Abstract
Trace element bioaccumulation in marine organisms is a rising international issue due to possible health concerns for humans. Thirteen trace elements were analyzed in the sediment, water, and muscular tissue of Red Sea fish. Additionally, the average daily intake (EDI), the cancer risk (CR), the hazard index (HI), and the target hazard quotient (THQ) of those elements have been taken into consideration when evaluating any possible health concerns related to their consumption. All species presented quantifiable values in muscle for all the analyzed elements (arsenic (As), lead (Pb), copper (Cu), aluminum (Al), boron (B), iron (Fe), barium (Ba), manganese (Mn), nickel (Ni), cadmium (Cd), chromium (Cr), zinc (Zn), and mercury (Hg), except for Cd and Hg, being Fe and Zn the most accumulated elements in all species. Conversely, in water samples, most elements were undeleted except for aluminum, boron, iron, and zinc. All Red Sea fish, however, had concentrations of Zn, Ni, Fe, Cu, and Mn below the upper limit allowed, although most species had higher levels of As, Cr, and Pb (0.48 ± 0.83–5.10 ± 0.79, 1.97 ± 0.46–5.25 ± 0.67 and 2.12 ± 1.01–6.83 ± 0.93 µg/g, respectively).
The studied Red Sea fish showed contamination degrees (CD) of Mn, Cu, Fe, Ni, Zn, and Pb were ≤ 1, indicating minimal contamination, with As and Cr showing higher contamination degrees. However, the pollution index values (MPI-elements) can be represented according to ascending order: Lethrinus ramak < Cephalopholis hemistiktos < Pagellus affinis < Trachurus japonicus < Cheilinus lunulatus < Siganus luridus < Parupeneus forsskali < Caesio suevica. The study found that edible tissues are safe for human consumption, with HI values for children and adults less than ten, indicating negligible non-cancer hazards. However, fish consumption presents health risks due to chromium, lead, and arsenic, with THQ values several times greater than 1, and CR-Ni, CR-Cr, and CR-As values exceeding the acceptable 10−4 value in all studied species. This study provides critical insights into trace element contamination in marine fish species, highlighting the need for ongoing monitoring and proactive measures to ensure safe marine fish consumption in the Aqaba Gulf.
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Introduction
Fish plays a significant role in the nutritional intake of humans and is a vital and excellent supply of omega-3 polyunsaturated fatty acids, minerals, amino acids, and vitamins in comparison to other animal meats and is also easily digested by consumers [5]. Various pollutants may be concentrated more in the Aqaba Gulf region as a result of these operations. Among these pollutants, trace elements pose a major risk to marine habitats due to their poisonous properties.
Trace elements are one of the most prevalent pollutants that marine organisms consume and move through trophic categories via food, sediment, water, or environmental factors [6]. In aquatic environments, fish inhabit the upper trophic levels and have the highest trophic position in the food chain [7]; they are largely responsible for the delivery of contaminants to people [8]. Trace elements accumulate in fish at minor levels via bioaccumulation and at higher concentrations via the biomagnification process; however, people may consume elements via food consumption, which may cause adverse health consequences in the short term [9, 10]. Non-essential elements like Ba, Cr, Pb, Al, As, Cd, and Hg have no biological significance in any manner [11], while essential trace elements like B, Cu, Fe, Mn, Zn, and Ni are required at trace levels for varieties of enzymatic and physiological activities [12, 13]. Elements require a great deal of attention because they cannot be biodegradable, endure for a long time in aquatic systems, and then build up via biomagnification at progressively higher levels throughout the food chain [14].
The bioaccumulation of trace elements in aquatic organisms is regulated by both internal and external variables. Environmental factors that reflect external variables are element bioactivity, temperatures, and the alkalinity of ambient aquatic habitats; internal variables include habitat, size, species, ecology, gender, eating habits, and physiological processes [15]. In the previous years, several studies have documented element pollutants in the carb and bivalve [16], shrimp [17] fish [18,19,20,21,22], crayfish [23, 24] mussel [25], aquatic macrophytes [26, 27] sediment [28,29,30], and seawater [31, 32].
Possible threats to health associated with trace element consumption have been established for several decades. Trace elements have either non-cancer or cancer risks for people [33]. Trace elements pose risks to human health, including liver dysfunction, kidney disease, and skeletal deformity, due to their prolonged and indecomposable presence within the human visceral organ systems [34]. Therefore, it is imperative to investigate the possible health concerns associated with consuming tainted meals. The following were the study’s principal objectives: (1) measure the levels of trace elements in the sediment, water, and muscular tissue of eight Red Sea fish species that were collected from the Aqaba Gulf at the Egyptian Red Sea coast; (2) identify the factors that lead to the bioaccumulation and biosedimentation of elements; (3) assess the possible environmental impacts of trace elements on the region’s aquatic ecosystems; and (4) ascertain the possible health hazards linked to eating Red Sea fish. In addition, the study aimed to provide baseline data for health and environmental policies to reduce the hazard effects of trace elements pollution along the Aqaba Gulf region while preserving the natural environment and human health.
Materials and Methods
Field of Investigation
The Aqaba Gulf, regarded as one of the most significant aquatic regions in the southern part of the Sinai Peninsula, stretches along the eastern shore of the Red Sea. It is 180 km long, 20 km wide, and 800 m deep. It is situated at 28° N latitudes, 34°23′ E longitudes, and 29°33′ N latitudes, 35°0′ E longitudes [35, 36]. Along the Gulf of Aqaba, there are several towns that are home to a variety of human activities. One such area is Nuweiba City, which is located on the western shore of the Aqaba Gulf. Here, strategic industries and a variety of human activities have an impact on the marine environment in front of the city. Nuweiba City is situated at 28°50′2.7″ N latitude and 34°37′29.6″ E longitude (Fig. 1).
Google map showing the samples’ collection area on Nuweiba City, Aqaba Gulf at the Egyptian Red Sea Coast
The region of investigation is subject to various sources of pollution, including petrochemical industries, fishing activities, and anthropogenic activities including tourism and ship transformation in Nuweiba port [36, 37]. Marine environment and public health are at risk due to these sources’ elevated levels of trace elements in the sediments, fish, and water. In this regard, studies on trace element concentrations and their impacts on the environment and public health are crucial.
Sample Collection
Seawater samples were collected at 3 locations (three samples per location) in the Aqaba Gulf using a Ruttner Water Sampler while sediment samples were collected from the same sites using Van Veen Grab Sampler. Eight Red Sea fish were purchased from the local fishermen in Nuweiba City at the collection time when water and sediment samples were collected during October and December 2023. Fish samples (five samples per species, Table 1) were kept in a container with ice and brought to the Faculty of Science laboratory et al.-Azhar University in Egypt. About 10 g of white muscular tissue was removed from the ventral surface anterior to the dorsal fin in the lab. In the lab, the muscular tissues were placed in plastic bags and frozen until analysis.
Trace Element Measurements
Cd, Al, As, Zn, B, Hg, Ba, Cr, Mn, Fe, Pb, Cu, and Ni levels were measured in water, sediment, and in the muscular tissues of Red Sea fish. Fresh samples weighing about 0.5 g were put in 50-mL digestion tubes containing ultrapure HNO3 (65%, 5 mL) and H2O2 (30%, 1 mL). On the hot plate, the mixture was heated until it was well-digested. Following a period of cooling at ambient temperature, the digested specimens were transferred to volumetric flasks and combined with 1% HNO3 to make an ending volume of 25 mL [38]. After filtering the seawater sample using a 0.45-µm filter, 50 mL of samples was acidified with 65% HNO3 and 37% HCl, purchased from Merck, Germany, according to APHA [39]. However, the collected sediment was dried overnight at 105 °C, then finely ground, homogenized, and sieved using a 63-µm mesh to select particles smaller than 63 µm. Microwave digestion was used to digest the prepared sample (1.0 g), which was put in a covered Teflon container (Anton-Paar microwave digestion system, Multiwave PRO, with Rotor 8NXF100) with acid mixtures of HNO3 (9 mL) and HCl (3 mL) according to EPA method 3051A [40]. Following a period of cooling at ambient temperature, the digested sediment was put in volumetric flasks and combined with deionized water to make an ending volume of 50 mL.
The final solutions of muscles, water, and sediment were determined to have trace elements contents using the ICP-OES technique (inductively coupled plasma optical emission spectrometry, Agilent 5100 series, Australia) and SVDV (synchronous vertical dual view) with continuous flow hydrogen generation and advanced cold vapor systems. The NIST (National Institute of Standards and Technology) provided standard reference material, an external reference, and a quality control sample to verify the accuracy and precision of the trace elements readings. The recoveries of standard reference metals were 90–110%. Trace element concentrations in the fish muscles (on a wet weight basis (ww-b)) and sediment (on a dry weight basis (dw-b)) were measured in µg/g, whereas those in the water were measured in mg/L. The limits of detection (LOD) and limits of quantification (LOQ) of trace elements are shown in Table 1S.
Bio-concentration Factor Calculation
According to Adolfsson-Erici et al. [41], the bioaccumulation factor (BAF) can be computed as represented in Eq. (1):
where M-fish represents the trace element level in fish muscles (mg/kg), and M-water represents the trace element level in water (mg/L). However, the Eq. (2) [42] was used to compute the biosedimentation factor (BSF):
where M-sediment represents the level of trace elements in the sediments (µg/g), and M-fish represents the level of trace elements in the fish muscles (µg/g).
Environmental Risk Measurement
Numerous indices are used to measure the degree of trace element contamination in aquatic species [43]. In this study, the degree of trace element pollution was assessed using the contamination degree (CD) and the metal pollution index (MPI).
Contamination Degree (CD)
Using element levels in the Red Sea fish, the CD was calculated as the following equation (Eq. (3)):
where CM represents trace element level in fish (μg/g ww-b), and CBL represents background concentrations of iron, lead, Cd, copper, Ni, and zinc [44].
CD values | Interpretation |
|---|---|
CD ≤ 1 | Minimal limit of contamination |
1 < CD ≤ 2 | Low contamination degree |
2 < CD ≤ 3 | Moderate contamination |
CD > 3 | High degree of contamination |
Metal Pollution Index (MPI)
An integrated method for evaluating trace element contamination is MPI. The MPI was estimated using the Eq. (4) [43]:
where M1 is the first element level, M2 is the second element level, M3 is the third element level, n is the number of examined elements and Mx is the xth element level (µg/g ww-b) in the Red Sea fish.
MPI values | Interpretation |
|---|---|
MPI ≤ 1 | Safe |
2 < CD ≤ 3 | Slightly polluted |
3 < CD ≤ 5 | Moderately polluted |
CD > 10 | Heavily polluted |
Health Risk Measurement
The potential health risks caused by trace elements ingested by consumption of the muscular tissue of the fish were evaluated according to a method reported by the US Environmental Protection Agency [45]. By measuring trace element levels in the muscles, the estimated daily intake (EDI), non-cancer, and cancer indices were all calculated.
Estimated Daily Intake (EDI)
The exposure dosage resulting from direct human eating of certain elements shown in muscular tissue was determined using the EDI (the daily average intake of a certain element over the lifespan). The subsequent equation (Eq. (5)) was used to compute the EDI [46].
where the EP relates to the lifespan of the exposure period (70 years); the IR denotes the ingestion rate of fish consumption by adults (41 g/day) and children (27 g/day); M denotes the trace element levels (μg/g ww-b) in muscular tissue; ER stands for exposure rate (365 days year−1); BW denotes the body weight of adults (70 kg) and children (30 kg); and AT (365 days × 70 years) is the average lifespan [45].
Target Hazard Quotient (THQ)
The THQ, a non-cancer evaluation of adverse health effects linked to the intake of certain trace element contaminants in muscular tissue, was developed for evaluating human health risk. The ratio of EDI to RfD (oral reference dosage) was employed for determining THQ as in Eq. (6):
The RfD values (mg/kg/day) were Ni (0.02), Cu (0.04), Ba (0.2), Pb (0.00357), Cr (0.003), As (0.003), Mn (0.14), Fe (0.7), and Zn (0.3), in accordance with guidelines provided by USEPA [45].
Hazard Index (HI)
According to Cui et al. [47], the HI is an additional computational equation that represents the effect of non-cancer hazards as the total of the THQ values for the trace elements being studied.
Cancer Risk (CR)
The following formula (Eq. (8)) was used to get the CR values, which represent the incremental risk of develo** cancer based on the cancer slope factor [CSF, 48, 49]: 1.7, 0.5, 0.0085, and 1.5 mg/kg/day for Ni, Cr, Pb, and As, respectively.
Statistical Calculation
The statistical program SPSS (version 22) was used to perform the statistical analyses. To prove homogeneity of variation and a normal distribution, Levene’s test was employed. To find any statistically significant differences (p < 0.05) between the trace element levels in the sediment, water, and fish species, analysis of variance (one-way ANOVA) was utilized to statistically examine the results [50]. Also, the correlations between the trace element levels in Red Sea fish were assessed using Pearson’s correlation coefficient. Tables displaying the statistics are formatted as means ± standard deviation.
Results and Discussion
A significant aquatic environmental issue for aquatic biota is the accumulation of trace elements in aquatic ecosystems because of their increased stability, bioaccumulation, and biomagnification capabilities. Additionally, when these elements move through the food chain, they eventually have an impact on individuals [51]. In aquatic environments, sediments play a crucial role by absorbing and storing a variety of necessary materials as well as hazardous pollutants [52]. Compared to water, analysis of sediment gives accurate estimations for contaminants, which are absorbed by particulates tending to sink on bottoms [53]. It is crucial to get up-to-date information on the levels of toxic trace elements in a variety of Red Sea species in order to comprehend the possible risk of trace elements in these fish to consumers. The concentration of trace elements, such as Cr, Al, Ba, As, B, Cd, Cu, Fe, Pb, Hg, Zn, Mn, and Ni in seawater, sediment, and fish, was determined using the ICP-OES technique.
Trace Element Levels in Sediment and Water Samples
Table 2 shows the levels of trace elements in the water and sediment of Aqaba Gulf stations. Thirteen trace element levels were reported in the water, and the levels of cadmium and mercury in the sediment were below the detection limit of the ICP-OES technique. Conversely, in water samples, most elements were undetected except for aluminum, boron, iron, and zinc. However, the trace elements in water samples from Aqaba Gulf stations varied from 0.01 ± 0.003 for Zn to 2.86 ± 0.06 mg/l for B elements. Moreover, the maximum levels of elements in sediment samples were recorded for iron (1327.00 ± 524.39 mg/kg), and the minimum levels exhibited 0.53 ± 0.06 mg/kg, for Pb elements. The examined essential trace elements in the water of the Aqaba Gulf were below the allowed level when compared to the acceptable limit [54]. Due to absorption by suspended matter and sediment particles, which quickly remove the trace elements from the water column, the majority of trace elements had low concentrations [55]. Trace element concentrations in the sediment are useful for evaluating pollution trends, and polluted sediment containing trace elements may serve as another source of contamination for the aquatic environment [56]. In the current study, the trace elements studied in the sediment of the Aqaba Gulf were also lower than in the upper continental crust [57].
The Levels of Trace Elements in Red Sea Fish
Fish pollution with trace elements poses a serious risk to both aquatic life and people. Assessing the level of element contamination in muscular tissues begins with measuring the level of trace elements [58]. The levels of trace elements in the muscular tissues of Red Sea samples collected from the Aqaba Gulf are represented in Table 3. The assessment of trace element levels in various fish species, including L. ramak, S. luridus, P. forsskali, T. japonicus, P. affinis, and C. lunulatus, reveals distinctive concentrations of aluminum, arsenic, boron, barium, chromium, copper, iron, lead, zinc, manganese, and nickel in their muscular tissues. In the comprehensive assessment of trace element concentrations within the muscular tissues of various fish species, noteworthy variations were discerned across multiple elements. This intricate pattern of element concentrations within distinct fish species provides valuable insights into the dynamics of trace element accumulation in marine ecosystems. Such variations are to be expected, as the accumulation of trace elements in muscular tissue is dependent on a number of variables, including the trace element concentration in the water, exposure duration, uptake mechanism, and the surrounding environment (pH, dissolved oxygen, temperature). For intrinsic factors, such as habitat, feeding habits, and age [59], several studies have demonstrated that fish trace element levels are mostly dependent on the type of environment they live in [58, 60, 61]. It is widely known that sediment is the primary mechanism for trace element pollution absorption and that it is essential to trace elements [62].
Arsenic exhibited its peak level at 5.10 ± 0.79 µg/g in P. forsskali, juxtaposed with its lowest level of 0.48 ± 0.83 µg/g in C. lunulatus. Al displayed its highest level at 4.36 ± 0.93 µg/g in C. suevica, while its lowest level was recorded at 1.93 ± 0.37 µg/g in L. ramak. Ba reached its zenith in C. lunulatus at 2.45 ± 0.80 µg/g, while L. ramak manifested the lowest level at 0.95 ± 0.65 µg/g. Pb levels peaked in P. forsskali at 6.83 ± 0.93 µg/g and reached their nadir in C. lunulatus at 2.12 ± 1.01 µg/g. Cr demonstrated a peak level of 5.25 ± 0.67 µg/g in C. suevica, contrasting with its nadir of 1.97 ± 0.46 µg/g in C. lunulatus. Cu levels were most elevated in C. lunulatus at 10.29 ± 1.66 µg/g and least in P. forsskali at 2.11 ± 0.51 µg/g. Fe levels displayed considerable disparity, with the highest observed in C. suevica at 81.35 ± 7.62 µg/g and the lowest in T. japonicus at 31.80 ± 5.94 µg/g. Moving to boron, S. luridus showcased the highest level at 10.51 ± 0.35 µg/g, whereas C. suevica featured the lowest at 5.18 ± 0.83 µg/g. Zn levels revealed a wide range, with P. forsskali featuring the highest at 19.75 ± 1.21 µg/g and C. hemistiktos registering the lowest at 7.02 ± 1.61 µg/g. Manganese (Mn) levels showed a peak of 1.31 ± 0.53 µg/g in C. lunulatus, contrasting with a trough of 0.50 ± 0.03 µg/g in P. affinis. Finally, nickel (Ni) levels reached their zenith in P. forsskali and C. hemistiktos (1.76 ± 0.40 µg/g), while L. ramak exhibited the lowest at 1.20 ± 0.31 µg/g. In the present study, Zn and Fe were the highest trace elements in the muscles of Red Sea fish, which was in agreement with the result of Younis et al. [63].
The essential elements, Al and Ba in the muscular tissues of studied fish were lower than the global acceptable limits provided by different agencies [64,65,66,67]. However, the levels of As were higher than the maximum permissible level in all Red Sea fish, except in C. lunulatus. Moreover, the levels of Pb in all studied fish were above the uppermost allowable limit. Furthermore, the levels of Cr were higher than the maximum allowable level in all fish, except in C. lunulatus and C. suevica.
Fish that live close to sediment consume humic materials, and benthic invertebrates collect and supply fish trace elements from the sediment [68]. Consequently, compared to demersal fish, benthic and benthopelagic organisms often show higher levels of trace elements [61]. Additionally, a previous investigation concluded that upper-trophic-level piscivorous organisms appear to collect more trace elements than omnivorous and herbivorous organisms in terms of trace element levels [62], which supports the present study. This result suggests that the trace element levels in aquatic organisms are not only affected by the surrounding environment but also bioaccumulated via their food [68, 69]. A comprehensive overview of trace element concentrations in various fish species, encompassing L. ramak, S. luridus, P. forsskali, T. japonicus, P. affinis, C. lunulatus, C. suevica, and C. hemistiktos, reveals distinctive patterns in their muscular tissues. Iron consistently dominates with the highest concentration, followed by varying levels of other trace elements. The lowest concentrations are notably found in manganese, nickel, and specific elements depending on the fish species, suggesting potential similarities or differences in element uptake and accumulation mechanisms.
A comparison of the trace element levels (µg/g ww-b) in marine fish species of the present study with the previous studies is represented in Table 4. The level of Al in the current study was lower than those recorded by Mziray and Kimirei [70]. The As level in the current study was within that recorded by Mziray and Kimirei [70] while it was higher than that reported by Al-Amri et al. [71]. The Cr level in the current study was higher than that recorded by [70,71,72], while it was lower than that reported by Younis et al. [21]. The Cu level in the current study was higher than that recorded by [71,72,73]. The Fe level in the current study was within that recorded by Mziray and Kimirei [70] and higher than that reported by [71, 72]. The Pb level in the current study was higher than that reported by [21, 58, 70, 72]. The Zn level in the current study was lower than that determined by Mziray and Kimirei [70] and higher than that reported by [21, 58, 71,72,73]. The Mn level in the current study was lower than that recorded by Mziray and Kimirei [70] and higher than that reported by [21, 72]. The Ni level in the current study was lower than that recorded by Younis et al. [21], while it was higher than that reported by [58, 70,71,72,73].
Trace Element Correlation Coefficient
Figure 2 displays the correlation coefficient between trace elements in the muscular tissue of Red Sea fish, as established by the heatmap data. In this study, significant positive correlations were reported for Al with Ba, Cr, Fe, and Mn; As-Pb; Ba-B; Ba-Mn; Mn-Fe, Zn-Pb, and Zn-Mn. According to Yakamercan et al. [75], the positive correlation indicates that the behavior is the same and has a common origin. On the other hand, As was shown to have significant negative associations with B, Ba, and Cu, as well as Cu-Pb. According to Jiang et al. [62], a negative correlation suggests the presence of various sources, mostly dyes and chemicals. Additionally, a hierarchical clustering method according to Euclidean distance was applied to construct relationships for interdependence between the eleven studied trace elements (Fig. 1S). The findings indicated that the ten trace elements were arranged into two major groups (Cu and Zn in cluster 1 and Al-As-B-Ba-Cr-Pb-Mn-Ni in cluster 2), with Fe standing out as belonging to a different group. These findings also indicated that most of the elements originated from the same origins, except for Fe. According to Chai et al. [76], contamination of the marine environment and the transition mechanism of trace elements on different substrates were also significant contributing factors to the origins of elements.
Heatmap showed the correlation coefficient between trace elements in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
BAF and BSF Values
Bioconcentrations of trace elements associate the number recovered from the portion of collected concentration in a specific organ of different species and the habitat quickly and effectively [77]. The BAF values of trace elements in the Red Sea species are represented in Fig. 3. All studied Red Sea species represented the BAF values in this sequencing order: B < Al < Fe < Ba < Zn.
BAF values of trace elements in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
All species possessed bioaccumulative capability with ascending as BAF-B < BAF-Al < BAF-Fe < BAF-Ba < BAF-Zn were reported in the muscles with the same way of ordination. Among all the species, the BAF value was the highest in P. forsskali (1975.3 for BAF-Zn) and the lowest in C. suevica (1.82 for BAF-B). In fact, the bioaccumulation of an aquatic species relies on its characteristics, metabolism of inspected tissue, invasion pathways, and habitat condition [78]. Based on the value ranges, BAF can be classified as follows: BAF < 1000: no accumulation probability; 1000 < BAF < 5000: bioaccumulative organism; BAF > 5000: extremely accumulative organism [79]. The current study revealed that BAF-Al, BAF-B, BAF-Ba, and BAF-Fe values in all studied fish were lower than 1000. However, BAF-Zn values in L. ramak, C. hemistiktos, P. affinis, and S. luridus were lower than 1000, whereas they were higher than 1000 in C. suevica, C. lunulatus, T. japonicas, and P. forsskali, which means these species are bioaccumulative organisms of Zn from water.
However, the BSF values based on the studied elements (Al, As, B, Ba, Cr, Cu, Fe, Pb, Zn, Mn, and Ni) in the Red Sea species were recorded in Fig. 4. All the studied Red Sea species exhibited BSF values that were < 1 recorded for Al, Mn, Fe, Ba, and Ni, while they were greater than 2 recorded for Cu and Pb. Fish can be classified according to the values of BSF > 2, 1 < BSF < 2, and BSF < 1 as macro-concentrators, micro-concentrators, and de-concentrators, respectively [80]. In the current study, the BSF-Al, BSF-Ba, BSF-Mn, and BSF-Ni were < 1 in all fish species, whereas the BSF-Pb was > 2 in all Red Sea fish. However, the BSF-Zn values were > 2 in all species except L. ramak (1.39), C. hemistiktos (1.20), P. affinis (1.24), and S. luridus (1.79). Moreover, BSF-As values were > 2 in all fish except C. hemistiktos (1.45), C. lunulatus (0.40), and S. luridus (1.04). Additionally, the BSF-B values were 1 < BSAF < 2 in all species except S. luridus (2.22). Furthermore, the BSF-Cr values were lower than 1 in all species except L. ramak (1.09), C. suevica (2.00), and P. forsskali (1.24). On the other hand, the BSF-Cu values were > 2 in all fish except L. ramak (1.81) and P. forsskali (1.71).
BSF-element values in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
PCA Analysis
In PCA, the components were taken into account whose eigenvalues were greater than 0.5 (Table 5). PCA explained 99.73% of the data variation, and a total of 8 significant PCs were extracted with an eigenvalue > 1. PC1 explained 88.27% of the total variances and exhibited an eigenvalue of 268.379. PC1 was dominated by Fe, with loadings of 0.99. The employed PCA revealed that the source of origin of the element was anthropogenic. B, As, Al, Cu, Pb, Ni, and Fe were the dominant compounds in PCA analysis due to their high loading scores in their respective components. PC2 explained around 7.36% of the total variance, and Zn contained the highest loading scores (0.89). Besides, PC3 explained 2.84% of the total variance and was dominated by Cu (0.67), whereas PC4 explained 0.82% of the total variance with a maximum loading of B (0.68). PC5 explained 0.45% of the total variance with a maximum loading of As (0.68) and B (0.50). The loadings of As and Pb are very close in PC5, which represents a similar source of these elements. However, PC6 explained around 7.82% and 6% of the total variance with the maximum loading of Zn (0.55) and Fe (0.67), respectively. Besides, PC7 explained 0.23% of the total variance with a maximum loading of Pb (0.82), and PC8 explained 0.04% of the total variance with a moderately favorable loading of Ni (0.52).
Environmental Risk Assessment
The degree of contamination was evaluated by the contamination factor and the element pollution index [81]. The contamination factor (CD) and element pollution index (MPI) were represented in Figs. 5 and 6, respectively.
The CD values of trace elements in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
The MPI values of trace elements in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
Contamination Degree (CD)
The CD values were calculated based on the levels of As, Cr, Cu, Fe, Pb, Zn, Mn, and Ni. However, the contamination factors for Cu, Fe, Pb, Zn, Mn, and Ni were lower than 1, which indicates a minimal limit of contamination in the Red Sea fish. Moreover, Cf-As in C. lunulatus, S. luridus, and C. hemistiktos were ≥ 1, while the remaining species recorded a high degree of contamination (CD-As > 3), which was ordered in the following sequence: T. japonicus (3.56) < L. ramak (3.58) < C. suevica (3.95) < P. affinis (5.00) < P. forsskali (5.10). On the other hand, the contamination degrees of Cr were denoted as a low contamination degree (1 < CD-Cr ≤ 2) in all studied fish samples except C. suevica (2.63), which was denoted as a moderate contamination degree. The CD values indicate the contamination level. The calculated CD values for Cu, Fe, Pb, Zn, Mn, and Ni were < 1, which indicates a minimal limit of contamination in the Red Sea fish (Fig. 5).
Element Pollution Index (MPI)
MPI is generally used to define the polluted degree of trace elements in the tissues of fish. It is considered that the higher value of the estimated MPI describes the higher degree of contamination in fish [82]. The MPI based on elements (Al, As, B, Ba, Cd, Cr, Cu, Fe, Pb, Zn, Hg, Mn, and Ni) in the muscles of nine Red Sea species is presented in Fig. 6. MPI varied from 2.63 in L. ramak to 4.63 in C. suevica and was severely contaminated. However, it was higher than 1 for CD-As and CD-Cr in the studied fish except in C. lunulatus. However, MPI compared total element levels between samples [83]. Hence, the more contaminated samples have higher MPI levels [42, 82]. In the present study, the contamination degree based on MPI values of trace elements in studied fishes can be classified as follows: L. ramak (2.63) < C. hemistiktos (3.10), < P. affinis (3.16), < (3.17) < T. japonicus (3.25), C. lunulatus (3.43) < S. luridus (3.50), < P. forsskali (3.92) < C. suevica (4.63). Low levels of MPI in the muscle might be related to low metabolic activity and low element-binding proteins in this muscle [84, 85]. The highest MPI value was obtained for C. suevica and the lowest for L. ramak. MPI was considered using trace element concentrations in the fish species and was used to compare the total element contents of the muscle of the examined fish.
Human Health Risk Assessment
Fish are one of the main sources of protein for the human diet worldwide, but they are also known as being the largest bioaccumulators of trace elements due to their position at the top of the food web and food chain in both freshwater [86] and marine ecosystems [87]. The high content of elements, including both transitional elements and elementloids, can have potential adverse effects on human health and the environment. However, it is important to note that to select a bioindicator species to assess human health effects, it should meet certain criteria, such as being commonly consumed in the area, widely distributed geographically, having the potential to accumulate high element concentrations, and having adequate tissue mass for residue analysis [88].
Estimated Daily Intake (EDI)
Trace elements of poisonous quality could incline people to health hazards through the consumption of defiled aquatic food; therefore, it is crucial for assessment [16]. Based on the oral reference dose RFD, the values of EDI were calculated to measure both the non-cancer and cancer risks of element consumption through seafood [89]. Besides, the EDI value denotes the exposure of trace elements, which is performed to evade any detrimental impact on human health [90]. Consumers’ daily exposure to trace elements through eating foods high in trace elements was employed to avoid any detrimental effects on humans during their lifespan [91]. The values of EDI were explored from selected 11 elements: Al, As, B, Ba, Cd, Cr, Cu, Fe, Pb, Zn, Hg, Mn, and Ni on the Red Sea fish consumption by children and adult consumers, as documented in Table 6. In addition, EDI was calculated, emphasizing the oral reference dose (RfD) for a specific chemical that elaborates the everyday exposition to noxious components and avoids any deleterious outcome on human health over lifetime exposure. The recorded EDI values were higher for child consumers compared to adult consumers, indicating that children are possibly more vulnerable to the health risks related to consuming trace elements in Red Sea fish. Other studies [75, 92, 93] also observed a similar pattern.
However, the EDI values for trace elements show a range of intake levels for children and adults. The EDI values (mg kg−1 day−1) of non-essential Al, As, Ba, Cd, Pb, Cr, and Hg and essential trace elements Cu, Fe, B, Zn, Mn, and Ni on Red Sea fish consumption by children and adult consumers were lower than the PTDI (permissible tolerable daily intake [94]). Therefore, the lower EDI than the permissible guidelines revealed that there is a possibility of a non-health impact associated with trace elements on consumers; mostly children would be more susceptible.
Target Hazard Quotient (THQ)
The allowable threshold level of THQ is one [45]. THQ for 11 elements: Al, As, B, Ba, Cd, Cr, Cu, Fe, Pb, Zn, Hg, Mn, and Ni in the muscles of Red Sea fish is illustrated in Table 7. However, the estimated THQ values were also higher in the child group than in the adult group for all studied elements. The THQ-essential elements, THQ-Al, and THQ-Ni values determined in edible Red Sea fish were under 1 [95], suggesting that eating muscles will not have any adverse health effects for consumers who consumed the studied Red Sea fish. However, the THQ-Cr values in the studied fish were also lower than 1, except in C. suevica for both consumers. The THQ-A values for adult consumers were < 1, except for P. forsskali (2.95), while they were higher than 1 for children consumers, only in L. ramak (1.08) > C. suevica (1.18) > P. affinis (1.50) > T. japonicus (1.07) > P. forsskali (1.53). Furthermore, the THQ-Pb values for adult consumers were < 1, except in P. forsskali (1.12), while they were higher than 1 for children consumers, only in C. hemistiktos (1.01), C. suevica (1.32), T. japonicus (1.48), and P. forsskali (1.72).
Hazard Index (HI)
The hazard index (HI) data for trace elements in nine Red Sea fish species shows a range of values for children and adults (Fig. 7). HI values for both adults and children through consumption of the eleven Red Sea fish species were evaluated based on the THQ values; if the HI value was higher than ten (HI > 10), the exposed consumer would face a significant non-cancer health risk, as recommended by Saha et al. [96]. The arranged hazard index (HI) values for children and adult consumers based on the types of fish are as follows: C. lunulatus (1.73 and 1.05, respectively) < S. luridus (2.32 and 1.46, respectively) < C. hemistiktos (2.53 and 1.60, respectively) < L. ramak (2.78 and 1.79, respectively) < P. affinis (3.30 and 2.09, respectively) < T. japonicus (3.53 and 2.26, respectively) < C. suevica (4.48 and 2.86, respectively) < P. forsskali (4.52 and 4.87, respectively). The HI values in the muscles of fish were less than ten, suggesting no non-cancer hazard for human consumption occurred.
The HI values of 11 trace elements in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
Cancer Risk (CR) Values
The cancer risk values of trace elements in the muscles of Red Sea fish vary across different species for children and adults (Fig. 8). The maximum values of CR-As for both children and adults were detected in P. forsskali (6.5E − 04 and 4.2E − 04, respectively) while the minimum values were determined in C. lunulatus (6.9E − 03 and 1.3E − 02, respectively).
The cancer risk (CR) values in marine fish from Aqaba Gulf at the Egyptian Red Sea Coast
CR values lower than 10−6 denote the elements’ negligible exposure, whereas 10−6 to 10−4 means the acceptable range, and higher than 10−4 indicates terrible exposure [74]. Estimated CR-As, CR-Ni, CR-Cr, and CR-Pb values in most studied species were higher in children than adults. For both consumers, the CR-Pb values in all studied Red Sea fish were within the limit of 10−4 to 10−6, though the other cancer risk values (CR-As, CR-Cr, and CR-Ni) showed higher cancer risk than the permissible limit as the increasing sequencing of CR-As > CR-Ni > CR-Cr. The CR values for children and adult consumers were ordered as the sequencing of CR-Pb < CR-Cr < CR-As < CR-Ni in all studied Red Sea fishes except C. lunulatus, which showed this sequencing: CR-Pb < CR-As < CR-Cr < CR-Ni.
Conclusion
Trace element pollution is a global problem that has implications for ecosystem functioning, global food safety, and global security. While extensive studies on trace element levels in marine fish have been carried out in many parts of the world to guide marine fish consumption, little or no studies exist in other parts of the world, including the Gulf of Aqaba Region. The study, therefore, aims to fill an important knowledge gap by providing information on thirteen trace element levels in eight (8) consumed marine fish species from the present Gulf and their possible implications for human health. Thirteen trace elements were analyzed in the sediment, water, and muscle of Red Sea fish from Nuweiba City, Aqaba Gulf, Egypt. The consumption of these polluted fish causes potential health hazards for its consumers. This study concluded that various trace elements accumulated at various concentrations in different fish species. The results exhibited that the bioaccumulation of essential elements in the muscle is well within the safe level as recommended by national and international agencies. However, the results of the non-essential trace elements in the present study indicated that several studied fish species could not be totally safe for human consumption due to their associated cancer and non-cancer potential health risks. An understanding of the adverse effects of trace elements on Red Sea fish and their permissible concentrations in aquatic environments would be extremely essential for fish conservation, fisheries development, and safe human consumption. Overall, monitoring trace element accumulation in Red Sea fish and assessing its health implications are crucial for human well-being.
Data Availability
The authors declare that data are available from the corresponding author at the readers’ request.
Code Availability
Not applicable.
References
Miao X, Hao Y, Tang X, **e Z, Liu L, Luo S, Huang Q, Zou S, Zhang C, Li J (2020) Analysis and health risk assessment of toxic and essential elements of the wild fish caught by anglers in Liuzhou as a large industrial city of China. Chemosphere 243:125337. https://doi.org/10.1016/j.chemosphere.2019.125337
Zhong W, Zhang Y, Wu Z, Yang R, Chen X, Yang J, Zhu L (2018) Health risk assessment of heavy metals in freshwater fish in the central and eastern North China. Ecotoxicol Environ Saf 157:343–349. https://doi.org/10.1016/j.ecoenv.2018.03.048
Korkmaz C, Ay Ö, Çolakfakıoğlu C, Erdem C (2019) Heavy metal levels in some edible crustacean and mollusk species marketed in Mersin, Thalass. Int J Mar Sci 35(1):65–71. https://doi.org/10.1007/s41208-018-0086-x
Tanamal C, Blais JM, Yumvihoze E, Chan HM (2021) Health risk assessment of inorganic arsenic exposure through fish consumption in Yellowknife, Northwest Territories, Canada. Hum Ecol Risk Assess: Int J 27(4):1072–1093. https://doi.org/10.1080/10807039.2020.1799187
Youssef DH, El-Said GF (2011) Assessment of some trace elements in surface sediments of Aqaba Gulf, Egypt. Environ Monit Assess 180:229–242. https://doi.org/10.1007/s10661-010-1784-x
Miri MEA, Amrane A, Jafari SJ, Eslami H, Hoseinzadeh E, Taghavi M (2017) Health risk assessment of heavy metal intake due to fish consumption in the Sistan region, Iran. Environ Monit Assess 189(11):1–10. https://doi.org/10.1007/s10661-017-6286-7
Kwaansa-Ansah EE, Nti SO, Opoku F (2019) Heavy metals concentration and human health risk assessment in seven commercial fish species from Asafo Market, Ghana. Food Sci Biotechnol 28(2):569–579. https://doi.org/10.1007/s10068-018-0485-z
Debipersadh S, Ogola HJO, Mearns K, Selvarajan R (2023) Bioaccumulation, bioindication and health risk assessment of heavy metals in Cape horse mackerel (Trachurus trachurus) and slinger seabream (Chrysoblephus puniceus) in the Durban Basin and Cape Vidal, South Africa. Arch Environ Contam Toxicol 85:165–180. https://doi.org/10.1007/s00244-023-01028-8
Schenone NF, Vackova L, Cirelli AF (2014) Differential tissue accumulation of arsenic and heavy metals from diets in three edible fish species. Aquac Nutr 20:364–371. https://ui.adsabs.harvard.edu/link_gateway/2014AqNut..20..364S/. https://doi.org/10.1111/anu.12085.
Abbas MMM, EL-Sharkawy SM, Mohamed HR (2023) Heavy metals assessment and health risk to consumers of two commercial fish species from polyculture fishponds in El-Sharkia and Kafr El-Sheikh, Egypt: physiological and biochemical study. Biol Trace Elem Reshttps://doi.org/10.1007/s12011-023-04007-1
Miedico O, Iammarino M, Pompa C, Tarallo M, Chiaravalle AE (2015) Assessment of lead, cadmium and mercury in seafood marketed in Puglia and Basilicata (Italy) by inductively coupled plasma mass spectrometry. Food Addit Contam: Part B 8(2):85–92. https://doi.org/10.1080/19393210.2014.989281
Kawser-Ahmed M, Baki MA, Kundu GK, Saiful IMM, Islam MM, Hossain M (2016) Human health risks from heavy metals in fish of Buriganga river, Bangladesh. SpringerPlus 5(1):1–12. https://doi.org/10.1186/s40064-016-3357/
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72. https://doi.org/10.2478/intox-2014-0009
Bettini SF, Ciani V, Franceschini V (2006) Recovery of the olfactory receptor neurons in the African Tilapia mariae following exposure to low copper level. Aquat Toxicol 76(3–4):321–328. https://doi.org/10.1016/j.aquatox.2005.10.009
Anandkumar A, Li J, Prabakaran K, ** Jia Z, Leng Z, Nagarajan RDD (2020) Accumulation of toxic elements in an invasive crayfish species (Procambarus clarkii) and its health risk assessment to humans. J Food Compos Anal 88:103449. https://doi.org/10.1016/j.jfca.2020.103449
Feng W, Wang Z, Xu H, Chen L, Zheng F (2020) Trace element concentrations in commercial fish, crabs, and bivalves from three lagoons in the South China Sea and implications for human health. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-019-06712-8
Yu B, Wang X, Dong KF, **ao G, Ma D (2020) Heavy metal concentrations in aquatic organisms (fishes, shrimp and crabs) and health risk assessment in China. Mar Pollut Bull 159:111505. https://doi.org/10.1016/j.marpolbul.2020.111505
El-Moselhy KM, Othman AI, El-Azem HA, El-Metwally MEA (2014) Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. Egypt J Basic Appl Sci 1:97–105. https://doi.org/10.1016/j.ejbas.2014.06.001
Ghanem M, Shehata S, Abu-Zaid M, Adel-Halim AM, Abbas MMM (2015) Accumulation of some HMs levels in the muscles of Diplodus sargus, inhabiting El-Mex Bay (Alexandria, Mediterranean Sea) with special references to its physiological responses. Int J Environ Sci Eng 6:1–13
Abubakr MI, Tarek OS, Ahmed AO, Khaled FF (2015) Combining multivariate analysis and human risk indices for assessing trace element contents in muscle tissues of commercially fish from Southern Red Sea, Saudi Arabia. Environ Sci Pollut Res 22(21):17012–17021. https://doi.org/10.1007/S11356-015-4921-9
Younis EM, Abdel-Warith AA, Al-Asgah NA, Elthebite SAM, Rahman M (2021) Nutritional value and bioaccumulation of heavy metals in muscle tissues of five commercially important marine fish species from the Red Sea. Saudi J Biol Sci 28(3):1860–1866. https://doi.org/10.1016/j.sjbs.2020.12.038
Lafi S, Al Solami (2022) Trace element content in coral reef-associated fish collected from the central Red Sea, Saudi Arabia. Oceanol Hydrobiol Stud 51(2):149–157. https://doi.org/10.26881/oandhs-2022.2.03
Abbas MMM, Abd El-Aziz MA, Kaddah MM, Hassan AM, El-Naggar HA (2022) Bioaccumulation, biosedimentation, and health hazards of elements in crayfish, Procambarus clarkii from El-Rahawi Drain and El-Qanatir in the River Nile, Egypt. Biol Trace Elem Res 201:3050–3059. https://doi.org/10.1007/s12011-022-03380-7
Abd El-Aziz ME, Hassan AM, Kaddah MM, El-Naggar HA, Abbas MMM (2022) Potential carcinogenic and non-carcinogenic health risks of heavy metals ingestion from consumption of the crayfish, Procambarus clarkii in El-Rahawy Drain and ElKanater in the River Nile, Egypt. Egypt J Aquat Biol Fish 26:667–686. https://doi.org/10.21608/ejabf.2022.244364
Yabanlı M, Katalay S, Yozukmaz A, İnanan BE (2015) Comparative study of heavy metals and selenium accumulation in the digestive gland and gills of Mytilus galloprovincialis (Lamarck, 1819) caught in Izmir Bay (Turkey). Turk J Biochem 40(2):140–148. https://doi.org/10.5505/tjb.2015.32448
Kassaye YA, Skipperud L, Einset J, Salbu B (2016) Aquatic macrophytes in Ethiopian Rift Valley lakes; their trace elements concentration and use as pollution indicators. Aquat Bot 134:18–25. https://doi.org/10.1016/j.aquabot.2016.06.004
Yozukmaz A, Yabanli M, Sel F (2018) Heavy metal bioaccumulation in Enteromorpha intestinalis, (L.) Nees, a macrophytic algae: the example of Kadin Creek (Western Anatolia). Braz Arch Biol Technol 61:e18160777. https://doi.org/10.1590/1678-4324-2018160777
El-Moselhy KM, Saad EM, El-Shaarway RF, Mohamadein LI, Mahmoud SA (2016) Assessment of trace elements pollution using sediments and bivalve Brachidontes variabilis as bioindicator in the Gulf of Suez, Egypt. Int J Mar Sci 6(26):1–13. https://doi.org/10.5376/ijms.2016.06.0025
Farhat HI, Gad A, Saleh A, Abd El Bakey SM (2022) Risks assessment of potentially toxic elements’ contamination in the Egyptian Red Sea surficial sediments. Land 11(9):1560. https://doi.org/10.3390/land1109156
Mosalem A, Redwan M, Abdel Moneim AA (2024) Distribution, speciation, and assessment of heavy metals in sediments from Wadi Asal, Red Sea, Egypt. Environ Monit Assess 196:215. https://doi.org/10.1007/s10661-024-12363-1
El-Metwally MEA, Othman AI, El-Moselhy KM (2019) Distribution and assessment of trace elements in the coastal area of the Red Sea, Egypt. Egypt J Aquat Biol Fish 23(2):1–13. https://doi.org/10.21608/fsrt.2023.238650.1108
Magdy SM, Madkour HA, Mansour AM, Askalany MS, Assran BB, El-Taher A, El Attar RM (2023) Heavy metal concentrations in surface waters of Hurghada and Environs, Red Sea Coast, Egypt, and their correlation with sediment distribution. Egypt J Aquat Res. https://doi.org/10.1016/j.ejar.2023.11.003
Oni AA, Babalola SO, Adeleye AD, Olagunju TE, Amama IA, Omole EO, Adegboye EA, Ohore OG (2022) Non-cancer and carcinogenic health risks associated with heavy metals and polycyclic aromatic hydrocarbons in well-water samples from an automobile junk market in Ibadan, SW-Nigeria. Heliyon 8(9):e10688. https://doi.org/10.1016/j.heliyon.2022.e10688
Moody EC, Coca SG, Sanders AP (2018) Toxic metals and chronic kidney disease: a systematic review of recent literature. Curr Environ Health Rep 5(4):453–463. https://doi.org/10.1007/s40572-018-0212-1
Mehanna S (2023) Population dynamics and assessment of the snubnose emperor L. ramak (L. bungus) from the Gulf of Aqaba, Egypt. Egypt J Aquat Biol Fish 27(3):643–654. https://doi.org/10.21608/ejabf.2023.305278
Elgendy AR, El-Sawy MA, Hassan AR, Khaled SS (2024) Anthropogenic heavy metal pollution in Nuweibaa, Gulf of Aqaba, Egypt: a threat to marine environment and water quality. Egypt J Aquat Biol Fish 28(1):1877–1896. https://doi.org/10.21608/ejabf.2024.344169
Mohamedein LI, El-Moselhy KM, El-Sawy MA (2023) Environmental impact assessment (EIA) of As, Se, Sn, and Hg in water and sediments from the Egyptian Red Sea Ports. Blue Econ 1:(1). https://doi.org/10.57241/2805-2994.1001
AOAC, Association of Official Analytical Chemists (2012) Official methods of analysis 15th ed Association of official analytical chemists Inc. Washington, DC USA, p 478
APHA, American Public Health Association (2023) American Water Works Association, Water Environment Federation. Lipps WC, Braun-Howland EB, Baxter TE, eds. Standard methods for the examination of water and wastewater. 24th ed. Washington DC: APHA Press
EPA (2023) Microwave assisted acid digestion of sediments (3051A method), sludges, soils, and oils, part of test methods for evaluating solid waste, physical/chemical methods
Adolfsson-Erici M, Åkerman G, Mclachlan MS (2012) Measuring bioconcentration factors in fish using exposure to multiple chemicals and internal benchmarking to correct for growth dilution. Environ Toxicol Chem 31:1853–1860. https://doi.org/10.1002/etc.1897
Usero J, Marilla J, Graccia I (2005) Heavy metal concentrations in molluscs from the Atlantic Coast of Sothern Spain. Chemosphere 59:1175–1181. https://doi.org/10.1016/j.chemosphere.2004.11.089
Tahity T, Islam MRU, Bhuiyan NZ, Choudhury TR, Yu J, Noman MA, Hosen MM, Quraishi SB, Paray BA, Arai T (2022) Heavy metals accumulation in organs of wild and farmed Barramundi from the Northern Bay of Bengal Coast, and its estimated human health risks. Toxics 10:410. https://doi.org/10.3390/toxics10080410
Abbas MMM (2023) Heavy metal levels and cancer risk assessments of the commercial denis, Sparus aurata collected from Bardawil Lake and private fish farm waters as a cultured source, Egypt. Biol Trace Elem Res. https://doi.org/10.1007/s12011-023-03880-0
USEPA United States Environmental Protection Agency (2018) US EPA regional screening levels RSLs, dataset-California open data. https://www.datacagov/dataset/us-epa-regional-screening-levels-rsls-november-2018/resource/b66c9172-a61a-4131-997f-01f45a473a08
Mwakalapa EB, Simukoko CK, Mmochi AJ, Mdegela RH, Berg V, Bjorge Muller MH, Polder A, Polder A (2019) Heavy metals in farmed and wild milkfish (Chanos chanos) and wild mullet (Mugil cephalus) along the coasts of Tanzania and associated health risk for humans and fish. Chemosphere 224:176–186. https://doi.org/10.1016/j.chemosphere.2019.02.063
Cui L, Ge J, Zhu Y, Yang Y, Wang J (2015) Concentrations, bioaccumulation, and human health risk assessment of organochlorine pesticides and heavy metals in edible fish from Wuhan, China. Environ Sci Pollut Res Int 22:15866–15879. https://doi.org/10.1007/s11356-015-4752-8
USEPA United States Environmental Protection Agency (2016) Integrated risk information system. https://www.epa.gov/iris/
Afifi MAM, Radwan M, Abbas MMM, Hwihy HM, Alabssawy AN, Khalaf-Allah HM (2024) Threat of heavy metal pollutants and parasites to freshwater fish with special reference to their risk of cancer to humans in Egypt. Aquaculture 587:740833. https://doi.org/10.1016/j.aquaculture.2024.740833
Dytham C (2011) Choosing and Using Statistics: A Biologist’s Guide. John Wiley & Sons
Naz S, Chatha AMM, Danabas D, Khan MF, Xu Y, Zhu P, Laiba S (2023) Bioaccumulation pattern and health risk assessment of trace elements in Cirrhinus mrigala at Panjnad Headworks Bahawalpur, Pakistan. Toxics 11(7):596. https://doi.org/10.3390/toxics11070596
Khedr AI, Goher ME, Salem SG (2023) Assessment of pollution and element toxicity in the bed sediment of El-Rayan Lakes, Fayoum, Egypt. SN Appl Sci 5:190. https://doi.org/10.1007/s42452-023-05398-5
Ibrahim ATA, Omar HM (2013) Seasonal variation of trace elements accumulation in muscles of the African catfish Clarias gariepinus and in River Nile water and sediments at Assiut Governorate, Egypt. J Biol Earth Sci 3(2):236–248
WHO, World Health Organization (2011) Guidelines for drinking water quality. WHO Publications, Geneva, Switzerland, p 564. https://apps.who.int/iris/bitstream/handle/10665/336875/WHO-HSE-PHE-EPE-11.01.07-eng.pdf
Creti P, Trinchella F, Scudiero R (2010) Trace element bioaccumulation and element lothionein content in tissues of the sea bream Sparus aurata from three different fish farming systems. Environ Monit Assess 165:321–329. https://doi.org/10.1007/s10661-009-0948-z
Kumar N, Chandan NK, Bhushan S (2023) Health risk assessment and element contamination in fish, water and soil sediments in the East Kolkata Wetlands, India, Ramsar site. Sci Rep 13:1546. https://doi.org/10.1038/s41598-023-28801-y
Rudnick RL, Gao S (2003) Composition of the continental crust. In: Rudnick RL (ed) The Crust, vol 3. Elsevier, pp 1–64. https://doi.org/10.1016/B0-08-043751-6/03016-4
Hossain MB, Tan** F, Rahman MS, Yu J, Akhter S, Noman MA, Sun J (2022) Elements bioaccumulation in 15 commonly consumed fishes from the Lower Meghna River and adjacent areas of Bangladesh and associated human health hazards. Toxics 10(3):139. https://doi.org/10.3390/toxics10030139
Jezierska B, Witeska M (2006) The element uptake and accumulation in fish living in polluted waters. In: Soil and water pollution monitoring, protection and remediation (pp 107–114) Springer Netherlands. https://doi.org/10.1007/978-1-4020-4728-2_6.
Hosseini M, Nabavi SMB, Nabavi SN, Pour NA (2015) Trace elements (Cd Co, Cu, Ni, Pb, Fe, and Hg) content in four fish commonly consumed in Iran: risk assessment for the consumers. Environ Monit Assess 187:237. https://doi.org/10.1007/s10661-015-4464-z
Yi Y, Tang C, Yi T, Yang Z, Zhang S (2017) Health risk assessment of trace elements in fish and accumulation patterns in food web in the upper Yangtze River, China. Ecotoxicol Environ Saf 145:295–302. https://doi.org/10.1016/j.ecoenv.2017.07.022
Jiang Z, Xu N, Liu B (2018) Metal concentrations and risk assessment in water, sediment and economic fish species with various habitat preferences and trophic guilds from Lake Caizi, Southeast China. Ecotoxicol Environ Saf 157:1–8. https://doi.org/10.1016/j.ecoenv.2018.03.078
Younis AM, Amin HF, Alkaladi A, Mosleh YYI (2015) Bioaccumulation of trace elements in fish, squids and crustaceans from the Red Sea, Jeddah Coast, Saudi Arabia. Open J Mar Sci 5:369–378. https://doi.org/10.4236/ojms.2015.54030
FAO Food and Agriculture Organization (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fishery Circular No 464. Rome, Italy. Available online at: http://www.fao.org/docrep/014/q5114e/q5114e.pdf
WHO, World Health Organization (1989) Revision of WHO guidelines for water quality. WHO, Geneva
USEPA United States Environmental Protection Agency (2000) Guidance for assessing chemical contaminant data for use in fish advisories, volume 1: fish sampling and analysis, 3rd ed. EPA-823-B-00–007. Washington DC, USA. Available online at: https://www.epa.gov/sites/default/files/2015-06/documents/volume1.pdf
WHO, World Health Organization (2007) Health risks of heavy metals from long-range transboundary air pollution. WHO Regional Office for Europe
Łuczyńska J, Paszczyk B, Nowosad J, Łuczyński MJ (2017) Mercury, fatty acids content and lipid quality indexes in muscles of freshwater and marine fish on the polish market. Risk assessment of fish consumption. Int J Environ Res Public Health 14:1120. https://doi.org/10.3390/ijerph14101120
Nowosad J, Kucharczyk D, Szmyt M, Łuczynska J, Tamás M, Horváth L (2021) Changes in cadmium concentration in muscles, ovaries, and eggs of silver European eel (Anguilla anguilla) during maturation under controlled conditions. Animals 11:1027. https://doi.org/10.3390/ani11041027
Mziray P, Kimirei IA (2016) Bioaccumulation of heavy metals in marine fishes (Siganus sutor, Lethrinus harak, and Rastrelliger kanagurta) from Dar es Salaam Tanzania. Reg Stud Mar Sci 7:72–80. https://doi.org/10.1016/j.rsma.2016.05.014
Al-Amri I, Kadim I, AlKindi A, Al-Harrasi A, Al-Hosni K, Al-Kiymi A, Al-Omairi M (2021) Determination and comparison of non-essential and essential elements in different species of fish available in Omani markets by using inductively coupled plasma-optical emission spectrometry. Acta Sci Nutr Health 5(1):60–73. https://doi.org/10.31080/ASNH.2020.05.0804
Hilal AA, Ismail NS (2008) Heavy metals in eleven common species of fish from the Gulf of Aqaba, Red Sea. Jordan J Biol Sci 1(1):13–18. https://api.semanticscholar.org/CorpusID:55058405
Saulick B, Bhoyroo V, Nazurally N, Lalljee B (2017) Heavy metal bioaccumulation in commercial Lethrinidae fish species in Mauritius. Ital J Food Saf 6(4):6–6607. https://doi.org/10.4081/ijfs.2017.6607
Baki MA, Hossain MM, Akter J, Quraishi SB, Shojib MFH, Ullah AA, Khan MF (2018) Concentration of trace elements in seafood (fishes, shrimp, lobster and crabs) and human health assessment in Saint Martin Island, Bangladesh. Ecotoxicol Environ Saf 159:153–163. https://doi.org/10.1016/j.ecoenv.2018.04.035
Yakamercan E (2021) Ari, A Aygün, A (2021) Land application of municipal sewage sludge: human health risk assessment of heavy metals. J Clean Prod 319:128568. https://doi.org/10.1016/j.jclepro.2021.128568
Chai X, XP, Hu BL, Wei N, Mu QL, He JR, He SQ (2015) Distribution, sources and assessment of trace elements in surface sediments of the Hangzhou Bay and its adjacent areas. Acta Sci Circum 35:3906–3916. https://doi.org/10.13671/j.hjkxxb.2015.0138
Vu CT, Lin C, Yeh G, Villanueva MC (2017) Bioaccumulation and potential sources of trace element contamination in fish species in Taiwan: assessment and possible human health implications. Environ Sci Pollut Res 24:19422–19434. https://doi.org/10.1007/s11356-017-9590-4
Ahmed AS, Sultana S, Habib A, Ullah H, Musa N, Hossain MB, Sarker MSI (2019) Bioaccumulation of trace elements in some commercially important fishes from a tropical river estuary suggests higher potential health risk in children than adults. PLoS ONE 14:e0219336. https://doi.org/10.1371/journal.pone.0219336
Ali MM, Ali ML, Proshad R, Islam S, Rahman Z, Kormoker T (2020) Assessment of trace elements in the demersal fishes of a coastal river in Bangladesh: a public health concern. Thalassas: An Int J Marine Sci 36(2):641–655. https://doi.org/10.1007/s41208-020-00227-7
Ziyaadini M, Yousefiyanpour Z, Ghasemzadeh J, Zahedi M (2017) Biota-sediment accumulation factor and concentration of HMs (Hg, Cd, As, Ni, Pb and Cu) in sediments and tissues of Chiton lamyi (Mollusca: Polyplacophora: Chitonidae) in Chabahar Bay, Iran. Iran J Fish Sci 16(4):1123–1134
Haseeb-ur-Rehman M, Munshi AB, Kalsoom UAS (2023) Element pollution and potential human health risk assessment in major seafood items (fish, crustaceans, and cephalopods). Mar Pollut Bull 188:114581. https://doi.org/10.1016/j.marpolbul.2023.114581
Ju YR, Chen CW, Chen CF, Chuang XY, Dong CD (2017) Assessment of trace elements in aquaculture fishes collected from southwest coast of Taiwan and human consumption risk. Int Biodeterior Biodegrad 124:314–325. https://doi.org/10.1016/j.ibiod.2017.04.003
El-Batrawy OA, El-Gammal MI, Mohamadein LI, Darwish DH, El-Moselhy KM (2018) Impact assessment of some heavy metals on tilapia fish, Oreochromis niloticus, in Burullus Lake, Egypt. J Basic Appl Zool 79:13. https://doi.org/10.1186/s41936-018-0028-4
Abdel-Khalek AA, Zayed HS, Elsayad SM (2020) Assessment of metal pollution impacts on Tilapia zillii and Mugil cephalus inhabiting Qaroun and Wadi El-Rayan lakes, Egypt, using integrated biomarkers. Environ Sci Pollut Res 27:26773–26785. https://doi.org/10.1007/s11356-020-09095-3
Tashi S, Gurung U, Dorji B, Wangchuk K (2022) Heavy metals in fish species: Schizothorax richardsonii, Salmo trutta and Neolissochilus hexagonolepis in relation to sizes and tissues of Punatsang Chhu. Environ Chem Ecotoxicol 4:78–88. https://doi.org/10.1016/j.enceco.2022.01.001
Thompson RM, Dunne JA, Woodward GUY (2012) Freshwater food webs: towards a more fundamental understanding of biodiversity and community dynamics. Freshw Biol 57:1329–1341. https://doi.org/10.1111/j.1365-2427.2012.02808.x
Vilches FO, Bobinac MA, Labudía AC et al (2019) Metals concentration and bioaccumulation in the marine-coastal trophic web from Buenos Aires province southern coast, Argentina. Chem Ecol 35:501–523. https://doi.org/10.1080/02757540.2019.1604693
Cunningham PA, Sullivan EE, Everett KH, Kovach SS, Rajan A, Barber MC (2019) Assessment of metal contamination in Arabian/Persian Gulf fish: a review. Mar Pollut Bull 143:264–283. https://doi.org/10.1016/j.marpolbul.2019.04.007
Liu Q, Liao Y, Shou L (2018) Concentration and potential health risk of trace elements in seafoods collected from Sanmen Bay and its adjacent areas, China. Mar Pollut Bull 131:356–364. https://doi.org/10.1016/j.marpolbul.2018.04.041
Abtahi M, Fakhri Y, Conti GO, Keramati H, Zandsalimi Y, Bahmani Z, Pouya RH, Sarkhosh M, Moradi B, Amanidaz N, Ghasemi SM (2017) Trace elements (As, Cr, Pb, Cd and Ni) concentrations in rice (Oryza sativa) from Iran and associated risk assessment: a systematic review. Toxin Rev 36:331–341. https://doi.org/10.1080/15569543.2017.1354307
Keshavarzi A, Kumar V, Ertunc G, Brevik EC (2021) Ecological risk assessment and source apportionment of heavy metals contamination: an appraisal based on the Tellus soil survey Environ. Geochem Health 43:2121–2142. https://doi.org/10.1007/s10653-020-00787-w
Duan B, Zhang W, Zheng H, Wu C, Zhang Q (2017) Bu Y (2017) Comparison of health risk assessments of heavy metals and As in sewage sludge from wastewater treatment plants (WWTPs) for adults and children in the urban district of Taiyuan, China. Int J Environ Res Public Health 14(10):1194. https://doi.org/10.3390/ijerph14101194
Tytła M, Widziewicz-Rzońca K (2023) Ecological and human health risk assessment of heavy metals in sewage sludge produced in Silesian Voivodeship, Poland: a case study. Environ Monit Assess 195(11):1373. https://doi.org/10.1007/s10661-023-11987-z
FAO/WHO (2004) Summary of evaluations performed by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) 1956–2003 (First through Sixty-First Meetings) Available online at: https://apps.who.int/iris/handle/10665/40305
USEPA United States Environmental Protection Agency (2011) Risk assessment guidance for Superfund. Volume I: (Part A: Human Health Evaluation Manual; Part E, Supplemental Guidance for Dermal Risk Assessment; Part F, Supplemental Guidance for Inhalation Risk Assessment) EPA US Environmental Protection Agency, Washington, DC. https://www.epa.gov/sites/default/files/2015-09/documents/efh-chapter10.pdf
Saha N, Mollah MZI, Alam MF, Safiur RM (2016) Seasonal investigation of trace elements in marine fishes captured from the Bay of Bengal and the implications for human health risk assessment. Food Control 70:110–118. https://doi.org/10.1016/j.foodcont.2016.05.040
Acknowledgements
Thanks are indebted to Allah, always and foremost, for his mercy, guidance, and help. The authors gratefully acknowledge the Department of Zoology, Faculty of Science, Al-Azhar University, Cairo, Egypt, for providing the necessary support. Finally, we thank the anonymous reviewers of this article for their careful work and constructive suggestions.
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Mohamed A. A. Shorbagy: methodology, investigation, and visualization; Mohamed A. Embaby: investigation, statistics and formal analysis, review, and editing; Mohamed H. Ghanem: writing, methodology, and writing—review and editing. Ahmed A. El-Kady: formal analysis, visualization, methodology, and editing. Mohamed S. Kourany: formal analysis, visualization, methodology, and editing. Shimaa M. Abdel-Moniem: investigation, methodology, conceptualization, and editing. Mahmoud Mahrous M. Abbas: writing—original draft, formal analysis, and editing. All authors read and approved the final manuscript.
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El-Shorbagy, M.A., Abdel-Moniem, S.M., Ghanem, M.H. et al. Elucidating the Environmental and Health Risks of Trace Element Pollution in Red Sea Fish from Nuweiba City, Aqaba Gulf, Egypt. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-024-04246-w
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DOI: https://doi.org/10.1007/s12011-024-04246-w