Skip to main content
Download PDF

Aquatic assessment of the chelating ability of Silica-stabilized magnetite nanocomposite to lead nitrate toxicity with emphasis to their impact on hepatorenal, oxidative stress, genotoxicity, histopathological, and bioaccumulation parameters in Oreochromis niloticus and Clarias gariepinus

BMC Veterinary Research volume 20, Article number: 262 (2024) Cite this article

Abstract

Background

In recent years, anthropogenic activities have released heavy metals and polluted the aquatic environment. This study investigated the ability of the silica-stabilized magnetite (Si-M) nanocomposite materials to dispose of lead nitrate (Pb(NO3)2) toxicity in Nile tilapia and African catfish.

Results

Preliminary toxicity tests were conducted and determined the median lethal concentration (LC50) of lead nitrate (Pb(NO3)2) to Nile tilapia and African catfish to be 5 mg/l. The sublethal concentration, equivalent to 1/20 of the 96-hour LC50 Pb(NO3)2, was selected for our experiment. Fish of each species were divided into four duplicated groups. The first group served as the control negative group, while the second group (Pb group) was exposed to 0.25 mg/l Pb(NO3)2 (1/20 of the 96-hour LC50). The third group (Si-MNPs) was exposed to silica-stabilized magnetite nanoparticles at a concentration of 1 mg/l, and the fourth group (Pb + Si-MNPs) was exposed simultaneously to Pb(NO3)2 and Si-MNPs at the same concentrations as the second and third groups. Throughout the experimental period, no mortalities or abnormal clinical observations were recorded in any of the treated groups, except for melanosis and abnormal nervous behavior observed in some fish in the Pb group. After three weeks of sublethal exposure, we analyzed hepatorenal indices, oxidative stress parameters, and genotoxicity. Values of alkaline phosphatase (ALP), gamma-glutamyl transferase (GGT), urea, and creatinine were significantly higher in the Pb-intoxicated groups compared to the control and Pb + Si-MNPs groups in both fish species. Oxidative stress parameters showed a significant decrease in reduced glutathione (GSH) concentration, along with a significant increase in malondialdehyde (MDA) and protein carbonyl content (PCC) concentrations, as well as DNA fragmentation percentage in the Pb group. However, these values were nearly restored to control levels in the Pb + Si-MNPs groups. High lead accumulation was observed in the liver and gills of the Pb group, with the least accumulation in the muscles of tilapia and catfish in the Pb + Si-MNPs group. Histopathological analysis of tissue samples from Pb-exposed groups of tilapia and catfish revealed brain vacuolation, gill fusion, hyperplasia, and marked hepatocellular and renal necrosis, contrasting with Pb + Si-MNP group, which appeared to have an apparently normal tissue structure.

Conclusions

Our results demonstrate that Si-MNPs are safe and effective aqueous additives in reducing the toxic effects of Pb (NO3)2 on fish tissue through the lead-chelating ability of Si-MNPs in water before being absorbed by fish.

Peer Review reports

Introduction

Heavy metals pose a significant global hazard to living organisms due to their inherent persistence, non-biodegradability, and bioaccumulation ability [1]. Anthropogenic activities have recently released these contaminants, polluting the aquatic environment [2]. Elements like mercury (Hg), cadmium (Cd), lead (Pb), and arsenic (As) have particularly detrimental effects on ecosystems, raising serious environmental and public health concerns [3, 4]. There is a risk that they may disrupt the natural balance of aquatic and terrestrial habitats, potentially leading to the decline or extinction of certain species. Furthermore, these metals accumulate in various fish tissues and muscles, posing potential public health threats to both fish and consumers through biomagnification [5,6,7,8].

Lead represents about 0.002% of the earth’s crust, a non-disintegrable heavy metal with no nutritional value [9]. However, many studies reported neurological, reproductive, immunological, gastrointestinal, and histochemical effects caused by lead intoxication in different animal species [10,11,12].

Nanotechnology offers a broad range of potential applications in aquaculture, including water purification and filtration using adsorption techniques. These methods have been utilized to remove and remediate water-borne toxicity caused by heavy metal ions in aqueous media [13,14,15]. Additionally, nanotechnology aids in preventing and managing fish diseases, thereby enhancing fish growth, health, and productivity [16,17,18,19].

Magnetite nanoparticles (Fe3O4 NPs) are well-known iron oxide nanoparticles, playing a significant role in metal chelation due to their biochemical, catalytic, and magnetic properties [20]. Recent literature indicates that positive metal ions are electrostatically attracted to the negatively charged surfaces of Fe3O4 nanoparticles, leading to their removal from water [21, 22]. Additionally, chemical or thermal activation of these adsorbents can enhance adsorption efficiency [23].

Silicates are non-toxic, environmentally friendly, thermally and chemically stable materials with effective adsorbing power and high magnetic ability. Silica can be safely applied in the food and aquaculture sectors [24]. Combining magnetite NPs with silica has been recognized as an emerging and effective approach to improve the adsorption efficiency of these nanoparticles by enhancing their chemical stability [25, 26].

In aquatic toxicology, Nile tilapia and African catfish are extensively used as living bioindicators of water pollution due to their high sensitivity to environmental changes and ability to tolerate various stressors [27, 28]. The impact of engineered nanoparticles on aquatic organisms and the environment, including their bioavailability and potential harmful effects, can be evaluated using biological endpoints or biomarkers such as hormones, hematology, genotoxicity, biochemical parameters, and histopathology [29].

The available information on the chelating ability of silica-stabilized nanomaterials, specifically magnetite iron oxides, with lead in aquatic animals is limited [30, 31]. Therefore, this study was designed to investigate the strong magnetic properties of silica-stabilized magnetite nanocomposite materials in chelating lead. Additionally, we examined their impact on hepatorenal indices, oxidative stress biomarkers, tissue genotoxicity indicated by DNA fragmentation, residual levels of lead in fish tissues, and histopathological alterations in both Nile tilapia and African catfish.

Materials and methods

Synthesis of magnetite nanoparticles

The magnetite nanoparticles were prepared according to Predoi [32] using a coprecipitation technique: A solution of ferrous and ferric ion salts in water was created by adding a base at room temperature while N2 gas was flowing. Then, 200 ml of a 0.02 M HCl solution was added while vigorously stirring at 8000 rpm for about 30 min, following the dissolution of 4.0 ml of 1 M FeCl3 and 1.0 ml of 2 M FeCl2 in deionized, deoxygenated (DD) water. This resulted in the formation of a brown precipitate.

Preparation of silica-stabilized magnetite (Si-M) nanocomposite materials

The (SiO2/Fe3O4) NPs were prepared through the hydrolysis of a silica solution obtained from rice husk [33] using the sol-gel phenomenon. This process combined 50 ml of ethanol with 0.2 g of previously prepared magnetite nanoparticles. This suspension underwent dispersion for 30 min under continuous exposure to a nitrogen flux and ultrasonication. Subsequently, 10 ml of the extracted silica solution was added, and the mixture was agitated for six hours. The resulting silica-stabilized Fe3O4 NPs (Si-MNPs) underwent multiple washes with ethanol and water before being vacuum dried for 24 h at 50oC to obtain the precipitate.

Characterization of silica-stabilized magnetite (Si-M) nanocomposite materials

Fourier transform infrared spectroscopy (FT-IR) of magnetite nanoparticles stabilized with silica was measured using a Nicolet Avatar 230 spectrometer with wavenumbers ranging from 400 cm− 1 and 4000 cm− 1 at a scan rate of 30 scans per minute (Fig. 1). In addition, SEM-EDAX analysis was performed for silica-stabilized magnetite nanoparticles to determine the changes in chemical constituents on their surfaces using a JEOL Quanta field emission gun (FEG) with 30 kv electrical power (Fig. 2a, b) equipped with Oxford EDAX (Japanese Corporation, Tokyo, Japan). DLS measurements using the Malvern Zeta-sized Nano-ZS nano series provide significantly better statistics than SEM; however, they necessitate more particles and commands of greater magnitude. The additional water content with the same batch of particles results in the mass distributions depicted in Fig. 3.

Fig. 1
figure 1

FTIR spectra of silica stabilized magnetite (Si-M) nanocomposite materials

Full size image
Fig. 2
figure 2

SEM images at different magnification of silica stabilized magnetite (Si-M) nanocomposite materials (a) and EDX analysis of silica stabilized magnetite (Si-M) nanocomposite materials

Full size image
Fig. 3
figure 3

DLS of silica stabilized magnetite (Si-M) nanocomposite materials

Full size image

Preparation of silica-stabilized magnetite (Si-M) nanocomposite materials stock solution

SiO2/Fe3O4 NP stock solutions were prepared by dispersing them in distilled water using a bath-type sonicator (40-kHz frequency Vibronics-250 W) over six hours, followed by 30 min of sonication each day before dosing. By using a peristaltic pump, NPs were kept suspended in water to minimize settling. At the final working concentration, the dispersion was excellent. Despite extensive sonication, aggregates of NPs were observed in the stock solution.

Preparation of lead nitrate stock solution

The experiment utilized lead nitrate (Pb(NO3)2) from AVI-CHEM Laboratories, India. To achieve the appropriate concentrations, Pb(NO3)2 was initially dissolved in deionized water to create a stock solution (1000 ppm), which was subsequently diluted to the desired concentration before being introduced into the aquarium water.

Experimental design

Lead nitrate LC50 value assessment

The LC50 treatment trial was conducted on 40 fish from each species. Nile tilapia and African catfish were divided separately into 4 groups, 10 fish in each, and exposed to 4 different concentrations of Pb(NO3)2 (3, 5, 7, and 10 mg/l) according to the study of Azua and Akaahan [34]. Fish feeding was stopped 48-h before starting the experiment to reduce basal metabolic rate and stress. Mortalities were recorded at 24, 48, 72, and 96 h. Mortality was observed and analyzed in each treatment group using the Finney probit analysis method [35].

Fish maintenance

Eighty apparently healthy Nile tilapia (Oreochromis niloticus) with an average body weight of 25 ± 5 g and 80 African catfish (Clarias gariepinus) with an average body weight of 60 ± 5 g were acquired from a private fish farm in Kafr El Sheikh governorate, Egypt. They were then carefully transferred to plastic fiberglass tanks equipped with aerators and transported to the wet lab of the Aquatic Animal Medicine and Management Department at the Faculty of Veterinary Medicine, Cairo University. Fish were kept for 2 weeks under observation, through which clinical examination was carried out to check the disease-free status of the fish prior to the beginning of the experiment. After acclimatization, each fish species was maintained in duplicates with a rate of 10 fish per glass aquaria (100 × 50 × 30 cm) supplied with de-chlorinated water with continuous oxygen aeration using electric air pumping compressors (Xilong, China). Fish were fed on a basal commercial diet containing 30% protein twice daily throughout the exposure duration. Water was routinely exchanged every 48 h. The physical and chemical mean values of water parameters were adjusted based on the American Public Health Association [36] guidelines as follows: dissolved oxygen, 5.5 ± 0.2 mg/l; pH 7.5 ± 0.3; temperature, 28 ± 1oC; unionized ammonia, 0.01 mg/l, and total alkalinity, 828 mg/l.

Experimental grouping

Separately, Nile tilapia and African catfish were divided into 4 groups. The first group served as the negative control group. The second group (Pb group) was exposed to 0.25 mg/l Pb(NO3)2 (1/20 of 96-h LC50). The third group (Si-MNPs) was exposed to silica-stabilized magnetite NPs (1 mg/l) based on the publication of Kaloyianni [37]. The fourth group (Pb + Si-MNPs) was exposed to Pb(NO3)2 simultaneously with the Si-MNPs at the same concentrations as the second and third groups. The exposure period was 3 weeks.

Biochemical analyses of hepatorenal indices

In each group, three fish were sampled by caudal venipuncture (2 ml/fish). Following anesthetization with MS222 (50 mg/l), blood samples were collected into sterile centrifuge tubes without anticoagulant and maintained for 6 h at ambient temperature for serum separation. After centrifugation of the serum at 3000 rpm for 10 min, samples were stored at -20 °C until further use. The activity of liver function enzymes, such as alkaline phosphatase (ALP) and gamma-glutamyl transferase (GGT), were examined as described by Reitman and Frankel [38]. Kidney function indices such as urea and creatinine were measured using the Tietz method [39]. Calorimetric analysis of the biochemical tests was performed using Spectrum diagnostic kits (Spectrum Diagnostics, Cairo, Egypt) per the manufacturer’s protocol, using STAT LAB SZSL0148, version 5.

Oxidative stress biomarkers analyses

Reduced glutathione (GSH) levels were determined according to Ellman [40]. The homogenate of liver, muscles, and gills tissues was mixed with DTNB, 0.2 M phosphate buffer (pH = 8), and 5,50-dithiobis-2-nitrobenzoic acid (DTNB). The levels of reduced glutathione are determined based on reduced DTNB levels, where glutathione produces a yellow color, and its absorbance is measured at 412 nm. Malondialdehyde (MDA) concentration was evaluated as an indicator of lipid peroxidation following the method by Ohkawa et al. [41]. The measurement involved using reactive species of thiobarbituric acid to determine MDA, with absorbance measured at 534 nm for the pink product. For protein oxidation assessment, protein carbonyl content (PCC) concentration was utilized as an index, following the procedure described by Reznick and Packer [42]. The carbonyl group was derivatized with dinitrophenylhydrazine, resulting in a stable dinitrophenylhydrazone, measured at 370 nm after derivatization.

Assessment of tissue genotoxicity by DNA fragmentation

The DNA fragmentation was determined using the method described by Abou-Zeid et al. [43]. Briefly, hepatic, branchial, and muscular tissues weighing 10 to 20 mg each were ground in 400 ml hypotonic lysis buffers. The resulting mixture was centrifuged at 3,000 rpm for 15 min at 4 °C, and the supernatant was divided into two parts. One part was utilized for gel electrophoresis, while the other, along with the pellet, was used for measuring fragmented DNA using diphenylamine at 578 nm. The percentage of DNA fragmentation in each sample was determined using the formula: %DNA fragmentation = (OD supernatant/OD supernatant + OD pellet) × 100.

Detection of lead residues in fish liver, gills, and muscles

After three weeks of experimental exposure, liver, gills, and muscle samples from each fish group were dissected. Approximately one gram of each organ was washed with distilled water, placed on clean slides, and dried at 70 °C for 24 h. 1 ml of concentrated HNO3 was added to each piece of dried tissue and placed in a clean tube for digestion. Following digestion, the samples were placed in a shaker water bath at 70 °C for four hours. Once digestion was finished, the tubes were cooled and diluted with 4 ml of distilled water, and a tissue digest aliquot was stored at room temperature. Lead detection was performed using an atomic absorption spectrophotometer (SensAA, GBC Scientific Equipment Ltd, Australia) [44, 45].

Histopathological examination

Fish dissection was conducted, and samples of the brain, gills, liver, kidney, and spleen were collected from tilapia and catfish representing each experimental group. These specimens were preserved in neutral buffered formalin (10%) for fixation before processing in various grades of alcohols and xylenes. Subsequently, the samples were embedded in melted paraffin wax. Sections of five µm thickness were cut on glass slides and stained with hematoxylin and eosin (H&E) for light microscopy [46]. Photomicrographs were examined and captured using a Leica DM4B light microscope (Leica, Germany) and a Leica DMC 4500 digital camera (Leica, Germany).

Statistical analysis

The significant differences among the various fish groups were analyzed using one-way ANOVA and Tukey’s multiple comparison post hoc tests using SPSS version 18. The data were presented as mean and standard error. A p-value of < 0.05 was considered statistically significant.

Results

Characterization of silica-stabilized magnetite (Si-M) nanocomposite materials

The FTIR results (Fig. 1) show vibrations from the Si-O-H and Si-O-Si groups. A broad band at 3500 cm− 1 indicates the stretching mode of the O-H group. Additionally, the SEM image (Fig. 2a) verifies the development of chemically synthesized iron oxide nanostructures, which were hexagonal and spherical. The SEM image reveals that most prepared nanoparticles were inhomogeneous, with a bright SiO2 spot inside a dark magnetic core-shell. Elemental composition analysis using energy dispersive X-ray spectroscopy (EDS) in Fig. 2b confirms the presence of Fe in the catalyst. Compared to SEM, DLS measurements yield better statistics due to the requirement of many particles. The DLS particle analysis confirms the presence of various nanoparticle sizes in the sample (Fig. 3).

Lead nitrate LC50 short-term exposure values

No mortality was observed in the control group over the 96-hour period. The lowest concentration of lead nitrate (Pb(NO3)2) at which mortality was detected in both fish groups was 3 mg/l. The highest mortalities, with 9 Nile tilapia fish and 7 African catfish, were observed in the 10 mg/l treatment groups after 48 h (Table 1). The 96-hour LC50 for Nile tilapia and African catfish was recorded to be 5 mg/l. A value of 0.25 mg/l, one-twentieth (1/20) of the LC50 value, was used for subsequent sub-lethal studies, following the approach described by Sprague [47].

Table 1 Numbers of dead fish at different concentrations of Pb (NO3)2 in the 96-hour LC50 experiment
Full size table

Clinical manifestations and mortalities of pb(NO3)2 exposed group

During the experimental period, no mortalities were recorded in all groups. However, the Nile tilapia fish group exposed to lead nitrate in water showed melanosis, abnormal nervous and swimming behavior, abnormal rapid movement of pectoral fins, and skeletal deformities such as scoliosis (Fig. 4).

Fig. 4
figure 4

Nile tilapia in Pb exposed group showing scoliosis

Full size image

Hepatorenal indices analyses

Liver function enzymes, including alkaline phosphatase (ALP) and gamma-glutamyl transferase (GGT), were measured in the serum of Nile tilapia and African catfish from all experimental groups. The levels of ALP and GGT in both tilapia and catfish showed a significant increase in the Pb group compared to the Si-MNPs, Pb + Si-MNPs, and control groups. Additionally, kidney function tests for urea and creatinine measured in tilapia fish serum across all groups demonstrated significantly higher levels in the Pb group compared to the other groups. In contrast, there was no marked significance in catfish serum creatinine levels between the Pb-exposed and other groups (Table 2).

Table 2 Hepatorenal function indices measured in Nile tilapia and African catfish
Full size table

Oxidative stress biomarkers

Reduced glutathione findings

In Nile tilapia, the concentration of GSH significantly decreased in the Pb group to 0.3, 0.2, and 0.25 in the liver, gills, and muscles, respectively, compared to the control group. However, its concentration returned nearly to normal levels in the liver and gills of the Pb + Si-MNPs group. Interestingly, the Pb + Si-MNPs group showed a significant increase in GSH concentration in the muscles compared to the control group (Table 3).

Table 3 GSH concentrations in Nile tilapia and African catfish
Full size table

In African catfish, the concentration of GSH significantly decreased in the Pb intoxicated group from 5.13, 2.5, and 2.1 to 1.03, 0.43, and 0.4 in the liver, gills, and muscles, respectively, compared to the control group. In contrast, its concentration was significantly elevated in the Pb + Si-MNPs group to 3.17, 2.13, and 2.77, respectively.

Lipid peroxidation findings

In Nile tilapia, MDA concentration significantly increased in the Pb group to 44.7, 31.7, and 12.6 in the liver, gills, and muscles, respectively. However, in the Pb + Si-MNPs group, MDA concentration significantly decreased in the liver and gills to 18 and 13, respectively, and returned nearly to levels comparable to the control group (Table 4).

Table 4 MDA concentrations in Nile tilapia and African catfish
Full size table

In African catfish, the concentration of MDA significantly increased to 40.67, 26, and 14.67 in the liver, gills, and muscles, respectively, in the Pb group compared to the control group. However, its concentration significantly improved and nearly reached control levels in the Pb + Si-MNPs group, measuring 15.67, 8.5, and 3, respectively.

Protein oxidation findings

In Nile tilapia, the PCC concentration significantly increased to 13, 15, and 11 in the Pb group’s liver, gills, and muscles, respectively, compared to the control group. However, its concentration was mitigated, nearly returning to control levels in the Pb + Si-MNPs group (Table 5).

Table 5 Protein oxidation concentrations in Nile tilapia and African catfish
Full size table

Similarly, in African catfish, the concentration of PCC significantly increased to 14, 17, and 8 in the liver, gills, and muscles, respectively, in the Pb group compared to the control group. However, its concentration significantly improved and nearly reached control levels in the Pb + Si-MNPs group, measuring 3.5, 2.5, and 2.83, respectively.

Tissue genotoxicity and DNA fragmentation findings

In Nile tilapia, the percentage of DNA fragmentation significantly increased in the Pb group to 79.3, 58, and 66 in the liver, gills, and muscles, respectively, compared to the control group. Conversely, its percentage significantly decreased in the liver, gills, and muscle tissues in the Pb + Si-MNPs group (Table 6).

Table 6 DNA fragmentation percentage in Nile tilapia and African catfish
Full size table

Similarly, in African catfish, the percentage of DNA fragmentation significantly increased in the Pb-intoxicated group to 66.6, 50, and 59 in the liver, gills, and muscles, respectively, compared to the control group. However, its percentage significantly decreased in all tissues in the Pb + Si-MNPs group to 20, 16.7, and 25, respectively, compared to the Pb group.

Lead residues accumulation in the liver, gills, and muscles

The accumulation of Pb was measured and recorded in the liver, gills, and muscles of Nile tilapia and African catfish. Pb residues in the liver, gills, and muscles of Nile tilapia and African catfish were significantly higher in the Pb-exposed group compared to the Pb + Si-MNPs group (Fig. 5a, b).

Fig. 5
figure 5

(a, b) Lead residues in liver, gills and muscles of experimental Nile tilapia and African catfish

Full size image

In Nile tilapia, high Pb accumulation was observed in the liver, followed by the gills, while in African catfish, high Pb accumulation was observed in the gills, followed by the liver. The lowest Pb concentration was recorded in the muscles of both species.

Histopathological findings

The histopathological evaluation of the collected tissue samples from Nile tilapia is depicted in Figs. 6 and 7. In the brain of tilapia fish from the Pb group, marked vacuolation, vasculitis, perivascular mononuclear inflammatory cell infiltration, and gliosis were observed. Conversely, other groups exhibited apparently normal brain structure.

Fig. 6
figure 6

Photomicrographs of different organs of Nile tilapia (H&E). Control group showing normal histological structure of all examined organs, Pb group: vacuolation (red arrow) and perivascular inflammatory cells infiltration (black arrow) and focal gliosis (green arrow) in brain. Gill hyperplasia and fusion (black arrow). Si-MNPs group: showing apparently normal structure of brain and gills Pb + Si-MNPs group showing apparently normal brain and gills

Full size image
Fig. 7
figure 7

Photomicrographs of different organs of Nile tilapia (H&E). Control group showing normal histological structure of all examined organs, Pb group showing Marked liver vacuolation. Hyperplasia in melano-macrophage centers (black arrows) in spleen. Si-MNPs group showing hepatocellular vacuolation in liver and apparently normal spleen. Pb + Si-MNPs showing hepatocellular vacuolation and mild melano-macrophage center activation in spleen

Full size image

The gills from the control and Si-MNPs groups showed histologically normal features, while the Pb group exhibited gill hyperplasia and fusion of secondary gill lamellae with intense inflammatory cell infiltration. The Pb + Si-MNPs group showed apparently normal gills.

In the liver sections, except for the control group, the rest of the experimental groups exhibited hepatocellular vacuolation. Hyperplasia and activation of melano-macrophage centers were detected in spleen specimens from the Pb groups, while apparently normal spleen was observed in the other experimental groups.

Microscopic examination of the different tissue samples from African catfish (Figs. 8 and 9) revealed an absence of detectable histopathological changes in the control and Si-MNPs groups. In the Pb groups, focal gliosis, edema, and neuronal degeneration were observed in brain sections. The Pb + Si-MNPs groups showed mild neuronal edema in a few sections, while most examined sections appeared normal.

Fig. 8
figure 8

Photomicrograph of different organs from African catfish (H&E). Control group showing normal histological structure of different organs. Pb group showing neuronal degeneration (black arrow) and focal gliosis (red arrow) in brain, destruction of secondary gill lamellae (green arrow). Si-MNPs group showing apparently normal structure of different organs. Pb + Si-MNPs group showing apparently normal brain and inflammatory cells infiltration in gills (white arrow)

Full size image
Fig. 9
figure 9

Photomicrograph of different organs from African catfish (H&E). Control group showing normal histological structure of different organs. Pb group showing hepatocellular necrosis (blue arrow) and hemorrhage (black arrow) in liver. Necrosis in renal tubules (yellow arrow) of kidneys. Si-MNPs group showing apparently normal structure of different organs. Pb + Si-MNPs showing apparently normal liver and congestion (red arrow) in kidneys

Full size image

Destruction of the secondary gill lamellae and mononuclear inflammatory cell infiltrations were observed in the Pb groups. Additionally, inflammation was noted in the gill tissue from the Pb + Si-MNPs groups.

Hepatocellular necrosis and hemorrhage were frequently detected in the liver of the Pb group, while the Si-MNPs groups exhibited apparently normal liver tissue. Renal tubular damage was subsided in kidney sections from the Pb + Si-MNPs groups, with mild vascular congestion observed in a few individuals.

Discussion

Aquatic organisms, particularly fish, are primary targets for heavy metal contamination and accumulation, making them valuable indicators of aquatic pollution levels [48]. In aquaculture, innovative strategies such as feed additives, probiotics, and nanoparticles offer cost-effective and environmentally friendly methods to control heavy metal contamination [49]. Metallic nanoparticles, including silica-stabilized magnetite (Si-M) nanocomposite materials, have gained widespread use in various applications like biomedical, food, agricultural, and electronics sectors due to their unique physical and chemical properties [50].

The superparamagnetic properties of silicates and magnetite (Fe3O4) nanoparticles make silica-stabilized magnetite (Si-M) nanocomposite materials effective in pharmaceutical and agricultural applications and the separation of heavy metals and toxic ions from water [51].

The characterization of the silica-stabilized magnetite nanocomposites used in the study is depicted in Fig. 1, demonstrating the presence of silica networks on the magnetite surface through Fe-O-Si bonds as indicated by significant FT-IR spectra [52]. Notably, a strong absorbance band at 1018 cm− 1 in Fig. 1 is attributed to the vibration of the Si-O-H and Si-O-Si bonds. Additionally, weak absorption peaks observed are attributed to vibrations of the C-H bonds of organic groups that remained during preparation [53]. The broadband observed at 3500 cm− 1 indicates the stretching mode of the O-H group, representing the water content of the silica-stabilized magnetite nanocomposite samples [54]. The distinctive Fe3O4 diffraction peaks are somewhat weakened due to the silica coat and mixed groups, allowing for the detection of amorphous silica diffraction peaks [55, 56].

Furthermore, Fig. 2a presents a typical FE-SEM image of magnetite nanoparticles stabilized with silica. The SEM image reveals that most nanoparticles are non-homogeneous, with a bright SiO2 spot inside the dark magnetic core-shell structure. An energy-dispersive X-ray spectroscopy (EDS) analysis was conducted on a silica-stabilized magnetite nanocomposite sample.

Figure 2b displays the EDS results derived from SEM analysis of the nanomaterial mentioned above, affirming the presence of Fe in the silica-stabilized magnetite (Si-M) NPs. Furthermore, the presence of O, Si, and Fe, along with the Fe peak exhibiting higher intensity than the Si peak, suggests the successful preparation of silica-stabilized magnetite nanocomposite materials.

Compared to SEM, DLS measurements offer significantly improved statistical data as they involve a larger number of particles. The DLS particle analysis further confirms the presence of various nanoparticle sizes within the sample, as illustrated in Fig. 3.

The silica-stabilized magnetite NPs were recently used in the aquaculture industry. In our study, 1 mg/l of Si-MNPs were added to the aquaria water. Based on studies by Zhu et al. [30], Kaloyianni et al. [37], and Jurewicz et al. [57], this dose most likely causes a minimal toxic effect on fish tissues and, at the same time, has a strong chelating ability to lead nitrate in water.

Concerning lead nitrate LC50 values recorded in this study, calculations were performed for each fish species across the four different groups, as illustrated in Table 1. The mortality percentage of tilapia fish and catfish increased with increasing lead concentrations. The 96-h LC50 for Nile tilapia and African catfish was determined to be 5 mg/l, consistent with the LC50 values reported by Kim et al. [58]. This explains that heavy metal toxicity depends on the exposure route, duration, and the absorbed dose [59,60,61].

Lead is a biologically non-essential metal for living organisms. However, continuous lead exposure causes various physiological, behavioral, and biochemical alterations in fish [62]. Most clinical manifestations were observed in the tilapia fish group exposed to lead. This is related to the higher sensitivity of Oreochromis species than Clarids [63]. The observed clinical signs align with those of Azua and Akaahan [64], who observed erratic swimming behavior upon fish exposure to lead nitrate due to its effect on brain cells, causing several neurological changes [65, 66].

Additionally, the presence of melanosis in the lead-exposed fish group reflects the stress experienced by the fish during the experimental duration. This stress can elevate the levels of catecholamines and corticosteroids, leading to physiological skin darkening [67]. Similarly, findings from Nwobi et al. [68] indicate that lead exposure can reduce various essential bone minerals, resulting in growth retardation and skeletal deformities, as shown in Fig. 4. In contrast, no abnormal clinical signs were observed in the Si-MNPs and Pb + Si-MNPs groups, consistent with the observations made by Karlsson et al. [69].

The liver plays a crucial role in lead accumulation and detoxification of xenobiotics, and any disruption in its normal function can lead to fish mortality [70, 71]. Liver enzymes are stress indicators for confirming diagnoses and evaluating tissue damage caused by environmental pollution and metal intoxication [72]. Lead exposure has been directly linked to elevated levels of ALP and GGT [73]. Our findings revealed a significant increase in ALP and GGT levels in the serum of Nile tilapia and African catfish in the Pb groups compared to other experimental groups (Table 2).

This increase in ALP and GGT levels has been reported in various fish species following lead intoxication, such as Oreochromis niloticus [48, 74], Cyprinus carpio [72, 75], African catfish [63], Mystus fish species [76], and Lethrinus harak fish [77]. Simultaneous elevation of ALP and GGT levels typically occurs in hepatobiliary diseases, cholestasis, hepatocellular necrosis, and hepatic dysfunction resulting from long-term lead exposure [78,79,80]. ALP elevation is commonly associated with biliary obstruction, while elevated GGT confirms the hepatogenic origin of increased ALP [81]. In some cases, ALP elevation is concurrently associated with liver and bone disorders, which could explain the observed skeletal deformities in some tilapia fish in the lead-intoxicated group [82].

Long-term exposure of fish to heavy metals can lead to kidney dysfunction [83, 84]. Changes in urea and creatinine values are considered indicators of the adverse impact of lead on kidney function mechanisms. Lead is absorbed directly from the gills into the bloodstream, distributed throughout the body tissues, and primarily excreted through the kidneys [85]. This direct absorption has an immediate effect on the glomerular filtration rate, as it leads to the production of reactive oxygen species, ultimately causing kidney dysfunction and nephrotoxicity [86].

Our study found an increase in urea levels in Pb-exposed tilapia and catfish groups (Table 2), consistent with findings by El-Khadragy et al. [87] and El-Khayat et al. [88]. Creatinine levels showed a significant increase only in tilapia fish serum, likely due to severe glomerular damage caused by lead exposure [63, 89]. In contrast, no significant elevation was recorded in creatinine levels measured in catfish serum after 3 weeks of exposure to lead nitrate, possibly due to the more resistant and hardy nature of Clarias species to aquatic pollutants than Nile tilapia [64]. Elevated urea and creatinine levels due to lead toxicity have been reported in several fish species, such as Cyprinus carpio and Oreochromis niloticus [75, 90].

Our results indicated improved liver and kidney function parameters in the Si-MNPs and Pb + Si-MNPs groups. This suggests that stabilized silica and magnetite nanoparticles protect against lead-induced hepato-renal damage [49].

Aquatic organisms readily absorb lead and are subsequently involved in the bioaccumulation process through the food chain [2, 91]. This leads to oxidative stress, primarily caused by the production of free radicals, which causes numerous disorders and excessive damage [92, 93]. Oxidative stress is an imbalance between the production of reactive oxygen species (ROS) and the cell’s ability to detoxify reactive intermediates and repair damage that may occur in cellular molecules, increasing ROS production and decreasing defense mechanisms [25, 94]. Although ROS is typically produced by the cell, oxidative stress can be caused by various external factors, such as exposure to heavy metals [95].

Changes in the activity of antioxidant enzymes and the accumulation of oxidative damage products serve as crucial markers for oxidative stress. Reduced levels of GSH and other thiols render cells more susceptible to oxidative damage, while heightened activity of antioxidant enzymes can partially mitigate this effect [96].

Our results support these findings, showing a significant decrease in GSH concentration in the Pb group’s liver, gills, and muscles compared to the control group in both tilapia and catfish, as shown in Table 3. GSH is a scavenging non-enzymatic antioxidant compound that, when present in low concentrations due to rapid utilization in the presence of high levels of ROS, makes fish more susceptible to oxidative damage [97]. The removal of H2O2 is a critical defense strategy of aquatic organisms against oxidative stress [98]. In our study, the concentration of GSH significantly increased in the Pb + Si-MNPs group compared to the control (Table 3).

These findings align with Alfakheri et al. [99], who observed a considerably lower GSH concentration in the Pb group compared to the control group. Similarly, Loveline et al. [100] found that lead increased oxidative stress in C. gariepinus compared to the control group. Additionally, Saliu and Bawa-Allah [101] noted a decrease in GSH, SOD, and CAT in African catfish (C. gariepinus) when exposed to Pb (NO3)2. Furthermore, Olagoke [102] reported lower levels of GSH and GST in exposed fish compared to the control group.

The production of MDA serves as a marker of lipid peroxidation resulting from the breakdown of polyunsaturated fatty acids due to oxidative stress [103]. Our data demonstrated a significant increase in the concentration of MDA in the liver, gills, and muscles of the Pb group compared to the control group in both tilapia and catfish. Conversely, its concentration significantly improved, nearly reaching the control value, in the Pb + Si-MNPs group (Table 4).

The liver plays a significant role in the accumulation and detoxification of heavy metals, which may be linked to the high concentration of these metals in the liver [104]. Our findings align with the higher MDA levels observed in catfish exposed to lead toxicity, as reported by Maiti et al. [105].

Protein carbonyl is generally associated with oxidative stress-induced protein damage, as indicated by various diseases or tissue lesions [106]. Therefore, PC can be a marker for enzyme breakdown, amino acid structure modifications, and protein function alterations [107]. Our results in Table 5 demonstrate the impact of lead on protein oxidation, with the concentration of PCC significantly increasing in the liver, gills, and muscles of the Pb group compared to the control group in both tilapia and catfish. However, its concentration significantly improved, nearly reaching the control value in the Pb + Si-MNPs group. These findings suggest that metal pollutants may induce protein damage due to oxidative stress.

Similar results were reported by Neeratanaphan et al. [108], who found higher levels of PC in catfish from a landfill reservoir. Additionally, Ibrahim [109] showed that all fish tissues exposed to HgCl2 had significantly elevated carbonyl protein levels.

Reactive oxygen species are produced due to reactions accelerated by heavy metals. These reactions can damage tissues and macromolecules such as DNA, proteins, and lipids through oxidative stress. Using DNA fragmentation as a monitoring technique for heavy metal pollution was suggested by Moussa et al. [110]. Our data showed a significant increase in the percentage of DNA fragmentation in the Pb group in the liver, gills, and muscles compared to the control group. However, this percentage significantly decreased in all tissues in the Pb + Si-MNPs group compared to the Pb group (Table 6).

These findings align with Sultana et al. [111], who established a link between DNA fragmentation and heavy metal levels in various fish tissues. Moreover, Mohamed et al. [112] noted that tilapia exposed to higher heavy metal levels in severely polluted areas showed a higher frequency of DNA fragmentation in the gills, liver, and muscles, potentially indicating a lack of effective DNA repair systems. Furthermore, studies by Moussa et al. [110], Jindal and Verma [113], and Ratn et al. [114] have shown that fish exposed to toxins for prolonged periods exhibit increased DNA damage.

Numerous studies indicated that silica nanoparticles (Si-NPs) contribute positively to plant growth and development, particularly under stressful conditions. Silica has found application in environmental remediation for eliminating metals, non-metals, and radioactive elements, filtering water, and minimizing the discharge of brine, heavy metals, and radioactive substances into water bodies. Research has shown that silica nanoparticles can mitigate oxidative stress by stimulating the excess production or expression of non-enzymatic antioxidant metabolites and enhancing the functions of antioxidants [115].

In this study, the Pb + Si-MNPs demonstrated significantly higher GSH concentrations, lower MDA and PCC levels, and reduced DNA fragmentation (Tables 3, 4, 5 and 6). Rajkumar and Tennyson [116] suggested that elevated GSH content can act as an initial defense mechanism against toxic heavy metals and may help avoid oxidative stress [117].

Lead accumulation was assessed in the liver, gills, and muscles of Nile tilapia and African catfish at the end of the experimental period. Our findings, illustrated in Fig. 5a, indicate that tilapia exhibited the highest lead accumulation in liver tissues, consistent with previous studies by Salman [45], Dural et al. [118], Souid et al. [119], and Zhai et al. [120] in various fish species. This heightened accumulation in tilapia liver tissue may be attributed to the liver’s natural ability to produce significant amounts of metallothionein, a low metal-binding protein crucial for heavy metal uptake and detoxification [121, 122].

Conversely, in catfish (Fig. 5b), elevated lead content was observed in the gills. Numerous studies have noted this trend, particularly following water-borne exposure in different fish species such as Tilapia zillii [123], Clarias gariepinus [104, 124], starry flounder (Platichthys stellatus) [125], Solea vulgaris [126], and common carp Cyprinus carpio [127]. The gills’ larger surface area, directly exposed to external water pollutants, facilitates rapid diffusion and absorption of toxic metals through respiration and osmoregulation mechanisms [124, 128]. Additionally, Clarias gariepinus possesses accessory respiratory organs (AROs) that may enhance the trapping, absorption, and accumulation of Pb content from water, reducing Pb distribution in liver and muscle tissues.

The variation in metal tissue storage and concentration among different fish species can be attributed to factors such as the pathway and rate of Pb uptake (water-borne or dietary exposure) and elimination, fish feeding habits (pelagic or benthic feeder), duration of exposure, fish age, size, and length, metabolic activity, and various water parameters including temperature, salinity, and other interacting agents [129].

A significant concern is directed to the public health implications of lead, its accumulation in fish meat, and its safety for human consumption [130, 131]. Our study indicated that lead accumulation in the muscle tissues of Nile tilapia and African catfish is notably low compared to other tissues, as noted by Victor et al. [124], Lee et al. [129], and El-Moselhy et al. [132]. Furthermore, the Pb + Si-MNPs group exhibited lower Pb residues in both tilapia and catfish muscles than the Pb-exposed group. This reduction may be attributed to the potent chelating ability of silica-stabilized magnetite (Si-M) nanoparticles in binding Pb ions [133].

The histopathological changes observed in the tissues of tilapia and catfish exposed to lead (Figs. 6, 7 and 8, and 9) align with significant alterations in liver and kidney function, oxidative stress parameters, and observed genotoxicity [22, 77, 134,135,136]. Previous research by Patnaik et al. [137] has described neurotoxic histopathological effects on fish brains due to lead exposure, including vacuolation and gliosis, linked to Pb-induced oxidative damage, glycolysis, and mitochondrial dysfunction.

The proliferative tissue response seen in the gills of the lead-exposed group corresponds with findings from studies by Parashar and Banerjee [138] and Muñoz et al. [139], indicating a direct local effect of Pb on gills. Similarly, hepatocellular vacuolation and necrosis, indicative of lead toxicity in fish, have been previously reported by Suiçmez et al. [140] and Khidr et al. [141], likely due to energy depletion and reduced protein synthesis [142]. Kidneys, crucial for detoxification, are targeted by heavy metals. Muñoz et al. [139] noted histopathological changes in the kidneys similar to those in our study.

The observed increase in melano-macrophage centers in the spleen of the Pb-exposed group may be attributed to their role in detoxification and involvement in innate and adaptive immunity [143]. Conversely, the Pb + Si-MNPs groups exhibited minimal tissue pathology, possibly due to the antioxidant properties of iron nanoparticles countering lead ion damage [144], along with the high magnetic affinity of silica-stabilized magnetite (Si-M) nanoparticles for lead in water, reducing fish absorption [145].

Conclusions

In conclusion, silica-stabilized magnetite (Si-M) nanoparticles exhibit a strong capability to chelate lead nitrate in water, thereby reducing lead absorption by fish. This property helps mitigate lead’s detrimental effects on hepatorenal function, oxidative stress parameters, genotoxicity, and histopathological changes. Additionally, it minimizes lead accumulation in fish muscle, ultimately enhancing fish health and performance and supporting sustainable aquaculture practices without negatively impacting human health.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  1. Lingamdinne LP, Yang JK, Chang YY, Koduru JR. Low-cost magnetized Lonicera japonica flower biomass for the sorption removal of heavy metals. Hydrometallurgy. 2016;165:81–9. https://doi.org/10.1016/j.hydromet.2015.10.022.

    Article  CAS  Google Scholar 

  2. Vasanthi N, Muthukumaravel K, Sathick O, Sugumaran J. Toxic effect of Mercury on the freshwater fish Oreochromis mossambicus. Res J Life Sci Bioinfo Pharmaceut Chem Sci. 2019;5(3):364–76.

    CAS  Google Scholar 

  3. Mohamed AA, Abdel Rahman AN, Mohammed HH, Ebraheim LLM, AboElMaaty AMA, Ali SA, Elhady WM. Neurobehavioral, apoptotic, and DNA damaging effects of sub-chronic profenofos exposure on the brain tissue of Cyprinus carpio L.: antagonistic role of geranium essential oil. Aquat Toxicol. 2020;224:105493. https://doi.org/10.1016/j.aquatox.2020.105493.

    Article  CAS  PubMed  Google Scholar 

  4. Naidu R, Biswas B, Willett IR, Cribb J, Singh BK, Nathanail CP, Coulon F, Semple KT, Jones KC, Barclay A, Aitken RJ. Chemical pollution: a growing peril and potential catastrophic risk to humanity. Environ Int. 2021;156:106616.

    Article  CAS  PubMed  Google Scholar 

  5. Ismail HTH, Mahboub HHH. Effect of acute exposure to nonylphenol on biochemical, hormonal, and hematological parameters and muscle tissues residues of Nile tilapia; Oreochromis niloticus. Vet World. 2016;9(6):616. https://doi.org/10.14202/vetworld.2016.616-625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Soni HB. Categories, causes and control of water pollution: a review. Int J Life Sci Leafl. 2019;107:4–12.

    Google Scholar 

  7. Opasola OA, Adeolu AT, Iyanda AY, Adewoye SO, Olawale SA. Bioaccumulation of heavy metals by Clarias gariepinus (African Catfish) in Asa River, Ilorin, Kwara State. J Health Pollut. 2019;9(21):190303. https://doi.org/10.5696/2156-9614-9.21.190303.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Yap CK, Al-Mutairi KA. Ecological-health risk assessments of heavy metals (Cu, Pb, and zn) in aquatic sediments from the ASEAN-5 emerging developing countries: a review and synthesis. Biology. 2022;11:7. https://doi.org/10.3390/biology1101000.

    Article  CAS  Google Scholar 

  9. Narayana PL, Lingamdinne LP, Karri RR, Devanesan S, AlSalhi MS, Reddy NS, Chang YY, Koduru JR. Predictive capability evaluation and optimization of pb(II) removal by reduced graphene oxide-based inverse spinel nickel ferrite nanocomposite. Environ Res. 2022;204:112029. https://doi.org/10.1016/j.envres.2021.112029.

    Article  CAS  PubMed  Google Scholar 

  10. Abdallah GM, El-Sayed el SM, Abo-Salem OM. Effect of lead toxicity on coenzyme Q levels in rat tissues. Food Chem Toxicol. 2010;48:1753–6. https://doi.org/10.1016/j.fct.2010.04.006.

    Article  CAS  PubMed  Google Scholar 

  11. Angeles M, Morcillo P, Cuesta A, Fish. Shell fish Immunol. 2016. https://doi.org/10.1016/j.fsi.2016.03.164.

    Article  Google Scholar 

  12. Ustao?lu F, Islam MS. Potential toxic elements in sediment of some rivers at Giresun, Northeast Turkey: a preliminary assessment for ecotoxicological status and health risk. Ecol Indic. 2020;113:106237.

    Article  Google Scholar 

  13. Tighadouini S, Radi S, Elidrissi A, Haboubi K, Bacquet M, Degoutin S, Zaghrioui M, Garcia Y. Removal of toxic heavy metals from river water samples using a porous silica surface modified with a new β-ketoenolic host. Beilstein J Nanotechnol. 2019;10(1):262–73. https://doi.org/10.3762/bjnano.10.25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Yang J, Hou B, Wang J, Tian B, Bi J, Wang N, Li X, Huang X. Nanomaterials for the removal of heavy metals from wastewater. Nanomaterials. 2019;9(3):424. https://doi.org/10.3390/nano9030424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Horvath G, Szalay Z, Simo F, Salgo K, Krcma F, Matejova S. Recycling of a waste water to iron oxide micro structures. Environ Res Commun. 2019;1(8):085001. https://doi.org/10.1088/2515-7620/ab37c1.

    Article  Google Scholar 

  16. Shah BR, Mraz J. Advances in nanotechnology for sustainable aquaculture and fisheries. Reviews Aquaculture. 2020;12(2):925–42.

    Article  Google Scholar 

  17. Dar AH, Rashid N, Majid I, Hussain S, Dar MA. Nanotechnology interventions in aquaculture and seafood preservation. Crit Rev Food Sci. 2019;1–10. https://doi.org/10.1080/10408398.1617232.

  18. Mahboub HH, Shahin K, Zaglool AW, Roushdy EM, Ahmed SSA. Efficacy of nano zinc oxide dietary supplements on growth performance, immunomodulation and disease resistance of African Catfish, Clarias gariepinus. Dis Aquat Org. 2020. https://doi.org/10.3354/dao003531.

    Article  Google Scholar 

  19. Rashidian G, Lazado CC, Mahboub HH, Mohammadi-Aloucheh R, Prokić MD, Nada HS, Faggio C. Chemically and green synthesized ZnO nanoparticles alter key immunological molecules in common carp (Cyprinus carpio) skin mucus. Int J Mol Sci. 2021;22:3270. https://doi.org/10.3390/ijms22063270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cornell RM, Schwertmann U. The Iron Oxides: structures, Properties, reactions, occurences and used. Weinheim: Wiley; 2003.

    Book  Google Scholar 

  21. Jalali M, Ghanati F, Modarres-Sanavi AM. Effect of Fe3O4 nanoparticles and iron chelate on the antioxidant capacity and nutritional value of soil-cultivated maize (Zea mays) plants. Crop Pasture Sci. 2016;67(6):621–8.

    Article  CAS  Google Scholar 

  22. Hong J, Xie J, Mirshahghassemi S, Lead J, Metal. (Cd, cr, Ni, Pb) removal from environmentally relevant waters using polyvinylpyrrolidone-coated magnetite nanoparticles. RSC Adv. 2020;10(6):3266–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kumar PS, Pavithra J, Suriya S, Ramesh M, Kumar KA. Sargassum Wightii, a marine alga is the source for the production of algal oil, bio-oil, and application in the dye wastewater treatment. Desalin Water Treat. 2015;55:1342–58. https://doi.org/10.1080/19443994.2014.924032.

    Article  CAS  Google Scholar 

  24. Alandiyjany MN, Kishawy ATY, Hassan AA, Eldoumani H, Elazab ST, El-Mandrawy SAM, Saleh AA, ElSawy NA, Attia YA, Arisha AH, Ibrahim D. Nano-silica and magnetized-silica mitigated lead toxicity: their efficacy on bioaccumulation risk, performance, and apoptotic targeted genes in Nile tilapia (Oreochromis niloticus). Aquat Toxicol. 2022;242:106054.

    Article  CAS  PubMed  Google Scholar 

  25. Jamasbi N, Ziarani GM, Mohajer F, Darroudi M, Badiei A, Varma RS, Karimi F. Silica-coated modified magnetic nanoparticles (Fe3O4@SiO2@(BuSO3H)3) as an efficient adsorbent for Pd2 + removal. Volume 307. Chemosphere; 2022. p. 135622.

  26. Karina S, Perdana AW, Prajaputra V, Isnaini N, Nuufus PH, Bismi A. Silica-Magnetite Composite as an eco-friendly adsorbent for aqueous tetracycline removal: kinetic and Isotherm studies. Ecol Eng Environ Technol. 2024;25(1):82–92. https://doi.org/10.12912/27197050/174225.

    Article  Google Scholar 

  27. Iheanacho SC, Odo GE. Neurotoxicity, oxidative stress biomarkers and haematological responses in African catfish (Clarias gariepinus) exposed to polyvinyl chloride microparticles. Comp Biochem Physiol C: Toxicol Pharmacol. 2020;232,108741. https://doi.org/10.1016/j.cbpc.2020.108741.

  28. Mahboub HH, Tartor YH. Carvacrol essential oil stimulates growth performance, immune response, and tolerance of Nile tilapia to Cryptococcus uniguttulatus infection. Dis Aquat Org. 2020;141:1–14. https://doi.org/10.3354/dao03506.

    Article  CAS  Google Scholar 

  29. Moore MN. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ. Int. 2006;32:967–76.

    CAS  Google Scholar 

  30. Zhu X, Tian S, Cai Z. Toxicity Assessment of Iron Oxide nanoparticles in zebrafish (Danio rerio) Early Life stages. PLoS ONE. 2012;7(9):e46286. https://doi.org/10.1371/journal.pone.0046286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Castro-Bugallo A, Gonzalez-Fernandez A, Guisande C, Barreiro A. Comparative responses to metal oxide nanoparticles in marine phytoplankton. Arch Environ Contam Toxicol. 2014;67:483–93. https://doi.org/10.1007/s00244-014-0044.4.

    Article  CAS  PubMed  Google Scholar 

  32. Predoi D. A Study on Iron Oxide Nanoparticles Coated with Dextrin Obtained by Coprecipitation. Digest Journal of Nanomaterials and Biostructures. 2007; Mar 1;2(1):169–73.

  33. Alahl AAS, Ezzeldin HA, Al-Kahtani AA, Pandey S, Kotp YH. Synthesis of a Novel Photocatalyst based on Silicotitanate nanoparticles for the removal of some Organic Matter from Polluted Water. Catalysts. 2023;13(6):981.

    Article  CAS  Google Scholar 

  34. Azua ET, Akaahan TJ. Toxic stress exhibited by juveniles of Clarias gariepinus exposed to different concentration of lead. J Res Environ Sci Toxicol. 2017;6:008–11. https://doi.org/10.14303/jrest.2017.016).

    Article  Google Scholar 

  35. Mishra AK, Mohanty B. Acute toxicity impacts of hexavalent chromium on behavior and histopathology of gill, kidney and liver of the freshwater fish, Channa punctatus (Bloch). Environ Toxicol Pharmacol. 2009;26:136–41.

    Article  Google Scholar 

  36. APHA (American Public Health Association). Standard Methods for the Examination of Water and Wastewater. Washington, DC, USA: American Public Health Association, Inc.; 1998.

    Google Scholar 

  37. Kaloyianni M, Dimitriadi A, Ovezik M, Stamkopoulou D, Feidantsis K, Kastrinaki G, Gallios G, Tsiaoussis I, Koumoundouros G, Bobori D. Magnetite nanoparticles effects on adverse responses of aquatic and terrestrial animal models. J Hazard Mater. 2020;383:121204.

    Article  CAS  PubMed  Google Scholar 

  38. Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957;28(1):56–63. https://doi.org/10.1093/AJCP/28.1.56.

    Article  CAS  PubMed  Google Scholar 

  39. Tietz N. Clinical Guide to Laboratory Tests; WB Saudners Company: Philadelphia, PA, USA, 1990; Volume 554, p. 556.

  40. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6. PMID: 13650640.

    Article  CAS  PubMed  Google Scholar 

  41. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95:351–8.

    Article  CAS  PubMed  Google Scholar 

  42. Reznick AZ, Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 1994;233:357–63. https://doi.org/10.1016/S0076-6879(94)33041-7.

    Article  CAS  PubMed  Google Scholar 

  43. Abou-Zeid SM, AbuBakr HO, Mohamed MA, El-Bahrawy A. Ameliorative effect of pumpkin seed oil against emamectin induced toxicity in mice. Biomed Pharmacother. 2018;98:242–51. https://doi.org/10.1016/j.biopha.2017.12.040.

    Article  CAS  PubMed  Google Scholar 

  44. Szkoda J, Żmudzki J. Determination of lead and cadmium in biological material by graphite furnace atomic absorption spectrometry method. Bull Vet Inst. 2005;49:89–92.

    Google Scholar 

  45. Salman NM. Accumulation of lead in the tissues and effects on growth rate of freshwater Cyprinus carpio. J Entomol Zool Stud. 2017;5(2):1499–502.

    Google Scholar 

  46. Bancroft JD, Gamble M. Theory and practice of histological techniques, 6th Edn. Elsevier, Churchill Livingstone. 2008.

  47. Sprague JB. Measurement of pollutant toxicity of fish, utilizing and applying bioassay results. Mars Res. 1973;4:3–32.

    Google Scholar 

  48. F?rat ?, Cogun HY, Y?zerero?lu TA, G?k G, F?rat ?, Kargin F, K?temen Y. A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem. 2011;37:657–66. https://doi.org/10.1007/s10695-011-9466-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mahboub HH, Beheiry RR, Shahin SE, Behairy A, Khedr MHE, Ibrahim SM, Elshopakey GE, Daoush WM, Altohamy DE, Ismail TA, El-Houseiny W. Adsorptivity of mercury on magnetite nano-particles and their influences on growth, economical, hemato-biochemical, histological parameters and bioaccumulation in Nile tilapia (Oreochromis niloticus). Aquat Toxicol. 2021;235:105828.

    Article  CAS  PubMed  Google Scholar 

  50. Saravanan A, Kumar PS, Karishma S, Vo DVN, Jeevanantham S, Yaashikaa PR, George CS. A review on biosynthesis of metal nanoparticles and its environmental applications. Chemosphere. 2021;264:128580.

    Article  CAS  PubMed  Google Scholar 

  51. Remya AS, Ramesh M, Saravanan M, Poopal RK, Bharathi S, Nataraj D. Iron oxide nanoparticles to an Indian major carp, Labeo rohita: impacts on hematology, iono regulation and gill Na+/K + ATPase activity. J King Saud University-Science. 2015;27(2):151–60.

    Article  Google Scholar 

  52. Ma M, Zhang Y, Yu W, Shen HY, Zhang HQ, Gu. N Colloids Surf a. 2003;212:219.

    Article  CAS  Google Scholar 

  53. Ali IM, Nassar MY, Kotp YH, Khalil M. Cylindrical-design, dehydration, and sorption properties of easily synthesized magnesium phosphosilicate nanopowder. Part Sci Technol. 2019;37(2):207–19.

    Article  CAS  Google Scholar 

  54. Kotp YH. Controlled synthesis and sorption properties of magnesium silicate nanoflower prepared by a surfactant-mediated method. Separ Sci Technol. 2017;52(4):657–70.

    Article  CAS  Google Scholar 

  55. Bagheri H, Afkhami A, Saber-Tehrani M, Khoshsafar H. Preparation and characterization of magnetic nanocomposite of Schiff base/silica/magnetite as a preconcentration phase for the trace determination of heavy metal ions in water, food and biological samples using atomic absorption spectrometry. Talanta. 2012;97:87–95.

    Article  CAS  PubMed  Google Scholar 

  56. Mohamed GA, Omar JA, Ezzeldin H, Kotp YH, Mohallel SA. Using Hydrogeochemical Approach in Groundwater Investigation of El Heiz Area, El Bahariya Oasis, Western Desert, Egypt. Egypt J Desert Res. 2023;73(1):213–37.

    Article  Google Scholar 

  57. Jurewicz A, Ilyas S, Uppal JK, Ivandic I, Korsching S, Mathur S. Evaluation of Magnetite nanoparticle-based toxicity on embryo – larvae stages of zebrafish (Danio rerio). ACS Appl Nano Mater. 2020;3(2):1621–9. https://doi.org/10.1021/acsanm.9b02330.

    Article  CAS  Google Scholar 

  58. Kim HJ, Mahboob S, Viayaraghavan P, Abdullah Al-Ghanim K, Al-Misned F, Ock Kim Y, Ahmed Z. Determination of toxic effects of lead acetate on different sizes of zebra fish (Danio rerio) in soft and hard water. J King Saud Univ Sci. 2020;32:1390–4. https://doi.org/10.1016/j.jksus.2019.11.032.

    Article  Google Scholar 

  59. Chaurasia MK, Nizam F, Ravichandran G, Arasu MV, Al-Dhabi NA, Arshad A, Elumalai P, Arockiaraj J. Molecular importance of prawn large heat shock proteins 60, 70 and 90. Fish Shellfish Immunol. 2016a;48:228–38.

    Article  CAS  PubMed  Google Scholar 

  60. Chaurasia MK, Ravichandran G, Nizam F, Arasu MV, Al-Dhabi NA, Arshad A, Harikrishnan R, Arockiaraj J. In-silico analysis and mRNA modulation of detoxification enzymes GST delta and kappa against various biotic and abiotic oxidative stressors. Fish Shellfish Immunol. 2016b;54:353–63.

    Article  CAS  PubMed  Google Scholar 

  61. Kumaresan V, Ravichandran G, Nizam F, Dhayanithi NB, Arasu MV, Al-Dhabi NA, Harikrishnan R, Arockiaraj J. Multifunctional murrel caspase 1, 2, 3, 8 and 9: conservation, uniqueness and their pathogen-induced expression pattern Fish Shellf. Immunol. 2016;49:493–504.

    CAS  Google Scholar 

  62. Hsu PC, Guo YL. Antioxidant nutrients and lead toxicity. Toxicology. 2002;180:33–44.

    Article  CAS  PubMed  Google Scholar 

  63. Osman AG, AbouelFadl KY, Abd El Baset M, Mahmoud UM, Kloas W, Moustafa MA. Bood biomarkers in Nile tilapia Oreochromis Niloticus Niloticus and African catfish Clarias gariepinus to evaluate water quality of the river Nile. J Fishscicom. 2018;12(1):1–15. https://doi.org/10.21767/1307-234x.1000141.

    Article  CAS  Google Scholar 

  64. Azua ET, Akaahan T. Toxic stress exhibited by juveniles of Clarias gariepinus exposed to different concentration of lead. J 2017 J Res Environ Sci Toxicol. 2017;ISSN(1):2315–5698.

    Google Scholar 

  65. Afshan S, Ali S, Ameen US, Farid M, Bharwan SA, Hannan F, Ahmad R. Effect of Different Heavy Metal Pollution on Fish. Res. J. Chem. Env. Sci. 2014; Volume 2 Issue 1 February 2014: 74–79.

  66. World Health Organization (WHO). WHO. guideline for clinical management of exposuretolead.2021; https://apps.who.int/iris/bitstream/handle/10665/347360/9789240037045-eng.pdf.

  67. Ahmed YH, Bashir DW, Abdel-moneam DA, Azouz RA, Galal MK. Histopathological, biochemical and molecular studies on the toxic effect of used engine oil on the health status of Oreochromis niloticus. Acta Histochem. 2019;121:563–74. https://doi.org/10.1016/j.acthis.2019.04.005.

    Article  CAS  PubMed  Google Scholar 

  68. Nwobi NL, Nwobi JC, Adejumo EN, et al. Blood lead levels, calcium metabolism and boneturnover among automobile technicians in Sagamu, Nigeria: implications for elevated risk of susceptibility to bone diseases. Toxicol Ind Health. 2021;37(11):705–13.

    Article  CAS  PubMed  Google Scholar 

  69. Karlsson HL, Cronholm P, Gustafsson J, Moller L. Copper oxide nanoparticles are highly toxic: a comparison between Metal Oxide nanoparticles and Carbon Nanotubes. Chem Res Toxicol. 2008;21:1726–32.

    Article  CAS  PubMed  Google Scholar 

  70. Pugazhvendan SR, Mariappan M, Leon PS, Balakrishnan JK. Bioaccumulation of lead in fresh water fish (Cyprinus Carpio). Int J C Res. 2012;4(7):146–8.

    Google Scholar 

  71. Mahboub HH, Shaheen AA. Mycological and histopathological identification of potential fish pathogens in Nile tilapia. Aquaculture. 2021;530:735849. https://doi.org/10.1016/j.aquaculture.2020.735849.

    Article  CAS  Google Scholar 

  72. Mohiseni M, Asayesh S, ShafieeBazarnoie S, Mohseni F, Moradi N, Matouri M, Mirzaee N. Biochemical Alteration Induced by Cadmium and lead in common carp via an experimental food chain. Iran J Toxicol. 2016; 10, 4, July-August 2016.

  73. Ţincu RC, Tomescu D, Coman L, Macovei RA. Biochemical parameters changes Induced by lead exposure. Farmacia. 2016;64:2.

    Google Scholar 

  74. Elgaml SA, Khalil R, Hashish EA, El-Murr A. Protective effects of Selenium and Alpha-Tocopherol against lead- Induced hepatic and renal toxicity in Oreochromis Niloticus. J Aquac Res Dev. 2015;6:1. https://doi.org/10.4172/2155-9546.1000299.

    Article  CAS  Google Scholar 

  75. Nourian K, Baghshani H, Shahsavani D. The effect of vitamin C on lead-induced plasma biochemical alterations in Fish, Cyprinus carpio. Iran J Toxicol. 2019;2:25–9.

    Article  Google Scholar 

  76. Tabrez S, Zughaibi TA, Javed M. Bioaccumulation of heavy metals and their toxicity assessment in Mystus Species. Saudi J Biol Sci. 2021;28:1459–64.

    Article  CAS  PubMed  Google Scholar 

  77. Al-Hasawi Z, Hassanine R. Effect of Heavy Metal Pollution on the blood biochemical parameters and liver histology of the Lethrinid Fish, Lethrinus harak from the Red Sea. Pakistan J Zool. 2022;1–8. https://doi.org/10.17582/journal.pjz/20220223170218.

  78. Al-Asgah NA, Abdel-Warith AA, Younis EM, Allam HY. Haematological and biochemical parameters and tissue accumulations of cadmium in Oreochromis niloticus exposed to various concentrations of cadmium chloride. Saudi J Biol Sci. 2015;22:543–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Majumder R, Kaviraj A. Cypermethrin induced stress and changes in growth of freshwater fish Oreochromis niloticus. Int Aquat Res. 2017;9:117–28. https://doi.org/10.1007/s40071-017-0161-6.

    Article  Google Scholar 

  80. Balali-Mood M, Naseri K, Tahergorabi Z, Khazdair MR, Sadeghi M. Toxic mechanisms of five heavy metals: Mercury, lead, Chromium, Cadmium, and Arsenic. Front Pharmacol. 2021;12:643972. https://doi.org/10.3389/fphar.2021.643972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Tang P, Liao Q, Tang Y, Yao X, Du C, Wang Y, Song F, Deng S, Wang Y, Qiu X, Yang F. Independent and combined associations of urinary metals exposure with markers of liver injury: results from the NHANES 2013–2016. Chemosphere. 2023;338:139455. https://doi.org/10.1016/j.chemosphere.2023.139455.

    Article  CAS  PubMed  Google Scholar 

  82. Walker HK, Hall WD, Hurst JW. Clinical methods: the history, physical, and Laboratory examinations. Volume PMID, 3rd ed. Boston: Butterworths; 1990. p. 21250045.

    Google Scholar 

  83. El-Houseiny W, Khalil AA, Abd-Elhakim YM, Badr HA. The potential role of turmeric and black pepper powder diet supplements in reversing cadmium-induced growth retardation, ATP depletion, hepatorenal damage, and testicular toxicity in Clarias gariepinus. Aquaculture. 2019;510:109–21. https://doi.org/10.1016/j.aquaculture.2019.05.045.

    Article  CAS  Google Scholar 

  84. El-Bouhy ZM, Reda RM, Mahboub HH, Gomaa FN. Chelation of mercury intoxication and testing different protective aspects of Lactococcus lactis probiotic in African catfish. Aquacult Res. 2021;00:1–14. https://doi.org/10.1111/are.15227.

    Article  CAS  Google Scholar 

  85. Patel M, Rogers JT, Pane EF, Wood CM. Renal responses to acute lead waterborne exposure in the freshwater rainbow trout (Oncorhynchusmykiss). Aquat Toxicol. 2006;80:362–71.

    Article  CAS  PubMed  Google Scholar 

  86. Nwobi NL, Nwob JC, Ogunbona RA, Adetunji AO, Anetor JI et al. Erythrocyte Acetylcholinesterase as a Biomarker of Environmental Lead Exposure 3 p.39. V. B. Patel editors, Biomarkers in Toxicology, Biomarkers in Disease: Methods, Discoveries and Applications. 2023. https://doi.org/10.1007/978-3-031-07392-2_4 Springer Nature Switzerland AG 2023.

  87. El-Khadragy M, Al-Olayan EM, Abou Arab A, Sebaee SE, Abou Donia MA, Elamin MH, et al. Effect of sub lethal concentrations of cadmium and lead on Oreochromis niloticus. Biomed Res. 2017;28(4):1–8.

    Google Scholar 

  88. El-Khayat HMM, Gaber HS, Flefel HE. Experimental studies on the toxicity of certain heavy metals and persistent organic pollutants on the Nile tilapia health. Egypt J Aquat Biology Fisheries. 2022;26(3):321–46.

    Article  Google Scholar 

  89. Hadi A, Shokr A, Alwan S. Effects of aluminum on the biochemical parameters of fresh water fish Tilapia zillii. Res J Appl Sci. 2009;3(1):33–41. ISSN:1993–6079.

    Google Scholar 

  90. Abdelzaher MF, Azab AM, Authman MMN, Shaban WM. Impact of Lead and Cadmium Chronic Exposure on Some Physiological Parameters of the Nile Tilapia (Oreochromis niloticus). Egyptian Journal of Aquatic Biology & Fisheries. 2022; 26(6):421–32.

  91. Garai P, Banerjee P, Mondal P, Saha NC. Effect of heavy metals on fishes: toxicity and bioaccumulation. J Clin Toxicol. S. 2021; 18.

  92. Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN. Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicol. 2014;7(2):60.

    Article  Google Scholar 

  93. Jomova K, Raptova R, Alomar SY, et al. Reactive oxygen species, toxicity, oxidative stress, and antioxidants: chronic diseases and aging. Arch Toxicol. 2023;97:2499–574. https://doi.org/10.1007/s00204-023-03562-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kamel S, Ahmed SAA, Elsayyad A et al. Toxicological insight of magnetite nanogel: neuro-ethological, hepato-renal, antioxidant, and histopathological traits in Clarias gariepinus. Aquacult Int. 2024. https://doi.org/10.1007/s10499-024-01456-w.

  95. Killian B, Yuan TH, Tsai CH, Chiu THT, Chen YH, Chan CC. Emission-related Heavy Metal Associated with oxidative stress in children: effect of antioxidant intake. Int J Environ Res Public Health. 2020;17(1):3920. https://doi.org/10.3390/ijerph17113920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Ferreira-Cravo M, Moreira DC, Hermes-Lima M. Glutathione depletion disrupts Redox Homeostasis in an anoxia-tolerant invertebrate. Antioxidants. 2023;12:1197. https://doi.org/10.3390/antiox12061197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Luo SY, Liu C, Ding J, Gao XM, Wang JQ, Zhang YB, Du C, Hou CC, Zhu JQ, Lou B, Wu XF, Shen WL. Scavenging reactive oxygen species is a potential strategy to protect Larimichthys crocea against environmental hypoxia by mitigating oxidative stress. Zool Res. Sep 2021;18(5):592–605. https://doi.org/10.24272/j.issn.2095-8137.2021.079. PMID: 34387415; PMCID: PMC8455462.

    Article  Google Scholar 

  98. Cheng CH, Ma HL, Liu GX, Deng YQ, Feng J, Jie YK, Guo ZX. Oxidative stress, DNA damage, and cellular response in hydrogen peroxide-induced cell injury of mud crab (Scylla paramamosain). Fish Shellfish Immunol. 2021;114:82–9.

    Article  CAS  PubMed  Google Scholar 

  99. Alfakheri M, Elarabany N, Bahnasawy M. Effects of lead on some oxidative stress of the African catfish, Clarias gariepinus. J Egypt Acad Soc Environ Develop. 2018;19(1):171–5.

    Article  Google Scholar 

  100. Loveline OC, Samuel PO, Arimoro F, Ayanwale A, Auta Y, Muhammed A. Effects of lead nitrate on catalase production levels in post juvenile Clarias gariepinus (Burchell, 1822). Int J Fish Aquacul. 2018;10:1–7.

    Article  CAS  Google Scholar 

  101. Saliu JK, Bawa-Allah KA. Toxicological effects of lead and zinc on the antioxidant enzyme activities of post juvenile Clarias gariepinus. Resour Environ. 2012;2:21–6.

    Article  Google Scholar 

  102. Olagoke O. Lipid peroxidation and antioxidant defense enzymes in Clarias gariepinus as useful Biomark-ers for Monitoring exposure to Polycyclic Aromatic Hydro-carbons. Lagos, Nige-ria: MSc Theses, University of Lagos; 2008. p. 70.

    Google Scholar 

  103. Alfanie I, Muhyi R, Suhartono E. Effect of Heavy Metal on Malondialdehyde and Advanced Oxidation Protein products Cencentration A Focus on Arsenic, Cadmium, and Mercury. J Med Bioeng. 2015;4:332–7. https://doi.org/10.12720/jomb.4.4.332-337.

    Article  CAS  Google Scholar 

  104. Al-Balawi HFA, Al-Akel AS, Al-Misned F, Suliman EAM, Al-Ghanim KA, Mahboob S, Ahmad Z. Effects of sub-lethal exposure of lead acetate on histopathology of gills, liver, kidney and muscle and its accumulation in these organs of clarias gariepinus. Braz Arch Biol Technol. 2013;56:293–302.

    Article  CAS  Google Scholar 

  105. Maiti AK, Saha NC, Paul G. Effect of lead on oxidative stress, na + K + ATPase activity and mitochondrial electron transport chain activity of the brain of Clarias batrachus L. Bull Environ Contam Toxic. 2010;84:672–6.

    Article  CAS  Google Scholar 

  106. Vona R, Pallotta L, Cappelletti M, Severi C, Matarrese P. The impact of oxidative stress in Human Pathology: Focus on Gastrointestinal disorders. Antioxidants. 2021;10:201. https://doi.org/10.3390/antiox10020201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kehm R, Baldensperger T, Raupbach J, Höhn A. Protein oxidation - formation mechanisms, detection and relevance as biomarkers in human diseases. Redox Biol. 2021;42:101901. https://doi.org/10.1016/j.redox.2021.101901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Neeratanaphan L, Kamollerd C, Suwannathada P, Suwannathada P, Tengjaroenkul B. Genotoxicity and oxidative stress in experimental hybrid catfish exposed to Heavy Metals in a municipal Landfill Reservoir. Int J Environ Res Public Health. 2020;17(6):1980. https://doi.org/10.3390/ijerph17061980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Ibrahim ATA. Effects of Mercury Chloride on oxidative stress biomarkers of some tissues of the African catfish Clarias gariepinus (Burchell, 1822). J Veterinar Sci Technol. 2015;6:242. https://doi.org/10.4172/2157-7579.1000242.

    Article  CAS  Google Scholar 

  110. Moussa MA, Mohamed HRH, Abdel-Khalek AA. Metal Accumulation and DNA damage in Oreochromis niloticus and Clarias gariepinus after Chronic exposure to discharges of the Batts Drain: potential risk to Human Health. Bull Environ Contam Toxicol. Jun; 2022;108(6):1064–73. https://doi.org/10.1007/s00128-022-03512-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Sultana S, Jabeen F, Sultana T, AL-Ghanim KA, Al-Misned F, Mahboob S. Assessment of heavy metals and its impact on DNA fragmentation in different fish species. Brazilian J Biology. 2020;80(4):823–8. https://doi.org/10.1590/1519-6984.221849.

    Article  CAS  Google Scholar 

  112. Mohammed EE, Mosad E, Zahran AM, Hameed DA, Taha EA, Mohamed MA. Acridine orange and flow cytometry: which is better to measure the effect of varicocele on sperm DNA integrity? Adv Urol. 2015;1–6. https://doi.org/10.1155/2015/814150.

  113. Jindal R, Verma S. In vivo genotoxicity and cytotoxicity assessment of cadmium chloride in peripheral erythrocytes of Labeo rohita (Hamilton). Ecotoxicol Environ Saf. 2015;118:1–10. https://doi.org/10.1016/j.ecoenv.2015.04.005.

    Article  CAS  PubMed  Google Scholar 

  114. Ratn A, Prasad R, Awasthi Y, Kumar M, Misra A, Trivedi SP. Zn2 + induced molecular responses associated with oxidative stress, DNA damage and histopathological lesions in liver and kidney of the fish, Channa punctatus (Bloch, 1793) Ecotoxicol Environ Saf. 2018;151:10–20. https://doi.org/10.1016/j.ecoenv.2017.12.058.

  115. Okeke ES, Nweze EJ, Ezike TC, Nwuche CO, Ezeorba TPC, Nwankwo CEI. Silicon-based nanoparticles for mitigating the effect of potentially toxic elements and plant stress in agroecosystems: A sustainable pathway towards food security. Science of the Total Environment. 2023; 898, 165446, ISSN 0048-9697, https://doi.org/10.1016/j.scitotenv.2023.165446.

  116. Rajkumar JSI, Tennyson S. Mercury Induced biochemical alterations as oxidative stress in Mugil cephalus in Short Term Toxicity Test. Curr World Environ. 2013;8:55–9.

    Article  CAS  Google Scholar 

  117. Lin Y, Miao L, Pan W, Huang X, Dengu JM, Zhang W, Ge X, Liu B, Ren M, Zhou Q, Xie J, Pan L, Xi B. Effect of Nitrite exposure on the antioxidant enzymes and glutathione system in the liver of bighead carp, Aristichthys nobilis Fish. Shellfish Immunol. 2018;76. https://doi.org/10.1016/j.fsi.2018.02.015.

  118. Dural M, Goksu ZL, Ozak AA. Investigation of heavy metal levels in economically important fish species captured from the Tuzla lagoon. Food Chem. 2007;102:415–21.

    Article  CAS  Google Scholar 

  119. Souid G, Souayed N, Yaktiti F, Maaroufi K. Lead accumulation pattern and molecular biomarkers of oxidative stress in seabream (Sparus aurata) under short term metal treatment. Drug Chem Toxicol. 2015;38:98–105.

    Article  CAS  PubMed  Google Scholar 

  120. Zhai Q, Wang H, Tian F, Zhao J, Zhang H, Chen W. Dietary Lactobacillus plantarum supplementation decreases tissue lead accumulation and alleviates lead toxicity in Nile tilapia (Oreochromis niloticus). Aquac Res. 2017;48:5094–103.

    Article  CAS  Google Scholar 

  121. Canli M, Stagg RM, Rodger G. The induction of metallothionein in tissues of the Norway lobster Nephrops norvegicus following exposure to cadmium, copper and zinc: the relationship between metallothionein and the metals. Environ Pollut. 1997;96:343–50.

    Article  CAS  PubMed  Google Scholar 

  122. Canli M, Atli G. The relationship between heavy metals (cd, cr, Cu, Fe, Pb and Zn) levels and the size of six Mediterranean fish species. Environ Pollut. 2003;121:129–36. PII: S0269-7491(02)00194-X.

    Article  CAS  PubMed  Google Scholar 

  123. Ay Ö, Kalay M, Tamer L, Canli M. Copper and lead Accumulation in tissues of a freshwater Fish Tilapia zillii and its effects on the branchial Na,K-ATPase activity. Bull Environ Contam Toxicol. 1999;62:160–8.

    Article  CAS  PubMed  Google Scholar 

  124. Victor K, Patience A, Oluwatoyin AJ. Accumulation of lead in the tissues of freshwater Catfish Clarias gariepinus exposed to static nominal concentrations of lead nitrate. Agric Biol J N Am. 2012;3(12): 510–515. https://doi.org/10.5251/abjna.2012.3.12.510.515 © 2012.

  125. Hwang IK, Kim KW, Kim JH, Kang JC. Toxic effects and depuration after the dietary lead(II) exposure on the bioaccumulation and hematological parameters in starry flounder (Platichthys stellatus). Environ Toxicol Pharmacol. 2016;45:328–33.

    Article  CAS  PubMed  Google Scholar 

  126. Kayhan FE, Büyükurganci N, Kaymak G. Accumulation of cadmium and lead in commercially important fish species in the Gulf of Gemlik, Marmara Sea, Turkey. Turkish J Aquat Sci. 2017;32(4):178–83.

    Article  Google Scholar 

  127. Giri SS, Kim MJ, Kim SG, Kim SW, Kang JW, Kwon J, Lee SB, Jung WJ, Sukumaran V, Park SC. Role of dietary curcumin against waterborne lead toxicity in common carp Cyprinus. Ecotoxicol Environ Saf. 2021;219:112318.

    Article  CAS  PubMed  Google Scholar 

  128. Dhaneesh KV, Gopi M, Ganeshamurthy R, Kumar TTA, Balasubramanian T. Bio-accumulation of metals on reef associated organisms of Lakshadweep Archipelago. Food Chem. 2012;131:985e91. https://doi.org/10.1371/journal.pone.0046286.

    Article  CAS  Google Scholar 

  129. Lee JW, Choia H, Hwanga UK, Kangb JC, Kangc YJ, Kimd KI, Kim JH. Toxic effects of lead exposure on bioaccumulation, oxidative stress, neurotoxicity, and immune responses in fish: a review. Environ Toxicol Pharmacol. 2019;68:101–8.

    Article  CAS  PubMed  Google Scholar 

  130. Stanek M, Dąbrowski J, Janicki B, Roślewska A, Strzelecka A. Impact of fish species on levels of lead accumulation in the meat of common bream (Abramis brama L.), white bream (Blicca bjoerkna L.) and common bleak (Alburnus alburnus L.) from the Vistula River (Poland). J Cent Eur Agric. 2015;16(2):62–71. https://doi.org/10.5513/JCEA01/16.2.1590.

    Article  Google Scholar 

  131. Mahboub HH, Shahin K, Mahmoud SM, Altohamy DE, Husseiny WA, Mansour DA, Shalaby SI, Gaballa MMS, Shaalan M, Alkafafy M, Abdel Rahman AN. Silica nanoparticles are novel aqueous additive mitigating heavy metals toxicity and improving the health of African catfish, Clarias gariepinus. Aquat Toxicol. 2022;249:106238. https://doi.org/10.1016/j.aquatox.2022.106238.

    Article  CAS  PubMed  Google Scholar 

  132. El-Moselhy KM, Othman AI, Abd El-Azem H, El-Metwally MEA. Bioaccumulation of heavy metals in some tissues of fish in the Red Sea. Egypt Egypt J Basic Appl Sci. 2014; 97e105.

  133. Sarma GK, Sen Gupta S, Bhattacharyya KG. Nanomaterials as versatile adsorbents for heavy metal ions in water: a review. Environ Sci Poll Res. 2019;26:6245–78.

    Article  CAS  Google Scholar 

  134. Chavan VR. Effect of lead on morphological and biochemical profile of fish liver. Int J Adv Sci Res. 2016; 1; Issue 9; Page 19–22.

  135. George OO, Amaeze NH, Babatunde E, Otitoloju AA. Genotoxic, histopathological and oxidative stress responses in Catfish, Clarias gariepinus, exposed to two antifouling paints. J Health Pollution. 2017 Dec 1;7(16):71–82.

  136. Authman MMN, Zaki MS, Khallaf EA, Abbas HH. Use of Fish as Bio-indicator of the effects of Heavy metals Pollution. J Aquac Res Dev. 2015;6:4. https://doi.org/10.4172/2155-9546.1000328.

    Article  CAS  Google Scholar 

  137. Patnaik BB, Howrelia H, Mathews T, Selvanayagam M. Histopathology of gill, liver, muscle and brain of Cyprinus carpio communis L. exposed to sublethal concentration of lead and cadmium. Afr J Biotechnol. 2011;10(57):12218–23.

    CAS  Google Scholar 

  138. Parashar RS, Banerjee TK. Toxic impact of lethal concentration of lead nitrate on the gills of air-breathing catfish Heteropneustes fossilis (Bloch). Veterinarski Arhiv. 2002;72(3):167–82.

    CAS  Google Scholar 

  139. Muñoz L, Weber P, Dressler V, Baldisserotto B, Vigliano FA. Histopathological biomarkers in juvenile silver catfish (Rhamdia quelen) exposed to a sublethal lead concentration. Ecotoxicol Environ Saf. 2015 Mar;1:113:241–7.

  140. Suiçmez M, Kayım M, Köseoğlu D, Hasdemir E. Toxic effects of lead on the liver and gills of Oncorhynchus mykiss WALBAUM 1792. Bulletin of Environmental Contamination & Toxicology. 2006 Oct 1;77(4).

  141. Khidr BM, Mekkawy IA, Harabawy AS, Ohaida AS. Effect of lead nitrate on the liver of the cichlid fish (Oreochromis niloticus): a light microscope study. Pakistan Journal of Biological Sciences: PJBS. 2012 Sep 1;15(18):854 – 62.

  142. Hinton DE, Lauren DL. Integrative histopathological approaches to detecting effects. Biol Indic Stress Fish. 1990;17:51.

    Google Scholar 

  143. Suresh N. Effect of cadmium chloride on liver, spleen and kidney melano macrophage centres in Tilapia mossambica. Journal of environmental biology. 2009 Jul 1;30(4).

  144. Rahman ANA, Elkhadrawy BA, Mansour AT, Abdel-Ghany HM, Yassin EMM, Elsayyad A, Alwutayd KM, Ismail SH, Mahboub HH. Alleviating effect of a Magnetite (Fe3O4) Nanogel againstwaterborne-lead-Induced physiological disturbances, histopathological changes, and lead Bioaccumulation in African Catfish. Gels. 2023;9:641. https://doi.org/10.3390/gels9080641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Moezzi A, Soltanali S, Torabian A, Hasani A. Removal of Lead from Aquatic Solution Using Synthesized Iron Nanoparticles. Int. J. Nanosci. Nanotechnol. 2017 March;13(1):83–90.

Download references

Acknowledgements

Y.H.K would like to thank Science and Technology Development Fund Authority (STDF) FLUG Call 1 - Project ID 46655, for supporting the devices used in full characterization of nanomaterial present in this study.

Funding

All authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB).

Author information

Authors and Affiliations

  1. Department of Veterinary Hygiene and Management, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Hanan S. Khalefa

  2. Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Huda O. AbuBakr & Samira H. Aljuaydi

  3. Department of Biochemistry, Faculty of Veterinary Medicine, Egyptian Chinese University, Cairo, Egypt

    Huda O. AbuBakr

  4. Hydrogeochemistry Department, Desert Research Center, Cairo, 11753, Egypt

    Yousra H. Kotp

  5. Department of Pathology, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Asmaa K. Al-Mokaddem

  6. Department of Aquatic Animal Medicine and Management, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Dalia A. Abdel-moneam

Authors
  1. Hanan S. Khalefa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huda O. AbuBakr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samira H. Aljuaydi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yousra H. Kotp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asmaa K. Al-Mokaddem
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dalia A. Abdel-moneam
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors have read and agreed to the submitted version of the manuscript. H.S.K. and D.A.A. contribute equally to this work. Conceptualization, methodology, investigation, experimental work, biochemical and tissue residual analyses, writing–original draft, writing–review and editing were performed by H.S.K. and D.A.A.; Methodology, writing–review and editing, oxidative stress parameters and DNA fragmentation were analyzed by H.O.A. and S.H.A.; Methodology, writing–original draft, full characterization of Nanomaterial were done by Y.H.K.; Histopathological analysis and writing–original draft, were performed by A.K.A.

Corresponding authors

Correspondence to Hanan S. Khalefa or Dalia A. Abdel-moneam.

Ethics declarations

Ethics approval and consent to participate

This study was performed in Faculty of Veterinary Medicine, Cairo University, Giza, Egypt, the fish farm owners provided their oral informed consent prior to the collection of experimental fish. All fish experimental protocols were conducted according to ethical guidelines of the Institutional Animal Use and Care Committee (Vet. CU. IACUC), for the use of laboratory animals with the approval code Vet CU25122023864.

Consent for publication

Not applicable.

Competing interests

The authors have no competing interests to declare that are relevant to the content of this article.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khalefa, H.S., AbuBakr, H.O., Aljuaydi, S.H. et al. Aquatic assessment of the chelating ability of Silica-stabilized magnetite nanocomposite to lead nitrate toxicity with emphasis to their impact on hepatorenal, oxidative stress, genotoxicity, histopathological, and bioaccumulation parameters in Oreochromis niloticus and Clarias gariepinus. BMC Vet Res 20, 262 (2024). https://doi.org/10.1186/s12917-024-04094-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-024-04094-9

Keywords

BMC Veterinary Research

ISSN: 1746-6148

Contact us