Status and Trends of Polybrominated Diphenyl Ethers (PBDEs) in Biota and Sediment

Polybrominated diphenyl ethers (PBDEs) are a group of 209 different congeners. Their main use is as flame retardants in different types of material including plastics, textiles, and electronic products. The three major commercial PBDE mixtures that have been produced are pentaBDE, octaBDE and decaBDE. Globally, decaBDE is the most widely used.

PBDEs are flame-retardants of the additive type, which means that they are physically combined with the material being treated rather than chemically combined (as in reactive flame retardants) and are more likely to diffuse out of the products (European Commission, 2001, 2003; Hutzinger and Thoma, 1987 cited in Alaee et al., 2003). Leakage of PBDE occurs during production, use, or disposal of products, and PBDEs are mainly transferred to the ocean via rivers and atmospheric transport (OSPAR, 2009). The presence of PBDEs in air samples from Arctic Canada, for example, provides evidence of their long-range transport (de Wit, 2002).

The advantage of these compounds for industry is their high resistance to acids, bases, heat, light, and reducing and oxidising compounds. However, this becomes a disadvantage in the environment where they persist for a very long time. Increased concentrations of these compounds have been measured in environmental samples since the 1970s (de Wit, 2002). PBDEs are toxic, are persistent in the environment and can bioaccumulate. As a result, the PBDE substances included in the commercial pentaBDE- and octaBDE-mixtures were banned in the European Union in 2004, and since 2009 have been listed under the Stockholm Convention (2009), meaning that a majority of countries worldwide have agreed to phase out these compounds.

PBDE has been reported to be neurotoxic and immunotoxic, and to affect thyroid hormone receptors in sensitive human populations (de Wit, 2002). Effects on behaviour learning (Eriksson et al., 2006a, b) and hormonal function (Legler, 2008) have been reported in mammals, while reduced reproductive success has been documented in birds (Fernie et al., 2009).

Smaller PBDE molecules are more toxic and bioaccumulate more readily than larger molecules. Debromination of highly brominated BDEs (such as decaBDE) to these smaller forms is a possibility and justifies monitoring based on a broad set of congeners. All PBDEs are hydrophobic or ultra-hydrophobic substances that do not dissolve in water and bind strongly to soil or sediment (PBDEs are more mobile in the atmosphere because they attach to airborne particulates; dust, soot, smoke, and liquid droplets). As a result, PBDEs in sediment are not very mobile and unlikely to volatilise from the water phase. The higher the degree of bromination, the lower the water solubility. PBDEs can be photodegraded in the environment (de Wit 2004; Pan et al., 2016).

The use of substance groups pentaBDE and octaBDE mixtures has been banned in the European Union since 2004 (Commission regulation (EC) No 552/2009). TetraBDE, pentaBDE, hexaBDE and heptaBDE were listed under the Stockholm Convention in 2009 and decaBDE in 2017 (Stockholm Convention, 2009; 2022; EU,2019). As a result, Parties to the Convention must act to eliminate the production and use of these compounds. Although there is no production within the European Union, existing stocks of PBDE-containing products may still act as a diffuse source.

The European Foods Safety Authority recommended eight substances (congeners) of certain interest to monitor: triBDE-28, tetraBDE-47, pentaBDE-99, pentaBDE-100, hexaBDE-153, hexaBDE-154, heptaBDE-183 and decaBDE-209 (EFSA, 2006). These were selected on the basis of analytical feasibility for their measurement, production volumes (as registered in 2006), their occurrence in food and feed, their persistence in the environment and their toxicity. For environmental monitoring within the European Union, environmental quality standards have been derived for these congeners excluding BDE-183 and BDE-209 (European Commission, 2011).

Assessment criteria

Two assessment criteria are used to assess PBDE concentrations in sediment and biota: background assessment concentrations (BACs) and Federal Environmental Quality Guidelines (FEQGs).

BACs were developed by OSPAR and for synthetic substances used for testing whether concentrations are close to zero - the ultimate aim of the OSPAR Hazardous Substances Strategy 2010-2020. BACs are statistical tools that for synthetic substances are defined in relation to low concentrations, which enable statistical testing of whether observed concentrations could be considered to be near zero. BACs are calculated according to the method set out in OSPAR (2020a; 2021).

FEQGs are used to assess the status of both sediment and biota (fish and shellfish). Concentrations below the FEQGs should not cause any chronic effects on marine organisms. They were developed under the Canadian Environmental Protection Act from 1999, are available for individual PBDE congeners in sediment and biota and were derived from ecotoxicological testing (Environment Canada, 2013). FEQGs are described in detail in the OSPAR (2020b) background document for sediment and biota.

An alternative to the use of the FEQGs for biota could be the Water Framework Directive (WFD) Environmental Quality Standards (EQS). The EQS is based on the human health QS (which was the lower of the calculated QSs). Due to the method used to assign the fish EQS value for PBDE (0,0085 μg kg^-1 wet weight) it is very low compared to typically reported environmental concentrations in biota (even in remote environments, e.g., the Arctic). Most PBDE data for biota therefore exceeds the EQS value (OSPAR 2020b). The EQS for PBDE is also low compared to analytical capabilities (LOW) of several monitoring laboratories. The QS for secondary poisoning is more similar to the FEQG (for BDE47; 44 μg kg^-1 wet weight). However, while the FEQGs are available for individual congeners the EQS is based on a sum of six PBDE congeners some of which are missing from some of OSPAR’s Coordinated Environmental Monitoring Programme (CEMP) data series and the QS provides a less stringent assessment of the more toxic homologues (OSPAR 2020b). The FEQGs were therefore chosen as the assessment criteria (for interested parties, an assessment of observations against the EQS is available at the link below and shows that the mean concentrations for all time series exceeds the EQS: https://dome.ices.dk/OHAT/trDocuments/2022/regional_assessment_biota_pbdes_health.html ).

For CEMP the organic contaminant concentrations in sediment are normalised to 2,5% organic carbon (the FEQGs were multiplied by a factor 2,5).
For fish, the FEQG is adjusted to a lipid weight basis (assuming the whole fish used in the toxicity trials have a 5% lipid content) by multiplying the FEQG (on a wet weight basis) by 20 (Table a, OSPAR 2020b). Fish concentrations are then usually assessed on a lipid weight basis. However, if the typical lipid content for the species / tissue is < 3% ( https://dome.ices.dk/OHAT/trDocuments/2022/help_ac_basis_conversion.html ), fish concentrations are assessed on a wet weight basis, with the FEQGs adjusted to a wet weight basis using the conversion factors found at https://dome.ices.dk/OHAT/trDocuments/2022/help_ac_basis_conversion.html . Shellfish concentrations are assessed on a dry weight basis (since too few samples have supporting lipid weight measurements) with the FEQGs adjusted to a dry weight basis using the conversion factors found at https://dome.ices.dk/OHAT/trDocuments/2022/help_ac_basis_conversion.html.

Table a notes: dw, dry weight; lw, lipid weight. notes: for sediment BACs are normalised to 2,5% organic carbon. For biota BACs and FEQGs are converted to other bases (ww, dw) using species-specific conversion factors ( https://dome.ices.dk/OHAT/trDocuments/2022/help_ac_basis_conversion.html ).
Denmark has reservations regarding the FEQG threshold values.

Sediment, fish, and shellfish status

Similar analyses explored status at the assessment area scale. Two summary measures were considered: the log ratio of the fitted concentration in the last monitoring year to the FEQG; and the log ratio of the fitted concentration in the last monitoring year to the BAC. Impacted monitoring sites were also included in these analyses.

Finally, concentration profiles across congeners at the assessment area scale were explored using the fitted log concentration in the last monitoring year.

The total number of stations with trend information was 32 for sediment and 186 for biota and for status information it was 78 for sediment and 250 for biota. Of these, 4 to 50% of stations were excluded during the selection process described above for the four different assessment types. The final number of stations for each assessment type used in each assessment area are shown in Table b.

Sediment and biota (fish, shellfish, bird eggs and mammals) temporal trends

For each PBDE congener and monitoring site with observations (see specifics below), contaminant temporal trends and status were assessed using the methods described in the contaminants’ online assessment tool ( http://dome.ices.dk/ohat/?assessmentperiod=2022 ). The results from the site-specific analyses were then synthesised to create a regional assessment based on mean concentration and trends within the 14 OSPAR contaminant assessment areas.

The temporal trend assessments included data from those monitoring sites that were representative of general conditions and excluded data from those monitoring sites impacted by a point source of PBDE.  Only stations with at least one year with data in the period 2015-2020 and at least five years of data along the whole time series are included in the regional assessment. The analysis was further restricted to assessment areas where there were at least three monitoring sites with trend information and where those monitoring sites had a reasonable geographic spread. For the temporal trend analysis of biota a few bird eggs and mammals time series from northerly regions were used as supplement to the fish and shellfish data. These are limited to the trend analysis and not used for the status as the thresholds for status analysis are specific to fish (Environment Canada, 2013).

For sediment, the PBDE concentrations are normalised to account for changes in the bulk physical composition of the sediment, such as particle size distribution or organic carbon content, for all areas included in the sediment assessment.

The temporal trend for each PBDE congener at each monitoring site was summarised by the estimated annual change in log concentration, with its associated standard error. The annual change in log concentration was then modelled by a linear mixed model with a fixed effect:

~    OSPAR contaminants assessment areas
and random effects:
~    congener + congener: OSPAR contaminants assessment area + monitoring site + congener: monitoring site [biota only] + residual variation.

The choice of fixed and random effects was motivated by the assumption that the PBDE congeners would have broadly similar trends, since they have similar sources. Thus, the fixed effect measures the common trend in PBDE congener in each contaminant’s assessment area and the random effects measure variation in trends:

• between congeners common across OSPAR contaminants assessment areas (congener);
• between congeners within OSPAR contaminants assessment areas (congener: contaminants assessment area);
• between congeners but common across tissues and species within monitoring sites (congener: monitoring site); and
• residual variation.

The residual variation is made up of two terms: the variation associated with the estimate of the trend from the individual time series, which is assumed known (and given by the square of the standard error); and a term which accounts for any additional residual variation not explained by the other fixed and random effects.

Evidence of trends in PBDE concentrations at the assessment area scale was then assessed by plotting the estimated fixed effects with point-wise 95% confidence intervals. Differences between congeners were explored by plotting the predicted trend for each congener and for each congener / assessment area combination with point-wise 95% confidence intervals.

Differences in methodology used for the QSR 2023 compared with the QSR 2010 and the Intermediate Assessment 2017

For the QSR 2023, a meta-analysis is used to synthesise the individual time series results and provide an assessment of temporal trend and a calculation of status at the assessment area level. Meta-analyses consider both the estimate of trend or status in each time series and the uncertainty in that estimate. This was the same method used in the Intermediate Assessment 2017 (OSPAR 2017) while they provide a more objective regional assessment than was possible in the QSR2010, where a simple tabulation of the trend and status at each monitoring site was presented.

In the QSR 2023 FEQGs are used to assess the status of both sediment and biota (Table a). No assessment criteria were used in the QSR 2010 or Intermediate Assessment 2017.

PBDE concentrations are measured in sediment and fish and shellfish samples taken annually (or every few years) from monitoring sites throughout much of the Arctic waters (biota only), Greater North Sea, Celtic Seas, and Bay of Biscay and Iberian Coast (biota only). The number of monitoring sites varies widely between assessment areas, with the Greater North Sea having the most. Only assessment areas with at least three monitoring sites and a reasonable geographic spread were included in the assessment of status and temporal trends. Observations for PBDE in biota spanned the period 1999-2020 and for PBDE in sediment the period 2006-2020 with data from at least one station.

PBDE concentrations in sediment, fish and shellfish were compared to the OSPAR Background Assessment Concentrations (BAC) and Federal Environmental Quality Guidelines (FEQG). Concentrations below the FEQG should not cause any chronic effects on marine organisms.

Mean sediment PBDE concentration for the various congeners (normalised to organic carbon) relative to the BAC for each assessment area are shown in Figure a. Mean congener sediment concentrations are above BAC except for BDE154 in the Irish and Scottish West coast and BDE85 and BDE28 in the Northern North Sea and Irish Sea. For fish and shellfish (Figure b), the mean concentration of only two congeners (BDE153 and BDE28) were below BAC in only one assessment area (the Northern Bay of Biscay).

All mean congener PBDE concentrations in sediment were significantly below the FEQG in all the assessment areas except BDE209 in the Irish Sea. While the other four sediment assessment areas do not have BDE209 above the FEQGs they are still a factor 10-100 above the concentrations found for the other congeners (Figure a). This could be a result of the relative lower FEQG for PBDE209 than other congeners (Table a). Alternatively, higher historic exposure and/or a longer lifetime in the sediments for BDE209 due to high particle affinity and low biodegradability (Söderstrom et al., 2004) could also impact the result.

Overall, no adverse biological effects are expected based on the status assessment except in the Irish Sea sediment.

Temporal trends in PBDE concentrations in sediment and biota were assessed in areas where there were at least five years of data. The percentage yearly change for PBDE in each assessment area is shown in Figure c and Figure d. In most regions trends were stable or downwards. For sediments all PBDE congeners show a downward trend in the Irish Sea.

For fish and shellfish all PBDE congeners show a downward trend in Northern North Sea (except for BDE28) and the Irish Sea. There are also downward trends for some congeners and areas: Skagerrak and Kattegat (BDE47), Southern North Sea (BDE153, BDE100, BDE99, BDE47 and BDE28), Channel (BDE47 and BDE28), Irish and Scottish West Coast (BDE154, BDE100, BDE99 and BDE47), Celtic Seas (BDE100 and BDE47), Northern Bay of Biscay (BDE154, and BDE47) and Iberian Sea (BDE 100, BDE99 and BDE66)

A summary of individual time series results per monitoring site (across the OSPAR Maritime Area) for PBDE concentrations in sediment and biota is presented here ( https://dome.ices.dk/OHAT/?assessmentperiod=2022 ). In summary, at 51 out of 566 sediment monitoring series (individual congeners) across the OSPAR Maritime Area, mean concentrations of PBDE in sediment are above the FEQG. In no site out of 77 sediment monitoring series (individual congeners), have concentrations increased over the assessment period. While 17 sites showed a downward trend.

For fish and shellfish of 1 765 series (individual congeners), only 36 were above the FEQG and 17 out of 853 mean concentrations have increased over the assessment period, while 248 showed downward trends.  It should be noted that not all individual time series results are included in the assessments (see number of time series used in each assessment area in Table b), due to the criteria set out in the assessment methods.

Confidence Assessment

There is high confidence in the quality of the data used for this assessment. The data have been collected over many years using established sampling methodologies. There is sufficient temporal and spatial coverage and no significant data gaps in the areas assessed over the relevant time periods. The synthesis of monitoring site data for the assessment area scale are based on established and internationally recognised protocols for monitoring and assessment per monitoring site, therefore there is also high confidence in the methodology.

PBDE concentrations in both sediment and biota have in general been stable (54% of assessed areas) or declining (46% of assessed areas) across the OSPAR assessment area for the past 20 years.  

Within the areas assessed, there is no reason to suspect general chronic effects on marine organisms as concentrations are in general below the FEQG. As the time series analysis further indicates stable to declining trends for all areas (averaged PBDEs) there is no reason to suspect that this will change over the coming years. However, no assessment areas had concentrations below the BAC (close to zero) and the environment is therefore still impacted by these man-made substances although this impact is declining.

For individual time series there is some variability but only a few stations show significantly increasing trends. This indicates that there are local conditions affecting these sites but does not change the overall picture of declining concentrations.

While status and trends are reported from all OSPAR Regions for biota, the sediment data is still limited to the Greater North Sea and the Celtic Seas. PBDE have a high affinity for particulates as they are highly hydrophobic, and therefore a potential long lifetime in sediments. Despite sediment concentrations being below the FEQGs it would be good to include data from all the Regions in future assessments.

There are few monitoring sites for the assessment of temporal trends and status of PBDE in sediment apart from Regions II and III. This means the assessment cannot be considered representative for the OSPAR Maritime Area as a whole. Cooperation between OSPAR and the Arctic Monitoring and Assessment Programme (AMAP) could improve access to data for Region I.

PBDE bioaccumulate, some congeners more than others (Environment Canada, 2013). A strategy is needed to make data from different monitoring species, such as shellfish and different trophic level fish, comparable.

The method used to assign the biota Environmental Quality Standard (EQS) that is derived within European Union to protect marine and freshwater ecosystems as well as humans from adverse effects of chemicals in the aquatic environments has resulted in a value for PBDE that is very low compared to typically reported environmental concentrations in biota (even for pristine areas). It therefore requires further investigation before it can be used in the OSPAR Maritime Area. Further, it is recommended to create congener specific values as the toxicity varies greatly between congeners as shown by the work on the FEQGs done by Environment Canada (2013; Table a).

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