Multiple persistent organic pollutants in mothers' breastmilk: Implications for infant dietary exposure and maternal thyroid hormone homeostasis in Uganda, East Africa

Henry Matovu; Zhong-Min Li; Bernhard Henkelmann; Silke Bernhöft; Meri De Angelis; Karl-Werner Schramm; Mika Sillanpää; Charles Drago Kato; Patrick Ssebugere

doi:10.1016/j.scitotenv.2021.145262

Multiple persistent organic pollutants in mothers' breastmilk: Implications for infant dietary exposure and maternal thyroid hormone homeostasis in Uganda, East Africa

Sci Total Environ. 2021 May 20:770:145262. doi: 10.1016/j.scitotenv.2021.145262. Epub 2021 Jan 20.

Authors

Henry Matovu¹, Zhong-Min Li², Bernhard Henkelmann³, Silke Bernhöft³, Meri De Angelis³, Karl-Werner Schramm⁴, Mika Sillanpää⁵, Charles Drago Kato⁶, Patrick Ssebugere⁷

Affiliations

¹ Department of Chemistry, Gulu University, P. O. Box 166, Gulu, Uganda; Department of Chemistry, Makerere University, P. O. Box 7062, Kampala, Uganda. Electronic address: hmatovu@cns.mak.ac.ug.
² Helmholtz Zentrum Muenchen, German National Research Centre for Environmental Health (GmbH), Molecular EXposomics (MEX), Ingolstaedter Landstrasse 1, Neuherberg, Munich, Germany; School of Life Sciences Weihenstephan (Nutrition), Technische Universität München, 85354 Freising, Germany.
³ Helmholtz Zentrum Muenchen, German National Research Centre for Environmental Health (GmbH), Molecular EXposomics (MEX), Ingolstaedter Landstrasse 1, Neuherberg, Munich, Germany.
⁴ Helmholtz Zentrum Muenchen, German National Research Centre for Environmental Health (GmbH), Molecular EXposomics (MEX), Ingolstaedter Landstrasse 1, Neuherberg, Munich, Germany; TUM, Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt, Department für Biowissenschaftliche Grundlagen, Weihenstephaner Steig 23, 85350 Freising, Germany.
⁵ Institute of Research and Development, Duy Tan University, Da Nang 550000, Viet Nam; Faculty of Environment and Chemical Engineering, Duy Tan University, Da Nang 550000, Viet Nam; Department of Chemical Engineering, School of Mining, Metallurgy and Chemical Engineering, University of Johannesburg, P. O. Box 17011, Doornfontein 2028, South Africa. Electronic address: mikaetapiosillanpaa@duytan.edu.vn.
⁶ School of Bio-security, Biotechnical and Laboratory Sciences, College of Veterinary Medicine, Animal Resources and Bio-security, Makerere University, P.O. Box 7062, Kampala, Uganda.
⁷ Department of Chemistry, Makerere University, P. O. Box 7062, Kampala, Uganda. Electronic address: ssebugere@cns.mak.ac.ug.

PMID: 33513488
DOI: 10.1016/j.scitotenv.2021.145262

Abstract

Persistent organic pollutants (POPs) are ubiquitous contaminants with adverse health effects in the ecosystem. One of such effects is endocrine disruption in humans and wildlife even at background exposure concentrations. This study assessed maternal breastmilk concentrations of POPs; brominated flame retardants (BFRs), polychlorinated biphenyls (PCBs) and polychlorinated dibenzo-p-dioxins/furans (PCDD/Fs), and the potential health risks posed to the nursing infants. We also evaluated the association of these POPs with total 3,3',5-triiodo-L-thyronine (T₃), L-thyroxine (T₄), and 3,3',5'-triiodo-L-thyronine (rT₃) levels measured in human breast milk. Thirty breastmilk samples were collected from Kampala, Uganda between August and December 2018. Hexabromobenzene was not detected while the maximum level of 2,2',4,4',5,5'-hexabrombiphenyl was 64.7 pg/g lw. The median levels of total indicator PCBs, PBDEs, dioxin-like PCBs, and PCDD/Fs in the samples were 159 pg/g lw, 511 pg/g lw, 1.16 pg TEQ/g lw, and 0.4 pg TEQ/g lw, respectively. These levels were lower than those reported in other countries. Owing to their bio accumulative nature, PCBs -81, -169, and ∑PCDD/Fs increased with increase in maternal age. Estimated dietary intakes for dioxin-like PCBs and PCDD/Fs were lower than those reported elsewhere but were higher than the WHO tolerable daily intakes suggesting potential health risks to nursing infants. In adjusted single pollutant models, PCB-126, PCB-169, and ∑PCB_TEQ were negatively associated with T₃, while 1,2,3,4,5,7,8-HpCDF was positively associated with rT₃. Although these associations did not persist in multipollutant models, our findings suggest potential thyroid hormone disruption by POPs in mothers. This may reduce the levels of thyroid hormones transferred from the mother to the neonates and, hence, adversely influence infant growth. A temporal study with a bigger sample size is required to corroborate these findings.

Keywords: Africa; Breastmilk; Dietary exposure; Persistent organic pollutants; Thyroid hormones.

MeSH terms

Dibenzofurans
Dibenzofurans, Polychlorinated
Dietary Exposure
Ecosystem
Environmental Pollutants* / analysis
Female
Homeostasis
Humans
Infant
Infant, Newborn
Milk, Human / chemistry
Mothers
Persistent Organic Pollutants
Polychlorinated Biphenyls* / analysis
Polychlorinated Dibenzodioxins* / analysis
Thyroid Hormones
Uganda

Substances

Dibenzofurans
Dibenzofurans, Polychlorinated
Environmental Pollutants
Polychlorinated Dibenzodioxins
Thyroid Hormones
Polychlorinated Biphenyls