Abstract
Adverse health effects related to accumulative cadmium (Cd) exposure have aroused widespread attention from the public in China. Knowledge on the relationships between Cd exposure and early renal effects is particularly limited for children, who are more susceptible to absorbing metals than adults. A typical Cd-polluted area of South China was selected to determine the Cd exposure and related early renal effects of the general population, including children. In total, 211 children and 806 adults were enrolled in the study. The urinary levels of Cd (U-Cd), β2-microglobulin (U-BMG), retinol binding protein (U-RBP), and N-acetyl-β-d-glucosaminidase (U-NAG) were measured. The relationship between U-Cd and ranked indicators of early renal effects was examined by multiple regression analysis. The average U-Cd ranged from 7.01 μg/g creatinine (boys) to 13.55 μg/g creatinine (women) in the Cd-polluted areas. These values are much higher than those of the control group and those that have been reported by other countries. In agreement with previous studies, environmental Cd pollution resulted in elevated Cd accumulation in the bodies of children, and it increased the concentration of NAG in their urine. Similarly, environmental Cd pollution increased NAG and BMG in the urine of adults. Multivariate models showed that the urinary excretion of BMG, RBP, and NAG was positively associated with Cd levels in the urine of both children and adults. The reference thresholds of U-Cd in relation to elevated U-BMG, U-RBP, and U-NAG were higher in children than adults after standardization for other covariates. These results reinforce the need to control and regulate the sources of environmental Cd contamination and to promote more effective risk management measures, especially for vulnerable groups.
Similar content being viewed by others
References
Akerstrom M, Barregard L, Lundh T, Sallsten G (2014) Variability of urinary cadmium excretion in spot urine samples, first morning voids, and 24 h urine in a healthy non-smoking population: implications for study design. J Expo Sci Env Epid 24:171–179. https://doi.org/10.1038/jes.2013.58
Bernard A (2004) Renal dysfunction induced by cadmium: biomarkers of critical effects. Biometals 17:519–523
Bernard A (2008) Cadmium & its adverse effects on human health Indian. J Med Res 128:557–564
Bernard A, Thielemans N, Roels H, Lauwerys R (1995) Association between nag-B and cadmium in urine with no evidence of a threshold. Occup Environ Med 52:177–180
Bi XY, Feng XB, Yang YG, Qiu GL, Lia GH (2006) Quantitative assessment of cadmium emission from zinc smelting and its influences on the surface soils and mosses in Hezhang County, Southwestern China. Atmos Environ 40:4228–4233
Brockhaus A, Collet W, Dolgner R, Engelke R (1988) Exposure to lead and cadmium of children living in different areas of North-West Germany—results of biological monitoring studies 1982–1986.pdf International archives of occupational and environmental health 60:22
Cai S, Yue L, Shang Q, Nordberg GF (1995) Cadmium exposure among residents in an area contaminated by irrigation water in China. Bull World Health Organ 73:9
Cai SW, Yue L, Hu ZN, Zhong XZ, Ye ZL, Xu HD, Liu YR, Ji RD, Zhang WH, Zhang FY (1990) Cadmium exposure and health-effects among residents in an irrigation area with ore dressing wastewater. Sci Total Environ 90:67–73
Cai Y, Aoshima K, Katoh T, Teranishi H, Kasuya M (2001) Renal tubular dysfunction in male inhabitants of a cadmium-polluted area in Toyama, Japan—an eleven-year follow-up study. J Epidemiol 11:180–189
CDC, Centers for Disease Control and Prevention (2009). Fourth National Report on Human Exposure to Environmental Chemicals Department of Health and Human Services Centers for Disease Control and Prevention
Chaumont A, Voisin C, Deumer G, Haufroid V, Annesi-Maesano I, Roels H, Thijs L, Staessen J, Bernard A (2013) Associations of urinary cadmium with age and urinary proteins: further evidence of physiological variations unrelated to metal accumulation and toxicity. Environ Health Perspect 121:1047–1053. https://doi.org/10.1289/ehp.1306607
Cheng S (2007) Heavy metal pollution in China: Origin, pattern and control—a state-of-the-art report with special reference to literature published in Chinese journals Environ Sci Pollut R 14:489–489
Cui YJ, Zhu YG, Zhai RH, Huang YZ, Qiu Y, Liang JZ (2005) Exposure to metal mixtures and human health impacts in a contaminated area in Nanning, China. Environ Int 31:784–790. https://doi.org/10.1016/j.envint.2005.05.025
de Burbure C et al (2003) Biomarkers of renal effects in children and adults with low environmental exposure to heavy metals. J Toxicol Env Heal A 66:783–798
de Burbure C, Buchet JP, Leroyer A, Nisse C, Haguenoer JM, Mutti A, Smerhovsky Z, Cikrt M, Trzcinka-Ochocka M, Razniewska G, Jakubowski M, Bernard A (2006) Renal and neurologic effects of cadmium, lead, mercury, and arsenic in children: evidence of early effects and multiple interactions at environmental exposure levels. Environ Health Perspect 114:584–590
Diazbarriga F, Santos MA, Mejia JD, Batres L, Yáñez L, Carrizales-Yáñez L (1993) Arsenic and cadmium exposure in children living near a smelter complex in San Luis Potosı, Mexico. Environ Res 62:9
Fassett RG, Venuthurupalli SK, Gobe GC, Coombes JS, Cooper MA, Hoy WE (2011) Biomarkers in chronic kidney disease: a review. Kidney Int 80:806–821. https://doi.org/10.1038/ki.2011.198
Fels LM et al (1998) Adverse effects of chronic low level lead exposure on kidney function—a risk group study in children. Nephrol Dial Transpl 13:2248–2256
Gao YH, Zhang Y, Yi J, Zhou J, Huang X, Shi X, Xiao S, Lin D (2016) A longitudinal study on urinary cadmium and renal tubular protein excretion of nickel-cadmium battery workers after cessation of cadmium exposure. Int Arch Occup Environ Health 89:1137–1145
He B, Yun ZJ, Shi JB, Jiang GB (2013) Research progress of heavy metal pollution in China: sources, analytical methods, status, and toxicity. Chinese Sci Bull 58:134–140
He ZY, Xu XS, Zou HB, Wang XD, Yu Y (2010) Geochronology, petrogenesis and metallogeny of Piaotang granitoids in the tungsten deposit region of South China. Geochem J 44:5
Health C (2010) Report on Human Biomonitoring of Environmental Chemicals in Canada. http://www.hc-sc.gc.ca/ewh-semt/pubs/contaminants/chms-ecms/section8-eng.php
Honda R, Swaddiwudhipong W, Nishijo M, Mahasakpan P, Teeyakasem W, Ruangyuttikarn W, Satarug S, Padungtod C, Nakagawa H (2010) Cadmium induced renal dysfunction among residents of rice farming area downstream from a zinc-mineralized belt in Thailand. Toxicol Lett 198:26–32
Horiguchi H, Oguma E, Sasaki S, Okubo H, Murakami K, Miyamoto K, Hosoi Y, Murata K, Kayama F (2013) Age-relevant renal effects of cadmium exposure through consumption of home-harvested rice in female Japanese farmers. Environ Int 56:1–9. https://doi.org/10.1016/j.envint.2013.03.001
Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 5:6
Huang M, Choi SJ, Kim DW, Kim NY, Bae HS, Yu SD, Kim DS, Kim H, Choi BS, Yu IJ, Park JD (2013) Evaluation of factors associated with cadmium exposure and kidney function in the general population. Environ Toxicol 28:563–570
Iwata K, Saito H, Moriyama M, Nakano A (1993) Renal tubular function after reduction of environmental cadmium exposure: a ten-year follow-up. Arch Environ Health 48:157–163. https://doi.org/10.1080/00039896.1993.9940814
Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:8
Jin TY, Nordberg M, Frech W, Dumont X, Bernard A, Ye TT, Kong Q, Wang Z, Li P, Lundström NG, Li Y, Nordberg GF (2002) Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). Biometals 15:397–410
Jin TY, Wu X, Tang Y, Nordberg M, Bernard A, Ye T, Kong Q, Lundström NG, Nordberg GF (2004) Environmental epidemiological study and estimation of benchmark dose for renal dysfunction in a cadmium-polluted area in China. Biometals 17:525–530
Johri N, Jacquillet G, Unwin R (2010) Heavy metal poisoning: the effects of cadmium on the kidney. Biometals 23:783–792
Ke S, Cheng XY, Zhang JY, Jia WJ, Li H, Luo HF, Ge PH, Liu ZM, Wang HM, He JS, Chen ZN (2015) Estimation of the benchmark dose of urinary cadmium as the reference level for renal dysfunction: a large sample study in five cadmium polluted areas in China. BMC Public Health 15:656
Kim YD, Yim DH, Eom SY, Moon SI, Park CH, Kim GB, Yu SD, Choi BS, Park JD, Kim H (2015) Temporal changes in urinary levels of cadmium, N-acetyl-beta-D-glucosaminidase and beta(2)-microglobulin in individuals in a cadmium-contaminated area. Environ Toxicol Phar 39:35–41
Lauwerys RR, Bernard AM, Roels HA, Buchet JP (1994) Cadmium—exposure markers as predictors of nephrotoxic effects. Clin Chem 40:1391–1394
Li YC, Wang LM, Jiang Y, Li XY, Zhang M, Hu N (2012) Prevalence of hypertension among Chinese adults in 2010 [In Chinese]. Chinese Journal of Preventive Medicine [Zhonghua Yu Fang Yi Xue Za Zhi] 46(5)
Li ZY, Ma ZW, van der Kuijp TJ, Yuan ZW, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853
Liang YH, Lei L, Nilsson J, Li H, Nordberg M, Bernard A, Nordberg GF, Bergdahl IA, Jin T (2012) Renal function after reduction in cadmium exposure: an 8-year follow-up of residents in cadmium-polluted areas. Environ Health Persp 120:223–228. https://doi.org/10.1289/ehp.1103699
MOHC, Ministry of Health of the People’s Republic of China (1998) Standard of China, GB/T. Discriminant standard for health hazard area caused by environmental cadmium pollution. Standards Press of, China, Beijing, pp 17221–11998
Moriguchi J, Inoue Y, Kamiyama S, Horiguchi M (2009) N-Acetyl-β-d-glucosaminidase (NAG) as the most sensitive marker of tubular dysfunction for monitoring residents in non-polluted areas. Toxicol Lett 190:8
Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J (2010) Cadmium exposure in the population: from health risks to strategies of prevention. Biometals 23:769–782. https://doi.org/10.1007/s10534-010-9343-z
Nogawa K, Kobayashi E, Okubo Y, Suwazono Y (2004) Environmental cadmium exposure, adverse effects and preventive measures in Japan. Biometals 17:581–587
Noonan CW, Sarasua SM, Campagna D, Kathman SJ, Lybarger JA, Mueller PW (2002) Effects of exposure to low levels of environmental cadmium on renal biomarkers. Environ Health Persp 110:151–155
Nordberg GF, Fowler BA, Nordberg M (2014) Handbook on the toxicology of metals. Academic Press
Nordberg GF, Jin T, Kong Q, Ye T, Cai S, Wang Z, Zhuang F, Wu X (1997) Biological monitoring of cadmium exposure and renal effects in a population group residing in a polluted area in China. Sci Total Environ 199:111–114
Nordberg GF, Jin T, Wu X, Lu J (2009) Prevalence of kidney dysfunction in humans—relationship to cadmium dose, metallothionein, immunological and metabolic factors. Biochimie 91:5
Nordberg GF, Nogawa K, Nordberg M, Friberg LT (2007) Cadmium. In: Handbook on the toxicology of metals. Third edition edn. Academic Press, pp 446–486
O'Connor RJ, Li Q, Stephens WE, Hammond D, Elton-Marshall T, Cummings KM, Giovino GA, Fong GT (2010) Cigarettes sold in China: design, emissions and metals. Tob Control 19:i47–i53
Prozialeck WC (2013) Biomarkers for cadmium. In: Encyclopedia of metalloproteins. Springer, New York, pp 272–277
Prozialeck WC, Edwards JR (2010) Early biomarkers of cadmium exposure and nephrotoxicity. Biometals 23:793–809. https://doi.org/10.1007/s10534-010-9288-2
Satarug S (2012) Long-term exposure to cadmium in food and cigarette smoke, liver effects and hepatocellular carcinoma. Curr Drug Metab 13:257–271
Satarug S, Baker JR, Urbenjapol S, Haswell-Elkins M, Reilly PEB, Williams DJ, Moore MR (2003) A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett 137:65–83
Sun H, Wang D, Zhou Z, Ding Z, Chen X, Xu Y, Huang L, Tang D (2016) Association of cadmium in urine and blood with age in a general population with low environmental exposure. Chemosphere 156:392–397. https://doi.org/10.1016/j.chemosphere.2016.05.013
Suwazono Y, Nogawa K, Uetani M, Kido T, Nakagawa H (2011) Reassessment of the threshold of urinary cadmium by using hybrid approach in a cadmium non-polluted area in Japan. Int J Hyg Envir Heal 214:175–178. https://doi.org/10.1016/j.ijheh.2010.09.002
Swaddiwudhipong W, Mahasakpan P, Jeekeeree W, Funkhiew T, Sanjum R, Apiwatpaiboon T, Phopueng I (2015) Renal and blood pressure effects from environmental cadmium exposure in Thai children. Environ Res 136:82–87. https://doi.org/10.1016/j.envres.2014.10.017
Tellez-Plaza M, Navas-Acien A, Caldwel KL, Menke A, Muntner P, Guallar E (2012) Reduction in cadmium exposure in the United States population, 1988-2008: The Contribution of Declining Smoking Rates. Environ Health Persp 120:204–209
Trzcinka-Ochocka M, Jakubowski M, Razniewska G, Halatek T, Gazewski A (2004) The effects of environmental cadmium exposure on kidney function: the possible influence of age. Environ Res 95:143–150. https://doi.org/10.1016/j.envres.2003.10.003
Wallin M, Sallsten G, Lundh T, Barregard L (2014) Low-level cadmium exposure and effects on kidney function. Occup Environ Med 71:848–854
Wang DY, Sun H, Wu Y, Zhou ZY, Ding Z, Chen XD, Xu Y (2016) Tubular and glomerular kidney effects in the Chinese general population with low environmental cadmium exposure. Chemosphere 147:3–8. https://doi.org/10.1016/j.chemosphere.2015.11.069
Watanabe T, Nakatsuka H, Shimbo S, Yaginuma-Sakurai K, Ikeda M (2013) High cadmium and low lead exposure of children in Japan. Int Arch Occup Environ Health 86:865–873
WHO, World Health Organization (1989) Evaluation of certain food additives and contaminants. Thirty-third report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organizaton, Geneva
WHO, World Health Organization (1996) Biological monitoring of chemical exposure in the workplace vol 1. World Health Organization, Geneva
Witte EC, Lambers Heerspink HJ, de Zeeuw D, Bakker SJL, de Jong PE, Gansevoort R (2009) First morning voids are more reliable than spot urine samples to assess microalbuminuria. J Am Soc Nephrol 20:436–443. https://doi.org/10.1681/Asn.2008030292
Wu XW, Liang Y, Jin T, Ye T, Kong Q, Wang Z, Lei L, Bergdahl IA, Nordberg GF (2008) Renal effects evolution in a Chinese population after reduction of cadmium exposure in rice. Environ Res 108:233–238
Yuan X, Wang J, Shang Y, Sun B (2014) Health risk assessment of cadmium via dietary intake by adults in China. J Sci Food Agric 94:373–380. https://doi.org/10.1002/jsfa.6394
Zhang W, Zheng J (2016) Comparison of dietary cadmium exposure among the general population from two cadmium-polluted regions in China. J Pollut Effects Control 4. https://doi.org/10.4172/2375-4397.1000167
Zhang WL, Du Y, Zhai MM, Shang Q (2014) Cadmium exposure and its health effects: a 19-year follow-up study of a polluted area in China. Sci Total Environ 470:224–228
Acknowledgements
This work was supported by the Special Environmental Research Fund for Public Welfare (No. 201009046) and received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no. 269233-GLOCOM (Global Partners in Contaminated Land Management).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
This work was supported by the Special Environmental Research Fund for Public Welfare (No. 201009046). The views expressed in the manuscript are only the views of the authors and do not necessarily reflect those of the funding agencies. The biological samples were collected after informed consent forms were written and returned by the participants. In addition, the participants and researchers of the entire study have no conflicts of interest.
Additional information
Responsible editor: Philippe Garrigues
Highlights
• Exposure to environmental Cd from tungsten-molybdenum mining activities has resulted in increased Cd accumulation in the bodies of school children, elevated excretion of U-NAG in the investigated school children and adults, and elevated U-BMG in adults.
• The urinary excretion of NAG, BMG, and RBP is significantly affected by cadmium in the urine of both children and adults after an adjustment for other covariates.
• Reference doses of U-Cd in relation to the elevation of early renal effect indicators were higher in children than adults.
Rights and permissions
About this article
Cite this article
Cui, X., Cheng, H., Liu, X. et al. Cadmium exposure and early renal effects in the children and adults living in a tungsten-molybdenum mining areas of South China. Environ Sci Pollut Res 25, 15089–15101 (2018). https://doi.org/10.1007/s11356-018-1631-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1631-0