Environmental toxicants in breast milk of Norwegian mothers and gut bacteria composition and metabolites in their infants at 1 month

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Abstract

Background

Early disruption of the microbial community may influence life-long health. Environmental toxicants can contaminate breast milk and the developing infant gut microbiome is directly exposed. We investigated whether environmental toxicants in breastmilk affect the composition and function of the infant gut microbiome at 1 month. We measured environmental toxicants in breastmilk, fecal short-chain fatty acids (SCFAs), and gut microbial composition from 16S rRNA gene amplicon sequencing using samples from 267 mother-child pairs in the Norwegian Microbiota Cohort (NoMIC). We tested 28 chemical exposures: polychlorinated biphenyls (PCBs), polybrominated flame retardants (PBDEs), per- and polyfluoroalkyl substances (PFASs), and organochlorine pesticides. We assessed chemical exposure and alpha diversity/SCFAs using elastic net regression modeling and generalized linear models, adjusting for confounders, and variation in beta diversity (UniFrac), taxa abundance (ANCOM), and predicted metagenomes (PiCRUSt) in low, medium, and high exposed groups.

Results

PBDE-28 and the surfactant perfluorooctanesulfonic acid (PFOS) were associated with less microbiome diversity. Some sub-OTUs of Lactobacillus, an important genus in early life, were lower in abundance in samples from infants with relative “high” (> 80th percentile) vs. “low” (< 20th percentile) toxicant exposure in this cohort. Moreover, breast milk toxicants were associated with microbiome functionality, explaining up to 34% of variance in acetic and propionic SCFAs, essential signaling molecules. Per one standard deviation of exposure, PBDE-28 was associated with less propionic acid (− 24% [95% CI − 35% to − 14%] relative to the mean), and PCB-209 with less acetic acid (− 15% [95% CI − 29% to − 0.4%]). Conversely, PFOA and dioxin-like PCB-167 were associated with 61% (95% CI 35% to 87%) and 22% (95% CI 8% to 35%) more propionic and acetic acid, respectively.

Conclusions

Environmental toxicant exposure may influence infant gut microbial function during a critical developmental window. Future studies are needed to replicate these novel findings and investigate whether this has any impact on child health.

Electronic supplementary material

The online version of this article (10.1186/s40168-019-0645-2) contains supplementary material, which is available to authorized users.

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Most cited references 43

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The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds.

Martin van den Berg, Linda S. Birnbaum, Michael H. Denison … (2006)

In June 2005, a World Health Organization (WHO)-International Programme on Chemical Safety expert meeting was held in Geneva during which the toxic equivalency factors (TEFs) for dioxin-like compounds, including some polychlorinated biphenyls (PCBs), were reevaluated. For this reevaluation process, the refined TEF database recently published by Haws et al. (2006, Toxicol. Sci. 89, 4-30) was used as a starting point. Decisions about a TEF value were made based on a combination of unweighted relative effect potency (REP) distributions from this database, expert judgment, and point estimates. Previous TEFs were assigned in increments of 0.01, 0.05, 0.1, etc., but for this reevaluation, it was decided to use half order of magnitude increments on a logarithmic scale of 0.03, 0.1, 0.3, etc. Changes were decided by the expert panel for 2,3,4,7,8-pentachlorodibenzofuran (PeCDF) (TEF = 0.3), 1,2,3,7,8-pentachlorodibenzofuran (PeCDF) (TEF = 0.03), octachlorodibenzo-p-dioxin and octachlorodibenzofuran (TEFs = 0.0003), 3,4,4',5-tetrachlorbiphenyl (PCB 81) (TEF = 0.0003), 3,3',4,4',5,5'-hexachlorobiphenyl (PCB 169) (TEF = 0.03), and a single TEF value (0.00003) for all relevant mono-ortho-substituted PCBs. Additivity, an important prerequisite of the TEF concept was again confirmed by results from recent in vivo mixture studies. Some experimental evidence shows that non-dioxin-like aryl hydrocarbon receptor agonists/antagonists are able to impact the overall toxic potency of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds, and this needs to be investigated further. Certain individual and groups of compounds were identified for possible future inclusion in the TEF concept, including 3,4,4'-TCB (PCB 37), polybrominated dibenzo-p-dioxins and dibenzofurans, mixed polyhalogenated dibenzo-p-dioxins and dibenzofurans, polyhalogenated naphthalenes, and polybrominated biphenyls. Concern was expressed about direct application of the TEF/total toxic equivalency (TEQ) approach to abiotic matrices, such as soil, sediment, etc., for direct application in human risk assessment. This is problematic as the present TEF scheme and TEQ methodology are primarily intended for estimating exposure and risks via oral ingestion (e.g., by dietary intake). A number of future approaches to determine alternative or additional TEFs were also identified. These included the use of a probabilistic methodology to determine TEFs that better describe the associated levels of uncertainty and "systemic" TEFs for blood and adipose tissue and TEQ for body burden.

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Effects of environmental pollutants on gut microbiota.

Yuanxiang Jin, Sisheng Wu, Zhaoyang Zeng … (2017)

Environmental pollutants have become an increasingly common health hazard in the last several decades. Recently, a number of studies have demonstrated the profound relationship between gut microbiota and our health. Gut microbiota are very sensitive to drugs, diet, and even environmental pollutants. In this review, we discuss the possible effects of environmental pollutants including antibiotics, heavy metals, persistent organic pollutants, pesticides, nanomaterials, and food additives on gut microbiota and their subsequent effects on health. We emphasize that gut microbiota are also essential for the toxicity evaluation of environmental pollution. In the future, more studies should focus on the relationship between environmental pollution, gut microbiota, and human health.

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Environmental toxicants and autism spectrum disorders: a systematic review

D Rossignol, S J Genuis, R Frye (2014)

Although the involvement of genetic abnormalities in autism spectrum disorders (ASD) is well-accepted, recent studies point to an equal contribution by environmental factors, particularly environmental toxicants. However, these toxicant-related studies in ASD have not been systematically reviewed to date. Therefore, we compiled publications investigating potential associations between environmental toxicants and ASD and arranged these publications into the following three categories: (a) studies examining estimated toxicant exposures in the environment during the preconceptional, gestational and early childhood periods; (b) studies investigating biomarkers of toxicants; and (c) studies examining potential genetic susceptibilities to toxicants. A literature search of nine electronic scientific databases through November 2013 was performed. In the first category examining ASD risk and estimated toxicant exposures in the environment, the majority of studies (34/37; 92%) reported an association. Most of these studies were retrospective case–control, ecological or prospective cohort studies, although a few had weaker study designs (for example, case reports or series). Toxicants implicated in ASD included pesticides, phthalates, polychlorinated biphenyls (PCBs), solvents, toxic waste sites, air pollutants and heavy metals, with the strongest evidence found for air pollutants and pesticides. Gestational exposure to methylmercury (through fish exposure, one study) and childhood exposure to pollutants in water supplies (two studies) were not found to be associated with ASD risk. In the second category of studies investigating biomarkers of toxicants and ASD, a large number was dedicated to examining heavy metals. Such studies demonstrated mixed findings, with only 19 of 40 (47%) case–control studies reporting higher concentrations of heavy metals in blood, urine, hair, brain or teeth of children with ASD compared with controls. Other biomarker studies reported that solvent, phthalate and pesticide levels were associated with ASD, whereas PCB studies were mixed. Seven studies reported a relationship between autism severity and heavy metal biomarkers, suggesting evidence of a dose–effect relationship. Overall, the evidence linking biomarkers of toxicants with ASD (the second category) was weaker compared with the evidence associating estimated exposures to toxicants in the environment and ASD risk (the first category) because many of the biomarker studies contained small sample sizes and the relationships between biomarkers and ASD were inconsistent across studies. Regarding the third category of studies investigating potential genetic susceptibilities to toxicants, 10 unique studies examined polymorphisms in genes associated with increased susceptibilities to toxicants, with 8 studies reporting that such polymorphisms were more common in ASD individuals (or their mothers, 1 study) compared with controls (one study examined multiple polymorphisms). Genes implicated in these studies included paraoxonase (PON1, three of five studies), glutathione S-transferase (GSTM1 and GSTP1, three of four studies), δ-aminolevulinic acid dehydratase (one study), SLC11A3 (one study) and the metal regulatory transcription factor 1 (one of two studies). Notably, many of the reviewed studies had significant limitations, including lack of replication, limited sample sizes, retrospective design, recall and publication biases, inadequate matching of cases and controls, and the use of nonstandard tools to diagnose ASD. The findings of this review suggest that the etiology of ASD may involve, at least in a subset of children, complex interactions between genetic factors and certain environmental toxicants that may act synergistically or in parallel during critical periods of neurodevelopment, in a manner that increases the likelihood of developing ASD. Because of the limitations of many of the reviewed studies, additional high-quality epidemiological studies concerning environmental toxicants and ASD are warranted to confirm and clarify many of these findings.

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Author and article information

Contributors

Nina Iszatt: nina.iszatt@fhi.no

Stefan Janssen: stefan.m.janssen@gmail.com

Virissa Lenters: virissa@gmail.com

Cecilie Dahl: cecilie.dahl@medisin.uio.no

Hein Stigum: hein.stigum@fhi.no

Rob Knight: robknight@ucsd.edu

Siddhartha Mandal: sid.stat.iitk@gmail.com

Shyamal Peddada: shyamal.peddada@gmail.com

Antonio González: antgonza@gmail.com

Tore Midtvedt: tore.midvedt@ki.se

Merete Eggesbø: +47 2107 8206 , merete.eggesbo@fhi.no

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 27 February 2019

Publication date PMC-release: 27 February 2019

Publication date Collection: 2019

Volume: 7

Electronic Location Identifier: 34

Affiliations

[1 ]ISNI 0000 0001 1541 4204, GRID grid.418193.6, Department of Environmental Exposure and Epidemiology, Infection Control and Environmental Health, , Norwegian Institute of Public Health, ; PO Box 222, Skøyen, 0213 Oslo, Norway

[2 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Department of Pediatrics, , University of California San Diego, ; 9500 Gilman Drive, La Jolla, CA 92093 USA

[3 ]ISNI 0000 0001 2176 9917, GRID grid.411327.2, Department of Pediatric Oncology, Hematology and Clinical Immunology, , Heinrich-Heine University Dusseldorf, ; Dusseldorf, Germany

[4 ]ISNI 0000 0004 1936 8921, GRID grid.5510.1, Department of Community Medicine and Global Health, , University of Oslo, ; Kirkeveien 166, Fredrik Holsts hus, 0450 Oslo, Norway

[5 ]ISNI 0000 0001 1541 4204, GRID grid.418193.6, Department of Non-communicable Disease, , Norwegian Institute of Public Health, ; PO Box 222, Skøyen, 0213 Oslo, Norway

[6 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Center for Microbiome Innovation, , University of California San Diego, ; 9500 Gilman Drive, La Jolla, CA 92093 USA

[7 ]ISNI 0000 0001 2107 4242, GRID grid.266100.3, Department of Computer Science and Engineering, , University of California San Diego, ; 9500 Gilman Drive, La Jolla, CA 92093 USA

[8 ]ISNI 0000 0004 1761 0198, GRID grid.415361.4, Public Health Foundation of India, ; Delhi NCR, Plot No. 47, Sector 44, Institutional Area Gurgaon, Gurgaon 122002, India

[9 ]ISNI 0000 0001 2110 5790, GRID grid.280664.e, Biostatistics Branch, , National Institute of Environmental Health Sciences (NIEHS), ; 111 T.W. Alexander Drive, Durham, NC 27709 USA

[10 ]ISNI 0000 0004 1937 0626, GRID grid.4714.6, Department of Microbiology, Tumor and Cell Biology, , Karolinska Institute, Nobels väg 16, Solna Campus, ; Box 280, SE-171 77 Stockholm, Sweden

Article

Publisher ID: 645

DOI: 10.1186/s40168-019-0645-2

PMC ID: 6393990

PubMed ID: 30813950

SO-VID: c24a1eec-ce59-4fdf-a45e-c69715807c42

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 28 September 2018

Date accepted : 3 February 2019

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Keywords: breast milk,toxicants,short-chain fatty acids,infant gut microbiome,birth cohort

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Keywords: breast milk, toxicants, short-chain fatty acids, infant gut microbiome, birth cohort

Environmental toxicants in breast milk of Norwegian mothers and gut bacteria composition and metabolites in their infants at 1 month

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Most cited references 43

The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds.

Effects of environmental pollutants on gut microbiota.

Environmental toxicants and autism spectrum disorders: a systematic review

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