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. 2023 Feb 28;192(2):223–232. doi: 10.1093/toxsci/kfad017

Excretion of polybrominated diphenyl ethers and AhR activation in breastmilk among firefighters

Alesia M Jung 1,2,2, Shawn C Beitel 3,2, Shannon L Gutenkunst 4,5, Dean Billheimer 6,7,8, Sara A Jahnke 9, Sally R Littau 10, Mandie White 11, Christiane Hoppe-Jones 12, Nathan J Cherrington 13,14, Jefferey L Burgess 15,16,✉
PMCID: PMC10109531  PMID: 36856729

Abstract

Excretion of toxicants accumulated from firefighter exposures through breastmilk represents a potential hazard. We investigated if firefighting exposures could increase the concentration of polybrominated diphenyl ethers (PBDEs) and aryl hydrocarbon receptor (AhR) activation in excreted breastmilk. Firefighters and nonfirefighters collected breastmilk samples prior to any firefighting responses (baseline) and at 2, 8, 24, 48, and 72 h after a structural fire (firefighters only). Five PBDE analytes (BDEs 15, 28, 47, 99, and 153) detected in at least 90% of samples were summed for analyses. The AhR in vitro DR CALUX bioassay assessed the mixture of dioxin-like compounds and toxicity from breastmilk extracts. Baseline PBDEs and AhR responses were compared between firefighters and nonfirefighters. Separate linear mixed models assessed changes in sum of PBDEs and AhR response among firefighters over time and effect modification by interior or exterior response was assessed. Baseline PBDE concentrations and AhR responses did not differ between the 21 firefighters and 10 nonfirefighters. There were no significant changes in sum of PBDEs or AhR response among firefighters over time postfire, and no variation by interior or exterior response. Plots of sum of PBDEs and AhR response over time demonstrated individual variation but no consistent pattern. Currently, our novel study results do not support forgoing breastfeeding after a fire exposure. However, given study limitations and the potential hazard of accumulated toxicants from firefighter exposures excreted via breastfeeding, future studies should consider additional contaminants and measures of toxicity by which firefighting may impact maternal and child health.

Keywords: firefighters, occupational exposure, polybrominated diphenyl ethers, aryl hydrocarbon receptor activation, maternal and child health

Although firefighters may be exposed to contaminants known to have negative effects on an individual’s overall health (Burgess et al., 2001; Daniels et al., 2014; Jung et al., 2021; Kales et al., 2007), the excretion of accumulated toxicants through the breastmilk of lactating firefighters may represent a potential hazard to breastfeeding infants. Among firefighter exposures, combustion products in smoke can consist of a complex mixture of benzene, heavy metals, polycyclic aromatic hydrocarbons (PAHs), and brominated flame-retardants, among others (IARC, 2010). Unfortunately, even with the advanced personal protective equipment firefighters wear, contaminants have been found to be elevated in their bodies after a fire, such as volatile organic compounds, PAHs, and polybrominated diphenyl ethers (PBDEs) (Burgess et al., 2020; Fent et al., 2020; Hoppe-Jones et al., 2021; Park et al., 2015).

Persistent organic pollutants (POPs), one group of compounds that firefighters may be exposed to during fire suppression, are known to resist chemical and biodegradation and bioaccumulate. Among POPs, dioxins, furans, polychlorinated biphenyls (PCBs), PBDEs, PAHs, and heavy metals have been found at elevated levels in firefighters compared with nonfirefighters (Dobraca et al., 2015; Fent et al., 2020; Mayer et al., 2021; Park et al., 2015). Elevated exposures to these compounds have been linked to learning disabilities, cancer, and birth defects, along with behavioral, neurological, reproductive, and immunological disorders (Engwa et al., 2019; Sweetman et al., 2005). Additional halogenated compounds including polychlorinated and polybrominated dibenzo-p-dioxins and dibenzofurans (PCDD/PCDFs and PBDD/PBDFs) can also accumulate in firefighters (Shaw et al., 2013). PBDEs, PBDDs, PBDFs, PCDDs, and PCDFs may have similar toxicities to dioxin-like compounds (Shaw et al., 2013), as they all interact with the aryl hydrocarbon receptor (AhR) (Hooper and McDonald, 2000). With the similar toxicity pathway involving dioxin-like compounds binding to the AhR, inducing AhR-related genes and subsequent transformation to toxic metabolites (Behnisch et al., 2001), the AhR in vitro DR CALUX bioassay was used to assess the overall AhR-mediated toxicity. With complex mixtures of contaminants in many matrices, in vitro bioassays can provide an assessment of the mixture by characterizing it as the overall response of a biological pathway without having to quantify many compounds.

PBDEs are of particular interest because they function as flame-retardants, and are found in a wide range of consumer products (Imm et al., 2009). They share planar structural similarities to dioxins, furans, PCBs, and PAHs, allowing them to interact with the AhR (Hooper and McDonald, 2000; Kodavanti and Loganathan, 2017; Peters et al., 2006). PBDEs can also have adverse effects similar to PCBs, including disruption of the immune, endocrine, and nervous systems (Kodavanti and Loganathan, 2017).

Though the prevalence of active-duty breastfeeding firefighters is unknown, there is concern for potential exposure to contaminants after the fire to breastfeeding children. Breastfeeding can provide many health benefits to infants, such as aiding the development of the immune system and decreasing the risk of developing diseases such as diabetes, cardiovascular disease, and various cancers (Binns et al., 2016; Dieterich et al., 2013; Mead, 2008). However, breastfeeding can also be a route of exposure to environmental contaminants such as heavy metals, per- and polyfluoroalkyl substances, and PBDEs, that may accumulate in body fat involved in breastmilk production (Marchitti et al., 2017; Mead, 2008; Mondal et al., 2014; Park et al., 2018). There are currently no research-based recommendations for breastfeeding postfire exposure and the scope of breastfeeding recommendations across U.S. fire departments is inconsistent. Published guidance from the National Fire Protection Association recommends that breastfeeding firefighters avoid unprotected exposure to toxic concentrations of heavy metals and other contaminants, but does not address specific work modifications (NFPA, 2022). Research examining contaminant exposure among female firefighters is limited; however, a previous study indicated that female firefighters had elevated serum concentrations of several per- and polyfluoroalkyl substances compared with office workers (Trowbridge et al., 2020). Because the recommended period of breastfeeding falls within a critical period of infant development, potential exposures to environmental contaminants that might negatively impact infant growth and development should be considered. Female firefighters may be exposed to elevated concentrations of contaminants during fire suppression activities and subsequently transfer these contaminants to their breastfeeding children.

Although firefighters have an increased risk of exposure to occupational toxicants, the degree that infants might be exposed via excretion of these compounds into breastmilk has yet to be determined. Therefore, the aims of this research were to identify if exposures obtained while firefighting increased the concentration of PBDEs and resulting overall AhR activation in excreted breastmilk, and the duration of potentially elevated levels.

Materials and methods

 

 

Participants

Study participants were recruited from a larger cohort study of female firefighters, the Health and Wellness of Women Firefighters Study, conducted by NDRI-USA and reviewed and approved by the NDRI-USA Institutional Review Board. The current study, including all study materials and protocols, was approved by the University of Arizona Institutional Review Board (approval No. 1000000379), and all participants provided informed consent prior to participation in the research. The women who participated resided in the United States, were at least 18 years old, and were breastfeeding at the time of the study. A total of 21 female incumbent firefighters and 10 female nonfirefighters were included in the study. The firefighters were distributed around the United States, with the nonfirefighter women being recruited by the participating firefighters, with similar age, ethnicity, and age of breastfeeding infant. Average age and other characteristics of the participants and their babies are listed in Table 1.

Table 1.

Characteristics of women firefighters and nonfirefighter controls

Firefighters
n = 21		 Nonfirefighters
n = 10		 p-Valuea
Age (years), mean (SD) 33.1 (2.9) 30.8 (4.0) .09
BMI (kg/m2), mean (SD) 24.8 (3.7) 27.3 (6.6) .32
Race/ethnicity, n (%) 1
 Non-Hispanic white 20 (95) 10 (100)
 Hispanic 1 (5) 0
Parity, n (%) .20
 Primiparous 10 (48) 3 (30)
 Multiparous 11 (52) 7 (70)
Age of current infant (months), mean (SD) 5.7 (2.8) 9.7(4.1) .02
Time between breastfeedings (hours), mean (SD) 3.3 (0.9) 4.4 (2.9) .28
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a

p-Values for continuous variables calculated using t-tests with unequal variances and for categorical variables using Fisher’s exact tests.

SD, standard deviation; BMI, body mass index.

Sample and data collection

Breastmilk samples were collected to measure concentrations of PBDEs along with AhR agonist activity using in vitro bioassays. A baseline breastmilk sample was collected from firefighters to represent an unexposed sample, which was collected a minimum of 72 h after any type of fire suppression activity. After responding to a fire, the participants were asked to provide 5 additional samples at the following times: 2, 8, 24, 48, and 72-h postfire. Only one baseline breastmilk sample was collected from each nonfirefighter. For sample collection, the participants washed their pump attachments in warm water prior to sample collection. The participants collected their sample with their breastmilk pump using the method they normally use, with the exception that they were asked not to apply any lotions, soaps, or perfumes prior to collection, and to wash their breasts with warm water before pumping. Polypropylene collection containers were supplied to the participants for the sample collection. Samples containers were frozen and shipped overnight to the University of Arizona, where they were processed immediately.

All participants completed a baseline survey administered at time of enrollment. Participants reported their age, height, weight, and race/ethnicity. Women were also asked to report details about the infant they were currently breastfeeding, including age of the infant, birth order, and the average time between breastfeedings. Firefighters also completed a postfire survey following the fire for which they provided postfire breastmilk samples. Information reported included type of fire, interior or exterior response since all firefighters reported responding to a structural fire, length of time spent on fire suppression activities, and time spent on air during fire suppression activities.

Sample preparation and extraction

Breastmilk samples were well mixed prior to processing. Lipid content was measured in duplicate using a Creamatocrit Plus (EKF Diagnostics, Boerne, Texas, U.S.) and aliquoted. All aliquots were stored at −80°C.

Extraction of breastmilk for AhR bioassay analysis began by denaturing the proteins by vortexing 10 ml of breastmilk with 5 ml of HPLC grade Acetone (Fisher Scientific, Hampton, New Hampshire, U.S.) for 2 min. A QuEChERS extraction kit EN 15662 method (Agilent Technologies, Santa Clara, California, U.S.) was then used where one pouch of powder was added to the sample and shaken vigorously for 2 min. Then 10 ml of HPLC grade hexane was added to the sample and shaken vigorously for 2 min. The sample was then centrifuged at 1000 × g for 3 min, and the supernatant was collected. Hexane was then added, shaken, vortexed again, for a total of 3 times, with the supernatant being combined. The supernatant was concentrated by evaporation under a gentle stream of nitrogen to a 1-ml volume. A clean-up step was then conducted by which a multilayer silica gel dioxin column (Sigma-Aldrich, St. Louis, Missouri, U.S.) was conditioned with 100 ml of hexane, the sample added, and then eluted with 100 ml of hexane. The eluted sample was then evaporated under a gentle stream of nitrogen, solvent exchanged to dimethyl sulfoxide (DMSO) (Sigma-Aldrich), and then brought up to 100 µl by weight. Extracts were stored at −20°C until analyzed.

Extraction of breastmilk for PBDE quantification followed a similar procedure as extraction for bioassay analysis with few modifications. Briefly, a 9 ml sample was spiked with a PBDE internal standard mix and extracted in the same manner as the AhR extraction procedure using acetone and the QuEChERS kit. A hand packed column consisting of glass wool, sodium sulfate, acidified silica (44% sulfuric acid), magnesium carbonate hydroxide pentahydrate, magnesium sulfate anhydrous, and potassium silicate anhydrous. The column was conditioned with 100 ml of hexane, sample added, and then eluted with 100 ml of hexane. The sample was evaporated under a gentle stream of nitrogen to approximately 1.0 ml. The sample was then run through a gel permeation chromatography column with a 1:1 mix of HPLC grade hexane: dichloromethane at a rate of 5 ml/min and collected during 13 and 17 min to isolate the PBDEs of interest and remove any remaining lipids. The resulting fraction was concentrated to dryness under a gentle stream of nitrogen, and then brought up to 100 µl by weight of nonane. Extracts were stored at −20°C until analyzed.

In vitro bioassay culture and exposure

DR CALUX cells (BioDetection Systems, Amsterdam, Netherlands) were cultured and exposed according to the manufacturer’s guidelines. Briefly, cells were seeded in 96-well plates at a density of 400,000 cells/ml, incubated at 37°C at 95% humidity and 5% CO2 for 24 h prior the exposure to sample extracts and reference compound at a final concentration of 0.8% DMSO. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (Sigma-Aldrich) was used as the model AhR agonist for this assay. The maximum concentration of sample was 0.8× in the well of the assay based on the 100× concentrated extract diluted by 125× to bring the solvent to 0.8%. All samples were tested in triplicate. Once exposed, cells were incubated for 24 h, then washed, lysed using a lysis reagent (BioDetection Systems), luminescence reagent added (BioDetection Systems), and luminescence read using a Molecular Devices FlexStation 3 multimode microplate reader (Molecular Devices, Sunnyvale, California, U.S.). Breastmilk extract results were calculated as TCDD equivalence to compare among samples, and lipid content was used for standardization.

Analytical quantification of PBDEs

Milk extracts were analyzed on a GC-MS/MS (Agilent Technologies). Limit of detections (LODs) and PBDE recoveries as well as values of measured PBDE congeners and AhR response levels above the LOD are presented in the Supplementary data. Isotopically labeled standards for each analyte were used to correct for losses during the extraction steps. Matrix spikes of both breastmilk and cow’s milk in each batch ensured that recoveries were within acceptable levels (80–120%) for each analyte. RoHS Screening PBDE Native PAR Spike Mix and RoHS screening PBDE cleanup spike mix (13C12, 99%) were purchased from Cambridge Isotope Laboratories Inc. (Tewksbry, Massachusetts, U.S.).

Statistical analysis

Baseline survey measurements of firefighters were compared with responses of nonfirefighters using 2-sample t-tests with unequal variances (for continuous variables) and Fisher’s exact tests (for categorical variables), where a p-value < .05 was considered statistically significant. Body mass index (BMI, kg/m2) was calculated using reported height and weight. Parity was determined using reported birth order and categorized as primiparous (current infant is first child), indicating the woman had given birth once, or multiparous (current infant is second child, third child, or other), indicating the woman had given birth previously.

Of the 9 PBDEs measured, 5 were above the limit of detection in at least 90% of all samples (BDEs 15, 28, 47, 99, and 153). Because of the strong correlations among these 5 PBDEs at baseline (Pearson’s correlation coefficient = 0.28–0.97) these PBDEs were summed and considered for the current analysis (hereafter referred to as sum PBDEs). PBDE and AhR response values were standardized using measured lipid content. The 2 main outcomes of interest were therefore sum PBDEs (ng/g lipid) and AhR response (TCDD/g lipid). One firefighter only had results for measured AhR activation and was not included in analysis of PBDEs. Because the distribution of PBDE levels was skewed, the data were log-10 transformed prior to all statistical analyses. Baseline levels of the main outcomes (sum PBDEs and AhR response) and the individual levels of the 5 PBDEs among firefighters were compared with nonfirefighters using 2-sample t-tests, and p < .05. Although statistical analyses were performed on the log-transformed data, for interpretability nontransformed group medians and interquartile ranges (IQR) were reported.

To investigate changes in levels of sum PBDEs and AhR response over time in firefighters after a fire, we performed a longitudinal data analysis using separate linear mixed models implemented with the lme4 R package (Bates et al., 2015). Linear mixed models contained categorical time (baseline, 2, 8, 24, 48, and 72-h postfire) as a fixed effect and participant as a random effect, allowing each firefighter to have a different intercept. We evaluated adjustment for potential confounding by other occupational variables of interest (total interior time at fire, total time on fire attack, reported percent time the firefighter was on air during fire attack, and reported percent time firefighter was on air during overhaul) by adding them to models one-at-a-time as a main effect and also as an interaction term with time. Variables that improved model fit (using the conditional Akaike information criterion as a metric) were included in our analyses. We also evaluated adjustment for age and BMI as a surrogate of prepregnancy BMI, previously reported to be associated with PBDE concentrations in human breastmilk (Daniels, 2010). Variables that were statistically significant (p-value < .05) were included in models.

Using our linear mixed models, we calculated the change in the main outcomes for each postfire time point compared with baseline. For sum PBDEs, these contrasts were presented as a ratio between postfire and baseline because the data had been log-transformed for analysis, then back-transformed to the original scale for interpretability. For AhR response, these contrasts were presented as the estimated difference between postfire and baseline. Results were adjusted for multiple comparisons using the dunnettx method in the emmeans R package (Russell V. Lenth (2021). emmeans: Estimated Marginal Means, aka Least-Squares Means, R package version 1.6.3. https://CRAN.R-project.org/package=emmeans). For a secondary analysis, we included interior or exterior response as an a priori effect modifier because previous research has demonstrated that firefighters who participated in interior responses had higher concentrations of urinary biomarkers of flame retardants than those who were exterior (Mayer et al., 2021). Sum of 5 PBDE and AhR response levels over time from the primary and secondary analyses were also plotted and stratified by (1) interior versus exterior response and by (2) participant. All analyses were performed using R version 3.6.2 (R Core Team, 2019).

Results

Our analysis included 21 firefighters and 10 nonfirefighters. The majority of participants were non-Hispanic white (97%) (Table 1). There were no significant differences between firefighters and nonfirefighters based on maternal age, BMI, race/ethnicity, and parity (p > .05). Firefighters were nonsignificantly older (mean 33.1 years compared with 30.8 years, p = .09) and had nonsignificantly lower BMI (mean 24.8 kg/m2 compared with 27.3 kg/m2, p = .32) than nonfirefighters. There was also no significant difference between firefighters and nonfirefighters regarding the frequency of breastfeeding (p = .28), though infants of firefighters were younger than infants of nonfirefighters (mean 5.7 months, standard deviation [SD] 2.8 compared with 9.7 months, SD 4.1; p = .02) (Table 1). All firefighters responded to structural fires prior to providing postfire breastmilk samples; 14 reported interior responses, 6 exterior responses, and 1 person did not specify a response.

Firefighters and nonfirefighters did not significantly differ based on their baseline PBDE and AhR response levels (Table 2). The 6 PBDEs not presented in the current analysis (BDEs 183, 197, 208, 206, and 209) are summarized in Supplementary Table 1. At baseline, the median level of sum PBDEs among firefighters was 9.89 ng/g lipid (IQR 5.07–15.26) and among nonfirefighters was 8.78 ng/g lipid (IQR 4.79–18.59), p = .76. The main contributors to this sum were BDE-47 and BDE-153, which comprised approximately 44% and 33% of the sum PBDEs across all participants, respectively. The mean AhR response level also did not vary between firefighters (31.57 pg TCDD/g lipid) and nonfirefighters (31.60 pg TCDD/g lipid) at baseline, p = .99.

Table 2.

Descriptive statistics of PBDEs levels and AhR responses in firefighters compared with nonfirefighters assessed at baseline

Firefighters
n = 21a 		Nonfirefighters
n = 10		 p-Valueb
PBDE (ng/g lipid),c median (IQR)
 BDE 15 0.07 (0.06–0.12) 0.09 (0.07–0.16) .82
 BDE 28 0.26 (0.17–0.48) 0.31 (0.14–0.44) .78
 BDE 47 3.77 (2.03–8.00) 3.52 (1.63–6.83) .71
 BDE 99 0.77 (0.36–1.12) 0.51 (0.24–1.07) .51
 BDE 153 3.21 (2.16–5.29) 2.91 (2.40–7.57) .79
 Sum of 5 PBDEs 9.89 (5.07–15.26) 8.78 (4.79–18.59) .76
AhR response (pg TCDD/g lipid), mean (SD) 31.57 (13.13) 31.60 (8.83) .99
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a

Twenty of 21 firefighters had measured PBDEs. All 21 firefighters had measured AhR response.

b

Due to skewness of distribution of PBDEs, PBDE p-values are calculated on log scale. Group medians and IQRs are not reported on the log scale for interpretability.

c

Values presented are standardized using measured fat content: (PBDE ng/ml)/(fat content g/ml) = standardized PBDE (ng/g lipid).

PBDE, polybrominated diphenyl ether; AhR, aryl hydrocarbon receptor; IQR, interquartile range; TCDD, 2,3,7,8-Tetrachlorodibenzodioxin; SD, standard deviation.

In our final linear mixed models, we did not observe significant changes in sum PBDEs among firefighters over time after a fire (Table 3), though the highest levels were observed 24 h after fire exposure for all fires combined and for interior fires and at 8 h for exterior fires. We would have detected (with 95% confidence) a difference between mean response at baseline and mean response at one of the postfire time points if responding to a fire changed mean sum PBDEs by a factor of 1.5. We also did not observe significant changes in AhR response levels among firefighters over time, after exposure to a fire (Table 4). Similarly, we would have detected (with 95% confidence) a difference between mean response at baseline and mean response at one of the postfire time points if responding to a fire changed mean AhR by a factor of 1.4, or 13.62 pg TCDD/g lipid.

Table 3.

Sum of 5 PBDEs (ng/g lipid) over time in firefighters postfire, by type of fire responsea

Time (Hours After Fire) Sum 5 PBDEs (ng/g Lipid) SE Ratio Compared with Baseline 95% CI
All fires (n = 20)b
 Baseline 9.9 2.0 — —
 2 9.8 2.0 0.99 0.78–1.26
 8 10.7 2.1 1.08 0.85–1.37
 24 12.0 2.4 1.21 0.95–1.54
 48 10.7 2.2 1.08 0.85–1.38
 72 10.6 2.1 1.07 0.84–1.35
Interior fires (n = 13)
 Baseline 9.9 2.6 — —
 2 9.4 2.5 0.95 0.71–1.29
 8 10.1 2.6 1.02 0.76–1.38
 24 12.3 3.2 1.24 0.92–1.68
 48 11.0 2.9 1.11 0.81–1.51
 72 11.4 3.0 1.15 0.85–1.55
Exterior fires (n = 6)
 Baseline 9.4 3.6 — —
 2 10.5 4.1 1.11 0.69–1.77
 8 11.2 4.3 1.19 0.76–1.85
 24 10.9 4.2 1.16 0.72–1.85
 48 9.2 3.6 0.98 0.61–1.56
 72 8.2 3.1 0.87 0.56–1.35
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a

Sum of 5 PBDEs includes BDEs 15, 28, 47, 99, and 153. Values presented have been back-transformed from log10 transformed values for interpretability.

b

Includes one fire response that was categorized as unknown (compared with interior or exterior).

PBDE, polybrominated diphenyl ether; SE, standard error; CI, confidence interval.

Table 4.

AhR response (pg TCDD/g lipid) over time in firefighters postfire, by type of fire responsea

Time (Hours After Fire) Estimated AhR Response (pg TCDD/g lipid) SE Estimated Difference Compared with Baseline 95% CI
All fires (n = 21)a
 Baseline 31.6 3.7 — —
 2 34.9 3.8 3.36 −6.34 to 13.05
 8 31.7 3.7 0.15 −9.40 to 9.71
 24 33.9 3.8 2.34 −7.35 to 12.04
 48 31.7 3.9 0.12 −9.73 to 9.96
 72 35.6 3.7 4.07 −5.49 to 13.62
Interior fires (n = 14) 
 Baseline 31.1 4.7 — —
 2 34.5 4.7 3.45 −8.77 to 15.68
 8 28.7 4.7 −2.33 −14.56 to 9.89
 24 34.0 4.7 2.87 −9.35 to 15.10
 48 30.9 4.8 −0.20 −12.69 to 12.30
 72 34.2 4.7 3.14 −9.09 to 15.37
Exterior fires (n = 6)
 Baseline 31.7 7.2 — —
 2 34.5 7.6 2.86 −16.91 to 22.63
 8 35.3 7.2 3.64 −15.03 to 22.32
 24 31.5 7.6 −0.21 −19.98 to 19.56
 48 30.1 7.6 −1.57 −21.32 to 18.17
 72 36.0 7.2 4.34 −14.33 to 23.02
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a

Includes 1 fire response that was categorized as unknown (compared with interior or exterior).

TCDD, 2,3,7,8-tetrachlorodibenzodioxin; SE, standard error; CI, confidence interval.

Initial examinations of the impact of other potential occupational confounders (total interior time at fire, total time on fire attack, reported percent time the firefighter was on air during fire attack, and reported percent time firefighter was on air during overhaul) in regression models yielded no significant results (results not shown), so these variables were not included in our analyses. Additionally, age and BMI were not significant in our models of sum PBDEs (p-value = .93 and .41, respectively) or our models of AhR response (p-value = .34 and .52, respectively) and were not included in our final models. In secondary analyses that included adjustment for effect modification by interior or exterior response, we similarly did not observe changes in sum PBDEs or AhR over time. Firefighters who reported interior responses did not have higher levels of sum PBDEs or AhR response compared with firefighters who reported exterior responses (Figs. 1 and 2). Plots of the sum PBDEs of individual firefighters over time (Figure 3) do not demonstrate a clear overall pattern over time, though there is variation in response between individuals. This remains true even when only firefighters who reported an interior response, who were hypothesized to have greater exposures than those who reported exterior responses, were considered. A similar lack of overall pattern over time, but variation between individuals, is observed for plots of AhR response levels of individual firefighters (Figure 4).

Figure 1.

Figure 1.

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Changes in sum of 5 PBDEs (BDes 15, 28, 47, 99, and 153) in firefighters following a structural fire, by interior (n = 13) or exterior response at fire (n = 6). Markers represent the estimated geometric mean for interior or exterior response at each time point and the bars represent the 95% CI, taken from the mixed model of log10(sum of 5 PBDEs) on the fixed categorical effects of time point, interior or exterior response, and their interaction, along with the random effect of firefighter (each firefighter was allowed to have a different intercept). Note that analyses were performed on the log10 scale (to make statistical tests valid for the skewed distribution of PBDEs), but results were back-transformed to the original scale for interpretability.

Figure 2.

Figure 2.

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Changes in AhR response levels in firefighters following a structural fire, by interior (n = 14) or exterior response at fire (n = 6). Markers represent the estimated mean for interior or exterior response at each time point and bars represent the 95% CI, taken from the mixed model of AhR response on the fixed categorical effects of time point, interior or exterior response, and their interaction, along with the random effect of firefighter (each firefighter was allowed to have a different intercept).

Figure 3.

Figure 3.

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Changes in sum of 5 PBDEs (BDEs 15, 28, 47, 99, and 153) in individual firefighters following a structural fire (n = 20). Markers represent the estimated geometric mean at each time point, taken from the mixed model of log10(sum of 5 PBDEs) on the fixed categorical effects of time point, interior or exterior response, and their interaction, along with the random effect of firefighter (each firefighter was allowed to have a different intercept). Note that analyses were performed on the log10 scale (to make statistical tests valid for the skewed distribution of PBDEs), but results were back-transformed to the original scale for interpretability.

Figure 4.

Figure 4.

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Changes in AhR response levels in individual firefighters following a structural fire (n = 21). Markers represent the estimated mean at each time point, taken from the mixed model of AhR response on the fixed categorical effects of time point, interior or exterior response, and their interaction, along with the random effect of firefighter (each firefighter was allowed to have a different intercept).

Discussion

We analyzed breastmilk extracts from female firefighters and nonfirefighters at baseline (prior to a fire exposure) and among firefighters at multiple timepoints after exposure to a structure fire. Baseline measurements of PBDEs and AhR response in breastmilk did not differ between firefighters and nonfirefighters. We also did not observe significant changes in sum PBDEs or AhR response among firefighters over time after fire exposure, and no variation by role at fire (interior or exterior response). Although plots of these outcomes varied over time between firefighters, there was no consistent overall pattern.

To our knowledge no prior studies of breastmilk comparing firefighters to nonfirefighters have been published. Furthermore, no studies of AhR in other biological samples comparing firefighters and nonfirefighters were identified. BDEs 47, 153, and 209 have been previously reported to be major contributors to the PBDE profile among firefighters (Ekpe et al., 2021; Park et al., 2015; Shaw et al., 2013). Findings from our analysis partially support these previous findings; BDE 47 and 153 comprised the majority of detected PBDEs among firefighters in our study, although BDE 209 was mostly below the level of detection. Previous studies evaluating serum PBDE concentrations have noted higher levels in firefighters compared with the general population (Ekpe et al., 2021; Park et al., 2015). A study of southern California firefighters detected higher levels of PBDEs (geometric mean 66.2 ng/g lipid, 95% CI 57.4–76.3) compared with those of adult men sampled in the 2003–2004 National Health and Nutrition Examination Survey (geometric mean 40.8 ng/g lipid, 95% CI 34.6–48.3) (Park et al., 2015). Similarly, a significant difference in PBDE concentrations was observed among Korean firefighters (mean 17.1 ng/g lipid, range 1.58–95.2 ng/g lipid) compared with the general population (1.39 ng/g lipid, range of nondetectable up to 7.53 ng/g lipid; p < .05). There is conflicting evidence whether or not concentrations of PBDEs and dioxin-like compounds in breastmilk and maternal blood are correlated (Kim et al., 2012; Todaka et al., 2010), however, a potentially low correlation could partially explain why our findings contrast with previous studies (Ekpe et al., 2021; Park et al., 2015).

In this novel investigation of firefighter breastmilk extracts, we did not observe significant changes in exposures over time after fire responses, which is generally consistent with findings from a limited number of longitudinal assessments of PBDE concentrations in postpartum breastmilk samples of nonfirefighters (Daniels et al., 2010; Dunn et al., 2010; Hooper et al., 2007; Lee et al., 2013). Early research reported that the concentrations of some PBDEs in breastmilk decreased 2–3% per month, during the first 6 postpartum months (Hooper et al., 2007). However, studies published since have largely been unable to detect significant changes in PBDEs during lactation, including over a 30-day period, 3-month period (examining day-to-day and month-to-month changes) and a 9-month period (Daniels et al., 2010; Dunn et al., 2010; Lee et al., 2013). Changes in concentrations of PBDEs may be highly variable between individuals (Daniels et al., 2010), which is supported by the wide variation that we observed between firefighters (Figure 3).

Though we were unable to identify other longitudinal assessments of AhR response in breastmilk, some studies have previously examined changes in concentrations of other dioxin-like compounds in breastmilk extracts, which could also potentially interact with the AhR-mediated toxicity pathway. Studies measuring metabolites of organochlorine pesticides, such as dichlorodiphenyldichloroethylene (DDE) and dichlorodiphenyltrichloroethane (DDT), reported declines in concentrations within the first 12 months postpartum (Du et al., 2016; Rogan et al., 1986). Other studies have examined levels of PCBs, though the findings are less consistent. A large study published in 1986, analyzing over 800 U.S. mothers, reported a decrease in measured PCBs over 6 months (20%) and 18 months (40%) (Rogan et al., 1986). However, a more recent 2007 study of 9 mothers did not observe such a substantial decline (<1% per month, over first 6 months postpartum) (Hooper et al., 2007).

Similar to our lack of longitudinal changes in the concentration of PBDEs in breastmilk following fire responses, a recent study of firefighters examining concentrations of serum PBDEs before and 24 h after a controlled structural fire exposure found that of the 6 most frequently detected PBDEs (BDEs 28, 47, 99, 100, 153, and 209), none were significantly increased 24 h after fire exposure (Mayer et al., 2021). Additionally, there were no significant changes in PBDE levels before and after fire exposure when stratified by job assignment (exterior, interior, or overhaul), similar to our analysis. No differences were seen when results were stratified by sex, though the number of women in the study was small (n = 4, 11%) (Mayer et al., 2021). However, Mayer et al. did observe elevated BDE 209 among firefighters compared with the general population (Mayer et al., 2021; Ospina et al., 2018). We did not assess BDE 209 in our current analysis, but conflicting evidence of correlations between PBDE concentrations in blood and breastmilk (Kim et al., 2012; Todaka et al., 2010) would have also limited any comparisons. A previous analysis of extracts from dermal wipes and urine samples collected from firefighters before and 2–4 h after a fire exposure observed an increased AhR response from dermal wipe extracts that was attenuated by the use of baby wipes postfire, as well as elevated urinary bioactivity postfire which correlated to 13 hydroxylated-PAHs (Beitel et al., 2020).

Breastmilk is widely acknowledged as the best source of nutrition for nearly all infants (Martin et al., 2016). Additionally, breastfeeding has many other clearly defined beneficial effects compared with the use of infant formula, including protection against infections through specific and nonspecific immune factors, long-term consequences for metabolism and disease risk later in life, and promotion of sensory and cognitive development (Cacho and Lawrence, 2017; Kramer et al., 2008; Oddy, 2002). However, potential environmental exposures through breastmilk should be considered given that early postnatal exposures to environmental contaminants through breastmilk have been associated with the development of diseases relating to immune dysfunction and infections (Cao et al., 2016), such as disruption of thyroid homeostasis, reproductive alterations, neurodevelopmental deficits, and cancer later in life (Linares et al., 2015). Neonatal exposure to certain PBDEs can result in indefinite aberrations in spontaneous behavior that intensify with increasing age (Eriksson et al., 2001). Similarly, PBDEs have been seen to have negative effects on cognitive development in animals within the first twelve months (Gascon et al., 2012). It is imperative to better understand the effects PBDEs specifically have on the body, along with be aware of additional exposure to children. Some research has shown an increase in concentrations of PBDEs in milk and serum and attributes this to increasing chronic exposure, whereas concentrations of other POPs including PCBs and dioxins are lessening in human serum and milk (Marchitti et al., 2017).

The health effects of firefighting on the offspring of children are largely unknown. However, there is a growing body of evidence that suggests that female firefighters are more likely to experience adverse reproductive health outcomes, including miscarriage and preterm birth compared with nonfirefighters (Jahnke et al., 2018;Jung et al., 2021, 2023). Additionally, risks for adverse pregnancy outcomes among firefighters may vary by roles in the fire service, examined as proxies for different occupational exposures (Jung et al., 2021, 2023). Other studies suggest that male firefighters have increased risk for infertility (Petersen et al., 2019) and that female firefighters have lower levels of anti-Müllerian hormone, a functional biomarker of ovarian reserve, compared with nonfirefighters (Davidson et al., 2022). Firefighting may be associated with adverse maternal and child health outcomes, though the mechanisms for these increased risks are not yet understood.

This was a unique study examining firefighter breastmilk that adds to the small but growing body of literature investigating occupational exposures among female firefighters. However, our overall sample size (21 firefighters and 10 nonfirefighter controls) limited our ability to adjust for potential confounders in regression models. We should have been able to detect differences between baseline and postfire time points if exposures at the fire caused an increase in sum PBDEs by a factor of 1.5 or an increase in the AhR response by a factor of 1.4 (increase in mean AhR activity equal to 13.62 pg TCDD/g lipid); this study was not powered to detect smaller changes in the sum PBDEs and AhR response. Finally, we evaluated only a limited set of contaminants (PBDEs) and a single measure of toxicity (AhR activation), so our study was not able to determine if other toxicants and measures of toxicity could be increased in firefighter breastmilk and with fireground exposure. Given these limitations and the known benefits of breastfeeding, our findings do not provide sufficient support for forgoing breastfeeding after a fire exposure to reduce exposure to PBDEs among breastfeeding infants. At this time, we cannot make any recommendations about the necessity or timing of pumping breastmilk for working firefighters who are also currently breastfeeding. Future studies should consider additional mechanisms, including other contaminants and measures of toxicity, by which firefighting may impact maternal and child health.

Supplementary Material

kfad017_Supplementary_Data
Click here for additional data file. (32.8KB, docx)

Acknowledgments

We would first like to thank the firefighters and their breastfeeding friends that participated in the current study. We would also like to thank Leanne M. Flahr, for her work processing and evaluating the study samples. Finally, we want to acknowledge the International Association of Women in Fire and Emergency Service (Women in Fire) for supporting the development of and recruitment for the Health and Wellness of Women Firefighters Study.

Contributor Information

Alesia M Jung, Department of Community, Environment and Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA; Department of Epidemiology and Biostatistics, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA.

Shawn C Beitel, Department of Community, Environment and Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA.

Shannon L Gutenkunst, Statistics Consulting Lab, BIO5 Institute, University of Arizona, Tucson, Arizona 85721, USA; Southwest Environmental Health Sciences Center, University of Arizona, Tucson, Arizona 85721, USA.

Dean Billheimer, Department of Epidemiology and Biostatistics, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA; Statistics Consulting Lab, BIO5 Institute, University of Arizona, Tucson, Arizona 85721, USA; Southwest Environmental Health Sciences Center, University of Arizona, Tucson, Arizona 85721, USA.

Sara A Jahnke, Center for Fire, Rescue, & EMS Health Research, NDRI-USA, Leawood, Kansas 66224, USA.

Sally R Littau, Department of Community, Environment and Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA.

Mandie White, Department of Community, Environment and Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA.

Christiane Hoppe-Jones, American Water, Belleville, Illinois 62223, USA.

Nathan J Cherrington, Southwest Environmental Health Sciences Center, University of Arizona, Tucson, Arizona 85721, USA; Department of Pharmacology and Toxicology, R. Ken Coit College of Pharmacy, University of Arizona, Tucson, Arizona 85721, USA.

Jefferey L Burgess, Department of Community, Environment and Policy, Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona 85724, USA; Southwest Environmental Health Sciences Center, University of Arizona, Tucson, Arizona 85721, USA.

 

The authors certify that all research involving human subjects was done under full compliance with all government policies and the Helsinki Declaration.

Supplementary data

Supplementary data are available at Toxicological Sciences online.

Funding

U.S. Federal Emergency Management Agency (FEMA) Assistance to Firefighters Grants (EMW-2015-FP-00848, EMW-2019-FP-00526); U.S. National Institute of Environmental Health Sciences (P30 ES006694, T32 ES007091).

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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Supplementary Materials

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