Chemosphere 82 (2011) 1253–1261

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Chemosphere

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

S. Marin a, P. Villalba a, J. Diaz-Ferrero b, G. Font c, V. Yusà a,⇑a Public Health Research Center (CSISP), 21 Avda Cataluña, 46020 Valencia, Spainb Environmental Laboratory, Institut Quimic de Sarria, Ramon Llull University, Via Augusta 390, 08017 Barcelona, Spainc Laboratory of Food Science and Toxicology, Faculty of Pharmacy, University of Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain

a r t i c l e i n f o

Article history:Received 30 June 2010Received in revised form 5 November 2010Accepted 7 December 2010Available online 8 January 2011

Keywords:PCDDsPCDFsDioxin-like PCBsFood productsDietary intake

0045-6535/$ - see front matter � 2010 Elsevier Ltd. Adoi:10.1016/j.chemosphere.2010.12.033

⇑ Corresponding author. Tel.: +34 961925865.E-mail address: yusa_vic@gva.es (V. Yusà).

a b s t r a c t

During 2006–2008, a monitoring program was conducted on 29 target compounds, including PCDD/Fsand dl-PCBs, comprising 150 randomly collected individual food samples marketed in the Region ofValencia, Spain, grouped into 8 categories (vegetables, cereals, fats and oils, eggs, milk and dairy products,fish products, meat and meat products and fish oil). For PCDD/Fs, the highest frequency of detection cor-responds to 1,2,3,4,6,7,8-HpCDD, OCDD, 2,3,4,7,8-PeCDF; and PCBs 118, 105 and 156 were the more fre-quent dl-PCBs. The food groups presenting higher contamination, expressed as toxic equivalents (WHO-TEQs), were fish oil (6.38 pg WHO-TEQ g�1 fat), fish (1.21 pg WHO-TEQ g�1 w.w.) and milk and dairyproducts (0.90 pg WHO-TEQ g�1 fat). Of all analysed samples, only two fish oils presented levels higherthan the EU limits for total WHO-TEQ. The average PCDD/Fs and dl-PCBs intakes were estimated as2.86 pg WHO-TEQ kg�1 b.w. d�1 and 4.58 pg WHO-TEQ kg�1 b.w. d�1, for adults and children, respec-tively, using the deterministic method for chronic exposure. The main contributors to total intake foradults were fish (59%), milk and dairy products (19%), and fat and oils (9%). The average daily intakefor adults (2.86 pg WHO-TEQ kg�1 b.w. d�1) is within range of TDI recommended by the WHO (1–4 pg WHO-TEQ kg�1 b.w. d�1), and slightly above the TWI and PTMI adopted by SCF and JECFArespectively.

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1. Introduction

Polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinateddibenzofurans (PCDFs), and polychlorinated biphenyls (PCBs) arethree classes of chemically and structurally related polyhalogenat-ed aromatic hydrocarbons and, with each of these groups consist-ing of 75, 135 and 209 theoretical individual congeners,respectively, based on the number and position of chlorine atomsin the chemical structure (Gilpin et al., 2003). They usually occuras a mixture of congeners, and their ubiquity, high chemical andmetabolic persistence, and potent toxicity of some of the congen-ers make them a well recognized class of persistent organic pollu-tants (POPs) which are included in the Stockholm Convention(United Nations Environment Programme (UNEP), 2001).

A subset of dioxins and dioxin-like PCBs (dl-PCBs), comprising17 laterally substituted PCDD/F and 12 non-ortho and mono-orthochlorine-substituted PCBs, induce a similar spectrum of biologicaleffects and toxic responses that are mediated through the arylhydrocarbon (Ah) receptor, which has been the basis for establish-

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ing the toxic equivalency factors (TEF) and the total toxic equiva-lent (TEQ) concepts (Van den Berg et al., 2006).

The World Health Organization (WHO) has set up a tolerabledaily intake (TDI) range of 1–4 pg TEQ kg�1 b.w. for dioxins (WorldHealth Organization (WHO), 2000). Likewise, a tolerable weekly in-take (TWI) of 14 pg WHO-TEQ kg�1 b.w. (body weight) has beendetermined by the European Union through the Scientific Commit-tee on Food (Scientific Committee on Food (SCF), 2001) and a strat-egy to reduce human intake levels to below this threshold has beenimplemented (European Commission, 2001). As part of this strat-egy, and to prevent the health risk from PCDD/Fs and dl-PCBs expo-sure, maximum levels for dioxins and for the sum of dioxins anddioxin-like PCBs in foodstuffs of animal origin and vegetable oils(European Commission, 2006b), as well as target and action levelshave been established in the EU in order to encourage a proactiveapproach to reducing the dioxins and dl-PCBs present in food(European Commission, 2006a).

Food consumption is the main route for human exposure toPCDD/Fs and dioxin-like PCBs, following bioaccumulation of thesecompounds in the aquatic and terrestrial food chains. Fish and sea-food, meat and meat products, and dairy products have been re-ported as some of the major sources of exposure in adults andchildren (Bordajandi et al., 2004). However, some authors have

1254 S. Marin et al. / Chemosphere 82 (2011) 1253–1261

showed a notable decline in levels in food and human dietaryexposure to PCDD/Fs and dl-PCBs (European Food Safety Authority(EFSA), June 2004) (Llobet et al., 2008). In contrast to this trend,several incidents of specific contamination in different countrieshave caused high levels of these pollutants in foodstuffs and conse-quently great concern (Covaci et al., 2002).

The strategies to reduce dioxin intakes has led to numerous sur-vey studies on the concentration of dioxins in particular food itemssuch as fish (Gomara et al., 2005), meat (Huwe et al., 2009), andbaby food (Lorán et al., 2010). Likewise, several studies have per-formed assessments of the intake of dioxins from the diet (Kroeset al., 2002), using different approaches such as market basket(Wang et al., 2009), monitoring programmes (Bilau et al., 2008),or total diet studies (Windal et al., 2010).

We present here the results of the monitoring program onPCDD, PCDF, and dl-PCBs in foods carried out for the Departmentof Public Health of the Valencian government, Spain, from 2006to 2008. The results were intended to assess the levels of the bio-logically active congeners in the main food groups, to evaluatewhether the present levels of dioxins and dioxin-like PCBs exceedthe maximum permitted levels of dioxins in food products accord-ing to EU Council regulation, to establish the contribution of diox-ins, furans and coplanar PCBs to the toxic equivalent quantities(WHO-TEQ) in the studied foodstuffs, and finally to asses the die-tary exposure of adults and children.

2. Materials and methods

2.1. Food sampling

Sampling of foodstuffs has been performed in the framework ofan official monitoring program performed as detailed in Commis-sion Regulation 1883/2006. A total of 150 food samples groupedin 8 categories: 8 vegetables (i.e. oranges, lettuces and potatoes),5 cereals (i.e. wheat and rice); 14 oils and fats (vegetable oils andanimal fats); 22 hen eggs; 19 milk and dairy products (cheese, milkand yoghurt); 38 fish (i.e. mackerel, salmon, eel, sardine and mus-sel); 40 meat and meat products (beef, pork, lamb and poultry) and4 fish oils were randomly collected from factories, local marketsand supermarkets during 2006–2008 by food inspectors from thePublic Health Department. Samples were analysed individuallyand then the results grouped to evaluate average levels and rangesin each food.

2.2. Chemical analysis and QA/QC

Determination of seventeen PCDD/Fs congeners together withtwelve dl-PCB congeners were carried out following analyticalmethods based on international norms for dioxin analysis, suchas EPA 1613 (EPA, 1994) and following the requirements of Com-mission Regulation 1883/2006 (European Commission, 2006c).Analyses were performed by the Environmental Laboratory, Insti-tut Químic de Sarrià; this laboratory has been accredited followingthe EN ISO/IEC 17025 standard. A detailed description of the chem-icals, methods, HRGC–HRMS instrumental determination and QA/QC procedures could be found in the supplementary data associ-ated to this article (see Appendix).

Prior to initiating the study, analytical methods were validated.Precision and accuracy were evaluated for each method at differentlevels. Studies for precision were performed on real samples andaccuracy studies were carried out with spiked samples. The ex-panded uncertainty for the sum of PCDD/Fs and sum of dl-PCBswere between 10% and 15% for most methods.

Recoveries of the labelled 13C12 surrogates analogues of eachcompound were determined. Most recoveries were in the range

of 60–110% for all matrices. In each sample, retention time andintensity rations of monitored ions were used as identification cri-teria. A deviation of the ion intensity ratios within 20% of the the-oretical value was considered acceptable. Quantification throughthe isotopic dilution method directly corrected analyte concentra-tions for surrogate recoveries.

Additionally, the method performance was assessed throughsuccessful participation (z < 1 in most cases) every year (since2000) in interlaboratory studies organized by the Norwegian Insti-tute of Public Health.

The total of PCDD/F and dl-PCB concentrations in each samplewas expressed as Toxic Equivalents (TEQ), which were calculatedby multiplying the individual congeners concentrations by theirrespective toxic equivalency factor (TEF), as established by theWorld Health Organisation in 1998 (Van den Berg et al., 1998),and were subsequently summed up to give the total concentra-tions as TEQ.

2.3. Exposure assessment

Dietary intake was calculated using the deterministic methodfor chronic exposure (Dorne et al., 2009). This point-estimated in-take was calculated by multiplying the respective average concen-tration (median) by the weight of the food consumed by an averageadult from Spain (17 years and over, 68.5 kg b.w.) per day. Alsoexposures for children (7–12 years; average weight, 34.5 kg) wereestimated.

Daily intake (pg WHO-TEQ kg b.w. d�1) = Occurrence (pg WHO-TEQ g�1 w.w.) � Consumption (g kg�1 b.w. d�1).

Exposure was calculated for both PCDD/Fs and dl-PCBs. For cal-culations, when a congener concentration was under the limit ofdetection (LOD), the value was assumed to be respective LOD(upper bound approach).

Consumption data by the general population of the analyzedfoods were obtained from the national food consumption surveyfor chemical exposure developed by Spanish Food Safety Authority(Agencia Española de Seguridad Alimentaria y Nutrición (AESAN),2006).

3. Results and discussion

3.1. PCDD/F and PCB levels

Table 1 shows the mean and range of concentrations of the 17PCDD/F congeners and 12 PCB congeners analysed, along with theirfrequencies of detection in each of the 8 groups of foodstuffsstudied.

For PCDDs, the highest overall frequency of detection corre-sponds to HpCDD and OCDD, which were detected in 90% and87% of all the analysed samples, respectively, with average concen-trations ranging from 36.10 � 10�3 pg g�1 w.w. in milk and dairyproducts to 197 � 10�3 pg g�1 w.w. in fish oil, for HpCDD; and47.05 � 10�3 pg g�1 w.w. in milk and dairy products to 630 �10�3 pg g�1 in fats and oils, for OCDD. In some food groups suchas meat products, eggs, cereals and dairy products, these two cong-eners were detected in all samples analysed.

OCDD and HpCDD were also the predominant congeners in adiet study developed in Catalonia (Spain) (Llobet et al., 2003),which reported the highest levels for fish and shellfish (averageof 4.03 ng kg�1 fat and 15.57 ng kg�1 fat, for HpCDD and OCDD,respectively), eggs (average of 3.38 ng kg�1 fat and 15.03 ngkg�1 fat, for HpCDD and OCDD, respectively) and meat (averageof 2.11 ng kg�1 fat and 12.39 ng kg�1 fat, for HpCDD and OCDD,respectively). These two highly chlorinated congeners also showedthe highest concentrations in other studies (Bocio and Domingo,

Table 1aMedian and range of PCDD/Fs and dl-PCBs concentrations (�10�3 pg g�1 w w ) corresponding to the different foods studied.

Congeners Vegetables (n = 10) Cereals (n = 5) FATS and OILS (n = 14) EGGS (n = 22)

Median (min–max) D� Median (min–max) D Median (min–max) D Median (min–max) D

PCDD/F congeners2,3,7.8-TCDD – – 0 – – 0 170 170 1 – – 01,2,3,7,8-PeCDD 6.47 6.47 1 12.70 12.70 1 93.55 (87.10–100) 2 10.50 (8.92–15.70) 51,2,3,4,7,8-HxCDD 6.69 6.69 1 10.30 10.30 1 50 50 1 47.30 (8.80–71.60) 51,2,3,6,7,8-HxCDD 11.20 11.20 1 18.65 (14.50–22.80) 2 95 (80–110) 2 21.70 (12–31.20) 91,2,3,7,8,9-HxCDD 10.60 10.60 1 22.10 (16.30–27.90) 2 – – 0 16.50 (11–20.10) 61,2,3,4,6,7,8-HpCDD 54.10 (22–156) 8 65.10 (22.50–87) 5 139 (0.23–323) 12 36.30 (20–125) 22OCDD 161 (68.5–538) 8 168 (61.10–228) 5 630 (1.04–957) 10 71.90 (23–423) 222,3,7,8-TCDF 27.20 (14.40–110) 8 52 (21.60–130) 5 55 (0.22–130) 8 32.75 (15.30–113) 221,2,3,7,8-PeCDF 18.85 (17.10–20.60) 2 20.30 (6.51–25.10) 3 – – 0 14.90 (11.10–40.70) 182,3,4,7,8-PeCDF 13.65 (7.85–52) 6 31.55 (13.90–55.80) 4 70 (50–230) 7 21.55 (12.60–45.60) 221,2,3,4,7,8-HxCDF 18.35 (8.81–79.10) 6 41.25 (18.70–92.40) 4 65 (20–100) 6 23.30 (12.60–61.90) 191,2,3,6,7,8-HxCDF 16.70 (7.93–33.40) 4 23.20 (7.57–48.70) 4 50 (20–80) 5 12.85 (8.30–30.50) 122,3,4,6,7,8-HxCDF – – 0 – – 0 – – 0 14.80 (9.39–25.90) 51,2,3,7,8,9-HxCDF 14.25 (8.59–41.70) 4 16.30 (7.17–42.90) 3 45 (20–70) 2 12.73 (8.76–16.70) 21,2,3,4,6,7,8-HpCDF 20.40 (5.36–75.60) 7 40.95 (28.90–100) 4 88.10 (30–130) 7 17.20 (9.09–120) 191,2,3,4,7,8,9-HpCDF – – 0 – – 0 – – 0 23.35 (9.40–55.70) 4OCDF 41.60 41.60 1 28.50 (25.40–31.60) 2 78.60 (77.20–80) 2 49.50 (28.40–198) 5

PCBs non-orthoPCB-77 143.50 (68.3–217) 8 435 (250–1002) 5 410 (2.83–3750) 13 499 (142–2612) 22PCB-81 – – 0 48.80 (36.3–61.3) 2 215.1 (0.31–430) 2 53.40 (23.4–162) 15PCB-126 36.00 (18.8–70.8) 3 127.5 (125–130) 2 367 (0.37–1653) 9 93.80 (29.1_155) 20PCB-169 – – 0 23.20 23.20 1 544.5 (136–1387) 4 30.90 (22.3–33.7) 5

PCB mono-orthoPCB-105 1396 (535–1999) 8 2254 (555–3248) 5 8620 (10.5–20 400) 14 4970 (1174–11 820) 22PCB-114 99.50 (45.5–128) 7 152 (57.5–272) 5 1230 (0.73–17 500) 11 303 (70.5–696) 22PCB-118 3878 (1457–4962) 8 7346 (1380–8469) 5 27 020 (26.8–885 000) 14 13 110 (3072–27 580) 22PCB-123 85.30 (45.1–98.3) 6 157 (77–297) 5 590.5 (0.62–10 900) 10 176.5 (49.1–575) 22PCB-156 169 (86.9–328) 8 371 (263–624) 5 7435 (1.7–103 000) 14 2231 (535–4023) 22PCB-157 83 (35.6–148) 8 109 (66.8–304) 5 2190 (0.51–23 900) 13 361.5 (102–770) 22PCB-167 156 (63.4–229) 8 266 (164–478) 5 2312 (0.99–45 400) 14 885 (265–1439) 22PCB-189 89 89 1 148.3 (45.6–251) 2 1495 (390–8445) 8 200.5 (63–410) 22

D: number of samples > LOD.

S. Marin et al. / Chemosphere 82 (2011) 1253–1261 1255

2005); (Bordajandi et al., 2004) in food samples surveyed in Spainduring 2002 and 2001, respectively.

On the other hand, the congeners less detected were 1,2,3,7,8,9HxCDD and TCDD with overall frequencies of 20% and 22%, respec-tively. This last congener is the most toxic, and was detected mainlyin meat (25%) and fish and fish oil (50%), with concentrationsranging from 2.27 � 10�3 pg g�1 w.w to 193 � 10�3 pg g�1 w.w.This same low frequency of detection for TCDD has also been re-ported in a diet study developed in Japan (Tsutsumi et al., 2001)that detected only some positive samples in two food groups (fishand shellfish, and meat and eggs) out of 14 food groups studied.

For furans, the most toxic congeners, 2,3,4,7,8-PeCDF, and2,3,7,8-TCDF, presented the highest overall frequency (86%), withaverage values of the latter ranging from 11.63 � 10�3 pg g�1 w.w.for milk and dairy products to 1.119 pg g�1 w.w. for fish oil. Theother nine furan congeners were detected in percentages between6% and 75% of all samples analysed, with higher concentrationsfound, in general, in fish oil and fats. The relevance of these twocongeners in different food samples has also been pointed out byother authors (Bordajandi et al., 2004).

With respect to PCB congeners, the most abundant is the mono-orto PCB-118, which was detected in practically all the food sam-ples, with average concentrations ranging from 3.878 pg g�1 w.w.in vegetables to 3467 pg g�1 w.w. in fish oil. The PCBs 105 and156 have a similar frequency of detection, but their concentrationsare substantially lower than for PCB-118 in the 8 food groups stud-ied. Likewise, the coplanar congener PCB-126, which has the high-est toxicity, also presents high frequency, particularly in eggs, dairyproducts, fish and meat, with mean concentrations between36.0 � 10�3 pg g�1 w.w. and 23.46 pg g�1 w.w.

The distribution of PCDD/Fs and PCBs congeners in the differentfood groups has also been studied. As an example, Fig. 1 shows theprofiles of a representative sample of dairy products (a) and fish(b). For fish, 2,3,7,8-TCDF, OCDD, and the two PeCDFs are the mostprominent dioxin congeners. However, for dairy products OCDDand 1,2,3,4,6,7,8-HpCDD have more importance. It is pertinent toemphasize the presence of highly chlorinated furans in the profileof fish compared with dairy products, although its contribution tothe toxicity is very limited owing to the very low WHO-TEF valueof the OCDF congener. Analogous profiles were reported in a studycarried out in the same area during 2004–2005 (Montaña et al.,2005).

For other foodstuffs, the congener OCDD shows the highest con-centrations, which is similar with the pattern observed in othersstudies that have stressed the relevance of this congener for non-contaminated samples (Focant et al., 2002). In the case of PCBs,comparable profile appears for the different foodstuffs, with a pre-dominance of the congeners 118, 105 and 156.

Fig. 2 depicts the percentage of each congener in the total dietbasket studied, both as concentrations and as toxic equivalents,and illustrates the exposure pattern to Dioxins and dl-PCBs owingto all food groups. For PCDD/F, the profile of concentrations wasdominated by 2,3,7,8-TCDF and OCDD congeners whose combinedconcentrations account for 42% of all PCDD/Fs. When the percent-age is expressed in toxic equivalents, the most abundant congenersare 2,3.4,7,8-PeCDF, 1,2,3,7,8-PeCDD and the 2,3,7,8 TCDD, that to-gether account for the 75% of total dioxins. This could be explainedbecause these three congeners present the highest WHO-TEF forPCDDs (TEF = 1) and for PCDFs (TEF = 0.5). For dl-PCBs, the mono-orto PCB-118 represents 56% of the total concentration, however,

Table 1bMedian and range of PCDD/Fs and dl-PCBs concentrations (�10�3 pg g�1 w w) corresponding to the different foods studied.

Congeners Milk and dairy products (n = 19) Fish products (n = 38) Meat and meat products (n = 40) Fish oil (n = 4)

Median (min–max) D Median (min–max) D Median (min–max) D Median (min–max) D

PCDD/F congeners2,3,7.8-TCDD 4.24 (2.27–6.21) 2 34.70 (9.18–91.3) 19 15 (4.92–187) 10 111.5 (30–193) 21,2,3,7,8-PeCDD 8.18 (1.41–55.10) 10 67.30 (16–196) 25 18 (4.51–104) 15 399 399 11,2,3,4,7,8-HxCDD 7.64 (1.57–34.20) 5 38.10 (12.6–57.1) 5 16 (6.08–64.8) 10 – – 01,2,3,6,7,8-HxCDD 7.87 (3.99–45.60) 10 62.80 (22.5–139) 15 15 (3.98–378) 22 234.5 (223–246) 21,2,3,7,8,9-HxCDD 6.83 (3.17–45.60) 7 44.45 (40.8–77.6) 4 16 (7.08–104) 11 – – 01,2,3,4,6,7,8-HpCDD 36.10 (7.31–436) 19 51.90 (23.7–244) 29 45 (13–590) 40 197 (90–233) 3OCDD 47.05 (12.30–1837) 18 87 (37.20–425) 27 152 (22.1–1281) 40 368 (220–1432) 32,3,7,8-TCDF 11.63 (1.84–45.80) 12 248 (22.5–1314) 38 18 (5.36–56) 35 1119 (70–5607) 41,2,3,7,8-PeCDF 6.52 (2.13–20.70) 3 53.70 (17.8–153) 30 13 (3.04–27.5) 15 280 (20–668) 32,3,4,7,8-PeCDF 16.85 (5.92–360) 18 183.5 (24.4–863) 36 22 (6.72–69.8) 35 267.5 (90–1827) 41,2,3,4,7,8-HxCDF 12 (3.41–196) 14 43.45 (16.5–306) 24 21 (4.9–63.3) 34 176 (165–187) 21,2,3,6,7,8-HxCDF 6.19 (2.60–115) 14 37.30 (10.9–98.4) 22 12 (4.75–41.02) 27 154.5 (142–167) 22,3,4,6,7,8-HxCDF 0 0 0 33.10 (22–38.1) 3 5 5 1 – – 01,2,3,7,8,9-HxCDF 5.03 (2.67–82) 11 56.50 (11.5–203) 18 10 (5.38–30.3) 20 218 (181–255) 21,2,3,4,6,7,8-HpCDF 9.92 (2.03–289) 17 30.70 (15.8–178) 22 25 (4.48–214) 37 155.5 (107–204) 21,2,3,4,7,8,9-HpCDF 2.17 (2.01–2.33) 2 31.90 (24.9–46.6) 3 14 (3.96–31.7) 5 – – 0OCDF 20.37 (4.75–317) 6 49.60 (10.1–169) 8 20 (8.56–199) 13 88.20 88 1

PCBs non-orthoPCB-77 153 (18.7–929) 19 8910 (136–90 570) 38 159 (33.7–888) 40 41 380 (141 100–66 740) 4PCB-81 26.40 (5.74–278) 13 665 (62.2–2543) 33 44.85 (15.6–241) 8 3810 (1300–4055) 3PCB-126 130 (45.1–1707) 18 7537 (183–34 400) 37 71.15 (13.7–1629) 36 23 460 (56 610–6889) 4PCB-169 25.75 (8.36–518) 18 1313 (67.9–7046) 35 61.60 (10.1–645) 22 3702 (610–15 310) 4

PCB mono-ortho3559 (1146–53 940) 19 15 490 (2116–1 537 000) 38 3484 (518–47 320) 40 1 368 000 (128 000–4 345 000) 4

PCB-114 280 (101–3775) 19 1 004 000 (141–81 140) 37 320 (52.1–2197) 40 62 950 (5860–350 200) 4PCB-118 12 340 (4485–115 300) 19 19 110 (6987–5 149 000) 38 13 170 (2122–110 300) 40 3 467 000 (328 000–9 383 000) 4PCB-123 133 (51.8–1512) 19 175 300 (123–137 800) 38 167 (23.5–2048) 38 42 040 (3680–1 540 000) 4PCB-156 1770 (626–74 000) 19 37 860 (222–774 700) 38 3682 (433–25 660) 40 383 600 (63 600–1 187 000) 4PCB-157 344 (122–6440) 19 111 100 (318–174 100) 38 717 (84–4705) 40 96 160 (14 900–337 800) 4PCB-167 779 (254–8655) 19 22 300 (661–486 700) 38 836 (154–7095) 40 220 400 (33 600–778 600) 4PCB-189 168 (48.4–13 620) 19 1 813 000 (115–200 700) 37 410 (45–3097) 40 37 640 (8880–96 680) 4

D: number of samples > LOD.

Fig. 1. PCDD/Fs and dl-PCBs profiles of a representative sample of dairy products and fish.

1256 S. Marin et al. / Chemosphere 82 (2011) 1253–1261

in terms of percentage from toxic equivalents, it is the most toxicPCB-126 (WHO-TEF = 0.1) and accounts for the highestcontribution.

In the market basket study carried out in Finland (Kivirantaet al., 2004), the most relevant congener, when concentrationswere considered, was OCDD accounting for 60%. However, consid-

ering toxic equivalents, the 2,3,4,7,8-PeCDF represents 65% of thetotal PCDD/F congeners. Likewise, the most relevant toxic contri-bution from dl-PCBs is provided by the PCB-126. The relevance ofthese two penta-PCDD/F congeners and the PCB-126 in the contri-bution to the total TEQ has also been stressed by other authors(Bordajandi et al., 2004; Arisawa et al., 2008; Fromme et al., 2009).

Fig. 2. Percentage of each PCDD/Fs and dl-PCBs congener, both as concentration and as TEQ, in the total diet basket studied.

S. Marin et al. / Chemosphere 82 (2011) 1253–1261 1257

3.2. Total TEQ in food groups

To asses the toxicity associated with the presence of PCDD/Fs anddl-PCBs in foodstuffs, the total TEQ values (sum of WHO-TEQ due toPCCD/Fs and PCBs) have been calculated for each food group.The groups presenting higher concentrations were fish oil(6.38 pg WHO-TEQ g�1 fat) and fish and fish products (average of1.21 pg WHO-TEQ g�1 w.w.). The average concentrations of the sixother food groups were vegetables (0.03 pg WHO-TEQ g�1 w.w.),cereals (0.06 pg WHO-TEQ g�1 w.w.), oils and fats (0.33 pg WHO-TEQ g�1 fat), meat (0.63 WHO-TEQ pg g�1 fat), eggs (0.75 WHO-TEQ pg g�1 fat) and dairy products (0.90 WHO-TEQ pg g�1 fat),(see Table 2). For a comparison of absolute values of contaminationacross the different groups, the basis on which results are expressedmust be taken into account. Table 3 shows the concentration ofdifferent food groups all expressed as pg WHO-TEQ g�1 w.w.

These levels are markedly lower than the mean levels reportedby European Food Safety Authority (EFSA) in a recent published re-port on samples collected during 1999–2008 from 19 EU MemberStates (European Food Safety Authority (EFSA), 2010). However, itcould be said that a proportion of samples in this report reflects notonly random monitoring but targeted monitoring, which providesa bias on the evaluation of background levels in Europe.

In a recent study carried out in France, (Tard et al., 2007) signif-icantly lower levels in fish oil were found (1.09 pg WHO-TEQ g�1 fat), mainly owing to the lower concentrations of PCBs,whereas the PCDD/Fs presented levels similar to those in our study.However, survey including 32 fish oil products carried out in the

Table 2Food groups specific median, mean and range (in pg WHO-TEQ g�1)a of PCDD/F + dl-PCBs,

PCDD/F + dl-PCBs PCDD

Median Mean Min–max Media

Vegetables� 0.03 0.04 0.02–0.10 0.03Cereals� 0.06 0.07 0.04–0.10 0.05Fats and oils 0.33 0.37 0.14–1.13 0.25Eggs 0.75 0.78 0.52–1.13 0.62Milk and dairy products 0.90 0.99 0.25–2.13 0.54Fish products� 1.21 1.55 0.08–5.48 0.21Meat and meat products 0.63 0.93 0.14–6.60 0.47Fish oils 6.38 6.55 0.60–12.82 0.74

a All food groups expressed on fat basis except the ones indicated by (�) expressed on

UK provides a similar median value of 5.7 ng WHO-TEQ kg�1 fat(Fernandes et al., 2006).

For fish and fish products, different authors have reported levelsin the same order of magnitude as our results (Tard et al., 2007)finding that fish and fish products appeared to be the most con-taminated food products with total mean concentrations rangingfrom 0.73 pg WHO-TEQ g�1 w.w. to 2.89 pg WHO-TEQ g�1 w.w.Levels slightly higher have been communicated in Finland (Kivi-ranta et al., 2004), whereas in Slovakia lower levels have beenfound (0.289 pg WHO-TEQ g�1 w.w) in fish samples collected fromshops (Chovancová et al., 2005).

Total TEQ values found in milk and dairy products ranged from0.25 pg WHO-TEQ g�1 fat to 2.13 pg WHO-TEQ g�1 fat. Concentra-tions in the same range were reported in recent studies conductedin other countries such as, France (Tard et al., 2007) and Belgium(Bilau et al., 2008). However, higher levels have been found inhomemade milk and butter in a monitoring study performed inSlovakia (Chovancová et al., 2005).

Also higher levels (3.06 pg WHO-TEQ g�1 fat) have been re-ported recently in a monitoring plan performed in Campania, Italy,including 79 cow milk samples (Esposito et al., 2009).

Total TEQ concentrations in meat and meat products rangedfrom 0.14 pg WHO-TEQ g�1 fat to 6.60 pg WHO-TEQ g�1 fat. Otherauthors have reported similar levels of dioxins for this food cate-gory (Tard et al., 2007). On the other hand, Hsu et al. (2007) havefound average levels of dl-PCBs and PCDD/Fs in some meat samplessuch as chicken (0.40 pg WHO-TEQ g�1 fat and 0.72 pg WHO-TEQ g�1 fat, respectively) or beef (0.36 pg WHO-TEQ g�1 fat and

PCCD/F and dl-PCBs.

/Fs dl-PCBs

n Mean Min–max Median Mean Min–max

0.04 0.02–0.09 0.005 0.01 0.002–0.010.06 0.03–0.09 0.01 0.01 0.01–0.010.26 0.11–0.43 0.05 0.12 0.02–0.700.64 0.42–1.05 0.14 0.14 0.05–0.270.60 0.23–1.23 0.36 0.39 0.02–0.970.28 0.06–0.78 0.97 1.27 0.01–4.700.69 0.11–5.88 0.14 0.24 0.03–2.131.22 0.14–3.27 4.59 5.32 0.32–11.80

wet weight.

Tabl

e3

Esti

mat

ion

ofth

ePC

DD

/F+

dl-P

CBs

diet

ary

inta

keth

roug

hdi

ffer

ent

food

sst

udie

dba

sed

onth

em

edia

nco

ncen

trat

ions

foun

d.

Occ

urr

ence

(pg

WH

O-

TEQ

g�1

ww

)C

onsu

mpt

ion

(gkg�

1b.

wd�

1)

Dai

lyin

take

(upp

erbo

un

d)(p

gW

HO

-TEQ

kg�

1b.

wd�

1)

Dai

lyin

take

(low

erbo

un

d)(p

gW

HO

-TEQ

kg�

1b.

wd�

1)

Med

ian

Adu

lts

Ch

ildr

enA

dult

sC

hil

dren

Food

grou

pU

pper

bou

nd

ND

=LO

DLo

wer

bou

nd

ND

=0

Adu

lts

Ch

ildr

enpg

WH

O-T

EQ(k

g�1

b.w

d�1)

% Con

trib

uti

onpg

WH

O-T

EQ(k

g�1

b.w

d�1)

% Con

trib

uti

onpg

WH

O-T

EQ(k

g�1

b.w

d�1)

% Con

trib

uti

onpg

WH

O-T

EQ(k

g�1

b.w

d�1)

% Con

trib

uti

on

Veg

etab

les

0.03

0.01

6.76

9.27

0.22

7.69

0.31

6.77

0.07

3.35

0.20

5.22

Cer

eals

0.06

0.03

2.67

5.21

0.16

5.59

0.31

6.77

0.08

3.83

0.24

6.27

Fats

and

oils

0.33

0.07

0.79

1.55

0.26

9.09

0.51

11.1

40.

052.

390.

287.

31Eg

gs0.

070.

040.

460.

720.

031.

050.

051.

090.

020.

960.

041.

04M

ilk

and

dair

ypr

odu

cts

0.06

0.03

5.33

12.9

70.

3411

.89

0.83

18.1

20.

157.

180.

6115

.93

Fish

prod

uct

s1.

211.

151.

411.

911.

7059

.44

2.30

50.2

21.

6277

.51

2.26

59.0

1M

eat

and

mea

tpr

odu

cts

0.06

0.04

2.47

4.58

0.15

5.24

0.27

5.90

0.10

4.78

0.21

5.48

Tota

l1.

821.

3619

.89

36.2

12.

8610

0.00

4.58

100.

002.

0910

0.00

3.83

100.

00

1258 S. Marin et al. / Chemosphere 82 (2011) 1253–1261

0.96 pg WHO-TEQ g�1 fat, respectively) higher than the average wefound for the samples included in this group.

In the present study 22 samples of commercial eggs from retailwere analysed, and all of them present levels much lower than themaximum limit established by the European Union of 6.0 pg WHO-TEQ g�1 fat. The average levels (0.75 pg WHO-TEQ g�1 fat) werecomparable to the concentrations from other studies (De Mulet al., 2008). However, Chovancová et al. (2005) reported mean lev-els of 2.24 pg WHO-TEQ g�1 fat in eggs from retailers, and levels upto ten times higher than the EU limit were found in free-range eggsfrom small private farms. Higher concentrations than those of ourstudy have also been observed recently by Van Overmeire et al.(2009), with levels from 3.29 to 95.35 pg WHO-TEQ g�1 fat in au-tumn and from 1.50 to 64.79 pg WHO-TEQ g�1 fat in spring inhome-produced eggs from Belgium.

TEQ concentrations of PCDD/Fs and PCDD/F-PCB in fats and veg-etable oils samples were much lower than the regulation limit val-ues set by the EU. The average concentrations found were0.05 pg WHO-TEQ g�1 fat and 0.25 pg WHO-TEQ g�1 fat for dl-PCBsand PCDD/F, respectively. Similar levels were found for PCDD/F inoil (0.28 pg WHO-TEQ g�1 fat) and margarine (0.43 pg WHO-TEQ g�1 fat) by Bocio and Domingo (2005) in samples from Spain.

The observed levels for vegetables and cereals were the lowest ofall food groups, with average PCDD/F-WHO-TEQ concentrationsof 0.03 pg WHO-TEQ g�1 w.w. for vegetables and 0.05 pg WHO-TEQ g�1 w.w. for cereals, and median PCBs-WHO-TEQ of0.005 pg WHO-TEQ g�1 w.w. for vegetables and 0.01 pg WHO-TEQ g�1 w.w. for cereals. These low levels are obviously related withthe low fat content of these products.

Other studies in recent years have also indicated the lowest lev-els in vegetables, fruits and cereals, measured by the concentrationsof PCDD/Fs in 18 major kind of foods from supermarkets and tradi-tional markets in Taiwan (Wang et al., 2009). The fruits, cereals andvegetables showed the lowest levels with average concentrations of,0.0011 pg WHO-TEQ g�1 w.w., 0.0166 pg WHO-TEQ g�1 w.w and0.0256 pg WHO-TEQ g�1 w.w. Likewise, Zhang et al. (2008) havefound lows levels for vegetables (0.0093 pg WHO-TEQ g�1 w.w.)and cereals (0.022 pg WHO-TEQ g�1 w.w.) in China. Bilau et al.(2008) measured dioxin- like compounds via CALUX bioassay insamples available on the Flemish market. Levels for fruits and vege-tables were below the limit of quantification. For cereals the levelsreported were 0.3 pg CALUX-TEQ g�1 product for PCDD/F and0.6 pg CALUX-TEQ g�1 product for dl-PCBs. These relatively highervalues for cereals could be linked with the analytical methodology.In fact, CALUX provides an estimate of the TEQ levels in the sampleexpressed as Bioanalytical Equivalents (BEQ), but a correction by theapparent recovery needs to be done.

As has been emphasized by different authors, an important dif-ference is the ratio between PCDD/Fs and dl-PCBs in aquatic andland-based products. As can be seen in Table 2, the contributionof PCDDs/Fs to the total TEQ is higher than that of PCBs for all foodgroups, except for fish products and fish oil. The dl-PCBs accountfor more than 80% of total TEQ in aquatic products, whereas forthe terrestrial ones its contribution ranges from 27% to 40%.

This elevated contribution of PCBs in fish products has also beenfound by Bordajandi et al. (2004), who reported contributionshigher than 70% (except for canned samples). However, contraryto our results, these authors reported that in dairy samples andmeat products PCDD/Fs and PCBs have a similar contribution.Hsu et al. (2007) found dl-PCBs contributions to total WHO-TEQof 31%, 46% and 59% for meat products, milk and dairy productsand the muscle meat of fish, respectively. These differences couldbe linked with the different sources of exposure between aquatic(sediments (Kitamura et al., 2009)) and land-based products(atmospheric deposition (Hassanin et al., 2006)). The relevant con-tribution of dl-PCBs for the dietary intake estimation based on TEQ

S. Marin et al. / Chemosphere 82 (2011) 1253–1261 1259

has been recognized by the European Union in establishing maxi-mum levels not only for PCDD/Fs but also for the sum of PCDD/Fs and dl-PCBs (European Commission, 2006b).

Except one sample of chicken (6.60 pg WHO-TEQ g�1 fat) andtwo samples of fish oil (11.99 pg WHO-TEQ g�1 fat and12.82 pg WHO-TEQ g�1 fat), the samples analyzed present concen-trations of PCDD/Fs and dl-PCBs below the EU maximum levels.Likewise, all vegetables and cereals, eggs, and milk and milk prod-ucts, showed concentrations lower than the actions levels set byRecommendation 2006/88/EC in order to stimulate a proactive ap-proach to reduce the presence of dioxins in food and feed (Euro-pean Commission, 2006a). This means that low contaminationcould be found nowadays in the food chain, and confirms the gen-eral reduction of the food concentrations of PCDD/Fs and dl-PCBsobserved in recent studies such as those conducted by Llobetet al. (2008) and Windal et al. (2010). This is coherent with a con-tinued decline observed in the emissions and atmospheric concen-trations of PCDD/Fs and dl-PCBs (Hassanin et al., 2006), thedecrease in concentrations in biota (Munschy et al., 2008), sedi-ments (Marvin et al., 2007) and breast milk (Schuhmacher et al.,2009), which was presumably due to enforcing legislation to re-duce exposure to dioxins, phasing out of PCBs, and implementationof control measures.

3.3. Estimate of dietary exposure to PCDD/Fs and dl-PCBs

Although this monitoring study has been designed mainly toasses contamination levels of PCDD/Fs and dl-PCBs in the majorfood groups, and to evaluate if the levels found are in accordancewith those established by the EU legislation, the results could also

Table 4Overview of the dietary intake (adults) of PCDD/F and dl-PCBs from studies published bet

Country (samplingyear)

Dietary intake(pgTEQ kg�1

b.w d�1)

Main productscontributing

Dietary data

The Netherlands(2001–2005)

0.8 Dairy, 38%; vegetableoils, 17%; meat, 17%;fish, 12%

Dietary record (individuover two consecutive d

Belgium (2008) 0.72 Dairy, 50%; fish, 22%;meat, 18%

24-h recall and FFQ

Spain (2006) 1.12 Fish, 58%; meat, 6.2%;vegetables, 2.5%

Regional survey

Taiwan (–) 0.53 (PCDD/Fonly)

Meat, 32%; Seafood,26%; dairy, 13%

24-h recall

France (2001–2004)

1.8 Seafood, 48%, dairy, 31;meat, 8%

Dietary record (over seconsecutive days)

Swedish (1998–2004)

1.5 Fish, 75%; dairy, 10%;meat, 5% (children, 1–24 years)

Household purchase andietary record (one we

Flanders (2003–2006)

1.74 Fish, 43%; added fats,22%; dairy, 17%; meat,13%

FFQ

Taiwan (2003) 1.5 Fish, 49%; meat, 20;fats and oils, 19

National survey (databanutritional ingredients)

Italy 2.28 Fish, 44%; dairy,27%;cereals, 9%

Dietary record (self-comdiary over 3–7 days)

Japan (2002–2006)

1.06 (�) Dietary record (consumconsecutive days)

China (2004–2006)

1.36 Fish, 44%; Livestock,19%; poultry, 12%

Regional survey

Spain (2006–2008)

2.86 Fish, 59%; dairy, 12%;fat and oils, 9%;vegetables, 8%; cereal,6%; meat, 5%; eggs, 1%.

National survey

NDA: Non detected approach; lb: lowerbound; mb: middlebound; ub: upperbound, FFQanalogous; TDS: Total Diet Study.�Fish, dairy products, vegetables, and seasonings and beverages positively correlated wi

be used to perform an approximate estimation of the average dailyintake of the population of the Region of Valencia.

The average estimated daily intake of the sum of PCDD/Fs anddl-PCBs (upper bound concentration) for a male adult of 68.5 kgbody weight was 2.86 pg WHO-TEQ kg�1 b.w. d�1, based on theTEFs from 1998 (see Table 3). This is considerably higher thanthe value of 1.12 pg WHO-TEQ kg�1 b.w. d�1estimated by Llobetet al. (2008) and slightly higher than the 2.63 pg WHO-TEQ kg�1 b.w. d�1 estimated by Bordajandi et al. (2004). It mustbe said that these three Spanish studies used quite different ap-proaches. Although all three utilize a deterministic assessment,the consumption data are from different sources. Besides, Bordaj-andi et al. (2004) analyze individual samples and uses the upperbound approach for TEQ calculations based on TEFs from 1998,whereas Llobet et al.(2008) measured the contaminants in com-posite samples, using the middle bound approach and 2005WHO-TEFs. Also, the food products collected within each foodgroup are not the same.

Likewise, it is complicated to compare the results of intake esti-mations between countries because there are important methodo-logical variances. There are differences in collection methods andthe number of foods analysed, as well as differences in the meansto study food consumption. Also, the LOD of the analytical meth-ods, the use of upper, middle o lower bound approaches or the TEFsutilized are other significant differences. Table 4 shows the averageestimated intake reported in some recent studies in different coun-tries, and also points out some methodological differences betweenthem. Our results (2.86 pg WHO-TEQ kg�1 b.w. d�1) were some-what higher than the maximum estimate intake in these studies,which were between 0.72 pg WHO-TEQ kg�1 b.w. d�1and 2.28 pgWHO-TEQ kg�1 b.w. d�1). Moreover, Arisawa et al. (2008) have

ween 2005 and 2010.

Study/Sampling-analysis

Dietary exposure model(51) (Lambe, 2002)

WHO-TEFs /NDA

Reference

al dataays)

MP and MB/Composite samples

Simple distribution(long-termconsumption)

2005/lb De Mulet al. (2008)

TDS/Compositesamples

Probabilistic 1998/mb

Windalet al. (2010)

MB/Compositesamples

Deterministic (pointestimates)

2005/mb

Llobet et al.(2008)

MB/Individual foodsamples

Deterministic (pointestimates)

2005/mb

Wang et al.(2009)

ven MP/Individual foodsamples

Deterministic (pointestimates)

1998/lb Tard et al.(2007)

dek)

MB and MP /Individual foodsamples

Deterministic (pointestimates)

1998/mb

Bergkvistet al. (2008)

MP/Individual foodsamples

Simple distribution Calux-TEQ

Bilau et al.(2008)

se of TDS/Compositesamples

Deterministic (pointestimates)

1998/ub Hsu et al.(2007)

piled Database Probabilistic 1998/ub Fattoreet al. (2006)

ption 3 Duplicate portions – 1998/lb Arisawaet al. (2008)

MB/Individual foodsamples

Deterministic (pointestimates)

1998/mb

Zhang et al.(2008)

MP/Individual foodsamples

Deterministic (pointestimates)

1998/ub Presentstudy

: food frequency questionnaire; MP: Monitoring Program; MB: Market Basket and

th total dioxins intake.

1260 S. Marin et al. / Chemosphere 82 (2011) 1253–1261

analyzed studies carried out in Europe, the USA, Taiwan and Japanand published between 1993–2007, and had established a range ofaverage intake between 0.33 pg WHO-TEQ kg�1 b.w. d�1 and3.57 pg WHO-TEQ kg�1 b.w. d�1. Our results are near the higherend of this range. All this means that apart from methodologicaldifferences, the comparatively high average intakes found in ourregion would be linked to a specific pattern of food intake andoccurrence of dioxins in the food products.

The present study shows that 1.69 pg WHO-TEQ kg�1 b.w. d�1

(59%) of the average total dietary exposure for an adult is due todl-PCBs, and 1.17 pg WHO-TEQ kg�1 b.w. d�1 corresponds toPCDD/Fs. The latter contribution is slightly higher than the0.91 pg WHO-TEQ kg�1 b.w. d�1 (1998 TEFs) found in our previousstudy carried out during 2004–2005 (Montaña et al., 2005).

Fish products were the main source, with nearly 60% of the die-tary intake of PCDD/Fs and dl-PCBs. Contributions of dairy prod-ucts, vegetables, oils and fats, and cereals, were much lower,accounting from 6% to 12% (see Table 3).

Others recently published studies have also emphasized the rel-evance of fish to the intake of PCDD/Fs and dl-PCBs (see Table 4).However, in the studies conducted in The Netherland (De Mulet al., 2008), and in Belgium (Windal et al., 2010), dairy productsappear to be the main source with a contribution of 38% and50%, respectively; while meat and meat products is the more rele-vant food group in the recent study carried out in Taiwan (Wanget al., 2009).

The toxicity of dioxins is related to the amount accumulated inthe body during a lifetime, the so-called body burden. Therefore,some toxicological reference intakes are established to ensure thatpeople are not exceeding a maximum body burden. A tolerableweekly intake (TWI) of 14 pg WHO-TEQ kg�1 b.w. has been estab-lished by the Scientific Committee on Food (Scientific Committeeon Food (SCF), 2001). Likewise, Joint FAO/WHO Expert Committeeon Food Additives (JECFA) (2002) set up a provisional tolerablemonthly intake (PTMI) of 70 pg WHO-TEQ kg�1 b.w. month�1

while WHO has stated a tolerable daily intake (TDI) of 1–4 pg WHO-TEQ kg�1 b.w. d�1 (World Health Organization (WHO),2000). In the present study, the average daily intake for adults(2.86 pg WHO-TEQ kg�1 b.w. d�1) is within range of the TDI recom-mended by the WHO (1–4 pg WHO-TEQ kg�1 b.w. d�1), andslightly above the TWI and PTMI adopted by SCF and JECFA respec-tively. However, if lowerbound approach is used, the estimateddaily intake (2.09 pg WHO-TEQ kg�1 b.w. d�1) is below the lattertoxicological reference.

For children (7–12 years), the mean daily intake is4.58 pg WHO-TEQ kg�1 b.w. d�1 using upperbound approach, and3.83 pg WHO-TEQ kg�1 b.w. d�1 with lowerbound. This higher in-take in children is partly due to the difference in food intake, butmainly to their relative body weight (see Table 3).

These results of estimate intakes above some toxicological ref-erence dose have to be interpreted cautiously when we are think-ing in terms of the risk for the population because the estimateintakes are point estimates whereas reference limits are definedfor life-long intake. Nevertheless, this estimated dietary intake isvery useful for temporal trend analysis. It would be prudent to re-duce the dioxin intake for those parts of the population with higherintakes of dioxins following the Dioxin Strategy implemented bythe EU.

Acknowledgments

This study was performed under the supervision of the GeneralDirection of Public Health of the Health Department of ValenciaGovernment. However, the views expressed in this paper do notnecessarily reflect the positions or policies of this HealthDepartment.

The authors are grateful to all inspectors from the Public HealthDepartment of Valencia Regional Government who participated inthe monitoring programme. They also thank the technicians of theEnvironmental Laboratory, Institut Quimic de Sarria.

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.chemosphere.2010.12.033.

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