Elsevier

Science of The Total Environment

Volume 670, 20 June 2019, Pages 1028-1036
Science of The Total Environment

Levels and determinants of adipose tissue cadmium concentrations in an adult cohort from Southern Spain

https://doi.org/10.1016/j.scitotenv.2019.03.114Get rights and content

Highlights

  • We explored levels and determinants of adipose tissue Cd levels in 226 adults.

  • Mean (±standard deviation) Cd concentration was 12.66±18.91 μg/Kg.

  • Age, smoking, egg consumption and use of paints were positively associated with Cd.

  • Obesity, sex = male, and meat consumption were negatively associated with Cd.

  • Adipose tissue Cd concentrations might be an adequate proxy for long-term exposure.

Abstract

This study was conceived as a first step to evaluate the suitability of adipose tissue cadmium (Cd) concentrations as a biomarker for the assessment of long-term exposure. Specifically, the aim of this work was to explore the socio-demographic, dietary, and lifestyle determinants of adipose tissue Cd concentrations.

The study population is a subsample of GraMo cohort. Adipose tissue samples were intraoperatively collected from 226 adult volunteers recruited in two public hospitals from Granada, Spain. Cd concentrations in adipose tissue were analyzed by High-Resolution Inductively Coupled Plasma Mass Spectrometry (HR-ICP-MS). Data on socio-demographic characteristics, lifestyle, diet and health status were collected by face-to-face interviews. Predictors of Cd concentrations were assessed by multivariable linear regression with a stepwise variable selection.

We found detectable levels of Cd in the adipose tissue of all the study participants, with a mean concentration (±standard deviation) of 12.66 ± 18.91 μg/kg. Smoking habit at recruitment was associated with increased adipose tissue Cd concentrations (β for smokers = 0.669 p < 0.001; β for former smokers = 0.502, p < 0.001; reference = non-smokers). Age was positively associated with Cd concentrations (β = 0.014, p < 0.001), and men showed lower concentrations than women (β = −0.424, p < 0.001). Obesity, measured as Body Mass Index (BMI), showed an inverse association with Cd concentrations (β = −0.038, p < 0.001). Egg consumption ≥2 portions/week (β = 0.241, p = 0.025) was positively associated with Cd concentrations. Perceived exposure to paints was also positively associated with Cd concentrations. The observed associations with age, smoking habit, BMI, and egg and meat consumption did not substantially change after sex/gender stratification. Our results are consistent with currently-known Cd sources and suggest other potential pathways, which might be population-specific.

As a whole, our findings underline the potential relevance of adipose tissue as a biological matrix for exposure characterization to Cd, as well as for the assessment of long-term clinical implications of the exposure, particularly in obesity-related diseases.

Introduction

Cadmium (Cd) is a metallic element widely used in industrial processes, such as certain paints, nickel-Cd batteries, as a stabiliser in thermoplastics (e.g. polyvinyl chloride), as well as in photography, lithography, tyres, and photoelectric cells in solar panels (Herron, 2003). Cd can also be found as an impurity in zinc, lead and copper ores and alloys, iron, steel, fossil fuels, cement and some fertilizers (IARC, 2012). Phosphorus fertilizers are frequently used in greenhouses (Rodríguez-Martín et al., 2013), which can be a source of Cd contamination of soils, water, and, consequently, the trophic chain (Pan et al., 2010). Other anthropogenic sources include recycling, mining and smelting of zinc-bearing ores, the incineration of waste, the combustion of fossil fuels, and the releases of landfills, among others. The global Cd emission in the mid-90s was estimated in 3000 Tm, decreasing by a half in Europe in the period 1990–2003 (UNEP, 2008). Natural sources of Cd can be found in the Earth's crust and oceans with an average abundance of 0.1–0.2 mg/kg.

Diet and smoking are considered the main sources of Cd exposure in the general population. Ambient air, drinking-water, contaminated soils and dust can also contribute to the exposure, although to a lesser extent, but they could be more relevant for children (Schwartz, 2004). High concentrations of Cd are commonly found in leafy vegetables, starchy roots, cereals/grains, nuts and pulses, and also in specific animal products, e.g. kidney, liver and certain shellfish (IARC, 2012). The mean dietary exposure for the European general population is estimated in 2.04 μg/kg b.w. per week (EFSA, 2012), similar to the figures reported for the Spanish population (AESAN, 2011). Smoking is considered a relevant source of Cd exposure because of the relatively high concentrations in tobacco leaves. In 2009 the CONTAM Panel of the European Food Safety Authority (EFSA) established a tolerable weekly intake of 2.5 μg/kg b.w., which can be easily exceeded in vegetarians, smokers, children and people living in contaminated areas (EFSA, 2009).

Cd is a persistent pollutant, which is slowly degraded in the environment and living organisms (Järup, 2003). Consequently, some of the abovementioned uses have been restricted under the REACH regulation in the European Union in recent years (European Parliament and Council Directive 2013/56/EU; European Commission Regulation 494/2011). However, the majority of the general population still show detectable levels of Cd in blood and urine (López-Herranz et al., 2016; Pirard et al., 2018). Although the health effects of the chronic exposure to low doses of Cd (such as those occurring in the general population) remain unclear, there are certain evidences of renal dysfunction and urinary stone disease, hypertension, lung and prostate cancer, osteoporosis, low birth weight in the offspring, spontaneous miscarriage, obesity, and diabetes (Prozialeck and Edwards, 2012; IARC, 2012; Tinkov et al., 2017; Zang et al., 2019). Indeed, Cd is considered to be a “carcinogenic to humans", by the International Agency for Research on Cancer (IARC, 2012).

Biomonitoring studies are frequently used to assess human exposure to environmental pollutants and their health implications, since internal levels of a pollutant typically account for the overall exposure from different sources and exposure pathways (Needham et al., 2007). The most common human biological matrices used to assess internal levels of Cd are blood and urine, although some research has been performed on hair, nails and saliva. The half-life of Cd strongly differs among biological compartments, e.g. from up to 60 years in the kidneys (Ramírez, 2002) to 3–4 months in blood (Talio et al., 2010). However, there is scant research on Cd concentrations in the adipose tissue, which is considered one of the main reservoirs of lipophilic pollutants as well as an important biological matrix in the development of certain chronic non-infectious diseases, e.g. cancer and metabolic syndrome. Nevertheless, research on adipose tissue concentrations of toxic and essential trace elements (TEs), as well as their biological implications, is still very scarce.

Considering the abovementioned statements, the present study was conceived as a first step to evaluate the suitability of adipose tissue Cd concentrations as a biomarker for the assessment of long-term exposure. Specifically, the aim of this work was to explore the socio-demographic, dietary, and lifestyle determinants of adipose tissue Cd concentrations.

Section snippets

Study area, design and characteristics of participants

This study is part of a wider research which aims to analyse and identify environmental factors affecting the development of chronic diseases in GraMo, an adult cohort in Southern Spain. Study participants were recruited in two public hospitals from Granada province: San Cecilio University Hospital in the city of Granada (240,000 inhabitants, urban area), and Santa Ana Hospital in the town of Motril (50,000 inhabitants, semi-rural area). The recruitment has been extensively described elsewhere (

Adipose tissue Cd concentrations in the study population

The adipose tissue concentrations of Cd and the characteristics of the study population are summarized in Table 1 and Fig. 1. We detected Cd in all (100%) the analyzed samples.

To the best of our knowledge, this is one of the very first epidemiological studies exploring Cd concentrations in human adipose tissue. Qin et al. (2010) observed mean adipose tissue Cd concentrations of 0.47 μg/kg in patients with uterine leiomyoma and of 0.38 μg/kg in a control group. The concentrations in our

Conclusions

We detected Cd in all the adipose tissue samples from the study population, and identified certain predictors of the exposure, such as age, sex/gender, BMI, smoking habit, eggs and meat consumption and exposure to paints (the latter only in men). This points to a potential relevance of adipose tissue Cd concentrations for exposure characterization as well as for the assessment of long-term effects of chronic exposure to low levels of Cd, which are currently being studied in GraMo cohort.

Conflict of interest

The authors declare no conflict of interest.

Acknowledgements

This study would have never been successful without the collaboration of the patients taking part in it. Dr. J.P. Arrebola is under contract within Ramon y Cajal program (RYC-2016-20155, Ministerio de Economía, Industria y Competitividad, Spain). This study was supported by research grants from CIBER de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, Junta de Andalucía and European Regional Development Fund – FEDER (PI16/01858, BA15/00093, FIS PI-11/0610, EF-0428-2016

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