OH-PCBs; OH-PBDEs; Pentachlorophenol; Bromophenols; TBBPA; Human exposure; Exposition pathways
Abstract :
[en] Many in vitro or in vivo studies highlighted the potential deleterious effects of phenolic organohalogenated compounds
(POHs) on the health, particularly on the thyroid system homeostasis, however few large scale human
epidemiological studies have been carried out, especially in Europe. Further studies monitoring the human
contamination by POHs, the sources of exposure and the influence of these compounds on thyroid health
are still needed. Therefore we determined the concentrations of 16 POHs (pentachlorophenol (PCP),
tetrabromobisphenol A (TBBPA), 4 bromophenols (BPs), 3 hydroxy-polybromodiphenylethers (OH-PBDEs)
and 7 hydroxy-polychlorobiphenyls (OH-PCBs)) in serum from 274 people aged from 18 to 76 years old living
in Liege (Belgium) and the surrounding area. A questionnaire about their alimentary habits, life style and
home environment was also administered to the volunteers. The predominant compound measured in the population
was PCP (median concentration of 593.0 pg mL−1). 4-OH-CB 107, 4-OH-CB 146 and 4-OH-CB 187 were
detected in all samples and contributed for 75% of the sum of OH-PCBs (ΣOH-PCBs). The median measured in
our population for ΣOH-PCBs was 143.7 pg mL−1. TBBPA and 2,4,6-tribromophenol were detected in 31% and
63.8% of the samples respectively while the detection frequency observed for the other BPs and the OH-PBDEs
was close to zero. We computed multivariate regression models in order to assess the influence of demographic
and lifestyle parameters on the PCP and ΣOH-PCBs contamination levels. Significant correlation was found between
the PCP concentration and sex, smoker status, sea fish consumption and level of education, although the
model seemed to be a poor (R2 = 0.14) predictor of the PCP concentration. The model computed for ΣOHPCBs
was more explanatory (R2 = 0.61) and involved age, BMI and sea fish consumption. Finally, we assessed the parameters affecting the ΣOH-PCBs/ΣPCBs ratio. The model proposed involved age, BMI, smoker status and
parent PCB level, and explained 41% of the variability of the ΣOH-PCBs/ΣPCBs ratio.
Disciplines :
Pharmacy, pharmacology & toxicology
Author, co-author :
Dufour, Patrice ; Université de Liège > Département de pharmacie > Chimie toxicologique
PIRARD, Catherine ; Centre Hospitalier Universitaire de Liège - CHU > Service de toxicologie
CHARLIER, Corinne ; Centre Hospitalier Universitaire de Liège - CHU > Service de toxicologie
Language :
English
Title :
Determination of phenolic organohalogens in human serum from a Belgian population and assessment of parameters affecting the human contamination
Alaee, M., Arias, P., Sjödin, A., Bergman, A., An overview of commercially used brominated flame retardants, their applications, their use patterns in different countries/regions and possible modes of release. Environ. Int. 29 (2003), 683–689, 10.1016/S0160-4120(03)00121-1.
Albert, B.B., Cutfield, W.S., Webster, D., Carll, J., Derraik, J.G.B., Jefferies, C., Gunn, A.J., Hofman, P.L., Etiology of increasing incidence of congenital hypothyroidism in New Zealand from 1993–2010. J. Clin. Endocrinol. Metab. 97 (2012), 3155–3160, 10.1210/jc.2012-1562.
Ali, N., Eqani, S.A.M.A.S., Malik, R.N., Neels, H., Covaci, A., Organohalogenated contaminants (OHCs) in human serum of mothers and children from Pakistan with urban and rural residential settings. Sci. Total Environ. 461–462 (2013), 655–662, 10.1016/j.scitotenv.2013.05.044.
Athanasiadou, M., Cuadra, S.N., Marsh, G., Bergman, Å., Jakobsson, K., Polybrominated diphenyl ethers (PBDEs) and bioaccumulative hydroxylated PBDE metabolites in young humans from Managua, Nicaragua. Environ. Health Perspect. 116 (2008), 400–408, 10.1289/ehp.10713.
Barry, Y., Bonaldi, C., Goulet, V., Coutant, R., Léger, J., Paty, A.-C., Delmas, D., Cheillan, D., Roussey, M., Increased incidence of congenital hypothyroidism in France from 1982 to 2012: a nationwide multicenter analysis. Ann. Epidemiol. 26 (2016), 100–105.e4, 10.1016/j.annepidem.2015.11.005.
Benvenga, S., Antonelli, A., Vita, R., Thyroid nodules and thyroid autoimmunity in the context of environmental pollution. Rev. Endocr. Metab. Disord. 16 (2015), 319–340, 10.1007/s11154-016-9327-6.
Boas, M., Feldt-Rasmussen, U., Main, K.M., Thyroid effects of endocrine disrupting chemicals. Mol. Cell. Endocrinol., Health Impacts Endocr. Disrupters 355 (2012), 240–248, 10.1016/j.mce.2011.09.005.
Brill, M.J.E., Diepstraten, J., van Rongen, A., van Kralingen, S., van den Anker, J.N., Knibbe, C.A.J., Impact of obesity on drug metabolism and elimination in adults and children. Clin. Pharmacokinet. 51 (2012), 277–304, 10.2165/11599410-000000000-00000.
Cariou, R., Antignac, J.-P., Zalko, D., Berrebi, A., Cravedi, J.-P., Maume, D., Marchand, P., Monteau, F., Riu, A., Andre, F., Bizec, B.L., Exposure assessment of French women and their newborns to tetrabromobisphenol-A: occurrence measurements in maternal adipose tissue, serum, breast milk and cord serum. Chemosphere 73 (2008), 1036–1041, 10.1016/j.chemosphere.2008.07.084.
Cheek, A.O., Kow, K., Chen, J., McLachlan, J.A., Potential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin. Environ. Health Perspect. 107 (1999), 273–278, 10.1289/ehp.99107273.
Dallaire, R., Dewailly, E., Pereg, D., Dery, S., Ayotte, P., Thyroid function and plasma concentrations of polyhalogenated compounds in Inuit adults. Environ. Health Perspect. 117 (2009), 1380–1386, 10.1289/ehp.0900633.
Dallaire, R., Muckle, G., Dewailly, É., Jacobson, S.W., Jacobson, J.L., Sandanger, T.M., Sandau, C.D., Ayotte, P., Thyroid hormone levels of pregnant Inuit women and their infants exposed to environmental contaminants. Environ. Health Perspect. 117 (2009), 1014–1020, 10.1289/ehp.0800219.
Dirtu, A.C., Jaspers, V.L.B., Cernat, R., Neels, H., Covaci, A., Distribution of PCBs, their hydroxylated metabolites, and other phenolic contaminants in human serum from two European countries†. Environ. Sci. Technol. 44 (2010), 2876–2883, 10.1021/es902149b.
Dufour, P., Pirard, C., Charlier, C., Validation of a novel and rapid method for the simultaneous determination of some phenolic organohalogens in human serum by GC–MS. J. Chromatogr. B 1036–1037 (2016), 66–75, 10.1016/j.jchromb.2016.10.002.
Eguchi, A., Nomiyama, K., Devanathan, G., Subramanian, A., Bulbule, K.A., Parthasarathy, P., Takahashi, S., Tanabe, S., Different profiles of anthropogenic and naturally produced organohalogen compounds in serum from residents living near a coastal area and e-waste recycling workers in India. Environ. Int. 47 (2012), 8–16, 10.1016/j.envint.2012.05.003.
Eguchi, A., Nomiyama, K., Minh Tue, N., Trang, P.T.K., Hung Viet, P., Takahashi, S., Tanabe, S., Residue profiles of organohalogen compounds in human serum from e-waste recycling sites in North Vietnam: association with thyroid hormone levels. Environ. Res. 137 (2015), 440–449, 10.1016/j.envres.2015.01.007.
El Majidi, N., Bouchard, M., Carrier, G., Systematic analysis of the relationship between standardized biological levels of polychlorinated biphenyls and thyroid function in pregnant women and newborns. Chemosphere 98 (2014), 1–17, 10.1016/j.chemosphere.2013.10.006.
Fängström, B., Athanasiadou, M., Grandjean, P., Weihe, P., Bergman, A., Hydroxylated PCB metabolites and PCBs in serum from pregnant Faroese women. Environ. Health Perspect. 110 (2002), 895–899, 10.1289/ehp.02110895.
Freitas, J., Cano, P., Craig-Veit, C., Goodson, M.L., Furlow, J.D., Murk, A.J., Detection of thyroid hormone receptor disruptors by a novel stable in vitro reporter gene assay. Toxicol. In Vitro 25 (2011), 257–266, 10.1016/j.tiv.2010.08.013.
Fujii, Y., Harada, K.H., Hitomi, T., Kobayashi, H., Koizumi, A., Haraguchi, K., Temporal trend and age-dependent serum concentration of phenolic organohalogen contaminants in Japanese men during 1989–2010. Environ. Pollut. 185 (2014), 228–233, 10.1016/j.envpol.2013.11.002.
Fujii, Y., Nishimura, E., Kato, Y., Harada, K.H., Koizumi, A., Haraguchi, K., Dietary exposure to phenolic and methoxylated organohalogen contaminants in relation to their concentrations in breast milk and serum in Japan. Environ. Int. 63 (2014), 19–25, 10.1016/j.envint.2013.10.016.
Glynn, A., Larsdotter, M., Aune, M., Darnerud, P.O., Bjerselius, R., Bergman, A., Changes in serum concentrations of polychlorinated biphenyls (PCBs), hydroxylated PCB metabolites and pentachlorophenol during pregnancy. Chemosphere 83 (2011), 144–151, 10.1016/j.chemosphere.2010.12.050.
Grimm, F.A., Hu, D., Kania-Korwel, I., Lehmler, H.-J., Ludewig, G., Hornbuckle, K.C., Duffel, M.W., Bergman, Å., Robertson, L.W., Metabolism and metabolites of polychlorinated biphenyls. Crit. Rev. Toxicol. 45 (2015), 245–272, 10.3109/10408444.2014.999365.
Guvenius, D.M., Aronsson, A., Ekman-Ordeberg, G., Bergman, A., Norén, K., Human prenatal and postnatal exposure to polybrominated diphenyl ethers, polychlorinated biphenyls, polychlorobiphenylols, and pentachlorophenol. Environ. Health Perspect. 111 (2003), 1235–1241, 10.1289/ehp.5946.
Hagmar, L., Björk, J., Sjödin, A., Bergman, A., Erfurth, E.M., Plasma levels of persistent organohalogens and hormone levels in adult male humans. Arch. Environ. Health 56 (2001), 138–143, 10.1080/00039890109604065.
Hamers, T., Kamstra, J.H., Sonneveld, E., Murk, A.J., Kester, M.H.A., Andersson, P.L., Legler, J., Brouwer, A., In vitro profiling of the endocrine-disrupting potency of brominated flame retardants. Toxicol. Sci. 92 (2006), 157–173, 10.1093/toxsci/kfj187.
Haraguchi, K., Kato, Y., Ohta, C., Koga, N., Endo, T., Marine sponge: a potential source for methoxylated polybrominated diphenyl ethers in the Asia-Pacific food web. J. Agric. Food Chem. 59 (2011), 13102–13109, 10.1021/jf203458r.
Haraguchi, K., Ito, Y., Takagi, M., Fujii, Y., Harada, K.H., Koizumi, A., Levels, profiles and dietary sources of hydroxylated PCBs and hydroxylated and methoxylated PBDEs in Japanese women serum samples. Environ. Int. 97 (2016), 155–162, 10.1016/j.envint.2016.08.022.
Hattemer-Frey, H.A., Travis, C.C., Pentachlorophenol: environmental partitioning and human exposure. Arch. Environ. Contam. Toxicol. 18 (1989), 482–489, 10.1007/BF01055013.
Herbert, J., Wilcox, J.N., Pham, K.T., Fremeau, R.T., Zeviani, M., Dwork, A., Soprano, D.R., Makover, A., Goodman, D.S., Zimmerman, E.A., Transthyretin: a choroid plexus-specific transport protein in human brain. The 1986 S. Weir Mitchell award. Neurology 36 (1986), 900–911, 10.1212/WNL.36.7.900.
Hinton, C.F., Harris, K.B., Borgfeld, L., Drummond-Borg, M., Eaton, R., Lorey, F., Therrell, B.L., Wallace, J., Pass, K.A., Trends in incidence rates of congenital hypothyroidism related to select demographic factors: data from the United States, California, Massachusetts, New York, and Texas. Pediatrics 125:Suppl. 2 (2010), S37–S47, 10.1542/peds.2009-1975D.
Hisada, A., Shimodaira, K., Okai, T., Watanabe, K., Takemori, H., Takasuga, T., Koyama, M., Watanabe, N., Suzuki, E., Shirakawa, M., Noda, Y., Komine, Y., Ariki, N., Kato, N., Yoshinaga, J., Associations between levels of hydroxylated PCBs and PCBs in serum of pregnant women and blood thyroid hormone levels and body size of neonates. Int. J. Hyg. Environ. Health 217 (2014), 546–553, 10.1016/j.ijheh.2013.10.004.
Hovander, L., Linderholm, L., Athanasiadou, M., Athanassiadis, I., Bignert, A., Fängström, B., Kocan, A., Petrik, J., Trnovec, T., Bergman, A., Levels of PCBs and their metabolites in the serum of residents of a highly contaminated area in eastern Slovakia. Environ. Sci. Technol. 40 (2006), 3696–3703, 10.1021/es0525657.
Kawashiro, Y., Fukata, H., Omori-Inoue, M., Kubonoya, K., Jotaki, T., Takigam, H., Sakai, S., Mori, C., Perinatal exposure to brominated flame retardants and polychlorinated biphenyls in Japan. Endocr. J. 55 (2008), 1071–1084, 10.1507/endocrj.K08E-155.
Koh, W.X., Hornbuckle, K.C., Marek, R.F., Wang, K., Thorne, P.S., Hydroxylated polychlorinated biphenyls in human sera from adolescents and their mothers living in two U.S. Midwestern communities. Chemosphere 147 (2016), 389–395, 10.1016/j.chemosphere.2015.12.113.
Koh, W.X., Hornbuckle, K.C., Wang, K., Thorne, P.S., Serum polychlorinated biphenyls and their hydroxylated metabolites are associated with demographic and behavioral factors in children and mothers. Environ. Int. 94 (2016), 538–545, 10.1016/j.envint.2016.06.014.
Kojima, H., Takeuchi, S., Uramaru, N., Sugihara, K., Yoshida, T., Kitamura, S., Nuclear hormone receptor activity of polybrominated diphenyl ethers and their hydroxylated and methoxylated metabolites in transactivation assays using Chinese hamster ovary cells. Environ. Health Perspect. 117 (2009), 1210–1218, 10.1289/ehp.0900753.
Landers, K.A., McKinnon, B.D., Li, H., Subramaniam, V.N., Mortimer, R.H., Richard, K., Carrier-mediated thyroid hormone transport into placenta by placental transthyretin. J. Clin. Endocrinol. Metab. 94 (2009), 2610–2616, 10.1210/jc.2009-0048.
Marchesini, G.R., Meimaridou, A., Haasnoot, W., Meulenberg, E., Albertus, F., Mizuguchi, M., Takeuchi, M., Irth, H., Murk, A.J., Biosensor discovery of thyroxine transport disrupting chemicals. Toxicol. Appl. Pharmacol. 232 (2008), 150–160, 10.1016/j.taap.2008.06.014.
Marek, R.F., Thorne, P.S., Wang, K., Dewall, J., Hornbuckle, K.C., PCBs and OH-PCBs in serum from children and mothers in urban and rural U.S. communities. Environ. Sci. Technol. 47 (2013), 3353–3361, 10.1021/es304455k.
McGrogan, A., Seaman, H.E., Wright, J.W., De Vries, C.S., The incidence of autoimmune thyroid disease: a systematic review of the literature. Clin. Endocrinol. 69 (2008), 687–696, 10.1111/j.1365-2265.2008.03338.x.
Meerts, I.A.T.M., Lilienthal, H., Hoving, S., Berg, J.H.J. van den, Weijers, B.M., Bergman, Å., Koeman, J.H., Brouwer, A., 2004. Developmental exposure to 4-hydroxy-2,3,3′,4′,5-pentachlorobiphenyl (4-OH-CB107): Long-term effects on brain development, behavior, and brain stem auditory evoked potentials in rats. Toxicol. Sci. 82, 207–218. doi: 10.1093/toxsci/kfh252.
Meijer, L., Weiss, J., Van Velzen, M., Brouwer, A., Bergman, A., Sauer, P.J.J., Serum concentrations of neutral and phenolic organohalogens in pregnant women and some of their infants in The Netherlands. Environ. Sci. Technol. 42 (2008), 3428–3433, 10.1021/es702446p.
Morgan, M., Jones, P., Sobus, J., Short-term variability and predictors of urinary pentachlorophenol levels in Ohio preschool children. Int. J. Environ. Res. Public Health 12 (2015), 800–815, 10.3390/ijerph120100800.
Park, J.-S., Bergman, A., Linderholm, L., Athanasiadou, M., Kocan, A., Petrik, J., Drobna, B., Trnovec, T., Charles, M.J., Hertz-Picciotto, I., Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia. Chemosphere 70 (2008), 1676–1684, 10.1016/j.chemosphere.2007.07.049.
Park, J.S., Petreas, M., Cohn, B.A., Cirillo, P.M., Factor-Litvak, P., Hydroxylated PCB metabolites (OH-PCBs) in archived serum from 1950–60s California mothers: a pilot study. Environ. Int. 35 (2009), 937–942, 10.1016/j.envint.2009.04.002.
Park, H.-Y., Park, J.-S., Sovcikova, E., Kocan, A., Linderholm, L., Bergman, A., Trnovec, T., Hertz-Picciotto, I., Exposure to hydroxylated polychlorinated biphenyls (OH-PCBs) in the prenatal period and subsequent neurodevelopment in eastern Slovakia. Environ. Health Perspect. 117 (2009), 1600–1606, 10.1289/ehp.0900611.
Phillips, D.L., Pirkle, J.L., Burse, V.W., Bernert, J.T., Omar Henderson, L., Needham, L.L., Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding. Arch. Environ. Contam. Toxicol. 18 (1989), 495–500, 10.1007/BF01055015.
C. Pirard, L. Dewalque, S. Compere, K. Firquet, C. Charlier. Assessment of the environmental levels and predictors of exposure to some endocrine disruptors in a Belgian adult population. Part I: focus on mercury, cadmium, organochlorine pesticides and PCBs. Int. J. Environ. Res. Public Health (Submitted for publication).
Préau, L., Fini, J.B., Morvan-Dubois, G., Demeneix, B., Thyroid hormone signaling during early neurogenesis and its significance as a vulnerable window for endocrine disruption. Biochim. Biophys. Acta 1849 (2015), 112–121, 10.1016/j.bbagrm.2014.06.015.
Qiu, X., Mercado-Feliciano, M., Bigsby, R.M., Hites, R.A., Measurement of polybrominated diphenyl ethers and metabolites in mouse plasma after exposure to a commercial pentabromodiphenyl ether mixture. Environ. Health Perspect. 115 (2007), 1052–1058, 10.1289/ehp.10011.
Quinete, N., Schettgen, T., Bertram, J., Kraus, T., Occurrence and distribution of PCB metabolites in blood and their potential health effects in humans: a review. Environ. Sci. Pollut. Res. Int. 21 (2014), 11951–11972, 10.1007/s11356-014-3136-9.
Roos, R., Andersson, P.L., Halldin, K., Hǻkansson, H., Westerholm, E., Hamers, T., Hamscher, G., Heikkinen, P., Korkalainen, M., Leslie, H.A., Niittynen, M., Sankari, S., Schmitz, H.-J., van der Ven, L.T.M., Viluksela, M., Schrenk, D., Hepatic effects of a highly purified 2,2′,3,4,4′,5,5′-heptachlorbiphenyl (PCB 180) in male and female rats. Toxicology 284 (2011), 42–53, 10.1016/j.tox.2011.03.013.
Rylander, C., Lund, E., Frøyland, L., Sandanger, T.M., Predictors of PCP, OH-PCBs, PCBs and chlorinated pesticides in a general female Norwegian population. Environ. Int. 43 (2012), 13–20, 10.1016/j.envint.2012.02.008.
Sandau, C.D., Ayotte, P., Dewailly, E., Duffe, J., Norstrom, R.J., Analysis of hydroxylated metabolites of PCBs (OH-PCBs) and other chlorinated phenolic compounds in whole blood from Canadian inuit. Environ. Health Perspect. 108 (2000), 611–616, 10.2307/3434880.
Sandau, C.D., Ayotte, P., Dewailly, E., Duffe, J., Norstrom, R.J., Pentachlorophenol and hydroxylated polychlorinated biphenyl metabolites in umbilical cord plasma of neonates from coastal populations in Québec. Environ. Health Perspect. 110 (2002), 411–417, 10.1289/ehp.02110411.
Schuur, A.G., Legger, F.F., van Meeteren, M.E., Moonen, M.J., van Leeuwen-Bol, I., Bergman, A., Visser, T.J., Brouwer, A., In vitro inhibition of thyroid hormone sulfation by hydroxylated metabolites of halogenated aromatic hydrocarbons. Chem. Res. Toxicol. 11 (1998), 1075–1081, 10.1021/tx9800046.
Shi, Z., Wang, Y., Niu, P., Wang, J., Sun, Z., Zhang, S., Wu, Y., Concurrent extraction, clean-up, and analysis of polybrominated diphenyl ethers, hexabromocyclododecane isomers, and tetrabromobisphenol A in human milk and serum. J. Sep. Sci. 36 (2013), 3402–3410, 10.1002/jssc.201300579.
Sjödin, A., Hagmar, L., Klasson-Wehler, E., Björk, J., Bergman, A., Influence of the consumption of fatty Baltic Sea fish on plasma levels of halogenated environmental contaminants in Latvian and Swedish men. Environ. Health Perspect. 108 (2000), 1035–1041, 10.2307/3434955.
Soechitram, S.D., Athanasiadou, M., Hovander, L., Bergman, A., Sauer, P.J.J., Fetal exposure to PCBs and their hydroxylated metabolites in a Dutch cohort. Environ. Health Perspect. 112 (2004), 1208–1212, 10.1289/ehp.6424.
Whitfield, F.B., Drew, M., Helidoniotis, F., Svoronos, D., Distribution of bromophenols in species of marine polychaetes and bryozoans from eastern Australia and the role of such animals in the flavor of edible ocean fish and prawns (shrimp). J. Agric. Food Chem. 47 (1999), 4756–4762, 10.1021/jf9904719.
Zevin, S., Benowitz, N.l., Drug interactions with tobacco smoking: an update. Clin. Pharmacokinet. 36 (1999), 425–438, 10.2165/00003088-199936060-00004.
Zheng, J., He, C.-T., Chen, S.-J., Yan, X., Guo, M.-N., Wang, M.-H., Yu, Y.-J., Yang, Z.-Y., Mai, B.-X., Disruption of thyroid hormone (TH) levels and TH-regulated gene expression by polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs), and hydroxylated PCBs in e-waste recycling workers. Environ. Int. 102 (2017), 138–144, 10.1016/j.envint.2017.02.009.
Zota, A.R., Park, J.-S., Wang, Y., Petreas, M., Zoeller, R.T., Woodruff, T.J., Polybrominated diphenyl ethers, hydroxylated polybrominated diphenyl ethers, and measures of thyroid function in second trimester pregnant women in California. Environ. Sci. Technol. 45 (2011), 7896–7905, 10.1021/es200422b.