Adipose tissue concentrations of arsenic, nickel, lead, tin, and titanium in adults from GraMo cohort in Southern Spain: An exploratory study
Graphical abstract
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
References (80)
- et al.
Biomonitoring of urinary metals in a population living in the vicinity of industrial sources: a comparison with the general population of Andalusia, Spain
Sci. Total Environ.
(2008) - et al.
Placental concentrations of heavy metals in a mother-child cohort
Environ. Res.
(2013) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review
Environ. Int.
(2008)- et al.
Predictors of concentrations of hexachlorobenzene in human adipose tissue: a multivariate analysis by gender in Southern Spain
Environ. Int.
(2009) - et al.
Human exposure to p,p’-dichlorodiphenyldichloroethylene (p,p’-DDE) in urban and semi-rural areas in southeast Spain: a gender perspective
Sci. Total Environ.
(2013) - et al.
Associations of accumulated exposure to persistent organic pollutants with serum lipids and obesity in an adult cohort from Southern Spain
Environ. Pollut.
(2014) - et al.
Historical exposure to persistent organic pollutants and risk of incident hypertension
Environ. Res.
(2015) - et al.
Tributyltin chloride leads to adiposity and impairs metabolic functions in the rat liver and pancreas
Toxicol. Lett.
(2015) - et al.
BIOAMBIENT.ES. Blood lead levels in a representative sample of the Spanish adult population: the BIOAMBIENT.ES project
Int. J. Hyg. Environ. Health
(2014) - et al.
Effects of arsenic on adipocyte metabolism: is arsenic an obesogen?
Mol. Cell. Endocrinol.
(2017)