- Email: [email protected]
Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in milk from Italian women living in Rome and Venice
Chemosphere 67 (2007) S301–S306 www.elsevier.com/locate/chemosphere
Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in milk from Italian women living in Rome and Venice Anna Maria Ingelido a,*, Terri Ballard b, Elena Dellatte a, Alessandro di Domenico a, Fabiola Ferri a, Anna Rita Fulgenzi a, Thomas Herrmann c, Nicola Iacovella a, Roberto Miniero a, Olaf Pa¨pke c, Maria Grazia Porpora d, Elena De Felip a a
Toxicological Chemistry Unit, Department of the Environment and Primary Prevention, Istituto Superiore di Sanita´, 00161 Rome, Italy b Food and Agricultural Organization, 00100 Rome, Italy c ERGO Forschungsgesellschaft mbH, 22305 Hamburg, Germany d Institute of Gynecological Sciences, Perinatology and Child Health, University ‘‘La Sapienza’’, 00161 Rome, Italy Accepted 26 May 2006 Available online 25 January 2007
Abstract The levels of selected polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) were measured in human milk samples from the areas of Venice and Rome, primarily in order to characterize the current levels of infant exposure to PCBs and PBDEs due to breast feeding in Italy. Sixteen non-dioxin-like PCBs, including the traditional indicator congeners, and 11 PBDEs, comprising the relevant PBDE-47, PBDE-99, and PBDE-153, were determined. Congeners were selected for analysis according to their relative abundance in human tissues, toxicological relevance, and diffusion in the environment. Dietary habits of the milk donors were recorded by questionnaires; mothers of the Venice area were classified into three groups according to their consumption of local fish, molluscs, and other fishery products. R16(PCBs) and R11(PBDEs) (ng g1 fat) for the areas of Venice and Rome were respectively, 250–390 and 240, and 1.6–2.8 and 4.1. An increase of fish and fishery product consumption could not be associated with an increase of PCB and PBDE levels in milk. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Breast milk; Fish consumption; Infant exposure; Organohalogenated contaminants; Polychlorinated biphenyls; Polybrominated diphenyl ethers
1. Introduction Human milk is the major route of excretion of persistent lipophilic chemicals — e.g., polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) — for lactating women and the major source of exposure to these substances for breast-fed infants (WHO, 1992; Lakind et al., 2000; Chao et al., 2004; Barr et al., 2004). *
Corresponding author. E-mail addresses: [email protected] (A.M. Ingelido), [email protected] (A. di Domenico). 0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.05.111
Perinatal exposure to PCBs and PBDEs occurs prenatally via the placenta and postnatally via breast milk. Although in humans it is difficult to distinguish between exposure of offspring by transplacental or by breast milk transfer, both human and animal data from different species indicate that accumulation of highly persistent chemicals ingested via milk far exceeds the contribution from maternal-foetal transfer (Gallenberg and Vodicnik, 1987; Eriksson et al., 2001). Furthermore, it has been shown that levels in breast milk reflect maternal body burden during pregnancy and are a dose-metric of prenatal exposure to the substances of interest. Accordingly, human milk constitutes a suitable
S302
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
matrix to examine potential perinatal exposures for breastfeeding infants and breast milk monitoring studies are of primary importance to carry out an adequate risk assessment at the actual levels of exposure. PCBs are environmental contaminants widely used in the western world for over 40 years since the 1930s. The toxicological risk associated to their perinatal exposure, including neurodevelopmental and immunological effects, has extensively been reviewed (WHO, 1992; Huisman et al., 1995; Chao et al., 2004; Weisglas-Kuperus et al., 2004). Unlike PCBs, PBDEs are still currently produced and used in large amounts worldwide primarily as flame retardants; starting with the 1980s, their occurrence in biota and the environment has been repeatedly reported (WHO, 1994; de Wit, 2002; Law et al., 2003; Hites, 2004). Increasing concern on their potential effects on neurobehavioral development in children caused by perinatal exposure has prompted a number of regulatory actions aimed at reducing maternal body burden. In fact, in spite of a still incomplete congener-specific toxicological characterization, many experimental studies consistently reported neurotoxic effects following perinatal exposure to PBDEs (Eriksson et al., 2001; Branchi et al., 2002). In order to characterize the current levels of infant exposure to PCBs and PBDEs in Italy due to breast feeding, milk from mothers of the general population of Rome and Venice and their surroundings was analyzed (di Domenico et al., 2002; Ingelido et al., 2004). In this latter case, an assessment of PCB and PBDE levels was carried out as a function of maternal fish consumption, remarkably higher than the national mean value in some subgroups of the local
population. In addition, to provide examples of the specific PCB and PBDE profiles detectable in the Venice lagoon, the outcome of analyses carried out on samples of edible benthonic molluscs — such as clams (Tapes sp.) and common cockles (Cardium edule) — has here been reported. Clams were obtained from a lagoon area under a moderate industrial impact, whereas cockles came from a fishing zone not directly exposed; both molluscs were collected during milk sampling (di Domenico et al., 2002, 2005). 2. Materials and methods 2.1. Sampling Milk samples were collected with a breast-pump into a glass container between weeks four and eight after delivery and stored at 20 °C until analysis. Mothers’ characteristics are reported in Table 1. Lactating mothers from the area of Rome (one group or pool, 10 donors) were enrolled in the period from January 2000 to July 2001. Mothers from Venice and its surroundings (three groups or pools differing in fish consumption level as follows: low consumption (LC), 10 donors; medium consumption (MC), 13 donors; high consumption (HC), six donors) were enrolled in the period from April 1998 to October 2000. Age distribution of mothers enrolled in all groups was 21–40 years. Data on dietary habits and lifestyle were obtained by questionnaires. Except for an excess fish consumption of the HC group, dietary habits of all subjects were substantially representative of the mean Italian diet (di Domenico et al., 2002; Ingelido et al., 2004).
Table 1 General informations on human milk donorsa Parameter
Groups of milk donor (Pools) Venice (LC)
Venice (MC)
Venice (HC)
Rome
Geographic areab Sampling date (month.year) Number of donors in the pool Age, mean (years) Age, range (years) Height, mean (cm) Height, range (cm) Body mass index, mean (before pregnancy) Body mass index, range (before pregnancy) Weight increase during pregnancy, mean (kg) Weight increase during pregnancy, range (kg) Residence area in last five years (fraction of donors in the pool)c Residence area in previous years (fraction of donors in the pool)c Smoking habits (fraction of donors in the pool)d
Venice 9.1998–7.2000 10 31 24–38 165 158–175 22.6 19.5–35.6 12.7 10–17 U, 80%; S, 20%
Venice 4.1998–10.2000 13 30 21–38 166 156–178 21.4 16.9–24.8 13.2 8.5–25.5 U, 85%; S, 15%
Venice 3.1999–7.2000 6 27 21–29 161 154–170 20.3 18.8–22.4 13.5 7–19 U, 50%; S, 50%
Rome 1.2000–7.2001 10 34 28–40 164 150–173 22.0 19.7–26.7 11.8 9–15 U, 100%
U, 80%; S, 20%
U, 85%; S, 15%
U, 89%; S, 11%
NS, 60%; FS, 30%; S, 10% 2.6%
NS, 77%; FS, 23% 3.1%
U, 33%; S, 50%; NA, 17% NS, 100%
Extracted lipids in pooled milk a
2.7%
NS, 67%; FS, 22%; S, 11% 2.9%
No donor with occupational exposure to PCBs or PBDEs. For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b City and surroundings. c Urban (U), suburban (S), rural (R). NA, not assessed. d Only cigarette smoke. Not smokers (NS), former smokers (FS), smokers (S).
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
2.2. Analysis For a given donors’ group, the milk pool was obtained by mixing the same quantity of milk from each donor. Portions (0.2–0.5 l) of the pooled samples were added with 13Clabelled standards, allowed to rest for hours, and subjected to a liquid–liquid extraction with ethyl ether and n-hexane to remove the lipid fractions. The latter were gravimetrically determined. Each lipid fraction was divided into portions for the determination of different groups of analytes. Clean-up was carried out by supercritical fluid extraction (SFE) followed by elution on silica gel for PCB analysis (Bayarri et al., 2001; di Domenico et al., 2002) and by a multi-step procedure for PBDE analysis (Pa¨pke et al., 2001). Quantitative determination was performed by highresolution gas chromatography coupled with low-resolution mass spectrometry (HRGC-LRMS) used in the selected ion monitoring mode (SIM). HRGC-HRMS(SIM) was employed as a confirmatory technique. The analysis of biota was carried out by excising the edible parts from many specimens, thereafter pooled by species to obtain two fresh matrices of approximately 200 g each. Pools were washed, drained off to remove excess water, and added with 13C-labelled standards. Spiked matrices were homogenized and freeze-dried. Gram amounts of the freeze-dried materials were subjected to extraction, cleanup, and HRGC-LRMS(SIM) and -HRMS(SIM) quantification procedures as previously reported (di Domenico et al., 1998; Bayarri et al., 2001). The PCB and PBDE congeners selected for assessment were, respectively: PCB-28, PCB-52, PCB-101, PCB-122, PCB-124, PCB-128, PCB-138, PCB-141, PCB-153, PCB170, PCB-180, PCB-183, PCB-187, PCB-194, PCB-206, and PCB-209; PBDE-17, PBDE-28, PBDE-47, PBDE-66, PBDE-99, PBDE-100, PBDE-138, PBDE-153, PBDE154, and PBDE-183. 3. Results and discussion Results of the congener-specific determinations of PCBs in human milk pooled samples are shown in Table 2. The sums of the concentrations of the 16 selected PCB congeners, R16(PCBs), estimated for Venice (LC, MC, and HC) and Rome are respectively, 390, 370, 250, and 240 ng g1 fat. Taking into account the analytical uncertainty, R16(PCBs) appears to be substantially the same for the LC and MC groups, whereas it is visibly lower at the highest fish consumption (HC group); the same pattern can be observed for most congeners. As visible in Fig. 1, the congener profiles of the four human milk samples do not exhibit significant differences. As expected, PCB-138, PCB-153, and PCB-180 are the most abundant congeners with the following concentration order: PCB-153 > PCB-138 > PCB180. Congener profiles of the two biota samples are consistent with human milk profiles as to the congeners with six chlorines or more, such as PCB-138, PCB-153, and PCB-180. However, the lower chlorinated congeners
S303
Table 2 Selected PCB congener concentrations (ng g1 fat) and distribution in human milk sample pools from Venice and Romea PCB
Venice (LC)
Venice (MC)
Venice (HC)
Rome
PCB-28 PCB-52 PCB-101 PCB-122 PCB-124 PCB-128 PCB-138 PCB-141 PCB-153 PCB-170 PCB-180 PCB-183 PCB-187 PCB-194 PCB-206 PCB-209 R16(PCBs)c
3.5 0.20 0.54 <0.07b <0.08 0.61 98 <0.4 120 38 96 9.5 18 8.9 0.74 0.37 390
6.2 0.33 1.1 <0.08 <0.09 <1 92 <0.8 130 30 76 9.2 20 6.5 0.70 0.50 370
2.1 0.26 0.91 <0.1 <0.1 <1 66 <0.9 87 20 48 6.3 13 3.9 0.46 0.28 250
3.5 0.26 0.59 <0.2 <0.2 0.66 58 <0.4 77 21 56 6.1 15 6.3 0.91 0.27 240
Values rounded off to two figures. a For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b The sign < indicates limit of quantification (LOQ). c Medium bound approach. Estimated analytical uncertainty (CV%),
PCB-28, PCB-52, and PCB-101 appear to be appreciably present in the molluscs analyzed but not in human milk. The difference between human and biota congener composition may well be a consequence of metabolism on PCB molecules with different number and distribution of chlorine substituents in the substratum (Borlakoglu and Walker, 1989). The R16(PCBs) values estimated for clams and common cockles are respectively, 640 and 430 ng g1 fat (5.4 and 3.5 ng g1 fresh weight). Results of the congener-specific determinations of PBDEs in human milk pooled samples are shown in Table 3. The sums of the concentrations of the 11 selected PBDE congeners, R11(PBDEs), estimated for Venice (LC, MC, and HC) and Rome are respectively, 2.8, 2.5, 1.6, and 4.1 ng g1 fat. Taking into account the analytical uncertainty, R11(PBDEs) appears to be substantially the same for the LC and MC groups, whereas it is visibly lower at the highest fish consumption (HC group). The combined concentrations of the three most abundant congeners PBDE-47, PBDE-99, and PBDE-153 range between 1.3 and 3.3 ng g1 fat: these values match those recently reported for some European countries, spanning from 1.5 to 5.3 ng/g fat (Strandman et al., 2000; Kalantzi et al., 2004) and on average in the order of 3 ng/g fat (Baumann et al., 2003; Meironyte´ Guvenius et al., 2003; Pirard et al., 2003; Thomsen et al., 2003). PBDE congener profiles are shown in Fig. 2. As observed in most studies on human milk (Strandman et al., 2000; Baumann et al., 2003; Meironyte´ Guvenius et al., 2003; Pirard et al., 2003; Thomsen et al., 2003; Kalantzi et al., 2004), in all our pools congeners PBDE-47,
S304
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
Fig. 1. Selected PCB congener profiles (normalized) in human milk sample pools from Venice (LC, MC, and HC) and Rome. For comparison, the corresponding profiles detected in clams and common cockles from the Venice lagoon are also shown. The concentrations of the predominant congener in each matrix are (matrix ID, PCB congener, ng g1 fat): LC, PCB-153, 120; MC, PCB-153, 130; HC, PCB-153, 87; Rome, PCB-153, 77; clams, PCB-138, 140; cockles, PCB-153, 120.
Table 3 Selected PBDE congener concentrations (ng g1 fat) and distribution in human milk sample pools from Venice and Romea PBDE
Venice (LC)
Venice (MC)
Venice (HC)
Rome
PBDE-17 PBDE-28 PBDE-47 PBDE-66 PBDE-85 PBDE-99 PBDE-100 PBDE-138 PBDE-153 PBDE-154 PBDE-183 R11(PBDEs)c
0.0038 0.065 1.5 0.015 0.035 0.41 0.28 <0.01 0.41 0.025 0.061 2.8
0.0042 0.064 0.90 0.037 0.045 0.51 0.19 0.020 0.47 0.047 0.19 2.5
<0.002b 0.036 0.55 <0.006 0.018 0.14 0.15 <0.01 0.60 0.020 0.050 1.6
0.0039 0.082 1.9 0.019 0.074 0.97 0.48 0.013 0.47 0.070 0.092 4.1
Values rounded off to two figures. a For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b The sign < indicates limit of quantification (LOQ). c Medium bound approach. Estimated analytical uncertainty (CV%),
PBDE-99, PBDE-100, and PBDE-153 are the most abundant, their sum accounting for over 80% of total concentration. It may be observed that, contrary to most congeners, PBDE-153 relative contribution progressively increases, to become the predominant congener in milk from the donors’ group at the highest level of fish consumption: this determines a contamination profile different from what is usually observed in human milk, with PBDE-47 standing out for its relative abundance. However, a pattern with
PBDE-153 as the predominant congener rather than PBDE-47 was recently observed in human milk samples from the Faroe Islands, a North Atlantic region with a diet traditionally based on seafood (Fa¨ngstro¨m et al., 2005). A PBDE-153 predominance was also occasionally noted in individual samples of milk, blood, and adipose tissue from the USA and The Netherlands (Schecter et al., 2003; She et al., 2004; Weiss et al., 2004). In our study, the apparent increase of PBDE-153 with increasing fish consumption do not totally reflect the congener profile found in benthonic molluscs, as the prevalent congeners in clams and cockles are respectively PBDE-99 and PBDE-47, with PBDE-153 levels being in the order of 15–20% of the PBDE-47 concentration. Similarly to PCBs, the PBDE patterns found in LC and Rome human milk pools seem to be in general agreement with the profile found in cockles; however, some relevant differences are visible with the PBDE profile detected in clams. The two biota samples are also characterized by different R11(PBDEs) values (40 and 15 ng g1 fat in clams and cockles, respectively). The biological differences between the two organisms and mostly between sampling sites might account for the sensible diversity in mollusc body burdens and profiles. Although a correlation between PBDE levels in lagoon biota and the body burden of local people was beyond the scope of our study, it is nevertheless of interest to highlight the presence of PBDEs in low trophic niches at levels comparable with those of several PCB congeners. The apparent absence of a positive correlation between PCB and PBDE cumulative and congener concentration levels and fish consumption in the human milk from the
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
S305
Fig. 2. Selected PBDE congener profiles (normalized) in human milk sample pools from Venice (LC, MC, and HC) and Rome. For comparison, the corresponding profiles detected in clams and common cockles from the Venice lagoon are also shown. The concentrations of the predominant congener in each matrix are (matrix ID, PBDE congener, ng g1 fat): LC, PBDE-47, 1.5; MC, PBDE-47, 0.90; HC, PBDE-153, 0.60; Rome, PBDE-47, 1.9; clams, PBDE-99, 18; cockles, PBDE-47, 5.2.
Venice area seems to be inconsistent with the results of other studies, that found increasing body burden of the aforesaid compounds with increasing fish consumption (Kostyniak et al., 1999; Stewart et al., 1999; Ohta et al., 2002); contrary to that, another work did not found any relationships (Lind et al., 2003). In our study, the absence of a positive correlation may be related to dietary habits of the milk donors (however, the most deviating outcome is associated with the HC pool, whose representativeness is limited due to the small number of donors). Questionnaires documented a diminished consumption of milk and related products among the three groups of donors from the Venice area with increasing fish consumption: dairy products are indeed recognized as a significant source of human dietary exposure to PCBs and PBDEs (Zuccato et al., 1999; Darnerud et al., 2001; EFSA, 2005). Furthermore, the levels of fish contamination (background levels) and the kind (chiefly lean fish) and amount of fish and fishery products consumed in the lagoon environment may also play a relevant role in determining the absence of a significant positive association between fish consumption and milk levels of PCBs and PBDEs. Acknowledgements The Authors wish to acknowledge Maria Pia Giammarinaro, Cristina Pedini, Francesca Salmistrari, Sandra Scantambulro, Sonia Smerghetto, Luigia Tagliapietre, and Angela Paterno for their kind assistance in milk sample collection. The worked described was co-financed by the Italian Ministry of the Environment (Rome) and the Isti-
tuto Superiore di Sanita` (Rome), Contract PR-27/IS ISS No. A-80 (1998–2005). References Barr, D.B., Wang, R.Y., Needham, L.L., 2004. Biologic monitoring of exposure to environmental chemicals throughout the life stages: requirements and issues for consideration for the national children’s study. Environmental Health Perspectives 113, 1083–1091. Baumann, B., Hijman, W., Van Beuzekom, S., Hoogerbrugge, R., Houweling, D., Zeilmaker, M., 2003. PBDEs in human milk from the Dutch 1998 monitoring programme. Organohalogen Compounds 61, 187–190. Bayarri, S., Turrio Baldassarri, L., Iacovella, N., Ferrara, F., di Domenico, A., 2001. PCDDs, PCDFs, PCBs, and DDE in edible marine species from the Adriatic sea. Chemosphere 43, 601–610. Borlakoglu, J.T., Walker, C.H., 1989. Comparative aspects of congener specific PCB metabolism. European Journal of Drug, Metabolism, and Pharmacokinetics 14, 127–131. Branchi, I., Alleva, E., Costa, L.G., 2002. Effects of perinatal exposure to a polybrominated diphenyl ether (PBDE 99) on mouse neurobehavioural development. Neurotoxicology 23, 375–384. Chao, H.R., Wang, S.L., Lee, C.C., Yu, H.Y., Lu, Y.K., Pa¨pke, O., 2004. Level of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs) in human milk and the input to infant body burden. Food and Chemical Toxicology 42, 1299–1308. Darnerud, P.O., Eriksen, G.S., Torkell, J., Larsen, P.B., Viluksela, M., 2001. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environmental Health Perspectives 109 (S1), 49–68. de Wit, C., 2002. An overview of brominated flame retardants in the environment. Chemosphere 46, 583–624. di Domenico, A., Turrio Baldassarri, L., Ziemacki, G., De Felip, E., Ferrari, G., La Rocca, C., Cardelli, M., Cedolini, G., Dalla Palma, M., Grassi, M., Roccabella, V., Volpi, F., Ferri, F., Iacovella, N., Rodriguez, F., D’Agostino, O., Sansoni, R., Settimo, G., 1998. Priority microcontaminants in biota samples from the Venice lagoon:
S306
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
a selection of concentration data and elements of risk analysis. Organohalogen Compounds 39, 199–204. di Domenico, A., Biagini, G., De Felip, E., Dellatte, E., Ferri, F., Ingelido, A.M., Miniero, R., 2002. Laguna Veneta — Scenari di rischio per la salute umana associati alla introduzione e alla presenza di microinquinanti chimici ad alto potenziale tossico (PR-27/IS) — Rapporto Finale — Sezione II. Sottoprogramma ‘‘Latte Umano’’. Report of the Istituto Superiore di Sanita` (Rome). di Domenico, A., De Felip, E., Dellatte, E., Ferri, F., Ingelido, A.M., Miniero, R., 2005. Laguna Veneta — Scenari di rischio per la salute umana associati alla introduzione e alla presenza di microinquinanti chimici ad alto potenziale tossico (PR-27/IS) — Rapporto Finale — Sezione V. Sottoprogramma ‘‘Biota’’. Report of the Istituto Superiore di Sanita` (Rome). EFSA, 2005. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the presence of nondioxin-like polychlorinated biphenyls (PCBs) in feed and food. The EFSA Journal 284, 1–137. Eriksson, P., Jakobsson, E., Fredriksson, A., 2001. Brominated flame retardants: a novel class of developmental neurotoxicants in our environment? Environmental Health and Perspectives 109, 903–908. ˚ ., 2005. A Fa¨ngstro¨m, B., Strid, A., Grandjean, P., Weihe, P., Bergman, A retrospective study of PBDEs and PCBs in human milk from the Faroe Islands. Environmental Health: A Global Access Science Source 4, 12. Gallenberg, L.A., Vodicnik, M.J., 1987. Transfer of persistent chemicals in milk. Drug Metabolism Review 21, 277–317. Hites, R.A., 2004. Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science and Technology 38, 945–956. Huisman, M., Koopman-Esseboom, C., Fidler, V., Hadders-Algra, M., van der Paauw, C.G., Tuinstra, L.G., Weisglas-Kuperus, N., Sauer, P.J., Touwen, B.C., Boersma, E.R., 1995. Perinatal exposure to polychlorinated biphenyls and dioxins and its effect on neonatal neurological development. Early Human Development 42, 111–127. Ingelido, A.M., Ballard, T., De Felip, E., Dellatte, E., Ferri, F., Fulgenzi, A.R., Herrmann, T., Iacovella, N., Miniero, R., Pa¨pke, O., Porpora, M.G., di Domenico, A., 2004. Levels of polybrominated diphenyl ethers in milk from Italian women living in Rome and Venice. Organohalogen Compounds 66, 2722–2727. Kalantzi, O.I., Alcock, R.E., Martin, F.L., Thomas, G.O., Jones, K.C., 2004. Polybrominated diphenyl ethers (PBDEs) and selected organochlorines in human breast milk samples from the United Kingdom. Organohalogen Compounds 61, 9–12. Kostyniak, P.J., Stinson, C., Greizerstein, H.B., Vena, J., Buck, G., Mendola, P., 1999. Relation of lake Ontario fish consumption, lifetime lactation, and parity to breast milk polychlorobiphenyl and pesticide concentrations. Environmental Research Section A 80, S166–S174. LaKind, J.S., Berlin, C.M., Park, C.N., Naiman, D.Q., Gudka, N.J., 2000. Methodology for characterizing distributions of incremental body burdens of 2,3,7,8-TCDD and DDE from breast milk in North American nursing infants. Journal of Toxicology Environment and Health A 59, 605–639. Law, R.J., Alaee, M., Allchin, C.R., Boon, J.P., Lebeuf, M., Lepom, P., Stern, G.A., 2003. Levels and trends of polybrominated diphenylethers and other brominated flame retardants in wildlife. Environment International 29, 757–770.
Lind, Y., Darnerud, P.O., Atuma, S., Aune, M., Becker, W., Bjerselius, R., Cnattingius, S., Glynn, A., 2003. Polybrominated diphenyl ethers in breast milk from Uppsala Country, Sweden. Environmental Research 93, 186–194. ˚, Meironyte´ Guvenius, D., Aronsson, A., Ekman-Ordebrg, G., Bergman, A Nore´n, K., 2003. Human prenatal and postnatal exposure to polybrominated diphenyl ethers, polychlorinated biphenyls, polychlorobiphenylols, and pentachlorophenol. Environmental Health and Perspectives 111, 1235–1241. Ohta, S., Ishizuka, D., Nishimura, H., Nakao, T., Aozasa, O., Shimidzu, Y., Ochiai, F., Kida, T., Nishi, M., Miyata, H., 2002. Comparison of polybrominated diphenyl ethers in fish, vegetables, and meats and levels in human milk of nursing women in Japan. Chemosphere 46, 689–696. Pa¨pke, O., Bathe, L., Bergman, A., Fu¨rst, P., Meyronyte´ Guvenius, D., Hermann, T., Nore´n, K., 2001. Determination of PBDEs in human milk from the United States — Comparison of results from three laboratories. Organohalogen Compounds 52, 197–200. Pirard, C., De Pauw, E., Focant, J.-F., 2003. Levels of selected PBDEs and PCBs in Belgian human milk. Organohalogen Compounds 64, 158–161. Schecter, A., Pavuk, M., Pa¨pke, O., Ryan, J.J., Birnbaum, L., Rosen, R., 2003. Polybrominated diphenyl ethers (PBDEs) in U.S. mothers’ milk. Environmental Health Perspectives 111, 1723–1729. She, J., Holden, A., Sharp, M., Tanner, M., Williams-Derry, C., Hooper, K., 2004. Unusual pattern of polybrominated biphenyl Ethers (PBDEs) in US breast milk. Organohalogen Compounds 66, 3945– 3950. Stewart, P., Darvill, T., Lonky, E., Reihman, J., Pagano, J., Bush, B., 1999. Assessment of prenatal exposure to PCBs from maternal consumption of great lakes fish: an analysis of PCB pattern and concentration. Environmental Research Section A 80, S87–S96. Strandman, T., Koistinen, J., Vartiainen, T., 2000. Polybrominated diphenyl ethers (PBDEs) in placenta and human milk. Organohalogen Compounds 47, 61–64. Thomsen, C., Frøshaug, M., Leknes, H., Becher, G., 2003. Brominated flame retardants in breast milk from Norway. Organohalogen Compounds 64, 33–36. Weisglas-Kuperus, N., Vreugdenhil, H.J.I., Mulder, P.G.H., 2004. Immunological effects of environmental exposure to polychlorinated biphenyls and dioxins in Dutch school children. Toxicology Letters 149, 281–285. Weiss, J.; Meijer, L.; Sauer, P.; Linderholm, L.; Athanassiadis, I.; ˚ , 2004. PBDE and HBCDD levels in blood from Dutch Bergman, A mothers and infants — Analysis project within the Dutch Groningen Infant Cohort. The Third International Workshop on Brominated Flame Retardants, pp. 71–74. WHO, 1992. Polychlorinated Biphenyls and Terphenils, second ed. In: Environmental Health Criteria, vol. 140 World Health Organisation, Geneva. WHO, 1994. Brominated diphenyl ethers. In: Environmental Health Criteria, vol. 162. World Health Organization, Geneva. Zuccato, E., Calvarese, S., Mariani, G., Mangiapan, S., Grasso, P., Guzzi, A., Fanelli, R., 1999. Levels, sources, and toxicity of polychlorinated biphenyls in the Italian diet. Chemosphere 38, 2753–2765.
Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in milk from Italian women living in Rome and Venice Anna Maria Ingelido a,*, Terri Ballard b, Elena Dellatte a, Alessandro di Domenico a, Fabiola Ferri a, Anna Rita Fulgenzi a, Thomas Herrmann c, Nicola Iacovella a, Roberto Miniero a, Olaf Pa¨pke c, Maria Grazia Porpora d, Elena De Felip a a
Toxicological Chemistry Unit, Department of the Environment and Primary Prevention, Istituto Superiore di Sanita´, 00161 Rome, Italy b Food and Agricultural Organization, 00100 Rome, Italy c ERGO Forschungsgesellschaft mbH, 22305 Hamburg, Germany d Institute of Gynecological Sciences, Perinatology and Child Health, University ‘‘La Sapienza’’, 00161 Rome, Italy Accepted 26 May 2006 Available online 25 January 2007
Abstract The levels of selected polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) were measured in human milk samples from the areas of Venice and Rome, primarily in order to characterize the current levels of infant exposure to PCBs and PBDEs due to breast feeding in Italy. Sixteen non-dioxin-like PCBs, including the traditional indicator congeners, and 11 PBDEs, comprising the relevant PBDE-47, PBDE-99, and PBDE-153, were determined. Congeners were selected for analysis according to their relative abundance in human tissues, toxicological relevance, and diffusion in the environment. Dietary habits of the milk donors were recorded by questionnaires; mothers of the Venice area were classified into three groups according to their consumption of local fish, molluscs, and other fishery products. R16(PCBs) and R11(PBDEs) (ng g1 fat) for the areas of Venice and Rome were respectively, 250–390 and 240, and 1.6–2.8 and 4.1. An increase of fish and fishery product consumption could not be associated with an increase of PCB and PBDE levels in milk. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Breast milk; Fish consumption; Infant exposure; Organohalogenated contaminants; Polychlorinated biphenyls; Polybrominated diphenyl ethers
1. Introduction Human milk is the major route of excretion of persistent lipophilic chemicals — e.g., polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) — for lactating women and the major source of exposure to these substances for breast-fed infants (WHO, 1992; Lakind et al., 2000; Chao et al., 2004; Barr et al., 2004). *
Corresponding author. E-mail addresses: [email protected] (A.M. Ingelido), [email protected] (A. di Domenico). 0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.05.111
Perinatal exposure to PCBs and PBDEs occurs prenatally via the placenta and postnatally via breast milk. Although in humans it is difficult to distinguish between exposure of offspring by transplacental or by breast milk transfer, both human and animal data from different species indicate that accumulation of highly persistent chemicals ingested via milk far exceeds the contribution from maternal-foetal transfer (Gallenberg and Vodicnik, 1987; Eriksson et al., 2001). Furthermore, it has been shown that levels in breast milk reflect maternal body burden during pregnancy and are a dose-metric of prenatal exposure to the substances of interest. Accordingly, human milk constitutes a suitable
S302
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
matrix to examine potential perinatal exposures for breastfeeding infants and breast milk monitoring studies are of primary importance to carry out an adequate risk assessment at the actual levels of exposure. PCBs are environmental contaminants widely used in the western world for over 40 years since the 1930s. The toxicological risk associated to their perinatal exposure, including neurodevelopmental and immunological effects, has extensively been reviewed (WHO, 1992; Huisman et al., 1995; Chao et al., 2004; Weisglas-Kuperus et al., 2004). Unlike PCBs, PBDEs are still currently produced and used in large amounts worldwide primarily as flame retardants; starting with the 1980s, their occurrence in biota and the environment has been repeatedly reported (WHO, 1994; de Wit, 2002; Law et al., 2003; Hites, 2004). Increasing concern on their potential effects on neurobehavioral development in children caused by perinatal exposure has prompted a number of regulatory actions aimed at reducing maternal body burden. In fact, in spite of a still incomplete congener-specific toxicological characterization, many experimental studies consistently reported neurotoxic effects following perinatal exposure to PBDEs (Eriksson et al., 2001; Branchi et al., 2002). In order to characterize the current levels of infant exposure to PCBs and PBDEs in Italy due to breast feeding, milk from mothers of the general population of Rome and Venice and their surroundings was analyzed (di Domenico et al., 2002; Ingelido et al., 2004). In this latter case, an assessment of PCB and PBDE levels was carried out as a function of maternal fish consumption, remarkably higher than the national mean value in some subgroups of the local
population. In addition, to provide examples of the specific PCB and PBDE profiles detectable in the Venice lagoon, the outcome of analyses carried out on samples of edible benthonic molluscs — such as clams (Tapes sp.) and common cockles (Cardium edule) — has here been reported. Clams were obtained from a lagoon area under a moderate industrial impact, whereas cockles came from a fishing zone not directly exposed; both molluscs were collected during milk sampling (di Domenico et al., 2002, 2005). 2. Materials and methods 2.1. Sampling Milk samples were collected with a breast-pump into a glass container between weeks four and eight after delivery and stored at 20 °C until analysis. Mothers’ characteristics are reported in Table 1. Lactating mothers from the area of Rome (one group or pool, 10 donors) were enrolled in the period from January 2000 to July 2001. Mothers from Venice and its surroundings (three groups or pools differing in fish consumption level as follows: low consumption (LC), 10 donors; medium consumption (MC), 13 donors; high consumption (HC), six donors) were enrolled in the period from April 1998 to October 2000. Age distribution of mothers enrolled in all groups was 21–40 years. Data on dietary habits and lifestyle were obtained by questionnaires. Except for an excess fish consumption of the HC group, dietary habits of all subjects were substantially representative of the mean Italian diet (di Domenico et al., 2002; Ingelido et al., 2004).
Table 1 General informations on human milk donorsa Parameter
Groups of milk donor (Pools) Venice (LC)
Venice (MC)
Venice (HC)
Rome
Geographic areab Sampling date (month.year) Number of donors in the pool Age, mean (years) Age, range (years) Height, mean (cm) Height, range (cm) Body mass index, mean (before pregnancy) Body mass index, range (before pregnancy) Weight increase during pregnancy, mean (kg) Weight increase during pregnancy, range (kg) Residence area in last five years (fraction of donors in the pool)c Residence area in previous years (fraction of donors in the pool)c Smoking habits (fraction of donors in the pool)d
Venice 9.1998–7.2000 10 31 24–38 165 158–175 22.6 19.5–35.6 12.7 10–17 U, 80%; S, 20%
Venice 4.1998–10.2000 13 30 21–38 166 156–178 21.4 16.9–24.8 13.2 8.5–25.5 U, 85%; S, 15%
Venice 3.1999–7.2000 6 27 21–29 161 154–170 20.3 18.8–22.4 13.5 7–19 U, 50%; S, 50%
Rome 1.2000–7.2001 10 34 28–40 164 150–173 22.0 19.7–26.7 11.8 9–15 U, 100%
U, 80%; S, 20%
U, 85%; S, 15%
U, 89%; S, 11%
NS, 60%; FS, 30%; S, 10% 2.6%
NS, 77%; FS, 23% 3.1%
U, 33%; S, 50%; NA, 17% NS, 100%
Extracted lipids in pooled milk a
2.7%
NS, 67%; FS, 22%; S, 11% 2.9%
No donor with occupational exposure to PCBs or PBDEs. For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b City and surroundings. c Urban (U), suburban (S), rural (R). NA, not assessed. d Only cigarette smoke. Not smokers (NS), former smokers (FS), smokers (S).
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
2.2. Analysis For a given donors’ group, the milk pool was obtained by mixing the same quantity of milk from each donor. Portions (0.2–0.5 l) of the pooled samples were added with 13Clabelled standards, allowed to rest for hours, and subjected to a liquid–liquid extraction with ethyl ether and n-hexane to remove the lipid fractions. The latter were gravimetrically determined. Each lipid fraction was divided into portions for the determination of different groups of analytes. Clean-up was carried out by supercritical fluid extraction (SFE) followed by elution on silica gel for PCB analysis (Bayarri et al., 2001; di Domenico et al., 2002) and by a multi-step procedure for PBDE analysis (Pa¨pke et al., 2001). Quantitative determination was performed by highresolution gas chromatography coupled with low-resolution mass spectrometry (HRGC-LRMS) used in the selected ion monitoring mode (SIM). HRGC-HRMS(SIM) was employed as a confirmatory technique. The analysis of biota was carried out by excising the edible parts from many specimens, thereafter pooled by species to obtain two fresh matrices of approximately 200 g each. Pools were washed, drained off to remove excess water, and added with 13C-labelled standards. Spiked matrices were homogenized and freeze-dried. Gram amounts of the freeze-dried materials were subjected to extraction, cleanup, and HRGC-LRMS(SIM) and -HRMS(SIM) quantification procedures as previously reported (di Domenico et al., 1998; Bayarri et al., 2001). The PCB and PBDE congeners selected for assessment were, respectively: PCB-28, PCB-52, PCB-101, PCB-122, PCB-124, PCB-128, PCB-138, PCB-141, PCB-153, PCB170, PCB-180, PCB-183, PCB-187, PCB-194, PCB-206, and PCB-209; PBDE-17, PBDE-28, PBDE-47, PBDE-66, PBDE-99, PBDE-100, PBDE-138, PBDE-153, PBDE154, and PBDE-183. 3. Results and discussion Results of the congener-specific determinations of PCBs in human milk pooled samples are shown in Table 2. The sums of the concentrations of the 16 selected PCB congeners, R16(PCBs), estimated for Venice (LC, MC, and HC) and Rome are respectively, 390, 370, 250, and 240 ng g1 fat. Taking into account the analytical uncertainty, R16(PCBs) appears to be substantially the same for the LC and MC groups, whereas it is visibly lower at the highest fish consumption (HC group); the same pattern can be observed for most congeners. As visible in Fig. 1, the congener profiles of the four human milk samples do not exhibit significant differences. As expected, PCB-138, PCB-153, and PCB-180 are the most abundant congeners with the following concentration order: PCB-153 > PCB-138 > PCB180. Congener profiles of the two biota samples are consistent with human milk profiles as to the congeners with six chlorines or more, such as PCB-138, PCB-153, and PCB-180. However, the lower chlorinated congeners
S303
Table 2 Selected PCB congener concentrations (ng g1 fat) and distribution in human milk sample pools from Venice and Romea PCB
Venice (LC)
Venice (MC)
Venice (HC)
Rome
PCB-28 PCB-52 PCB-101 PCB-122 PCB-124 PCB-128 PCB-138 PCB-141 PCB-153 PCB-170 PCB-180 PCB-183 PCB-187 PCB-194 PCB-206 PCB-209 R16(PCBs)c
3.5 0.20 0.54 <0.07b <0.08 0.61 98 <0.4 120 38 96 9.5 18 8.9 0.74 0.37 390
6.2 0.33 1.1 <0.08 <0.09 <1 92 <0.8 130 30 76 9.2 20 6.5 0.70 0.50 370
2.1 0.26 0.91 <0.1 <0.1 <1 66 <0.9 87 20 48 6.3 13 3.9 0.46 0.28 250
3.5 0.26 0.59 <0.2 <0.2 0.66 58 <0.4 77 21 56 6.1 15 6.3 0.91 0.27 240
Values rounded off to two figures. a For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b The sign < indicates limit of quantification (LOQ). c Medium bound approach. Estimated analytical uncertainty (CV%),
PCB-28, PCB-52, and PCB-101 appear to be appreciably present in the molluscs analyzed but not in human milk. The difference between human and biota congener composition may well be a consequence of metabolism on PCB molecules with different number and distribution of chlorine substituents in the substratum (Borlakoglu and Walker, 1989). The R16(PCBs) values estimated for clams and common cockles are respectively, 640 and 430 ng g1 fat (5.4 and 3.5 ng g1 fresh weight). Results of the congener-specific determinations of PBDEs in human milk pooled samples are shown in Table 3. The sums of the concentrations of the 11 selected PBDE congeners, R11(PBDEs), estimated for Venice (LC, MC, and HC) and Rome are respectively, 2.8, 2.5, 1.6, and 4.1 ng g1 fat. Taking into account the analytical uncertainty, R11(PBDEs) appears to be substantially the same for the LC and MC groups, whereas it is visibly lower at the highest fish consumption (HC group). The combined concentrations of the three most abundant congeners PBDE-47, PBDE-99, and PBDE-153 range between 1.3 and 3.3 ng g1 fat: these values match those recently reported for some European countries, spanning from 1.5 to 5.3 ng/g fat (Strandman et al., 2000; Kalantzi et al., 2004) and on average in the order of 3 ng/g fat (Baumann et al., 2003; Meironyte´ Guvenius et al., 2003; Pirard et al., 2003; Thomsen et al., 2003). PBDE congener profiles are shown in Fig. 2. As observed in most studies on human milk (Strandman et al., 2000; Baumann et al., 2003; Meironyte´ Guvenius et al., 2003; Pirard et al., 2003; Thomsen et al., 2003; Kalantzi et al., 2004), in all our pools congeners PBDE-47,
S304
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
Fig. 1. Selected PCB congener profiles (normalized) in human milk sample pools from Venice (LC, MC, and HC) and Rome. For comparison, the corresponding profiles detected in clams and common cockles from the Venice lagoon are also shown. The concentrations of the predominant congener in each matrix are (matrix ID, PCB congener, ng g1 fat): LC, PCB-153, 120; MC, PCB-153, 130; HC, PCB-153, 87; Rome, PCB-153, 77; clams, PCB-138, 140; cockles, PCB-153, 120.
Table 3 Selected PBDE congener concentrations (ng g1 fat) and distribution in human milk sample pools from Venice and Romea PBDE
Venice (LC)
Venice (MC)
Venice (HC)
Rome
PBDE-17 PBDE-28 PBDE-47 PBDE-66 PBDE-85 PBDE-99 PBDE-100 PBDE-138 PBDE-153 PBDE-154 PBDE-183 R11(PBDEs)c
0.0038 0.065 1.5 0.015 0.035 0.41 0.28 <0.01 0.41 0.025 0.061 2.8
0.0042 0.064 0.90 0.037 0.045 0.51 0.19 0.020 0.47 0.047 0.19 2.5
<0.002b 0.036 0.55 <0.006 0.018 0.14 0.15 <0.01 0.60 0.020 0.050 1.6
0.0039 0.082 1.9 0.019 0.074 0.97 0.48 0.013 0.47 0.070 0.092 4.1
Values rounded off to two figures. a For the area of Venice, LC, MC, and HC indicate low, medium, and high consumption of local fish and fishery products. b The sign < indicates limit of quantification (LOQ). c Medium bound approach. Estimated analytical uncertainty (CV%),
PBDE-99, PBDE-100, and PBDE-153 are the most abundant, their sum accounting for over 80% of total concentration. It may be observed that, contrary to most congeners, PBDE-153 relative contribution progressively increases, to become the predominant congener in milk from the donors’ group at the highest level of fish consumption: this determines a contamination profile different from what is usually observed in human milk, with PBDE-47 standing out for its relative abundance. However, a pattern with
PBDE-153 as the predominant congener rather than PBDE-47 was recently observed in human milk samples from the Faroe Islands, a North Atlantic region with a diet traditionally based on seafood (Fa¨ngstro¨m et al., 2005). A PBDE-153 predominance was also occasionally noted in individual samples of milk, blood, and adipose tissue from the USA and The Netherlands (Schecter et al., 2003; She et al., 2004; Weiss et al., 2004). In our study, the apparent increase of PBDE-153 with increasing fish consumption do not totally reflect the congener profile found in benthonic molluscs, as the prevalent congeners in clams and cockles are respectively PBDE-99 and PBDE-47, with PBDE-153 levels being in the order of 15–20% of the PBDE-47 concentration. Similarly to PCBs, the PBDE patterns found in LC and Rome human milk pools seem to be in general agreement with the profile found in cockles; however, some relevant differences are visible with the PBDE profile detected in clams. The two biota samples are also characterized by different R11(PBDEs) values (40 and 15 ng g1 fat in clams and cockles, respectively). The biological differences between the two organisms and mostly between sampling sites might account for the sensible diversity in mollusc body burdens and profiles. Although a correlation between PBDE levels in lagoon biota and the body burden of local people was beyond the scope of our study, it is nevertheless of interest to highlight the presence of PBDEs in low trophic niches at levels comparable with those of several PCB congeners. The apparent absence of a positive correlation between PCB and PBDE cumulative and congener concentration levels and fish consumption in the human milk from the
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
S305
Fig. 2. Selected PBDE congener profiles (normalized) in human milk sample pools from Venice (LC, MC, and HC) and Rome. For comparison, the corresponding profiles detected in clams and common cockles from the Venice lagoon are also shown. The concentrations of the predominant congener in each matrix are (matrix ID, PBDE congener, ng g1 fat): LC, PBDE-47, 1.5; MC, PBDE-47, 0.90; HC, PBDE-153, 0.60; Rome, PBDE-47, 1.9; clams, PBDE-99, 18; cockles, PBDE-47, 5.2.
Venice area seems to be inconsistent with the results of other studies, that found increasing body burden of the aforesaid compounds with increasing fish consumption (Kostyniak et al., 1999; Stewart et al., 1999; Ohta et al., 2002); contrary to that, another work did not found any relationships (Lind et al., 2003). In our study, the absence of a positive correlation may be related to dietary habits of the milk donors (however, the most deviating outcome is associated with the HC pool, whose representativeness is limited due to the small number of donors). Questionnaires documented a diminished consumption of milk and related products among the three groups of donors from the Venice area with increasing fish consumption: dairy products are indeed recognized as a significant source of human dietary exposure to PCBs and PBDEs (Zuccato et al., 1999; Darnerud et al., 2001; EFSA, 2005). Furthermore, the levels of fish contamination (background levels) and the kind (chiefly lean fish) and amount of fish and fishery products consumed in the lagoon environment may also play a relevant role in determining the absence of a significant positive association between fish consumption and milk levels of PCBs and PBDEs. Acknowledgements The Authors wish to acknowledge Maria Pia Giammarinaro, Cristina Pedini, Francesca Salmistrari, Sandra Scantambulro, Sonia Smerghetto, Luigia Tagliapietre, and Angela Paterno for their kind assistance in milk sample collection. The worked described was co-financed by the Italian Ministry of the Environment (Rome) and the Isti-
tuto Superiore di Sanita` (Rome), Contract PR-27/IS ISS No. A-80 (1998–2005). References Barr, D.B., Wang, R.Y., Needham, L.L., 2004. Biologic monitoring of exposure to environmental chemicals throughout the life stages: requirements and issues for consideration for the national children’s study. Environmental Health Perspectives 113, 1083–1091. Baumann, B., Hijman, W., Van Beuzekom, S., Hoogerbrugge, R., Houweling, D., Zeilmaker, M., 2003. PBDEs in human milk from the Dutch 1998 monitoring programme. Organohalogen Compounds 61, 187–190. Bayarri, S., Turrio Baldassarri, L., Iacovella, N., Ferrara, F., di Domenico, A., 2001. PCDDs, PCDFs, PCBs, and DDE in edible marine species from the Adriatic sea. Chemosphere 43, 601–610. Borlakoglu, J.T., Walker, C.H., 1989. Comparative aspects of congener specific PCB metabolism. European Journal of Drug, Metabolism, and Pharmacokinetics 14, 127–131. Branchi, I., Alleva, E., Costa, L.G., 2002. Effects of perinatal exposure to a polybrominated diphenyl ether (PBDE 99) on mouse neurobehavioural development. Neurotoxicology 23, 375–384. Chao, H.R., Wang, S.L., Lee, C.C., Yu, H.Y., Lu, Y.K., Pa¨pke, O., 2004. Level of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs) in human milk and the input to infant body burden. Food and Chemical Toxicology 42, 1299–1308. Darnerud, P.O., Eriksen, G.S., Torkell, J., Larsen, P.B., Viluksela, M., 2001. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environmental Health Perspectives 109 (S1), 49–68. de Wit, C., 2002. An overview of brominated flame retardants in the environment. Chemosphere 46, 583–624. di Domenico, A., Turrio Baldassarri, L., Ziemacki, G., De Felip, E., Ferrari, G., La Rocca, C., Cardelli, M., Cedolini, G., Dalla Palma, M., Grassi, M., Roccabella, V., Volpi, F., Ferri, F., Iacovella, N., Rodriguez, F., D’Agostino, O., Sansoni, R., Settimo, G., 1998. Priority microcontaminants in biota samples from the Venice lagoon:
S306
A.M. Ingelido et al. / Chemosphere 67 (2007) S301–S306
a selection of concentration data and elements of risk analysis. Organohalogen Compounds 39, 199–204. di Domenico, A., Biagini, G., De Felip, E., Dellatte, E., Ferri, F., Ingelido, A.M., Miniero, R., 2002. Laguna Veneta — Scenari di rischio per la salute umana associati alla introduzione e alla presenza di microinquinanti chimici ad alto potenziale tossico (PR-27/IS) — Rapporto Finale — Sezione II. Sottoprogramma ‘‘Latte Umano’’. Report of the Istituto Superiore di Sanita` (Rome). di Domenico, A., De Felip, E., Dellatte, E., Ferri, F., Ingelido, A.M., Miniero, R., 2005. Laguna Veneta — Scenari di rischio per la salute umana associati alla introduzione e alla presenza di microinquinanti chimici ad alto potenziale tossico (PR-27/IS) — Rapporto Finale — Sezione V. Sottoprogramma ‘‘Biota’’. Report of the Istituto Superiore di Sanita` (Rome). EFSA, 2005. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the presence of nondioxin-like polychlorinated biphenyls (PCBs) in feed and food. The EFSA Journal 284, 1–137. Eriksson, P., Jakobsson, E., Fredriksson, A., 2001. Brominated flame retardants: a novel class of developmental neurotoxicants in our environment? Environmental Health and Perspectives 109, 903–908. ˚ ., 2005. A Fa¨ngstro¨m, B., Strid, A., Grandjean, P., Weihe, P., Bergman, A retrospective study of PBDEs and PCBs in human milk from the Faroe Islands. Environmental Health: A Global Access Science Source 4, 12. Gallenberg, L.A., Vodicnik, M.J., 1987. Transfer of persistent chemicals in milk. Drug Metabolism Review 21, 277–317. Hites, R.A., 2004. Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science and Technology 38, 945–956. Huisman, M., Koopman-Esseboom, C., Fidler, V., Hadders-Algra, M., van der Paauw, C.G., Tuinstra, L.G., Weisglas-Kuperus, N., Sauer, P.J., Touwen, B.C., Boersma, E.R., 1995. Perinatal exposure to polychlorinated biphenyls and dioxins and its effect on neonatal neurological development. Early Human Development 42, 111–127. Ingelido, A.M., Ballard, T., De Felip, E., Dellatte, E., Ferri, F., Fulgenzi, A.R., Herrmann, T., Iacovella, N., Miniero, R., Pa¨pke, O., Porpora, M.G., di Domenico, A., 2004. Levels of polybrominated diphenyl ethers in milk from Italian women living in Rome and Venice. Organohalogen Compounds 66, 2722–2727. Kalantzi, O.I., Alcock, R.E., Martin, F.L., Thomas, G.O., Jones, K.C., 2004. Polybrominated diphenyl ethers (PBDEs) and selected organochlorines in human breast milk samples from the United Kingdom. Organohalogen Compounds 61, 9–12. Kostyniak, P.J., Stinson, C., Greizerstein, H.B., Vena, J., Buck, G., Mendola, P., 1999. Relation of lake Ontario fish consumption, lifetime lactation, and parity to breast milk polychlorobiphenyl and pesticide concentrations. Environmental Research Section A 80, S166–S174. LaKind, J.S., Berlin, C.M., Park, C.N., Naiman, D.Q., Gudka, N.J., 2000. Methodology for characterizing distributions of incremental body burdens of 2,3,7,8-TCDD and DDE from breast milk in North American nursing infants. Journal of Toxicology Environment and Health A 59, 605–639. Law, R.J., Alaee, M., Allchin, C.R., Boon, J.P., Lebeuf, M., Lepom, P., Stern, G.A., 2003. Levels and trends of polybrominated diphenylethers and other brominated flame retardants in wildlife. Environment International 29, 757–770.
Lind, Y., Darnerud, P.O., Atuma, S., Aune, M., Becker, W., Bjerselius, R., Cnattingius, S., Glynn, A., 2003. Polybrominated diphenyl ethers in breast milk from Uppsala Country, Sweden. Environmental Research 93, 186–194. ˚, Meironyte´ Guvenius, D., Aronsson, A., Ekman-Ordebrg, G., Bergman, A Nore´n, K., 2003. Human prenatal and postnatal exposure to polybrominated diphenyl ethers, polychlorinated biphenyls, polychlorobiphenylols, and pentachlorophenol. Environmental Health and Perspectives 111, 1235–1241. Ohta, S., Ishizuka, D., Nishimura, H., Nakao, T., Aozasa, O., Shimidzu, Y., Ochiai, F., Kida, T., Nishi, M., Miyata, H., 2002. Comparison of polybrominated diphenyl ethers in fish, vegetables, and meats and levels in human milk of nursing women in Japan. Chemosphere 46, 689–696. Pa¨pke, O., Bathe, L., Bergman, A., Fu¨rst, P., Meyronyte´ Guvenius, D., Hermann, T., Nore´n, K., 2001. Determination of PBDEs in human milk from the United States — Comparison of results from three laboratories. Organohalogen Compounds 52, 197–200. Pirard, C., De Pauw, E., Focant, J.-F., 2003. Levels of selected PBDEs and PCBs in Belgian human milk. Organohalogen Compounds 64, 158–161. Schecter, A., Pavuk, M., Pa¨pke, O., Ryan, J.J., Birnbaum, L., Rosen, R., 2003. Polybrominated diphenyl ethers (PBDEs) in U.S. mothers’ milk. Environmental Health Perspectives 111, 1723–1729. She, J., Holden, A., Sharp, M., Tanner, M., Williams-Derry, C., Hooper, K., 2004. Unusual pattern of polybrominated biphenyl Ethers (PBDEs) in US breast milk. Organohalogen Compounds 66, 3945– 3950. Stewart, P., Darvill, T., Lonky, E., Reihman, J., Pagano, J., Bush, B., 1999. Assessment of prenatal exposure to PCBs from maternal consumption of great lakes fish: an analysis of PCB pattern and concentration. Environmental Research Section A 80, S87–S96. Strandman, T., Koistinen, J., Vartiainen, T., 2000. Polybrominated diphenyl ethers (PBDEs) in placenta and human milk. Organohalogen Compounds 47, 61–64. Thomsen, C., Frøshaug, M., Leknes, H., Becher, G., 2003. Brominated flame retardants in breast milk from Norway. Organohalogen Compounds 64, 33–36. Weisglas-Kuperus, N., Vreugdenhil, H.J.I., Mulder, P.G.H., 2004. Immunological effects of environmental exposure to polychlorinated biphenyls and dioxins in Dutch school children. Toxicology Letters 149, 281–285. Weiss, J.; Meijer, L.; Sauer, P.; Linderholm, L.; Athanassiadis, I.; ˚ , 2004. PBDE and HBCDD levels in blood from Dutch Bergman, A mothers and infants — Analysis project within the Dutch Groningen Infant Cohort. The Third International Workshop on Brominated Flame Retardants, pp. 71–74. WHO, 1992. Polychlorinated Biphenyls and Terphenils, second ed. In: Environmental Health Criteria, vol. 140 World Health Organisation, Geneva. WHO, 1994. Brominated diphenyl ethers. In: Environmental Health Criteria, vol. 162. World Health Organization, Geneva. Zuccato, E., Calvarese, S., Mariani, G., Mangiapan, S., Grasso, P., Guzzi, A., Fanelli, R., 1999. Levels, sources, and toxicity of polychlorinated biphenyls in the Italian diet. Chemosphere 38, 2753–2765.