ESPEN. 2019;33:283–9.PubMedCrossRef
46.
go back to reference Holmes P, James KA, Levy LS. Is low-level environmental mercury exposure of concern to human health? The Science of the total environment. 2009;408(2):171–82.PubMedCrossRef Holmes P, James KA, Levy LS. Is low-level environmental mercury exposure of concern to human health? The Science of the total environment. 2009;408(2):171–82.PubMedCrossRef
47.
go back to reference Zhou X, Wang H, Lian S, Wang J, Wu R. Effect of Copper, Zinc, and Selenium on the Formation of Bovine Neutrophil Extracellular Traps. Biol Trace Elem Res. 2021;199(9):3312–8.PubMedCrossRef Zhou X, Wang H, Lian S, Wang J, Wu R. Effect of Copper, Zinc, and Selenium on the Formation of Bovine Neutrophil Extracellular Traps. Biol Trace Elem Res. 2021;199(9):3312–8.PubMedCrossRef
48.
go back to reference Lominadze D, Saari JT, Percival SS, Schuschke DA. Proinflammatory effects of copper deficiency on neutrophils and lung endothelial cells. Immunol Cell Biol. 2004;82(3):231–8.PubMedCrossRef Lominadze D, Saari JT, Percival SS, Schuschke DA. Proinflammatory effects of copper deficiency on neutrophils and lung endothelial cells. Immunol Cell Biol. 2004;82(3):231–8.PubMedCrossRef
49.
go back to reference Urbanowicz T, Hanć A, Olasińska-Wiśniewska A, Rodzki M, Witkowska A, Michalak M, Perek B, Haneya A, Jemielity M. Serum copper concentration reflect inflammatory activation in the complex coronary artery disease - A pilot study. Journal of trace elements in medicine and biology : organ of the Society for Minerals and Trace Elements (GMS). 2022;74:127064.PubMedCrossRef Urbanowicz T, Hanć A, Olasińska-Wiśniewska A, Rodzki M, Witkowska A, Michalak M, Perek B, Haneya A, Jemielity M. Serum copper concentration reflect inflammatory activation in the complex coronary artery disease - A pilot study. Journal of trace elements in medicine and biology : organ of the Society for Minerals and Trace Elements (GMS). 2022;74:127064.PubMedCrossRef
50.
go back to reference Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G. Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr. 2008;138(2):305–10.PubMedCrossRef Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G. Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr. 2008;138(2):305–10.PubMedCrossRef
51.
go back to reference Lo K, Yang JL, Chen CL, Liu L, Huang YQ, Feng YQ, Yang AM. Associations between blood and urinary manganese with metabolic syndrome and its components: Cross-sectional analysis of National Health and Nutrition Examination Survey 2011–2016. Sci Total Environ. 2021;780:146527.PubMedCrossRef Lo K, Yang JL, Chen CL, Liu L, Huang YQ, Feng YQ, Yang AM. Associations between blood and urinary manganese with metabolic syndrome and its components: Cross-sectional analysis of National Health and Nutrition Examination Survey 2011–2016. Sci Total Environ. 2021;780:146527.PubMedCrossRef
52.
go back to reference Tuschl K, Meyer E, Valdivia LE, Zhao N, Dadswell C, Abdul-Sada A, Hung CY, Simpson MA, Chong WK, Jacques TS, et al. Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood-onset parkinsonism-dystonia. Nat Commun. 2016;7:11601.PubMedPubMedCentralCrossRef Tuschl K, Meyer E, Valdivia LE, Zhao N, Dadswell C, Abdul-Sada A, Hung CY, Simpson MA, Chong WK, Jacques TS, et al. Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood-onset parkinsonism-dystonia. Nat Commun. 2016;7:11601.PubMedPubMedCentralCrossRef
53.
go back to reference Palzes VA, Sagiv SK, Baker JM, Rojas-Valverde D, Gutiérrez-Vargas R, Winkler MS, Fuhrimann S, Staudacher P, Menezes-Filho JA, Reiss AL, et al. Manganese exposure and working memory-related brain activity in smallholder farmworkers in Costa Rica: Results from a pilot study. Environ Res. 2019;173:539–48.PubMedPubMedCentralCrossRef Palzes VA, Sagiv SK, Baker JM, Rojas-Valverde D, Gutiérrez-Vargas R, Winkler MS, Fuhrimann S, Staudacher P, Menezes-Filho JA, Reiss AL, et al. Manganese exposure and working memory-related brain activity in smallholder farmworkers in Costa Rica: Results from a pilot study. Environ Res. 2019;173:539–48.PubMedPubMedCentralCrossRef
54.
go back to reference Finley JW. Does environmental exposure to manganese pose a health risk to healthy adults? Nutr Rev. 2004;62(4):148–53.PubMedCrossRef Finley JW. Does environmental exposure to manganese pose a health risk to healthy adults? Nutr Rev. 2004;62(4):148–53.PubMedCrossRef
55.
go back to reference Huang Q, Wan J, Nan W, Li S, He B, Peng Z. Association between manganese exposure in heavy metals mixtures and the prevalence of sarcopenia in US adults from NHANES 2011–2018. J Hazard Mater. 2024;464:133005.PubMedCrossRef Huang Q, Wan J, Nan W, Li S, He B, Peng Z. Association between manganese exposure in heavy metals mixtures and the prevalence of sarcopenia in US adults from NHANES 2011–2018. J Hazard Mater. 2024;464:133005.PubMedCrossRef
56.
go back to reference Liu Y, Yu M, Cui J, Du Y, Teng X, Zhang Z. Heat shock proteins took part in oxidative stress-mediated inflammatory injury via NF-κB pathway in excess manganese-treated chicken livers. Ecotoxicol Environ Saf. 2021;226:112833.PubMedCrossRef Liu Y, Yu M, Cui J, Du Y, Teng X, Zhang Z. Heat shock proteins took part in oxidative stress-mediated inflammatory injury via NF-κB pathway in excess manganese-treated chicken livers. Ecotoxicol Environ Saf. 2021;226:112833.PubMedCrossRef
59.
go back to reference Jarosz M, Olbert M, Wyszogrodzka G, Młyniec K, Librowski T. Antioxidant and anti-inflammatory effects of zinc. Zinc-dependent NF-κB signaling Inflammopharmacology. 2017;25(1):11–24.PubMed Jarosz M, Olbert M, Wyszogrodzka G, Młyniec K, Librowski T. Antioxidant and anti-inflammatory effects of zinc. Zinc-dependent NF-κB signaling Inflammopharmacology. 2017;25(1):11–24.PubMed
60.
go back to reference Someya Y, Tanihata J, Sato S, Kawano F, Shirato K, Sugiyama M, Kawashima Y, Nomura S, Tachiyashiki K, Imaizumi K. Zinc-deficiency induced changes in the distribution of rat white blood cells. J Nutr Sci Vitaminol. 2009;55(2):162–9.PubMedCrossRef Someya Y, Tanihata J, Sato S, Kawano F, Shirato K, Sugiyama M, Kawashima Y, Nomura S, Tachiyashiki K, Imaizumi K. Zinc-deficiency induced changes in the distribution of rat white blood cells. J Nutr Sci Vitaminol. 2009;55(2):162–9.PubMedCrossRef
61.
go back to reference Sakakibara Y, Sato S, Kawashima Y, Someya Y, Shirato K, Tachiyashiki K, Imaizumi K. Different recovery responses from dietary zinc-deficiency in the distribution of rat granulocytes. J Nutr Sci Vitaminol. 2011;57(2):197–201.PubMedCrossRef Sakakibara Y, Sato S, Kawashima Y, Someya Y, Shirato K, Tachiyashiki K, Imaizumi K. Different recovery responses from dietary zinc-deficiency in the distribution of rat granulocytes. J Nutr Sci Vitaminol. 2011;57(2):197–201.PubMedCrossRef
62.
go back to reference Tutkun L, Gunduzoz M, Turksoy VA, Deniz S, Oztan O, Cetintepe SP, Iritas SB, Yilmaz FM. Arsenic-induced inflammation in workers. Mol Biol Rep. 2019;46(2):2371–8.PubMedCrossRef Tutkun L, Gunduzoz M, Turksoy VA, Deniz S, Oztan O, Cetintepe SP, Iritas SB, Yilmaz FM. Arsenic-induced inflammation in workers. Mol Biol Rep. 2019;46(2):2371–8.PubMedCrossRef
63.
go back to reference Turksoy VA, Tutkun L, Gunduzoz M, Oztan O, Deniz S, Iritas SB. Changing levels of selenium and zinc in cadmium-exposed workers: probable association with the intensity of inflammation. Mol Biol Rep. 2019;46(5):5455–64.PubMedCrossRef Turksoy VA, Tutkun L, Gunduzoz M, Oztan O, Deniz S, Iritas SB. Changing levels of selenium and zinc in cadmium-exposed workers: probable association with the intensity of inflammation. Mol Biol Rep. 2019;46(5):5455–64.PubMedCrossRef
64.
go back to reference Wang X, Bin W, Zhou M, Xiao L, Xu T, Yang S, Nie X, Xie L, Yu L, Mu G, et al. Systemic inflammation mediates the association of heavy metal exposures with liver injury: A study in general Chinese urban adults. J Hazard Mater. 2021;419:126497.PubMedCrossRef Wang X, Bin W, Zhou M, Xiao L, Xu T, Yang S, Nie X, Xie L, Yu L, Mu G, et al. Systemic inflammation mediates the association of heavy metal exposures with liver injury: A study in general Chinese urban adults. J Hazard Mater. 2021;419:126497.PubMedCrossRef
65.
go back to reference Meng Y, Wang K, Wang T, Tu Y, Gong S, Zhang Y, Zhang G, Au W, Christiani DC, Xia ZL. Early occupational exposure to lead on neutrophil-to-lymphocyte ratio and genotoxicity. Environ Int. 2021;151:106448.PubMedCrossRef Meng Y, Wang K, Wang T, Tu Y, Gong S, Zhang Y, Zhang G, Au W, Christiani DC, Xia ZL. Early occupational exposure to lead on neutrophil-to-lymphocyte ratio and genotoxicity. Environ Int. 2021;151:106448.PubMedCrossRef
Metadata
Title
Association between multiple-heavy-metal exposures and systemic immune inflammation in a middle-aged and elderly Chinese general population
Authors
Linhai Zhao
Yanfei Wei
Qiumei Liu
Jiansheng Cai
Xiaoting Mo
Xu Tang
Xuexiu Wang
Lidong Qin
Yujian Liang
Jiejing Cao
Chuwu Huang
Yufu Lu
Tiantian Zhang
Lei Luo
Jiahui Rong
Songju Wu
Wenjia Jin
Qinyi Guan
Kaisheng Teng
You Li
Jian Qin
Zhiyong Zhang
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2024
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-024-18638-z

Other articles of this Issue 1/2024

BMC Public Health 1/2024 Go to the issue