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Article

Polylactic Acid-Based Microplastic Particles Induced Oxidative Damage in Brain and Gills of Goldfish Carassius auratus

by
Alla Khosrovyan
1,*,
Hranush Melkonyan
2,3,
Lilit Rshtuni
3,
Bardukh Gabrielyan
2,† and
Anne Kahru
1,4,†
1
Laboratory of Environmental Toxicology, National Institute of Chemical Physics and Biophysics (NICPB/KBFI), 23 Akadeemia tee, 12618 Tallinn, Estonia
2
Scientific Center of Zoology and Hydroecology NAS RA, 7 P. Sevak Str., Yerevan 0014, Armenia
3
Institute of Biomedicine and Pharmacy, Russian-Armenian University, 123 H. Emin Str., Yerevan 0051, Armenia
4
Estonian Academy of Sciences, 6 Kohtu, 10130 Tallinn, Estonia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Water 2023, 15(11), 2133; https://doi.org/10.3390/w15112133
Submission received: 5 May 2023 / Revised: 26 May 2023 / Accepted: 31 May 2023 / Published: 4 June 2023
(This article belongs to the Special Issue The Ecological Effects of Micro(nano)plastics in the Water Environment)
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Abstract

:
The effect of 96 h exposure of the goldfish Carassius auratus to two different types of bioplastic particles, originating from commercial shopping bag (Bag, ~5 mm) and polylactic acid-based (PLA) cup (Cup, ≤5 mm), and petroleum-based polyamide particles (PA, 0–180 µm) was studied. All particles were studied as virgin and after simulated UV-degradation (at concentration 30 mg L−1). The experiments were conducted according to OECD 203 test guidelines. The toxicity endpoint evaluated in fish brain and gills was lipid peroxidation (LPO) quantified as nmol thiobarbituric acid reactive substances (TBARs) mg−1 protein. The results indicated that indicatively compostable PLA bioplastic Cup induced significant LPO in the brain and/or gills of the goldfish, in contrast to the particles from Bag and PA (in the brain, Cup > Bag > PA; in the gills, Cup > Bag). The UV-degradation of the particles of all studied types had no significant effect on the LPO level compared to virgin particles. While the increase of LPO in fish gills and brain upon exposure to PLA-plastic particles can be transitory in the long-term perspective, our results point to the necessity of a thorough investigation of the hazard of bioplastics at different state of environmental degradation/weathering.

1. Introduction

Bioplastics are modern alternatives to petroleum-based plastics. Made from renewable biomass such as vegetable oil or corn starch or produced by microorganisms [1,2], in the public perception, bioplastic is associated with biodegradability, indicating a sustainable alternative for humans and the environment. The environmental hazard of petroleum-based plastics has been increasingly evaluated for many species (mostly aquatic) [3]. Exposure to it has caused oxidative stress or damage to marine and estuarine bivalves [4,5] and planarias [6], damage to gut epithelium, inflammatory responses in freshwater chironomids [7], and the depletion of energy reserves in marine worms [8]. On the other hand, no effect on the life cycle of chironomids and zooplankton has been shown [9,10], while the successful egestion of ingested microplastics by chironomid and zebrafish has been demonstrated [11].
While the hazards posed by bioplastics—an increasingly marketed green alternative to petroleum-based plastics—is considerably less studied [12,13], the available data points to the toxicity and problematic degradability of bioplastics. For example, bioplastics made from polylactic acid (PLA) cannot be easily colonized by microorganisms due to their high molecular weight; these plastics are not biodegradable [12,14]. They can only be decomposed at industrial composting facilities involving high-temperature, -humidity, and -pH conditions optimal for that process [15,16]. For instance, an oxo-degradable polyethylene commercial bag did not show significant mass loss or molecular weight changes after incubation at 70 °C for 365 days [17]. Four shopping bags (oxo-biodegradable and biodegradable) were tested for biodegradability in soil, air, and marine water, but none showed adequate signs of degradation (changes in chemical composition such as appearance of carbonyl stretch) or functional deterioration (unsuitability to hold any weight) after 3 years [18]. A compostable bag, although it disappeared completely in seawater after 3 months, remained intact when buried in soil [18]. Out of five biodegradable polyesters (PLA, poly(lactic-co-glycolic acid)—PLGA, polycaprolactone—PCL, poly(3-hydroxybutyrate)—PHB, and Ecoflex) exposed to fresh and seawater for one year, only PLGA degraded fully, while PHB only experienced surface erosion, and PLA and PCL showed no sign of degradation (e.g., mass loss of polymers) [19].
In addition to problematic biodegradability, bioplastics can be as toxic as petroleum-based ones. The toxicological effects of bioplastics include inflammatory reactions to PLA-based implants and drug delivery systems in rats and humans [20], and altered intestinal microbiome and epithelial damage in zebrafish after 5 days of exposure to bio-based PET and PLA particles (111–135 µm, at 10–17 mg L−1) [21]. Microfragments of 10% PLA-based plastic reduced the biomass and chlorophyll content of maize leaves [22]. Residues of biodegradable plastic film (Bio) changed wheat rhizosphere’s bacterial communities, exerting selective pressure on various bacterial taxa. It also altered soil chemical properties, causing a significant increase in carbon, as measured via nitrogen ratio compared to the control [23]. Finally, biodegradable plastics can be stronger vectors of pollutants than petroleum-based plastics [24,25]. Hence, bioplastics are potent enough to induce changes and must therefore be thoroughly examined for their ecotoxicity before policymakers make decisions regarding the beneficial use of bioplastics, especially if the ecological risks of bioplastics are largely unknown [21].
Biomarkers have been successfully used for the evaluation of the toxicity of environmental contaminants, including metals [26,27], pesticides [28,29], pharmaceuticals [30], and plastic particles [12,31,32,33]. The most commonly used biomarkers are those connected to oxidative stress, the most common response of living organisms to environmental contaminants. It refers to a condition in which a cell or tissue deviates from a homeostatic reductive state [34], caused, for instance, by free radicals derived from oxygen (reactive oxygen species, ROS). While ROS are normally produced during metabolic reactions in any aerobic organism as a result of its normal biochemical and physiological processes [35], their production is augmented once the organism is exposed to a stressor, such as environmental contaminants [36]. ROS can target nucleic acids, proteins, and lipids, damaging their structure and function [37,38]. The increased levels of ROS might result in oxidative damage if not counteracted by the antioxidant system of the cell that scavenges and destroys them. The cell’s capacity to detoxify these oxidative agents or failure to prevent oxidative damage can be assessed by measuring biomarkers indicating the peroxidation of the cell lipid membranes, called lipid peroxidation (LPO). Elevated levels of malondialdehyde (MDA), one of the end products of LPO (measured as thiobarbituric acid reactive substances—TBARS), may point to oxidative stress caused by ROS [39]. LPO leads to the loss of membrane function and can decrease the fluidity of the cell membranes, impeding the passage of proteins and nutrients [40]. The end products of peroxidation can also cause DNA and protein damage [41].
The cyprinid Carassius auratus, the goldfish, is a commonly used fish model in ecotoxicity studies due to its wide availability and easy handling. Goldfish have been successfully used in both short-term (e.g., as short as 60 min) and long-term (e.g., nearly two months) exposure studies employing various endpoints (e.g., oxidative stress, LPO, behavioral changes, neurotoxicity, transcriptomic changes) [42,43,44,45,46,47,48]. In particular, C. auratus has shown significantly elevated MDA levels in the brain and liver (but not in the gills) after exposure to 0.5 mg L−1 of polyvinyl chloride (PVC) microplastic (0.1 to 1000 μm size) for 96 h [49]. Microplastic particles were shown to accumulate in the gills of caged C. auratus deployed in the Qinhuai River (China) for 28 days, although this was not apparently correlated with the concentration of microplastic in the riverine water and sediment [50].
In the current work, we present data from a preliminary study that analyzed and compared the potential toxicity of two types of plastic material—bioplastic vs. petroleum-based plastic—to fish. As the model fish, the standard aquatic test organism, goldfish C. auratus, was used. To better address the environmental impact of plastic, two states of each plastic type were considered: before and after simulated environmental degradation (exposure to artificial UV irradiation). UV degradation is an environmentally relevant degradation pathway for any plastic discarded into the environment. The potential toxicity of plastic particles was evaluated by determining the oxidative damage biomarker LPO. The results address missing data on the comparative toxicity of bioplastics and conventional plastics to aquatic organisms, contributing to the risk assessment of bioplastics. By considering different states of plastic (virgin and UV-weathered), this paper offers new information about the potential toxicity of UV-degraded microplastics.

2. Materials and Methods

2.1. Plastic Particles: Types, States, Concentration

Two types of plastic material were considered in this study: bioplastic and petroleum-based plastic. Bioplastic material was obtained from two products/items sold in supermarkets: a fruit and vegetable bag (BioBag brand) and a cup (Bag and Cup, hereinafter). The Bag was made of “4th generation raw material, with a higher content of renewable sources”, according to the description on the website of the brand (https://biobagworld.com/products/retail-2/ (accessed on 4 May 2023). The Cup was made of PLA, as indicated by the manufacturer (Figure 1). Both products bore a “compostable” emblem, in accordance with the European Standard EN 13432, and hence, both of these materials were declared as fully biodegradable. Particles were obtained using an electric coffee grinder. After grinding, the Bag particles became tightly folded and were further cut manually with scissors into small (still tightly folded) pieces of ~5 mm (Figure 1a). The particles obtained after grinding the Cup measured ≤ 5 mm, with different shapes and relatively rigid edges (Figure 1b). Petroleum-based plastic particles (polyamide, PA) were used as has been described previously [9,10,11]. Briefly, the polyamide particles were obtained from Abifor company (Wutoeschingen, Germany) and consisted of particles of different shapes and sizes ranging from 0 to 180 µm (Figure 1c).
The particles used were in two different states: virgin (before being subjected to UV irradiation) and UV-degraded (after UV irradiation to simulate photo degradation). UV irradiation was applied under the conditions described elsewhere [10,51]. Briefly, UV degradation was simulated via exposure to five UV-C light tubes (15 W each, max. wavelength 254 nm) for 26 days in a customized irradiation chamber. The temperature in the chamber was regularly checked and varied from 33–35 °C. PA microplastic particles were UV-irradiated in a clean-water environment and were air dried before being used in the experiments. Bioplastic particles were UV-irradiated in a dry environment. During the irradiation period, the particles were regularly mixed to ensure uniform exposure and hence degradation. After UV irradiation, the PA particles changed in color (acquired a brownish color) and buoyancy (sank to the bottom of the vessel); the release of small particles from the PA and the Cup was observed. The concentration of the plastic particles (30 mg L−1) was within the environmental concentration range commonly reported [52,53].

2.2. Water Parameters

Water temperature, pH, total dissolved solids, and oxygen content, a set of parameters suggested by the OECD 203 guidelines for fish acute toxicity static tests [54], were measured before, during, and at the end of the acclimation and exposure periods using portable devices (Hanna Instruments, Woonsocket, RI, USA). The water hardness was obtained from the municipal water supply company for the area where the Scientific Center of Zoology and Hydroecology (SCZHE) is located (the experiment was conducted at the premises of the SCZHE).

2.3. Organisms and Exposure

2.3.1. Acclimation

Eighty goldfish (C. auratus) of predominantly 3–4 g body weight were obtained from a local commercial supplier and acclimated in 60 L plastic tanks (40 × 60 × 25 cm) for 10 days (48 h of settlement and 8 days of acclimation). The tanks were filled with dechlorinated tap water and were constantly aerated. During this period, water temperature, pH, total dissolved solids, and oxygen content were checked daily, and fish mortality and behavior were monitored. Fish were fed daily with standard granulated fish food (Tetra) obtained from the same supplier. The water in the tanks was partially (~30% of volume) renewed on the fourth day with dechlorinated tap water to prevent possible mortality of fish due to water quality deterioration. Acclimation was performed in accordance with the OECD 203 guidelines for fish acute toxicity static tests [54].

2.3.2. Experiment

The experiments were performed in similar tanks under the same environmental conditions as for acclimation (water type, ambient temperature, photoperiod, food type, etc.). The plastic particles used in the experiments were denoted as follows: Bag-V (virgin state of the bioplastic Bag), Bag-UV (irradiated state of the Bag), Cup-V (virgin state of the bioplastic Cup), Cup-UV (irradiated state of the Cup), PA-V (virgin state of the petroleum-based polyamide), and PA-UV (irradiated state of the polyamide). The particles were added to the tanks and mixed prior to fish introduction. Each tank was randomly populated with 9 fish from the acclimation tanks; feeding was provided daily throughout the experimental period (96 h). No water renewal occurred during this period. Shortly after the addition of the particles, most sank to the bottom where the fish fed (Figure S2).
As a control medium, the same dechlorinated tap water was used. The experiments were performed in one replicate, in accordance with the OECD 203 guidelines for fish acute toxicity static tests [54].

2.4. Oxidative Damage Biomarker—LPO

At the end of the exposure period (96 h), the fish were euthanized in accordance with the Directive 2010/63/EU for the humane killing of fish for scientific research and the requirements of the ad hoc ethical committee at the SCZHE. Two or three fish were gradually captured with a net, transferred to a bowl with an overdose of MS-222 (tricaine methanesulfonate) for anesthesia, and subsequently euthanized by cervical dislocation.
Euthanized fish were kept at −80 °C until later use. For biomarker analysis, gill and brain samples were collected, washed in the 0.1 M phosphate buffer (pH 7.5), and dried on filter paper. Three sub-samples were drawn from the pooled sample tissue (gill or brain) for each experimental group (three replicates). Each replicate was weighed and manually homogenized with a pestle and a few sand particles in the phosphate buffer (2 mL).
A few droplets of ethanol-based 2,4-dimethyl-6-tert-butylphenol solution (5 mM) were added to the supernatant in order to prevent LPO in samples. LPO was determined by the presence of thiobarbituric acid reactive substances (TBARs). To determine this, a reaction mixture containing 250 µL of 30% trichloroacetic acid and 0.5 M hydrochloric acid, 500 µL of 0.75% 2-thiobarbituric acid, and 500 µL of sample in a glass vial (total volume 1.5 mL) was incubated for 20 min in a boiling water bath. After cooling and centrifugation (10 min at 1000 g), LPO was determined by absorbance at 532 nm (molar extinction coefficient 156 × 103 M−1 cm−1 (MRC Spectro UV-18 spectrophotometer)). The results were expressed per amount of protein in the sample as nmol of TBARs per mg−1 of protein.

2.5. Total Protein

Total protein analysis was carried out colorimetrically (at 595 nm) using Bradford reagent (Coomassie brilliant blue × 5 concentrate, 99.7 vol% ethanol and 85% phosphoric acid) and 20 µL of tissue homogenate. Bovine serum albumin was used to construct a standard curve for the measurement of protein concentrations in the samples [55].

2.6. Statistical Analysis

The mean values of triple sub-samples per experimental group were determined using MS Excel. One-way ANOVA analysis with Tukey post hoc tests (p < 0.05) for significant differences was run in R (version 3.6.1, 5 July 2019). Our assumptions regarding normality and homoscedasticity were verified.

3. Results

3.1. Validity of the Test

As no mortality of fish occurred during either the acclimation or exposure periods, the conditions for test validity were satisfied. Moreover, fish did not exhibit any unusual swimming or feeding behavior. The characteristics of the overlying water (dechlorinated tap) used in the experiment are presented in Table 1.

3.2. Significant Impact of Plastic Exposure on the Oxidative Damage Biomarker (Lipid Peroxidation) in the Brain and Gills of Carassius auratus

3.2.1. Comparison with the Control

LPO levels (nmol of TBARs per mg of protein) in fish brain and gills across experimental groups are shown in Figure 2. Values significantly different from the control are denoted by * (p < 0.05).

3.2.2. Lipid Peroxidation in the Brain and Gills: Virgin Particles (Bag, Cup, and PA)

Significant differences in the LPO levels among the groups exposed to virgin plastic were observed, as follows: in the brain, Cup-V > Bag-V (44 vs. 26 nmol mg−1, correspondingly) and Cup-V > PA-V (44 vs. 13 nmol mg−1, correspondingly); in the gill, Cup-V > Bag-V (119 vs. 52 nmol mg−1, correspondingly) (Figure 2 and Figure S3).

3.2.3. Lipid Peroxidation in the Fish Brain: UV-Degraded Particles (Bag, Cup, and PA)

Significant differences in the LPO levels among the groups exposed to UV-degraded plastic were observed, as follows: in the brain, Bag-UV > Cup-UV (52 vs. 14 nmol mg−1, correspondingly) and Bag-UV > PA-UV (14 vs. 6 nmol mg−1, correspondingly). However, the LPO level of Bag-UV was not significantly different from that of the control (Figure 2 and Figure S4).

3.2.4. Lipid Peroxidation in Fish Brain and Gills: Virgin and UV-Degraded Particles (Cup)

Significant differences were found in both organs only between the virgin and UV-degraded PLA Cup groups. Exposure to the virgin Cup resulted in the significantly higher LPO in both organs than exposure to UV-degraded Cup: in the brain, Cup-V > Bag-V (44 vs. 14 nmol mg−1, correspondingly); in the gill, Cup-V > Bag-V (119 vs. 48 nmol mg−1, correspondingly) (Figure 2 and Figure S5).

3.2.5. Comparison of Lipid Peroxidation in Fish Brain and Gills upon Exposure of Fish to Different Types of Studied Plastic Particles

No significant differences between the brain and gills were found. However, in general, LPO evidence in the gill was generally greater than in the brain (Figure 2).

4. Discussion

In this work, the potential of two types of plastic material (petroleum-based and bioplastic), both in two different states (virgin and UV-degraded) to cause oxidative damage (LPO) in the brain and gill of the goldfish C. auratus was examined.

4.1. Impact of Exposure to Plastic Particles on Lipid Peroxidation in Carassius auratus Brain and Gills

The oxidative damage to the brain and gills of goldfish after exposure for 96 h to the virgin PLA-based Cup was the most remarkable event observed, significantly exceeding that of the control (Figure 2). Importantly, other researchers have reported elevated oxidative damage in these organs after exposing even larger goldfish (10.3 ± 4.1 g; 5–7 cm) to a lower concentration (0.5 mg L−1) of virgin PVC microplastic (0.1–1000 µm, 50% less than 140 µm) for the same period (four days); meanwhile, at a lower PVC concentration (0.1 mg L−1), the differences were insignificant [56]. Low or physiological LPO rates cannot suppress the cell’s antioxidant defense systems, while higher LPO rates provide evidence that the cell repair capacity was exceeded [57]. Apparently, the particles of the PLA bioplastic had greater potency in compromising the cell defense system, compared to the petroleum-based PA or Bag bioplastic. There could be several possible reasons, although the exact mechanisms of the effect of plastic particles on organisms (DNA damage, neurotoxicity, reproduction impairment, oxidative stress, histopatological changes) remain largely unknown [49,56]. Firstly, the occurrence of stress or damage signs in fish may be triggered by the ingestion of particles. For example, in one study, the adult zebrafish Danio rerio ingested polyethylene microplastics (~60 µm, at 50 and 100 mg L−1) during a 96 h exposure period, and this led to significantly reduced acetylcholinesterase activity in the brain (neurotoxiciy biomarker) and increased gill glutathione-S-transferase activity (GST, oxidative stress biomarker) [58]. In addition to the above-mentioned elevated LPO levels in the brain and liver of C. auratus exposed to virgin PVC microparticles, intestinal villi were also shortened [56]. Even if the particles are finally rejected (expelled) by fish, damage can still occur. For example, the chewing and expelling of polystyrene and polyethylene acrylate particles (2.5–5 mm) resulted in a deep incision in the lower lip and pharyngeal pad of C. auratus [59]. Although we observed that C. auratus was selective in choosing food (avoided the uptake of Bag particles), an accidental uptake of hard PLA Cup particles from the contaminated environment could have taken place, and this could challenge the cell’s defense system. Fish often co-capture plastic particles with food [48] or confuse food with plastic particles which resemble their food: e.g., for goldfish, green color resembles plant and dark colors resemble insects [60]. An accidental uptake of plastic particles is considered the main cause of ingestions reported in the literature [61,62]. Although the ingestion of particles by the goldfish was not quantified in this study as being beyond its scope, the active ingestion of plastic particles was assumed to have taken place.
Secondly, mechanical abrasion caused by particles’ edges can also lead to a biomarker response [49]. Physical damage to the gut epithelium may let gut microorganisms enter into the other tissues of organisms, as a result of which the immune system is activated for protection and tissue repair. For example, in insects, melanogenesis (immune system response) is initiated to encapsulate and defend the organism against pathogens [63]. ROS, as part of an inflammatory reaction to physical damage, may not be counteracted by the oxidative defense system of organisms during a short exposure period. For example, 48 h exposure to larger polyethylene particles (63–500 µm) led to significantly higher LPO levels (and also significantly less GST activity) in the aquatic larvae Chironomus riparius than exposure to smaller particles (<32 µm) [10]. The pool of PLA Cup bioplastic used in the current study consisted of particles of various sizes and shapes, which had relatively rigid edges, compared to soft PA and Bag particles (Figure 1). Hence, physical abrasion of the gill tissue by Cup particles could have also contributed to the significantly elevated LPO levels observed (Figure 2).
On the other hand, ingestion may not necessarily damage the organs, as damages are organ-specific, depending on particle concentration and exposure time. For example, despite the presence of PVC particles at 1 mg L−1 (0.1–1000 µm, 50% of which were less than 140 µm in size) in the gut of fish Barbodes gonionotus, intestinal damage was not observed by histological examination [49]. Ingestion of the same particles at 0.5 mg L−1 caused no oxidative injury or histomorphological alteration in the gill but led to a significant increase in brain and liver LPO levels in the goldfish. Nevertheless, regardless of the reason for the observed LPO levels, the potency of the PLA Cup particles to cause LPO in the gill and brain of goldfish during such a short exposure time (96 h) indicates the urgent need for further studies.

4.2. Lipid Peroxidation in Carassius auratus Brain and Gill upon Exposure to Virgin Plastic Particles: Bioplastic versus Petroleum-Based Plastic

The brain LPO levels after exposure to the virgin Bag and Cup particles significantly exceeded that of the virgin PA group (Figure S3). However, the brain and gill LPO evidence significantly exceeded that of the control only after exposure to the Cup particles (Figure 2). Hence, exposure to the virgin Bag and PA particles caused low (physiological) levels of LPO, apparently not posing a threat to the fish, in contrast to the effect of the virgin PLA Cup particles. Although we have not been able to clarify the cause-and-effect relationship behind this effect, our results suggest that bioplastics (perceived by the society as environmentally safe) could harm aquatic organisms and must be investigated as thoroughly as possible regarding the potential adverse effects on the resident communities.

4.3. Lipid Peroxidation in Carassius auratus Brain and Gill upon Exposure to UV-Degraded Plastic Particles: Bioplastic versus Petroleum-Based Plastic

The UV irradiation of plastic particles breaks the polymer molecules into smaller pieces by breaking down polymeric C–C bonds and leading to chain scission [64,65]. This, in turn, makes the plastic brittle and hence increases the share of smaller particles, contributing to a greater availability of particles to organisms. In addition, in the process of photo-oxidation, free radicals are formed by the breaking of C–H bonds, which further react with oxygen to form a peroxyl radical and other oxygen-containing functional groups. For example, olefins, aldehydes, and ketones formed during this process contain unsaturated double bonds, which are more susceptible to photo-oxidation [21,64,66,67]. Hence, chemical changes occurring in the plastic polymer matrix following UV-irradiation were expected to result in a more pronounced effect of UV-degraded particles on the fish, compared to virgin ones.
However, although the brain LPO levels after exposure to the Bag-UV significantly exceeded those of PA-UV and Cup-UV exposure (Figure S4), no significant oxidative damage (compared to the control) occurred as a result of exposure to UV-degraded particles: LPO levels in both organs after exposure to UV-degraded particles of all studied types remained within the physiological range of LPO (Figure 2).

4.4. Lipid Peroxidation in Carassius auratus Brain and Gill upon Exposure to Virgin and UV-Degraded Plastic Particles of Different Types: Bag, PLA-Based Cup, PA

The LPO levels observed after exposure to virgin plastic of all types were greater than their UV-degraded counterparts (Figure 2). Specifically, in the case of the PLA Cup, brain and gill LPO levels after exposure to virgin particles were significantly greater than the levels after exposure to the UV-degraded PLA Cup (Figure S5). Hence, our results demonstrate a lower effect of UV-degraded plastic particles compared to the virgin ones. Published data has also demonstrated a decrease in the toxicity of leachate obtained after the UV irradiation of plastic material, suggesting that the toxicity of particles may depend on the irradiation time. For example, in a 96 h exposure study, a leachate from a biodegradable bag became more toxic to copepod Nitocra spinipes after being exposed to artificial sun application for 96, 192, and 288 h than before irradiation. Meanwhile, a leachate from a DVD case only became toxic after 192 h of irradiation [68].

4.5. Effects of Exposure to Plastic Particles in Lipid Peroxidation in Two Studied Fish Organs: Gills versus Brain

The LPO levels in the gills were generally greater than those in the brain (Figure 2). Such an elevation in the gill LPO level was presumably related to the direct exposure of gills to plastic particles. Several studies have reported higher susceptibility of gills compared to other organs of fish to the adverse effects of environmental pollutants. For example, small fibrous microplastic (>20 µm) was lodged more in the gills than in the guts of 13 fish species sampled from China coastal areas [69]. The LPO levels in the gills of fish Anabas testudineus exposed to herbicide were greater than those in the brain tissue [70]. However, gill response seems to be species-, microplastic-, and concentration-specific. For example, in [70], another fish, Heteropneustes fossilis, showed no difference between gill and brain LPO levels upon exposure to the same herbicide. Brain and liver LPO levels significantly increased in the goldfish exposed to PVC at 0.5 mg L−1, while no difference was found in gill response [56].
In this work, LPO in gills was greater after exposure to particles from the pool that included a larger share of small particles (PLA Cup and PA in both states) (Figure 2). This may be related to irritation, inflammation, or other physiological responses to the adherence of small particles to the gills. On the other hand, microplastics could not adhere permanently to the gill filaments due to the rinsing out of the gills and mucus excretion [71]. Lipid damage may depend on fish species, toxicant type and size, and target organ, among other factors. In C. auratus exposed to PVC microplastic particles at 0.5 mg L−1, the LPO level in the brain was higher than that in the gills, where it remained at the control level [56].
The observed effects may be transitory during the life cycle of the goldfish and may not necessarily lead to long-term harm. In living organisms, various antioxidation pathways exist and the end products are quickly removed. For example, the experimental exposure of C. auratus to sodium arsenite (for 1–7 days) demonstrated oxidative stress development in the liver during the first days, followed by its reduction by the fourth day due to de novo synthesis of reduced glutathione, which fostered the detoxification of arsenic [72]. Nevertheless, although the end products of oxidative damage are not very sensitive indicators of LPO in in vivo studies [72], our results highlighted a necessity for a more profound study on the potential toxicity of bioplastic items discarded into the environment.

5. Conclusions

In conclusion, the effect of 96 h exposure of the goldfish C. auratus to bioplastic and petroleum-based plastic particles (in both virgin and UV-degraded states) on gill and brain LPO was evaluated using the quantification of TBARs. The results indicated that virgin particles originating from a commercial (indicatively compostable) PLA bioplastic Cup were apparently more harmful than the particles originating from the bioplastic shopping Bag and petroleum-based polyamide PA: the PLA Cup particles induced significant oxidative damage to the brain and/or gills of the goldfish. The effect of particles, in order of the LPO level, was as follows: (i) for the fish brain: PLA Cup > Bag > PA (44, 26, 13 nmol TBARS mg−1, correspondingly); and (ii) for the fish gills: PLA Cup > Bag (119 and 52 nmol TBARS mg−1). However, the UV-degraded counterparts of the Cup PLA particles did not demonstrate a potential to cause oxidative damage. The need for a comprehensive evaluation of the hazards of bioplastics at different stages of environmental degradation/weathering is urgent.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w15112133/s1, Figure S1: PLA-based Cup (material indicated by arrow) on the left and biodegradable shopping bag (https://biobagworld.com/products/retail-2/, accessed on 4 May 2023) on the right. Both products had a sign of “compostable” in accordance with the European Standard EN 13432 and hence were declared as fully biodegradable materials; Figure S2: Particles of biodegradable shopping bag sunk within a few days after addition to the tank; Figure S3: Lipid peroxidation measured as nmol TBARS mg-1 protein (mean ± SD, n = 3) in brain (left) and gill (right) of Carassius auratus exposed to virgin plastic materials: bioplastics (Bag and Cup) and petroleum-based polyamide (PA). V: material before subjecting to UV irradiation (virgin). Same letters show significant differences between denoted groups (p < 0.05); Figure S4: Lipid peroxidation measured as nmol TBARS mg-1 protein (mean ± SD, n = 3) in the brain of Carassius auratus exposed to UV-degraded plastic particles: bioplastics (Bag and Cup) and petroleum-based polyamide (PA). UV: material after subjecting to UV degradation for 26 days. Same letters show significant differences between denoted groups (p < 0.05); Figure S5: Lipid peroxidation measured as nmol TBARS mg-1 protein (mean ± SD, n = 3) in brain and gill of Carassius auratus exposed to virgin and UV-degraded bioplastics (Cup). V: material before subjecting to UV irradiation (virgin), UV: material after subjecting to UV degradation for 26 days. Same letters show significant differences between denoted groups (p < 0.05).

Author Contributions

Conceptualization, A.K. (Alla Khosrovyan) and A.K. (Anne Kahru); Formal analysis, A.K. (Alla Khosrovyan); Investigation, A.K. (Alla Khosrovyan), B.G. and H.M.; Methodology, A.K. (Alla Khosrovyan), H.M. and L.R.; Project administration, B.G. and A.K. (Anne Kahru); Resources, B.G. and L.R.; writing—original draft, A.K. (Alla Khosrovyan); writing—review and editing, B.G. and A.K. (Anne Kahru). All authors have read and agreed to the published version of the manuscript.

Funding

The research was funded by Estonian Research Council grants (Mobilitas Pluss MOBJD509, TT13 and PRG749) and European Regional Development Fund grants (NAMUR+ 2014-2020.4.01.16-0123 and TK134). The work was also supported by the Science Committee of Armenia, grant No. 21T-1F183.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 15 02133 g001 550
Figure 1. Plastic particles used in the experiment: (a)—fragments of tightly folded particles from a soft, compostable shopping bag (Bag, ~5 mm); (b)—fragments of a hard, compostable PLA-based cup (Cup, ≤5 mm); (c)—petroleum-based polyamide particles (PA, 0–180 µm). Top panels: particles before being subjected to UV-degradation. Bottom panels: after being subjected to UV degradation for 26 days (UV-degraded for 26 days).
Figure 1. Plastic particles used in the experiment: (a)—fragments of tightly folded particles from a soft, compostable shopping bag (Bag, ~5 mm); (b)—fragments of a hard, compostable PLA-based cup (Cup, ≤5 mm); (c)—petroleum-based polyamide particles (PA, 0–180 µm). Top panels: particles before being subjected to UV-degradation. Bottom panels: after being subjected to UV degradation for 26 days (UV-degraded for 26 days).
Water 15 02133 g001
Water 15 02133 g002 550
Figure 2. Lipid peroxidation measured as nmol of TBARS per mg−1 of protein (mean ± SD, n = 3) in the brain and gills of Carassius auratus exposed to two types of bioplastics (Bag and Cup) and petroleum-based polyamide (PA) particles. V: material before subjecting to UV irradiation (virgin), UV: material after subjecting to UV degradation for 26 days. Significant differences (p < 0.05): *—compared to the control, a—compared to Cup-V.
Figure 2. Lipid peroxidation measured as nmol of TBARS per mg−1 of protein (mean ± SD, n = 3) in the brain and gills of Carassius auratus exposed to two types of bioplastics (Bag and Cup) and petroleum-based polyamide (PA) particles. V: material before subjecting to UV irradiation (virgin), UV: material after subjecting to UV degradation for 26 days. Significant differences (p < 0.05): *—compared to the control, a—compared to Cup-V.
Water 15 02133 g002
Table
Table 1. The characteristics of the overlying water used for the 96 h experiment at various periods: initial (dechlorinated tap water) and during acclimation and exposure periods.
Table 1. The characteristics of the overlying water used for the 96 h experiment at various periods: initial (dechlorinated tap water) and during acclimation and exposure periods.
WaterTDS
mg L−1		Conductivity
µS/cm		Oxygen
mg L−1		pHT
°C		TH
mg L−1
Initial771558.77.619100
Acclimation,
exposure		84–97155–1796.87–7.987.6–7.819–20-
Notes: TDS: total dissolved solids, TH: total hardness, -: not measured.
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Khosrovyan, A.; Melkonyan, H.; Rshtuni, L.; Gabrielyan, B.; Kahru, A. Polylactic Acid-Based Microplastic Particles Induced Oxidative Damage in Brain and Gills of Goldfish Carassius auratus. Water 2023, 15, 2133. https://doi.org/10.3390/w15112133

AMA Style

Khosrovyan A, Melkonyan H, Rshtuni L, Gabrielyan B, Kahru A. Polylactic Acid-Based Microplastic Particles Induced Oxidative Damage in Brain and Gills of Goldfish Carassius auratus. Water. 2023; 15(11):2133. https://doi.org/10.3390/w15112133

Chicago/Turabian Style

Khosrovyan, Alla, Hranush Melkonyan, Lilit Rshtuni, Bardukh Gabrielyan, and Anne Kahru. 2023. "Polylactic Acid-Based Microplastic Particles Induced Oxidative Damage in Brain and Gills of Goldfish Carassius auratus" Water 15, no. 11: 2133. https://doi.org/10.3390/w15112133

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