Abstract
The presence of selected polybrominated diphenyl ethers (BDE-28, -47, -99, -100, -153, -154, and -183) was investigated in human milk samples collected from first-time mothers living in Zagreb, capital of Croatia. Samples from 2020 and 2010 were analyzed, and the first temporal comparison between the profiles and levels of these compounds in this area was obtained. A statistically significant difference between mass fractions depending on the sampling year was observed only for BDE-99, with values in 2020 higher than in 2010. BDE-153, whose median value (0.25 and 0.26 ng g−1 lipid weight (l.w.) in 2010 and 2020, respectively) did not decrease in the 10-year period, was the most frequently detected congener in samples from both years. ΣPBDEs ranged from < LOD to 3.53 ng g−1 l.w. (median 0.25 ng g−1 l.w.), and from 0.14 to 6.75 ng g−1 l.w. (median 0.55 ng g−1 l.w.) in 2010 and 2020, respectively. Maternal age and reported fish consumption had no effect on observed PBDE mass fractions, while for BDE-153, positive significant correlation (p > 0.05) was observed of its detected mass fraction with mother’s body mass index (BMI) before pregnancy and after childbirth. Infants median estimated daily intake (EDI) via milk ingestion for ΣPBDE was higher in 2020 (3.221 ng kg−1 bw day−1) compared to 2010 (1.429 ng kg−1 bw day−1), but both values were well below threshold value, indicating that human milk consumption in this specific case is unlikely to raise health risks to infants.
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The data presented in this study are available from the corresponding author on reasonable request.
References
Aerts R, Van Overmeire I, Colles A et al (2019) Determinants of persistent organic pollutant (POP) concentrations in human breast milk of a cross-sectional sample of primiparous mothers in Belgium. Environ Int 131:104979. https://doi.org/10.1016/j.envint.2019.104979
AMAP (2021) AMAP assessment 2021: human health in the arctic. Tromsø, Norway
Antignac JP, Main KM, Virtanen HE et al (2016) Country-specific chemical signatures of persistent organic pollutants (POPs) in breast milk of French, Danish and Finnish women *. Environ Pollut 218:728–738. https://doi.org/10.1016/j.envpol.2016.07.069
Cano-Sancho G, Alexandre-Gouabau MC, Moyon T et al (2020) Simultaneous exploration of nutrients and pollutants in human milk and their impact on preterm infant growth: an integrative cross-platform approach. Environ Res 182:109018. https://doi.org/10.1016/j.envres.2019.109018
Čechová E, Vojta Š, Kukučka P et al (2017) Legacy and alternative halogenated flame retardants in human milk in Europe: implications for children’s health. Environ Int 108:137–145. https://doi.org/10.1016/j.envint.2017.08.008
Chen T, Huang M, Li J et al (2019) Polybrominated diphenyl ethers and novel brominated flame retardants in human milk from the general population in Beijing, China: occurrence, temporal trends, nursing infants’ exposure and risk assessment. Sci Total Environ 689:278–286. https://doi.org/10.1016/j.scitotenv.2019.06.442
Dimitriadou L, Malarvannan G, Covaci A et al (2016) Levels and profiles of brominated and chlorinated contaminants in human breast milk from Thessaloniki, Greece. Sci Total Environ 539:350–358. https://doi.org/10.1016/j.scitotenv.2015.08.137
Drage DS, Harden FA, Je T et al (2019a) Human biomonitoring in Australian children: brominated flame retardants decrease from 2006 to 2015. Environ Int 122:363–368. https://doi.org/10.1016/j.envint.2018.11.044
Drage DS, Heffernan AL, Cunningham TK et al (2019b) Serum measures of hexabromocyclododecane (HBCDD) and polyborminated diphenyl ethers (PBDEs) in reproductive-aged women in the United Kingdom. Environ Res 177:108631. https://doi.org/10.1016/j.envres.2019.108631
Dvoršćak M, Jagić K, Besednik L et al (2022a) First application of microwave-assisted extraction in the analysis of polybrominated diphenyl ethers in human milk. Microchem J 179:107447. https://doi.org/10.1016/j.microc.2022.107447
Dvoršćak M, Jakovljević I, Jagić K et al (2022b) Polybrominated diphenyl ethers and polycyclic aromatic hydrocarbons in dust from different indoor environments in Zagreb, Croatia: levels and human exposure assessment. Indoor Air 32:e13145
US EPA (2008) Child-specific exposure factors handbook. Epa/600/R-06/096F 448pp. EPA/600/R-06/096F
U.S. EPA (2010) An exposure assessment of polybrominated diphenyl ethers. US EPA 378. https://doi.org/10.1080/15287390903212436
US EPA 2011 (2011) Exposure factors handbook: 2011 Edition. US Environ Prot Agency EPA/600/R-:1–1466. EPA/600/R-090/052F
Fiedler H (2023) Metadata analysis of persistent organic pollutants in national pools of human milk in support of the Stockholm convention implementation. Environ Heal 1:41–52. https://doi.org/10.1021/envhealth.3c00020
Fiedler H, Li X, Zhang J (2023) Persistent organic pollutants in human milk from primiparae: correlations, global, regional, and national time-trends. Chemosphere 313:137484. https://doi.org/10.1016/j.chemosphere.2022.137484
Fromme H, Fuchs V, Albrecht M et al (2022) Polychlorinated dioxins and dibenzofurans (PCDD/F), polybrominated dioxins and dibenzofurans (PBDD/F), polychlorinated biphenyls (PCB), polybrominated diphenyl ethers (PBDE), and per- and polyfluoroalkyl substances (PFAS) in German breast milk samples (LUPE 8). Sci Total Environ 825:154066. https://doi.org/10.1016/j.scitotenv.2022.154066
Gibson EA, Siegel EL, Eniola F et al (2018) Effects of polybrominated diphenyl ethers on child cognitive, behavioral, and motor development. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15081636
Guo W, Holden A, Crispo S et al (2016) PBDE levels in breast milk are decreasing in California. Chemosphere 150:505–513. https://doi.org/10.1016/j.chemosphere.2015.11.032
Gyllenhammar I, Aune M, Fridén U et al (2021) Are temporal trends of some persistent organochlorine and organobromine compounds in Swedish breast milk slowing down? Environ Res 197:111117. https://doi.org/10.1016/j.envres.2021.111117
Iszatt N, Janssen S, Lenters V et al (2019) Environmental toxicants in breast milk of Norwegian mothers and gut bacteria composition and metabolites in their infants at 1 month. Microbiome 7:1–14. https://doi.org/10.1186/s40168-019-0645-2
Jagić K, Dvoršćak M, Klinčić D (2021) Analysis of brominated flame retardants in the aquatic environment: a review. Arh Hig Rada Toksikol 72:254–267. https://doi.org/10.2478/aiht-2021-72-3576
Klinčić D, Romanić SH, Sarić MM et al (2014) Polychlorinated biphenyls and organochlorine pesticides in human milk samples from two regions in Croatia. Environ Toxicol Pharmacol 37:543–552. https://doi.org/10.1016/j.etap.2014.01.009
Klinčić D, Tariba Lovaković B, Jagić K, Dvoršćak M (2021) Polybrominated diphenyl ethers and the multi-element profile of house dust in Croatia: indoor sources, influencing factors of their accumulation and health risk assessment for humans. Sci Total Environ 800:149430. https://doi.org/10.1016/j.scitotenv.2021.149430
Kuo L, Cade SE, Cullinan V, Schultz IR (2019) Polybrominated diphenyl ethers (PBDEs) in plasma from E-waste recyclers, outdoor and indoor workers in the Puget Sound, WA region. Chemosphere 219:209–216. https://doi.org/10.1016/j.chemosphere.2018.12.006
Matovu H, Sillanpää M, Ssebugere P (2019) Polybrominated diphenyl ethers in mothers’ breast milk and associated health risk to nursing infants in Uganda. Sci Total Environ 692:1106–1115. https://doi.org/10.1016/j.scitotenv.2019.07.335
Mcgrath TJ, Ball AS, Clarke BO (2017) Critical review of soil contamination by polybrominated diphenyl ethers (PBDEs) and novel brominated flame retardants (NBFRs); concentrations, sources and congener profiles *. Environ Pollut 230:741–757. https://doi.org/10.1016/j.envpol.2017.07.009
Orta-García ST, Ochoa-Martínez ÁC, Varela-Silva JA, Pérez-Maldonado IN (2018) Polybrominated diphenyl ethers (PBDEs) levels in blood samples from children living in the metropolitan area of Guadalajara, Jalisco, Mexico. Int J Environ Health Res 28:90–101. https://doi.org/10.1080/09603123.2018.1429578
Parry E, Zota AR, Park J, Woodruff TJ (2018) Polybrominated diphenyl ethers (PBDEs) and hydroxylated PBDE metabolites (OH-PBDEs): a 6-year temporal trend in Northern California pregnant women. Chemosphere 195:777–783. https://doi.org/10.1016/j.chemosphere.2017.12.065
Rovira J, Martínez MÁ, Mari M et al (2022) Mixture of environmental pollutants in breast milk from a Spanish cohort of nursing mothers. Environ Int 166:107375. https://doi.org/10.1016/j.envint.2022.107375
Runkel AA, Križanec B, Lipičar E et al (2021) Organohalogens: a persisting burden in Slovenia? Environ Res 198:111224. https://doi.org/10.1016/j.envres.2021.111224
Souza MCO, Devóz PP, Ximenez JPB et al (2022) Potential health risk to Brazilian infants by polybrominated diphenyl ethers exposure via breast milk intake. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph191711138
Tao F, Abou-Elwafa Abdallah M, Ashworth DC et al (2017) Emerging and legacy flame retardants in UK human milk and food suggest slow response to restrictions on use of PBDEs and HBCDD. Environ Int 105:95–104. https://doi.org/10.1016/j.envint.2017.05.010
Varshavsky JR, Sen S, Robinson JF et al (2020) Racial/ethnic and geographic differences in polybrominated diphenyl ether (PBDE) levels across maternal, placental, and fetal tissues during mid-gestation. Sci Rep 10:1–14. https://doi.org/10.1038/s41598-020-69067-y
Wemken N, Drage DS, Cellarius C et al (2020) Emerging and legacy brominated flame retardants in the breast milk of first time Irish mothers suggest positive response to restrictions on use of HBCDD and Penta- and Octa-BDE formulations. Environ Res 180:108805. https://doi.org/10.1016/j.envres.2019.108805
World Health Organization (2017) The international code of marketing of breast-milk substitutes: frequently asked questions (2017 Update). Licence: C, Geneva
Zhao X, Shi Z (2021) Legacy brominated flame retardants in human milk from the general population in Beijing, China: Biomonitoring, temporal trends from 2011 to 2018, and nursing infant’s exposure assessment. Chemosphere 285:131533. https://doi.org/10.1016/j.chemosphere.2021.131533
Zota AR, Mitro SD, Robinson JF et al (2018) Polybrominated diphenyl ethers (PBDEs) and hydroxylated PBDE metabolites (OH-PBDEs) in maternal and fetal tissues, and associations with fetal cytochrome P450 gene expression. Environ Int 112:269–278. https://doi.org/10.1016/j.envint.2017.12.030
Acknowledgements
The authors owe a special thanks to all participating mothers and Blanka Tariba Lovaković for help with the interpretation of statistical analysis results. This study was performed using the facilities and equipment funded within the European Regional Development Fund project KK.01.1.1.02.0007 “Research and Education Centre of Environmental Health and Radiation Protection – Reconstruction and Expansion of the Institute for Medical Research and Occupational Health”.
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This study was financed by the Croatian Science Foundation (project Grant HrZZ-UIP-2017-05-6713).
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Methodology, investigation, validation, visualization, conceptualization were contributed to DM, JK; methodology, investigation were contributed to JI, SI; visualization, conceptualization, interpretation, resources, supervision were contributed to KD.
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Ethics Committee of the Institute for Medical Research and Occupational Health approved the study (100-21/17-7), and all the participating mothers signed the informed consent for participation in the study.
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Dvoršćak, M., Jagić, K., Jakovljević, I. et al. Polybrominated Diphenyl Ethers in Human Milk of Croatian First-Time Mothers: 2010 Versus 2020. Arch Environ Contam Toxicol 86, 101–111 (2024). https://doi.org/10.1007/s00244-023-01048-4
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DOI: https://doi.org/10.1007/s00244-023-01048-4