Associations of residential and occupational history with the distribution of persistent pollutant mixtures in adipose tissue samples

https://doi.org/10.1016/j.envres.2020.110687Get rights and content

Highlights

  • We explored mixtures of persistent pollutants in adipose tissue of 227 adults.

  • We studied associations of pollutant’ concentrations with residence and occupation.

  • Relevant differences between urban, industrial and rural zones were found.

  • Exposure patterns differed depending on the occupational history.

Abstract

This research aims to explore clusters of a mixture of 15 Persistent Toxic Substances (PTSs) in the adipose tissue of 227 individuals of an adult cohort from Granada Province (Southern Spain). Information about residence and occupation during participants lifetime was gathered by means of validated questionnaires. Clusters of pollutants in the study population were identified by Principal Component Analyses (PCA). PCA analyses revealed three major clusters of pollutants: PC1, representing predominantly an assortment of metal(loid)s, namely aluminium, arsenic, chromium, nickel and lead; PC2, including mostly Organochlorine Pesticides (OCPs), such as HCB, β-HCH and p,p’-DDE; and PC3, gathering mainly a mixture of Polychlorinated Biphenyls (PCB-138, PCB-153 and PCB-180) and metals (cadmium, cobalt and chromium). The patterns of distribution of individual pollutants and their mixtures were explored through Geographic Information Systems and multivariable linear regression models. Living in rural areas was associated with decreased levels of the mixture of PCBs and metals. Residents of industrial and heavy traffic areas showed increased levels of the mixture of metal(loid)s. Those living in rural and semi-rural areas at recruitment had decreased levels of the OCP mixture. Occupational history related to agriculture and food industry was associated with increased levels of the mixture of metal(loid)s, whereas those who had been involved in motor and industrial activities showed increased levels of the OCP mixture. Participants who had worked in cleaning and housekeeping activities for long periods showed decreased levels of the mixture of PCBs and metals. Our research revealed suggestive clusters of exposure, that emphasized the need for further epidemiological studies to address the effect of environmental pollutants from a mixture perspective. Results also highlight the potential of adipose tissue as a matrix for exposure assessment to combinations of different families of contaminants.

Introduction

Persistent Toxic Substances (PTSs) are a group of chemicals of high concern due to their ubiquity in the environment, in addition to their toxicity, persistence, and bioaccumulation characteristics (Jones and de Voogt, 1999; United Nations Environment Program, 2018; Wong et al., 2012). PTSs include several pollutants particularly relevant for public health, such as Persistent Organic Pollutants (POPs). POPs comprise Polychlorinated Biphenyls (PCBs), which have been used in several industrial applications (Cetin et al., 2007; Eljarrat et al., 2008); and Organochlorine Pesticides (OCPs), widely used in agriculture, seed preservation and public health campaigns in the past, but whose residues are still present nowadays in soils and animal tissues, including human tissues, in spite of strict legal restrictions on their production and uses since the 1980s decade (Arrebola et al., 2013a; Fernández et al., 2000; Luzardo et al., 2006; Mercado et al., 2013). As a result, human exposure to low levels of POPs is frequent and generalized (Centers for Disease Control and Prevention, 2009; Porta et al., 2008), and has been linked to several chronic diseases (Arrebola et al., 2013b; Charazac et al., 2019; Koskenniemi et al., 2015; Lee et al., 2014; Li et al., 2006; Porta, 2006).

On the other side, current and past toxic metal(loid) contamination in soils, water and food caused by industry, mining, pesticides and transports has been widely reported (Castro-González and Méndez-Armenta, 2008; Lokeshappa et al., 2012; Mohmand et al., 2015; Peris et al., 2007), and mitigation measures have been undertaken in order to reduce the exposure to these substances and their related health consequences. Some metal(loid)s, such as aluminium (Al), cadmium (Cd), nickel (Ni), lead (Pb), and arsenic (As), do not have a known biological function in the human organism and there are evidences of potential adverse effects for human health even at very low concentrations. Others, like chromium (Cr) and cobalt (Co), play a role in some biological processes, but at certain doses can contribute to the development of diseases (Agarwal et al., 2011; Byrne et al., 2013; Freire et al., 2018; Jaishankar et al., 2014; Sabath and Robles-Osorio, 2012; Tinkov et al., 2015).

Considering the ubiquity of the exposure to most PTSs, human biomonitoring has become essential in order to assess the body burden of many different pollutants, since internal pollutant levels account for all possible exposure routes (Louro et al., 2019). Human biomonitoring studies have traditionally focused on blood, serum, urine, nails and/or hair measurements, some of them providing meaningful information about severity and timing of the exposure (Clarkson et al., 2012; Porta et al., 2008). However, adipose tissue is considered a major matrix for long-term POP accumulation, offering promising insights for exposure assessment (Artacho-Cordón et al., 2016; Mustieles and Arrebola, 2020). Nevertheless, adipose tissue POP concentrations have been scarcely used in the epidemiological context because of the invasive techniques required for sampling (Artacho-Cordón et al., 2015; La Merrill Michele et al., 2013; Lee et al., 2017; Mustieles and Arrebola, 2020). On the other hand, little has been investigated about the biological meaning of metal(loid)s concentrations in adipose tissue, although it has been recently suggested as a potentially relevant matrix for exposure and effect assessment (Echeverría et al., 2019; Freire et al., 2020; Mustieles and Arrebola, 2020; Qin et al., 2010; Rodríguez-Pérez et al., 2018; Tinkov et al., 2015).

General populations are frequently exposed to PTSs through air, water and food produced in a contaminated area/soil, among others. Notable inter-regional differences have been found in the internal PTS levels that, interestingly, have also been reported in subgroups within the same geographical region, e.g., rural vs urban zones (Harner et al., 2004), near vs far from industry facilities (García-Pérez et al., 2007), as well as clean vs polluted drinking water from aquifers (Schwarzenbach et al., 2010).

Occupational exposure to PTSs has been analyzed before, linking activities like agriculture, industry, cleaning and building with the internal levels of some contaminants (Okeme and Arrandale, 2019; Schettgen et al., 2018; Varona et al., 2010). Accordingly, some occupations might be considered to pose a higher risk of developing PTS-related diseases, such as mining and other industrial activities (Montano, 2014). Housekeeping and informal cleaning are usually thought to be less hazardous, although they involve frequent contact with products containing a number of highly toxic substances (Bello et al., 2009; Medina-Ramon et al., 2003).

It is noteworthy that the majority of the abovementioned information has been generated based on studies focused on individual pollutants, even when the overall mixture effects might be more important than the exposure to low doses of one single chemical (Kortenkamp, 2007; Solomon et al., 2016; Svingen and Vinggaard, 2016). Indeed, addressing human exposure characterization from a mixture perspective would help to identify clusters particularly exposed and, consequently, potentially vulnerable subpopulations.

This research is framed within GraMo adult cohort, in which our group has previously characterized exposure levels to different PTSs and their potential health effects (Arrebola et al, 2009, 2010, 2014a, 2014b, 2015; Echeverría et al., 2019; Freire et al., 2020; Rodríguez-Pérez et al., 2018). Specifically, the present work aimed to perform a step forward on human exposure assessment by identifying clusters of individuals with similar co-exposure profiles, and studying their relationship with participants’ occupational and residential history.

Section snippets

Study area

This study was conceived as part of a wider research aimed to analyze environmental factors affecting the development of chronic diseases in GraMo, an adult cohort set up in the province of Granada, Southern Spain (Fig. 1).

Granada Province, in the South-West of Spain, includes rural, semi-rural and urban zones, with a population of over 915,000 inhabitants within an area of 12,531 km2. Landscape and soil exhibit strong variations between the Mediterranean coast, the interior valleys and the

Adipose tissue concentrations of individual pollutants and their mixtures in the study population

Adipose tissue concentrations of the selected contaminants are listed in Table 2. Among the metal(loid)s, the highest median concentrations corresponded to Al (10100 ng/g adipose tissue), followed by Ni, Cr and Pb. As, Co and Cd were found in the lowest median concentrations (<10 ng/g adipose tissue). PCB-153 and PCB-180 were the POPs found in the highest median concentrations (>180 ng/g lipid), whereas α-HCH, β-HCH and dicofol accounted for the lowest (<10 ng/g lipid). The distribution of

Conclusion

The present study offers novel insights on the distribution of clusters of PTSs in adipose tissue of a widely characterized population from Southern Spain, and the influence of lifetime residence and occupation on them. These analyses will help further elucidation of the long-term potential health effects of these chemicals, as it is currently being performed in GraMo cohort.

Credit author statement

Ruth Echeverría: Software, Formal analysis, Visualization, Writing – original draft, Writing – review & editing, Petra Vrhovnik: Resources, Writing – review & editing, Inmaculada Salcedo-Bellido: Writing – review & editing, Francisco M. Pérez-Carrascosa: Data curation, Celia Gómez-Peña: Writing – review & editing, Željka Fiket: Resources, Writing – review & editing, Piedad Martín-Olmedo: Writing – review & editing, Nicolás Olea: Writing – review & editing, Mariana F. Fernández: Writing – review

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 research would have not been possible without the collaboration of the participants in GraMo cohort. This article will be part of the Ph.D. thesis of Ruth Echeverría in the context of the “Clinical Medicine and Public Health Program” of the University of Granada.

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