Elsevier

Science of The Total Environment

Volume 441, 15 December 2012, Pages 49-56
Science of The Total Environment

Levels of polychlorinated dibenzo-p-dioxins, dibenzofurans and dioxin-like polychlorinated biphenyls in placentas from the Spanish INMA birth cohort study

https://doi.org/10.1016/j.scitotenv.2012.09.075Get rights and content

Abstract

Because fetuses are considered significantly more sensitive to various environment toxicants, there is a need for continuous biomonitoring of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and dioxin-like polychlorinated biphenyls PCBs (DL-PCBs) to assess their impact on this susceptible population. The aim of this study was to assess the concentration of PCDD/Fs and DL-PCBs in placenta samples from women participating in the Spanish Environment and Childhood (INMA) birth cohort study and to evaluate whether maternal and child characteristics predict placenta concentrations of these pollutants. The presence of PCDD/Fs and DL-PCBs was investigated in 50 placenta samples selected at random in the recruitment period 2000–2008. Multivariable regression models were constructed. Mothers had a mean age at delivery of 30.7 years (18.0–38.0 years), pre-pregnancy BMI of 23.3 kg/m2 (18.0–40.2 kg/m2), and 31% were smokers. Median total concentrations of PCDD/Fs and DL-PCBs were 6.9 pg WHO-TEQ/g lipid and 2.1 pg WHO-TEQ/g lipid, respectively. In comparison to the few previous studies in placenta, total TEQ levels were among the lowest recorded in comparable general populations. The congener distribution pattern and the frequencies and concentrations of PCDD/F and DL-PCB congeners were similar to previous reports in placenta. PCDD/F and DL-PCB exposure was related to the age of the mother and the year of the delivery. Although placental concentrations cannot be considered wholly appropriate predictors for evaluating fetal exposure to these contaminants, they can provide a good indication of both maternal and infant prenatal and postnatal exposure and can be used as a proxy for fetal exposure.

Highlights

► An important human health concern is the influence of PCDD/Fs and PCBs on offspring, stemming from prenatal exposure. ► In comparison to previous studies, total TEQ levels were among the lowest recorded in comparable populations. ► Maternal age and year of the delivery were associated with levels of exposure.

Introduction

Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) are a group of organochlorine, toxic, persistent, lipophilic and bioaccumulative chemicals that undergo a slow metabolism and are eliminated with difficulty in humans (Agency of Research for Cancer, IARC). There are 210 different congeners of dioxins and furans, and humans can be simultaneously exposed to several PCDD/F compounds. From a toxicological point of view, seven 2,3,7,8-subtituted PCDDs and ten 2,3,7,8-subtituted PCDFs are the most toxic congeners, according to the World Health Organization (WHO)-defined total toxic equivalent (TEQ) concept. Among these, 2,3,7,8-tetra-chlorodibenzo-p-dioxin (TCDD) has been classified as a carcinogen (class I) by the IARC (2007).

PCDD/Fs are largely formed as unintentional by-products in numerous chemical processes and almost every combustion process (COM, 2001). The most important route of human exposure to complex mixtures of PCDD/Fs and polychlorinated biphenyls (PCBs) is food consumption, which contributes more than 90% of total exposure (Liem et al., 2000). Fat-containing animal products, especially fish and other seafood, make a major contribution to the dietary intake of PCDD/Fs in Spain (Bocio and Domingo, 2005, Marin et al., 2011) and in other European countries (Windal et al., 2010, Malgorzata et al., 2011). In Spain, the intake of dioxins in the daily diet was estimated to be 3.0 pg I-TEQ/kg of body weight/day, i.e., 210 pg I-TEQ/day for a typical male adult (70 kg body weight) (Fernández et al., 2004). The temporal trend of dioxin intake, well documented in European countries, showed an increase until the 1970s–80s, followed by a gradual decrease (Fernandez et al., 2008).

Experimental animals exposed to these chemicals have evidenced immunological, neurochemical, neurotoxic, carcinogenic and endocrinal changes, among other toxic effects (Geyer et al., 2000). There is growing concern that prenatal PCDD/F and PCB exposure may promote human health disorders that sometimes do not manifest for many years and may even persist for multiple generations (Bruner-Tran and Osteen, 2011). Accumulation of these compounds in fatty tissue during the life of the mother may be a major source of this exposure, both during gestation and via breast-feeding (Schecter et al., 1998, Suzuki et al., 2005, Wang et al., 2004). Trans-placental exposure to high levels of these compounds in children from Yusho (Japan) and Yu-cheng (Taiwan) (Guo et al., 2004) was related to numerous adverse health effects, including: growth retardation in fetuses and infants (Konishi et al., 2009), delayed cognitive development and behavior problems (Guo et al., 2004, Wittsiepe et al., 2008), thyroid deficiency (Pavuk et al., 2003, Wang et al., 2005), reproductive effects (Virtanen et al., 2012) and carcinogenic effects (Demers et al., 2002). PCDD/Fs and PCBs also have the potential to disrupt multiple endocrine pathways and induce toxic responses. Depending on the age at exposure, these disruptive effects may be permanent, especially when exposure occurs during the period in which “programming” of the endocrine system is in progress (Mocarelli et al., 2008).

Over the past decade, data on background PCDD/F levels in different tissues in the human population have been reported in various European countries, especially in maternal blood and breast milk (Kiviranta et al., 2005, Wingfors et al., 2000, Wittsiepe et al., 2008). However, there are very limited data on umbilical cord blood or placenta tissue levels. Because fetuses and infants are considered significantly more sensitive than are adults to multiple environment toxicants, the possibility of adverse effects after exposure during the prenatal period is of particular concern. There is a need for continuous monitoring of human exposure to PCDD/Fs in order to evaluate the health risk associated with this exposure, especially in susceptible populations.

In compliance with the National Implementation Plan of the United Nations Stockholm Convention, the Spanish Ministry of Environment and Rural Affairs funded the Institute of Health Carlos III to carry out a Human Biomonitoring program on Persistent Organic Pollutants (POPs) in the general population, including information on PCDD/F levels in newborns. In order to gather data on this susceptible population, the Institute proposed the analysis of dioxins in the INMA—Infancia y MedioAmbiente (Environment and Childhood) birth cohort study.

The aim of this study was to assess the concentration of PCDD/Fs and DL-PCBs in placentas from Spanish pregnant women participating in the INMA birth cohort and to evaluate whether maternal and child characteristics predict placenta concentrations of these pollutants.

Section snippets

Study population and recruitment

The INMA Project (http://www.proyectoinma.org/) is a population-based birth cohort study conducted in Spain that was recently updated in detail (Guxens et al., 2011). Its main goal is to investigate the role during pregnancy and early childhood of environmental pollutants present in air, water and diet in regard to child growth and development. The study population includes pregnant women and offspring from the general population in each of seven study areas (Fig. 1). Placenta samples were only

Results

Table 1 shows some characteristics of the 50 mothers and their infants. The mean age of mothers at delivery was 30.7 years, and the mean pre-pregnancy BMI was within normal weight status category. Around one third of women were smokers during pregnancy, half of the women were primiparous, and a quarter had university education. The mean birth weight was 3.4 kg, the mean duration of gestation was 40 weeks, and none of the children were small for gestational age (SGA).

Total WHO-TEQ concentrations of

Discussion

The most abundant PCDD/F congeners in the placentas of our cohort were some of those with the longest half lives (1,2,3,6,7,8-HxCDD; 1,2,3,4,6,7,8-HpCDD; 2,3,4,7,8-PCDF and OCDD), in agreement with other reports (Leino et al., 2011, Suzuki et al., 2005, Virtanen et al., 2012, Wang et al., 2004).

Previous studies observed a greater accumulation of 2,3,7,8-TeCDD, 1,2,3,7,8-PeCDD and 2,3,4,7,8-PeCDF congeners in placenta than in cord blood and breast milk from the same subjects; it was argued that

Conclusion

The present results confirm the technical and biological feasibility of using placentas to assess prenatal exposure to PCDD/Fs and DL-PCBs. The pattern, frequencies and concentrations of PCDD/F and DL-PCB congeners found in placenta tissue were similar to those reported in placentas from women in Europe. The data indicated that fetal exposure was dependent on maternal age (greater concentration with higher mother age) and year of the delivery (lower levels in more recently collected samples).

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Acknowledgments

The authors are indebted to all participants, without whom this work would not have been possible. They are also grateful to Richard Davies for the editorial assistance.

Funding: This work was supported by grants from the EU Commission (CONTAMED FP7-ENV-212502), the Spanish Ministry of Environment—Instituto de Salud Carlos III by contract agreement SEG 1251/07 (BOE 34495 and DOCV 6198), the Spanish Ministry of Health (FIS-INMA G03/176; EUS2008-03574 and FIS 09/02647, FIS 11/0610, FIS 11/02591),

References (52)

  • H. Kiviranta et al.

    Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in the general population in Finland

    Chemosphere

    (2005)
  • K. Konishi et al.

    Prenatal exposure to PCDDs/PCDFs and dioxin-like PCBs in relation to birth weight

    Environ Res

    (2009)
  • M.J. Lopez-Espinosa et al.

    Dioxins in adipose tissue of women in Southern Spain

    Chemosphere

    (2008)
  • S. Marin et al.

    Congener profile, occurrence and estimated dietary intake of dioxins and dioxin-like PCBs in foods marketed in the region of Valencia (Spain)

    Chemosphere

    (2011)
  • P. Myllynen et al.

    Human placenta: a human organ for developmental toxicology research and biomonitoring

    Placenta

    (2005)
  • S. Nakano et al.

    Maternal–fetal distribution and transfer of dioxins in pregnant women in Japan, and attempts to reduce maternal transfer with Chlorella (Chlorella pyrenoidosa) supplements

    Chemosphere

    (2005)
  • M. Pavuk et al.

    Serum 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) levels and thyroid function in Air Force veterans of the Vietnam War

    Ann Epidemiol

    (2003)
  • A. Schecter et al.

    Concentrations of polychlorinated dibenzo-p-dioxins and dibenzofurans in human placental and fetal tissues from the U.S. and in placentas from Yu-Cheng exposed mothers

    Chemosphere

    (1996)
  • M. Schuhmacher et al.

    PCDD/F and non-ortho PCB concentrations in adipose tissue of individuals living in the vicinity of a hazardous waste incinerator

    Chemosphere

    (2004)
  • M. Schuhmacher et al.

    Concentrations of PCDD/Fs, PCBs and PBDEs in breast milk of women from Catalonia, Spain: a follow-up study

    Environ Int

    (2009)
  • K. Suominen et al.

    Occurrence of PCDD/F, PCB, PBDE, PFAS, and organotin compounds in fish meal, fish oil and fish feed

    Chemosphere

    (2011)
  • T. Todaka et al.

    Concentrations of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in blood and breast milk collected from 60 mothers in Sapporo City, Japan

    Chemosphere

    (2008)
  • T. Todaka et al.

    Relationship between the concentrations of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and polychlorinated biphenyls in maternal blood and those in breast milk

    Chemosphere

    (2010)
  • K. Tsukimori et al.

    Comparison of the concentrations of polychlorinated biphenyls and dioxins in mothers affected by the Yusho incident and their children

    Chemosphere

    (2011)
  • S.L. Wang et al.

    Infant exposure to polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs)—correlation between prenatal and postnatal exposure

    Chemosphere

    (2004)
  • I. Windal et al.

    Dietary intake of PCDD/Fs and dioxin-like PCBs of the Belgian population

    Chemosphere

    (2010)
  • Cited by (13)

    • Fatty acids, polychlorinated dibenzo-p-dioxins and dibenzofurans, and dioxin-like polychlorinated biphenyls in paired muscle and skin from fish from the Bohai coast, China: Benefits and risks associated with fish consumption

      2018, Science of the Total Environment
      Citation Excerpt :

      Pearson correlations were assessed to identify relationships between the lipid, fatty acid, and pollutant concentrations in the muscle and skin. Each concentration below the limit of detection was replaced with a value of half of the detection limit before statistical analyses were performed (Champoux et al., 2017; Fernandez et al., 2012; Ministry of Ecology and Environment of the People's Republic of China, 2009). The concentrations of different fatty acids, including four nutritionally important PUFAs (LIN (linoleic acid), ALA (18:3 alpha-linolenic acid), EPA, and DHA), saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), and PUFAs (including n-6 and n-3 family acids) in the muscle and skin samples from 13 fish and one squid species are shown in Table 1.

    • Placental transfer of persistent organic pollutants and feasibility using the placenta as a non-invasive biomonitoring matrix

      2018, Science of the Total Environment
      Citation Excerpt :

      Prenatal exposure to POPs is a crucial health issue because the fetus is more vulnerable and has lower metabolic and immune capabilities to these contaminants than do adults (Barr et al., 2007; Tan et al., 2009; Wu et al., 2010; Vizcaino et al., 2014). Previous studies have reported that in utero exposure to POPs is associated with growth retardation, behavioral problems, and thyroid deficiency (Guo et al., 2004; Konishi et al., 2009; Fernandez et al., 2012; Kim et al., 2015a, 2015b, 2015c, 2015d). Based on this evidence, many countries have conducted biomonitoring programs of POPs using mother-fetus paired matrices such as maternal and cord blood, to understand the associations between maternal exposure to POPs and the health outcomes of newborn infants (Frederiksen et al., 2010; Foster et al., 2011; Choi et al., 2014; Kim et al., 2015c).

    • State of the art on public risk assessment of combined human exposure to multiple chemical contaminants

      2016, Trends in Food Science and Technology
      Citation Excerpt :

      CYP3A is known to be involved in chemical degradation reactions in vertebrates (Spurgeon et al., 2010). It has also been related with the transfer of dioxins from the placenta because is affected by the affinity of dioxins for the aryl hydrocarbon (Ah) receptors present in placental tissue, as well for the binding to cytochrome P450 1A2 (CYP1A2) protein (Fernandez et al., 2012). Metabolomics has emerged as a tool to explore and compare the metabolite profiles of the GI tract under different host conditions and perturbations due to the broad variety of metabolites that could be formed (Martin, Collino, Rezzi, & Kochhar, 2012).

    • Organophosphate ester flame retardants and plasticizers in human placenta in Eastern China

      2016, Science of the Total Environment
      Citation Excerpt :

      Prenatal exposure to xenobiotics may lead to adverse effects on fetuses, which are especially vulnerable due to their small size, their rapid growth and development in utero, and their limited ability to detoxify harmful substances (Eskenazi et al., 1999). Many studies have focused on the maternal body burden and prenatal exposure of fetuses to different types of pollutants, such as polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) (Chan et al., 2007; Fernandez et al., 2012), polychlorinated biphenyls (PCBs) and PBDEs (Fernandez et al., 2012; Ma et al., 2012), persistent organochlorine compounds (Bergonzi et al., 2011). However, to date, there have been no studies on fetal exposure to OPEs.

    View all citing articles on Scopus
    View full text