Effects of the chronic exposure to cerium dioxide nanoparticles in Oncorhynchus mykiss: Assessment of oxidative stress, neurotoxicity and histological alterations (2024)

Introduction

Nanotechnology is a growing science based on the application and production of equipment and/or material at a nanometer scale ranging from 1 μm to 1 nm (Park et al., 2007). Nanoparticles (NPs) are chemical compounds with small dimensions, usually less than 100 nm (Ju-Nam and Lead, 2008; Felix et al., 2013). Nanoparticles, due to their small size, have improved physicochemical properties compared to larger particles of the same substance. Among these improved properties, once can identify among others, better optical behavior and enhanced chemical reactivity (Ju-Nam and Lead, 2008; Gaiser et al., 2012; Xia et al., 2013). Given their versatility, NPs are currently used in domestic products, foods, sunscreens, medicine, optical equipment, cosmetics, textiles, bioremediation processes, paints and electronics production (Handy and Shaw, 2007; Gaiser et al., 2009; Dahle and Arai, 2015). One of the most common NPs in use at present is composed of cerium dioxide (CeO2-NPs). Also called nanoceria, CeO2-NPs are used as a fuel additive, as a catalyst in petroleum refining, as a semiconductor, and as an absorber of UV radiation in sun lotion (Park et al., 2008a,b; Cassee et al., 2011; Dahle and Arai, 2015). CeO2-NPs, like many others, are also used for pharmaceutical purposes (Dahle and Arai, 2015). Cerium (Ce) is the most abundant of rare-earth metals found in the Earth’s crust (Dahle and Arai, 2015). Thus, it is one of the most viable and valuable NPs that exists today (Hedrick, 2004; Wang et al., 2008; Xia et al., 2013). Because of their widespread use, CeO2-NPs can be dispersed into the environment, especially in the aquatic compartment, causing putative changes in aquatic organisms (Gaiser et al., 2009).

The growing increase in the use of NPs (and nanomaterials in general) by the industry has led to an increasing concern about the potential impact of NPs on human health and in the environment (Dreher, 2004; Xia et al., 2013). However, despite their extensive use, some critical aspects of NPs are still largely unknown. Some studies in the areas of human toxicology and ecotoxicology of NPs have been developed. Even so, this amount of data is still insufficient to understand the long-term effects of NPs in organisms, mostly aquatic. Among the effects caused by NPs, the alterations in the structure and function of cells and tissues, and in the activity of specific key enzymes, should be further investigated and discussed. The existent literature suggests that CeO2-NPs can elicit antagonistic responses in biological systems. In some case, it can have benefit but also harmful effects in biota (Tarnuzzer et al., 2005; Schubert et al., 2006; Heckert et al., 2008; Park et al., 2008a,b; Nalabotu et al., 2011; Arnold et al., 2013; Xia et al., 2013). One of the beneficial effects of NPs is related with their antioxidant activity, which can act against reactive oxygen species and free radicals (Heckert et al., 2008; Lee et al., 2013). NPs can also protect normal cells against the injury caused by radiation, in case of anticancer treatments (Tarnuzzer et al., 2005). On the contrary, other studies showed harmful effects in human lung epithelial cells, and liver damage in a chronical exposure in rats (Park et al., 2008a,b). It has been proposed that the metabolism of NPs is probably accomplished by a hepatic route, by excretion into the bile, which seems to be a more likely mechanism instead of renal or branchial excretion (Handy et al., 2008; Dahle and Arai, 2015). Despite these indications of mechanistic nature, only a few studies with aquatic organisms exposed to CeO2-NPs have been published so far. Among these, CeO2-NPs elicited genotoxic effects in Daphnia magna (Lee et al., 2009), caused growth inhibitory effects in Pseudokirchneriella subcapitata (Hoecke et al., 2009), significant increases in single-strand DNA breaks, lipid peroxidation and superoxide dismutase activity in Corophium volutator (Dogra et al., 2016), and simultaneously reduced the immunotoxic potential and increased mortality in Oncorhynchus mykiss (Gagnon et al., 2018).

Some metal oxides NPs can disrupt the biochemical balance of living organisms, leading to adaptive responses, measurable by biomarkers that are based on compromised biochemical processes due to xenobiotic exposure. These biomarkers can represent the health status of the biota and early-warning signs of environmental threats (Xia et al., 2013). Large varieties of substances that cause oxidative stress in aquatic species were already found in water (Valavanidis et al., 2006; Ray et al., 2012). Oxidative stress is defined as an imbalance between the production of reactive oxygen species (ROS) during the oxidative metabolism in mitochondria and cellular antioxidant defenses (Betteridge, 2000). It is related with the increase in the production of oxidant species, or with the significant decrease in the efficiency of the antioxidant defenses (Schafer and Buettner, 2001). Some examples of biomarkers involved in the antioxidant response are glutathione S-transferases (GSTs) and catalase (CAT) (Depledge and Fossi, 1994; Timbrell, 1998). GSTs are a set of enzymes that lead to the conjugation of glutathione with diverse compounds with electrophilic centers, helping their excretion (Modesto and Martinez, 2010). CAT is also important for the defense of the organism against oxidative damage (Rahman, 2007). This enzyme is part of the antioxidant defense system that exists in peroxisomes (Modesto and Martinez, 2010), and its primary function is the reduction of hydrogen peroxide, produced from the metabolism of fatty acids (Xia et al., 2013), into water and molecular oxygen (Aebi, 1984). Among all cholinesterases, AChE is a biomarker of neurotoxicity, since it hydrolyses the neurotransmitter acetylcholine into choline and acetate (Tripathi and Srivastava, 2008), mainly at the central nervous system of living organisms. Thus, the proper function of the nervous systems depends on the activity of this enzyme, which is concentrated at the neuromuscular and cholinergic synapses (Chung and Bieber, 1993; Bajgar and Herink, 1997; Tripathi and Srivastava, 2008). Furthermore, a severe oxidative stress can cause tissue alterations, trigger apoptosis and induce injured cell death (necrosis) (Lennon et al., 1991; Limón-Pacheco and Gonsebatt, 2009; Rodrigues et al., 2017). Tissue alterations are usually observed in two main fish organs: the gills, because of their extensive surface and superficial location, being in constant contact with the pollutant agents, and the liver which is responsible for the excretion and metabolism of the contaminants (Bucher and Hofer, 1993; Jobling and Sumpter, 1993; Camargo and Martinez, 2007). To face such environmental stressors, including NPs, fish show adaptive changes, through impairment of biochemical and structural traits in cells and tissues, which may be monitored by using a biomarker approach (Van der Oost et al., 2003).

Based on previous studies, nanoparticles are able to interact with living systems leading to deleterious conditions and effects, including oxidative stress (Manke et al., 2013). Moreover it has recently shown that CeO2-NPs could be involved in the exertion of oxidative stress scenarios (Dogra et al., 2016). In addition, physical interference resulting in inhibition of AChE activity was already reported to occur after exposure to several types of nanoparticles (Wang et al., 2009). Furthermore, histopathological effects were already reported in fish cells and tissues as results of exposure and up-take of waterborne metallic NPs (Gaiser et al., 2009; Al-Bairuty et al., 2013).

The main goal of this work was to evaluate the toxic effects in rainbow trout resulting from a chronic exposure (28 days) to ecologically relevant amounts of CeO2-NPs by measuring the oxidative stress response (determination of the activity of the enzymes GSTs and CAT in the liver and gills), neurotoxicity (determination of the activity of AChE in the eyes) and histopathological (gills and liver tissue alterations) biomarkers. According to the existent knowledge, the here-proposed toxicological parameters seem suitable to diagnose the exposure of fish to environmentally relevant levels of NPs, namely CeO2-NPs.

Section snippets

Chemicals

Cerium (IV) oxide nanopowder (CeO2-NP) used in this study was acquired from Sigma-Aldrich (Schnelldorf, Germany) with a degree of purity of 99.95% and size under 50 nm (CeO2-NP; CAS number 1306-38-3). Exposure media were prepared by successive dispersion of the stock solution (10 mg/L) in dechlorinated tap water. Hydrogen peroxide (H2O2; CAS: 7722-84-1), reduced glutathione (GSH; CAS: 70-18-8), 1-chloro-2,4-dinitrobenzene (CDNB; CAS: 97-00-7), acetylthiocholine iodide (CAS: 1866-15-5), 5,5

Glutathione S-transferases

GSTs activity in liver showed no significant differences among the experimental groups (One-Way ANOVAs: F3,56 = 2.192, p = 0.101) (Fig. 1A). However, GSTs activity in gills was significantly different among exposure groups (One-Way ANOVA: F3,56 = 3.563, P = 0.021), being highest in the group exposed to the maximum concentration of CeO2-NPs (Dunnett test, p < 0.05) (Fig. 1B).

Catalase

The liver catalase activity showed to be significantly increased (One-Way ANOVA: F3,56 = 3.818, P = 0.015; Dunnett’ test:

Discussion

This study was conducted with the primary goal of understanding the potential impacts of chronic exposure of CeO2-NPs on the freshwater fish rainbow trout. The number of studies about the toxicity of CeO2-NPs in aquatic species is scarce, and none was so far performed with rainbow trout, as far as it is known. Given the potential toxicity of such NPs and the absence of toxicity data for freshwater fish species, it seems important that overviews of long-terms, ecologically realistic assessments

Conclusions

This study provided the first evidences of the long-term effects of CeO2-NPs, in terms of pathological and physiological effects in rainbow trout. Fish subjected to chronical exposure to these NPs evidenced alterations of minimal or moderate pathological importance in the liver and also of marked pathological importance in the gills. The analyses of the enzymatic activity of GSTs identified a significant metabolic response in gills of fish exposed to the higher tested level of NPs. The absence

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.

Acknowledgements

This research was supported by CIIMAR and CESAM through the Strategic Funding UID/Multi/04423/2013 and UID/AMB/50017-POCI-01-0145-FEDER-007638, respectively through national funds provided by FCT – Foundation for Science and Technology (PIDDAC) and European Regional Development Fund (ERDF), in the framework of the programme PT2020. Bruno Nunes was hired through the Investigator FCT program (IF/01744/2013). A special thanks to Miriam Babic and Céu Costa for the fish maintenance and histological

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Effects of the chronic exposure to cerium dioxide nanoparticles in Oncorhynchus mykiss: Assessment of oxidative stress, neurotoxicity and histological alterations (2024)

FAQs

Is cerium oxide nanoparticles toxic? ›

Studies have shown CeO2-NP to be toxic to cancer cells, inhibit invasion, and sensitize cancer cells to radiation therapy.

Is cerium oxide toxic? ›

Cerium Compounds: Cerium compounds are mildly to moderately toxic, depending on the particular compound. In an animal study, cerium carbonate, cerium fluoride, and cerium oxide were not found to be acutely toxic, showed no signs of dermal irritation, and were minimally irritating to eyes.

Is cerium oxide toxic to fish? ›

Abstract. Metal oxide nanomaterials can cause oxidative, cardiorespiratory, and osmoregulatory stress in freshwater fish.

What are the most harmful nanoparticles? ›

Our results indicate that, out of all nanoparticles studied, Copper- and Zinc-based nanomaterials present the highest toxicity, whatever their oxidation status.

What are the toxic effects of nanoparticles? ›

Materials which by themselves are not very harmful could be toxic if they are inhaled in the form of nanoparticles. The effects of inhaled nanoparticles in the body may include lung inflammation and heart problems.

What does cerium do to the body? ›

Cerium is mostly dangerous in the working environment, due to the fact that damps and gasses can be inhaled with air. This can cause lung embolisms, especially during long-term exposure. Cerium can be a threat to the liver when it accumulates in the human body.

What are the disadvantages of cerium oxide? ›

Many uses of cerium oxide nanoparticles result in the particle making their way into nature, which increases the odds of exposure, potential health effects, and ecological implications.

What are the protective effects of cerium oxide nanoparticles? ›

Conclusions: Our finding revealed that CeO2 NPs has potential protective effects by increasing antioxidant activity, and reducing inflammation.

What is the toxicity level of cerium? ›

It was further divided by 10 due to their short test period, and outcome of 0.0089 mg/m3 was deemed to be the lowest reliable concentration without any effect. Finally, it was converted to 0.0072 mg/m3 for cerium as its 'non-toxic level*'.

What products contain cerium oxide? ›

Face
  • Face.
  • Blush.
  • Primer.
  • Remover.
  • Eyes.
  • Brow Liner.
  • Lips.
  • Lip Balm.

Is cerium oxide radioactive? ›

Cerium(IV) oxide is a powerful oxidizing agent at high temperatures and will react with combustible organic materials. While cerium is not radioactive, the impure commercial grade may contain traces of thorium, which is radioactive. Cerium serves no known biological function.

How do you get rid of nanoparticles in your body? ›

Even insoluble nanoparticles which reach the finely branched alveoli in the lungs can be removed by macrophage cells engulfing them and carrying them out to the mucus, but only 20 to 30 per cent of them are cleared in this way. Nanoparticles in the blood can also be filtered out by the kidneys and excreted in urine.

How long do nanoparticles stay in the body? ›

The blood half-lives of the various iron oxide nanoparticles currently in clinical use vary from 1 h to 24-36 h [69]. However, specific biodistribution and clearance parameters depend on particle properties such as surface characteristics, shape, and size [71].

What cells can nanoparticles cause damage to? ›

Summary: New research by scientists shows that when cellular barriers are exposed to metal nanoparticles, cellular messengers are released that may cause damage to the DNA of developing brain cells.

What is the risk of nanoparticles in the brain? ›

Exposure to silica nanoparticles results in neurotoxic effects, whereas very low levels increase the oxidative stress and alter the microglial function, with a highly negative impact on the striatum and dopaminergic neurons [94].

What are the examples of nanotechnology in human health? ›

Nanotechnology is evolving rapidly in industrial applications, medical imaging, disease diagnosis, drug delivery, cancer treatment, and gene therapy, and also to aid in visual imaging.

What are the nanotechnology in the human body? ›

They are small enough to enter the body, travel around, enter the cells and interact with DNA and proteins. Some examples of nano-devices or nano-implants are the so-called smart pills, organ replace- ments, neural interfaces, and brain implants.

What is an unusual fact about cerium? ›

It can decompose slowly in cold water, and very rapidly in hot water. The metal can be attacked by alkaline solutions, dilute and concentrate acids. When scratched with a knife, the pure metal of cerium may ignite. Cerium is one of the most abundant of the rare-earth metals.

What chemical is named after a goddess? ›

Vanadium owes its name to these colours: it was named for the Scandinavian goddess of beauty and fertility, Vanadís (Freyja) because those names were originally given to several of the delightful colours adopted by vanadium-containing compounds.

What are 2 common uses for cerium? ›

It is used as a pigment. Cerium is also used in flat-screen TVs, low-energy light bulbs and floodlights. Cerium has no known biological role. Cerium is the most abundant of the lanthanides.

Is cerium oxide effective? ›

Reduced cerium oxide has been shown to be a highly efficient and durable second-generation high-temperature desulfurization sorbent. During the sulfidation phase of the cycle, H2S concentration was reduced to near 1 ppmv at a temperature of 700°C.

What is anticancer activity of cerium oxide nanoparticles? ›

Cerium oxide nanoparticles are associated with anticancer effects. While protecting normal cells, these nanoparticles exert their anticancer effects via oxidative stress and apoptosis in the cancer cells.

What are the applications of cerium oxide nanoparticles? ›

Cerium oxide is considered to be a lanthanide metal oxide and is used as an ultraviolet absorber [2], [3], catalyst [4], [5], polishing agent, gas sensors etc [6], [7], [8], [9], [10]. For commercial purpose, nanoceria plays a vital role in cosmetic products, consumer products, instruments and high technology.

What is the effect of copper oxide nanoparticles? ›

Copper oxide nanoparticles (CuO-NPs) have shown a strong antimicrobial activity against a wide range of microbial pathogens, some of which can be found in water (Abboud et al., 2014). CuO-NPs can be synthesized from algae.

What is the most common oxidation states of cerium CE )? ›

Hence, the most common oxidation states of cerium are +3 and +4.

What are the safety precautions for cerium oxide? ›

Precautionary statement(s) P261 Avoid breathing dust/ fume/ gas/ mist/ vapours/ spray. P264 Wash skin thoroughly after handling. P271 Use only outdoors or in a well-ventilated area. P280 Wear protective gloves/ eye protection/ face protection.

What minerals contain cerium? ›

Cerium chiefly is obtained from cerium-rich monazite and bastnasite. It also is found in allanite, cerite, samarskite and the titanium mineral perovskite.

Where is cerium found in the human body? ›

Cerium can be found primarily in blood, cerebrospinal fluid (CSF), saliva, and urine. Cerium is a chemical element with symbol Ce and atomic number 58.

What is cerium oxide in medicine? ›

Cerium oxide nanoparticle (CONP) has adaptable redox properties and can modulate reactive oxygen species for multiple pathological conditions and at various stages of disease development and progression (A). Several factors can dictate the redox activity of CONP.

What are cerium oxide nanoparticles? ›

Cerium oxide nanoparticles, nanoceria, are inorganic antioxidants that have catalytic activities which mimic those of the neuroprotective enzymes SOD and catalase. Kong et al.87 have shown that nanoceria preserves retinal morphology and prevents loss of retinal function in a rat light damage model.

What are the advantages of cerium oxide nanoparticles? ›

Cerium oxide is capable of scavenging gaseous free radicals that is nitric oxide, which is found in the living cells and these nanoparticles have the ability to interchange between the Ce3+ and Ce4+ redox states which is provided by the substantial oxygen storage capacity in their structure.

Where is cerium oxide used? ›

Cerium oxides are used as adsorbents, impetuses, vaporous sensors, and radiants. THE capacity of adsorption in oxides of ceria depends upon variables such as morphology, size, shape, and surface area (Yu et al., 2017). Nanoscale ceria has some interesting properties like blue color change during the adsorption process.

What are the properties of cerium oxide nanoparticles? ›

These particles are called nanoparticles, and they exhibit unique electronic, optical, magnetic, and mechanical properties, which make them different from the bulk material. These properties of nanomaterials help them to find a variety of applications in the biomedical, agricultural, and environmental domains.

Is cerium toxic to humans? ›

Cerium is mostly dangerous in the working environment, due to the fact that damps and gasses can be inhaled with air. This can cause lung embolisms, especially during long-term exposure. Cerium can be a threat to the liver when it accumulates in the human body.

How do you know if a nanoparticle is toxic? ›

Mechanisms of Nanoparticle Toxicity. The toxicity of NPs is largely determined by their physical and chemical characteristics, such as their size, shape, specific surface area, surface charge, catalytic activity, and the presence or absence of a shell and active groups on the surface.

Are carbon nanoparticles toxic? ›

It is believed that the toxic effects depend primarily on the CNTs' functionalization methods and the types of nanotubes present. One of the in vivo studies showed that properly functionalized CNTs were non-toxic to animals, whereas pristine CNTs were hazardous to the lungs of mice.

Are metal nanoparticles toxic? ›

The Liver And Metallic Nanoparticles Toxicity

Previous in vivo studies have shown that different types of MNPs: nano-metal monomers and nano-metal oxides, tend to deposit in the liver with extensive toxic effects. As shown in Table 1, MNPs entering the body cause changes in inflammatory cytokines.

What does cerium do in the human body? ›

Cerium has no known biological role in humans but is not particularly toxic, except with intense or continued exposure.

What neurological disease might arise from nanoparticle inhalation? ›

In the latter case, gold nanoparticles might cause three types of severe neurological pathologies: astrogliosis, also known as reactive astrocytosis, characterized by an increased number of astrocytes that is caused by the death of adjacent neurons, which leads to scar formation and the inhibition of axon regeneration, ...

How long do nanoparticles stay in your system? ›

The blood half-lives of the various iron oxide nanoparticles currently in clinical use vary from 1 h to 24-36 h [69]. However, specific biodistribution and clearance parameters depend on particle properties such as surface characteristics, shape, and size [71].

Can nanoparticles cause cell damage? ›

The addition of different types of nanoparticles to various primary cell cultures or transformed cell lines may result in cell death or other toxicological outcomes, depending on the size of the nanomaterial.

Can nanoparticles cause cell death? ›

Specifically, the nanoparticles were found to drive cell death through lipid peroxidation leading to proteotoxicity and necrotic cell death, whereas Ag+ ions increased cellular hydrogen peroxide levels leading to oxidative stress and apoptotic cell death.

Why are people worried about nanoparticles? ›

Many held a common belief that nanoparticles may have a higher risk of toxicity compared to larger particles, due to its higher chemical reactivity and biological activity. These nanoscopic particles can enter the body through inhalation, ingestion and dermal penetration because of the small size of these substances.

Can nanoparticles damage DNA? ›

Since it is now known that the nanoparticles induce DNA damage in several ways, it becomes crucial to understand how these NPs interact with the DNA and its associated set of proteins to hinder the repair mechanism and cause DNA damage finally.

What is the danger of silver nanoparticles? ›

Silver nanoparticles may be absorbed through the lungs, intestine, and through the skin into circulation and thus may reach such organs as the liver, kidney, spleen, brain, heart and testes. Nanosilver may cause mild eyes and skin irritations. It can also act as a mild skin allergen.

Are nanoparticles carcinogenic? ›

Copper-oxide nanoparticles

Elevated oxidative stress may lead to DNA damage, which in turn has the potential for carcinogenesis.

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