Abstract
In this study, the concentrations of 9 elements (Al, As, Cd, Cr, Fe, Mn, Ni, Se and Zn) in the muscle tissue of 10 different fish species consisting of sea and freshwater fish of certain origin in local markets and the fish market in Konya were determined. According to the findings of the study, the highest mean concentrations of Al, Fe and Cr were found in Flathead grey mullet, As and Se in Gilthead seabream, Mn and Zn in European pilchard, Cd and Ni in Mediterranean horse mackerel. The estimated daily intake, target hazard quotient (THQ), hazard index (HI) and cancer risk (CR) risk values for inorganic arsenic were determined using human health risk assessment methods based on metal levels in muscle tissue of fish. THQ and HI results revealed that non-carcinogenic health effects from the intake of individual or combined metals in fish species are not expected for consumers. This situation indicates that there are no non-cancer health risks. However, consumption of red mullet and European anchovy fish exposes individuals to inorganic arsenic, increasing the risk of cancer as their CR values were found not to be in acceptable ranges. The results were compared with limit values specified in national and international quality criteria. Only the average Cd concentrations in Carp, European barracuda and Mediterranean horse mackerel were found above the limit values of MHPRC (MHPRC (2013) National food safety standard, maximum levels of contaminants in foods), TFC (2011) and EC (Commission regulation no. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of European Union, 20.12.2006).
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Introduction
In recent years, there has been a growing global apprehension regarding the pollution of aquatic environments with heavy metals. This concern arises from their persistent and non-biodegradable characteristics, which result in detrimental effects on organisms (Jiang et al. 2016). Metals are a subject of concern among environmental pollutants, as they possess the capability to bioaccumulate in aquatic ecosystems and exhibit potential toxic effects. Heavy metals play essential roles as cofactors in numerous enzymatic reactions and are necessary for various metabolic activities in both animals and humans (Javed and Usmani 2016). Metals are commonly released into the environment during mining and industrial processes prompting increased precautionary measures worldwide. Many investigations have been carried out to explore the occurrence and impacts of heavy metals in the aquatic environment. (Korkmaz et al. 2017; Varol and Sünbül 2019; Ahmad et al. 2022).
Heavy metals are released into the aquatic environment either in solution or suspension, originating from natural or human-related sources such as urban discharges, agricultural runoff, mining activities, incineration, and industrial waste discharges. Organisms then absorb these heavy metals, potentially becoming a source of heavy metal pollution in aquatic ecosystems. (Makedonski et al. 2017; Javed and Usmani 2016).
Fish represent a wide variety of shapes, sizes and habitats and make up more than 40% of all vertebrate species worldwide. This places them in a crucial role within aquatic ecosystems, usually occupying the top of the food chain (Yap and Al-Mutairi, 2022). Heavy metals generally accumulate in the vital organs of fish such as liver, kidney, muscle, and gills (Javed and Usmani 2016).
While Turkey’s aquaculture production was 582 thousand tons in 2000, it increased to 800 thousand tons in 2021. While the average amount of fish per capita in European countries is 28.3 kg/year, the world average is 13.8 kg/year (Yüksel et al. 2011). This amount has been reported as an average of 6.3 kg/year per person in our country (TMAF 2019). Fish is a favored dietary option because it provides a high-quality protein source, minimal levels of saturated fat, and omega-3 fatty acids known for their health-enhancing attributes. (Parvin et al. 2023). However, contaminants in the food chain can be transferred to humans through seafood consumption, leading to adverse effects on human health. For instance, heavy metals have the potential to harm the human liver, kidneys, nervous and vascular systems, and even contribute to the development of cancer (Xu et al. 2021). Fish serve as indicators of pollution in freshwater systems, and assessing toxic levels in fish can be employed to gauge the potential risk associated with human consumption (Mahamood et al. 2023). When heavy metals found in fish are consumed above the recommended consumption limits, they can cause serious health problems in humans such as developmental abnormalities, nervous system disorders, liver and kidney damage, reproductive and hematological effects, cancer and cardiovascular diseases. For this purpose, exhaustive research has been conducted on the edible portions of fish to ascertain their impact on human health. (Aissioui et al. 2021).
These methodologies assist researchers in assessing and quantifying the potential health consequences linked to heavy metal exposure(Varol and Sünbül 2019). Both the non-carcinogenic health risks (THQ) and carcinogenic health risks (CR) can be quantified and evaluated using human health risk assessment methods. These assessments consider factors such as the amount and frequency of fish consumption to determine the potential health impacts of heavy metal exposure (USEPA 2018). Many researchers have employed these risk calculation methods in their studies (Zhu et al. 2015; Gu et al. 2015; Kawser Ahmed et al. 2016; Varol et al. 2018).
This study aimed to assess the concentrations of heavy metals in the muscle tissues of ten distinct fish species commonly consumed and preferred by the local population in Konya.
Heavy metal accumulation in different fish species in Turkey has not been extensively investigated. Previous studies have mainly focused on only a few fish species. It is important to analyze various fish species for better assessment of consumption-related risks. The aim of this study was to determine the concentrations of 9 heavy metals in the muscle tissues of ten different fish species commonly consumed and preferred by the local population in Konya, to evaluate the human health risks associated with fish consumption, and as well as comparing these results with other fish species. Additionally, the study compares the results with the maximum allowable limits set by national and international standards.
Material and methods
Sample collection
In this research, five samples for per species from ten different fish grown in different habitats were purchased from a local fish market in Konya, Türkiye. (Table 1). Fish samples were transported to the laboratory in the cold chain and where the length and weight of each sample were documented (Table 1).
Metal analysis
After weighing homogenized fish muscle samples (approximately 0.5 g), 6 ml of HNO3, (65%) 2 ml of H2O2 (30%), and 2 ml of distilled water were added. After waiting for a while for the acid to come out, the samples were placed in the microwave (Sineo-Mds 10) and dissolved. Microwave samples were diluted with ultrapure water filtered through filter paper into 25 mL polypropylene tubes (Gümüş and Akköz 2021). Samples ready for analysis were measured in an Inductively Coupled Plasma-Optic Absorption Spectrophotometer (ICP-OES-Agilent 720).
Each sample was analyzed in three repetitions in the device calibrated with six different calibrating points and average values were used as data. The accuracy of the analytical method was tested with the fish reference material (TORT-2, Lobster Hepatopancreas). Sensitivity levels varied between 90 and 106% (Table 2). The highest degree of sensitivity was determined in Fe, the lowest degree of sensitivity was determined in Se.
Risk assessment on human health
Hazard index (HI) Target hazard quotient (THQ) and Estimated daily intake (EDI), were calculated according to USEPA (2019) to quantify the human health risk assessment that may occur in consumers with fish consumption.
The estimated daily intake (EDI) of HMs for adults was calculated according to the following eq. (1)
The daily fish consumption per capita in Türkiye is 15 g/person/day according to TMAF (2019). THQ also refers to the risk of non-carcinogenic effects of levels of metals ingested. THQ refers to the risks of non-carcinogenic effects of metals ingested into the body (Eq. 2).
HI is the total of the THQ values for the metals under investigation. An HI > 1 suggests the presence of non-carcinogenic health risks for the consumer. Conversely, an HI < 1 indicates an absence of anticipated non-carcinogenic health effects (Çulha et al. 2016; Tokatlı and Ustaoğlu 2021) (Eq. 3).
In this study, the calculation of cancer risk specifically targeted inorganic arsenic. The cancer risk (CR) was determined utilizing the following equation (Eq. 4).
Within this research, the average values of 11 metals identified in the muscle tissues of fish species were applied in the computations of EDI, THQ, and CR. Only the inorganic form of arsenic is toxic. The inorganic arsenic form accounts for 1–10% of total arsenic (Kalantzi et al. 2016). Therefore, inorganic arsenic values were used instead of total arsenic values for EDI, THQ and CR calculations. In our study, it was accepted that inorganic arsenic constituted 3% of the total arsenic (Copat et al. 2013). The assessment of the computed CR coefficients is as follows: 10–4 > CR > 10–6 is considered acceptable (USEPA 2019; Varol et al. 2019).
Metal pollution index (MPI)
It is calculated by taking the geometric mean of the elements detected in fish muscles. The MPI value was calculated using the following equation (mg/kg) (Shue et al. 2014).
Statistical analysis
The differences of heavy metals between species were evaluated by analysis of variance (p < 0,05). Pearson Correlation Index was used to evaluate the relationship between heavy metals in fish species. All statistical calculations were made using the SPSS 21.0 statistical program.
Results and discussion
In this study, the levels of heavy metals recorded in the muscle tissues of 10 different fish species, which were Common carp (Cyprinus carpio), Rainbow trout (Oncorhynchus mykiss), Red mullet (Mullus barbatus), G. seabream (Sparus aurata), E. barracuda (Sphyraena sphyraena), E. pilchard (Sardina pilchardus) E. seabass (Dicentrarchus labrax), E. anchovy (Engraulis encrasicolus), F. grey mullet (Mugil cephalus) ve M. horse mackerel (Trachurus mediterraneus), were summarized in Table 3. The results obtained were compared with other studies in the literature in Table S1.
According to the results obtained in this study, lower metal content was detected in the cultured fish species such as gilthead seabream, European seabass, and rainbow trout.The highest concentrations of 8 (Al, As, Cd, Cr, Fe, Se, Mn, Ni, Zn) of the 9 metals analysed in our study were found in marine fish. Among the species obtained from the Aegean Sea, 3 metals (Fe, Mn, Zn) in E. pilchard, 2 metals (As, Zn) in G. seabream, 1 metal (Cr) in F. grey mullet were found in the highest concentrations. M. horse mackerel had the highest concentration of Cd metal and European anchovy had the highest concentration of Se metal in the species taken from the Black Sea. Rainbow trout was found to have the highest concentration of Se metal only in freshwater species. The toxic content of the Red mullet fish living in the demersal zone was found to be about 3 times higher than that of the European anchovy living in the pelagic zone according to the ecological habitats of the fish species we analyzed in the study. Naccari et al. (2015) reported that demersal fish absorb metals more due to living on sediment, similar to the results we found in our study.
Al ranks as the Earth’s third most abundant element and finds extensive applications in various aspects of human life. Al levels in food stuffs are reported to range from 0.1 to 20 mg/kg (Varol et al. 2019). Natural sources, food preparation water, feedstuffs and cooking utensils contribute to the presence of Al in food. In this study, the average Al concentrations ranged between 0.718 and 7.549 mg/kg value. In the present investigation, as shown in Table 3, Flathead grey mullet exhibited the highest contamination levels, followed by Common carp, Red mullet, M. horse mackerel, European barracuda, European pilchard, European seabass, Rainbow trout, European anchovy and Gilthead seabream. Among the ten fish species, Al concentrations in Common carp and Flathead grey mullet were statistically significantly higher than the other species (p < 0.05).
The average As concentrations ranged between 0.427 and 1.39 mg/kg. Average As concentrations ranged from highest to lowest in G. seabream (1.423 mg/kg), E. anchovy (1.19 mg/kg), E. pilchard (1.16 mg/kg), R. mullet (1.078 mg/kg), E. barracuda (1,048) mg/kg), M. horse mackerel (0.856 mg/kg), F. grey mullet (0.659 mg/kg), E. seabass (0.609 mg/kg), and Rainbow trout (0.427 mg) with the lowest average As concentration freshwater fish (Table 3). Svobodova et al. (2002) found the average concentration of Rainbow trout in Czech Republic to be between 0.498 and 1.133 mg/kg. Varol et al.(2019) found mean arsenic values (0.24 mg/kg) in European barracuda similar to our study. Barbosa et al. (2021) found similar results to this study in G. seabream farmed in Portugal (1.18 mg/kg). The As concentration in ten fish species was statistically significantly higher (p < 0.05) in G. seabream than in the other species. The average concentrations of inorganic arsenic in all fish species were considerably lower than the maximum allowable limit of 2 mg/kg by the FSANZ (2013) and MHPRC (2013) (Table S2).
High intakes of cadmium can cause disturbances in calcium metabolism, kidney stone formation, chronic renal failure, proteinuria, renal tubular dysfunction, pulmonary fibrosis and coronary atherosclerosis (ATSDR 2012). the M. horse mackerel exhibited the highest average Cd concentrations at 0.171 mg/kg, while the F. grey mullet displayed the lowest mean Cd concentrations at 0.030 mg/kg. It was found the average Cd value of M. horse mackerel in İskenderun Bay as 0.27 mg/kg (Ersoy and Çelik 2010). It was found the average Cd value in E. anchovy as 0.0026 mg/kg in their study (Varol et al. 2019). Average muscle Cd levels for seafood from Turkish territorial waters have been reported as 0.05–0.26 mg/kg (Tuzen and Soylak 2007). Out of the ten fish species, whiting and M. horse mackerel showed significantly higher Cd concentrations than the other species (p < 0.05). Mean Cd concentrations in Common carp, E. barracuda and M. horse mackerel were above MHPRC (2013) (0.1 mg/kg), GDFA (2021) (0.1 mg/kg) and EC (2006) (0.05 mg/kg) limits while other fish were found below these limits (Table S2).
Chromium (Cr) is considered an essential trace element and is present in the human body and is known to control blood sugar and cholesterol levels. Human exposure to Cr is through inhalation, consumption of Cr containing foods and contact with Cr compounds (Ukhurebor et al. 2021). Mean Cr concentrations varied between 0.062 and 0.577 mg/kg. Cr levels reported in fish species caught from the Mediterranean Sea spanned from 0.27 to 0.35 mg/kg (Türkmen et al. 2009). Cr levels reported for muscle tissues of some fish species in the Black Sea vary between 0.53 and 0.68 mg/kg (Alkan et al. 2016). It was reported that Cr in some fish species in Mersin Bay was found to be below the detection limits (Karayakar et al. 2010). Average chromium levels found in fish in France range between 0.05 and 0.57 mg/kg (Guérin et al. 2011). The mean Cr levels of aquatic species in the Black Sea, Marmara, Aegean and Mediterranean Sea vary among 0.07–0.85 mg/kg (Topçuoglu et al. 2002).
In this current study, the average chromium (Cr) concentrations detected in the fish species closely matched those documented in the existing literature. The average Cr concentrations in all fish species remained within the permissible limits set by MHPRC (2013) (2 mg/kg), IAEA (2003) (0.73 mg/kg) (Table S2). Of the ten fish species, F. grey mullet showed significantly higher Cr concentrations than the other species (p < 0.05).
Iron is an essential element in humans. Rarely, iron toxicity is found in humans living in environments subject to anthropogenic stresses. Iron deficiency is prevalent in humans, and its insufficiency leads to anemia (Ikem and Egiebor 2005).
F. grey mullet (18.47 mg/kg), E. pilchard (11.01 mg/kg), and R. mullet (10.73 mg/kg) with the highest average Fe concentrations. The lowest average Fe concentrations were reported in Rainbow trout (1.977 mg/kg) and E. barracuda (1.349 mg/kg). Varol et al. (2019) examined ten fish species and found that the highest Fe concentrations were E. anchovy 22.35 mg/kg, M. horse mackerel 11.63 mg/kg, and G. seabream 2.79 mg/kg R. mullet 2.57 mg/kg. In some fish species in Mersin Bay, Fe concentrations were found in the range of 0.19–3.61 mg/kg (Ersoy and Çelik 2010), and 9.21–129 mg/kg (Türkmen et al. 2009). Except for Except for F. grey mullet, E. pilchard and R. mullet, average Fe concentrations were lower than the literature. Of the ten fish species, E. anchovy and F. grey mullet showed significantly higher Fe concentrations than the other species (p < 0.05). The average Fe concentrations in all fish species are below the maximum allowable limit set by (GDFA 2021) (50 mg/kg), (IAEA 2003) (146 mg/kg) (Table S2).
Manganese is one of the least toxic of the heavy metals and an essential element for animals and humans (Gümüş and Akköz 2021). The mean Mn concentrations in ten fish species varied between 0.183and0.646 mg/kg. The average Mn concentrations detected in fish muscles ranged from 0.39to0.82 mg/kg (Elnabris et al. 2013), < 0.0002–0.39 mg/kg (Korkmaz et al. 2019a), 0.093–2.023 mg/kg (Varol and Sünbül 2019), 0.13–0.65 mg/kg (Ersoy and Çelik 2010), 1.09–1.92 mg/kg (Gümüş and Akköz 2021). The average Mn concentrations in all fish species fall below the maximum allowable threshold established by (GDFA 2021) (20 mg/kg), (IAEA 2003) (3.52 mg/kg) (Table S2). Of the ten fish species, E. pilchard showed significantly higher Mn concentrations than the other species (p < 0.05).
Nickel is a naturally occurring element found in the Earth’s crust, comprising approximately 6% of its composition. While nickel is essential for normal growth and reproduction in animals and humans, excessive consumption of nickel can be carcinogenic (Malik et al. 2010). No significant variances in nickel concentrations were observed between fish species. (p > 0.05). The average Ni values in ten fish species varied from 0.379–1.065 mg/kg. The average Ni concentrations detected in fish muscles ranged from < 0.01–0.58 mg/kg (Gümüş and Akköz 2021), 0.16–0.254 mg/kg (Varol et al. 2019), 0.06–0.37 mg/kg (Ersoy and Çelik 2010) and 0.01–3.43 mg/kg (Ateş et al. 2015) (Table S1). The findings of this study align with the outcomes of prior research on Ni levels.
It reaches humans through crops grown on selenium-contaminated farmland and through the food chain. Selenium deficiency leads to thyroid hormone disorders and heart disease (Kaptan and Tekin-Özan 2014). Mean Se concentrations varied between 0.345 and 0.715 mg/kg. The mean Se concentrations detected in fish muscles ranged from < 0.01 to 0.33 mg/kg (Gümüş and Akköz 2021). Significant differences in Se concentrations were found between fish species (p > 0.05). The present results are consistent with the results of former studies on Selenium levels.
Like in Mn, the highest average Zn concentration was found in E. pilchard (14.54 mg/kg) and the lowest in Gilthead seabream (0.579 mg/kg). Among the ten fish species, sardine showed significantly higher Zn concentration than the other fish species (p < 0.05). The average Zn concentrations detected in fish muscles vary between 8.4 and 12.3 mg/kg (Bat et al. 2019), 2.35–15.81 mg/kg (Karayakar et al. 2010), 8.20–23.75 mg/kg (Ozparlak et al. 2012), 11.75–23.58 mg/kg (Korkmaz et al. 2017). Our current findings indicate lower levels of Zn compared to those reported in previous studies. The mean Zn concentrations in all fish species are below the maximum permissible limit set by (2021) (50 mg/kg), WHO/FAO (2015) (67.1 mg/kg) IAEA (2003) (40 mg/kg) (Table S2).
Toxic and non-toxic metals
The study findings revealed that among the fish species examined, F. gray mullet had the highest concentrations of toxic metals, while E. anchovy had the lowest levels of toxic metal content (Fig. 1). In terms of non-toxic metals, the species with the highest content was determined as E. anchovy, while the species with the lowest content was determined as Gilthead seabream (Fig. 2). The variations in concentrations of both toxic and non-toxic metals among different fish species can be attributed to the specific habitat and feeding habits of each species. As an illustration, mullet, which is a bottom-dwelling fish that feeds on benthic organisms, may accumulate higher levels of toxic metals compared to other fish species. This is due to its feeding behavior and proximity to the sediment where metals may be present (Naccari et al. 2015; Varol et al. 2019).
Risk assessment
The EDI values for the analyzed fish samples were comfortably below the TDI thresholds, signifying that the consumption of these studied fish samples carries no health risk related to the intake of the investigated heavy metals. EDI values of Fe were higher in E. anchovy, R. mullet, Gilthead seabream and F. grey mullet, while EDI values of Zn were higher in other fish species. The calculated EDI values for each metal in every species were significantly below their respective TDI values, indicating that the daily consumption of nine different metals (loids) through the ingestion of ten fish species in this study does not present any adverse health effects for humans. Among the metals, Cr and Mn had the highest TDI/EDI ratio (> 1000), while Ni and Cd had the lowest TDI/EDI ratio (< 40) (Table 4).
Nonetheless, relying solely on EDI analysis is insufficient to assess the safety of food sources. Therefore, THQ values were calculated (Table 5). THQ and HI values of all metals in fish species remained below 1. (Table 5). These results suggest that metal intake does not pose a non-carcinogenic health risk to consumers.
Among the fish species examined, F. grey mullet had the highest HI value (1.62E−02) due to the high THQ of Cd, Se and inorganic As (Table 5). Similar results have been reported by many researchers (Kamunda et al. 2016; Makedonski et al. 2017; Korkmaz et al. 2017, 2019b; Varol et al. 2019). Due to their low RfD values compared to their concentrations, Se, Cd and inorganic As are the three main contributors to HI; the least contributing metals are Ni and Co. Due to their low RfD values compared to their concentrations, Se, Cd and inorganic As are the three main contributors to HI, with Ni and Co metals contributing the least.
In this study, CR value > 10−4 in E. anchovy and R. mullet was found < 10−6 in Rainbow trout E. barracuda, E. seabream, M. horse mackerel, E. seabass E. pilchard, F. grey mullet and Common carp (Table 5). These findings indicate that consumption of E. anchovy and R. mullet may pose a carcinogenic risk due to exposure to inorganic As. of the fish species, trout is safer in terms of carcinogenic risk.
Metal pollution index (MPI)
If the MPI value is > 1, it indicates that there is contamination, while that is < 1 indicates that there is no contamination (Rakocevic et al. 2018). In this study, MPI values were found to be well below 1 in all fish. The highest MPI value was found in F. Grey mullet (0.009) (Fig. 3).
Conclusion
The health risk assessment results (EDI, THQ, and HI) for the mean concentrations of heavy metals in the muscle tissue, which is the edible portion of various fish species indicated no discernible threat to human health. However, the combination value of the trace metals identified in the study, HI was measured as < 1 for the fish consumed and assessed, indicating no potential health risk to human health. Health risks may vary for different populations depending on the amounts consumed. Therefore, the contaminant levels of fish caught from industrialized areas should be determined and potential health risks should be identified at regular intervals. Low fish consumption (15 g/day) may have c ontributed to the low health risk assessment.
The impact of heavy metal concentration and its effects on fish should be monitored from time to time to perfectly understand the effects of these pollutants on fish growth and the viability of population dynamics. Therefore, it is very important and beneficial to monitor and control pollutants such as heavy metals that adversely affect human health by leaving residues in fish. Fish, which are an important source of protein, need to be checked periodically by relevant organizations to avoid being affected by heavy metal pollution.
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
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All authors take public responsibility for the content of the work submitted for review. The authors confrm their contribution to the paper as follows: Hadeel Abduljabbar Abbas Almafrachı: Investigation, Methodology, Software, Methodology. Writing–review & editing. Numan Emre Gümüş: Investigation, Conceptualization, Methodology. review & editing. İlkay Çorak Öcal: Investigation, Conceptualization, Supervision.
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Almafrachi, H.A.A., Gümüş, N.E. & Çorak Öcal, İ. Heavy metal bioaccumulation in fish: ımplications for human health risk assessment in ten commercial fish species from Konya, Türkiye. Int. J. Environ. Sci. Technol. (2024). https://doi.org/10.1007/s13762-024-05875-3
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DOI: https://doi.org/10.1007/s13762-024-05875-3