Adipose tissue concentrations of arsenic, nickel, lead, tin, and titanium in adults from GraMo cohort in Southern Spain: An exploratory study

https://doi.org/10.1016/j.scitotenv.2020.137458Get rights and content

Highlights

  • Ni, Pb, Sn, and Ti were present in 100% of adipose tissue samples from adults.

  • Detectable concentrations of As were found in 51% of adipose tissue samples.

  • Ni was the metal showing the highest median concentration (0.56 μg/g).

Abstract

Background

Adipose tissue has been acknowledged as a potential target for obesogenic pollutants, including toxic metal(loid)s. However, the presence of these chemicals in the adipose tissue has been poorly characterized.

Objective

To examine the distributions of adipose tissue concentrations of five toxic metal(loid)s (i.e., arsenic [As], nickel [Ni], lead [Pb], tin [Sn], and titanium [Ti]) in adults, and potential socio-demographic and lifestyle factors associated with metal(loid) concentrations.

Methods

The study population consisted of a subsample of 228 subjects from GraMo cohort in Southern Spain (N = 387). Adipose tissue samples were intra-operatively collected from adults recruited in 2003–2004 in two public hospitals, and concentrations of metal(loid)s in adipose tissue were analyzed in 2015 by High-Resolution Inductively Coupled Plasma Mass Spectrometry. Data on socio-demographic and lifestyle factors were obtained by baseline questionnaire completion. Linear and multinomial regression was used to identify factors associated with metal(loid) levels.

Results

Ni, Pb, Sn, and Ti were detected in all adipose tissue samples, and As in 51% of them. Ni was the metal showing the highest median concentration (0.56 μg/g), followed by Ti (0.31 μg/g), Pb (0.08 μg/g), Sn (0.06 μg/g), and As (0.003 μg/g). Predictors of As levels included area of residence, social class, and oily fish intake; for Ni: area of residence and consumption of cheese, meat, eggs, and canned food; for Pb: vegetables intake and industrial occupation; for Sn: age, body mass index, and consumption of lean fish, eggs, and milk; and cheese intake for Ti. Some of these predictors were sex-specific, particularly those regarding dietary intake.

Conclusions

This exploratory study provides the first evidence of the occurrence of Ni, Pb, Sn, Ti, and As in adipose tissue from adult population, and highlights the potential of this tissue as a biological matrix for studying exposure levels and chronic health effects of toxic metal(loid)s.

Introduction

Humans are simultaneously exposed to multiple toxic chemicals, among which metallic/metalloid elements are of special concern as they are ubiquitous and are often present at high levels in the environmental compartments and occupational setting. The most common human biological matrices used to assess internal levels of metals are blood and urine (Campos et al., 2019; Gil and Hernández, 2015). However, blood and urinary levels may serve as a useful indicator for assessing levels of recent metal exposure, with some exceptions such as urinary cadmium (Cd) biomarker which is considered as indicative of long-term Cd exposure. Some human studies have also used levels in hair, nails, and placenta as indicators of metal bioaccumulation (Amaya et al., 2013; Gil et al., 2011; Gil and Hernández, 2015). The use of non-conventional biological matrices such as adipose tissue for assessing body burden of toxic metals has been far less common (Echeverría et al., 2019; Qin et al., 2010; Rodríguez-Pérez et al., 2018).

Arsenic (As), nickel (Ni), lead (Pb), tin (Sn), and titanium (Ti) are metal(oid)s naturally occurring in the environment. As, Ni, and Pb are among the most toxic environmental pollutants (ATSDR, 2017). Chronic exposure to these three elements has been associated with a variety of adverse health effects in humans, including adverse reproductive outcomes and neurodevelopmental impairment in children (Freire et al., 2019; Quansah et al., 2015; Rodríguez-Barranco et al., 2013), obesity, diabetes, and cardiovascular disorders (Feng et al., 2015; Navas-Acien et al., 2006, Navas-Acien et al., 2007; Scannell Bryan et al., 2019; Wang et al., 2018a; Zhang et al., 2012), respiratory tract disease and pulmonary function deficits (Moitra et al., 2018; Sanchez et al., 2018), renal dysfunction (Cheng et al., 2018; Orr and Bridges, 2017; Wang et al., 2018b), and immune and gastrointestinal effects (Dangleben et al., 2013; Abdul et al., 2015; Vázquez et al., 2015). Moreover, inorganic As and Ni compounds are classified by the International Agency for Research on Cancer (IARC) as carcinogenic or possibly carcinogenic to humans (Group 1), while inorganic Pb compounds are classified as possibly carcinogenic to humans (Group 2B) (IARC, 2012; Mulware, 2013).

Human activities causing environmental As contamination include smelting of metals and coal burning, while inorganic As compounds can occur in groundwater from natural or anthropogenic sources. In non-occupationally exposed populations, exposure to As occurs primarily through drinking water and diet, particularly via seafood intake (ATSDR, 2007; Vázquez et al., 2015). Humans may be exposed to Pb through a number of food sources, drinking water, and air. In the general population, diet and surface dusts are currently considered the major contributors to blood Pb levels (ATSDR, 2017; Vázquez et al., 2015). Ni is used in the manufacturing of electronics, metal alloys, and batteries, being released to the atmosphere by combustion of fuel oil, municipal incineration, and industries involved in Ni refining, steel production, and other Ni alloy production (ATSDR, 2005a).

Tin metal (Sn) is extensively used to line cans for food, beverages, and aerosols, and it is also present in brass, bronze, pewter, and some soldering materials. Organotin compounds are widely used in personal care products, heat stabilizers, food additives, food packages, plastic pipes, pesticides, and paints (Antizar-Ladislao, 2008; ATSDR, 2005b). Titanium dioxide (TiO2) particles are extensively used in an increasing variety of consumer products, including paints, varnishes, plastic, ceramics, rubber, and printing ink, floor coverings, coated textiles, and in the production of electronic components, dental impression, and medical implant prosthesis. TiO2 particles are also used as food additives and as ingredients in a wide range of pharmaceutical products and cosmetics, such as sunscreens and toothpastes (CDC, 2011). In spite of the extensive use of Sn compounds and TiO2 particles, little research has been conducted on human biomonitoring and potential health effects. Higher exposure to Sn compounds has been related to metabolic and adverse reproductive effects in humans (Liu et al., 2018; Rantakokko et al., 2012, Rantakokko et al., 2014). TiO2 nanoparticles can induce inflammation and chromosome damage (Baranowska-Wójcik et al., 2020), whereas there is no consistent evidence of a link between occupational TiO2 exposure and risk of lung cancer (CDC, 2011).

Adipose tissue is involved in several physiological functions, including metabolic regulation, energy storage, endocrine functions, and modulation of persistent pollutant toxicity; adipose tissue may also act as a target of obesogenic pollutants (La Merrill et al., 2013). Moreover, it has been recently hypothesized that the presence of metallic/metalloid elements in adipose tissue may be associated with obesity-related metabolic disturbances (Tinkov et al., 2015). In this context, the present report represents a continuation of previous efforts of our research group focused on the characterization of metal concentrations in human adipose tissue, a potential biological matrix for the accumulation of lipophilic metallic elements (Echeverría et al., 2019; Rodríguez-Pérez et al., 2018). The objectives of the current exploratory study were: 1) to examine the distribution of adipose tissue concentrations of As, Ni, Pb, Sn, and Ti in a cohort of adults in Southern Spain, and 2) to examine potential associations of a set of socio-demographic and lifestyle variables with the adipose tissue metal(loid) concentrations.

Section snippets

Study population

This research work is part of a larger, ongoing prospective study (GraMo cohort) that aims to investigate the role of various environmental exposures, including persistent organic pollutants, non-persistent chemicals, and metallic/metalloid elements, on the risk of chronic diseases in adults. The cohort was recruited in 2003–2004 in two public hospitals in the province of Granada, Southern Spain, i.e.: San Cecilio University Hospital in the city of Granada (240,000 inhabitants) and Santa Ana

Results

Table 1 summarizes general characteristics of study participants, among which 127 (56%) were males. Nearly one-third were 18–39 years old, did not complete primary school, and lived in a rural area and close to an industrial area; 78% belonged to manual social classes; 10% had worked in the industry sector in the past 10 years, 16% in construction, 7% in restoration activities, and up to 42% in agriculture; 60% of participants were current or ex-smokers, and up to 67% were overweight or obese.

Discussion

This exploratory study assessed the concentrations of three well-known toxic metal(loid)s (As, Ni, and Pb) and two other ubiquitous but largely understudied metals (Sn and Ti) in adipose tissue samples from a hospital-based cohort in Spain, and examined associations with socio-demographic and lifestyle factors. The obtained results provide the first evidence of the wide presence of various toxic metal(loid)s in adipose tissue from adult population, suggesting that adipose tissue concentrations

Conclusions

The present data reveal a wide presence of Ni, Pb, Sn, and Ti in adipose tissue samples from adults, and presence of As in half of the adipose tissue samples. The observed results suggest that adipose tissue concentrations may be related to certain dietary habits and socio-demographic characteristics. This is a novel study that underlines the relevance of adipose tissue as a potential target organ for toxic metal(loid)s, and highlights the usefulness of this biological matrix for studying

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This study would have never been successful without the collaboration of the patients taking part in it. This research was funded in part by grants from Instituto de Salud Carlos III (ISCIII), Junta de Andalucía and European Regional Development Fund – FEDER (FIS PI-16/01858, FIS PI-11/0610, FIS PI-13/02406, BA15/00093, and EF-0428-2016), and Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP). The authors are also grateful to the ISCIII for the postdoctoral research

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