Toxic effects on enzymatic activity, gene expression and histopathological biomarkers in organisms exposed to microplastics and nanoplastics: a review
Environmental Sciences Europe volume 34, Article number: 80 (2022)
Microplastics (MPs) and nanoplastics (NPs) have become an important global environmental issue due to their widespread contamination in the environment. This review summarizes existing literature on the effects of MPs/NPs on three important biomarkers including enzymatic activity, gene expression, and histopathology in various organisms from 2016 to 2021 and suggests a path forward for future research. Application of enzymatic activity, gene expression, and histopathology biomarkers are increasingly used in experimental toxicology studies of MPs/NPs because of their early signs of environmental stress to organisms. Between 2016 to 2021, 70% of published studies focused on aquatic organisms, compared to terrestrial organisms. Zebrafish were widely used as a model organism to study adverse impacts of MPs/NPs. Polystyrene (PS) were the most important polymer used in experimental toxicology studies of MPs/NPs. Fewer studies focused on the histopathological alterations compared to studies on enzymatic activity and gene expression of different organisms exposed to MPs/NPs. There is a growing need to better understand toxic effects of environmentally relevant concentrations of MPs/NPs on enzymatic activity, gene expression, and histopathology biomarkers of both aquatic and terrestrial organisms.
Plastic is one of the most widely used materials in modern society . However, current production and consumption is unsustainable . Plastics are widely used for a wide range of consumer products . Since the creation of the first commercial plastic polymers in the 1950s, an estimated 9.2 billion metric tons of plastic has been produced and more than 6.9 billion metric tons has ended up in landfills around the world, or worse, ‘leaking’ into the environment . In 2019, global plastic production reached 368 million metric tons , but is estimated to double within 20 years . Synthetic plastic production has increased by 8.3 billion metric tons since the 1950s, and is anticipated to reach 33 billion metric tons by 2050 . Asia is the largest manufacturer of plastic materials (51%,China: 31%, Japan: 3%, rest of Asia:18%, followed by Europe (16%, North American Free Trade Agreement (NAFTA: 19%, Middle East Africa (7% and Latin America (4% .
Plastics comprise different polymer types, such as polyethylene (PE), polystyrene (PS), polyvinylchloride (PVC), polyethylene terephthalate (PET), polyamide (PA), polypropylene (PP) and polyhydroxybutyrate (PHB), based on polymer structure and characteristics and have different applications . Over production and use of plastics, followed by waste mismanagement has resulted in increasing amounts of plastic waste leaking into the environment. Borrelle et al.  estimated that 19–23 million metric tons of plastic waste generated globally in 2016 entered aquatic ecosystems but is predicted to reach up to 53 million metric tons annually by 2030. Most consumer plastics are designed for single-use with limited recyclability (< 10%), and has resulted in increased global production and consumption leading to unprecedented plastic waste generation and widespread plastic pollution [13, 137]. In 2015, around 60–99 million metric tons of plastic waste globally were produced, and it is expected to reach 155–265 million metric tons by 2060 .
Plastic pollution caused by tiny plastic particles are classified according to their sizes. Microplastics (MPs) are particles < 5 mm , but even classified from 1 to 1000 μm , and nanoplastics (NPs) are particles < 1 µm or 1000 nm [5, 23, 38, 54, 75, 140]. Although a clear distinction between MP and NP size definitions have not been agreed upon , this review uses size definitions of < 5 mm and < 1 µm for MPs and NPs, respectively.
MPs/NPs are classified as primary or secondary based on their origin in the environment. Primary MPs/NPs are intentionally manufactured plastics in micro/nano-size ranges (e.g., microbeads) intended for industrial or commercial uses including hygiene and personal care products like scrubbers in cosmetics or clothing drilling fluids and paints that are easily discharged into the environment . Secondary MPs/NPs arise from physical, chemical, and biological degradation of larger plastics discarded in the environment. Sources of secondary MPs/NPs include water bottles, wastewater treatment plants, disposable packaging, and agricultural mulch film [39, 122].
Organisms that ingest MPs/NPs are exposed to a wide range of chemicals from various plastic additives added during production and other pollutants . Plastic additives are plasticizers (e.g., phthalates, bisphenol A) colorants, UV filters, flame retardants. Furthermore, persistent organic pollutants such as polychlorinated biphenyls (PCBs), organochlorine/organophosphorus pesticides, polycyclic aromatic hydrocarbons (PAHs) and metals can be adsorbed onto MP/NP surfaces in the aquatic environments [74, 135]. One recent study reported that combinations of MPs and chlorpyrifos reduced nutritional parameter concentrations in muscle of rainbow trout (Oncorhynchus mykiss) .
As of 2020 there have been 2500 studies on occurrence of MPs/NPs in the environment, sampling techniques, and impacts on organisms [5, 12]. Exposure of organisms to MPs/NPs produces physical and chemical toxic effects, including enzymatic activity, gene expression, and histopathological effects [1, 52, 58, 69]. Ingestion of MPs/NPs alters expression of immunity-related genes, genes associated with immune function and antioxidant enzyme [30, 109, 164]. Oxidative stress is an important response that induces following interaction between plastic and cellular environment . Reactive oxygen species (ROS) are generated by induction of oxidative stress, which is one of the most well-documented toxicity mechanisms of MP/NP polymers in organisms [109, 117]. Overproduction of ROS is damaging to gut homeostasis and increases lethality of immune regulatory catalase. Thus, antioxidant enzyme activity against ROS is critical . MPs alter digestive enzyme activities and energy acquisition in the marine bivalve (Mytilus galloprovincialis) .
Vertebrates including fish and mammals are considered suitable model organisms for the investigation of different types of pollution. The potential of various model organisms exposed to MP pollution is dependent on characteristics of individual species such as environmental stress tolerance, their ecological status, type of feeding, behavioral flexibility and life history strategies, and MPs properties such as their type, size and concentration. Zebrafish were one of the most studied groups of fish in toxicological studies [83, 101, 127, 162]. The main characteristics that render zebrafish interesting for toxicological studies are their small size, genetic similarities with humans, ease of breed, short life cycle and inexpensive maintenance. Mollusca and Crustacea are also known as suitable model organisms due to their feeding filtration type, omnipresence, their role in trophic systems, which are primarily primary consumers, and major contribution to human nutrition. According to review of previous studies, Molluscs and Crustaceans were marked as the most studied taxa among invertebrates .
Although there has been a dramatic increase in the number of studies on toxicological effects of MPs/NPs on organisms, there has been no comprehensive review of this literature. This comprehensive review examined and analyzed existing literature on enzymatic activity, gene expression, and histopathological effects on terrestrial and aquatic organisms exposed to individual MPs/NPs and their combination with other pollutants. Gaps identified in the literature based on this review will help inform recommendations for future research.
Research papers from January 2016 to November 2021 were searched from ScienceDirect, Google Scholar and Web of Science databases using the terms (“microplastic” OR “nanoplastic”) and (“enzyme activity” OR “gene expression” OR “histopathology”). The search returned 249 research papers on the effect of MPs/NPs on enzyme activity, gene expression and histopathology with different terrestrial and aquatic organisms used as experimental organisms (Additional file 1: Table S1). Studies on interactive effects of MPs/NPs and other contaminants were also included in this review.
All types of MPs/NPs (i.e., PA, PE, PP, PVC, PET, PHB and PS) particles of different sizes of nano and micro were included in this study. The PE family includes both high density PE (HDPE) and low-density PE (LDPE). Plastic particles of 1 μm to 5 mm were considered MPs, whereas particles of < 1 μm were considered NPs. MP size ranges were assigned according to de Sá et al.  into the following classes: < 50 μm (including NPs); 50–100 μm; 100–200 μm; 200–400 μm; 400–800 μm; 800–1600 μm; > 1600 μm; or not specified.
Studies were summarized according to the following criteria: species and common name of organisms, MPs type and size, contaminants absorbed to MPs, MPs and contaminant concentration, duration of the experiment, toxicological effect (enzyme activity, gene expression and histopathology) and organism tissues (Additional file 1: Table S1). Any article that included data from more than one of the above parameters resulted in the same number of studies as the number of elements per assumption. For example, if one article only reported on fish, it was regarded as one study; however, if it reported on both fish and Mollusca, it was regarded as two studies. Therefore, the number of studies examined in the results shows the number of interactions of the parameters (e.g., organism group, MP type, MP size), rather than the total number of publications. Figures were created using Microsoft Excel 2016.
Results and discussion
Reports of organisms exposed to MPs/NPs
MPs/NPs are easily ingested by aquatic and terrestrial organisms and transferred along the food chain [21, 65]. Contamination of MPs/NPs in terrestrial environments is considered potentially more hazardous compared to aquatic environments due to their direct impacts on food chains such as plants, insects, and animals that are directly consumed by humans . Previous reports suggest that soil is a major terrestrial sink of MPs/NPs . Thus, MP/NP pollution in terrestrial environments might be 4- to 23-fold greater than in oceans .
This review returned 249 research papers on the effects of MPs/NPs on enzyme activity, gene expression and histopathology of different organisms. Fish (38.15%), Mollusca (17.67%), crustacea (9.64%) and mammals (6.43%) were the most studied groups, whereas limited studies (< 1%) were conducted on amphibians and microbiota (Fig. 1). Most studies focused on aquatic organisms (~ 70%), compared to terrestrial organisms, presumably due to different methods and difficulties in maintaining and handling terrestrial organisms under controlled laboratory conditions. Zebrafish were increasingly used as a model organism (43.47%) among fish studies because of their small size, ease of rearing, short life cycle, genetic similarities with humans and cost-effective maintenance. Around 100–200 eggs are produced in a single spawning of zebrafish. In addition, larvae can survive for 7 days on yolk sac contents, providing a reliable and cost-effective method for investigating potentially toxic effects of environmental pollutants .
Control groups (negative and positive controls) in toxicological studies play an important role to compare pollutant effects on study organisms. The control group is free of carriers known as a negative control group. For example, in a study on MPs accumulation patterns and transfer of BaP to D. rerio, the positive control group of BaP (100 nM waterborne BaP) was analyzed separately against the negative control group to show detectable biomarker response in organisms.
In studies on effects of MPs/NPs on Molluscs, species such as Mytilus galloprovincialis [6, 37, 43, 114, 158, 169], Mytilus coruscus [44, 48, 139], Mytilus spp. [22, 113, 120, 131], and Mytilus edulis [104, 105], and clams such as Corbicula fluminea [45, 46, 90], Tegillarca granosa [150, 154, 189], Mactra veneriformis , and Ruditapes philippinarum [119, 143] are the most studied Mollusca. Previous studies have shown that mussels can easily ingest MPS/NPs via their effective water filtration capacity in natural  and laboratory conditions and are considered as reliable model organisms for experimental studies [2, 120, 169]. In addition, MPs/NPs are captured and aggregated in gills and digestive glands or adhere to other organs such as adductor muscles, foot and mantle of mussels that lead to harmful toxicological effects. For example, M. galloprovincialis exposed to 3 μm PS-MPs showed modulation of multixenobiotic resistance activity . Among studies on Mollusca organisms, only one other study has considered the impact of PET-MPs on snails (Achatina fulica), in which MPs induced significant villi damage in gastrointestinal walls of snails and reduced glutathione peroxidase and total antioxidant activity .
Most studies on effects of MPs/NPs from 2016 to 2021 on Crustacea occur in shrimp and Daphnia species which are considered model organisms for toxicological research. Studies on shrimp species include Litopenaeus vannamei [58, 163, 168], Penaeus monodon, Marsupenaeus japonicas , Artemia salina , Artemia franciscana [32, 47, 160], Macrobrachium nipponense , and Artemia parthenogenetica . Studies on Daphnia species include Daphnia magna [34, 62, 81, 102, 153, 180], Daphnia pulex [97, 98, 171, 182]. In a study by Liu et al. [96, 97], typical environmental NPs concentrations of 1 µg L−1 modulated response of antioxidant defenses, gene transcription, vitellogenin synthesis and development in Daphnia pulex.
Mice were the most widely studied mammal model organism in experimental studies on effect of MPs/NPs on enzyme activity, gene expression and histopathology [49, 147, 185, 186]. Some studies also used rats [7, 57, 61]. Most research on the biological toxicity of MPs/NPs have been conducted on marine and aquatic organisms (e.g., fish and invertebrates). However, few studies have been performed on the health effects of MPs/NPs on higher trophic level organisms such as mammals (including humans). In medical research, mice and rats are the most commonly studied mammalian model organisms. Jin et al.  showed 0.5 μm, 4 μm, and 10 μm PS-MPs cause testicular inflammation and the disruption of blood–testis barrier in mice.
Other groups of organisms including Annelida (4.47%), plants (4.88%), and nematodes (4.88%) were used in some studies on the effects of MPs/NPs on enzyme activity, gene expression and histopathology (Fig. 1). Annelida species such as Eisenia fetida [85, 88, 176], Tubifex , Lumbricus terrestris  and Eisenia andrei  were used in different experimental studies. Lettuce (Lactuca sativa) , Soybean (Glycine max L. Merrill) , Vallisneria natans , Sea cucumber (Apostichopus japonicus) , rice (Oryza sativa) [172, 181], maize , Utricularia vulgaris , Salvinia cucullate , Allium cepa , cucumber (Cucumis sativus) , Vicia faba , wheat (Triticum aestivum) , radish, wheat and corn  were various plants exposed to MPs/NPs.
MP/NP pollution has been recognized as worse in agroecosystems rather than other terrestrial ecosystems because of intensive agricultural activities such as wastewater irrigation, high use of plastic mulch and sewage sludge . MPs have been found in a wide range of agricultural soils around the world, with concentrations ranging from 10 to 12,560 MPs kg−1 [20, 42]. Furthermore, plant diversity is an important property of terrestrial environments, and over 300,000 species are the main food source for humans [35, 87]. Therefore, evaluating the ecotoxicology of MPs/NPs to food crops and other soil biota are an essential aspect of risk assessments due to their potentially adverse effects on crop yield and quality and trophic transfer to humans through the food chain. Most studies on the toxicity of MPs/NPs to plants were published in 2021, indicating that this is an emerging issue. However, the limited number of studies and uncertainty of results make it difficult to gain a better understanding of MP/NP effects of on terrestrial plant species and the underlying toxicity mechanisms.
Typical properties of a free-living nematode (Caenorhabditis elegans) include translucent body, tiny size, easy cultivation, and short generation cycle allows researchers to use nematodes as model organisms for toxicological studies . In addition, gene expression, enzymatic activities and histopathological effects have been widely used to evaluate toxic effect of MPs/NPs on nematodes [18, 19, 86, 128, 129, 141, 179]. The first study was reported in 2018, which assessed the toxicity of PA, PE, PP, PVC and PS MPs/NPs in C. elegans .
Few studies were found on MP/NP effects of on algae and limited studies reported on insect (2.44%), bacteria (2.03%), Echinodermata (1.63%), cnidaria (1.22%), and rotifer (1.22%). Various species of algae including Chlamydomonas reinhardtii [28, 77, 177], Euglena gracilis , Chlorella sp , Cladocopium goreaui , Karenia mikimotoi , Skeletonema costatum , Phaeodactylum tricornutum , and Chlorella vulgaris  are applied on experimental studies and enzymatic activities and gene expression are investigated. However, no studies have investigated histopathological effects of MPs/NPs on algae. Microalgae are common in all aquatic environments and occupy lower trophic levels . Microalgae have advantages in environmental purification (e.g., wastewater) and short growth cycles .
Studies have used insects including honeybees (Apis mellifera) [26, 164], Chironomus riparius [17, 110, 142], E. fetida as model organisms exposed to MPs/NPs, where enzymatic activities gene expression and histopathological effects were observed. Honeybees are important pollinators of crops, and their presence is critical for preservation of biodiversity within environments . In addition, honeybees are potential sentinel monitors for evaluating environmental pollution, because of their sensitivity they are affected by environmental contaminants (e.g., heavy metals) . Liebezeit and Liebezeit  indicated that honey was contaminated by MP fibers (40 µm to ~ 9 mm) and fragments (10–20 µm), which has garnered attention from scientists as well as media.
Microorganisms including heterotrophs, autotrophs, and symbiotic organisms are attached and grow on marine plastics, which may act as vectors . Many resistant bacteria have been detected on MPs in aquaculture environments. Arcobacter and Colwellia in seafloor sediment can colonize on LDPE . M. aeruginosa, a dominant species causes cyanobacterial blooms showed that the activity of superoxide dismutase (SOD) and catalase (CAT) were significantly affected with exposure to PVC, PS and PE MPs . Studies on the effects of MPs/NPs on bacteria began in 2020 and various effects of enzyme and gene expression were observed [80, 96, 103, 166, 188].
Recently, studies have reported hazards caused by MPs/NPs to Cnidaria (1.64%) such as Tubastrea aurea , Symbiodinium tridacnidorum, Cladocopium sp , and Pocillopora damicornis  and rotifer (1.23%) such as Brachionus koreanus [63, 64], and Brachionus rotundiformis . Corals showed stress response , or histopathological effect  when exposed to the MPs/NPs environment. Little information is available on the impact of MPs/NPs on rotifers and coral species in coral reef ecosystems and underpinning mechanism. Rotifers play key roles to transfer material and energy into aquatic food chains. Also, they are reliable model organisms for MP/NP ecotoxicology studies due to their tiny size, short life cycle, genetic homogeneity, easy maintenance in laboratory, high fertility, and filter feeding behavior .
Only single studies have been conducted on Echinodermata , amphibians , and microbiota  organism groups. Sea urchins (Sterechinus neumayeri) are the most common echinoid in Antarctic shallow waters and play an important trophic role as predators and grazers. The widespread distribution of S. neumayeri across the Southern Ocean, as well as its high trophic flexibility, suggest that this organism could be exposed to MPs/NPs pollution, which could easily be taken up by S. neumayeri individuals and cells . Given the worldwide decline in amphibian species, the threat of MPs/NPs to these organisms remains largely unknown . MPs were reported in the gastrointestinal tract of several anuran species (e.g., Pelophylax nigromaculatus, Rana limnochari, Microhyla ornata, and Bufo gargarizans), demonstrating that amphibians can ingest MPs . Tadpoles (Physalaemus cuvieri) subjected to PE MPs showed locomotor changes, anxiety-like behaviors, as well as anti-predatory defensive response deficit after exposing to predators. Recently, Lajmanovich et al.  indicated that PE MPs (40–48 μm) significantly affected in enzymatic activities of S. squalirostris. No studies have investigated MPs/NPs impacts on gene expression and histopathology of tadpoles. Therefore, we proposed researchers to draw studies on the effects of MPs/NPs on these biochemical parameters. MPs have a significant impact on sedimentary microbial ecosystems . Thus, investigating the influence mechanisms of MPs/NPs on estuarine microbiota is important to improve our understanding the ecological risk of MP/NP pollution in estuarine environments and on marine microbial communities.
MP/NP polymer types
MP/NP polymer types commonly reported include PS (58.48%) and PE (15.92%), followed by PVC (7.27%), PET (3.81%), PP (3.11%), LDPE (3.11%), HDPE (3.11%), PA (1.73%), PHB (0.35%) (Fig. 2), and not specified (3.11%). PS was the most common MP/NP type and was reported in 169 studies. PS and PE polymers are known as one of the most widely used plastics and synthesized for a broad spectrum of applications, including food packaging, personal care products, building insulation. PP and PVC are also widely synthesized for using in different applications . For example, PP is used in food packaging, sweet and snack wrappers, hinged caps, automotive parts, and PVC is used in window frames, profiles, floor and wall covering, and pipes . In 2012, ~ 32.7 million metric tons of PS plastics was generated globally . In Europe, PE comprised 25.31%, PP 19.4%, PVC 10%, and PS 6.2% of total production . MPs/NPs polymers with a wide range of densities could also affect MPs/NPs behavior in the marine environment.
Styrene monomers in PS polymers is a carcinogen in nature and may pose a severe damage to the aquatic organism . According to previous studies in the marine environment, PS, PE, PP, PVC, and PA are a frequently detected form of MPs NPs in the marine and terrestrial environment [12, 31, 83, 149]. PS is lightweight, and therefore it is easily mobile and therefore spreads across in the marine environment. PE and PET have lower and higher densities than water, respectively, that lead to the distribution of these MPs between different compartments . Some studies provided important information for the ecological risk assessment of PP and PVC MPs/NPs in different organisms [16, 25, 85].
Although benthic aquatic organisms are likely to encounter denser polymers, such as PET and PVC, it is primarily dense microfibres that have been documented in benthic invertebrates [29, 125]. In aquatic environments, microbial communities (the plastisphere) can attach to and form a biofilm around MPs . MP ingestion is another mechanism that can alter transport of MPs in the water column. MP ingestion can impact transport of MPs via vertical migration and long-range transport, and the buoyancy of particles can be altered through encapsulation in fecal pellets . Sediments and soils can act as an important sink for MPs following weathering and transformation in the environment. Undisturbed sediments may even provide a useful temporal MP pollution archive . This study showed that despite the wide distribution of PP and PVC in the marine environment, studies on their toxicological effects including enzymatic activity, gene expression, and histopathological effect on various organisms are limited. Given the particulate nature (nano/micro) of PP and PVC, it is crucial to investigate their hazardous effects in organisms. However, more studies are necessary to investigate the impacts of MPs/NPs on enzymatic activity, gene expression, and histopathology on different organisms.
Reports published by PlasticsEurope,  showed around 7.9% polyurethane (PUR) was applied in building insulation, pillows and mattresses, insulating foams for fridges. However, studies on the toxicological effects of PUR on different organisms are scarce. For example, combined effects of PUR foam MPs and polybrominated diphenyl-ether (PBDE) on the E. fetida, which showed accumulation of chemicals derived from MPs to E. fetida . However, we have not found studies on the risk toxicological effects of PUR MPs/NPs on enzymatic activity, gene expression, and histopathology of different organisms. Therefore, more studies are required to providing information for future investigation addressing the effects of PUR MPs/NPs on various terrestrial and marine organisms. MPs/NPs can enter humans via food webs and pose potential health threats [15, 82]. It is estimated that 52,000 MP particles enter the human body per year through diet and an additional 69,000 MPs from inhalation . Thus, the lungs and digestive systems are the first places of contact for MPs/NPs, and MPs/NPs penetrate these barriers before inducing of toxicities . Direct contact of MPs/NPs and various cell types showed subsequent cellular toxicity, which depends on cell types and MPs/NPs physicochemical features. Thus, studies on the toxicological effects of MPs/NPs on human cells are required.
Different shapes of MPs including fragments, pellets, fibers, foam, films are found in aquatic ecosystems, which had different capacities for adsorbing pollutants, which had an impact on different biomarker responses. The MP fragments had various surface features, such as sharp edges with fractures and degraded rough surfaces, demonstrating their potential for internal abrasion, and may show morphological effects on fish gills. Sharp edges of PS MPs increase physical microinjuries of O. mykiss on the gill, gut, and skin . Further studies are required to compare the toxicological effects of MPs shape on different tissues of living organisms.
Toxicological effects of MPs/NPs (enzymatic activity, gene expression, and histopathological effect)
Studies on the effects of MPs/NPs on enzymatic activity, gene expression, and histopathological effect of various organisms increased in 2020 and 2021 (Fig. 3). Studies on the effects of MPs/NPs on enzymatic activity (60 studies in 2020 and 53 studies in 2021) were higher than enzymatic activity (41 studies in 2020 and 44 studies in 2021) and histopathological effect (19 studies in 2020 and 41 studies in 2021) of organisms increased in 2020 and 2021.
Biomarkers are increasingly used as worldwide-recognized tools to evaluate the possible biological effects in organisms exposed to environmental contaminants. Biomarkers are also incorporated in environmental quality and environmental monitoring programs . Biomarkers usually occur at the subcellular level of biological organization, and these subcellular responses to environmental stressors could appear before other impacts, such as disease, mortality, or population alteration . The use of enzymatic activity, gene expression, and histopathological biomarkers in toxicology is becoming increasingly important for pollution assessments [17, 58, 94, 115].
This approach is also useful for determining the mechanisms by which environmental stressors induce complex molecular and cellular changes, as well as their interdependence. Among many suggested ecotoxicological biomarkers in the last decade, those biomarkers that show the imbalance between pro-oxidant and antioxidant status and lead to adverse effects such as DNA damage, gene expression, lipid peroxidation and enzyme inhibition as an earlier sign of environmental disturbance [10, 99]. Biomarkers of oxidative stress include alterations in antioxidant defenses and oxidative damage . Genotoxic pollutants alter the genetic material of marine organisms, causing DNA damage, genes and chromosomal changes. Assessment and validation of biological markers in sentinel species for biomarker application in environmental monitoring programs is critical under various field conditions. DNA damage and changes in the expression of a gene encoding DNA repair mechanism prepare an important role for measuring the impact of MPs/NPs on organisms .
Histopathology is a sensitive biomarker of xenobiotic-induced sublethal stress. In both laboratory studies, histopathological changes have been widely used as biomarkers in the evaluation of the health of fish exposed to contaminants . Histopathological evaluation is widely considered as a potential tool for determining the extent of injury in organisms caused by acute and chronic effects of environmental stressors . Histopathological changes of specific organs show condition and time-integrated endogenous and exogenous effects on the organism resulting from changes at lower levels of biological organization . This study showed that studies on the effects of MPs/NPs on organisms are lower that studies on gene expression and enzymatic activity. Solvents used in histopathological protocols may solve MPs/NPs and effects on results. Considering the importance of histopathological alterations as a valuable biomarker of environmental stressors, more studies are required on the impacts of MPs/NPs on histopathological changes of various organisms.
Some biomarker responses including enzyme activity, gene expression, and histopathological damages are highlighted in Additional file 1: Table S1. Superoxide dismutases (SOD), Catalase (CAT), glutathione peroxidase (GPx), acetylcholinesterase (AChE), glutathione s transferase (GSH), peroxidase (POD), and Cytochrome P450 are commonly analyzed enzymes in toxicological studies. Deregulatory effects of MPs/NPs on hepatic genes, immune genes, stress response and detoxification genes, estrogenic (vtg1) or organic (cyp1a), genes encoding proteins have been reported in different organisms as well. According to analyzed tissues for histopathological damages in studies inflammation, necrosis, hyperplasia, villi damage, epithelial damage, and MPS/NPs accumulation are reported. Studies showed different size of MPs/NPs, polymer types, and shapes have different response on organisms.
Impact of different plastic sizes
The number of studies related to the effects of individual MPs and both MPs/NPs on enzymatic activity, gene expression, and histopathological biomarkers in different organisms has increased from just three studies in 2016 to 56 studies in 2021 (Fig. 4a). Around 59.04% and 11.75% of publications used plastic particles sizes of < 50 µm and 50–100 µm, respectively (Fig. 4b). Few studies (0.60%) used MPs > 1600 µm.
MP/NP particle size plays an important role in the changes of biomarkers including enzymatic activity, gene expression, and histopathology in exposed organisms [1, 33, 51]. Size-dependent accumulation of MPs/NPs has proven that smaller plastic particles could reach specific tissues such as gut, liver and larger plastic particles were only trapped in gills and the digestive tract of fish . The small size of MPs/NPs facilitates internalization by organisms and, thus, consequent accumulation in the food chain. Trophic transfer of MPs/NPs along the aquatic food chain and implications for human health are important.
Inflammation caused by 0.5 µm PS MPs in zebrafish gut were found to be more severe than that caused by 50 µm PS MPs . The size-dependent toxicity of MPs/NPs has been widely reported in sea organisms. A study conducted by Kinjo et al.  showed that larger MPs of PS retained in the digestive tract of M. galloprovincialis are longer than smaller particles. In another study, histological changes were observed in the liver, intestine, and gill of goldfish (Carassius auratus) exposed to PS MPs and severe changes showed a size-dependent pattern of PS MPs .
Until recently, there were few studies on the transfer of MPs/NPs to humans and the potential health consequences. Since humans are the final consumers in the food web, introduction of MPs/NPs into humans is possible, due to consumption of aquatic products that contain MPs/NPs. PS NPs enter in human gastric adenocarcinoma cells through an energy-dependent mechanism. In addition, size and dose are the factors that affect the internalization of NPs in cells. Smaller NPs also significantly change expression of genes involved in inflammation . Similarly, He et al.  showed PS NPs with size of 50 nm can be rapidly internalized by human hepatocellular carcinoma (HepG2) cells. As a result, size-dependent toxicity should be considered when assessing the toxicity of MPs/NPs in various organisms.
MPs/NPs as carriers for other contaminants
Around 90 studies were conducted to investigate combined effects of contaminants and MPs/NPs on enzymatic activity, gene expression, and histopathological biomarkers in different organisms (Fig. 5). Most studies used chemical elements, PAH, PCB, pesticides, medication, hormone, triclosan, sewage, and antibiotic as contaminants combined with MPs/NPs. Studies on combined effects of chemical elements, PAH, and pesticides with MPs/NPs are higher than other contaminants (Fig. 5). For example, only a single study has been conducted on sewage and hormones (cite it here).
Environmental MPs/NPs can be regarded as a complex cocktail of contaminants. Plastic-combined with environmental chemicals are readily released in the gut of animals and may subsequently transfer along the aquatic food chain. Interaction of MPs/NPs with other contaminants could affect its uptake by organisms and their combined toxicity. Physico-chemical properties of water are regarded to change the biomarker response of organisms. Thus, the assessment of water quality of exposed water to MPs/NPs is suggested. Many parameters including weathering, salinity, pH, and dissolve organic matter influence the durability and affect interaction of MPs/NPs with other contaminants . For example, higher histopathological damages in combined PS MPs and chlorpyrifos showed were observed in O. mykiss, which show increase adverse effects of chlorpyrifos in fish . In another study, induction of cytochrome P450 1A (cyp1a) was indicated when D. rerio were fed artemia incubated with a combined of MPs and benzo[a]pyrene (BaP) . PE MPs grow cadmium uptake in lettuce by changing the soil microenvironment .
MPs/NPs are hydrophobic in nature and have a large surface area that allows adsorption of heavy metals on its surface, and play a role to accumulate the pollutants in the body. Several factors influence MPs behaviors, the amount of MPs deposited, retained, and transported, including human activity (e.g., inappropriate waste management), MPs characteristics (e.g., density, shape and size), environmental topography and condition. Size of MPs/NPs, their surface ionic charges, and age of particle affect adsorption capacity of metals. Studies have shown that MPs increase the accumulation and toxicity of cadmium and copper in liver, gut, gills of adult D. rerio [100, 126]. Few studies also reported reduced bioavailability and toxicity of MPs/NPs combined with contaminants such as phenanthrene, and PAH [144, 159]. The binding affinity of MPs/NPs with other contaminants also has a significant effect on their bioavailability.
Due to the growing issue of plastic and MPs/NPs pollution, it is becoming critical to solve, and better understand the fate and toxicity of these particles in the environment. In recent years, there has been a dramatic increase in MPs/NPs studies. While most studies have focused on reporting presence of MPs/NPs in the environment and biota, few studies have examined their impacts on biomarkers of organisms including enzymatic activity, gene expression, and histopathology. Early exposure studies used very high concentrations of virgin MPs/NPs in laboratory-controlled experiments that were not considered environmentally relevant, resulting in a shift in recent years to environmentally relevant MPs/NPs concentrations [5, 14, 76, 151, 156]. In the natural environment, MPs/NPs occur in different size combinations and concentrations. Thus, more studies, based on these environmentally relevant parameters, are required to better understand their impacts on enzymatic activity, gene expression, and histopathology biomarkers on organisms. In response, recent research has begun to shift from individual species to focus on multiple species, multi-generational studies [5, 18, 63, 178] (Haegerbaeumer et al. 2019).
The density of MPs/NPs polymers is also an important factor for their distribution in water, which affects their interaction with aquatic organisms. For example, PP and PE pose greater risks for organisms that live near the surface because they float in water, whereas PS, PVC, and PET may impact benthic organisms more, because they sink. In the natural environment, plastics are exposed to degradation via weathering, whereas virgin MPs/NPs are used in most laboratory studies, which affect sorption of other contaminants, aggregations, and even organism toxicity. Both long-term and short-term studies using virgin and weathered MPs/NPs will be required to better understand impacts of weathered and degraded plastics in the environment. Recovery periods of MPs/NPs in laboratory studies should also be examined for future studies.
MPs/NPs contamination in the environment and in biota has been widely recognized as a rapidly emerging pollution problem. This review focussed on 256 studies on the effects of MPs/NPs on enzymatic activity, gene expression, and histopathology biomarkers on organisms from 2016 to 2021. While studies on MPs/NPs toxicity in biota have also increased dramatically to better understand these emerging contaminants, this review found that most studies (~ 70%) have focused on aquatic organisms, and of these, only a few species have been studied. Although impacts of MPs/NPs of biomarkers on terrestrial organisms are less well studied, some researchers consider impacts of MPs/NPs on terrestrial ecosystems may be more harmful to humans due to reliance on agricultural systems for food. Therefore, this was identified as a major knowledge gap that requires further study. Other important knowledge gaps that need to be addressed are that most laboratory toxicology studies use limited size ranges, single polymer categories and virgin MPs/NPs concentrations which are much higher than found in the environment. Thus, measured impacts of enzymatic activity, gene expression, and histopathology biomarkers on organisms are often not environmentally relevant. MPs/NPs occur in different size combinations and concentrations in the natural environment. Thus more studies, based on these environmentally relevant parameters, are required to better understand toxic effects of MPs/NPs on enzymatic activity, gene expression, and histopathology biomarkers of both aquatic and terrestrial organisms.
Availability of data and materials
All data are publicly available, with sources described in the manuscript and supplementary material.
Abarghouei S, Hedayati A, Raeisi M, Hadavand BS, Rezaei H, Abed-Elmdoust A (2021) Size-dependent effects of microplastic on uptake, immune system, related gene expression and histopathology of goldfish (Carassius auratus). Chemosphere 276:129977. https://doi.org/10.1016/J.CHEMOSPHERE.2021.129977
Abdelsaleheen O, AbdolahpurMonikh F, Keski-Saari S, Akkanen J, Taskinen J, Kortet R (2021) The joint adverse effects of aged nanoscale plastic debris and their co-occurring benzo[α]pyrene in freshwater mussel (Anodonta anatina). Sci Total Environ 798:149196. https://doi.org/10.1016/J.SCITOTENV.2021.149196
Adams SM, Giesy JP, Tremblay LA, Eason CT (2001) The use of biomarkers in ecological risk assessment: recommendations from the Christchurch conference on biomarkers in ecotoxicology. Biomarkers 6:1–6. https://doi.org/10.1080/135475001452724
Ajith N, Arumugam S, Parthasarathy S, Manupoori S, Janakiraman S (2020) Global distribution of microplastics and its impact on marine environment—a review. Environ Sci Pollut Res 2020(27):25970–25986. https://doi.org/10.1007/S11356-020-09015-5
Allen S, Allen D, Karbalaei S, Maselli V, Walker TR (2022) Micro(nano)plastics sources, fate, and effects: What we know after ten years of research. J Hazard Mater Adv 6:100057. https://doi.org/10.1016/J.HAZADV.2022.100057
Alnajar N, Jha AN, Turner A (2021) Impacts of microplastic fibres on the marine mussel, Mytilus galloprovinciallis. Chemosphere 262:128290. https://doi.org/10.1016/J.CHEMOSPHERE.2020.128290
Amereh F, Babaei M, Eslami A, Fazelipour S, Rafiee M (2020) The emerging risk of exposure to nano(micro)plastics on endocrine disturbance and reproductive toxicity: from a hypothetical scenario to a global public health challenge. Environ Pollut 261:114158. https://doi.org/10.1016/J.ENVPOL.2020.114158
Badiou-Bénéteau A, Benneveau A, Géret F, Delatte H, Becker N, Brunet JL, Reynaud B, Belzunces LP (2013) Honeybee biomarkers as promising tools to monitor environmental quality. Environ Int 60:31–41. https://doi.org/10.1016/J.ENVINT.2013.07.002
Batel A, Linti F, Scherer M, Erdinger L, Braunbeck T (2016) Transfer of benzo [a] pyrene from microplastics to Artemia nauplii and further to zebrafish via a trophic food web experiment: CYP1A induction and visual tracking of persistent organic pollutants. Environ Toxicol Chem 35:1656–1666
Ben Ameur W, de Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64:241–251. https://doi.org/10.1016/J.MARPOLBUL.2011.11.026
Bergami E, KrupinskiEmerenciano A, González-Aravena M, Cárdenas CA, Hernández P, Silva JRMC, Corsi I (2019) Polystyrene nanoparticles affect the innate immune system of the Antarctic sea urchin Sterechinus neumayeri. Polar Biol 2019(42):743–757. https://doi.org/10.1007/S00300-019-02468-6
Bhagat J, Zang L, Nishimura N, Shimada Y (2020) Zebrafish: an emerging model to study microplastic and nanoplastic toxicity. Sci Total Environ 728:138707. https://doi.org/10.1016/J.SCITOTENV.2020.138707
Borrelle SB, Ringma J, Lavender Law K, Monnahan CC, Lebreton L, McGivern A, Murphy E, Jambeck J, Leonard GH, Hilleary MA, Eriksen M, Possingham HP, De Frond H, Gerber LR, Polidoro B, Tahir A, Bernard M, Mallos N, Barnes M, Rochman CM (2020) Predicted growth in plastic waste exceeds efforts to mitigate plastic pollution. Science (80-) 369:1515–1518. https://doi.org/10.1126/SCIENCE.ABA3656/SUPPL_FILE/ABA3656-BORRELLE-SM-DATA-S4.CSV
Bour A, Avio CG, Gorbi S, Regoli F, Hylland K (2018) Presence of microplastics in benthic and epibenthic organisms: Influence of habitat, feeding mode and trophic level. Environ Pollut 243:1217–1225. https://doi.org/10.1016/J.ENVPOL.2018.09.115
Bouwmeester H, Hollman PCH, Peters RJB (2015) Potential health impact of environmentally released micro- and nanoplastics in the human food production chain: experiences from nanotoxicology. Environ Sci Technol 49:8932–8947. https://doi.org/10.1021/ACS.EST.5B01090/ASSET/IMAGES/MEDIUM/ES-2015-01090H_0005.GIF
Boyle D, Catarino A, Clark N, Henry TB (2020) Polyvinyl chloride (PVC) plastic fragments release Pb additives that are bioavailable in zebrafish. Environ Pollut 263:114422
Carrasco-Navarro V, Muñiz-González AB, Sorvari J, Martínez-Guitarte JL (2021) Altered gene expression in Chironomus riparius (insecta) in response to tire rubber and polystyrene microplastics. Environ Pollut 285:117462. https://doi.org/10.1016/J.ENVPOL.2021.117462
Chen H, Hua X, Li H, Wang C, Dang Y, Ding P, Yu Y (2021a) Transgenerational neurotoxicity of polystyrene microplastics induced by oxidative stress in Caenorhabditis elegans. Chemosphere 272:129642. https://doi.org/10.1016/J.CHEMOSPHERE.2021.129642
Chen H, Hua X, Yang Y, Wang C, Jin L, Dong C, Chang Z, Ding P, Xiang M, Li H, Yu Y (2021b) Chronic exposure to UV-aged microplastics induces neurotoxicity by affecting dopamine, glutamate, and serotonin neurotransmission in Caenorhabditis elegans. J Hazard Mater 419:126482. https://doi.org/10.1016/J.JHAZMAT.2021.126482
Chen Y, Leng Y, Liu X, Wang J (2020) Microplastic pollution in vegetable farmlands of suburb Wuhan, central China. Environ Pollut 257:113449. https://doi.org/10.1016/J.ENVPOL.2019.113449
Cheng Y, Zhu L, Song W, Jiang C, Li B, Du Z, Wang J, Wang J, Li D, Zhang K (2020) Combined effects of mulch film-derived microplastics and atrazine on oxidative stress and gene expression in earthworm (Eisenia fetida). Sci Total Environ 746:141280. https://doi.org/10.1016/J.SCITOTENV.2020.141280
Cole M, Liddle C, Consolandi G, Drago C, Hird C, Lindeque PK, Galloway TS (2020) Microplastics, microfibres and nanoplastics cause variable sub-lethal responses in mussels (Mytilus spp.). Mar Pollut Bull 160:111552. https://doi.org/10.1016/J.MARPOLBUL.2020.111552
Cowger W, Booth AM, Hamilton BM, Thaysez C, Primpke S, Munno K, Lusher AL, Dehaut A, Vaz VP, Liboiron M, Devriese LI, Hermabessiere L, Rochman C, Athey SN, Lynch JM, Frond H De, Gray A, Jones OAH, Brander S, Steele C, Moore S, Sanchez A, Nel H (2020) Reporting Guidelines to Increase the Reproducibility and Comparability of Research on Microplastics. Appl. Spectrosc. vol. 74, Issue 9, pp 1066-1077 74, 1066–1077. https://doi.org/10.1364/AS.74.001066.
Cox KD, Covernton GA, Davies HL, Dower JF, Juanes F, Dudas SE (2019) Human consumption of microplastics. Environ Sci Technol 53:7068–7074. https://doi.org/10.1021/ACS.EST.9B01517/ASSET/IMAGES/MEDIUM/ES-2019-015177_0005.GIF
de Sá LC, Oliveira M, Ribeiro F, Rocha TL, Futter MN (2018) Studies of the effects of microplastics on aquatic organisms: what do we know and where should we focus our efforts in the future? Sci Total Environ 645:1029–1039. https://doi.org/10.1016/J.SCITOTENV.2018.07.207
Deng Y, Jiang X, Zhao H, Yang S, Gao J, Wu Y, Diao Q, Hou C (2021) Microplastic polystyrene ingestion promotes the susceptibility of honeybee to viral infection. Environ Sci Technol 55:11680–11692. https://doi.org/10.1021/ACS.EST.1C01619/SUPPL_FILE/ES1C01619_SI_003.MP4
Déniel M, Errien N, Daniel P, Caruso A, Lagarde F (2019) Current methods to monitor microalgae–nanoparticle interaction and associated effects. Aquat Toxicol 217:105311. https://doi.org/10.1016/J.AQUATOX.2019.105311
Déniel M, Errien N, Lagarde F, Zanella M, Caruso A (2020) Interactions between polystyrene nanoparticles and Chlamydomonas reinhardtii monitored by infrared spectroscopy combined with molecular biology. Environ Pollut 266:115227. https://doi.org/10.1016/J.ENVPOL.2020.115227
Du S, Zhu R, Cai Y, Xu N, Yap PS, Zhang Y, He Y, Zhang Y (2021) Environmental fate and impacts of microplastics in aquatic ecosystems: a review. RSC Adv 11:15762–15784. https://doi.org/10.1039/D1RA00880C
Elizalde-Velázquez A, Crago J, Zhao X, Green MJ, Cañas-Carrell JE (2020) In vivo effects on the immune function of fathead minnow (Pimephales promelas) following ingestion and intraperitoneal injection of polystyrene nanoplastics. Sci Total Environ 735:139461. https://doi.org/10.1016/J.SCITOTENV.2020.139461
Enders K, Lenz R, Stedmon CA, Nielsen TG (2015) Abundance, size and polymer composition of marine microplastics ≥ 10 μm in the Atlantic Ocean and their modelled vertical distribution. Mar Pollut Bull 100:70–81. https://doi.org/10.1016/J.MARPOLBUL.2015.09.027
Eom HJ, Nam SE, Rhee JS (2020) Polystyrene microplastics induce mortality through acute cell stress and inhibition of cholinergic activity in a brine shrimp. Mol Cell Toxicol 2020(16):233–243. https://doi.org/10.1007/S13273-020-00088-4
Espinosa C, Esteban MÁ, Cuesta A (2019) Dietary administration of PVC and PE microplastics produces histological damage, oxidative stress and immunoregulation in European sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol 95:574–583. https://doi.org/10.1016/j.fsi.2019.10.072
Fadare OO, Wan B, Guo LH, Xin Y, Qin W, Yang Y (2019) Humic acid alleviates the toxicity of polystyrene nanoplastic particles to Daphnia magna. Environ Sci Nano 6:1466–1477. https://doi.org/10.1039/C8EN01457D
FAO. Global Plan of Action for the Conservation and Sustainable Utilisation of Plant Genetic Resources for Food and Agriculture. 1996; Leipzig, Germany.
Forte M, Iachetta G, Tussellino M, Carotenuto R, Prisco M, De Falco M, Laforgia V, Valiante S (2016) Polystyrene nanoparticles internalization in human gastric adenocarcinoma cells. Toxicol Vitr 31:126–136. https://doi.org/10.1016/J.TIV.2015.11.006
Franzellitti S, Capolupo M, Wathsala RHGR, Valbonesi P, Fabbri E (2019) The Multixenobiotic resistance system as a possible protective response triggered by microplastic ingestion in Mediterranean mussels (Mytilus galloprovincialis): larvae and adult stages. Comp Biochem Physiol Part C Toxicol Pharmacol 219:50–58. https://doi.org/10.1016/J.CBPC.2019.02.005
Frias JPGL, Nash R (2019) Microplastics: Finding a consensus on the definition. Mar Pollut Bull 138:145–147. https://doi.org/10.1016/J.MARPOLBUL.2018.11.022
Galafassi S, Nizzetto L, Volta P (2019) Plastic sources: a survey across scientific and grey literature for their inventory and relative contribution to microplastics pollution in natural environments, with an emphasis on surface water. Sci Total Environ 693:133499. https://doi.org/10.1016/J.SCITOTENV.2019.07.305
Gaylor MO, Harvey E, Hale RC (2013) Polybrominated diphenyl ether (PBDE) accumulation by earthworms (Eisenia fetida) exposed to biosolids-, polyurethane foam microparticle-, and penta-BDE-amended soils. Environ Sci Technol 47:13831–13839. https://doi.org/10.1021/ES403750A/SUPPL_FILE/ES403750A_SI_001.PDF
Geyer R, Jambeck JR, Law KL (2017) Production, use, and fate of all plastics ever made. Sci Adv 3:e1700782
Gong W, Zhang W, Jiang M, Li S, Liang G, Bu Q, Xu L, Zhu H, Lu A (2021) Species-dependent response of food crops to polystyrene nanoplastics and microplastics. Sci Total Environ 796:148750. https://doi.org/10.1016/J.SCITOTENV.2021.148750
González-Soto N, Hatfield J, Katsumiti A, Duroudier N, Lacave JM, Bilbao E, Orbea A, Navarro E, Cajaraville MP (2019) Impacts of dietary exposure to different sized polystyrene microplastics alone and with sorbed benzo[a]pyrene on biomarkers and whole organism responses in mussels Mytilus galloprovincialis. Sci Total Environ 684:548–566. https://doi.org/10.1016/J.SCITOTENV.2019.05.161
Gu H, Wei S, Hu M, Wei H, Wang X, Shang Y, Li L, Shi H, Wang Y (2020) Microplastics aggravate the adverse effects of BDE-47 on physiological and defense performance in mussels. J Hazard Mater 398:122909. https://doi.org/10.1016/J.JHAZMAT.2020.122909
Guilhermino L, Vieira LR, Ribeiro D, Tavares AS, Cardoso V, Alves A, Almeida JM (2018) Uptake and effects of the antimicrobial florfenicol, microplastics and their mixtures on freshwater exotic invasive bivalve Corbicula fluminea. Sci Total Environ 622–623:1131–1142. https://doi.org/10.1016/J.SCITOTENV.2017.12.020
Guo X, Cai Y, Ma C, Han L, Yang Z (2021) Combined toxicity of micro/nano scale polystyrene plastics and ciprofloxacin to Corbicula fluminea in freshwater sediments. Sci Total Environ 789:147887. https://doi.org/10.1016/J.SCITOTENV.2021.147887
Han X, Zheng Y, Dai C, Duan H, Gao M, Ali MR, Sui L (2020) Effect of polystyrene microplastics and temperature on growth, intestinal histology and immune responses of brine shrimp Artemia franciscana. J Oceanol Limnol 2020(39):979–988. https://doi.org/10.1007/S00343-020-0118-2
Han Y, Zhou W, Tang Y, Shi W, Shao Y, Ren P, Zhang J, Xiao G, Sun H, Liu G (2021a) Microplastics aggravate the bioaccumulation of three veterinary antibiotics in the thick shell mussel Mytilus coruscus and induce synergistic immunotoxic effects. Sci Total Environ 770:145273. https://doi.org/10.1016/J.SCITOTENV.2021.145273
Han YH, Song YM, Kim GW, Ha CS, Lee JS, Kim MH, Son HY, Lee GY, Gautam R, Heo Y (2021b) No prominent toxicity of polyethylene microplastics observed in neonatal mice following intratracheal instillation to dams during gestational and neonatal period. Toxicol Res 37:443–450. https://doi.org/10.1007/S43188-020-00086-7/FIGURES/2
Hanachi P, Karbalaei S, Yu S (2021a) Combined polystyrene microplastics and chlorpyrifos decrease levels of nutritional parameters in muscle of rainbow trout (Oncorhynchus mykiss). Environ Sci Pollut Res 2021(28):64908–64920. https://doi.org/10.1007/S11356-021-15536-4
Hanachi P, Kazemi S, Zivary S, Karbalaei S, AbolghasemGhadami S (2021b) The effect of polyethylene terephthalate and abamectin on oxidative damages and expression of vtg and cyp1a genes in juvenile zebrafish. Environ Nanotechnol Monit Manag. 16:100565. https://doi.org/10.1016/J.ENMM.2021.100565
Hanachi P, Malaki M, Karbalaei S. Effect of polystyrene microplastic and chlorpyrifos pesticide on superoxide dismutase activity in tissues of rainbow trout (Oncorhynchus mykiss). 2020.
Harrison JP, Schratzberger M, Sapp M, Osborn AM (2014) Rapid bacterial colonization of low-density polyethylene microplastics in coastal sediment microcosms. BMC Microbiol 14:1–15. https://doi.org/10.1186/S12866-014-0232-4/FIGURES/6
Hartmann NB, Hüffer T, Thompson RC, Hassellöv M, Verschoor A, Daugaard AE, Rist S, Karlsson T, Brennholt N, Cole M, Herrling MP, Hess MC, Ivleva NP, Lusher AL, Wagner M (2019) Are we speaking the same language? Recommendations for a definition and categorization framework for plastic debris. Environ Sci Technol 53:1039–1047. https://doi.org/10.1021/ACS.EST.8B05297/ASSET/IMAGES/MEDIUM/ES-2018-05297K_0006.GIF
He Y, Li J, Chen J, Miao X, Li G, He Q, Xu H, Li H, Wei Y (2020) Cytotoxic effects of polystyrene nanoplastics with different surface functionalization on human HepG2 cells. Sci Total Environ 723:138180. https://doi.org/10.1016/J.SCITOTENV.2020.138180
Horton AA, Walton A, Spurgeon DJ, Lahive E, Svendsen C (2017) Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci Total Environ 586:127–141. https://doi.org/10.1016/J.SCITOTENV.2017.01.190
Hou J, Lei Z, Cui L, Hou Y, Yang L, An R, Wang Q, Li S, Zhang H, Zhang L (2021b) Polystyrene microplastics lead to pyroptosis and apoptosis of ovarian granulosa cells via NLRP3/Caspase-1 signaling pathway in rats. Ecotoxicol Environ Saf 212:112012. https://doi.org/10.1016/J.ECOENV.2021.112012
Hsieh SL, Wu YC, Xu RQ, Chen YT, Chen CW, Singhania RR, Dong CD (2021) Effect of polyethylene microplastics on oxidative stress and histopathology damages in Litopenaeus vannamei. Environ Pollut 288:117800. https://doi.org/10.1016/J.ENVPOL.2021.117800
Hu L, Chernick M, Hinton DE, Shi H (2018) Microplastics in small waterbodies and tadpoles from Yangtze River Delta. China Environ Sci Technol 52:8885–8893. https://doi.org/10.1021/ACS.EST.8B02279/SUPPL_FILE/ES8B02279_SI_001.PDF
Hung KLJ, Kingston JM, Albrecht M, Holway DA, Kohn JR. The worldwide importance of honey bees as pollinators in natural habitats. Proc R Soc B Biol Sci. 2018; 285. https://doi.org/10.1098/RSPB.2017.2140.
Ijaz MU, Shahzadi S, Samad A, Ehsan N, Ahmed H, Tahir A, Rehman H, Anwar H (2021) Dose-dependent effect of polystyrene microplastics on the testicular tissues of the male Sprague Dawley rats. Dose Response 19:15593258211019882. https://doi.org/10.1177/15593258211019882
Imhof HK, Rusek J, Thiel M, Wolinska J, Laforsch C (2017) Do microplastic particles affect Daphnia magna at the morphological, life history and molecular level? PLoS ONE 12:e0187590. https://doi.org/10.1371/JOURNAL.PONE.0187590
Jeong CB, Kang HM, Byeon E, Kim MS, Ha SY, Kim M, Jung JH, Lee JS (2021) Phenotypic and transcriptomic responses of the rotifer Brachionus koreanus by single and combined exposures to nano-sized microplastics and water-accommodated fractions of crude oil. J Hazard Mater 416:125703. https://doi.org/10.1016/J.JHAZMAT.2021.125703
Jeong CB, Won EJ, Kang HM, Lee MC, Hwang DS, Hwang UK, Zhou B, Souissi S, Lee SJ, Lee JS (2016) Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ Sci Technol 50:8849–8857. https://doi.org/10.1021/ACS.EST.6B01441/SUPPL_FILE/ES6B01441_SI_001.PDF
Jeong J, Choi J (2019) Adverse outcome pathways potentially related to hazard identification of microplastics based on toxicity mechanisms. Chemosphere 231:249–255. https://doi.org/10.1016/J.CHEMOSPHERE.2019.05.003
Jiang X, Chen H, Liao Y, Ye Z, Li M, Klobučar G (2019) Ecotoxicity and genotoxicity of polystyrene microplastics on higher plant Vicia faba. Environ Pollut 250:831–838. https://doi.org/10.1016/J.ENVPOL.2019.04.055
Jin H, Ma T, Sha X, Liu Z, Zhou Y, Meng X, Chen Y, Han X, Ding J (2021) Polystyrene microplastics induced male reproductive toxicity in mice. J Hazard Mater 401:123430. https://doi.org/10.1016/J.JHAZMAT.2020.123430
Jin Y, Xia J, Pan Z, Yang J, Wang W, Fu Z (2018) Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ Pollut 235:322–329. https://doi.org/10.1016/j.envpol.2017.12.088
Karbalaei S, Hanachi P, Rafiee G, Seifori P, Walker TR (2021) Toxicity of polystyrene microplastics on juvenile Oncorhynchus mykiss (rainbow trout) after individual and combined exposure with chlorpyrifos. J Hazard Mater 403:123980. https://doi.org/10.1016/J.JHAZMAT.2020.123980
Karbalaei S, Hanachi P, Walker TR, Cole M (2018) Occurrence, sources, human health impacts and mitigation of microplastic pollution. Environ Sci Pollut Res 25:36046–36063. https://doi.org/10.1007/s11356-018-3508-7
Kim JH, Yu YB, Choi JH (2021) Toxic effects on bioaccumulation, hematological parameters, oxidative stress, immune responses and neurotoxicity in fish exposed to microplastics: a review. J Hazard Mater 413:125423. https://doi.org/10.1016/J.JHAZMAT.2021.125423
Kinigopoulou V, Pashalidis I, Kalderis D, Anastopoulos I (2022) Microplastics as carriers of inorganic and organic contaminants in the environment: a review of recent progress. J Mol Liq 350:118580. https://doi.org/10.1016/J.MOLLIQ.2022.118580
Kinjo A, Mizukawa K, Takada H, Inoue K (2019) Size-dependent elimination of ingested microplastics in the Mediterranean mussel Mytilus galloprovincialis. Mar Pollut Bull 149:110512. https://doi.org/10.1016/J.MARPOLBUL.2019.110512
Koelmans AA, Bakir A, Burton GA, Janssen CR (2016) Microplastic as a vector for chemicals in the aquatic environment: critical review and model-supported reinterpretation of empirical studies. Environ Sci Technol 50:3315–3326. https://doi.org/10.1021/ACS.EST.5B06069/SUPPL_FILE/ES5B06069_SI_001.PDF
Koelmans AA, Mohamed Nor NH, Hermsen E, Kooi M, Mintenig SM, De France J (2019) Microplastics in freshwaters and drinking water: Critical review and assessment of data quality. Water Res 155:410–422. https://doi.org/10.1016/J.WATRES.2019.02.054
Koelmans AA, Redondo-Hasselerharm PE, Mohamed Nor NH, Kooi M (2020) Solving the nonalignment of methods and approaches used in microplastic research to consistently characterize risk. Environ Sci Technol 54:12307–12315. https://doi.org/10.1021/ACS.EST.0C02982/ASSET/IMAGES/LARGE/ES0C02982_0004.JPEG
Lagarde F, Olivier O, Zanella M, Daniel P, Hiard S, Caruso A (2016) Microplastic interactions with freshwater microalgae: Hetero-aggregation and changes in plastic density appear strongly dependent on polymer type. Environ Pollut 215:331–339. https://doi.org/10.1016/J.ENVPOL.2016.05.006
Lajmanovich RC, Attademo AM, Lener G, Cuzziol Boccioni AP, Peltzer PM, Martinuzzi CS, Demonte LD, Repetti MR (2021) Glyphosate and glufosinate ammonium, herbicides commonly used on genetically modified crops, and their interaction with microplastics: Ecotoxicity in anuran tadpoles. Sci Total Environ 804:150177. https://doi.org/10.1016/J.SCITOTENV.2021.150177
Lebreton L, Andrady A (2019) Future scenarios of global plastic waste generation and disposal. Palgrave Commun. 51:1–11. https://doi.org/10.1057/s41599-018-0212-7
Lee J, Jeong S, Long C, Chandran K (2021a) Size dependent impacts of a model microplastic on nitrification induced by interaction with nitrifying bacteria. J Hazard Mater 424:127363. https://doi.org/10.1016/J.JHAZMAT.2021.127363
Lee Y, Yoon DS, Lee YH, Kwak JI, An YJ, Lee JS, Park JC (2021b) Combined exposure to microplastics and zinc produces sex-specific responses in the water flea Daphnia magna. J Hazard Mater 420:126652. https://doi.org/10.1016/J.JHAZMAT.2021.126652
Lehner R, Weder C, Petri-Fink A, Rothen-Rutishauser B (2019) Emergence of nanoplastic in the environment and possible impact on human health. Environ Sci Technol. https://doi.org/10.1021/ACS.EST.8B05512/ASSET/IMAGES/MEDIUM/ES-2018-055122_0006.GIF
Lei L, Wu S, Lu S, Liu M, Song Y, Fu Z, Shi H, Raley-Susman KM, He D (2018) Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci Total Environ 619–620:1–8. https://doi.org/10.1016/J.SCITOTENV.2017.11.103
Leung MCK, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, Meyer JN (2008) Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106:5–28. https://doi.org/10.1093/TOXSCI/KFN121
Li B, Song W, Cheng Y, Zhang K, Tian H, Du Z, Wang J, Wang J, Zhang W, Zhu L (2021a) Ecotoxicological effects of different size ranges of industrial-grade polyethylene and polypropylene microplastics on earthworms Eisenia fetida. Sci Total Environ 783:147007. https://doi.org/10.1016/J.SCITOTENV.2021.147007
Li D, Ji J, Yuan Y, Wang D (2020a) Toxicity comparison of nanopolystyrene with three metal oxide nanoparticles in nematode Caenorhabditis elegans. Chemosphere 245:125625. https://doi.org/10.1016/J.CHEMOSPHERE.2019.125625
Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69. https://doi.org/10.1111/NPH.12778
Li M, Liu Y, Xu G, Wang Y, Yu Y (2021b) Impacts of polyethylene microplastics on bioavailability and toxicity of metals in soil. Sci Total Environ 760:144037. https://doi.org/10.1016/J.SCITOTENV.2020.144037
Li Y, Liu Z, Yang Y, Jiang Q, Wu D, Huang Y, Jiao Y, Chen Q, Huang Y, Zhao Y (2021c) Effects of nanoplastics on energy metabolism in the oriental river prawn (Macrobrachium nipponense). Environ Pollut 268:115890. https://doi.org/10.1016/J.ENVPOL.2020.115890
Li Z, Feng C, Pang W, Tian C, Zhao Y (2021d) Nanoplastic-induced genotoxicity and intestinal damage in freshwater benthic clams (Corbicula fluminea): comparison with microplastics. ACS Nano 15:9469–9481. https://doi.org/10.1021/ACSNANO.1C02407/SUPPL_FILE/NN1C02407_SI_001.PDF
Liao B, Wang J, Xiao B, Yang X, Xie Z, Li D, Li C (2021) Effects of acute microplastic exposure on physiological parameters in Tubastrea aurea corals. Mar Pollut Bull 165:112173. https://doi.org/10.1016/J.MARPOLBUL.2021.112173
Liao YC, Jahitbek N, Li M, Wang XL, Jiang LJ (2019) Effects of microplastics on the growth, physiology, and biochemical characteristics of wheat (Triticum aestivum). Huan Jing Ke Xue Huanjing Kexue 40:4661–4667. https://doi.org/10.13227/J.HJKX.201903113
Liebezeit G, Liebezeit E (2013) Non-pollen particulates in honey and sugar. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:2136–2140. https://doi.org/10.1080/19440049.2013.843025
Limonta G, Mancia A, Abelli L, Fossi MC, Caliani I, Panti C (2021) Effects of microplastics on head kidney gene expression and enzymatic biomarkers in adult zebrafish. Comp Biochem Physiol Part C Toxicol Pharmacol 245:109037. https://doi.org/10.1016/J.CBPC.2021.109037
Lithner D, Larsson A, Dave G (2011) Environmental and health hazard ranking and assessment of plastic polymers based on chemical composition. Sci Total Environ 409:3309–3324. https://doi.org/10.1016/J.SCITOTENV.2011.04.038
Liu X, Ma J, Yang C, Wang L, Tang J. The toxicity effects of nano/microplastics on an antibiotic producing strain—Streptomyces coelicolor M145. Sci Total Environ. 2020; 142804. https://doi.org/10.1016/j.scitotenv.2020.142804.
Liu Z, Cai M, Wu D, Yu P, Jiao Y, Jiang Q, Zhao Y (2020) Effects of nanoplastics at predicted environmental concentration on Daphnia pulex after exposure through multiple generations. Environ Pollut 256:113506. https://doi.org/10.1016/J.ENVPOL.2019.113506
Liu Z, Cai M, Yu P, Chen M, Wu D, Zhang M, Zhao Y (2018) Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic. Aquat Toxicol 204:1–8. https://doi.org/10.1016/J.AQUATOX.2018.08.017
Livingstone DR. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. [WWW Document]. Mar Pollut Bull. 2001.
Lu K, Qiao R, An H, Zhang Y (2018) Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish (Danio rerio). Chemosphere 202:514–520. https://doi.org/10.1016/j.chemosphere.2018.03.145
Lu Y, Zhang Y, Deng Y, Jiang W, Zhao Y, Geng J, Ding L, Ren H (2016) Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ Sci Technol 50:4054–4060. https://doi.org/10.1021/acs.est.6b00183
Lyu K, Cao C, Li D, Akbar S, Yang Z (2021) The thermal regime modifies the response of aquatic keystone species Daphnia to microplastics: evidence from population fitness, accumulation, histopathological analysis and candidate gene expression. Sci Total Environ 783:147154. https://doi.org/10.1016/J.SCITOTENV.2021.147154
Machado MC, Vimbela GV, Silva-Oliveira TT, Bose A, Tripathi A (2020) The response of Synechococcus sp. PCC 7002 to micro-/nano polyethylene particles—investigation of a key anthropogenic stressor. PLoS ONE 15:e0232745. https://doi.org/10.1371/JOURNAL.PONE.0232745
Magara G, Elia AC, Syberg K, Khan FR (2018) Single contaminant and combined exposures of polyethylene microplastics and fluoranthene: accumulation and oxidative stress response in the blue mussel, Mytilus edulis. J Toxicol Environ Health Part a 81:761–773. https://doi.org/10.1080/15287394.2018.1488639
Magara G, Khan FR, Pinti M, Syberg K, Inzirillo A, Elia AC (2019) Effects of combined exposures of fluoranthene and polyethylene or polyhydroxybutyrate microplastics on oxidative stress biomarkers in the blue mussel (Mytilus edulis). J Toxicol Environ Health Part A 82:616–625. https://doi.org/10.1080/15287394.2019.1633451
Maity S, Chatterjee A, Guchhait R, De S, Pramanick K (2020) Cytogenotoxic potential of a hazardous material, polystyrene microparticles on Allium cepa L. J Hazard Mater 385:121560. https://doi.org/10.1016/J.JHAZMAT.2019.121560
Matthews S, Mai L, Jeong CB, Lee JS, Zeng EY, Xu EG (2021) Key mechanisms of micro- and nanoplastic (MNP) toxicity across taxonomic groups. Comp Biochem Physiol Part C Toxicol Pharmacol 247:109056. https://doi.org/10.1016/J.CBPC.2021.109056
Mohsen M, Lin C, Liu S, Yang H (2021) Existence of microplastics in the edible part of the sea cucumber Apostichopus japonicus. Chemosphere 287:132062. https://doi.org/10.1016/J.CHEMOSPHERE.2021.132062
Muhammad A, Zhou X, He J, Zhang N, Shen X, Sun C, Yan B, Shao Y (2021) Toxic effects of acute exposure to polystyrene microplastics and nanoplastics on the model insect, silkworm Bombyx mori. Environ Pollut 285:117255. https://doi.org/10.1016/J.ENVPOL.2021.117255
Muñiz-González AB, Silva CJM, Patricio Silva AL, Campos D, Pestana JLT, Martínez-Guitarte JL (2021) Suborganismal responses of the aquatic midge Chironomus riparius to polyethylene microplastics. Sci Total Environ 783:146981. https://doi.org/10.1016/J.SCITOTENV.2021.146981
Natarajan L, Omer S, Jetly N, Jenifer MA, Chandrasekaran N, Suraishkumar GK, Mukherjee A (2020) Eco-corona formation lessens the toxic effects of polystyrene nanoplastics towards marine microalgae Chlorella sp. Environ Res 188:109842. https://doi.org/10.1016/J.ENVRES.2020.109842
Ng EL, Huerta Lwanga E, Eldridge SM, Johnston P, Hu HW, Geissen V, Chen D (2018) An overview of microplastic and nanoplastic pollution in agroecosystems. Sci Total Environ 627:1377–1388. https://doi.org/10.1016/J.SCITOTENV.2018.01.341
Nunes B, Simões MI, Navarro JC, Castro BB (2020) First ecotoxicological characterization of paraffin microparticles: a biomarker approach in a marine suspension-feeder Mytilus sp. Environ Sci Pollut Res 2020(27):41946–41960. https://doi.org/10.1007/S11356-020-10055-0
O’Brien CJ, Hong HC, Bryant EE, Connor KM (2021) The observation of starch digestion in blue mussel Mytilus galloprovincialis exposed to microplastic particles under varied food conditions. PLoS ONE 16:e0253802. https://doi.org/10.1371/JOURNAL.PONE.0253802
Oleksiak MF (2008) Changes in gene expression due to chronic exposure to environmental pollutants. Aquat Toxicol 90:161–171
Onyena AP, Aniche DC, Ogbolu BO, Rakib MRJ, Uddin J, Walker TR (2021) Governance strategies for mitigating microplastic pollution in the marine environment: a review. Microplastics 2022(1):15–46. https://doi.org/10.3390/MICROPLASTICS1010003
Parenti CC, Ghilardi A, Della Torre C, Magni S, Del Giacco L, Binelli A (2019) Evaluation of the infiltration of polystyrene nanobeads in zebrafish embryo tissues after short-term exposure and the related biochemical and behavioural effects. Environ Pollut 254:112947. https://doi.org/10.1016/J.ENVPOL.2019.07.115
Parker BW, Beckingham BA, Ingram BC, Ballenger JC, Weinstein JE, Sancho G (2020) Microplastic and tire wear particle occurrence in fishes from an urban estuary: Influence of feeding characteristics on exposure risk. Mar Pollut Bull 160:111539. https://doi.org/10.1016/J.MARPOLBUL.2020.111539
Parolini M, De Felice B, Gazzotti S, Annunziata L, Sugni M, Bacchetta R, Ortenzi MA (2020) Oxidative stress-related effects induced by micronized polyethylene terephthalate microparticles in the Manila clam. J Toxicol Environ Health Part a 83:168–179. https://doi.org/10.1080/15287394.2020.1737852
Paul-Pont I, Lacroix C, González Fernández C, Hégaret H, Lambert C, Le Goïc N, Frère L, Cassone AL, Sussarellu R, Fabioux C, Guyomarch J, Albentosa M, Huvet A, Soudant P (2016) Exposure of marine mussels Mytilus spp. to polystyrene microplastics: toxicity and influence on fluoranthene bioaccumulation. Environ Pollut 216:724–737. https://doi.org/10.1016/J.ENVPOL.2016.06.039
Pehlivan N, Gedik K (2021) Particle size-dependent biomolecular footprints of interactive microplastics in maize. Environ Pollut 277:116772. https://doi.org/10.1016/J.ENVPOL.2021.116772
Peng L, Fu D, Qi H, Lan CQ, Yu H, Ge C (2020) Micro- and nano-plastics in marine environment: source, distribution and threats—a review. Sci Total Environ 698:134254. https://doi.org/10.1016/J.SCITOTENV.2019.134254
PlasticsEurope, 2020. Plastics—the Facts 2020 by PlasticsEurope, https://issuu.com/plasticseuropeebook/docs/plastics_the_facts-web-dec2020 [WWW Document]. URL https://issuu.com/plasticseuropeebook/docs/plastics_the_facts-web-dec2020. Accessed 12 May 21.
Prendergast-Miller MT, Katsiamides A, Abbass M, Sturzenbaum SR, Thorpe KL, Hodson ME (2019) Polyester-derived microfibre impacts on the soil-dwelling earthworm Lumbricus terrestris. Environ Pollut 251:453–459. https://doi.org/10.1016/J.ENVPOL.2019.05.037
Provencher JF, Au SY, Horn D, Mallory ML, Walker TR, Kurek J, Erdle LM, Weis JS, Lusher A. Animals and microplastics: ingestion, transport, breakdown, and trophic transfer. Polluting Text. 2022;33–62. https://doi.org/10.4324/9781003165385-4.
Qiao R, Lu K, Deng Y, Ren H, Zhang Y (2019a) Combined effects of polystyrene microplastics and natural organic matter on the accumulation and toxicity of copper in zebrafish. Sci Total Environ 682:128–137. https://doi.org/10.1016/j.scitotenv.2019.05.163
Qiao R, Sheng C, Lu Y, Zhang Y, Ren H, Lemos B (2019b) Microplastics induce intestinal inflammation, oxidative stress, and disorders of metabolome and microbiome in zebrafish. Sci Total Environ 662:246–253. https://doi.org/10.1016/j.scitotenv.2019.01.245
Qiu Y, Luo L, Yang Y, Kong Y, Li Y, Wang D (2020) Potential toxicity of nanopolystyrene on lifespan and aging process of nematode Caenorhabditis elegans. Sci Total Environ 705:135918. https://doi.org/10.1016/J.SCITOTENV.2019.135918
Qu M, Li D, Qiu Y, Wang D (2020) Neuronal ERK MAPK signaling in response to low-dose nanopolystyrene exposure by suppressing insulin peptide expression in Caenorhabditis elegans. Sci Total Environ 724:138378. https://doi.org/10.1016/J.SCITOTENV.2020.138378
Reisser J, Shaw J, Hallegraeff G, Proietti M, Barnes DKA, Thums M, Wilcox C, Hardesty BD, Pattiaratchi C (2014) Millimeter-sized marine plastics: a new pelagic habitat for microorganisms and invertebrates. PLoS ONE 9:e100289. https://doi.org/10.1371/JOURNAL.PONE.0100289
Revel M, Lagarde F, Perrein-Ettajani H, Bruneau M, Akcha F, Sussarellu R, Rouxel J, Costil K, Decottignies P, Cognie B, Châtel A, Mouneyrac C (2019) Tissue-specific biomarker responses in the blue mussel Mytilus spp. exposed to a mixture of microplastics at environmentally relevant concentrations. Front Environ Sci 7:33. https://doi.org/10.3389/FENVS.2019.00033/BIBTEX
Rhodes CJ (2018) Plastic pollution and potential solutions. Sci Prog 101:207–260. https://doi.org/10.3184/003685018X15294876706211
Ripken C, Khalturin K, Shoguchi E (2020) Response of coral reef dinoflagellates to nanoplastics under experimental conditions suggests downregulation of cellular metabolism. Microorg. 2020(8):1759. https://doi.org/10.3390/MICROORGANISMS8111759
Rochman CM (2018) Microplastics research—from sink to source. Science (80-). 360:28–29. https://doi.org/10.1126/SCIENCE.AAR7734
Rochman CM (2015) The complex mixture, fate and toxicity of chemicals associated with plastic debris in the marine environment. Marine anthropogenic litter. Springer, Cham, pp 117–140
Rodriguez-Seijo A, Lourenço J, Rocha-Santos TAP, da Costa J, Duarte AC, Vala H, Pereira R (2017) Histopathological and molecular effects of microplastics in Eisenia andrei Bouché. Environ Pollut 220:495–503. https://doi.org/10.1016/J.ENVPOL.2016.09.092
Schnurr REJ, Alboiu V, Chaudhary M, Corbett RA, Quanz ME, Sankar K, Srain HS, Thavarajah V, Xanthos D, Walker TR (2018) Reducing marine pollution from single-use plastics (SUPs): a review. Mar Pollut Bull 137:157–171. https://doi.org/10.1016/J.MARPOLBUL.2018.10.001
Scopetani C, Esterhuizen M, Cincinelli A, Pflugmacher S (2020) Microplastics exposure causes negligible effects on the oxidative response enzymes glutathione reductase and peroxidase in the oligochaete Tubifex tubifex. Toxics 2020(8):14. https://doi.org/10.3390/TOXICS8010014
Shang Y, Gu H, Li S, Chang X, Sokolova I, Fang JKH, Wei S, Chen X, Hu M, Huang W, Wang Y (2021) Microplastics and food shortage impair the byssal attachment of thick-shelled mussel Mytilus coruscus. Mar Environ Res 171:105455. https://doi.org/10.1016/J.MARENVRES.2021.105455
Shim WJ, Hong SH, Eo SE (2017) Identification methods in microplastic analysis: a review. Anal Methods 9:1384–1391. https://doi.org/10.1039/C6AY02558G
Shao H, Wang D (2020) Long-term and low-dose exposure to nanopolystyrene induces a protective strategy to maintain functional state of intestine barrier in nematode Caenorhabditis elegans. Environ Pollut 258:113649. https://doi.org/10.1016/J.ENVPOL.2019.113649
Silva CJM, Patrício Silva AL, Campos D, Machado AL, Pestana JLT, Gravato C (2021) Oxidative damage and decreased aerobic energy production due to ingestion of polyethylene microplastics by Chironomus riparius (Diptera) larvae. J Hazard Mater 402:123775. https://doi.org/10.1016/J.JHAZMAT.2020.123775
Sıkdokur E, Belivermiş M, Sezer N, Pekmez M, Bulan ÖK, Kılıç Ö (2020) Effects of microplastics and mercury on manila clam Ruditapes philippinarum: feeding rate, immunomodulation, histopathology and oxidative stress. Environ Pollut 262:114247. https://doi.org/10.1016/J.ENVPOL.2020.114247
Sleight VA, Bakir A, Thompson RC, Henry TB (2017) Assessment of microplastic-sorbed contaminant bioavailability through analysis of biomarker gene expression in larval zebrafish. Mar Pollut Bull 116:291–297. https://doi.org/10.1016/j.marpolbul.2016.12.055
Song C, Liu Z, Wang C, Li S, Kitamura Y (2020) Different interaction performance between microplastics and microalgae: the bio-elimination potential of Chlorella sp. L38 and Phaeodactylum tricornutum MASCC-0025. Sci Total Environ 723:138146. https://doi.org/10.1016/J.SCITOTENV.2020.138146
Song Y, Cao C, Qiu R, Hu J, Liu M, Lu S, Shi H, Raley-Susman KM, He D (2019b) Uptake and adverse effects of polyethylene terephthalate microplastics fibers on terrestrial snails (Achatina fulica) after soil exposure. Environ Pollut 250:447–455. https://doi.org/10.1016/J.ENVPOL.2019.04.066
Stock V, Böhmert L, Lisicki E, Block R, Cara-Carmona J, Pack LK, Selb R, Lichtenstein D, Voss L, Henderson CJ, Zabinsky E, Sieg H, Braeuning A, Lampen A (2019) Uptake and effects of orally ingested polystyrene microplastic particles in vitro and in vivo. Arch Toxicol 93:1817–1833. https://doi.org/10.1007/s00204-019-02478-7
Su Y, Zhang K, Zhou Z, Wang J, Yang X, Tang J, Li H, Lin S (2020) Microplastic exposure represses the growth of endosymbiotic dinoflagellate Cladocopium goreaui in culture through affecting its apoptosis and metabolism. Chemosphere 244:125485. https://doi.org/10.1016/J.CHEMOSPHERE.2019.125485
Suman TY, Jia PP, Li WG, Junaid M, Xin GY, Wang Y, Pei DS (2020) Acute and chronic effects of polystyrene microplastics on brine shrimp: first evidence highlighting the molecular mechanism through transcriptome analysis. J Hazard Mater 400:123220. https://doi.org/10.1016/J.JHAZMAT.2020.123220
Sun S, Shi W, Tang Y, Han Y, Du X, Zhou W, Hu Y, Zhou C, Liu G (2020) Immunotoxicity of petroleum hydrocarbons and microplastics alone or in combination to a bivalve species: synergic impacts and potential toxication mechanisms. Sci Total Environ 728:138852. https://doi.org/10.1016/J.SCITOTENV.2020.138852
Sun Y, Ren X, Rene ER, Wang Z, Zhou L, Zhang Z, Wang Q (2021) The degradation performance of different microplastics and their effect on microbial community during composting process. Bioresour Technol 332:125133. https://doi.org/10.1016/J.BIORTECH.2021.125133
Tang J, Ni X, Zhou Z, Wang L, Lin S (2018) Acute microplastic exposure raises stress response and suppresses detoxification and immune capacities in the scleractinian coral Pocillopora damicornis. Environ Pollut 243:66–74. https://doi.org/10.1016/J.ENVPOL.2018.08.045
Tang J, Wang X, Yin J, Han Y, Yang J, Lu X, Xie T, Akbar S, Lyu K, Yang Z (2019) Molecular characterization of thioredoxin reductase in waterflea Daphnia magna and its expression regulation by polystyrene microplastics. Aquat Toxicol 208:90–97. https://doi.org/10.1016/J.AQUATOX.2019.01.001
Tang Y, Zhou W, Sun S, Du X, Han Y, Shi W, Liu G (2020) Immunotoxicity and neurotoxicity of bisphenol A and microplastics alone or in combination to a bivalve species, Tegillarca Granosa. Environ Pollut 265:115115. https://doi.org/10.1016/J.ENVPOL.2020.115115
Teh SJ, Adams SM, Hinton DE (1997) Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat Toxicol 37:51–70. https://doi.org/10.1016/S0166-445X(96)00808-9
Teng J, Zhao J, Zhu X, Shan E, Wang Q (2021) Oxidative stress biomarkers, physiological responses and proteomic profiling in oyster (Crassostrea gigas) exposed to microplastics with irregular-shaped PE and PET microplastic. Sci Total Environ 786:147425. https://doi.org/10.1016/J.SCITOTENV.2021.147425
Toussaint B, Raffael B, Angers-Loustau A, Gilliland D, Kestens V, Petrillo M, Rio-Echevarria IM, Van den Eede G (2019) Review of micro- and nanoplastic contamination in the food chain. Food Additiv Contam. 36:639–673. https://doi.org/10.1080/19440049.2019.1583381
Trestrail C, Walpitagama M, Miranda A, Nugegoda D, Shimeta J (2021) Microplastics alter digestive enzyme activities in the marine bivalve, Mytilus Galloprovincialis. Sci Total Environ 779:146418. https://doi.org/10.1016/J.SCITOTENV.2021.146418
Trevisan R, Voy C, Chen S, Di Giulio RT (2019) Nanoplastics decrease the toxicity of a complex PAH mixture but impair mitochondrial energy production in developing Zebrafish. Environ Sci Technol 53:8405–8415. https://doi.org/10.1021/ACS.EST.9B02003/SUPPL_FILE/ES9B02003_SI_001.PDF
Varó I, Perini A, Torreblanca A, Garcia Y, Bergami E, Vannuccini ML, Corsi I (2019) Time-dependent effects of polystyrene nanoparticles in brine shrimp Artemia franciscana at physiological, biochemical and molecular levels. Sci Total Environ 675:570–580. https://doi.org/10.1016/j.scitotenv.2019.04.157
Walker TR, McGuinty E. 2021. Plastics. Palgrave Handb Glob Sustain. 1–12. https://doi.org/10.1007/978-3-030-38948-2_55-1.
Wan Z, Wang C, Zhou J, Shen M, Wang X, Fu Z, Jin Y (2019) Effects of polystyrene microplastics on the composition of the microbiome and metabolism in larval zebrafish. Chemosphere 217:646–658. https://doi.org/10.1016/j.chemosphere.2018.11.070
Wang F, Wang X, Song N (2021a) Polyethylene microplastics increase cadmium uptake in lettuce (Lactuca sativa L.) by altering the soil microenvironment. Sci Total Environ 784:147133. https://doi.org/10.1016/J.SCITOTENV.2021.147133
Wang K, Li J, Zhao L, Mu X, Wang C, Wang M, Xue X, Qi S, Wu L (2021b) Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. J Hazard Mater 402:123828. https://doi.org/10.1016/J.JHAZMAT.2020.123828
Wang L, Gao Y, Jiang W, Chen J, Chen Y, Zhang X, Wang G (2021c) Microplastics with cadmium inhibit the growth of Vallisneria natans (Lour.) Hara rather than reduce cadmium toxicity. Chemosphere 266:128979. https://doi.org/10.1016/J.CHEMOSPHERE.2020.128979
Wang S, Li Q, Huang S, Zhao W, Zheng Z (2021d) Single and combined effects of microplastics and lead on the freshwater algae Microcystis aeruginosa. Ecotoxicol Environ Saf 208:111664. https://doi.org/10.1016/J.ECOENV.2020.111664
Wang Y, Mao Z, Zhang M, Ding G, Sun J, Du M, Liu Q, Cong Y, Jin F, Zhang W, Wang J (2019) The uptake and elimination of polystyrene microplastics by the brine shrimp, Artemia parthenogenetica, and its impact on its feeding behavior and intestinal histology. Chemosphere 234:123–131. https://doi.org/10.1016/J.CHEMOSPHERE.2019.05.267
Wang Z, Fan L, Wang J, Xie S, Zhang C, Zhou J, Zhang L, Xu G, Zou J (2021e) Insight into the immune and microbial response of the white-leg shrimp Litopenaeus vannamei to microplastics. Mar Environ Res 169:105377. https://doi.org/10.1016/J.MARENVRES.2021.105377
Wei Q, Hu CY, Zhang RR, Gu YY, Sun AL, Zhang ZM, Shi XZ, Chen J, Wang TZ (2021) Comparative evaluation of high-density polyethylene and polystyrene microplastics pollutants: uptake, elimination and effects in mussel. Mar Environ Res 169:105329. https://doi.org/10.1016/J.MARENVRES.2021.105329
Wright RJ, Langille MGI, Walker TR (2020) Food or just a free ride? A meta-analysis reveals the global diversity of the plastisphere. ISME J 202015:789–806. https://doi.org/10.1038/s41396-020-00814-9
Wu D, Liu Z, Cai M, Jiao Y, Li Y, Chen Q, Zhao Y (2019) Molecular characterisation of cytochrome P450 enzymes in waterflea (Daphnia pulex) and their expression regulation by polystyrene nanoplastics. Aquat Toxicol 217:105350. https://doi.org/10.1016/J.AQUATOX.2019.105350
Wu X, Hou H, Liu Y, Yin S, Bian S, Liang S, Wan C, Yuan S, Xiao K, Liu B, Hu J, Yang J (2021) Microplastics affect rice (Oryza sativa L.) quality by interfering metabolite accumulation and energy expenditure pathways: a field study. J Hazard Mater 422:126834. https://doi.org/10.1016/J.JHAZMAT.2021.126834
Lu X-M, Jiang X-Q, Liu X-P (2021) Response process and adaptation mechanism of estuarine benthic microbiota to polyvinyl chloride microplastics with and without phthalates. Sci Total Environ 806:150693. https://doi.org/10.1016/J.SCITOTENV.2021.150693
Xiao Y, Jiang X, Liao Y, Zhao W, Zhao P, Li M (2020) Adverse physiological and molecular level effects of polystyrene microplastics on freshwater microalgae. Chemosphere 255:126914. https://doi.org/10.1016/J.CHEMOSPHERE.2020.126914
Xu G, Liu Y, Yu Y (2021) Effects of polystyrene microplastics on uptake and toxicity of phenanthrene in soybean. Sci Total Environ 783:147016. https://doi.org/10.1016/J.SCITOTENV.2021.147016
Xu G, Yu Y (2021) Polystyrene microplastics impact the occurrence of antibiotic resistance genes in earthworms by size-dependent toxic effects. J Hazard Mater 416:125847. https://doi.org/10.1016/J.JHAZMAT.2021.125847
Yan Z, Xu L, Zhang W, Yang G, Zhao Z, Wang Y, Li X (2021) Comparative toxic effects of microplastics and nanoplastics on Chlamydomonas reinhardtii: growth inhibition, oxidative stress, and cell morphology. J Water Process Eng 43:102291. https://doi.org/10.1016/J.JWPE.2021.102291
Yu H, Qi W, Cao X, Wang Y, Li Y, Xu Y, Zhang X, Peng J, Qu J (2021) Impact of microplastics on the foraging, photosynthesis and digestive systems of submerged carnivorous macrophytes under low and high nutrient concentrations. Environ Pollut 292:118220. https://doi.org/10.1016/J.ENVPOL.2021.118220
Yu Y, Chen H, Hua X, Dang Y, Han Y, Yu Z, Chen X, Ding P, Li H (2020) Polystyrene microplastics (PS-MPs) toxicity induced oxidative stress and intestinal injury in nematode Caenorhabditis elegans. Sci Total Environ 726:138679. https://doi.org/10.1016/J.SCITOTENV.2020.138679
Zhang P, Yan Z, Lu G, Ji Y (2019) Single and combined effects of microplastics and roxithromycin on Daphnia magna. Environ Sci Pollut Res 2019(26):17010–17020. https://doi.org/10.1007/S11356-019-05031-2
Zhang Q, Zhao M, Meng F, Xiao Y, Dai W, Luan Y (2021a) Effect of polystyrene microplastics on rice seed germination and antioxidant enzyme activity. Toxics 2021(9):179. https://doi.org/10.3390/TOXICS9080179
Zhang W, Liu Z, Tang S, Li D, Jiang Q, Zhang T (2020) Transcriptional response provides insights into the effect of chronic polystyrene nanoplastic exposure on Daphnia pulex. Chemosphere 238:124563. https://doi.org/10.1016/J.CHEMOSPHERE.2019.124563
Zhang X, Wang X, Yan B (2021b) Single and combined effects of phenanthrene and polystyrene microplastics on oxidative stress of the clam (Mactra veneriformis). Sci Total Environ 771:144728. https://doi.org/10.1016/J.SCITOTENV.2020.144728
Zhao S, Ward JE, Danley M, Mincer TJ (2018) Field-based evidence for microplastic in marine aggregates and mussels: implications for trophic transfer. Environ Sci Technol 52:11038–11048. https://doi.org/10.1021/ACS.EST.8B03467/SUPPL_FILE/ES8B03467_SI_001.PDF
Zhao T, Tan L, Zhu X, Huang W, Wang J (2020) Size-dependent oxidative stress effect of nano/micro-scaled polystyrene on Karenia mikimotoi. Mar Pollut Bull 154:111074. https://doi.org/10.1016/J.MARPOLBUL.2020.111074
Zheng H, Wang J, Wei X, Chang L, Liu S (2021a) Proinflammatory properties and lipid disturbance of polystyrene microplastics in the livers of mice with acute colitis. Sci Total Environ 750:143085. https://doi.org/10.1016/j.scitotenv.2020.143085
Zheng JL, Wang D, Chen X, Song HZ, Xiang LP, Yu HX, Peng LB, Zhu QL (2021b) Nutritional-status dependent effects of microplastics on activity and expression of alkaline phosphatase and alpha-amylase in Brachionus rotundiformis. Sci Total Environ 806:150213. https://doi.org/10.1016/J.SCITOTENV.2021.150213
Zheng X, Zhang W, Yuan Y, Li Y, Liu X, Wang X, Fan Z (2021c) Growth inhibition, toxin production and oxidative stress caused by three microplastics in Microcystis aeruginosa. Ecotoxicol Environ Saf 208:111575. https://doi.org/10.1016/J.ECOENV.2020.111575
Zhou W, Tang Y, Du X, Han Y, Shi W, Sun S, Zhang W, Zheng H, Liu G (2021) Fine polystyrene microplastics render immune responses more vulnerable to two veterinary antibiotics in a bivalve species. Mar Pollut Bull 164:111995. https://doi.org/10.1016/J.MARPOLBUL.2021.111995
Zhu ZL, Wang SC, Zhao FF, Wang SG, Liu FF, Liu GZ (2019) Joint toxicity of microplastics with triclosan to marine microalgae Skeletonema costatum. Environ Pollut 246:509–517. https://doi.org/10.1016/J.ENVPOL.2018.12.044
The authors would like to acknowledge Dr. Abbas Abdollahi for his critical review and valuable suggestions.
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: Table S1. Studies summarizing the following criteria: species and common name of organisms, MPs type and size, contaminants absorbed to MPs, MPs and contaminant concentration, duration of the experiment, toxicological effect (enzyme activity, gene expression and histopathology) and organism tissues.
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Patra, I., Huy, D.T.N., Alsaikhan, F. et al. Toxic effects on enzymatic activity, gene expression and histopathological biomarkers in organisms exposed to microplastics and nanoplastics: a review. Environ Sci Eur 34, 80 (2022). https://doi.org/10.1186/s12302-022-00652-w