Dietary and Household Sources of Prenatal Exposure to

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Dietary and household sources of prenatal exposure to polybrominated diphenyl ethers (PBDEs) in the INMA birth cohort (Spain) Olga Costa, Maria Jose Lopez-Espinosa, Esther Vizcaino , Mario Murcia, Carmen Iñiguez, Eva María Navarrete-Muñoz, Joan O. Grimalt, Adonina Tardon, Ferran Ballester, and Ana Fernandez-Somoano Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b06263 • Publication Date (Web): 28 Apr 2016 Downloaded from http://pubs.acs.org on May 3, 2016

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Environmental Science & Technology

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Dietary and household sources of prenatal exposure to polybrominated diphenyl

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ethers (PBDEs) in the INMA birth cohort (Spain)

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Olga Costaa, Maria-Jose Lopez-Espinosaa,b*, Esther Vizcainoc,d, Mario Murciab,a,

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Carmen Iñigueza,b, Eva M. Navarrete-Muñozb,e, Joan O. Grimaltd, Adonina Tardonc,b,

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Ferran Ballestera,b, Ana Fernandez-Somoanoc,b

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a

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Jaume I–Universitat de València, Avenida de Catalunya 21, 46020 Valencia, Spain

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b

Epidemiology and Environmental Health Joint Research Unit, FISABIO–Universitat

Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP),

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Calle Monforte de Lemos 3-5, 28029 Madrid, Spain.

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c

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del Cristo s/n, 33006 Oviedo, Asturias, Spain.

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d

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Water Research (IDÆA-CSIC), Jordi Girona 18, 08034 Barcelona, Spain.

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e

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Juan de Alicante, 03550 Alicante, Spain.

Department of Preventive Medicine and Public Health, University of Oviedo, Campus

Department of Environmental Chemistry, Institute of Environmental Assessment and

Department of Public Health, Miguel Hernandez University, Ctra. Nacional 332, San

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Corresponding author: *Maria-Jose Lopez-Espinosa

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Foundation for the Promotion of Health and Biomedical Research in the Valencian

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Region, FISABIO-Public Health, Valencia, Spain, Avda Catalunya 21, 46020 Valencia,

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Spain. E-mail: [email protected]; Phone: (+34) 961925941.

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Conflict of interest: The authors declare no competing financial interest.

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Word count: 7631

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Full text: 4931

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Tables and figures: 2700

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Abstract

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This study looked at predictors of exposure to polybrominated diphenyl ethers (PBDEs)

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with a focus on dietary and household-level factors. Concentrations of BDE-47, -99,

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-153, and -209 and their sum (∑PBDEs) were measured in cord serum. Spanish women

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(n=541) completed two semi-quantitative food frequency questionnaires during the first

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and third trimesters of pregnancy. The daily mean intake (grams) of eggs, dairy

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products, meat, cereals and pasta, vegetables and pulses, fruits, shellfish and

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cephalopods, and fish, and the weekly mean intake (servings) of lean, large oily, other

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oily, and other fish from both questionnaires were averaged. Information on house size,

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curtains and carpets at home, mattress type, housekeeping frequency, and television use

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was also collected later in gestation. Multivariate censored regression was used to assess

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the association between PBDE concentration (log2 transformed) and potential

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predictors. BDE-47, -99, -209 and ∑PBDE concentrations increased by 13.6%(95%

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CI:0.0, 29.0%), 21.1%(2.3, 43.5%), 21.7%(0.4, 47.5%) and 11.5%(2.2, 21.7%),

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respectively, per interquartile range increment in daily intake of shellfish and

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cephalopods. Fish intake was associated with BDE-99 (20.8%[1.7, 43.4%]). When fish

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was disaggregated by types, BDE-99 and ∑PBDEs increased by 13.8%(4.0, 24.7%) and

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5.7%(0.8, 10.8%), respectively, per 1-serving/week increment in large oily fish intake.

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BDE-153 was associated with higher housekeeping frequency (35.9%[0.4, 83.9%]) and

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BDE-209 with foam mattress use (48.9%[5.8, 109.7%]). In conclusion, seafood

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consumption, higher housekeeping frequency, and foam mattress were associated with

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prenatal PBDE exposure.

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Key words: Cord, diet, fish, household sources, PBDEs, prenatal exposure.

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TOC Art:

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INTRODUCTION

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Polybrominated diphenyl ethers (PBDEs) are synthetic chemicals commonly used to

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reduce flammability in many types of commercial and household products, such as

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plastics, electronics, furniture, textiles, and construction materials.(1) The use and

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production of DecaBDE has been phased out in the US and restricted in Europe, but it is

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still produced in other parts of the world.(2,

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mixtures have been banned in many parts of the world(4, 5) and they were added to the

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list of persistent organic pollutants under the Stockholm Convention in 2009.(6) PBDEs

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are not chemically bound to the products that contain them, which makes these

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contaminants more likely to leach out from the goods into house dust, which is

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unintentionally inhaled and ingested.(1) Hence, household dust may make a considerable

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contribution to human PBDE body burden.(7-9)

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Nowadays, the in-use reservoirs of PBDEs, such as electronics, plastics, or household

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furnishing, are considerable. In addition, disposal reservoirs of goods containing PBDEs

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(e.g., landfills, sewage and hazardous waste treatment plants, and e-waste recycling

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facilities) may also be important for the dispersal of PBDEs and their incorporation and

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biomagnification along the aquatic food chain.(10) Therefore, another important source

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of PBDE exposure for non-occupationally exposed populations is diet,(7, 8) since these

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chemicals are persistent, lipophilic, accumulate in organisms, and biomagnify along the

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food chain.(11) Studies of PBDE concentrations in foodstuffs have highlighted seafood

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in Asia and Europe and meat and meat products in the US as the main contributors to

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daily food intake of these contaminants.(7, 8)

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PBDEs have been detected in the blood of pregnant women and children(12-14) and

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concerns have recently emerged, given their endocrine-disrupting properties.(15) In

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humans, the fetal period is one of the stages of greatest vulnerability to PBDE exposure,

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The PentaBDE and OctaBDE technical


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since even low levels of synthetic compounds could produce irreversible and irreparable

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damage.(15) While few human studies on the possible effects of PBDE exposure on fetal

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development have been published to date, recent evidence suggests that prenatal

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exposure to these compounds could be associated with disturbed hormone levels during

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pregnancy,(16) fetal growth,(17) and neurodevelopment in infants and toddlers.(18, 19) It is

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thus essential to identify and describe sources of prenatal exposure to PBDEs. To date,

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sociodemographic predictors of the body burden of these compounds have been studied

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quite extensively,(20-25) but data on food intake and indoor exposure are scarce.(26, 27) The

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present study aimed to look at predictors of cord serum concentrations of four PBDEs

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(BDE-47, -99, -153, and -209) and their sum (∑PBDEs) with a focus on dietary and

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household-level factors.

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EXPERIMENTAL SECTION

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Study design

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Population-based birth cohorts were established in several areas of Spain as part of the

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INMA Project.(28) The population in the present study consisted of pregnant women

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who agreed to participate in the INMA cohorts of Asturias and Valencia, which are the

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only two INMA cohorts with PBDEs measured in cord serum. The Asturias cohort is

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located in northern Spain on the shores of the “Cantabrian Sea” (in the Atlantic Ocean)

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and the Valencia cohort is located in eastern Spain on the Mediterranean coast.

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A total of 1,349 eligible women (age ≥ 16 years, singleton pregnancy, enrollment at 10–

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13 weeks of gestation, no assisted conception, delivery scheduled at the reference

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hospital, and no communication handicap) agreed to participate (recruitment period:

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2003-2007). The participation rates were 45% and 54% in the Asturias and Valencia

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cohorts, respectively. Excluding the women who withdrew from the study, were lost to

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follow-up, or with induced or spontaneous abortions or fetal deaths, 1,272 (94%)


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women were followed up to delivery (2004-2008). Cord blood samples were collected

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from 853 (67%) of these participants. A total of 541 cord serum samples (around 99%

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[n=322] and 42% [n=219] from the Asturias and Valencia cohorts, respectively) were

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available for PBDE determinations and were included in this study. In Valencia, the

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lower proportion of existing samples for PBDE determinations was due to logistic

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reasons, since only a sub-sample of all the initially collected cord blood samples were

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available for the determination of these contaminants.

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All the mothers gave their written informed consent prior to inclusion. The Ethics

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Committees of the San Agustin Hospital in Aviles (Asturias) and La Fe Hospital in

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Valencia approved the research protocol.

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Serum collection

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Cord blood was collected at birth by trained midwives following the same protocol in

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both birth cohorts.(28) Briefly, venous cord blood (volume: 5 mL) was collected with a

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glass syringe in the delivery room within 10 minutes after placental delivery. Part of the

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collected samples were placed in Vacutainer blood collection tubes and stored in the

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dark at 4ºC (1-2 hours from the extraction) until centrifugation for 15 minutes at 2500-

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3000 rpm. The serum obtained was aliquoted in 2 mL glass criyotubes and

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anonymously stored at -80°C.

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Analysis of PBDEs

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The analytical methods and quality control procedures employed in the laboratory have

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been described elsewhere.(29) Briefly, 1 mL of serum was spiked with the surrogate

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standards tetrabromobenzene (TBB) and decachlorobiphenyl (PCB 209) and vortex

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stirred for 30 s at 2,000 rpm. n-Hexane (3 mL) was added, followed by concentrated

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sulfuric acid (2 mL). After reacting, the mixture was stirred for 30 s and the supernatant

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n-hexane phase was separated by centrifugation. The remaining sulfuric acid solution


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was re-extracted twice with 2 mL of n-hexane (each by 30 s of stirring and

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centrifugation). The combined n-hexane extracts (7 mL) were additionally cleaned with

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sulfuric acid (2 mL, stirring for 30 s). Then, the n-hexane phase was separated by

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centrifugation and reduced to a small volume under a gentle nitrogen stream. The

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extract was transferred to gas chromatography (GC) vials using four 25 µL isooctane

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rinses. PCB 142, BDE-118 (20 µl) and [13C]-BDE-209 (10 µL) were added as internal

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standards before injection. BDE congeners were analyzed by GC coupled to mass

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spectrometry in chemical ionization and negative ion recording.

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A total of 14 PBDEs were analyzed. BDE-17, BDE-66, BDE-71, BDE-85 BDE-138 and

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BDE-190 were detected in limit of detection [LOD]) are also explored since available data on

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dietary and household-level factors of pre- or postnatal BDE-209 exposure are scarce.

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In addition, this congener is still in use in some parts of the world, including Europe,(3)

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and, consequently, concentrations in human bodies are very likely to increase. LODs

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were calculated as three times the standard deviation (SD) of the procedural blank

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levels. The LODs for BDE-47, -99, -153, and -209 were 2.59, 2.38, 1.24, and 9.12

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pg/mL in Asturias, and 2.30, 2.10, 1.19, and 5.94 pg/mL in Valencia. Samples were

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analyzed in two different batches, one per cohort, and therefore LODs were somewhat

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different for each cohort. The laboratory is in compliance with the Arctic Monitoring

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and Assessment Program (AMAP) for persistent organic pollutants in human serum

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(Centre de Toxicologie, Institut National de Sante Publique du Quebec). The same


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samples from the AMAP were analyzed in the two different batches to ensure

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comparable results and concentrations were always within 20% of the consensus values.

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Enzymatic techniques were used to determine total cholesterol and triglycerides, and

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total serum lipid concentrations were calculated from these measurements.(30)

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Dietary and household sources of exposure

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Two semi-quantitative food frequency questionnaires (FFQs) were administered by

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trained interviewers in two different interviews: the first one (10−13 weeks) collected

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information from the last menstrual period to the end of the first trimester, and the

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second FFQ (28−32 weeks) covered the period since the first FFQ was administered.

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The 101-item FFQ was an adapted version of Willett’s questionnaire,(31) developed and

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validated for use among adults living in Spain(32) and later in pregnant Mediterranean

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women, with satisfactory coefficients for validity and reproducibility.(33) Participants

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were asked how often, on average, they had consumed each item type over the past 3−4

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months (with nine possible responses ranging from “never or less than once a month” to

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“six or more per day”). Their responses were transformed to average daily intake in

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grams for each food item using standard units or serving sizes specified in the FFQ.

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Each food group (eggs, dairy products, meat, cereals and pasta, vegetables and pulses,

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fruits, shellfish and cephalopods, and fish) was obtained by summing the daily intake of

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individual items included in the group. The fish group was disaggregated into lean fish,

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large oily fish, other oily fish, and other fish. The items included in these groups are

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described in the Supporting Information (Table S1). In addition, the total energy intake

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was primarily obtained from food composition tables of the US Department of

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Agriculture(34) and other tables published for Spanish foods.(35)

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In the present study, the mean of the two FFQs for each item was used as an estimation

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of daily average intake of each food item. For statistical analysis, the intake of food


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groups was expressed in daily grams, and the intakes of specific fish groups were

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expressed in weekly servings.

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Questions that may be related with PBDE exposure were also selected from a

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questionnaire administered at gestational weeks 28−32 on sociodemographic and

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lifestyle variables(1): house size (m2), curtains at home (yes and no), carpets at home

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(yes and no), type of mattress (foam: mattress with one or more types of foam

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[polyurethane, viscoelastic, and latex, among others] as the support system, and

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innerspring: mattress with a steel coil support system covered by padding or upholstery

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materials, which can include various foams, fiber, and additional layers of smaller steel

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springs), housekeeping frequency (≤ or >1 times/week, including sweeping, vacuuming

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dusting, and mopping), and television use (hours/week). Questions on household-level

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factors of PBDE exposure were only requested later in gestation and referred to the

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whole pregnancy.

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Covariates

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The pregnant women completed two detailed in-person questionnaires (weeks 10−13,

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and 28−32) on anthropometric, sociodemographic and lifestyle information. The

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maternal variables considered to be included in the models were: age (years), pre-

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pregnancy body mass index (BMI, kg/m2), country of origin (Spain and other), zone of

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residence (rural and non-rural), working at week 12 of pregnancy (yes and no), parity

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(primiparous and multiparous), previous lactation (none, and < or ≥6 months, since

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lactation is a mechanism for the excretion of PBDEs(36)), education (until primary,

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secondary, and university studies), social class (Class I: managerial jobs, senior

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technical staff, and commercial managers, Class II: skilled non-manual workers, Class

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III: manual workers) defined according to the most privileged occupation of the mother

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or the father during pregnancy using a widely used Spanish adaptation of the


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international ISCO88 coding system,(37) smoking at week 12 of pregnancy (yes and no),

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passive smoking (yes and no) in at least two environments from among the home,

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workplace and leisure areas/restaurants, alcohol intake at week 12 of pregnancy (yes

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and no), and season of the last menstrual period.

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Data analyses

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For descriptive purposes, a number (percentage) is presented for categorical variables,

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and mean and SD are given for continuous variables. Differences between the two

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cohorts were explored by Chi square, t-Student, or Mann-Whitney tests, while logistic

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regression models adjusted by cohort were used to explore the differences in study

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variables between the excluded and included women. Percentage above LOD, geometric

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mean (GM), geometric SD (GSD), median and percentiles (P) 25, 75 and 95 of PBDEs

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are presented. Contaminant concentrations are expressed in pg/mL or ng/g lipid, the

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latter dividing serum residue concentrations by total serum lipid levels. Missing values

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of lipids (n=48) were imputed at random based on a normal probability distribution

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using the mean and the SD of the lipids as parameters. Censored linear regression

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models were used to estimate the GM and GSD of the PBDEs and to explore the

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differences in contaminant concentrations between cohorts.

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For statistical purposes, censored linear regression models were also performed to study

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the association between PBDEs (after log2-transformation [log2(PBDE)] to account for

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right-skewed distributions) and sources of exposure. When there are values below LOD

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in the dependent variable, censored models provide maximum likelihood estimates of

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the coefficients.(38) A two-step procedure was used for model building. First, covariates

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associated with each PBDE at the p-value

Dietary and Household Sources of Prenatal Exposure to

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