Accumulation of short-, medium-, and long- chain chlorinated paraffins in tissues of laying hens after dietary exposure
Introduction
Chlorinated paraffins (CPs), a family of polychlorinated n-alkane chains (CxH2x+2−yCly) with varying chain length and chlorination degrees in the range 30–70% w/w, have been used since the late 1970s in many industrial applications such as lubricants in metal-working fluids, flame-retardants and plasticisers (European Food Safety Authority (EFSA) panel on contaminants in the food chain (CONTAM), 2020).
Consequently, CPs are produced in large volumes (estimated at 1,000,000 tonnes per year, Glüge, Wang, Bogdal, Scheringer, & Hungerbühler, 2016). Unfortunately, part of those CPs are released during production, uses and improper disposal of polymeric products containing these additives (Glüge et al., 2016). Thus, the CPs environmental levels usually surpass most of the levels of other halogenated contaminants such as polychlorobiphenyls, organochlorine pesticides or dioxins (Krätschmer et al., 2019, Niu et al., 2020, Zhou et al., 2018). CPs have been reported in most environmental compartments, such as air (Niu et al., 2020), water (Wang, Jia et al., 2019), soil (Aamir et al., 2019), sediment (Chen et al., 2011), biota (Yuan et al., 2019), food (Harada et al., 2011, Lee et al., 2020) and even human matrices (Wang, Gao, Wang, & Jiang, 2018). The ubiquity of CPs in the environment make them chemicals of concern, notably because they share similar physio-chemical properties with other halogenated contaminants that are considered hazardous for human health.
CPs are sub-categorised into short-chain CPs (SCCPs, C10-C13), medium-chain CPs (MCCPs, C14-C17), and long-chain CPs (LCCPs, C≥18). SCCPs were classified as possibly carcinogenic to humans in 1990 by the International Agency for Research on Cancer (IARC working Group on the Evaluation of Carcinogenic Risk to Humans, 1990), and were later shown to cause chronic toxicity to marine species and mammals (Wang, Zhu et al., 2019). As a consequence, they have been phased out in Europe and North America (European Union, 2006, Government of Canada, 2009, United States Environmental Protection Agency (US EPA), 2015) since the 2010s and included in the Annex A of the Stockholm convention in 2017 (Conference of the Parties of the Stockholm Convention, 2017). However, there is a lack of toxicity and toxicokinetics data on MCCPs and LCCPs, though recent occurrence studies on terrestrial and marine ecosystems show their potential for bioaccumulation (Yuan et al., 2019). Recently, the EFSA published a scientific opinion on CPs concluding that risk assessment in Europe was hardly feasible, based on the few submitted toxicological and occurrence data (EFSA CONTAM panel, 2020) at the time of their evaluation. In particular, they emphasised the need for further information on the influence of the chain length and the chlorination degree of CPs on their toxicokinetics in humans and experimental animals.
To date, the few published toxicokinetics experiments focused on SCCPs and MCCPs mainly. In rodents, 14C-labelled SCCPs have been reported to be distributed primarily in fat, liver, bile and egg yolks (Biessmann et al., 1982, Biessmann et al., 1983). The authors also showed that lower chlorinated compounds could undergo degradation to CO2, whereas the higher chlorinated compounds could not. Later, Fisk, Cymbalisty, Tomy, and Muir (1998) showed accumulation of SCCPs and MCCPs congeners in dietary exposed rainbow trout. In their study, the depuration half-lives varied from 5 to 53 days depending on the octanol–water partition coefficient (Kow) and carbon chain length, indicating an influence of the homologue structure on the accumulation potential. More recently, Geng et al. (2016) observed SCCPs absorption and depuration in rats after a single-dose exposure. Alike other persistent organic pollutants, SCCPs distributed in tissues sensitive to the chlorine content. These studies demonstrated well the influence of the homologue structure on the bioaccumulation but were limited to C10-C14 chain lengths. In parallel, one study on SCCPs, MCCPs, and LCCPs in exposed aquatic invertebrates via contaminated water and feed revealed the strong potential of LCCPs for accumulation (Castro, Sobek, Yuan, & Breitholtz, 2019). However, contaminants have been shown to feature diverse accumulation behaviours in aquatic or terrestrial species (Sun et al., 2017). It was therefore of particular interest to extend the knowledge on the toxicokinetics of SCCPs, MCCPs and LCCPs at a homologue level on terrestrial vertebrates.
In the present study, the laying hen was selected as model organism, as it is a widely distributed farmed animal around the globe. Two previous experiments on hens confirmed the accumulation of SCCPs in abdominal fat, liver and kidney, although the relative concentration in the tissues did not follow the same trends (Sun et al., 2017, Ueberschär et al., 2007). In a previous work (Mézière et al., 2021), we exposed laying hens to an exposure mixture of CPs with various chain lengths and chlorination degrees, at environmentally relevant levels (5 × 200 ng/g ww, Dong, Li, Su, & Wang, 2019). Substantial amounts of CPs were found in eggs, suggesting that CPs could be absorbed and distributed in laying hens. In this study, we hypothesised that this distribution would be dependent on the homologue formula. We thus collected various tissues and fluids (muscle, liver, fat, serum, and the rest of the carcass) at days 77 and 91, days at which we believed the steady-state was reached. Additionally, excreta (faeces + urine) was collected to attempt a mass balance. The results provide valuable data on bio availability and distribution of CPs in the hens. In particular, to our knowledge this is the first time that LCCPs fate in terrestrial birds has been reported.
Section snippets
Chemicals
The chemicals used in this study, including the five CP technical mixtures for feed fortification, internal and external standards, and other chemicals and solvents used during the sample preparation are detailed in the supplementary data (Section S1) and are the same as in our previous study (Mézière et al., 2021). The five CP technical mixtures cover a range of chain lengths and chlorine contents: SCCPs low %Cl (Chlorowax™ 500C SCCPs, low chlorine content), SCCPs high %Cl (Paroil™ 179 HV,
Results and discussion
The body weight of hens (day 77 and day 91) at slaughter did not significantly differ between the control (1646 ± 84 g) and the exposed (1661 ± 82 g) groups (P > 0.1) (Table S4), nor between exposed hens slaughtered at day 77 or day 91 of the exposure. Additionally, the feed ingested daily was constant over time (P > 0.1), and reached 66 ± 5 g/kg bw/day. Thus, all exposed hens were exposed to the same amount of CPs over the experiment.
As previously reported (Mézière et al., 2021), the control
Concluding remarks and perspectives
The present study aimed to provide a preliminary investigation on the distribution behaviour of CPs in exposed laying hens, depending on their chain length and chlorine number. The exposure of laying hens to five CPs technical mixtures of different chain lengths (SCCPs, MCCPs, LCCPs) and degree of chlorination (low versus high) enabled highlighting the bioavailability of all CP subcategories. However, striking differences according to the chain length and degree of chlorination were observed
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors acknowledge the French Ministry of Agriculture and Food, General Directorate for Food (DGAl) for its financial support. The authors are grateful to (i) Juliane Glüge and Lena Schinkel for kindly providing the I-42 technical mixture, (ii) to the technical staff of the experimental unit PEAT (INRAE, Nouzilly, France) and particularly Nicolas Besné and Philippe Didier for the preparation of feed, rearing hens and collecting eggs, (iii) to Thierry Bordeau, Pascal Chartrin and
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2022, Environment InternationalCitation Excerpt :Breast muscle, egg albumen and bile fluid contained little CPs, whereas a large part of the given dose was excreted via urine and faeces. Also in laying hens, accumulation, and distribution of SCCPs, MCCPs, and LCCPs (five CP products given in the diet) were followed by chemical analyses (Mézière et al., 2021a, 2021b). All CPs were detected in the liver and in this organ, accumulation ratios increased with chlorine content and chain length up to an optimum at C32Cl11.