A review of microplastic pollution in commercial fish for human consumption

Introduction

In recent years, plastics have been widely used by society with immense applications in different industries due to their excellent physical and chemical properties such as lightness, durability, low production cost, high power to weight ratio, and low thermal conductivity among other properties [1, 2]. Plastics end up in the environment during their production and after their application; cause them as one of the mass-produced urban waste materials contributing to the environmental contamination and pollution especially in the marine litter [2], [3], [4]. Among plastic particles, microplastics (MPs) with a diameter <5 mm have received worldwide attention as an emerging environmental pollution and one of the four major global environmental threat together with ozone depletion, global climate changes, and ocean acidification with health hazard to human [5], [6], [7]. These MPs can be divided into two main groups: (1) primary MPs produced by plastic pellets (plastic beads), fibers, films, granules and powders used in manufactured products such as cosmetics, sunscreens, detergents, and drug vectors [8]; (2) secondary MPs produced by physical, chemical, and biological degradation of larger piece of plastics gradually through mechanical abrasion, UV-radiation, light degradation, and biological degradation in the environment [9]. MPs have been detected in different environments and media such as rivers, oceans, sewages, sediments, and soil [10], [11], [12]. They also have been observed in food products as varied as beer, canned sardines, honey, and drinking water [13, 14] which finally come into the food table and direct contact with human [15]. Widespread use of plastics and environmental contamination associated to plastics will certainly lead to human exposure to MPs. Human are exposed to plastic particles every day through the oral inhalation of nanoplastic-containing aerosols, diet, and dermal contact [16], [17], [18]. Exposure due to ingestion of contaminated foods [19] results to the intake of 39,000–52,000 particles per person per year [20] and even more by taking into account the settling dust on plates during mealtimes [21]. In considering the high level of food contamination with MPs, this level of intake is not surprising. Indeed, related pollution from other sources (e.g., packaging containers) is still unknown [22]. Considering that plastic debris accounting for about 60–80% of all marine litter and reaching to 90–95% in some areas, sea products are a primary source of food for humans [2, 3]. MPs ingestion is confirmed by various marine organisms (zooplankton, bivalves, fish, copepods, etc.) [23], [24], [25], with their accumulation in different tissues (gill, digestive gland, gut, circulatory system, etc.) [26], [27], [28], and transportation through the food chains (e.g., transfer in planktonic food web, through zooplankton to fish, from mussel to crab, etc.) [29], [30], [31]. Hence, accumulation and distribution of MPs by commercially important aquatic organisms is expected to lead to greater exposure risk for human populations with possible adverse effects over time. Several authors reported that the accumulation and distribution of MPs in marine organisms is species-specific with a dependency to the particle size. So that, MPs of 8–10 μm are mainly resided in crab gill and gut [26]; MPs of 10 μm can be transported into the circulatory system of mussels [23]; and MPs of 5 μm are accumulated in the liver of zebrafish [31]. Accumulation of MPs in tissues could induce physical stress and damage, oxidative stress, inflammation, and immune responses [32] (Figure 1).

Figure 1:

Conceptual model of the potential routes for the transport of microplastics in marine environment, and their bioavailability and toxicity.

Indeed, MPs present in the environment contain other contaminants as a vector, including heavy metals, additives, pharmaceuticals, pesticides and various other persistent organic pollutants [33], [34], [35]. Such contaminants may be transferred through organisms from smallest planktivorous to large fish and mammals and affect marine food chains [26, 36, 37]. Although the effects of MPs on humans cells and tissues have remained rather unclear [38, 39], several authors have heightened that MPs enter the human respiratory, digestive, and circulatory systems, acting as both chemical and stressors physical to the human system, and linked to several human diseases including diabetes, obesity, endocrine disturbance, cancer, cardiovascular, reproductive and developmental problems, which pose a significant risk to human health [40], [41], [42], [43], [44]. Evidence of MPs detection in human stools indicates that the quantity taken in is remarkably large [45]. While most in vitro studies have identified the correlation between properties of MPs and human health risk after exposure to plastic additives [34, 46, 47] and the toxic effects on aquatic organisms, studies documenting the tissue accumulation of MPs and potential health risk in mammals are lacking. To date, little evidence of MPs impact on human cell viability have been found [48], [49], [50]; however, it is unknown whether the applied range of exposure concentrations in such studies is completely representative of the MPs accumulated in the body tissues. Moreover, uncertainties about the concentrations of MP exposure and intake rates resulted in many controversies in the context of the probable risks of MPs to human health [38, 51]. So, the evaluation of the amount of MPs introduced to the human system seems to be pivotal. Regarding the long-term human consumption of commercial fish as a main food supply, the central aim of this work was to review the published literature on the contamination of commercial fishes by MPs and the potential intake to human from the exposure to MPs through the commercial fish’s muscle consumption.

Microplastic in commercial fish for human consumption

Globally, most humans consume seafood products especially fish due to its economic well-being and nutritional security, so that it provides approximately 15% of people’s need to animal protein intake [52]. However, the capacity for fish to ingest MPs has increased the concern of human consumption [53, 54]. Marine fishes may ingest MPs either intentionally through feeding in the water column or accidently through ingesting seafood resembling prey and/or by consumption prey that previously ingested MPs themselves [36, 55]. In considering that human consume at least 100 fish species with plastic debris contamination, a big concern have raised [56]. Therefore, fish consumption in addition to the air, water and several other types of food represents a long-term exposure route to the human population. Fishes are known to be the most common model species used in MPs studies [57, 58] as well as bioindicators of contaminants in the marine environment [59] and biomonitors to evaluate the health of aquatic ecosystems [60]. Other species such as zebra fish and medaka have also been used in MPs exposure experiments with reported endpoints such as growth inhibition, mortality, and metabolism disorder [61]. It was suggested that the degree of MPs ingestion by fish depends on bioavailability and concentration of the pollutant in water, environmental factors, physiology of the organism, feeding behavior, and exposure time [59]. Importantly, more than 150 fish species in situ have been widely reported to ingest MPs in different amounts [61]. The primary uptake pathway of MPs in fish is widely considered to be ingestion. The ingested MPs are expected to be probably resided in the intestinal tract (gut), translocate to the edible tissues, and ultimately be eliminated [62]. The accumulation of MPs in different tissues of fish (e.g., muscle, gills, and liver) is not the same. Since the gut of fish is usually not consumed, the accumulation of MPs in this organ does not provide direct evidence for human exposure. In addition, uptake across the fish gill is less likely because the respiratory epithelium of the gill is tighter than that of mammalian lungs [61, 63]. However, the evidence of 1 µm latex spheres uptake in rainbow trout and presence in the surface and subsurface epidermal cells of the skin and in phagocytes underlying the gill surface [64] highlights the entry of MPs through fish epithelial cells while consumption of the gill or skin tissue could present another route of human exposure to MPs. Overall, dietary MPs exposure via fish may be possible after leaching and translocation across the gut or gill and enter the circulatory fluid. As fish considered hotspots of marine biota contamination by MPs and studies on MPs in fish species have increased along with time, a number of studies recently examined the contamination of commercial fish from sea and other origins by MPs are summarised in Table 1. The presence of MPs in muscle has been reported in previous case studies [59, 65]. The accordance of MPs up to 5 mm in the muscle of fish beside the accumulation of plastic film inside the liver was reported by them. Considering that muscle constitute the most edible part of fish specious and the great concern of potential risks to humans, estimating pollutants in fish muscle is important contrary to their lower accumulation potential than gill and liver [59]. Thus the accumulation of MPs in edible parts of marine organisms could become an issue of food safety [66]. However, there have been far fewer efforts in recent years conducted on MPs in muscle of commercial fish species compared with gut, liver, and gill.

Akhbarizadeh et al. assessed the concentration of MPs in muscles of four commercial fish species including Shrimp scad, Orange-spotted grouper, Pickhandle barracuda, and Bartail fathead categorized in both benthic and pelagic in the northeast of Persian Gulf [59]. The results showed MPs in all samples. A significant positive correlation (p<0.01) was also observed between MPs concentrations and length of fish. The highest MPs concentration was observed in Bartail fathead (Platycephalus indicus) with a mean of 18.50 ± 4.55 item/10 g of fish muscle. Overall, benthic fish had a higher MPs content in their muscles, supporting the hypothesis about the relationship between habitat of organisms and feeding behavior. Other factors such as local human activity, the levels of contamination, and the location were also thought to be important for accumulation of MPs in fish muscle. A large number of detected MPs were less than 300 mm colorful (black, transparent and blue, respectively).

They further investigated the risk/benefit of fish consumption in human. The amount of 300 and <100 g/week of fish meal consumption with no human health risk was considered for adults and children, respectively. As a result, the estimated mean intake of 555, 240, 233, and 169 items/300 g-week was calculated for MPs consumption from fish muscles associated to P. indicus, Epinephelus coioides, A. djedaba, and S. jello, respectively. Thus, a possible health threat to the consumers was warned following consumption of the studied fish at high doses.

Abbasi et al. perused the presence of MPs in the muscle of bartail flathead (P. indicus), greater lizardfish (Saurida tumbil), northern whiting (Sillago sihama), and tongue sole (Cynoglossus abbreviatus) as commercially important species [65]. Similar to the study of Akhbarizadeh et al. [59] the most abundant of MPs was detected in P. indicus. However, MPs concentrations (the number per individual) seemed to be higher in all species of demersal and pelagic fish. MP was mostly of fibrous and fragments of various size (<100 µm to >1,000 µm) and color. The presence of MPs in non-digestive organs represented the probable exposure route to humans after consuming contaminated seafood. Finding of distinct smooth fibrous fragments and particles with micrometers in diameter or less in non-digestive organs highlighted the possibility of passaging across the gill or gut epithelium via cell internalization and other translocation.

Karami et al. also reported that skin, gastrointestinal, and gills are the direct pathways for MPs to reach fish muscles [76]. They investigated the presence of MPs in edible flesh (whole fish, excluding the viscera and gills) and excised organs (viscera and gills) of four commonly consumed fish. The higher numbers of MPs were in skin, gills, and muscle than the liver and gut. However, larger MPs were generally in the gastrointestinal tract and gills compared to other organs. In addition, 36 out of 61 isolated particles in four of 30 consumed dried fish species were identified as plastic polymers. The annual ingestion of anthropogenic particles by the consumers was also estimated between 0 and 246 MPs per annum.

Akhbarizadeh et al. quantified the bioaccumulation, biomagnification, and potential human intake of MPs in muscles and gills of three popular and commercial fish species (E. coioides, P. indicus, and Liza klunzingeri) collected from northeast of Persian Gulf [66]. Of the total fish species, MPs were found in muscles of all. It was considered that benthic species and deposit feeders are more susceptible to intake plastic particles on seabed sediments. Indeed, the inactive and less motile fish among benthic species seem to be more vulnerable to pollutant accumulation. Among these, L. klunzingeri and E. coioides had the highest (mean 0.275 items/g muscle) and lowest (mean 0.158 items/g muscle) MPs level in their muscles, respectively. There was no significant correlation between body size and MPs detection in all specie. MPs were detected in a wide variety of shape (mostly fragments and fiber), color, and size (almost ˂50–8000 µm). Regarding higher amounts of MPs extracted from the gills compare to the muscle, showed that MPs were not biomagnified in muscle of the fish. The results of the biomagnification factor (BMF) and trophic magnification factor (TMF) confirmed they claim.

They further estimated the human intake of MPs after fish consumption. Considering 0.227 and 0.116 kg of fish meal size for adults and children, the estimated mean intake of MPs following consumption of fish species were 36, 41, and 61 items/227 g for adults and 18, 20, and 30 items/116 g for children, respectively. They finally highlighted the possible risks of chronic seafood consumption for human population especially pregnant/lactating women and their children that should be controlled.

Barboza et al. analysed three commercially important fish species, Dicentrachus labrax, Trachurus trachurus, and Scomber colias, from North East Atlantic Ocean regarding MPs [77]. From the 150 analysed fish (50 per species), 81 MPs were found in dorsal muscle of 48 fish (32%) with a total mean (±SD) of 0.054 ± 0.099 MP items/g. Detected MPs were in a wide variety of color (mostly blue and whitish), shape (mostly fragments and fiber), and size (fibers in the size range 151–1,500 µm and fragments lower than 100 µm). They reported that absorption and presence of the most part of the fragment MPs lower than 150 µm and thin fiber in dorsal muscle of fish resulted likely from uptake through skin, gills, and direct uptake from the abdominal cavity. They also reported that based on the EFSA recommendation for human weekly intake of fish (300 g of the analysed species per week) and estimated mean of MPs, human consumption of three fish analysed ranged from 112 MP items/year (1-year-old children) to 842 MP items/year (adults or the general population). This amount ranged from 518 to 3078 MP items/year/capita in selected European and American countries based on (EUMOFA, NOAA). Assuming dorsal muscle as the only consumed parts of the fish, 46% of the MPs could be absorbed by human consumers. They emphasized the urgent need for risk assessment, more research on the toxicity of MPs, and assumption of measures to minimize human exposure to MPs.

Daniel et al. studied the presence of MPs in the edible tissues (muscle and skin) of nine commercially important pelagic fish species from Cochin coast of Kerala, India [78]. A total of 270 fishes were analysed (n=30 per species) and only 7% of fishes had MPs in their edible tissues. The average abundance of MPs in these tissues was 0.07 ± 0.26 items/fish or 0.005 ± 0.02 items/g, which was not significantly different among the fish species. The detected MPs were in the various shapes, colors, and sizes. Two different morphotype were obtained including fragments as the most common morphotype (55.6%) followed by fibres (31.6%). Particles of five different colors were obtained from edible tissue. However, isolated transparent-white MPs were the most. Particles in the size class of 100–200 μm formed the major share in edible tissue with a range from 115 to 210 μm. No significant correlation between length of fish and size of particles and very weak correlation between length of fish and number of MPs was reported. An estimated 40–45 items/year of MPs for Indians reported by the author as a risk exposure when considering 8–9 kg of fish consumption per capita and the average quantity of MPs (0.005 ± 0.02 items/g) in pelagic fishes. However, 1 MP per 200 g of edible fish tissue in only 7% of the examined fishes assumed very low to create significant human health hazard.

Zitouni et al. reported the occurrence of small size MPs (≤3 µm) in the muscle of adult benthopelagic fish Serranus scriba (L.1758), from Tunisian coasts [79]. MPs were found in all samples (100%) with an average abundance of MPs varied from 1.78 ± 0.26 to 6.03 ± 0.47 items/g of fish tissue. The size of MPs ranged from 0.45 µm to <3 µm (∼60%) with the most particles in small size (<1.2–0.45 µm) found in the muscle of the sampled fish. Fragment was the most collected plastic shape detected in muscle samples. The size distribution of the MPs extracted from the muscle indicated that small-sized MPs are easily absorbed by organisms, trapped in the digestive tract, and then transported to different tissues via the circulatory system which highlighted the hypothesis of high transfer of MPs into the human diet.

Possible impacts of MPs to human health

Although there is a huge lack of knowledge about the accumulation and effects of consuming MPs in human bodies [84, 88], potential pathways have been suggested regarding harm effects [17, 38] (Figure 2). Moreover, MPs are biopersistent to chemical degradation and mechanical clearance when inhaled or ingested. Thus, they may becoming embedded or lodged [38]. MPs can cause harm to human body via both physical and chemical pathways. Once MPs are in the gut, they may be responsible for release of constituent monomers, additives and absorbed toxins, which cause negative biological responses such as oxidative stress, inflammation, cell apoptosis, tissue necrosis, localized cell and tissue damage, fibrosis, genotoxicity, and potentially carcinogenesis [38, 46, 89–92]. Mammalian system modeling shows that MPs have the capacity to penetrate the human body across living cells via cellular uptake to the lymphatic and circulatory system in the lungs or gut [38]. It has been assumed that uptake will depend on the surface functional groups, size, solubility, shape, and surface chemistry of MPs. Negative surface charge and smaller sizes are most likely to cause to cross the GIT and lung mucus gel layer and increased contact to the underlying epithelial cells [93, 94]. After contact the airway or gastrointestinal epithelium, MPs have several routes of absorption and translocation, such as persorption and endocytic pathways [38]. MPs on the scale of a few microns may be directly absorbed by cells in the lungs or gut after ingestion, while MPs up to 10 μm would be taken up by specialized cells possibly via Peyer’s patch in the intestine [95]. Particles larger than 130 μm can slowly penetrate tissue in the form of persorption and through paracellular transport [96]. In addition, MPs with certain characteristics would be able to translocate across living cells (e.g., M cells or dendritic cells), to the lymphatic and/or circulatory system [95, 97–99], cross the blood-brain barriers and the placenta, penetrate and accumulate in organs [23, 84, 97, 100], and impact the immune system and cell health. The severity of adverse effects depends on the exposure characteristics, nature of the toxic chemical and individual susceptibility. However, the physical effects of accumulated MPs is not yet fully understood which requires further investigation [38, 92]. In vitro testing shows a potential effects of MPs in cells on cell viability, pro-inflammatory responses, and gene expression [101]. Furthermore, in vivo testing on mice showed that ingestion of a low concentration of 5 μm of polystyrene MPs per day resulted to decreased sperm count as well as spermatogenic cells after 42 days [102]. Applied concentration was lower than the estimated amount for human ingestion (5 g of MPs per week) [103]. The presence of MPs in human faces reported by Wright and Kelly [38] and Smith et al. [104] indicated that human body’s excretory system can eliminate more than 90% of the ingested micro- and nanoplastics [38, 104]. In general, less than 10% of ingested particles can be absorbed and reach to the human bloodstream. Although the mechanism of elimination are not fully understood, factors such as the shape, size, polymer type, and additive chemicals of MPs ingested by humans can affect retention and clearance rates of them [100]. MPs and synthetic fibers released from daily objects and activities can also be inhaled, leading to an approximately exposure of 272 MPs/day [105]. Uptake of inhaled MPs and how deep in the lung they can deposit will depend on their size, shape, wettability, and density of particles. In high concentration, particles can cause a dust overload response that induce release of chemotactic factors and enhance vascular permeability, leading to chronic inflammation by prevention of macrophage migration [106]. In considering the pro-inflammatory property and high oxidant activity of MPs in lungs [107], high concentrations of airborne MPs can result in lung disease after chronic exposure, potentially leading to the enhancement of malignant lesions, similarly has been noticed in occupational exposure [17]. On the other hand, inhaled MPs on the airway may not be immersed in the respiratory system lining fluid because of their hydrophobicity, being subjected to mucociliary clearance and leading to exposure via the gut. Dermal exposure to MPs is also inevitable because of the widespread presence of MPs in the environment. Regarding the use of MPs in the composition of personal care products with directly contact to the skin, dermal exposure is a topic worth investigating [108]. It has been assumed that plastic particle <100 nm could cross the epithelial barrier, potentially [18]. After internalization, human epithelial cells will be suffered from cytotoxicity due to oxidative stress [46]. A combination of the available in vitro and in vivo toxicological data, regarding the mechanisms of toxicity related to MPs, concluded that formation of reactive oxygen species and consequent oxidative stress and inflammation are the significant toxicological threats to both animal and human health [109]. Plastic can be considered an inert material; however, within the body, MPs could cause harm through different pathways, such as colonization by microbes that serve as a harmful bacteria, resulting in direct toxicological, nutritional, immunological and developmental effects [104]. Sharma and Chatterjee also reported the possibility of human chromosomes alteration after MPs ingestion, resulting to obesity, infertility, and cancer [90]. Additionally, plastic particles adsorb and accumulate high levels of persistent organic pollutants (POPs), hydrophobic organic contaminants (HOCs), metals, non-metals, and additives/monomers and will raise concern that MPs can transfer hazardous chemical contaminants to marine animals consumed by humans, subsequently pose specific threats to juvenile animals and humans and affect their biological systems even at low doses [38, 92, 100, 104]. For example, Sb resealed from this vector can cause nausea, vomiting, and diarrhoea in humans [18]. Also, embolization of small vessels was observed in animals following long term oral administration PVC granules [110]. Given this fact, plastic debris are already considered vectors of many hazardous materials [111, 112], which cause a great concern regarding the possibility of MPs transferring from sea goods to humans through the food chain, resulting to the potential health risks to humans [113, 114]. Nevertheless, the actual risk to human is a subject of debate [22, 115, 116]. Hence, further scientific investigations estimating the exact human exposure to plastics through their diet and subsequently their toxicological effects seem to be necessary.

Figure 2:

Overview of potential routes of exposure to microplastics and toxicity impacts in the human body.

Risk management

Generally, risk management are fallen into two main categories include risk avoidance (RA) and risk reduction (RR). The RA is the prevention of any exposer risk that causes harm and damage, while RR deals with mitigating potential losses. Since, in the RA strategy the risk is completely avoided therefore RA is impossible due to the sources (tyres, synthetic textiles, marine coatings, road markings, personal care products, plastic pellets and city dust) and ways in which microplastics enter the environment [117]. On the other hand, due to modern lifestyle and inescapable role of plastic in human life, the eliminating is not probable. But, RR can be considered as the main way of risk management. Microplastics can pose a risk in different ways such as: physical (piercing, cutting and obstruction), chemical (as a vector for additives, pesticides, heavy metal) and biological (as a vector for pathogens). So, the cost-effective reduce-reuse-recycle (3Rs) strategies [118] with replacing could be main ways for RR. However, maintenance and keep water/wastewater treatment plants in line help to remove a lot of microplastics. For example, wastewater treatment plants are responsible for removing more than 90% of incoming microplastics. In recent years, “zeroplastic” strategies that proposed by NGOs can also be followed as a principal. Some other measurement that seriously affected on microplastic reduction are consist of; stop single-use plastic material, plant based/natural clothing, use emollient and filter in laundries and stop using cosmetics containing microplastic.

Conclusions

To date, several studies have evaluated the presence of MPs in marine, such as commercial fish, and their potential impacts on human health. However, few studies considered muscle of fish as a target tissue for the presence of MPs leading to direct human consumption with a potential health risk. To the best of our knowledge, this is the first review work regarding this subject by reviewing all articles estimated MPs analysis in muscle of fish. From the reviewing of published studies, MPs were found in the muscles of 26 fish species from 46 different species, spanning over seven countries. Thus, 56.5% of the commercial fish samples analysed contained MPs, with concentrations varied from 0.005 ± 0.02 in fish species from India to 6.03 ± 0.47 in fish species from Tanzania. Given the fact that fish is used in human food table across the word, its contamination by MP raises the concern about public health risk, particularly when consider the average consumption of MPs through other food products contaminated by these particles. Moreover, MPs may be as a carrier for other chemical contaminants from the environment and its habitants and transfer them to fish and to other abiotic and biotic products, subsequently pose specific risks to juvenile animals and humans. However, there is a little obvious evidence for direct health effects of MPs in human health, available observations suggested different harm effects such as inflammation, oxidative stress, genotoxicity, and carcinogenesis. Nonetheless, further studies are needed to fill knowledge gaps of all the potential impacts of MPs to human health with an effort to make plastic pollution a priority for both the scientific community and legislators worldwide.