Equilibrium Passive Sampling of POP in Lipid-Rich and Lean Fish

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Equilibrium Passive Sampling of POP in Lipid-Rich and Lean Fish Tissue: Quality Control Using Performance Reference Compounds Tatsiana P. Rusina,† Pernilla Carlsson,†,‡ Branislav Vrana,† and Foppe Smedes*,† †

Research Centre for Toxic Compounds in the Environment (RECETOX), Masaryk University, Kamenice 753/5, 625 00 Brno, Czech Republic ‡ Norwegian Institute for Water Research (NIVA), Tromsø office, Fram-Centre, P.O. Box 6606, Langnes, 9296 Tromsø, Norway S Supporting Information *

ABSTRACT: Passive sampling is widely used to measure levels of contaminants in various environmental matrices, including fish tissue. Equilibrium passive sampling (EPS) of persistent organic pollutants (POP) in fish tissue has been hitherto limited to application in lipid-rich tissue. We tested several exposure methods to extend EPS applicability to lean tissue. Thin-film polydimethylsiloxane (PDMS) passive samplers were exposed statically to intact fillet and fish homogenate and dynamically by rolling with cut fillet cubes. The release of performance reference compounds (PRC) dosed to passive samplers prior to exposure was used to monitor the exchange process. The sampler−tissue exchange was isotropic, and PRC were shown to be good indicators of sampler−tissue equilibration status. The dynamic exposures demonstrated equilibrium attainment in less than 2 days for all three tested fish species, including lean fish containing 1% lipid. Lipid-based concentrations derived from EPS were in good agreement with lipid-normalized concentrations obtained using conventional solvent extraction. The developed in-tissue EPS method is robust and has potential for application in chemical monitoring of biota and bioaccumulation studies.

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INTRODUCTION Passive sampling is used to estimate freely dissolved concentrations (CW) of persistent organic pollutants (POP) in sediment pore water and surface water as a relevant parameter for assessing exposure to aquatic organism.1,2 The CW is proportional to chemical activity and enables the quantification of the driving force for partition-controlled uptake by organisms and for spontaneous diffusive transport between environmental compartments3 as well the basis for establishing environmental quality assessment criteria.4 Equilibrium passive sampling (EPS) in habitat water, sediment, and fish helps to estimate the degree of thermodynamic equilibrium for POP between these media, which in turn helps to evaluate bioaccumulation.5,6 Polydimethylsiloxane (PDMS)-based passive samplers have been applied in the EPS of POP in fish tissue.7−9 Equilibrium could be confirmed by obtained equal POP concentrations in passive samplers of multiple polymer film thicknesses.7 Concentrations of POP absorbed in PDMS at equilibrium were converted to lipid-based concentrations (CL⇌tissue) using lipid-PDMS partition coefficients.9 Estimated CL⇌tissue from exposure to intact tissue showed good agreement with lipidnormalized concentrations in fish tissue (CL) obtained by conventional solvent extraction, while exposure to tissue homogenate showed a 2-fold higher uptake by the passive sampler, which would lead to an overestimation of CL⇌tissue.7 © XXXX American Chemical Society

Application of in-tissue EPS was shown to be limited to rather lipid-rich fish tissues as equilibrium could not be attained for lean tissue (e.g., lipid content of ≤1%), even after 7 days of sampler exposure in tissue.7 This is because the POP uptake capacity of lean tissue is much smaller than that of lipid-rich tissue, and depletion of POP in the tissue near the sampler surface may occur throughout the contact period with the sampler. Resulting lower concentrations at the sampler surface compared to the bulk tissue reduce the uptake rate and, to restore the concentration, POP need to diffuse from deeper tissue layers to reach the sampler. Consequently, equilibrium may not be attained before tissue decay starts. Therefore, we investigated whether EPS can be applied to fish tissues of very different lipid content, including very lean ones, using thin PDMS films exposed in several ways. The necessary requirements for application of EPS are minimum POP depletion and equilibrium attainment in a practical time span before tissue decay starts. These criteria were assessed by monitoring the POP uptake to PDMS over time and quantifying release of performance reference compounds (PRC) dosed to the passive sampler prior to exposure. To Received: June 18, 2017 Revised: August 20, 2017 Accepted: August 25, 2017

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DOI: 10.1021/acs.est.7b03113 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology 1 1 1 = + ko k tissue kp

our knowledge, the use of PRC release to evaluate equilibration progress has not been applied for in-tissue EPS so far. Second, we wanted to further investigate whether applying intact, homogenized, or cut tissue of various lipid content, including lean tissue, alters its partitioning properties during EPS and, consequently, affects CL⇌tissue. Finally, for the evaluation of the EPS approach, we investigated how CL⇌tissue compares with CL for fish species of different lipid content.

In analogy to aqueous passive sampling, eq 2 can be transformed to:13 δ δP 1 = tissue + ko Dtissue DPKPtissue

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(3)

where δtissue is the diffusion layer at the sampler surface, δP is the half thickness of the polymer, and Dtissue and DP are the diffusion coefficients in tissue and polymer, respectively. Adopting the premise that investigated hydrophobic compounds dominantly reside in lipid, Dtissue will be positively influenced by the lipid fraction (f L), while KPtissue is inversely related to f L, i.e., KPtissue = KPL/f L, where KPL is the polymer− lipid partition coefficient. This implies that k0 will be high in lipid-rich tissues, while low KPtissue requires transport from only a small amount of tissue to attain equilibrium. Consequently, in combination with the high DP of HOC in silicones,14 equilibrium attainment is fast in lipid-rich tissues. For leaner tissue, k0 will be dominantly determined by δtissue/Dtissue because Dtissue will decrease when KPtissue increases. A higher KPtissue implies that a larger volume of tissue needs to be extracted to attain equilibrium. Note that δtissue in eq 3 does not mean the tissue layer thickness to be extracted but a diffusive layer thickness between sampler and bulk tissue, through which compounds need to migrate from bulk tissue to the sampler. Because the bulk phase is static, the consequence of continuous sampler uptake is a gradual increase of δtissue with exposure time.16 Therefore, first order kinetic exchange models do not apply to describe sampler uptake and release in a static exposure,7 and more-complicated modeling thus would be required, similar to static passive sampling in sediments or other semisolid media.15,16 Clearly, in routine in-tissue EPS, achievement of equilibrium is preferred. To attain equilibrium, (1) indicates the importance of high A/VP value, i.e., application of thin samplers. Furthermore, the gradual increase of δtissue in static exposure requires regularly or continuously available fresh tissue at the sampler interface,7 e.g., by relocation of the sampler. Equilibrium Passive Sampling in Fish Tissue. A total of three parallel EPS exposure methods were performed: (1) contact exposure to intact fillet, sampler in static contact; (2) contact exposure to tissue homogenate, sampler in static contact; and (3) rolling exposure to cubes of fish fillet, sampler in dynamic contact. To prevent the POP concentration in the tissue to be affected by sampler uptake (tissue depletion), the sorption capacity in used fish tissue should be much higher than the sorption capacity in the passive sampler. Sorption capacities of sampler and tissue can be compared by expressing both in units of lipid mass:7

EXPERIMENTAL SECTION Materials and Methods. The PDMS SSP-M823 sheets (Specialty Silicone Products, Ballston Spa, NY), 30 × 30 cm and 0.125 or 0.250 mm thick, were cut into 1.5 × 10 cm strips with a total surface area of 30 cm2 (200−400 mg). Prior to use, the PDMS samplers were pre-extracted in a Soxhlet extractor with ethyl acetate for 4 days to remove nonpolymerized monomers, followed by methanol extraction to remove any other impurities. Furthermore, passive samplers were dosed with 13 PCB−PRC, ranging from PCB 1 to PCB 204 and not occurring in technical mixtures, using previously reported procedures.10,11,11 More details on the consumables used can be found in section S1−1 of the Supporting Information. Fish Samples. A total of three fish species of very different lipid content were used: farmed salmon (Salmon salar), farmed carp (Cyprinus carpio), and wild pike-perch (Sander lucioperca). A single salmon (3 kg) and four pike-perches (∼1 kg each) were purchased in a fish shop in Brno (Czech Republic) and used without being frozen before the experiment. A single carp of 1.5 kg was obtained from a local aquaculture company (Czech Republic), stored at −20 °C in a freezer, and thawed before use. Prior to experiments, each fish was dissected, and its intestines were removed from the abdominal cavity. The fish tissue was used for EPS as intact fillets, homogenate, or cut into cubes. Additionally, portions of homogenate were used for the determination of water content, lipid content, and total POP concentrations in each fish sample. The fish tissue was homogenized using a kitchen blender. The water content was determined in a homogenate subsample from the weight loss after drying at 105 °C until a constant weight was achieved. Fish homogenate was extracted according to Smedes,12 and portions of the extract were used for determination of the lipid content and POP concentrations as described in sections S1−2, S1−4 and S1−5 in the Supporting Information. Sampler−Tissue Exchange. Compound exchange between tissue and sampler follows Fick’s first law and is ruled by the following equation: Ako ⎛ dC P CP ⎞ = ⎟ ⎜C tissue − dt VP ⎝ KPtissue ⎠

(2)

(1)

where dCP is the compound’s concentration change in the sampler over time interval dt, A is the surface area of the sampler, k0 is the overall mass transport coefficient, VP is the volume of the sampler (product of sampler mass mP and density ρP), Ctissue is the concentration in the tissue, and KPtissue is the polymer−tissue partition coefficient. Dividing CP by KPtissue converts the sampler’s compound concentration to its equivalent in tissue. The concentration difference between tissue and sampler (the term in brackets) drives the tissuesampler exchange. The rate of exchange depends on the overall mass transport resistance (1/k0), being the sum of the transport resistances in the tissue (1/ktissue) and polymer (1/kP) by:

mPKPL mtissuefL

(4)

where mP and mtissue are the sampler and the tissue mass, respectively. For a negligible depletion, the ratio in eq 4 should be 95% release of all sampler-dosed PRC, including the slowest exchanging congener, e.g., PCB 204. The application of PRC release kinetics for correction of nonequilibrium status of POP is not yet fully developed, although this may be possible in future using appropriate modeling25 and further studies on sampler−tissue mass transfer parameters. For individual compounds, however, the release of their isotope labeled

Figure 3. Lipid-based concentrations obtained by in-tissue EPS (CL⇌tissue) plotted vs lipid-normalized concentrations obtained using solvent extraction of fish tissue (CL). Contact exposure to fillet is represented by shaded squares, contact exposure to homogenate is represented by triangles, and rolling exposure to fish cubes is represented by circles. The dashed line represents unity.

sorption capacity of tissue protein19−21 may become significant and increase the overall capacity, what should lead to a lower CL⇌tissue. An underestimation of CL could be connected to the lipid determination, as for lean tissue, a small amount of coextracted nonlipid material could easily lead to an overestimation of the lipid fraction. Furthermore, the low lipid level in fish tissue might be present in a dispersed or dissolved form exhibiting lower sorption capacity than pure lipid.9 In contrast to CL, the CL⇌tissue does not depend on measured lipid content F

DOI: 10.1021/acs.est.7b03113 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

trophic levels from the same habitat can be used for bioaccumulation and biomagnification assessment. Such assessment can also include CL⇌sediment derived from passive sampling in sediments.5,6 Because abiotic CL⇌media, obtained using EPS well-represents the actual thermodynamic exposure level to which organisms are subjected, CL⇌media seems to be a valid parameter for environmental quality monitoring. If the relations between intissue EPS and aqueous passive sampling are sufficiently substantiated,33 aqueous passive sampling may be a better alternative to biota monitoring, in which the tissue itself is extracted. Replacing biota monitoring with aqueous passive sampling is cost-effective and will contribute to animal welfare. Additionally, biota exposure to bioaccumulative compounds that may pose a risk but do not occur in the organism because they metabolize can nevertheless be assessed using passive sampling in water.

surrogates, dosed to the sampler prior to exposure, will closely reflect the uptake because native and its isotope-labeled compounds are expected to have equal ke and KPL values. Subsequently, CP∞ can be calculated by15

C P∞ = C P

Q0 Q 0 − QP

(6)

where CP is the contaminant concentration in the sampler, and Q0 and QP are its isotope labeled surrogate concentrations in the sampler before and after exposure, respectively. Measured levels of indicator PCB in the fish tissue based on wet weight (see section S14 of the Supporting Information) were a factor of 10−20 lower than the maximum allowed level established by EU regulation for freshwater fish fillet intended for consumption.26 Nevertheless, at this low contamination level in fish tissue, sensitivity of the in-tissue EPS method was sufficient in spite of the limited sampler mass used to avoid depletion of available tissue amounts. A higher sensitivity can be achieved using a larger sampler size in parallel with an equivalently larger mass of fish tissue. Considering the presented developments of in-tissue EPS methodology, we believe that CL⇌tissue expressed on a model lipid basis is an ideal parameter to represent POP contamination levels in fish in a mutually comparable manner. In-tissue EPS excludes the laborious determination of lipid content with related uncertainties and is analytically easier to execute because the matrix effect is diminished compared to solvent extraction of tissue. Co-extraction of lipid is limited to ∼6 mg g−1 PDMS sampler, and absorbed lipid showed no effect on sampler uptake.18,27 Recently, a new polymer passive sampler with considerable higher sorption capacity was proposed,28 but wide suitability for in-tissue EPS is doubtful due to the associated longer equilibrium times. As alternative to PDMS used in this study, LDPE could be applied for in-tissue EPS. Its higher lipid sorption is a disadvantage compared to PDMS, but LDPE’s smaller KPL range for different compounds18 may be an advantage for bioanalytical screening.29 Thermodynamic Exposure Level. CP∞ obtained from EPS in different environmental media allows the direct comparison of contamination levels between media in mutually directly comparable units and their differences quantify thermodynamic gradients which can be used in multimedia assessments.30,31,31 The conversion of C P ∞ to C L⇌media expressed on a defined lipid type (e.g., triolein) provides a measure in environmentally relevant units that can be compared with CL⇌tissue, as KPL are similar for different types of storage lipids.18,29,32 In lipids other than storage lipids, partitioning was expected to be lower by up to a factor of 2.3.20 Nevertheless, CL⇌tissue may more accurately represent the chemical activity or the thermodynamic level inside the organism than CL expressed on tissue lipid of unknown complex composition. Furthermore, CL⇌tissue can be compared to its equivalent for water, i.e., CL⇌water, by converting CP∞ obtained from aqueous passive sampling.5 Obtained CL⇌water should not be understood as a prediction of internal concentration in organisms but rather as the thermodynamic exposure level within the given habitat. Equal CL⇌water and CL⇌tissue indicate that the considered organism is at thermodynamic equilibrium with habitat water. Consequently, CL⇌water does not include concentration enhancement through biomagnification, but the difference of CL⇌water with the CL⇌tissue levels for biota species of different

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.7b03113. Analytical procedures, experimental details, retained PRC fractions in PDMS samplers, modeling uptake using relocations, used equations, uptake and release parameters for all contact exposures, additional graphs, and average POP concentrations in fish. (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: +420-549-493-097; fax: +420-549-492-840; e-mail: [email protected]. ORCID

Foppe Smedes: 0000-0002-1018-0063 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was supported by the Czech Science Foundation, grant go. GACR 15-16512S, “Investigation of accumulation of persistent bioaccumulative toxic organic substances into aquatic organisms”. The authors acknowledge the technical support of Jaromiŕ Sobotka and Ondřej Audy.

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DOI: 10.1021/acs.est.7b03113 Environ. Sci. Technol. XXXX, XXX, XXX−XXX