Science of the Total Environment 472 (2014) 496–501

Contents lists available at ScienceDirect

Science of the Total Environment

j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv

Concentrations of persistent organic pollutants (POPs) in human bloodsamples from Mexico City, Mexico

Sandra Orta-García a,b,e, Francisco Pérez-Vázquez a,b, Carolina González-Vega a,b, José Antonio Varela-Silva a,b,Lidia Hernández-González d, Iván Pérez-Maldonado a,b,c,⁎a Laboratorio de Toxicología Molecular, Centro de Investigación Aplicada en Ambiente y Salud (CIAAS), Coordinación para la Innovación y Aplicación de la Ciencia y la Tecnología (CIACYT),Universidad Autónoma de San Luis Potosí, Mexicob Facultad de Medicina, Universidad Autónoma de San Luis Potosí, San Luis Potosí, Mexicoc Facultad de Enfermería, Universidad Autónoma de Zacatecas, Mexicod Centro de Innovación Aplicada en Tecnologías Competitivas (CIATEC), León, Guanajuato, Mexicoe Unidad Académica Multidisciplinaria Zona Media, Universidad Autónoma de San Luis Potosí, Rioverde, San Luis Potosí, Mexico

H I G H L I G H T S

• Serum PBDE, PCB, p,p′-DDT and p,p′-DDE levels were assessed in the blood of people living in Mexico City.• The total PBDE levels in the blood ranged from non-detectable to 350 ng/g lipid.• The mean total PCB level in the blood of the participants in the study was 32.0 ng/g lipid ± 1.3 ng/g lipid.• The mean blood level of total DDT (sum of p,p′-DDT and p,p′-DDE) was approximately 11.5 ± 4.5 ng/g lipid.

⁎ Corresponding author at: Avenida Sierra Leona NoSección, San Luis Potosí 78210, SLP, Mexico. Tel.: +528268460.

E-mail address: ivan.perez@uaslp.mx (I. Pérez-Maldon

0048-9697/$ – see front matter © 2013 Elsevier B.V. All rihttp://dx.doi.org/10.1016/j.scitotenv.2013.11.059

a b s t r a c t

a r t i c l e i n f o

Article history:Received 9 September 2013Received in revised form 31 October 2013Accepted 12 November 2013Available online 1 December 2013

Keywords:BiomonitoringMexicop,p′-DDEPBDEsPCBsPOPs

Studies inMexico have demonstrated exposure to persistent organic pollutants (POPs) in people living in differ-ent sites through the country. However, studies evaluating exposure to POPs in people living inMexico City (oneof most contaminated places in the world) are scarce. Therefore, the aim of this study was to assess the levels ofpolybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane(DDT) and itsmetabolite dichlorodiphenyldichloroethylene (DDE) in the blood as exposure biomarkers in peopleliving inMexico City. A total of 123 participants (blood donors aged 20–60 years) were recruited during 2010 inMexico City. Quantitative analyses of blood samples were performed using gas chromatography coupled withmass spectrometry. Levels of the assessed compounds ranged from non-detectable (bLOD) to 350 ng/g lipid;from 8.20 to 91.0 ng/g lipid and from bLOD to 34.0 ng/g lipid for total PBDEs, total PCBs and total DDT, respec-tively. The current study indicates POP exposure in the people assessed and highlights the need for furtherbiomonitoring studies of these POPs in the region. In this regard, biomonitoring of toxins on a global scale maybe the first step towards the prevention of toxin-induced illnesses in the population.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Persistent organic pollutants (POPs) are substances that persist inthe environment, bioaccumulate in the food web, and pose a risk ofcausing adverse effects to human health and the environment (UNEP,2011). POPs are widespread, and as a result of transport mechanismsfrom the site of use, they have been detected even in remote locations(e.g. the Arctic region; Valera et al., 2013; Bjerregaard et al., 2013; deWit et al., 2006; Hung et al., 2005). POPs include chemicals such as

. 550, Colonia Lomas Segunda444 8262300; fax: +52 444

ado).

ghts reserved.

dioxins/furans, polychlorinated biphenyls (PCBs), chlorinated pesti-cides such as dichlorodiphenyltrichloroethane (DDT) and its metabo-lites, brominated flame retardants (such as polybrominated diphenylethers), and perfluorinated compounds, among others (UNEP, 2011).Recently, three subfamilies of compounds included in the POP familyhave gained increased interest in Mexico: polybrominated diphenylethers (PBDEs), PCBs and DDT and its metabolites.

PBDEs are used as flame retardants in awide range of products, suchas textiles, automotive parts, construction materials, printed circuitboards, televisions, computer housings and other household electronicequipment. In general, they are applied as an additive (not chemicallybound to the material), therefore, they are able to leak out of productsinto the environment (Costa et al., 2008). PCBs are a family of lipophiliccompounds once used extensively in industry, particularly as heat

497S. Orta-García et al. / Science of the Total Environment 472 (2014) 496–501

transfer chemicals in electric transformers and capacitors, as well ashydraulic fluids and lubricants in heavy electrical equipment (ATSDR,2000). In addition, DDT [1,1,1-trichloro-2,2-di(4-chlorophenyl)ethane]was the most widely used organochlorine pesticide in the world. It isconsidered a pollutant with high persistence due to its half-life of upto 15 years in the environment (ATSDR, 2002; Turusov et al., 2002).

In Mexico, sources of POPs exist in various contaminated areas, suchas those associatedwithmining, agriculture,major industry, small-scaleindustry, oil fields, and non-controlled waste disposal sites (Trejo-Acevedo et al., 2009). Moreover, studies in these hot spots haveshown that the populations living in these areas are exposed to POPs(Domínguez-Cortinas et al., 2013; Martínez-Salinas et al., 2011;Martínez-Salinas et al., 2012; Orta-Garcia et al., 2012; Perez-Maldonado et al., 2010; Trejo-Acevedo et al., 2012a,b). In this regard,studies evaluating POP exposure in people living in Mexico City (oneof most contaminated places in the world) are scarce (Rodríguez-Dozal et al., 2012). Moreover, studies that assessed PBDE exposure inpeople living in Mexico City have not been performed.

Taking these data into account, it is important to evaluate the expo-sure levels to different POPs in people living in developing countriessuch as Mexico. Therefore, the aim of this study was to assess the levelsof PBDEs, PCBs, DDT and DDE in the blood of people living in MexicoCity.

2. Materials and methods

2.1. Population

A total of 123 participants (blood donors aged 20–60 years) wererecruited during 2010 in Mexico City (Fig. 1). The volunteers wereselected randomly from a regional hospital where they received treat-ment and were invited to participate in this study. Eligible participantswere 18 years or older, smokers were excluded, participants wereexcluded if they were using drugs and none of the participants hadbeen occupationally exposed to PBDEs or involved in the manufactureof PBDE commercial products. Blood samples were collected in theclinical laboratory of theGeneral Hospital inMexico City (blood samplesremaining after clinical analyses were obtained for POP analyses). Afterinformed consent agreements were signed, a short questionnaire wascirculated and blood samples were taken. Blood samples were drawnfrom the cubital vein into 10 mL vacuum tubes. The tubes containingblood were centrifuged at 3000 rpm for 10 min. The serum was thentransferred using hexane-rinsed Pasteur pipettes into hexane-rinsedbrown glass bottles. Serum was stored at −20 °C until analysis. Thequestionnaire registered characteristics such as source of drinkingwater, occupational history of parents, age, weight, height, and number

Mexico City

Fig. 1. Location of community studied.

of seafood meals per week, exposure to medicaments, environmentaltobacco smoke exposure and infectious diseases in the last month. Thestudywas approved by the ethical committee of the School of Medicine,Universidad Autonoma de San Luis Potosi.

2.2. PBDE analyses

All PBDE analyses of serum samples were performed according toPerez-Maldonado et al. (2009). In brief, the serum samples (2 mL)were denatured with 6 M hydrochloric acid (1 mL) and 2-propanol(6 mL) with mixing between each addition and extracted with n-hexane/methyl-tert-butyl ether (6 mL, 1:1 by volume). The organiclayer was isolated and thewater phase re-extractedwith additional sol-vent. The organic phase was washed with potassium chloride in water(1%). The solvent was evaporated and the lipid content gravimetricallydetermined for each sample. Co-extracted lipids were removed usinga silica/silica:sulfuric acid column packed in a 3-mL solid phase extrac-tion cartridge.We performed final analytical determination of the targetanalytes using gas chromatography (GC-HP6890) coupled with a massspectrometer (MS-HP5973). A DB-5HT column, 15 m × 0.25 mm ID,0.10-μm film thickness was used (J&W Scientific, Bellefonte, PA, USA).Column temperatures were: initial, 80 °C (1 min), and final, 300 °C(rates: 10 °C/min up to 270 °C and 30.0 °C/min up to 300 °C). Injectortemperature was 250 °C operated in pulsed splitless mode. Heliumwas used as the carrier gas at a linear velocity of 1.0 mL/min. Themass spectrometer was operated in Selective Ion Mode (SIM). Weused BDE 77 (2 ng/mL) as an internal standard. Under these conditionsand using the data of nine replicates near the lowest concentrationattainable at the calibration curve, the method detection limits for allPBDEs assessed were approximately 0.10 ng/mL. Internal controls at2.0 ng/mL, 4.0 ng/mL and 6.0 ng/mL for all compounds were includedin all the analyses series. At these concentrations the between-assayvariation coefficient was 3.0% (±2.0%) and average recovery for allcompounds was between 93% and 118%. For quality control, organiccontaminants in fortified human serum [National Institute of Standardsand Technology (NIST) SRM1958]were used; the average recoverywas95 ± 5% for all compounds tested. The results on lipid-weight basiswere calculated as reported previously (Bergonzi et al., 2009).

2.3. DDT, DDE and PCB analyses

The quantification of DDT, DDE and PCBswas performed as reportedby Trejo-Acevedo et al. (2009)., p,p′-DDE, p,p′-DDT and fourteen PCBcongeners (International Union for Pure and Applied Chemistry Nos.28, 52, 99, 101, 105, 118, 128, 138, 153, 156, 170, 180, 183, and 187)were quantified. Briefly, a 2 mL aliquot of serum was first extractedwith a mixture of ammonium sulfate/ethanol/hexane (1:1:3), and theextract was then concentrated and cleaned up on Florisil columns.Quantitative analyses were performed using gas chromatography(GC-HP6890) coupled with a mass spectrometer (MS-HP5973). AHP5-MS column, 60 m × 0.25 mm ID, 0.25-μm film thickness wasused (J&W Scientific, Bellefonte, PA, USA). Column temperatureswere: initial, 100 °C (2 min), and final, 310 °C (rates: 20 °C/min upto 200 °C, 10.0 °C/min up to 245 °C, 4.0 °C/min up to 280 °C and30 °C/min up to 310 °C). Injector temperature was 270 °C operated inpulsed splitless mode. Helium was used as the carrier gas at a linearvelocity of 1.0 mL/min. The mass spectrometer was operated in Selec-tive Ion Mode (SIM). α-Hexachlorocyclohexane-C13, endrin-C13 andPCB-141-C13 were added as internal standards to all samples. Underthese conditions and using the data fromnine replicates near the lowestconcentration attainable on the calibration curve, themethod detectionlimits for the pesticides and PCBs were both approximately 0.30 ng/mL.Internal controls at 0.5 ng/mL, 1.0 ng/mL, 5.0 ng/mL and 10.0 ng/mL forall compoundswere included in all the analyses series. At these concen-trations the between-assay variation coefficient was 4.5% (±2.0%) andaverage recovery for all compounds was between 85% and 115%. For

Table 2PBDEs concentration in serum blood of people living in Mexico City (ng/g lipid).

Congenerabbreviationa

Meanb SDc PC25d PC50 PC75 PC95 Mine Maxf

Total lipids(g/L)

5.90 1.90 2.90 4.80 6.90 8.60 2.30 9.50

BDE 47 1.40g 0.31 0.85 1.00 1.30 29.0 bLOD 32.0BDE 99 3.00 0.32 1.10 2.50 6.10 15.0 bLOD 17.0BDE 100 3.50 0.40 1.00 3.10 7.90 19.0 bLOD 23.0BDE 153 2.40 2.30 0.90 1.70 48.0 75.0 bLOD 150BDE 154 5.00 3.90 1.00 3.50 51.0 72.0 bLOD 130Total PBDEs 15.3 6.70 4.30 13.5 74.0 140 bLOD 350

Blood concentrations are shown in ng/g lipid.The method detection limits (MDL) for all PBDEs were approximately 0.10 ng/mL.

a Compounds were named following the newly proposed nomenclature presented byBergman et al. (2012).

b Values are geometric means.c Standard deviation (SD).d Percentile (PC).e Minimum (Min).f Maximum (Max).g p b 0.05 when compared to other congeners.

Table 3PCBs concentration in serum blood of people living in Mexico City (ng/g lipid).

Congener abbreviation Meana SDb PC25c PC50 PC75 PC95 Mind Maxe

PCB 28 4.10 0.40 3.30 3.90 5.20 5.70 bLOD 5.80PCB 52 2.80 0.50 bLOD 3.20 4.90 9.10 bLOD 42.0PCB 99 2.60 0.40 bLOD 3.20 3.30 3.60 bLOD 5.00PCB 105 3.00 0.50 bLOD 3.40 4.10 4.70 bLOD 5.20PCB 118 3.50 1.60 2.90 3.80 4.20 4.30 bLOD 5.00PCB 128 6.50f 3.20 4.40 5.80 7.10 9.60 4.00 20.0PCB 138 1.80 0.50 bLOD 1.50 4.30 5.90 bLOD 13.0PCB 153 1.90 0.10 bLOD 1.80 2.30 7.50 bLOD 8.50

498 S. Orta-García et al. / Science of the Total Environment 472 (2014) 496–501

quality control, organic contaminants in fortified human serum[National Institute of Standards and Technology (NIST) SRM 1958]were used. Our average recovery was 90–110% for all tested analytes.The results on lipid-weight basis were calculated as reported previously(Bergonzi et al., 2009).

2.4. Statistical analyses

The distribution of each analyte (mean, median, standard deviation,etc.) was examined and is reported for those in whichmore than 60% ofsamples were above the detection limits. To satisfy normality criteria,levels of PBDEs, PCBs, DDT and DDE were logarithm-transformed.Therefore, all the results are presented as geometric means. Mean levelsof PBDE congeners and PCB congeners were compared by one-wayanalysis of variance (ANOVA) followed by the Tukey's test. For DDTand DDE a Student t-test was used. If the concentration of an individualcongener (PBDES, PCBs, DDT and DDE) was less than the LOD, itsconcentration was assumed to be LOD / 2 for statistical analysis. Forall statistical analyses we used JMP-IN Start Statistics Software 5.0(SAS Institute).

3. Results

The characteristics of the study population are shown in Table 1. Al-most 55% of the subjects were male. The mean body mass index (BMI)was 25 kg/m2 for all participants. Approximately 65% of participantshad attended only elementary school, 25% had attended high-schooland 10% higher education.

The concentrations of PBDE congeners in serum samples are shownin Table 2. The total PBDE levels ranged from non-detectable (bLOD) to350 ng/g lipid, with a mean total PBDE level of 15.3 ± 6.7 ng/g lipid(geometric mean ± standard deviation). The dominant congeners inthis study were BDE 154 (5.00 ± 3.90 ng/g lipid), followed by BDE100 (3.50 ± 0.40 ng/g lipid), BDE 99 (3.00 ± 0.32 ng/g lipid), BDE153 (2.40 ± 2.30 ng/g lipid) and BDE 47 (1.40 ± 0.31 ng/g lipid;Table 2). Moreover, the BDE 153 congener was detected in approxi-mately 95% of the samples, while the detection rates for BDE 154(30%), BDE 99 (55%), BDE-100 (60%), and BDE 47 (85%) were lowerthan that for BDE 153.

Table 3 shows the levels of PCBs found in the blood of subjects livingin the studied site (PCB 101 was not detectable; for this reason we didnot include these values in Table 3). The mean total PCB level in thestudy participants was 34.5 ± 9.90 ng/g lipid (range 8.20 to 91.0 ng/glipid). The congeners with the highest concentration in the bloodwere PCB 128 (6.50 ± 3.20 ng/g lipid; geometric mean ± standarddeviation) and PCB 156 (5.30 ± 1.90 ng/g lipid), followed by congenerssuch as PCB 28 (4.10 ± 0.40 ng/g lipid), PCB 118 (3.50 ± 1.60 ng/glipid), PCB 105 (3.0 ± 0.50 ng/g lipid), PCB 52 (2.80 ± 0.50 ng/glipid) and PCB 99 (2.60 ± 0.40 ng/g lipid). Congeners with concentra-tions lower than 2.00 ng/g lipid were PCB 138, PCB 153, PCB 170, PCB180, PCB 183 and PCB 187. In our analyses of congeners, we assessedthree Dioxin-like PCB congeners (PCB 105, PCB 118 and PCB 156) andthe other nine PCBs analyzed were non-Dioxin-like PCB congeners.The mean total level of non-Dioxin-like PCB congeners was

Table 1Population characteristics.

Mean ± SD (range)

Age (years) 40.5 ± 12.0 (26.0–52.5)Men (%) 55.0Female (%) 45.0BMI (kg/m2) 25.0 ± 4.5 (22.0–29.0)Education (%)Elementary school 65.0High-school 25.0Higher education 10.0

approximately 18.8 ng/g lipid and was 15.7 ng/g lipid for Dioxin-likePCB congeners.

The mean blood levels of total DDT, p,p′-DDT and p,p′-DDE in thepopulation studied are shown in Table 4. The mean blood level of totalDDT (sum of p,p′-DDT and p,p′-DDE) was approximately 11.9 ±4.70 ng/g lipid. Moreover, the mean blood level for p,p′-DDT was3.0 ± 1.20 ng/g lipid and for p,p′-DDE was 8.90 ± 3.60 ng/g lipid(Table 4). An important finding in our study was that all subjects(100%) had detectable levels of the metabolite p,p′-DDE (data notshown). Finally, the DDT/DDE quotient in blood samples was 0.34,suggesting past exposure to the insecticide.

Finally, Fig. 2 shows the mean total levels of the three compoundfamilies studied. PCBs showed the highest blood concentration of thestudied compounds with a mean total level of 34.5 ± 9.90 ng/g lipid,followed by PBDEs with a mean level of 15.3 ± 6.70 ng/g lipid andthe mean concentration of total DDT was 11.9 ± 4.70 ng/g lipid.

4. Discussion

Prohibition or stronger restrictions on the application or emissionof POPs have been necessary; this was the aim of the Stockholm

PCB 156 5.30f 1.90 3.90 4.50 5.20 5.70 4.20 8.80PCB 170 1.00 0.30 bLOD 0.80 2.30 4.40 bLOD 6.50PCB 180 1.00 0.30 bLOD 0.50 1.90 3.80 bLOD 4.70PCB 183 0.50 0.20 bLOD 0.30 0.70 4.50 bLOD 6.50PCB 187 0.50 0.30 bLOD 0.50 1.00 3.90 bLOD 7.10Total PCBs 34.5 9.90 14.3 31.0 38.0 60.0 8.2 91.0

Blood concentrations are shown in ng/g lipid.The method detection limits (LOD) for all PCBs were approximately 0.30 ng/mL.

a Values are geometric means.b Standard Deviation (SD).c Percentile (PC).d Minimum (Min).e Maximum (Max).f p b 0.05 when compared to other congeners.

Table 4DDT and DDE concentrations in serum blood of people living in Mexico City (ng/g lipid).

Congener Meana SDb PC25c PC50 PC75 PC95 Mind Maxe

DDT 3.00 1.20 bLOD 2.50 4.80 7.50 bLOD 8.00DDE 8.90f 3.60 bLOD 7.70 11.5 15.3 bLOD 26.0Total DDT 11.9 4.70 bLOD 9.90 15.5 23.8 bLOD 34.0

Blood concentrations are shown in ng/g lipid.The method detection limits (LOD) for DDT and DDE were approximately 0.70 ng/mL.

a Values are geometric means.b Standard Deviation (SD).c Percentile (PC).d Minimum (Min).e Maximum (Max).f p b 0.05 when compared to DDT.

499S. Orta-García et al. / Science of the Total Environment 472 (2014) 496–501

Convention on POPs (UNEP, 2011). Moreover, this convention sought todetermine baseline exposures to POPs in the general population. In thisregard, in Mexico several monitoring studies have been performedthrough the country with the purpose to obtain a profile on peopleexposure to POPs. For example, exposure to public health insecticidessuch as dichlorodiphenyltrichloroethane (DDT) has been assessed inmalaria areas (Ortiz-Pérez et al., 2005; Pérez-Maldonado et al., 2004,2006); to polycyclic aromatic hydrocarbons (PAHs) in indigenouscommunities exposed to biomass combustion or in communitiesexposed to brick kiln smoke (Martínez-Salinas et al., 2010, 2012;Pruneda-Álvarez et al., 2012), to PCBs in communities exposed tobrick kiln smoke (Trejo-Acevedo et al., 2009) or in non-controlledwaste disposal sites (Costilla-Salazar et al., 2011; Trejo-Acevedo et al.,2013), and to PBDEs in industrial and urban communities (Perez-Maldonado et al., 2009; Orta-Garcia et al., 2012). In this regard, the pur-pose of the present study was to screen the people living in Mexico Cityin order to assess baseline exposures to POPs.

The results showed that the concentration of total PBDEs in serumsamples collected during 2010 from adults living in Mexico City was15.3 ng/g lipid. When the levels of total PBDEs in the study populationwere compared with levels found in other studies, we noted that thelevels in the present study were higher than those previously reportedin other areas around the world (Huang et al., 2013; Kalantzi et al.,2011; Kim et al., 2012; Lenters et al., 2013;Wang et al., 2013). For exam-ple, a study performed in human serum samples (n = 61) collected inAttika, Greece and analyzed for PBDEs, total PBDE concentrations(sum of BDE 47, BDE 99, BDE 100, BDE 153 and BDE 154) in allsamples (n = 61) ranged from 0.68 to 13.0 ng/g lipid, with a medianof 1.10 ng/g lipid (Kalantzi et al., 2011). Similar to the levels in Greece,720 serum samples were collected from non-occupationally exposedstudy participants in Korea in 2009 and 2010 (Kim et al., 2012). Themedian concentration of total PBDEs (the sum of BDE 28, BDE 47, BDE99, BDE 100, BDE 153, BDE 154, and BDE 183) was 4.90 ng/g lipid

CompoundsDDTs PCBs PBDEsB

loo

d C

on

cen

trat

ion

s (n

g/g

lip

id)

0

5

10

15

20

25

30

35 *

Fig. 2. Total PBDE, total PCB and total DDT concentrations in serum blood of Mexicanpeople. Serum blood concentrations are shown in ng/g lipid. Values are geometricmeans ± standard deviation (SD). *p b 0.05 when compared to other compounds.

(Kim et al., 2012). It is important to note that themean total PBDE levelsfound in Greece (1.07 ng/g lipid) and Korea (4.97 ng/g lipid) were sim-ilar to the median values observed in Europe (range: 0.75–7.80 ng/glipid for different countries; Bjermo et al., 2013; Chovancová et al.,2012; Kalantzi et al., 2011; Link et al., 2012), but much lower thanthat observed in North America as shown by our data and NHANES IVdata (NHANES, 2009). The mean level found in subjects aged 20 yearsand older in NHANES IV was approximately 30.0 ng/g lipid, approxi-mately 2 times higher than those found in the people living in MexicoCity. The results showed in this study are also similar to levels foundin a previous study performed in our country (Perez-Maldonado et al.,2009). In Perez-Maldonado et al. (2009) study mean level of approxi-mately 7.10 ng/g lipid for total PBDEs was found in Mexican children.On the other hand, higher levels of total PBDEs than those found inour study were observed in subjects living in e-waste recycling sites(Shen et al., 2010). For example, in a study analyzing blood samplescollected from two e-waste recycling sites in Southeast China: Luqiao(where PCBs-containing e-wastes were recycled) and Wenling (wherePBDE-containing e-wastes were recycled), the mean total PBDEs level(the sum of BDE 28, BDE 47, BDE 99, BDE 100, BDE 153, BDE 154, BDE180, and BDE 209) was 120 ng/g lipid in the blood of subjects fromLuqiao, while for subjects living in Wenling the level was 360 ng/glipid (Shen et al., 2010). An important finding in our study was thatBDE 153 (detected in 95% of assessed samples) and BDE 154 (highermean levels when compared with other congeners) were the dominantcongeners. In contrast, previous studies showed that the concentrationof BDE 47 was much higher than that of BDE 153 in North America(NHANES, 2009; Windham et al., 2010; Eskenazi et al., 2011). In thepast, the largest market for penta-BDE technical mixture was NorthAmerica, which accounted for approximately 95% of its sale in 2001(Birnbaum and Staskal, 2004). It is likely that BDE 47 was the mostdominant congener in North American sera because it was a majorcomponent of the penta-BDE technical mixture, such as BDE 71,accounting for 38% of the mixture by mass (La Guardia et al., 2006).The findings in our studymay be related to changes in the environmen-tal accumulation pattern over time, but could also be affected by tempo-ral changes. The notion of a temporal change is supported by a studyperformed in the Faroe Islands (Fängström et al., 2005a). In that studyassessed blood concentrations of polybrominated diphenyl ethers(PBDEs) in pregnant women in 1994–1995 and in their children at7 years of age. Maternal serum was dominated by BDE 47, while BDE153 dominated in the children's serum seven years later. The above-mentioned results were also supported by analyses of human milkfrom the Faroe Islands, where BDE 153 showed a dramatic increasebetween 1994–1995 and 1998–1999 (Fängström et al., 2005b). However, there is nodefinite explanation for this change in the accumulationprofile of PBDEs. Another possibility could be the metabolism of BDE209, leading to the formation of BDE 153 and BDE 154, or the higherpersistence of BDE 153 and BDE 154 than that of lower brominatedcongeners such as BDE 47. Moreover, these results may indicate thatsources of lower brominated diphenyl ethers are decreasing.

When the PCB levels in the blood found in this studywere comparedwith levels reported in others studies around the world, we noted thatpeople living in Mexico City had a similar mean total PCB level(34.5 ng/g lipid) to adults living in other locations around the world(Henríquez-Hernández et al., 2011; NHANES, 2009; Schettgen et al.,2011; Medehouenou et al., 2011; Wilhelm et al., 2003). In this regard,the mean total level of PCBs in subjects aged 20 years and older inNHANES IV in the United States of America was approximately25.0 ng/g lipid (NHANES, 2009). In a study performed in Canadiansaged 65 years and older, the mean total PCB level (the study assessed15 PCB congeners) was approximately 30.0 ng/g lipid (Medehouenouet al., 2011). On the other hand, Henríquez-Hernández et al. (2011)performed a study in Spain in a representative sample of the generalpopulation of the Spanish Archipelago of the Canary Islands andanalyzed 607 serum samples from subjects aged between 6 and

500 S. Orta-García et al. / Science of the Total Environment 472 (2014) 496–501

75 years. Themedian concentration of the sumof PCBs analyzed (18 PCBcongeners) was approximately 48.0 ng/g lipid. However, lower concen-trations of total PCBs in the blood were observed when the level in ourstudy subjects (mean level of 34.5 ng/g lipid) was compared with thelevels found in subjects (467 ng/g lipid) aged between 55 and 74 yearswho lived at sites near the General Electric capacitor facility whichused PCBs from 1944 to 1977 in New York, USA (Fitzgerald et al., 2012).

DDTwas heavily used inMexico in agriculture and inmalaria controlprograms. Therefore, human exposure to DDT has been reported in nu-merous communities in Mexico (Yáñez et al., 2002; Perez-Maldonadoet al., 2009, 2010; Trejo-Acevedo et al., 2009; Martínez-Salinas et al.,2012; Waliszewski et al., 2012; Herrero-Mercado et al., 2011), due tothe presence of this insecticide in different environmental media(Yáñez et al., 2002; Martinez et al., 2012; Martínez-Salinas et al., 2010,2012; González-Mille et al., 2010). However, our study site is not an ag-ricultural or an endemicmalaria area. Therefore, the DDT and DDE levelsfound in participants in our study could be explained by the alimentaryhabits that expose them to a higher rate of organochlorine pesticideresidues. In this context, the blood levels of p,p′-DDT (3.00 ng/g lipid),p,p′-DDE (8.90 ng/g lipid) and total DDT (11.9 ng/g lipid) found in thisstudy were lower than the levels found in adults assessed in monitoringstudies across the country as mentioned above. For example, in a studyperformed by Waliszewski et al. (2012), the blood serum of inhabitantsof Veracruz, Mexico was analyzed and p,p′-DDE was found to be themajor organochlorine component, detected in 100% of samples at amean concentration of 16.0 μg/g lipid, p,p′-DDT was present in 41% ofmonitored samples at a mean concentration of 3.10 μg/g lipid, and amean total DDT level of approximately 19.0 μg/g lipid was noted(Waliszewski et al., 2012). Moreover, an interesting finding wasobserved when the results of our study were compared with the levelsfound in participants in the NHANES IV study (20 years and older),where higher levels in the United States of America participants inNHANES IV (300 ng/g lipid; NHANES, 2009)were foundwhen comparedwith the levels found in our study (12.0 ng/g lipid).

It is important to remember that comparisons of POP concentrationsacross regions or countries are not straightforward as several factors canbe important determinants of serum POPs and must be taken into ac-count. These include time aspects such as the age of participants andtime of blood collection, technical considerations and the specific con-geners measured.

On the other hand, in several regions around the world the concen-trations of old POPs (such as DDT and PCBs) in environmental and bio-logicalmatrixes have decreased as production of these compounds havebeen banned (Sjödin et al., 2004). In contrast, an increase in the concen-trations of new POPs (such as PBDEs) over the years has been observed(Sjödin et al., 2004). In Mexico the data are scarce to evaluate the ten-dency through the years. Therefore, more studies are necessary inMexico in order to assess the true trend in these compounds in Mexico.

Our exploratory study has several limitations, the most notable ofwhich is the small sample size. However, this POP screening studyshowed the need for biomonitoring programs for surveillance of thegeneral population. Thus, a national environmental health program forindividuals is needed. Moreover, biomonitoring of toxins on a globalscale may be the first step towards the prevention of toxin-induced ill-nesses in the population.

Acknowledgments

This work was supported by grant from the Consejo Nacional deCiencia y Tecnología, Mexico, CONACYT–SEMARNAT 107900.

References

ATSDR. Toxicological profile for polychlorinated biphenyls, Agency for ToxicSubstances and Disease Registry. Atlanta, GA: US Public Health Service; 2000[http://www.atsdr.cdc.gov/toxprofiles/tp17.pdf. Accessed on 02-09-2013].

ATSDR. Toxicological profile for DDT/DDE/DDD, Agency for Toxic Substances and DiseaseRegistry. Atlanta, GA: US Public Health Service; 2002 [http://www.atsdr.cdc.gov/toxprofiles/tp35.pdf. Accessed on 02-09-2013].

Bergman A, Ryden A, Law RJ, de Boer J, Covaci A, Alaee M, et al. A novel abbreviation stan-dard for organobromine, organochlorine and organophosphorus flame retardantsand some characteristics of the chemicals. Environ Int 2012;49:57–82.

Bergonzi R, De Palma G, Tomasi C, Cristina Ricossa M, Apostoli P. Evaluation of differentmethods to determine total serum lipids for normalization of circulating organochlo-rine compounds. Int Arch Occup Environ Health 2009;82:1241–7.

Birnbaum LS, Staskal DF. Brominated flame retardants: cause for concern? Environ HealthPerspect 2004;112:9–17.

Bjermo H, Darnerud PO, Lignell S, Pearson M, Rantakokko P, Nälsén C, et al. Fish intakeand breastfeeding time are associated with serum concentrations of organochlorinesin a Swedish population. Environ Int 2013;51:88–96.

Bjerregaard P, Pedersen HS, Nielsen NO, Dewailly E. Population surveys in Greenland1993–2009: temporal trend of PCBs and pesticides in the general Inuit populationby age and urbanisation. Sci Total Environ 2013;454–455:283–8.

Chovancová J, Conka K, Fabišiková A, Sejáková ZS, Dömötörová M, Drobná B, et al.PCDD/PCDF, dl-PCB and PBDE serum levels of Slovak general population.Chemosphere 2012;88:1383–9.

Costa LG, Giordano G, Tagliaferri S, Caglieri A, Mutti A. Polybrominated diphenyl ether(PBDE) flame retardants: environmental contamination, human body burden andpotential adverse health effects. Acta Biomed 2008;79:172–83.

Costilla-Salazar R, Trejo-Acevedo A, Rocha-Amador D, Gaspar-Ramirez O, Díaz-Barriga F,Pérez-Maldonado IN. Assessment of polychlorinated biphenyls and mercury levelsin soil and biological samples from San Felipe, Nuevo Mercurio, Zacatecas, Mexico.Bull Environ Contam Toxicol 2011;86:212–6.

de Wit CA, Alaee M, Muir DC. Levels and trends of brominated flame retardants in theArctic. Chemosphere 2006;64(2):209–33.

Domínguez-Cortinas G, Díaz-Barriga F, Martínez-Salinas RI, Cossío P, Pérez-Maldonado IN.Exposure to chemical mixtures in Mexican children: high-risk scenarios. Environ SciPollut Res Int 2013;20:351–7.

Eskenazi B, Fenster L, Castorina R, Marks AR, Sjödin A, Rosas LG, et al. A comparison ofPBDE serum concentrations in Mexican and Mexican–American children living inCalifornia. Environ Health Perspect 2011;119:1442–8.

Fängström B, Hovander L, Bignert A, Athanassiadis I, Linderholm L, Grandjean P, et al.Concentrations of polybrominated diphenyl ethers, polychlonnated biphenyls, andpolychlorobiphenylols in serum from pregnant Faroese women and their children7 years later. Environ Sci Technol 2005a;39:9457–63.

Fängström B, Strid A, Grandjean P, Weihe P, Bergman A. A retrospective study of PBDEsand PCBs in human milk from the Faroe Islands. Environ Health 2005b;4:12.

Fitzgerald EF, Shrestha S, Gomez MI, McCaffrey RJ, Zimmerman EA, Kannan K, et al.Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) andneuropsychological status among older adults in New York. Neurotoxicology2012;33:8–15.

González-Mille DJ, Ilizaliturri-Hernández CA, Espinosa-Reyes G, Costilla-Salazar R,Díaz-Barriga F, Ize-Lema I, et al. Exposure to persistent organic pollutants(POPs) and DNA damage as an indicator of environmental stress in fish of differ-ent feeding habits of Coatzacoalcos, Veracruz, Mexico. Ecotoxicology 2010;19:1238–48.

Henríquez-Hernández LA, Luzardo OP, Almeida-González M, Alvarez-León EE,Serra-Majem L, Zumbado M, et al. Background levels of polychlorinated biphenylsin the population of the Canary Islands (Spain). Environ Res 2011;111:10–6.

Herrero-Mercado M, Waliszewski SM, Caba M, Martínez-Valenzuela C, Gómez Arroyo S,Villalobos Pietrini R, et al. Organochlorine pesticide gradient levels among maternaladipose tissue, maternal blood serum and umbilical blood serum. Bull EnvironContam Toxicol 2011;86:289–93.

Huang F, Wen S, Li J, Zhong Y, Zhao Y, Wu Y. The human body burden of polybrominateddiphenyl ethers and their relationships with thyroid hormones in the general popu-lation in Northern China. Sci Total Environ 2013;466–467C:609–15.

Hung H, Blanchard P, Halsall CJ, Bidleman TF, Stern GA, Fellin P, et al. Temporal and spatialvariabilities of atmospheric polychlorinated biphenyls (PCBs), organochlorine (OC)pesticides and polycyclic aromatic hydrocarbons (PAHs) in the Canadian Arctic:results from a decade of monitoring. Sci Total Environ 2005;342(1–3):119–44.

Kalantzi OI, Geens T, Covaci A, Siskos PA. Distribution of polybrominated diphenyl ethers(PBDEs) and other persistent organic pollutants in human serum from Greece. Envi-ron Int 2011;37:349–53.

Kim J, Kang JH, Park H, Baek SY, Kim YH, Chang YS. Assessment of polybrominateddiphenyl ethers (PBDEs) in serum from the Korean general population. EnvironPollut 2012;164:46–52.

La Guardia MJ, Hale RC, Harvey E. Detailed polybrominated diphenyl ether (PBDE) conge-ner composition of the widely used penta-, octa-, and deca- PBDE technical flameretardant mixtures. Environ Sci Technol 2006;40:6247–54.

Lenters V, Thomsen C, Smit LA, Jönsson BA, PedersenHS, Ludwicki JK, et al. Serum concen-trations of polybrominated diphenyl ethers (PBDEs) and a polybrominated biphenyl(PBB) in men from Greenland, Poland and Ukraine. Environ Int 2013;61C:8–16.

Link B, Gabrio T, Mann V, Schilling B, Maisner V, König M, et al. Polybrominated diphenylethers (PBDE) in blood of children in Baden-Württemberg between 2002/03 and2008/09. Int J Hyg Environ Health 2012;215:224–8.

Martinez F, Trejo-Acevedo A, Betanzos AF, Espinosa-Reyes G, Alegría-Torres JA, PérezMaldonado IN. Assessment of DDT and DDE levels in soil, dust, and blood samplesfrom Chihuahua Mexico. Arch Environ Contam Toxicol 2012;62:351–8.

Martínez-Salinas RI, Elena Leal M, Batres-Esquivel LE, Domínguez-Cortinas G, Calderón J,Díaz-Barriga F, et al. Exposure of children to polycyclic aromatic hydrocarbons inMexico: assessment of multiple sources. Int Arch Occup Environ Health 2010;83:617–23.

501S. Orta-García et al. / Science of the Total Environment 472 (2014) 496–501

Martinez-Salinas RI, Diaz-Barriga F, Batres-Esquivel LE, Perez-Maldonado IN. Assessmentof the levels of DDT and its metabolites in soil and dust samples from Chiapas,Mexico. Bull Environ Contam Toxicol 2011;86:33–7.

Martínez-Salinas RI, Pérez-Maldonado IN, Batres-Esquivel LE, Flores-Ramírez R,Díaz-Barriga F. Assessment of DDT, DDE, and 1-hydroxypyrene levels in bloodand urine samples in children from Chiapas Mexico. Environ Sci Pollut Res Int2012;19:2658–66.

Medehouenou TC, Ayotte P, Carmichael PH, Kröger E, Verreault R, Lindsay J, et al.Polychlorinated biphenyls and organochlorine pesticides in plasma of older Cana-dians. Environ Res 2011;111:1313–20.

NHANES IV. Fourth national report on human exposure to environmental chemicals.Atlanta, Georgia: Department of Health and Human Services Centers for DiseaseControl and Prevention; 2009.

Orta-Garcia ST, León-Moreno LC, González-Vega C, Dominguez-Cortinas G, Espinosa-ReyesG, Pérez-Maldonado IN. Assessment of the levels of polybrominated diphenyl ethersin blood samples from Guadalajara, Jalisco, Mexico. Bull Environ Contam Toxicol2012;89:925–9.

Ortiz-Pérez MD, Torres-Dosal A, Batres LE, López-Guzmán OD, Grimaldo M, Carranza C,et al. Environmental health assessment of deltamethrin in a malarious area ofMexico: environmental persistence, toxicokinetics, and genotoxicity in exposed chil-dren. Environ Health Perspect 2005;113:782–6.

Pérez-Maldonado IN, Díaz-Barriga F, De la Fuente H, González-Amaro R, Calderón J, YañezL. DDT induces apoptosis in human mononuclear cells in vitro and is associated withincreased apoptosis in exposed children. Environ Res 2004;94:38–46.

Pérez-Maldonado IN, Athanasiadou M, Yáñez L, González-Amaro R, Bergman A,Díaz-Barriga F. DDE-induced apoptosis in children exposed to the DDT metabolite.Sci Total Environ 2006;370:343–51.

Perez-Maldonado IN, Ramirez-Jimenez M del R, Martınez-Arevalo LP, Lopez-Guzman OD,Athanasiadou M, Bergman A, et al. Exposure assessment of polybrominated diphenylethers (PBDEs) in Mexican children. Chemosphere 2009;75:1215–20.

Perez-Maldonado IN, Trejo A, Ruepert C, Jovel R del C, MendezMP, Ferrari M, et al. Assess-ment of DDT levels in selected environmental media and biological samples fromMexico and Central America. Chemosphere 2010;78:1244–9.

Pruneda-Álvarez LG, Pérez-Vázquez FJ, Salgado-Bustamante M, Martínez-Salinas RI,Pelallo-Martínez NA, Pérez-Maldonado IN. Exposure to indoor air pollutants (polycy-clic aromatic hydrocarbons, toluene, benzene) inMexican indigenouswomen. IndoorAir 2012;22:140–7.

Rodríguez-Dozal S, Riojas Rodríguez H, Hernández-Ávila M, Van Oostdam J, Weber JP,Needham LL, et al. Persistent organic pollutant concentrations in first birth mothersacross Mexico. J Expo Sci Environ Epidemiol 2012;22:60–9.

Schettgen T, GubeM, Alt A, FrommeH, Kraus T. Pilot study on the exposure of the Germangeneral population to non-dioxin-like and dioxin-like PCBs. Int J Hyg Environ Health2011;214:319–25.

Shen H, Ding G, Han G, Wang X, Xu X, Han J, et al. Distribution of PCDD/Fs, PCBs, PBDEsand organochlorine residues in children's blood from Zhejiang. China. Chemosphere2010;80:170–5.

Sjödin A, Jones RS, Focant JF, Lapeza C, Wang RY, McGahee EE, et al. Retrospectivetime-trend study of polybrominated diphenyl ether and polybrominated andpolychlorinated biphenyl levels in human serum from the United States. EnvironHealth Perspect 2004;112:654–8.

Trejo-Acevedo A, Díaz-Barriga F, Carrizales L, Domínguez G, Costilla R, Ize-Lema I, et al.Exposure assessment of persistent organic pollutants andmetals inMexican children.Chemosphere 2009;74:974–80.

Trejo-Acevedo A, Rivero-Pérez NE, Flores-Ramirez R, Orta-García ST, Pruneda-Álvarez LG,Pérez-Maldonado IN. Assessment of the levels of hexachlorocyclohexane in bloodsamples from Mexico. Bull Environ Contam Toxicol 2012a;88:833–7.

Trejo-Acevedo A, Rivero-Pérez NE, Flores-Ramírez R, Orta-García ST, Varela-Silva JA,Pérez-Maldonado IN. Assessment of the levels of persistent organic pollutants and1-hydroxypyrene in blood and urine samples from Mexican children living in an en-demic malaria area in Mexico. Bull Environ Contam Toxicol 2012b;88:828–32.

Trejo-Acevedo A, Rivero-Pérez NE, Flores-Ramírez R, Díaz-Barriga F, Ochoa Angeles C,Pérez-Maldonado IN. Assessment of persistent organic pollutants levels in bloodsamples from Quintana Roo, Mexico. Int J Hyg Environ Health 2013;216:284–9.

Turusov V, Rakitsky V, Tomatis L. Dichlorodiphenyltrichloroethane (DDT): ubiquity, per-sistence and risks. Environ Health Perspect 2002;110:125–8.

UNEP. Stockholm convention on persistent organic pollutants (POPs). Geneva, Switzerland:Text and annexes; 2011 [20011-64 Available from: www.unep.org].

Valera B, Ayotte P, Poirier P, Dewailly E. Associations between plasma persistent organic pol-lutant levels and blood pressure in Inuit adults from Nunavik. Environ Int 2013;59:282–9.

Waliszewski SM, Caba M, Herrero-Mercado M, Saldariaga-Noreña H, Meza E, Zepeda R,et al. Organochlorine pesticide residue levels in blood serum of inhabitants from Ve-racruz, Mexico. Environ Monit Assess 2012;184:5613–21.

Wang HS, Jiang GM, Chen ZJ, Du J, Man YB, Giesy JP, et al. Concentrations and conge-ner profiles of polybrominated diphenyl ethers (PBDEs) in blood plasma fromHong Kong: implications for sources and exposure route. J Hazard Mater2013;261C:253–9.

Wilhelm M, Ewers U, Schulz C. Revised and new reference values for some persistent or-ganic pollutants (POPs) in blood for human biomonitoring in environmental medi-cine. Int J Hyg Environ Health 2003;206:223–9.

Windham GC, Pinney SM, Sjodin A, Lum R, Jones RS, Needham LL, et al. Body burdens ofbrominated flame retardants and other persistent organo-halogenated compoundsand their descriptors in US girls. Environ Res 2010;110:251–7.

Yáñez L, Ortiz-Pérez D, Batres LE, Borja-Aburto VH, Díaz-Barriga F. Levels of dichlorodi-phenyltrichloroethane and deltamethrin in humans and environmental samples inmalarious areas of Mexico. Environ Res 2002;88:174–81.