Elsevier

Science of The Total Environment

Volume 634, 1 September 2018, Pages 235-242
Science of The Total Environment

Differential contribution of animal and vegetable food items on persistent organic pollutant serum concentrations in Spanish adults. Data from BIOAMBIENT.ES project

https://doi.org/10.1016/j.scitotenv.2018.03.283Get rights and content

Highlights

  • We studied the effect of diet on 26 POP serum levels in Spanish adult population.

  • Animal-based food had a 2.1–4.0× stronger effect on most POPs than plant-based food.

  • Fish was the main animal-based contributor to OCPs, PCBs, PFOS, and PFDA.

  • Cold meat was the main animal-based contributor to PFOA and PFHxS.

  • Fruits and vegetables were the main plant-based contributors to PCBs and OCPs.

Abstract

Diet is considered the main source of Persistent Organic Pollutant (POP) exposure in the general population, although there are still several gaps of knowledge regarding the differential contribution of main food groups. The aim of this study was to identify dietary patterns that contribute to human exposure to organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and Perfluoroalkyl Substances (PFASs).

Study population (n = 1880, 18–65 years old) was recruited during 2009–2010 in all the main geographical areas of Spain. For this work, exposure was estimated by chemical analyses of serum levels of 6 PCBs (n = 1880), 13 OCPs (n = 934), and 6 (PFASs) in a subsample of 755 (n = 755). Dietary habits and covariates were gathered via self-administered questionnaires. Data analyses were performed by means of multivariable linear regression and weighted quantile sum regression.

Both the consumption of animal-based and plant-based food were positively associated with the individual concentrations of p,p´-DDE, hexachlorobenzene, and PCB-congeners −138, −153, and  180. The contribution of animal-based products was 2.1–4.0× stronger except in p,p´-DDE, to which both patterns had similar contributions. In PFASs only animal food was positively associated with the exposure levels. The main animal-based contributors to PCB exposure were fish (49–64%) and eggs (19–36%), while OCP concentrations were mainly influenced by dairy products (32–48%) and fish (47–48%). PFOA and PFHxS were mainly explained by cold-meat (34–37%), fish (25–26%), and eggs (19–21%), while PFOS and PFDA were primarily influenced by fish consumption (44–77%). In the case of plant-based items, fruits (25–82%) and vegetables (18–63%) accounted for the majority of the variability of PCB and OCP concentrations.

Our results highlight the relevance of dietary POP exposure as well as the need for the consideration of nutritional interventions in public health programs aiming to reduce POP exposure in the general population.

Graphical abstract

Dietary predictors of POP serum concentrations in Spanish adults.

Unlabelled Image
  1. Download : Download high-res image (239KB)
  2. Download : Download full-size image

Introduction

Persistent Organic Pollutants (POPs) constitute a heterogeneous group of chemicals (mostly of man-made origin), which are usually highly resistant to degradation, tend to bioaccumulate in living organisms, and have been used throughout 20th and 21st centuries for very diverse purposes (Porta et al., 2002).

Organochlorine pesticides (OCPs), which are among the most well-known POPs, have been used for both agriculture and public health interventions. One of the most studied OCPs is dichlorodiphenyltrichloroethane (DDT), which has been used extensively worldwide in agriculture and for vector control since 1939 (Turusov et al., 2002). p,-Dichlorodiphenyldichloroethylene (p,p´-DDE) is the main metabolite of DDT, and it is still found as predominant OCP in the general population, and it is even more persistent than the parent compound (Ramos et al., 2017). Hexachlorobenzene (HCB), was used as a fungicide, but other sources of exposure include the emission of chemical industry by-products, combustion reactions, wood preservation agents, and metallurgical processes (Barber et al., 2005). Lindane (γ-HCH) has been used both as an insecticide as well as pharmaceutical treatment for lice and scabies (Vijgen et al., 2011). Polychlorinated biphenyls (PCBs) include a wide group of 209 congeners which have been used in multitude of industrial applications, e.g., in thermal insulation or as coolant (ATSDR, 2000). Although banned in Spain since 1986, they are commonly found in the environment, and living organisms, including non-occupationally-exposed populations. Concentrations of three of these congeners, i.e. PCB-138, PCB-153, and PCB-180, are frequently used as biomarkers of the total exposure of PCBs (Huetos et al., 2014).

Since the early 1970s, most countries have banned or severely restricted the production, handling, and disposal of several (although not all) OCPs and PCBs, due to their high persistence in the environment and their proven or suspected adverse effects, including reproductive disorders, teratogenicity, endocrine disruption, immunosuppression, and carcinogenicity (Arrebola et al., 2014; Luo et al., 2017; Porta et al., 2002; Schæbel et al., 2017). Therefore, exposure levels in the general populations have declined over the last decades (Schoeters et al., 2017). However, virtually all humans have detectable levels of some of these chemicals, and there still exist a wide variety in both inter- and intra-population exposure levels (CDC, 2017), indicating that an important part of the exposure might be modifiable.

Perfluoroalkyl Substances (PFASs) are a class of chemicals with both hydrophobic and oleophobic properties which are used in a variety of consumer products and industrial processes, e.g. liquid repellant, industrial surfactants, or firefighting foams (Schultz et al., 2003). Their ubiquity, persistence and bioaccumulation result in their widespread presence in the environment and the general population, as a consequence of direct emissions during manufacturing, use, or disposal of products as well as transformation of other precursors into PFASs (Armitage et al., 2009; CDC, 2017). It has been suggested that human long-term exposure to low doses of PFASs, particularly at critical stages of development, may increase the risk of certain chronic conditions, e.g. metabolic and thyroid disruption, or inmunotoxicity (Corsini et al., 2014; Heindel et al., 2017; Luo et al., 2017), although results are still controversial.

On the other hand, diet (particularly food from animal-origin) is considered the most important contributor of POP body burden in the general population (Darnerud et al., 2006). However, epidemiological studies have reported controversial findings on which specific food items have the highest contribution to POP exposure, probably related to the specific characteristics of each population, including different lifestyle and nutritional habits (Boada et al., 2014).

In 2008, the Spanish Ministry of Agriculture, Food and the Environment promoted a national Human Biomonitoring program (HBM). The purpose of this program was to enhance the current understanding of the distribution of priority environmental pollutants, such as metals, pesticides, flame retardants, perfluorinated compounds, and PCBs, in the Spanish population and to establish reference values (Bartolomé et al., 2015; Cañas et al., 2014; Huetos et al., 2014; López-Herranz et al., 2016; Ramos et al., 2017). In this regard, we designed BIOAMBIENT.ES project, a nationwide cross-sectional study, aimed at obtaining a representative sample of the Spanish occupied population.

The aim of the present study was to identify dietary patterns that contribute to human exposure to OCPs, PCBs, and PFASs in a sample of adults representing all the main Spanish regions.

Section snippets

Study population

BIOAMBIENT.ES is a nationwide cross-sectional epidemiological study with a stratified cluster sampling designed to cover all geographical areas, sex and occupational sectors, and aimed to obtain a representative sample of the Spanish active workforce. The design of the study has been extensively described elsewhere (Pérez-Gómez et al., 2013). In brief, volunteers were consecutively selected among occupationally active population > 16 years, residents in Spain for at least 5 years, which underwent

Results

The main characteristics and serum POP concentrations of the study population have been previously reported and discussed elsewhere (Bartolomé et al., 2017; Huetos et al., 2014; Ramos et al., 2017). However, for explicative purposes, a general description of POP concentrations in the study population is included as supplementary material (Table S1). Frequencies of consumption of different food items are shown in Table 1.

As previously stated, all the analyses using POP concentrations as

Discussion

Our results from this nationwide human biomonitoring survey highlight the relevant contribution of the diet on POP exposure in the Spanish population, particularly of animal-based food items, confirming previous reports (Agudo et al., 2009; Bjermo et al., 2013; Gómara et al., 2005; Llobet et al., 2003; Porta et al., 2012). Nevertheless, we also evidenced a non-negligible role of plant-based foods on the concentrations of certain POPs, which was even slightly stronger in the case of p,p´-DDE.

Acknowledgments

This work was funded as part of a research agreement between the Spanish Ministry of Agriculture and Fisheries, Food and the Environment and the Institute of Health Carlos III (Project N_ SEG 1251/07, 1210/10 and 1321/15). The authors would like to thank M. A. Lucena and the volunteers of BIOAMBIENT.ES and healthcare staff from the Societies for Prevention: IBERMUTUAMUR, MUTUALIA, MC-PREVENCIÓN, MUGATRA, UNIMAT PREVENCIÓN, and PREVIMAC. Dr. J.P. Arrebola is under a research contract funded by

References (59)

  • L.D. Boada et al.

    Consumption of foods of animal origin as determinant of contamination by organochlorine pesticides and polychlorobiphenyls: results from a population-based study in Spain

    Chemosphere

    (2014)
  • A.I. Cañas et al.

    Blood lead levels in a representative sample of the Spanish adult population: the BIOAMBIENT.ES project

    Int. J. Hyg. Environ. Health

    (2014)
  • E. Corsini et al.

    Perfluorinated compounds: emerging POPs with potential immunotoxicity

    Toxicol. Lett.

    (2014)
  • P.O. Darnerud et al.

    Dietary intake estimations of organohalogen contaminants (dioxins, PCB, PBDE and chlorinated pesticides, e.g. DDT) based on Swedish market basket data

    Food Chem. Toxicol.

    (2006)
  • M. Esteban et al.

    Aspectos prácticos de la fase preanalítica del estudio de biovigilancia BIOAMBIENT.ES

    Gac. Sanit.

    (2013)
  • M. Fernández-Rodríguez et al.

    Levels and predictors of persistent organic pollutants in an adult population from four Spanish regions

    Sci. Total Environ.

    (2015)
  • M. Gasull et al.

    The relative influence of diet and serum concentrations of organochlorine compounds on K-ras mutations in exocrine pancreatic cancer

    Chemosphere

    (2010)
  • M. Gasull et al.

    Empirical analyses of the influence of diet on human concentrations of persistent organic pollutants: a systematic review of all studies conducted in Spain

    Environ. Int.

    (2011)
  • J.J. Heindel et al.

    Metabolism disrupting chemicals and metabolic disorders

    Reprod. Toxicol.

    (2017)
  • O. Huetos et al.

    Serum PCB levels in a representative sample of the SPANISH adult population: the BIOAMBIENT.ES project

    Sci. Total Environ.

    (2014)
  • E. Junqué et al.

    Integrated assessment of infant exposure to persistent organic pollutants and mercury via dietary intake in a central western Mediterranean site (Menorca Island)

    Environ. Res.

    (2017)
  • H. Kahleova et al.

    The effect of a vegetarian versus conventional hypocaloric diet on serum concentrations of persistent organic pollutants in patients with type 2 diabetes

    Nutr. Metab. Cardiovasc. Dis.

    (2016)
  • J.M. Llobet et al.

    Levels of polychlorinated biphenyls in foods from Catalonia, Spain: estimated dietary intake

    J. Food Prot.

    (2003)
  • S. Llop et al.

    Concentrations and determinants of organochlorine levels among pregnant women in Eastern Spain

    Sci. Total Environ.

    (2010)
  • D. Luo et al.

    Association of in utero exposure to organochlorine pesticides with thyroid hormone levels in cord blood of newborns

    Environ. Pollut.

    (2017)
  • L. Marushka et al.

    Association between fish consumption, dietary omega-3 fatty acids and persistent organic pollutants intake, and type 2 diabetes in 18 First Nations in Ontario, Canada

    Environ. Res.

    (2017)
  • L.A. Mercado et al.

    Serum concentrations of p,p'-dichlorodiphenyltrichloroethane (p,p'-DDE) in a sample of agricultural workers from Bolivia

    Chemosphere

    (2013)
  • C. Miyashita et al.

    Demographic, behavioral, dietary, and socioeconomic characteristics related to persistent organic pollutants and mercury levels in pregnant women in Japan

    Chemosphere

    (2015)
  • M. Porta et al.

    Grupo de Trabajo sobre Compuestos Tóxicos Persistentes y Salud del IMIM

    Gac. Sanit.

    (2002)
  • Cited by (0)

    1

    BIOAMBIENT.ES: J.L. Aleixandre, N. Aragonés, A.I. Cañas, E. Calvo, M. Cervantes-Amat, M.V. Cortés, G. Díaz, S. Gómez, S. González, O. Huetos, J.A. Jimenez, G. López-Abente, A. López-Herranz, J. Mayor, C.F. Méndez, M.A. Molina, M. Pollán, R. Pastor, C. Rodriguez, M. Rosado, M. Ruiz-Moraga and J. Román.

    View full text