Effects of microplastics on the intestines

Abstract

Microplastics (MPs) are small pieces of plastic less than 5 mm in diameter. They are formed both as a primary product, which has found use in textiles and microspheres in cosmetics, and as a secondary product, resulting from the degradation of larger pieces of plastic due to physical, chemical, and even biological factors. The intestinal barrier is one of the body’s lines of defence against the entry of MPs molecules into the body. It can enter the body through various mechanisms and cause accumulation in the intestines and other organs. Furthermore, MPs can cause changes in the function of the intestinal barrier and increase its permeability, causing increased accumulation of particles. However, the actual extent of human exposure is still unknown due to discrepancies in the methodology of the available studies. Therefore, new validated analytical methods and long-term studies are needed to better understand the effects of microplastics on intestinal health.

Background

Microplastics: characteristics and origin

Plastics are a human made milestone due to their versatility and ability to transform many industries. Due to a variety of properties such as lightness, strength, and corrosion resistance, these synthetic polymers are used in countless fields, from medicine to construction, resulting in their widespread availability [1, 2]. Statistical data clearly showed a drastic increase in global plastic production from 1.5 million tons in 1950 to almost 360 million tons in 2018 [3]. However, there is also another side to plastics, as improper waste management in our daily lives has led to an increase in microplastic pollution of the ecosystem. Microplastics (MPs) are now ubiquitous in the environment, which unfortunately translates into growing health concerns around the world. The situation is even worse because plastics do not degrade quickly compared to the natural polymers previously used in industry. Microplastics are tiny pieces of plastic less than 5 mm in diameter. It is formed as both a primary product, which was used in textiles and microspheres in cosmetics, and as a secondary product, resulting from the degradation of larger pieces of plastic due to physical, chemical, and even biological factors [4]. Secondary MPs also includes textile fibre fragments that are released on an ongoing basis when synthetic fabrics and agricultural films are washed and left on agricultural land. However, the main source of secondary plastic microplastics is plastic trash left on beaches and decomposing when exposed to the elements [5]. The chemical composition of microplastics can be divided into six main groups: polyethylene (PE), polystyrene (PS), polypropylene (PP), polyurethane (PUR), polyvinyl chloride, and polyethylene terephthalate (PET) [6]. Microplastics can also be divided into five basic categories based on their shape and form: pellets, fragments, films, fibres, and foams. Each of these groups and categories has unique properties and sources, which is important to understand their environmental impact, their ability to penetrate marine and terrestrial ecosystems or accumulate in living organisms [7].

Distribution and environmental presence of microplastics

Alarmingly, its presence has been reported even in the most remote corners of the Earth, encompassing ecosystems such as marine environments, freshwater reservoirs, soil, and even the atmosphere [8]. Plastic waste enters seawater and can then be transported over very long distances by ocean currents located at different latitudes [9]. MPs contamination is commonly observed in the marine ecosystem and, consequently, it is widely spread among fauna.

MPs can undergo many processes, such as environmental ageing and even further degradation, to form nanoplastics. These, in turn, are more harmful due to their higher surface to volume ratio and ability to absorb more contaminants and be easily inhaled or ingested [10].

Microplastic degradation in the environment

Abiotic degradation refers to the transformation of polymers by fragmentation of larger fragments into MPs as a result of the action of various physical and chemical factors, the most important of which are abrasion, UV radiation, hydrolysis, and thermal influence [11]. Plastics contain a wide range of chemical bonds, including ester bonds (-COO) in PET, amide bonds (NH–CO) in nylon, and carbon skeleton compounds (C–C) found in PE and PP [12].

Interestingly, the existence of these bonds may have a significant impact on the degradation of microplastics through cometabolism, a microbiological phenomenon in which microorganisms decompose organic compounds in the environment. This effect can be intensified depending on the amount of substrates and carbon supplied and, consequently, the energy generated [13]. This energy increases the production of proteins, including microbial enzymes, improving the efficiency of substrate decomposition. Factors such as environmental pH, oxygenation, radiation, or salinity can significantly affect the growth of these microorganisms and thus indirectly affect biodegradation [14].

These specialised enzymes break down the complex polymer structure into easie to manage components. The most important chemical substances that contribute to better biodegradation include laccase [15], oxidase, depolymerases and hydrolases, which hydrolyse complex molecules into simpler structures, a number of organic acids (e.g. oxalic acid) [16], chitinase obtained from fungi is able to significantly degrade materials made of PE and PET [17].

The mentioned microorganisms include a large group of bacteria that have the ability to effectively decompose MPs using bacterial enzymes, including PET hydrolase (PETase) and mono-(2-hydroxyethyl terephthalate) hydrolase (MHETase). Many bacterial taxa have a huge impact on the wastewater treatment process through the enzymatic degradation of plastics, including the following: Vibrio, Campylobacter, and Arcobacter [18]. Studies have shown that it is possible to degrade MPs by: S. panacihumi, Aneurinibacillus spp., Brevibacillus spp. [19], while strains of B. amyloliquefaciens degrade PW [20].

In the fungi kingdom, many species are also responsible for the biodegradation of MPs. The use of low-density polyethylene (LDPE) as a carbon source for a group of fungi including Fusarium sp., A. japonicas, and A. flavus resulted in the growth and extracellular production of enzymes that then degraded this plastic [21]. Enzymes produced by fungi, such as cutinases, lipases, and esterases, may be responsible for the hydrolysis of plastics [22]. Lignin degrading enzymes, i.e. laccases and peroxidases, can degrade LDPE through anaerobic and aerobic processes [23].

Naturally in the environment, yeasts are also able to decompose plastic residues; a perfect example is the degradation and assimilation of PE by the marine yeast Rhodotorula mucilaginosa [24]. Currently, many researchers use yeast as a model organism in the laboratory, which may have a future in terms of plastic degradation. The use of genetic engineering methods can significantly support this process by overexpressing genes that increase the production of hydrolytic enzymes [25, 26].

Algae also have a very important impact on MPs degradation. Various species of phytoplankton produce enzymes, including lipases, esterases, and cellulases, which can help to better bond with the plastic surface, thus initiating the process of plastic biodegradation and fragmentation. For example, microalgae can settle on the surfaces of plastics, including PET, and catalyse the hydrolysis of this plastic by producing the PETease enzyme [27]. Many species of algae can create the so-called biofilms, including those on plastic surfaces. This property has a significant impact on microplastic contaminated lakes and ponds [28]. Moreover, many microorganisms are able to create the so-called biofilm, including in the aquatic environment. Additionally, the structure of the biofilm allows for a more efficient use of resources and protection of microorganisms against unfavourable environmental conditions, supporting the degradation process of MPs [29].

Impact of MPs on the environment, flora and fauna

Many studies clearly show that microplastics have a degrading effect on ecosystems. It has been shown that in areas affected by heavy microplastic pollution, the total number of plants and animals decreases dramatically. Negative effects of MPs are also observed in processes related to the nitrogen cycle, oxygen production by plants, and reduction of carbon dioxide emissions into the atmosphere [30]. Reduced plant productivity is observed as a result of soil depletion. Microplastics may be responsible for the composition of the soil microflora, which is primarily responsible for all the processes of metabolising harmful substances [31].

MPs are small in size and their colours are often similar to those of natural tiny marine organisms that fish feed on. This causes them to be absorbed in large amounts by fish, causing physiological changes in their bodies. MPs contamination is commonly observed in the marine ecosystem and, consequently, it is widely spread among fauna.

Human exposure to microplastics through the food chain

However, the most dangerous problem is its transmission to humans through the food chain [32]. Research shows that microplastics have been found in the digestive tracts of the fish we eat every day, so consuming seafood exposes people to microplastics [33]. For example, some studies have found microplastics in fish caught in coastal waters and the open ocean [34]. When people eat these fish, microplastics can enter their bodies, potentially causing negative health effects, such as physically damaging tissues. Substances used in plastics production also have an adverse impact on human health. The ingress of microplastics can cause disruptions in the endocrine system, which can be caused by substances such as bisphenol A (BPA) and phthalates [35].

Furthermore, microplastics have the ability to absorb and concentrate chemical pollutants and heavy metals, which may increase the risk of toxicity for people who eat contaminated fish [36]. As researchers point out in their reports, MPs are the main carriers of heavy metals in groundwater, and traces of plastics have also been recorded in tap and bottled water [37].

Microplastics pose a threat to human life

Further and more diverse research is needed to provide a more accurate assessment of the consequences of human exposure to microplastics. Unfortunately, we already know that MPs have a negative impact on human health and are not benign. The impact of microplastics on human health is a topic of intensive research. Recent studies have clearly demonstrated the presence of microplastics of 20–100 μm in all tissues of the human body, among which the most common MPs were those of PVC origin [38].

The highest amount of microplastics was found in lung tissue, which is particularly exposed to the inhalation of small fragments of these pollutants from the air. Inhalation of microplastics poses a serious threat to respiratory health. These pollutants can cause inflammatory reactions, cause damage to lung tissue, and contribute to the development of chronic diseases [39].

Significant amounts of microplastics have also been discovered in the small intestine and colon. The presence of microplastics in these tissues is concerning for many reasons. First, the small and large intestines play a key role in the digestion and absorption of nutrients. Microplastic pollution can lead to disorders in the functioning of these organs, resulting in problems in the balance of water and electrolytes in the body, and its disruption can affect overall homeostasis [40].

The tonsils, which are an important element of the immune system, are largely exposed to MPs. Exposure to microplastics can affect the ability of the body to fight infection [41].

The presence of microplastics in the placenta is alarming because it can suggest that these contaminants can penetrate the developing foetus. Scientists have also noted that microplastics can enter the bloodstream through inhalation, ingestion, and even skin contact, suggesting that our exposure to these particles is widespread and constant. These findings indicate a potential threat to human health, as the presence of microplastics in the body can lead to unpredictable health effects, including inflammation and disruption of internal systems [42].

Microplastics and the intestinal barrier

Certain changes in the structure of microplastics also occur in the digestive tract of mammals. Both the transit time of particles and the retention time may vary and depend on the species and size of the microplastics [43, 44]. Data on the transit and retention of microplastics in humans are limited. However, Zhu et al. indicate that particles ranging in size from 20 to 100 μm were found in all tissues they examined, with the highest accumulation occurring in lung tissue [45]. Stock et al. studied the effect of digestion on the physicochemical properties of microplastics. The authors demonstrated the high resistance of the tested particles to artificial digestion [46]. Furthermore, Popa et al. present conclusions in their review paper that the toxic effects of microplastics remain after exposure to the digestive tract [47].

Structure of the intestinal barrier

The intestinal barrier consists of multiple layers. The outer layer consists of mucus, defence proteins such as anti-microbial proteins and secretory immunoglobulin A (sIgA), and the commensal intestinal microbiota, the middle layer consists of intestinal epithelial cells (IECs), while the inner layer consists of immune cells. All of these components are essential for maintaining the integrity of the intestinal barrier and protecting against pathogens [48].

The first line of defence against potentially harmful substances is the mucus layer. It is secreted mainly by goblet cells (GCs). GCs are divided into two types: ic-connecting crypt goblet cells (icGCs), which are located on the surface of the colon lumen and more closely resemble enterocytes, show expression of Muc17, Dmbt1, Hes1, among others. On the contrary, the second type are classic cup cells located in the lower crypt, showing expression of Muc2, Clca1, Fcgbp, among others [49]. CGs show the ability to absorb luminal antigens to cause an adaptive immune response. Some microorganisms attack CGs to enter the host organism [50]. Mucus is composed of water, lipids, electrolytes, proteins, and other substances. However, the main functional and structural components of mucus are mucins (MUC), which are high molecular weight glycoproteins; the main mucus glycoprotein is MUC2 [51]. The thickness of the mucus and the type of MUC vary according to the different sections of the gastrointestinal tract. However, in the large intestine, two layers are distinguished: the outer and inner [52]. The commensal gut microbiota is incorporated into the loose outer layer, while the inner layer excludes microorganisms [53].

Intestinal epithelial cells are divided into enterocytes, GC, enteroendocrine cells, Paneth cells (PC) and microfold cells. They can be renewed by a pool of stem cells located in intestinal crypts. Self-renewal of the intestinal epithelium can occur every 3 to 5 days [54]. Enterocytes belong to a group of absorptive cells. The function of enterocytes is divided into certain zones, located along the axis of the villi [55]. PCs secrete antimicrobial substances into the intestinal lumen (e.g. α-defensin, lysozyme (Lyz), crypt-like peptides, phospholipases), and show phagocytosis ability. When the Atg16L1 gene is mutated, PC function is impaired, intestinal barrier integrity is reduced, and therefore the predisposition to inflammatory bowel disease (IBD) increases [56, 57]. Enteroendocrine cells (EECs) are classified according to the hormone they produce. They secrete different hormones depending on their location. Examples of hormones secreted in the intestine by EECs are glucagon-like peptides 1 (GLP-1), peptide gradient YY (PYY) [58, 59]. EECs in the gut make up about 1% of the total intestinal epithelial cell population. EECs receive various types of stimuli, both dietary and non-food, via, for example, various types of receptor, sensory transporters. Additionally, EEC can be activated through transient receptor potential ankyrin A1 (Trpa1), as a result of the detection of intestinal bacteria, which can cause the activation of intestinal neurones [60, 61].

The inner layer of the intestinal barrier is composed of B cells, T cells, dendritic cells, macrophages, eosinophils, and others [62, 63]. They are responsible for protecting the body from harmful microorganisms or their pathogens. However, an abnormal and excessive inflammatory response is associated with a predisposition to intestinal inflammation. The gut microbiota also has an impact on the functional maturation of the immune system of the body [64].

One of the essential components of the intestinal barrier is tight junctions (TJ). These are transmembrane proteins consisting of occludin, claudin, tricellulin, junctional adhesion molecule-A (JAM-A), zonula occludens (ZO), and cingulin. The TJ pathways are mainly distinguished between two- and three-celled [65]. Their function includes sealing the intercellular space, regulating paracellular permeability, and maintaining the homeostasis of the intestinal epithelial layer [66].

The proper functioning of all components of the intestinal barrier is essential for the proper functioning of both the intestines and the entire body.

Effects of Microplastics (MPs) on the intestine barrier

MPs can be absorbed by the intestinal tract through endocytosis in enterocytes, paracellular uptake, or transcytosis by microfold cells [67]. In addition, DeLoid et al. indicated that MPs translocation across the intestinal barrier is possible through macropinocytosis, phagocytosis, various types of endocytosis mediated by, for example, caffeoles, clathrin-coated cavities, and endophilin [68].

The effects of MPs on the intestinal barrier are polymer specific. Polystyrene microplastic (PS-MPs) was observed to cause disruption in TJ by the ROS dependent NF-κB/NLRP3/MLCK pathway signaling [69]. In a study by Jin et al. in animal models, the researchers showed that exposure to polystyrene MP resulted in reduced mucus production and therefore a lower mucus layer, which was a consequence of a decrease in Muc1, Muc2, Muc3 [70]. PS-NP can increase Muc2 expression of Muc2 through the Ho1/p38/IL-10 axis, in turn, Muc2 shows the ability to reduce the intestinal toxicity of PS-NP [71]. In another study by Liang et al. the authors also confirmed that microplas-tics and nanoplastics reduced mucus and exacerbated intestinal barrier dysfunction through reactive oxygen species (ROS) mediated apoptosis of intestinal epithelial cells [72]. In their study, Li et al. observed that after 28 weeks of exposure to polystyrene nanoparticles (PS-NP), the mucus layer decreased in mice and intestinal epithelial cells eroded. Additionally, the number of villi and intestinal crypts decreased. Furthermore, levels of occludin, claudin-1, and ZO-1 were reduced in intestinal tissues after exposure to PS-NP. They also showed an increased proportion of.

B lymphocytes in the mesenteric lymph nodes (MLN) and a decrease in the percentage of T lymphocytes in intraepithelial lymphocytes (IEL) [73]. PS-MPs of 5 μm cause more severe TJ disruption than 1 μm particles [69]. Furthermore, microplastic exposure can alter the morphology of intestinal epithelial cells and affect the TJ complex by causing a decrease in the transcription level of TJ proteins [74]. When the TJ is damaged and/or ruptured, MP easily passes through the intestinal barrier and there is an accumulation of MP particles in various organs [75]. Huang et al. in their animal model study showed that MP, through an exosomal miR-126a-3p-dependent pathway, can alter intestinal barrier function through oxidative damage. Furthermore, Muc2 expression and mucus production decreased significantly after exposure to MP. Furthermore, TJ gene expression showed a significant decrease [76]. Another study showed that PS-NP can cause intestinal inflammation through activation of nuclear factor-kappa B/NOD-like receptor family pyrin domain containing 3 (NF-κB/NLRP3). In contrast, after damage to the intestinal barrier, the gut microbiota releases lipopolysaccharides (LPS) and the gut-hepatic axis is activated, predisposing to hepatitis [77]. In the study, Domenech et al. tested the long term effects of PS-NP on human Caco-2 cells. They observed over-expression of the HO1 and SOD2 genes after 8 weeks of exposure to PS-NP. They also note that the ageing of nanoplastic particles could alter their properties and change the absorption of environmental contaminants, which could consequently alter their toxicity [78].

Another study showed that plastic particles (< 100 nm) can penetrate the barrier of Caco-2 /HT29 colon adenocarcinoma cells (human cell line). Particles < 10 μm in size are moved across the intestinal barrier via transcytosis by M cells, while PVC particles (5–110 μm) were displaced by persorption [79]. A 60 day exposure to PVC MPs also increases intestinal barrier permeability in rodents and reduces the intestinal mucus layer [80]. In addition, the effect of benzo [ a ] pyrene (B ( a ) P) on PS-MP changes its physicochemical properties, activating the Notch signaling pathway causing damage to the intestinal mucosal bar-rier. There is an increase in intestinal permeability that can lead to translocation of intestinal bacteria [81].

Exposure to PP MPs can lead to activation of the TLR4/NF-κB pathway that induces inflammation and apoptosis of intestinal epithelial cells resulting in damage and dysfunction of the intestinal barrier [82].

Lv et al. evaluated the effect of dietary restrictions on the intestinal effects of PS-MP in mice. After a 5-week escrow, they observed that MP accumulation was high-er in mice with a food intake of 60%, compared to rodents with a normal diet. In addition, dietary restriction worsened the intestinal barrier dysfunction of MP-laden animals [83].

A summary of the effects of microplastics on the intestinal barrier is shown in Fig. 1.

Fig. 1.

Effects of microplastics on the intestinal barrier. The figure shows changes occurring in the intestinal epithelium after exposure to microplastics. Microplastics disrupt the integrity of the intestinal barrier by damaging tight junctions, destabilizing the mucus layer, and altering the intestinal microbiota. As a result, the protective and homeostatic functions of the intestinal epithelium are weakened

Recent multiomic analyses have shown that PS-NPs at environmentally relevant concentrations can disrupt intestinal homeostasis. These studies, integrating microbiota profiling, metabolomics, and transcriptomics, revealed changes in gut microbiota composition, metabolic pathways, and inflammatory responses induced by PS-NPs [84, 85].

The effect of MP on the intestinal microbiota

The diversity of the intestinal microbiota is influenced by a variety of individual and environmental factors, including smoking, engagement in physical activity, stress, sleep disorders, and the use of medications such as antibiotics. Other important factors are age, ethnicity, genetic factors, disease status, and diet. Exposure to microplastics in everyday life may represent an additional, emerging factor affecting the composition of the intestinal microbiota [86–88].

The intestinal microbiota is a complex ecosystem of microorganisms, consisting of over 250 species of viruses, bacteria, fungi and archaea. The main phyla of bacteria include Firmicutes, which belong to the classes Bacilli, Clostridia, and Negativicutes; Bacteroidetes, which include Bacteroidia, Flavobacteria, Cytophagian, Sphingobacteria, and Verrucomicrobia; Actinobacteria; Proteobacteria; and one archaea phylum, Euryarchaeota [89]. Recent data indicate that MP can cause changes in the bacterial community, triggering intestinal dysbiosis. As mentioned earlier, MPs can probably induce inflammation, increase intestinal permeability, and reduce the mucus layer in the intestinal epithelium [90]. Much of the scientific evidence that assesses the effects of MP exposure comes from animal model studies. However, it is believed that this knowledge may also be helpful in estimating potential exposure in humans. However, a major challenge in conducting research is the lack of standardised sampling techniques and the limited amount of data on the effects of chronic exposure [91]. MP-induced dysbiosis can lead to the growth of bacteria such as Firmicutes and Proteobacteria and a reduction in the number of Bacterioidetes and Actinobcteria (Fig. 2). It is likely that changes in the microbiota may lead to a number of immunological, structural and functional changes in the intestinal mucosa [90].

Fig. 2.

MPs have been shown to alter both the abundance and diversity of the intestinal microbiota. Current evidence indicates that exposure to MPs may promote the expansion of several bacterial groups, including Chlamydia, Firmicutes, Verrucomicrobia, and members of Proteobacteria. Conversely, reductions have been reported in taxa such as Bacteroidetes, Actinobacteria, and specific subclasses of Proteobacteria (α-, β-, and γI-Proteobacteria). These shifts in microbial composition are often associated with intestinal dysbiosis and may contribute to impaired intestinal barrier function. Exposure to MPs has been linked to increased intestinal permeability, disruption of TJ integrity, and the upregulation of immune and inflammatory pathways. Collectively, these alterations suggest that MPs can weaken mucosal defence mechanisms and promote a inflammation (based on [90])

Studies on animal model

Jing et al. will evaluate the effects of micro/nanoplastic (MNPKs) exposure on the hematopoietic system. They observed that dysbiosis may be one of the causes of damage to this system. The Chao1 index showed changes in abundance and the Shannon index showed changes in diversity. The analysis showed that MNPKs can strongly influence the diversity of intestinal microbiota, causing a decrease in Akkermansia and Bacteroidetes, Mucispirillum and Helicobacter. Particles with a diameter of 10 and 5 μm had a greater impact on diversity. In addition, a correlation was observed between changes in the microbiota and the concentration of pro-inflammatory cytokines Il-17 A, MIP-1beta (macrophage protein) and IL-12p70 [92]. Jin et al. reported a reduction in Actinobacteria and a decrease in intestinal mucus secretion after exposure to 5 μm polylistreins [70]. Lu et al.‘s observation showed that exposure to PS MPs reduced the relative abundance of Firmicutes and Proteobacteria in feces [93]. Oral exposure to 100-nm PS in honey bees resulted in decreased body weight and intestinal dysplasia. Changes in the microbiota included a reduction in the abundance of Lactobacillus and Bifidobacterium on days 10 and 15 of exposure, respectively [94]. In turn, Liu et al. showed a decrease in the number of Bacteroidetes and an increase in the number of Firmicutes, which was accompanied by an increase in the number of Lactobacillus and a decrease in the number of Parabacteroides [95]. Zhang et al. demonstrated that exposure to PS at medium doses (5000 nm) and high doses (20 nm) leads to changes in the diversity of the gut microbiota by reducing the ratio of Firmicutes to Bacteroidetes. Additionally, changes in the microbiota were associated with abnormal metabolism of short-chain fatty acids. Long-term exposure to smaller-sized PS-MNPs may possibly reduce SCFA levels, although initially the opposite effect was observed due to stress-induced metabolic activity of the gut microbiota, which led to a short-term increase in SCFAs. It could probably be influenced by the initial growth of Lachnospiraceae and Clostridia [96].

Current research findings regarding the impact of MPs on the composition of the gut microbiota are ambiguous. This includes the phylum Firmicutes, whose levels have shown both increases and decreases in various studies. The previously mentioned systematic review by Souza-Silva et al. [90] reported an increase in Firmicutes; however, the included studies were highly heterogeneous. The doses used and exposure times of microplastics varied across the analyzed studies. Furthermore, not all authors provided data on microplastic shape. Therefore, the results should be interpreted with caution, as methodological inconsistencies significantly hinder comparisons between studies and the formulation of clear conclusions.

Studies involving human participants

The study by Zhang et al. assessed the level of exposure to MPs among people working in a plastic factory and those living in nearby areas. A significant presence of polyurethane was demonstrated in intestinal secretions in people in the high exposure group. Exposure to MPs was associated with an increase in overall gut microbiota abundance which has been linked to gastrointestinal diseases as well as a decrease in beneficial bacterial populations. At the phylum level, Bacteroidetes and Firmicutes were the dominant strains in the gut microbiota. The relative abundance of Bifidobacterium, Streptococcus, and Sphingomonas in the high-exposure group was significantly lower than in the low exposure group. However, the study included only 20 participants from a single Asian center, which limits the robustness and generalizability of the findings [97]. Interesting observations were recently made by Liu et al. They compared the composition of microorganisms in mother-child pairs, analysing the microbiota of the placenta and the composition of microorganisms in the meconium of newborns. The diversity of placental and meconium microflora was mainly associated with 3 phyla: Proteobacteria, Bacteroidetes, and Firmicutes, and was related to exposure to MPs and the size of the particles. The main types of MPs identified were polamide and polyurethane (PU), although negative associations were also observed between ethylene vinyl acetate copolymer and Parabacteroides in the meconium and placenta, and PE and Bacteroides in the placenta. It should be noted that this study was also characterized by a small sample size [98]. Nugrahapraja et al. showed for an Indonesian population that exposure to PS caused a reduction in the relative abundance of Clostridium and Roseburia, and HDPE, a PE derivative, caused a reduction in the relative abundance of Bacteroides. However, these changes were not significant, probably because the contamination threshold was not too high [99]. Zha et al. made interesting observations when assessing changes in the microbiota in people eating takeaway meals from plastic boxes. It turned out that exposure to MNPs from plastic packaging can contribute to changes not only in the intestinal microbiota but also in the oral cavity. People who ate these meals more often had higher levels of Collinsella in the intestines, while people who occasionally used this method of food storage had higher levels of Faecalibacterium. Furthermore, the authors indicate that partial reduction of the size and quantity of MNPs cannot repair MNP-induced dysbiosis [100].

The current epidemiological evidence regarding MPs on gut microbiota, based on the cited human studies, should be interpreted with caution due to their significant methodological limitations, such as small sample size and limited geographical representation (predominance of Asian populations).

Microplastics vs. intestinal diseases

Microplastic is ubiquitous in food and drinking water. Consequently, consciously or not, smaller or larger amounts of it are inevitably consumed. This can cause potential health risks. In particular, an increase in the incidence of cancer, immune disorders, lung disease, cardiovascular disease, intestinal disease, or even risks to pregnant women [67]. Recent analysis has shown that in Taiwan over the past 10 years, the incidence of UC has increased more than 1.5 times. Importantly, the staple diet of people living there is seafood from polluted waters. A link is suggested between the increase in IBD and the prevalence and pollution of microplastics [101]. Zhang et al. in their study using spectrometry, showed that microplastic is found in both adult and infant feces. The authors of the study noted that infants are at high exposure to microplastic due to the chews, bottles and toys they use. This shows that people are already in contact with plastic from birth [102]. In turn, Ibrahim et al. detected microplastic in the human colon through colectomy sampling [40]. Importantly, 15 types of microplastic were detected in the feces, although PET and polyamide were found the most. In addition, the study found that patients with IBD have significantly higher concentrations of microplastic compared to a group of healthy individuals. It has been hypothesized that microplastic exposure may positively correlate with the onset of disease, or that disease may increase microplastic retention [103]. Moreover, another study confirms this suspicion. Mice that were exposed to sodium sulfate through which colitis was induced were analyzed. The administration of water that contained polystyrene nanoparticles (PS-NPs) exacerbated colitis through the mitogen-activated protein kinase (MAPK) signaling pathway. In addition, PS-NPs were found to increase oxidative stress, but also impaired lipid metabolism in the liver [104]. In turn, another in vitro study similarly showed that several types of plastic could significantly affect the inhibition of lipid digestion. These types of plastic included PS, PE, PET, polyvinyl chloride, and poly(lactic-co-glycolic acid). The analysis found that the higher the concentration of PS, the lower the lipid digestion. In addition, the authors suggest that this is due to the plastic’s effect on reducing the bioavailability of lipid droplets. This appears to happen through mechanisms such as the formation of lipid-microplastic heteroaggregates, alteration of the enzyme structure and lipase adsorption. Ultimately, reduced lipid digestion can negatively affect health [105]. In their study, Lamprecht et al. created a mouse model of IBD and then exposed them to PS particles. Compared to the control group, the IBD mice showed increased PS concentrations in the ulcerated areas, but also in the mucus layer. In addition, the adhesion of PS particles was increased in the colon tissue of mice with IBD. Importantly, we found that the smaller the PS particles, the more the deposition of PS in the colon increased [106]. In another study on mice, where they were fed three types of PS, that is, PS, PS-COOH and PS-NH2, they were found to induce similar clinical features to Crohn’s disease (CD), where the ileum is involved. Necroptosis of intestinal epithelial cells, induction of pro-inflammatory cytokines and impairment of intestinal structure were demonstrated [107]. In another study, the effects of PS at a dose of 2.3 mg/kg/day were analyzed in healthy mice and patients with colitis. In the group of healthy mice, PS caused an increase in sulfated mucins in cup cells, an increase in endocrine cells and a decrease in the proportion of macrophages. In contrast, in the group with colitis, it caused an intensification of colitis. This inflammation was characterized by an increase in inflammation and an increase in the frequency of ulcers, but also by a decrease in mucins in the cup cells. It seems that exposure to PS particles can lead to a more severe course of intestinal inflammation [108]. In addition to this study, there are few that examine the effects of MPs on the course and symptoms of artificially induced colitis. However, they all mention the consequences of exposure, which include increased structural damage to the intestine, increased inflammation and permeability of the colon, inhibition of mucus secretion, shortening of the colon, but also promotion of hepatic disorders [109–111]. Liu et al. in their study on mice in which they artificially induced acute colitis via DSS, showed that PS increased the storm of pro-inflammatory cytokines, i.e. tumor necrosis factor-alpha (TNF-α), interleukin-1 beta (IL-1β) and interferon-gamma (IFN-γ) [112]. Another study showed that PS-NPs can promote duodenal damage in mice with artificially induced intestinal inflammation. In addition, they showed increased intestinal permeability and reactive oxygen species (ROS), but also NF-κB expression [113]. Animal studies provide the primary evidence base for the effects of MPs on the gut and related diseases. However, interspecies differences must be taken into account when analyzing these studies. These include changes in the microbiota, xenobiotic metabolism, and the intestinal barrier.

Herrala et al. showed that PE particles can affect human colon cancer cells. They found that PE can reduce cell viability and induce oxidative stress, mainly promoting mitochondrial superoxide [114]. In addition, plastic particles smaller than 1 μm can cause cell movement. Which could potentially induce metastasis and thus disease progression [115]. Recently, attention has been drawn to an increase in the incidence of early-onset colorectal cancer, that is, before the age of 50. It has been suggested that the environmental factor of microplastic proliferation has influenced the development of this disease. It is possible that by damaging the integrity of the colonic mucosal barrier, MPs contributes to the impairment of its protective function [116]. Tamargo et al. showed that microplastic, by affecting the gut microbiota, can induce intestinal diseases [117]. In addition, symptoms of intestinal microplastic toxicity appear to include diarrhea, abdominal pain, blood in the stool, fatigue, decreased appetite, but also weight loss [67].

Recently, Fournier et al. demonstrated in vitro that the effect of MPs on the human digestive ecosystem causes an increase in the number of potentially harmful pathogens and a decrease in the number of beneficial bacteria, such as Christensenellaceae and Akkermansiaceae [118]. In addition, phthalates and bisphenols have been shown to disrupt hormonal activity and glucocorticoid metabolism. Ultimately, this may be linked to the pathogenesis of IBD [119].Damage to the mucosa by nanoplastics is associated with numerous negative effects. These include genotoxicity, cytotoxicity, and inflammation. The internalisation of MPs can activate immune processes, inducing proinflammatory cytokines such as IL-6 and TNF-α. This, in turn, leads to increased inflammation and cellular damage. ROS can contribute to the severity of cellular damage, causing damage to cellular macromolecules, including proteins, lipids, and DNA. ROS also exacerbate and perpetuate intestinal dysbiosis. These processes may lead to cell death. These alterations are implicated in the development of IBD [120].

Conclusions

The increase in global plastic production has many negative effects on both the environment and human health. Plastics production generates large amounts of waste, including microplastics, which can contribute to an increased risk of inflammatory bowel disease. Microplastics can be absorbed by the body through various mechanisms in the intestinal barrier, leading to accumulation of their particles in both the intestines and various organs. The direct effect of MPs on the intestinal barrier can cause loss of function of tight junction proteins, reduction of mucus, and apoptosis of intestinal epithelial cells, resulting in easier entry of MPs and pathogenic microorganisms into the body. However, the actual extent of human exposure to the environment is still unknown due to discrepancies in the methodology of the available studies. Therefore, the establishment of standardised and harmonised sampling and processing methods is crucial to enabling meaningful comparisons of data from different studies. The findings and studies underscore the urgent need for further research into the sources and effects of exposure to plastic microplastics. Implementing measures to reduce microplastic emissions and increasing public awareness of the problem is critical to protecting public health. In the context of global plastic microplastic pollution, understanding the mechanisms of their transport and accumulation in the human body and developing strategies to minimise exposure is not only a scientific challenge, but also a global health priority.

Authors’ contributions

Conceptualization, S.J.-C. and R.F writing—original draft preparation, S.J-C., A.S.-D., K.F., D.W.; writing—review and editing, S.J.-C., A.S.-D., K.F., D.W., R.F.; visualization, S.J-C., A.S.-D.; supervision, R.F.

Funding

No funding was received for this article.

Data availability

No datasets were generated or analysed during the current study.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.