How Do Measured PBDE and HCBD Levels in River Fish Compare to The

Environmental Research 160 (2018) 203–211

Contents lists available at ScienceDirect

Environmental Research

journal homepage: www.elsevier.com/locate/envres

How do measured PBDE and HCBD levels in river ﬁsh compare to the T European Environmental Quality Standards?

⁎ Ethel Eljarrata, , Damià Barcelóa,b a Water and Soil Quality Research Group, Dept. of Environmental Chemistry, IDAEA-CSIC, Jordi Girona 18-26, 08034 Barcelona, Spain b Catalan Institute for Water Research (ICRA), H2O Building, Scientiﬁc and Technological Park of the University of Girona, Emili Grahit 101, 17003 Girona, Spain

ABSTRACT

This study evaluates the current situation regarding PBDE and HBCD levels in different river fish species. We collected published data in the last five years in different countries around the world. These levels of pollution were compared with Environmental Quality Standards (EQS) for biota established by the European Directive in the field of water policy. Although HBCD situation is not critical, with only some values exceeding the limit about 5 times, the PBDE levels clearly exceeded the established EQS, with 25% of fish samples exceeding up to ten thousand times. Although it is expected that levels of pollution by PBDEs will decrease over the next years due to the ban in their use, it is not expected that this decrease will reach the EQS values by the end of 2021, as demanded by the European Directive. Hence, it is necessary to implement new strategies in order to minimize the impact of PBDEs on the environment.

1. Introduction homogeneous materials shall be tolerated (ECD, 2009; Kemmlein et al., 2009). For the US and Canadian markets, companies decided to phase Flame retardants (FRs) are a group of compounds which are added out voluntarily the production, import and sale of Deca-BDE by the end or applied to materials (plastics, furniture, vehicles, electronic of 2012 (BSEF, 2012). However, in Asia, the use of Deca-BDE is not devices …) to increase their fire resistance. One of the most widely used under any regulatory restrictions (BSEF, 2009). FRs were polybromodiphenyl ethers (PBDEs), which are typically pro- Hexabromocyclododecane (HBCD) is another widely applied bro- duced at three different degrees of bromination, i.e., Penta-BDE, Octa- minated FR, mainly used in thermal insulation building materials, up- BDE, and Deca-BDE commercial mixtures. These compounds have a holstery textiles, and electronics as a flame retardant. The technical high lipophilicity (log Kow 5.98–9.97) and therefore they can be product consists of several isomers, the most abundant ones being α-, β- bioaccumulated and biomagnified along the food chain (Eljarrat et al., and γ-HBCD. While γ-HBCD dominates the technical product, α-HBCD 2007; Barón et al., 2014, 2015a). Moreover, several toxic properties accumulates mainly in the food chain (Morris et al., 2004; Covaci et al., have been reported for PBDEs: they can act as endocrine disruptors and 2006). The physical-chemical properties of HBCD are similar to some affect neurological, thyroid and liver activity (Hana et al., 2004; Lee PBDEs (log Kow 5.6) and therefore it can be found in wildlife (Guerra et al., 2010). et al., 2012) and in humans (Eljarrat et al., 2009). Some studies indicate Due to its presence in the environment and its proved toxicity, a possible role of HBCD as an endocrine disruptor (Palace et al., 2008). Penta- and Octa-BDE commercial mixtures have been banned in the HBCD has recently been listed as a POP, and the Stockholm European Union (EU) and in some states of the USA from 2004 (La Convention decided to add it under Annex A, legislating its manu- Guardia et al., 2006), and also banned in Canada from 2006. In 2009, facture and formulation. However, under specific circumstances (i.e., they were designated as new persistent organic pollutants (POPs) and their use is allowed for expanded polystyrene and extruded polystyrene the Stockholm Convention decided to add the commercial mixtures in buildings), HBCD may still be used until 2024. with four, five, six and seven bromines to the Annex A, to end their On the other hand, chemical pollution of surface water poses a production and use (UNEP, 2015). As regards the Deca-BDE commercial threat to the aquatic environment, with effects such as acute and mixture, only in the EU was their use strictly prohibited in 2008: Deca- chronic toxicity in aquatic organisms, accumulation of pollutants in the BDE can no longer be used in electronics and electrical applications, but ecosystem and loss of habitats and biodiversity, and also poses a threat a maximum concentration value of 0.1% of total PBDEs by mass in to human health. The Directive 2013/39/EU of the European

⁎ Corresponding author. E-mail address: [email protected] (E. Eljarrat). http://dx.doi.org/10.1016/j.envres.2017.09.011 Received 7 July 2017; Received in revised form 7 September 2017; Accepted 9 September 2017 Available online 06 October 2017 0013-9351/ © 2017 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211 parliament as regards priority substances in the field of water policy EQS was set at 0.0085 ng/g ww, and refers to the sum of the con- (European Commission, 2013) lays down a strategy against the pollu- centrations of congener numbers 28, 47, 99, 100, 153 and 154. For tion of water. That strategy involves the identification of priority sub- HBCD, biota EQS was set at 167 ng/g ww. These EQS should be taken stances amongst those that pose a significant risk to, or via, the aquatic into account for the first time in river basin management plans covering environment at Union level. Moreover, this Directive established En- the period 2015–2021, and should be met by the end of 2021. vironmental Quality Standards (EQS) in biota for some pollutants, such It is well known that POPs can be found for decades in the aquatic as PBDEs and HBCD. environment at levels posing a significant risk, even if extensive mea- A considerable number of studies reporting PBDE levels in river fish sures to reduce or eliminate emissions of such substances have already samples worldwide have been undertaken since Andersson and been taken. That because, additional measures to those already taken, Blomkvist (1981) first indicated that these compounds were present in including at international level must be promote to reduce or eliminate fish samples collected from Viskan River basin (Sweden) where a discharges, emissions and losses of those substances so as to achieve the number of textile industrial companies. Despite its ban, and due to its established EQS. persistent nature, PBDEs continue to be detected in practically all analysed samples showing their ubiquity in river environments. Law 3. Data collection et al. (2008) reviewed PBDE and HBCD concentrations in a variety of matrices including fish. Typical concentrations for European freshwater Given the ban on the production and use of PBDEs and HBCD, it is to fish are from the hundreds of pg/g wet weight (ww) to 700 and 150 ng/ be expected that their environmental levels will decline over the years. g ww for PBDEs and HBCD, respectively. For PBDEs, these values are Therefore, in order to evaluate the current situation, the literature well above the established EQS, whereas for HBCD, the values fall search has been restricted to the last 5 years (2012–2017) (publication within the established EQS. However, it is to be expected that biota year). On the other hand, and taking into account that biota EQS were levels have declined in recent years. The objective of this study was to established on a European directive, the search has focused on studies review and collect all available and published data (last 5 years) in carried out in Europe, but also in other areas of the world in order to European river basins, as well as in other places around the world, and compare the situation in different continents. to assess whether the established EQS are being met at present. It should be pointed out that PBDE and HBCD data are generally expressed as concentrations in lipid weight basis. However, EQS in 2. Directive 2013/39/EU in the field of water policy biota are expressed in wet weight basis. That because, all collected data must be transformed from lipid weight (lw) to ww basis. However, not The Water Framework Directive 2000/60/EC of the European always the necessary information to perform this transformation was Parliament (European Commission, 2000) introduced a legal frame- available. Taking into account that fish lipid content varies according to work to protect and restore the water environment across Europe. It species, age, season and location, two different approaches were made establishes rules to halt deterioration in the status of water bodies, in- defining two scenarios: the best scenario, in which fish lipid content cluding rivers, lakes and groundwater. Scientific, environmental and was established at 0.5% ww; and the worst scenario, in which fish lipid socio-economic factors, including human health considerations, have content was set at 20% ww (Geyer et al., 1994). been taken into account in developing a cost-effective and propor- Table 1 shows a summary of published works with PBDE and HBCD tionate policy on the prevention and control of chemical pollution of levels in fish samples collected around the world. As can be seen, we waters. That strategy involved the identification of priority substances found 13 published papers dealing with PBDE data in 15 different amongst those that pose a significant risk to the aquatic environment. European countries (Belgium, Bosnia and Herzegovina, Croatia, Czech On 20 November 2001, the list of priority substances was established Republic, France, Germany, Greece, Italy, Latvia, Poland, Serbia, Slo- setting the first list of 33 substances or groups of substances that were venia, Spain, The Netherlands and UK), as well as 7 works in North prioritised at Union level. This list already included PBDEs. Later, it was America, 8 papers in Asia (China and Korea) and 2 works in Africa concluded that it was appropriate to amend the list of priority sub- (South Africa and Tanzania). Finally, one study in a remote area stances by identifying new substances. The list of priority substances (Antarctica) has been also published. The European studies analysed was recently revised under the Directive 2013/39/EU (European fish samples collected between 2007 and 2015, with the exception of Commission, 2013), including 45 substances (or groups of substances) one work based on samples collected between 2000 and 2009. Similar among which the HBCD is already included. ranges of years are evaluated in the works carried out in North America Moreover, the Directive 2008/105/EU, which entered into force in (2004–2014) and Asia (2009–2014). As regards the fish samples, a January 2009, has defined EQSs for priority substances in water. great variety of species are studied, among which the most common are However, scientific knowledge about the fate and effects of pollutants carps, trout and European eels. in water has evolved significantly over recent years. More is known Within the reported data expressed in ww basis, PBDE concentra- about which compartment of the aquatic environment (water, sediment tion levels in European fish ranged between

204 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

Table 1 Summary of PBDE and HBCD range levels (expressed in ng/g ww) in ﬁsh samples collected around the world.

Country Year River or Location Specie n PBDEs HBCDs Refs.

EUROPE

France, Germany, Sweden, 2007–10 Götaälv, Mersey, Rhone, Common bream (Abramis brama) 348 – 0.20–386 Rüdel et al. (2012) The Netherlands and UK Tees, Western Scheldt, Lake Common sole (Solea solea) Belau

Germany nr Elbe and Rhine Rivers European Eel (Anguilla anguilla) 61 < LOD – 46.3 – Sühring et al. (2013)

Spaina 2010 Llobregat, Ebro, Júcar and Andalusian Barbel (LucioBarbus 48 < LOD – 2.60 – Santín et al. (2013) Guadalquivir Rivers sclateri) Black Bass (Mycropterus salmpoides) < LOD – 104 – Bleak (Alburnus alburnus) Brown Trout (Salmon trutta) Common Carp (Cyprinus carpio) Ebro Barbel (Barbus graellsii) European Eel (Anguila anguila) Iberian Gudgeon(Gobio lonzanoi) Iberian Nase (PseudoChondrostoma polylepis) Mediterranean Barbel (Barbus guiraonis) Pike (Esox lucius) Pumpkinseed (Leponis gibbosus) Wels Catﬁsh (Silurus glanis)

UK 2007–11 Thames, Kennet, Nene and Bleak (Alburnus alburnus) 48 2−44 – Jürgens et al. (2013) Glen Rivers Roach (Rutilus rutilus)

Czech Republic 2010 Labe, Vltava, Bílina, Common bream (Abramis brama) 48 0.21–19.9 0.02–11.6 Hloušková et al. Lužická Nisa, Morava and Common carp (Cyprinus carpio) (2013) Dyje Rivers Crucian carp (Carassius carassius) European chub (Squalius cephalus) European perch (Perca ﬂuviatilis) Grayling (Thymallus thymallus) Gudgeon (Gobio gobio) Rainbow trout (Oncorhynchus mykiss) Roach (Rutilus rutilus) Rudd (Scardinius erythrophthalmus)

Belgium and The Netherlands 2010 Scheldt estuary Common sole (Solea solea) 59 0.17–3.97 – Van Ael et al. (2014) European ﬂounder (Platichthys ﬂesus)

Poland 2010–12 Vistula and European Eel (Anguilla anguilla) 153 0.07–8.19 0.16–17.5 Szlinder-Richert Szczecin lagoons, Puck Buy, et al. (2014) Mazurian, Nidzkie and Jamno Lakes

Italya 2011–12 Lake Maggiore Shad (Alosa agone) 123 0.75–8.82 0.14–6.16 Poma et al. (2014) Whiteﬁsh (Coregonus lavaretus) 29.8–353 5.40–246

Denmark 2012 nr Cod (Gadus callarias) 11 –

Belgium 2000–09 Flanders region European Eel (Anguilla anguilla) 26 0.77–93 0.58–751 Malarvannan et al. (2015)

Italya 2010 Po River Common bream (Abramis brama) 12 0.38–4.57 0.006–0.83 Luigi et al. (2015) Common carp (Cyprinus carpio) Sanders (Sander lucioperca) 15.1–183 0.24–33.3 Sheatﬁshes (Silurus glanis)

France 2011–12 Loire estuary European Eel (Anguilla anguilla) 45 0.1–18.1 – Couderc et al. (2015)

(continued on next page)

205 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

Table 1 (continued)

Country Year River or Location Specie n PBDEs HBCDs Refs.

Czech Republica 2010 Labe and Vltava Rivers Asp (Aspius aspius) 59 – 0.02–6.06 Svihlikova et al. Common bream (Abramis brama) (2015) Common carp (Cyprinus carpio) – 0.63–242 Crucian carp (Carassius carassius) European chub (Squalius cephalus) Nase carp (Chondrostoma nasus) Roach (Rutilus rutilus)

Latvia 2013–14 Aluksnes, Kiesezers, European Eel (Anguilla anguilla) 58 0.28–26.7 – Zacs et al. (2016) Liepajas, Sivers and Usmas Lakes

UK 2007–12 Thames River Roach (Rutilus rutilus) 42 2.30–24.5 – Lu et al. (2017)

Italy, Greece, Slovenia, 2014–15 Adige, Evrotas and Sava Bullhead (Cottus gobio) 27 0.03–3.26 – Giulivo et al. (2017) Croatia, Bosnia and Rivers Chub (Squalius cephalus) Herzegovina and Serbiaa Common barbel (Barbus barbus) 1.18–130 – Grayling (Thymallus thymallus) Marble trout (Salmo marmoratus) Menida (Squalius keadicus) Rainbow trout (Oncorhynchus mykiss) Riverine brown trout (Salmo trutta fario)

NORTH AMERICA

USA 2004–09 Erie, Huron, Michigan, Lake trout (Salvelinus namaycush) 290 6.7–114 – Crimmins et al. (2012) Ontario and Superior Lakes Walleye (Sander vitreus)

Canadaa 2008–12 St. Lawrence River Muskellunge (Esox masquinongy) 50 0.47–120 – Houde et al. (2014) Northern pike (Esox lucius) Yellow perch (Perca ﬂavescens) 18.8–4806 –

USA 2009–10 Columbia River Largescale suckers (Catostomus 74

USAa 2013–14 Illinois Common carp (Cyprinus carpio) nr 0.075–41.4 – Widelka et al. (2014) Largemouth bass (Micropterus salmoides) 3–1654 –

Canada 2006–13 Great Lakes (Detroit, Erie, Bluegill (Lepomis macrochirus) 470 1–390 – Gandhi et al. (2017) Huron, Ontario, St. Clair, Brown bullhead (Ameiurus nebulosus) Superior) Brown trout (Salmo trutta) Burbot (Lota lota) Channel catﬁsh (Ictalurus punctatus) Chinook salmon (Oncorhynchus tshawytscha) Cisco (Coregonus artedi) Coho salmon (Oncorhynchus kisutch) Common carp (Cyprinus carpio) Lake trout (Salvelinus namaycush) Lake whiteﬁsh (Coregonus clupeaformis) Largemouth bass (Micropterus salmoides) Longnose sucker (Catostomus catostomus) Pumpkinseed (Lepomis gibbosus) Rainbow trout (Oncorhynchus mykiss) Walleye (Sander vitreus) White bass (Morone chrysops) White sucker (Catostomus commersonii)

USA 2008–09 Ecoregions of Eastern 15 species including members of the 497 0.14–311 – Batt et al. (2017) Highlands, Plains and sunﬁsh, trout/salmon, pike, temperate Lowlands, and bass, perch, and catﬁsh families the West and Mountains

North Americaa 2010 Great Lakes (Erie, Huron, Lake trout (Salvelinus namaycush) 15 0.54–2.48 < LOD – 0.61 Guo et al. (2017) Michigan, Ontario, Walleye (Sander vitreus) Superior) 21.7–99 < LOD – 24.4

(continued on next page)

206 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

Table 1 (continued)

Country Year River or Location Specie n PBDEs HBCDs Refs.

ASIA

Chinaa 2009 Taihu Lake 24 ﬁsh species including herbivorous 200 0.03–1.33 – Yu et al. (2012) (3), omnivorous (10) and carnivorous (11) 1.08–53.2 –

Chinaa 2010 e-waste-recycling Chinese hooksnout carp (Opsariichthys 29 10.2–43.2 – Mo et al. (2012) site (south China) bidens) Mosquito fish (Gambusia affinis) 406–1726 – Paradise fish (Macropodus opercularis)

Chinaa 2010 Dongjiang River Crucian carp (Carassius carassius) 34 0.18–2.8 < LOD – 4.16 He et al. (2012 and Mud carp (Cirrhina molitorella) 2013) Nile tilapia (Tilapia nilotica) Plecostomus (Hypostomus plecostomus) 7–112 < LOD – 166

Chinaa 2010 Liaohe River (Northeast Grass carp (Ctenopharyngodon idellus) 18 0.05–0.20 – Ren et al. (2013) China) Pond loach (Misgurnus anguillicaudatus) 1.88–7.94 – Wild carp (Hemiculter leucisculus)

Chinaa 2007–11 High mountain lakes and Oxygymnocypris stewartii 79 – < LOD – 0.07 Zhu et al., 2013 rivers of the Tibetan Schizopygopsis younghusbandi Plateau Schizothorax macropogon – < LOD – 2.74 Schizothorax o′connori Schizothorax waltoni Gymoncypris waddellii Gymoncypris przewalskii Racomatibetanus

Chinaa 2009–12 Tai Lake and Yangtze River Common carp (Cyprinus carpio) 71 0.006–0.49 < LOD – 1.58 Su et al. (2014) (Eastern China) Shrimp (Elminius modestus) Yellow catﬁsh (Pelteobagrus fulvidraco) 0.23–19.5 < LOD – 63.3

Koreaa 2010 Nakdong, Nam and Seomjin Crucian carp (Carassius auratus)26– 0.009–0.38 Jeong et al. (2014) Rivers – 0.34–15.2

China 2010 Longtang town, Qingyuan Mud carp (Cirrhinus molitorella) 10 – 0.07–240 Tang et al. (2015) County Northern snakehead (Channa argus)

Korea 2011–12 Nakdong River Amur three-lips (Opsariichthys 90 0.15–9.4 – Kim et al. (2015) uncirostris amurensis) Barbel steed (Hemibarbus labeo) Bluegill (Lepomis macrochirus) Giant Chinese bitterling (Acanthorhodeus macropterus) Largemouth bass (Micropterus salmoides) Predatory carp (Erythroculter erythropterus) Yellowhead catﬁsh (Tachysurus fulvidraco)

Chinaa 2014 Pearl River Delta Mud carp (Cirrhinus molitorella) 120 0.03–3.45 – Sun et al. (2016) Plecostomus (Hypostomus plecostomus) Tilapia (Tilapia nilotica) 1.38–138 –

Chinaa 2013 Tai Lake and Common carp (Cyprinus carpio) 25 0.02–0.22 – Du et al. (2017) Dianshan Lake Crucian carp (Carassius auratus) Pond snail (Bellamya aeruginosa) 0.92–8.6 – Silver carp (Hypophthalmichthys molitrix)

AFRICA

Tanzaniaa 2011 Babati, Nyasa, Tanganyika Tilapia: Oreochromis sp. 201 < LOD – 0.02 < LOD – 0.03 Polder et al. (2014) and Victoria Lakes Oreochromis niloticus Oreochromis tanganicae < LOD – 0.90 < LOD – 1.24

South Africaa 2013 Vaal River Carp 12 0.02–0.17 0.05 −0.07 Chokwe et al. (2015)

0.93–6.60 2.12–2.80

(continued on next page)

207 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

Table 1 (continued)

Country Year River or Location Specie n PBDEs HBCDs Refs.

REMOTE AREAS

Antarcticaa 2008–11 King George Island Nototheniidae family: Trematomus 31 0.006–0.57 – Lana et al. (2014) newnesi Notothenia coriiceps 0.24–22.8 – Notothenia rossii nr Not reported. LOD Limit of detection. a Studies in which the transformation from lw to ww was not possible. Two scenarios were established: the top row corresponds to the best scenario (fish lipid content of 0.5% ww), and the bottom row corresponds to the worst scenario (fish lipid content of 20% ww). works in Africa (South Africa and Tanzania). The ranges of years works (Rüdel et al., 2012; Malarvannan et al., 2015) and in one Chinese evaluated are similar to those of PBDE papers, between 2007 and 2013. study (Tang et al., 2015) range of concentration reaches values up to As regards the fish samples, a great variety of species are also studied, 751 ng/g ww, exceeding the limit about 5 times. among which the most common are carps and breams. In order to better assess the degree of non-compliance, it is neces- HBCD concentration levels in European fish ranged between 0.02 sary to have individual data of each fish sample analysed. However, this and 751 ng/g ww, being somewhat higher than those found for PBDEs. information is not always available in published papers, in which we However, although HBCD levels are higher, since the European EQS basically find the concentration ranges. From the total of studies pre- established for HBCD is rather orders of magnitude higher than that of sented in Table 1, we have been able to compile the information of PBDEs, only a part of the European fish samples exceeded the HBCD levels of PBDEs in each fish studied for 8 published papers, 5 studies EQS. Moreover, and unlike for PBDEs, HBCD levels in North America carried out in Europe (Sühring et al., 2013; Santín et al., 2013; (

Fig. 1. Percentage of ﬁsh samples exceeding the European EQS value for PBDEs. Data obtained from: 1 (Sühring et al., 2013); 2 (Santín et al., 2013); 3 (Malarvannan et al., 2015); 4 (Luigi et al., 2015); 5 (Giulivo et al., 2017); 6 (Nilsen et al., 2014); 7 (Batt et al., 2017); and 8 (Guo et al., 2017). BS = Best Scenario; WS = Worst Scenario.

208 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211 beginning to yield declines in concentration in environmental samples recycling. It is important to consider here the problem related to dis- (Law et al., 2014; Barón et al., 2015b). But in the case of POPs, their carded electronic products, also called e-waste. The amounts of e-waste ban does not solve the environmental problem in the short or medium have increased exponentially during the last years, and the quantity term. For instance, a study in the Lake Ontario (Canada) showed that produced globally is expected to increase up to 50 million metric tons in since 1997, penta-BDE levels have declined at an annual rate of 4.5% 2018 (Baldé et al., 2014). In many countries, handling and disposal of e- (ECC Canada). If we take into account an annual decrease of 5%, after waste is unregulated. In 2014, only about 15% of global e-waste was 10 years, samples actually with levels higher than 100 times the EQS recycled with the highest standards (Baldé et al., 2014). Moreover, the (up to 96%), will present concentrations about 0.40 ng/g ww, being recycling process of plastic from e-waste containing PBDEs is largely still 50 times above the value established by the European directive. uncontrolled and is found in many recycled products, such as children Thus, it will take several decades to reach levels of pollution re- toys, household goods, video tape casings and electronics. Thus, it is commended by the legislation. necessary to develop recommendations for waste management to en- It should be noted that EQS value developed for biota monitoring sure the minimum environmental impact, and to identify the best under the WFD is criticized by some authors (Jürgens et al., 2013). It is available techniques and best environmental practices for the recycling worth noting that the EQS value for PBDEs was calculated to protect of articles containing PBDEs. human consumers based on observed effects of only one congener In addition to recycling, there are other PBDE waste treatment (BDE-99) on rats and including very large safety factors (European methods such as landfill and especially incineration. Recently, Redfern Commission, 2011). Indeed, in developing the proposed PBDE EQSs the et al. (2017) found that combustion sources and illegal open burning of authors of the dossier on PBDEs thought that 44.4 ng/g ww for the sum e-waste globally emit 6.75 PBDE tonnes per year, being important PBDE of 6 BDEs is sufficient to protect wildlife predators. Hence the current emitters. The effectiveness of reducing PBDE emissions will be delayed EQS for PBDEs seems to be controversial and it should be revised as if mitigation of PBDE emissions from combustion sources is ignored. soon as new toxicological data will be available. In any case, the al- That because control of PBDE emissions from combustion sources ternative EQS value of 44.4 ng/g ww would improve the situation, but should be implemented. we would still be with a large number of studies with levels above this Finally, due to the ongoing restrictions on PBDEs, there has been a new EQS value, both in Europe and in the rest of the world (see shift in the use of alternative FRs. Attention must also be paid to the Table 1). Remember that considering the worst scenario, up to 25% and occurrence and time trends of these new pollutants in river sediments 30% of fish samples exceeded the EQS up to 10,000 times (85 ng/g ww) and fish samples. There are already some studies with levels of some in Europe and North America, respectively. This means that, at least emerging FRs in European river fish. For instance, Santín et al. (2013) these same percentages of samples would be those exceeding the al- reported concentration levels of decabromodiphenylethane (DBDPE), ternative EQS value set at 44.4 ng/g ww. the substitute of Deca-BDE, up to 26 ng/g ww, and of Dechlorane 602, a It is therefore evident that further actions are needed in order to chlorinated FR, up to 35 ng/g ww. On the other hand, Giulivo et al. achieve the good surface water chemical status (with regard to PBDEs) (2017) analysed different organophosphate FRs, and detected values up by the end of 2027. Precisely this is already proposed by the European to 130 ng/g ww. It is clear that more studies on the occurrence and directive: “taking measures additional to those already taken, including at behaviour of these emerging pollutants, and especially with regard to international level, to reduce or eliminate discharges, emissions and losses of their toxicity, are strongly recommended. Moreover, it is to be expected those substances so as to achieve the objectives”. In this sense, and taking that these levels will increase in future years. Therefore, within a few into account that there is already a ban on the production and use of years we may stay in a similar situation to the current one with PBDEs, PBDEs at international scale through the Stockholm Convention, it is in which, in spite of its ban at international scale, the pollution levels necessary to carry out new strategies. It is essential and necessary to are and will be for decades an environmental problem. identify and evaluate the current sources of PBDE pollution. Although In this sense, and taking into account the need to protect materials there should be no primary sources due to its ban, we may be facing against potential fires to avoid property damage and loss of life, it secondary sources of pollution. This is the case of large existing stores of would be advisable for the industry to develop flame retardants that do banned PBDEs in consumer products. PBDE congeners will continue to not cause an environmental impact. Moreover, a committee of experts be released into the environment during the use, disposal and recycling of the Stockholm Convention proposes alternatives such as changes in of existing fire retardant containing goods. product design, industrial processes and other practices that do not This is a similar situation to PCB contamination. While manufacture require the use of any flame retardant. For example, electronic products of PCBs has reportedly ceased, the potential or actual release of PCBs can be redesigned to separate the high voltage parts from the outer into the environment has not, since significant quantities of existing covers, or protected with metal instead of plastic. Fire resistance con- PCBs continue in use or in storage. Electrical transformers and capa- struction techniques can eliminate the need to use flame retardant citors are one such major source of PCBs. Within the policy framework chemicals in the insulation material, replacing it with alternative ma- set out in the Stockholm Convention, an exception is made to allow terials such as fibers. In this way, it would be possible to reduce the continued use of such equipment until 2025. Recommendations have consumption of flame retardants thus reducing their environmental been published aimed to provide practical safe management, re- impact. classification and elimination of contaminated equipment (UNEP, 2002). Moreover, the final steps of the decontamination process may Acknowledgements involve the generation of hazardous residues that must be treated in accordance with the regulations on trans-boundary movements of ha- This work was funded by the European Union Seventh Framework zardous waste. Programme (FP7/2007–2013) under the Globaqua project (No. In the same way, whereas disposal operations that would allow for 603629), by the Spanish Ministry of Economy and Competitiveness the potential recovery, recycling or reuse of the POPs content of the through the Redes de Excelencia project NET-SCARCE (CTM2015- waste have been strictly prohibited, an exemption allowing for re- 69780-REDC) and by the Generalitat de Catalunya (Consolidated cycling of articles that contain PBDEs and the use and final disposal of Research Groups 2014 SGR 418 - Water and Soil Quality Unit). articles manufactured from recycled materials that contain PBDEs has been established until 2030. Recycling of articles containing PBDEs References inevitably increases releases of these pollutants which can result in environmental and health risks. A considerable fraction of PBDEs con- Andersson, O., Blomkvist, G., 1981. Polybrominated aromatic pollutants found in fish in taining waste is recycled, with little information about the fate during Sweden. Chemosphere 10, 1051–1060.

209 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

Baldé, C.P., Wang, F., Kuehr, R., Huisman, J., 2014. The Global E-waste Monitor. United enantiomer-specific profiles of hexabromocyclododecane and tetrabromobisphenol A Nations University, IAS – SCYCLE, Bonn, Germany. 〈http://i.unu.edu/media/unu. in an aquatic environment in a highly industrialized area, South China: vertical edu/news/52624/UNU-1stGlobal-E-Waste-Monitor-2014-small.pdf〉 (accessed July profile, phase partition, and bioaccumulation. Environ. Pollut. 179, 105–110. 2017). Hloušková, V., Lanková, D., Kalachová, K., Hrádková, P., Poustka, J., Hajšlová, J., Barón, E., Máñez, M., Andreu, A., Sergio, F., Hiraldo, F., Eljarrat, E., Barceló, D., 2014. Pulkrabová, J., 2013. Occurrence of brominated flame retardants and perfluoroalkyl Bioaccumulation and biomagnification of emerging and classical flame retardants in substances in fish from the Czech aquatic ecosystem. Sci. Total Environ. 461–462, bird eggs of 14 species from Doñana Natural Space and surrounding areas (South- 88–98. western Spain). Environ. Int. 68, 118–126. Houde, M., Berryman, D., Lafontaine, Y., Verreault, J., 2014. Novel brominated flame Barón, B., Giménez, J., Verborgh, P., Gauffier, P., de Stephanis, R., Eljarrat, E., Barceló, retardants and dechloranes in three fish species from the St. Lawrence river, Canada. D., 2015Fa. Bioaccumulation and biomagnification of classical flame retardants, re- Sci. Total Environ. 479–480, 48–56. lated halogenated natural compounds and alternative flame retardants in three del- Jeong, G.H., Hwang, N.R., Hwang, E.H., Lee, B.C., Yoon, J., 2014. phinids from Southern European waters. Environ. Pollut. 203, 107–115. Hexabromocyclododecanes in crucian carp and sediment from the major rivers in Barón, E., Bosch, C., Máñez, M., Andreu, A., Sergio, F., Hiraldo, F., Eljarrat, E., Barceló, Korea. Sci. Total Environ. 470–471, 1471–1478. D., 2015Fb. Temporal trends in classical and alternative flame retardants in bird eggs Jürgens, M.D., Johnson, A.C., Jones, K.C., Hughes, D., Lawlor, A.J., 2013. The presence of from Doñana natural space and surrounding areas (South-western Spain) between EU priority substances mercury, hexachlorobenzene, hexachlorobutadiene and 1999 and 2012. Chemosphere 138, 316–323. PBDEs in wild fish from four English rivers. Sci. Total Environ. 461–462, 441–452. Batt, A.L., Wathen, J.B., Lazorchak, J.M., Olsen, A.R., Kincaid, T.M., 2017. Statistical Kemmlein, S., Herzke, D., Law, R.J., 2009. Brominated flame retardants in the European survey of persistent organic pollutants: risk estimations to humans and wildlife chemicals policy of REACH-Regulation and determination in materials. J. through consumption of fish from U.S. rivers. Environ. Sci. Technol. 51, 3021–3031. Chromatogr. A 1216, 320–333. BSEF (Bromine Science and Environmental Forum), 2009. Total Market Demand. Kim, U.J., Jo, H., Lee, I.S., Joo, G.J., Oh, J.E., 2015. Investigation of bioaccumulation and (Accessed 5 Aug 2009). 〈http://www.bsef.com〉. biotransformation of polybrominated diphenyl ethers, hydroxylated and methoxy- BSEF (Bromine Science and Environmental Forum), 2012. Legislation on lated derivatives in varying trophic level freshwater fishes. Chemosphere 137, Decabromodiphenyl Ether (Deca-BDE) in North America (USA and Canada). 〈http:// 108–114. www.bsef.com/regulation/north-america/deca-bde-3〉. La Guardia, M.J., Hale, R.C., Harvey, E., 2006. Detailed polybrominated diphenyl ether Chokwe, T.B., Okonkwo, J.O., Sibali, L.L., Ncube, E.J., 2015. Alkylphenol ethoxylates and (PBDE) congener composition of the widely used Penta-, Octa-, and Deca-PBDE brominated flame retardants in water, fish (carp) and sediment samples from the Vaal technical flame-retardant mixtures. Environ. Sci. Technol. 40, 6247–6254. River, South Africa. Environ. Sci. Pollut. Res. 22, 11922–11929. Lana, N.B., Berton, P., Covaci, A., Ciocco, N.F., Barrera-Oro, E., Atencio, A., Altamirano, Couderc, M., Poirier, L., Zalouk-Vergnoux, A., Kamari, A., Blanchet-Letrouvé, I., J.C., 2014. Fingerprint of persistent organic pollutants in tissues of Antarctic no- Marchand, P., Vénisseau, A., Veyrand, B., Mouneyrac, C., Le Bizec, B., 2015. tothenioid fish. Sci. Total Environ. 499, 89–98. Occurrence of POPs and other persistent organic contaminants in the European eel Law, R.J., Herzke, D., Harrad, S., Morris, S., Bersuder, P., Allchin, C.R., 2008. Levels and (Anguilla anguilla) from the Loire estuary, France. Sci. Total Environ. 505, 199–215. trends of HBCD and BDEs in the European and Asian environments, with some in- Covaci, A., Gerecke, A., Law, R., Voorspoels, S., Kohler, M., Heeb, N., Leslie, H., Allchin, formation for other BFRs. Chemosphere 73, 223–241. C., de Boer, J., 2006. Hexabromocyclododecanes (HBCDs) in the environment and Law, R.J., Covaci, A., Harrad, S., Herzke, D., Abdallah, M.A.E., Fernie, K., Toms, L.M.L., humans: a review. Environ. Sci. Technol. 40, 3679–3688. Takigami, H., 2014. Levels and trends of PBDEs and HBCDs in the global environ- Crimmins, B.S., Pagano, J.J., Xia, X., Hopke, P.K., Milligan, M.S., Holsen, T.M., 2012. ment: status at the end of 2012. Environ. Int. 65, 147–158. Polybrominated diphenyl ethers (PBDEs): turning the corner in Great Lakes Trout Lee, E., Kim, T.H., Choi, J.S., Nabanata, P., Kim, N.Y., Ahn, M.Y., Jung, K.K., Kang, I.H., 1980–2009. Environ. Sci. Technol. 46, 9890–9897. Kim, T.S., Kwack, S.J., Park, K.L., Kim, S.H., Kang, T.S., Lee, J., Lee, B.M., Kim, H.S., Du, X., Chang, H., Zhou, Y., Qiu, Y., Wu, Y., Lin, Z., Zhu, Z., Zhao, J., 2017. 2010. Evaluation of liver and thyroid toxicity in Sprague-Dawley rats after exposure Polybrominated diphenyl ethers and its methoxylated analogues in biota and sedi- to polybrominated diphenyl ether BDE-209. J. Toxicol. Sci. 35 (4), 535–545. ment samples from two freshwater lakes in Yangtze River delta. Environ. Earth Sci. Lu, Q., Jürgens, M.D., Johnson, A.C., Graf, C., Sweetman, A., Crosse, J., Whitehead, P., 76, 171. 2017. Persistent organic pollutants in sediment and fish in the river Thames catch- ECC Canada Environment and Climate Change Canada. Polybrominated Diphenyl Ethers ment (UK). Sci. Total Environ. 576, 78–84. (PBDEs) in Fish and Sediment. 〈https://www.ec.gc.ca/indicateurs-indicators/ Luigi, V., Giuseppe, M., Claudio, R., 2015. Emerging and priority contaminants with default.asp?Lang=en&n=0970C75C-1〉. (Accessed July 2017). endocrine active potentials in sediments and fish from the River Po (Italy). Environ. ECD. 2009. Official Journal of the European Union Commission Decision 2005/717/EC - Sci. Pollut. Res. 22, 14050–14066. Exemption of DecaBDE From the Prohibition on Use, C 116 (May 9, 2008). Malarvannan, G., Belpaire, C., Geeraerts, C., Eulaers, I., Neels, H., Covaci, A., 2015. Eljarrat, E., Labandeira, A., Marsh, G., Raldua, D., Barceló, D., 2007. Decabrominated Organophosphorus flame retardants in the European eel in Flanders, Belgium: diphenyl ether in river fish and sediment samples collected downstream an industrial Occurrence, fate and human health risk. Environ. Res. 140, 604–610. park. Chemosphere 69, 1278–1286. Mo, L., Wu, J.P., Luo, X.J., Zou, F.S., Mai, B.X., 2012. Bioaccumulation of polybrominated Eljarrat, E., Guerra, P., Martínez, E., Farré, M., Alvarez, J.G., López-Teijón, M., Barceló, diphenyl ethers, decabromodiphenyl ethane, and 1,2-bis(2,4,6-tribromophenoxy) D., 2009. Hexabromocyclododecane in human breast milk: levels and enantiomeric ethane flame retardants in kingfishers (Alcedo atthis) from an electronic waste–r- patterns. Environ. Sci. Technol. 43, 1940–1946. ecycling site in South China. Environ. Toxicol. Chem. 31, 2153–2158. European Commission, 2000. Directive 2000/60/EC of the European Parliament and of Morris, S., Allchin, C., Zegers, B., Haftka, J., Boon, J., Leonards, P., Van Leeuwen, S., de the Council of 23 October 2000 establishing a framework for community action in the Boer, J., 2004. Distribution and fate of HBCD and TBBPA brominated flame re- field of water policy. J. Eur. Communities L327, 1–72. tardants in north sea estuaries and aquatic food webs. Environ. Sci. Technol. 38, European Commission, 2011. PBDE EQS dossier2011. 〈https://circabc.europa.eu/sd/d/ 5497–5504. d07ed9f5-0760-4561-b642-04bc1e4a580e/PBDE%20EQS%20dossier%202011.pdf〉 Nilsen, E., Zaugg, S., Alvarez, D., Morace, J., Waite, I., Counihan, T., Hardiman, J., Torres, (Accessed July 2017). L., Patiño, R., Mesa, M., Grove, R., 2014. Contaminants of legacy and emerging European Commission, 2013. Directive 2013/39/EU of the European Parliament and of concern in largescale suckers (Catostomus macrocheilus) and the foodweb in the the Council amending directives 2000/60/EC and 2008/105/EC as regards priority lower Columbia River, Oregon and Washington, USA. Sci. Total Environ. 484, substances in the field of water policy. J. Eur. Union L 226, 1–17. 344–352. Gandhi, N., Gewurtz, S.B., Drouillard, K.G., Kolic, T., MacPherson, K., Reiner, E.J., Palace, V.P., Pleskach, K., Halldorson, T., Danell, R., Wautier, K., Evans, B., 2008. Bhavsar, S.P., 2017. Polybrominated diphenyl ethers (PBDEs) in Great Lakes fish: Biotransformation enzymes and thyroid axis disruption in juvenile rainbow trout levels, patterns, trends and implications for human exposure. Sci. Total Environ. 576, (Oncorhynchus mykiss) exposed to hexabromocyclododecane diastereoisomers. 907–916. Environ. Sci. Technol. 42, 1967–1972. Geyer, H.J., Scheunert, I., Brueggemann, R., Matthies, M., Steinberg, C.E.W., Zitko, V., Polder, A., Müller, M.B., Lyche, J.L., Mdegela, R.H., Nonga, H.E., Mabiki, F.P., Mbise, T.J., Kettrup, A., Garrison, W., 1994. The relevance of aquatic organisms' lipid content to Skaare, J.U., Sandvik, M., Skjerve, E., Lie, E., 2014. Levels and patterns of persistent the toxicity of lipophilic chemicals: toxicity of lindane to different fish species. organic pollutants (POPs) in tilapia (Oreochromis sp.)from four different lakes in Ecotoxicol. Environ. Saf. 28, 53–70. Tanzania: geographical differences and implications for human health. Sci. Total Giulivo, M., Capri, E., Kalogianni, E., Milacic, R., Bellini, A., Ferrari, F., Eljarrat, E., Environ. 488–489, 252–260. Barceló, D., 2017. Occurrence of halogenated and organophosphate flame retardants Poma, G., Volta, P., Roscioli, C., Bettinetti, R., Guzzella, L., 2014. Concentrations and in sediment and fish samples from three European river basins. Sci. Total Environ. trophic interactions of novel brominated flame retardants, HBCD, and PBDEs in 586, 782–791. zooplankton and fish from Lake Maggiore (Northern Italy). Sci. Total Environ. 481, Guerra, P., Alaee, M., Jiménez, B., Pacepavicius, G., Marvin, C., MacInnis, G., Eljarrat, E., 401–408. Barceló, D., Champoux, L., Fernie, K., 2012. Emerging and historical brominated Redfern, F.M., Lee, W.J., Yan, P., Mwangi, J.K., Wang, L.C., Shih, C.H., 2017. Overview flame retardants in peregrine falcon (Falco peregrinus) eggs from Canada and Spain. and perspectives on emissions of polybrominated diphenyl ethers on a global basis: Environ. Int. 40, 179–186. evaporative and fugitive releases from commercial pbde mixtures and emissions from Guo, J., Venier, M., Salamova, A., Hites, R.A., 2017. Bioaccumulation of dechloranes, combustion sources. Aerosol Air Qual. Res. 17, 1117–1131. organophosphate esters, and other flame retardants in Great Lakes fish. Sci. Total Ren, G., Wang, Z., Yu, Z., Wang, Y., Ma, S., Wu, M., Sheng, G., Fu, J., 2013. Primary Environ. 583, 1–9. investigation on contamination pattern of legacy and emerging halogenated organic Hana, R.P., Stephen, B., Richard, J.A., Carol, J.E., 2004. Toxicological profile for poly- pollutions in freshwater fish from Liaohe River, Northeast China. Environ. Pollut. brominated diphenyl ethers. Agency Toxic. Subst. Dis. Regist. 619. 172, 94–99. He, M.J., Luo, X.J., Chen, M.Y., Sun, Y.X., Chen, S.J., Mai, B.X., 2012. Bioaccumulation of Rüdel, H., Müller, J., Quack, M., Klein, R., 2012. Monitoring of hexabromocyclododecane polybrominated diphenyl ethers and decabromodiphenyl ethane in fi sh from a river diastereomers in fish from European freshwaters and estuaries. Environ. Sci. Pollut. system in a highly industrialized area, South China. Sci. Total Environ. 419, 109–115. Res. 19, 772–783. He, M.J., Luo, X.J., Yu, L.H., Wu, J.P., Chen, S.J., Mai, B.X., 2013. Diasteroisomer and Santín, G., Barón, E., Eljarrat, E., Barceló, D., 2013. Emerging and historical halogenated

210 E. Eljarrat, D. Barceló Environmental Research 160 (2018) 203–211

flame retardants in fish samples from Iberian rivers. J. Hazard. Mat. 263P, 116–121. UNEP, 2002. PCB Transformers and Capacitors From Management to Reclassification and Sühring, R., Möller, A., Freese, M., Pohlmann, J.D., Wolschke, H., Sturm, R., Xie, Z., Disposal. 〈http://www.pops.int/documents/guidance/nipsfinal/PCBtranscap.pdf〉 Hanel, R., Ebinghaus, R., 2013. Brominated flame retardants and dechloranes in eels (accessed July 2017). from German rivers. Chemosphere 90, 118–124. UNEP, 2015. Listing of POPs in the Stockholm Convention. Su, G., Saunders, D., Yu, Y., Yu, H., Zhang, X., Liu, H., Giesy, J.P., 2014. Occurrence of Van Ael, E., Covaci, A., Blust, R., Bervoets, L., 2014. Corrigendum to “Persistent organic additive brominated flame retardants in aquatic organisms from Tai Lake and pollutants in the Scheldt estuary: environmental distribution and bioaccumulation” Yangtze River in Eastern China, 2009–2012. Chemosphere 114, 340–346. [Environ. Int. 48C (2012) 17–27]. Environ. Int. 63, 246–251. Sun, R., Luo, X., Tang, B., Li, Z., Wang, T., Tao, L., Mai, B., 2016. Persistent halogenated Vorkamp, K., Bossi, R., Bester, K., Bollmann, U.E., Boutrup, S., 2014. New priority sub- compounds in fish from rivers in the Pearl River Delta, South China: geographical stances of the European Water Framework Directive: biocides, pesticides and bro- pattern and implications for anthropogenic effects on the environment. Environ. Res. minated flame retardants in the aquatic environment of Denmark. Sci. Total Environ. 146, 371–378. 470–471, 459–468. Svihlikova, V., Lankova, D., Poustka, J., Tomaniova, M., Hajslova, J., Pulkrabova, J., Widelka, M., Lydy, M.J., Wu, Y., Chen, D., 2014. Statewide surveillance of halogenated 2015. Perfluoroalkyl substances (PFASs) and other halogenated compounds in fish flame retardants in fish in Illinois, USA. Environ. Pollut. 214, 627–634. from the upper Labe River basin. Chemosphere 129, 170–178. Yu, Y.X., Zhang, S.H., Huang, N.B., Li, J.L., Pang, Y.P., Zhang, X.Y., Yu, Z.Q., Xu, Z.G., Szlinder-Richert, J., Ruczynska, W., Nermer, T., Usydus, Z., Robak, S., 2014. The occur- 2012. Polybrominated diphenyl ethers and polychlorinated biphenyls in freshwater rence of organic contaminants in European eel (Anguilla anguilla) in Poland: an en- fish from Taihu Lake, China: their levels and the factors that influence biomagnifi- vironmental quality assessment. Chemosphere 114, 282–290. cation. Environ. Toxicol. Chem. 31, 542–549. Tang, B., Zeng, Y.H., Luo, X.J., Zheng, X.B., Mai, B.X., 2015. Bioaccumulative char- Zacs, D., Rjabova, J., Fernandes, A., Bartkevics, V., 2016. Brominated, chlorinated and acteristics of tetrabromobisphenol A and hexabromocyclododecanes in multi-tissues mixed brominated/chlorinated persistent organic pollutants in European eels of prey and predator fish from an e-waste site, South China. Environ. Sci. Pollut. Res. (Anquilla anquilla) from Latvian lakes. Food Addit. Contam.: Part A 33, 460–472. 22, 12011–12017.

211