Abstract
Concentrations of toxic metals (Cd, Hg and Pb) in the edible tissues of seven commercial fish species (Mullus barbatus, Merlangius merlangus, Scophthalmus maximus, Mugil cephalus, Engraulis encrasicolus, Trachurus mediterraneus and Sarda sarda) collected from Sinop coasts of the southern Black Sea were detected in 11 years. In several fish samples, the concentrations of elements (Cd, Hg and Pb) were not detected or were below the detection level. The present study showed that Pb was the most and Cd was the least accumulated metal in the studied fish species. The concentrations of those metals are below the international organizations’ recommended limit. It was shown that the estimated metal dose values for daily average consumption and hazarded quotients (HI) in fish samples are below safety levels for human consumption (HI˂1). From the human health point of view, this study showed that there was no possible health risk to people due to intake of any studied species under the current consumption rate in the country for 11 years. This study could be useful as a baseline data for metals exposure.
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Introduction
Fish are healthy foods with high nutritional value for humans [1]. It is considered to be a good source of high biological value protein, which contains a good balance of good amino acids and fats, and highly useful polyunsaturated fatty acids. In addition, fish are easily digestible and a good source for most B-complex vitamins and contain important minerals. Due to their good taste and low cost compared to red meat, fish provide the opportunity for consumers to meet their daily nutritional needs as an animal protein source [2]. Despite their known benefits, fish can biologically accumulate non-essential toxic metals, which can pose potential people health risks to consumers even at small quantities.
It is well known that environmental problems come to the forefront in parallel with both industrial and population growth [3]. The amounts of toxic heavy metals in marine coastal environment and marine organisms especially fish have been of notably concern owing to their toxic effects which are threats in human beings. Heavy metals have the tendency to accumulate in fish, which in turn may enter the human metabolism due to consumption causing major health risks. Cd and Hg are the very toxic metals, followed by Pb. They are non-essential metals, as they are toxic, even in trace amounts, due to its high toxicity, bio-accumulative properties, and deleterious effects on biota [4, 5]. Fish can easily accumulate toxic metals, especially Cd, Hg and Pb, which are among the most important of these contaminants [6].
The Black Sea accumulates terrestrial contaminants, mostly through rivers. However, it accumulates many contaminants in the Black Sea by means of industrial, shipping, agricultural, domestic, touristic, harbour and fishing activities on its coasts. Fish are exposed to contaminants such as toxic metals in polluted waters. Toxic metals from the anthropogenic activities are continually entered into the marine ecosystem [7]. They are major health risks owing to of their toxicity, bioaccumulation, biomagnifications and long-persistence in the food chain. For example, mercury, cadmium and lead are highly toxic and may be reason for mental and central nervous system detriment. It is therefore necessary to detect and observe metal amounts in seafood, because metal ions can readily accumulate in fish more than those in other foodstuffs. Non-essential metals are toxic to fish even at very low concentrations. As a result of the risks associated with the consumption of metals, in order to assess the potential risks associated with the consumption of contaminated fish, it is necessary to periodically evaluate their level of concentration in the commercial fisheries of Turkey [8].
Although Sinop province is small, it is an important fishing centre [9, 10]. The ability of fishes to concentrate heavy metals in their muscles is well known. Considering the above information, we selected muscles as the primary site of metal accumulation in this study, and since fish are an essential component of human diet, they need to be carefully screened to ensure that excessive high heavy metal levels are not transmitted through ingestion to people. The present study is related to the monitoring of toxic metal distribution in the seven commercial fish from the southern Black Sea between 2009 and 2019 and to evaluate them in terms of human health. The daily intakes of the toxic metals from the consumption of the fish samples were also estimated for infant, children and adults, and hazard quotients (HIs) in fish samples were calculated to determine the health risks due to the consumption of commercial fish. In addition, the results were compared with values permitted by national and international organizations. In all Turkish seas particularly in the Black Sea, many studies have been conducted concerning metal accumulation in fish. The difference between this study and the others is that it is a regular monitoring study for 11 years.
Materials and Methods
Study Area
Sinop Peninsula is a natural port and an attractive centre for fishermen (Fig. 1). Since the coasts of Sinop have few settlements and no industrial activity, these coasts are regarded as clean region [11]. An important part of the Southern Black Sea fishing is obtained from here. Not only fishermen in Sinop but also fishermen in other Black Sea provinces catch fish from here. For 11 years, samples of seven fish species that went from commercial fishing boats for sale to fishing markets in Sinop of the southern Black Sea were obtained for toxic metal analysis. Fish samples were taken every year during the fishing season. T.R. the Ministry of Food, Agriculture and Livestock [12] has determined the minimum sizes of 9 cm for anchovy (Engraulis encrasicolus); 13 cm for red mullet (Mullus barbatus), Mediterranean horse mackerel (Trachurus mediterraneus) and whiting (Merlangius merlangus); 20 cm for flathead grey mullet (Mugil cephalus); 25 cm for Atlantic bonito (Sarda sarda) and 45 cm for turbot (Scophthalmus maximus) [13].
Metal Analysis
For toxic metal analysis, sampled fish individuals from each species were measured and rinsed in clean sea water. All samples were stored deep frozen at −21 °C until their analysis. In each sampling, at least 20 specimens for anchovy, red mullet, Mediterranean horse mackerel and whiting; 10 for flathead grey mullet; 5 for Atlantic bonito and 3 for turbot were used. Metal analyses in fish tissues were measured by accredited laboratories with ICP/MS by applying TURKAK Test TS EN ISO/IEC 17025 NMKL 161, 170, and 186 methods. The measurement limit values of metals are 0.002 for cadmium, 0.001 for mercury and 0.005 for lead.
Health Risk Assessment
Risk from metal intake through ingestion may be characterized using a hazard index (HI) as the ratio of the estimated metal dose (EDI mg/kg of body weight per day) and the reference dose (Rf. D mg/kg year). The RfD values for Hg and Cd are 0.0003 and 0.001 mg/kg day−1, respectively [14]. RfD is not available for Pb. The U.S. Department of Health and Human Services Public Health Service [15] pointed out that it would be unsuitable to develop a RfD for inorganic Pb and its compounds because some of the sanitary impacts related with exposure to Pb happen at blood Pb levels as low as to be essentially without a threshold [16]. Therefore, the RfD value for Pb in this study was 0.0035 as used by many researchers [17,18,19]. The HI was calculated by using the equation below:
If HI > 1.0, then the EDI of a particular metal exceeds the Rf. D, indicating that there is a potential risk associated with that metal. The estimated daily intake (EDI) depends on both the metal concentration and the amount of consumption of fish. The Turkish Statistical Institute reported that the average amount of fish consumed per capita between 2009 and 2019 was changed as 5.4 to 7.6 kg per year [12]. However, this amount is higher in people living in the cities on the Black Sea coast [1]. The EDIs of metals were determined using the following equation:
where Cmetal is the concentration of metals in fish; W represents the daily average consumption of fish is given as: 0.013, 0.027 and 0.041 kg/day for infants, children and adults, respectively [20]; and m is the body weight of 10 kg for infants, 30 kg for children and 70 kg for adults.
Statistical Analysis
The samples were analysed in triplicate and the average results were used to represent the data. The Durbin-Watson test was used to measure of autocorrelation in residuals from regression analysis. Autocorrelation is the similarity of a time series over successive time intervals. The significance was set at 0.05 and statistical software was performed by IBM SPSS-21 to examine the effect of years and the metal concentrations in fish species. Microsoft Excel 2010 was used for conducting other calculations. All values were being expressed on mg/kg wet wt. basis.
Results and Discussion
The concentrations of toxic metals (Hg, Cd and Pb) in muscle tissue of seven commercial fish species under this study for 11 years are presented in Fig. 2. There were significant differences in toxic metal levels between fish species. It revealed that the order of mean concentrations of the toxic metals in the muscles of all fish species is recorded as follows: Pb > Hg > Cd.
Toxic metals are not necessary for living metabolism at any level. Even the lowest levels of these metals can harm living organisms and indirectly humans through food. Toxic metals (Cd, Hg and Pb) therefore have been included in the hazardous metals’ legislation of the European Union and Turkish Food Codex. The European Commission Regulation [21] and Turkish Legislation [22] indicate that maximum levels of Pb, Hg and Cd are 0.30, 0.50 and 0.05 mg/kg wet wt., respectively. In this study, no toxic metal value exceeded the allowable values in the fish species studied (Fig. 2).
Hg concentrations in the muscle tissues of seven commercial fish species from the southern Black Sea were detected from 0.0033 to 0.083 mg/kg wet wt. Maximum Hg levels were found in red mullet (0.083 mg/kg wet wt.) in 2015, followed by a turbot with 0.065 mg/kg wet wt. in 2012. Similarly, the mean Pb value was the highest in turbot and red mullet, whereas the lowest was found in anchovy. Based on the increasing Hg and Pb values in benthic species, it may indicate that the biggest difference occurs between pelagic and benthic species. Although they are non-migratory and benthic species, different Hg and Pb accumulations were observed in their tissues. These differences may have resulted from the variation in their diet and accumulation strategies. Generally, the benthic species accumulated higher concentrations of the Hg, due to the greater exposure to Hg-enriched sediment and interactions with benthic organisms in the enriched sediment.
Although there is no industrial pollution in Sinop, organic material originating from domestic wastes and land-based pollution is dumped on the shores [23]. Hg concentrations were found relatively higher enrichment values than other metals. It is assumed that the high enrichment factor values show an anthropogenic source of heavy metals [24]. They concluded that Hg may be transported from the atmosphere as vapour then to the coastal environment.
According to the mean metal values, the highest Cd level was found in anchovy followed by turbot and Mediterranean horse mackerel and the lowest in flathead grey mullet and whiting. This difference may be due to the pelagic fish feeding through different water bodies.
While fish are an important source of protein, rapid industrialisation and mechanized farming practices affect fish, leading to an increase in the concentration of toxic metals in fish. Depending on their feeding habits and habitats, age, and size of the fish, metal concentrations can differ between species. Ecological requirements, metabolism and feeding patterns, behaviour and body size are suggested to be the result of different metal levels in different species of fish.
In the study, the Durbin-Watson test was applied to show whether there is “autocorrelation” on 11-year data. This is done in 3 steps. In the first step, the normality test of the data was performed for homogeneous distribution. If the data is normal, Shapiro-Wilk (Sig.) is used; if not, a logarithmic transformation is made. Therefore, values less than 0.05 have been converted as Log. Then, ANOVA was applied for these data. In the second step, the regression test was performed and R2 values greater than 0.4 were determined. In the 3rd step, the values that should be meaningful, that is, p2 less than 0.05, were calculated. Results are presented in Table 1.
The Durbin-Watson (DW) test was applied to the data that provided the above three steps. If the values found are between 1.5 < DW <2.5, there is no “autocorrelation”, i.e. no trend here. If DW results are DW <1.5, there is a positive correlation between residues, meaning that trend metal levels have increased over the years. If the DW results are 2.5 < DW, there is a negative correlation between residues, which means that trend metal levels have decreased over the years. Accordingly, annual decreases of levels were observed for Hg in anchovy, Cd in Mediterranean horse mackerel and Pb in Atlantic bonito (Table 1). No correlation could be found in trend analysis for other fish species.
It is important to investigate these yearly fluctuations. In the North Sea, the Sound and the Great Belt, the time trend analysis (Pleuronectes platessa and Platichthys flesus—11 years) showed a recent decrease in Pb concentrations, whereas the yearly variation among the Cd, Cu, Hg and Zn concentrations was high [25]. Polak-Juszczak reported that there was a downward trend in the contents of Pb, Hg and As, an upward trend which was noted in Zn and no change trends in Cu and Cd in Baltic fish between 1991 and 1997. It was stated that differences of the heavy metal content in tissue depend on the fish species as well as on their habitat [26].
Daily Intake of Metals and Hazard Quotient
This study was also conducted for the fish muscle as this tissue was the most important part consumed by people. According to Turkish the Ministry of Agriculture and Forest General Directorate of Fisheries and Aquaculture [12], estimates of fish consumption in Turkey indicated that the adult population consumes 21 g wet wt./person/day of fish species. This amount is higher for the coastal cities of the Black Sea, especially Sinop [8]. The EDI (estimated daily intake) values presented in Table 2 were estimated by assuming that infants, children and adults will consume 0.013, 0.027 and 0.041 kg fish per day, respectively. The result revealed that the EDI values for the examined fish samples were below the recommended values, indicating that health risk associated with the intake of these toxic metals through the consumption of seven commercial fish species was absent.
The daily intakes (EDI) of the metals were estimated as the means of Hg, Cd and Pb in commercial fish species and the mean consumption of fish per day for infants, children and adults, respectively, as reported by the UNSCEAR [20]. Table 2 shows that EDIs of toxic metals (Hg, Cd, Pb) are much below the recommended values of the FAO (2004) [27]. Estimated hazarded quotients (HI) of the metals suggest that these toxic metals in fish samples do not pose any apparent threat to the population, where the HIs of all the considered metals were below the value of 1 (US-EPA) as shown in Table 2.
Comparison of the Results with the Available Literature
Comparisons were made with heavy levels found in the literature for the studied commercial fish species from elsewhere, where possible, on those from different waters in the Black Sea (Table 3).
Hg in Fish Species
Hg is very well known as one of the most toxic metals to humans and fishes. The average levels of Hg revealed in the edible tissues of the seven commercial fish studied were found to be low. Compared to other metals, Hg has been less studied as it is more expensive to measure and takes a lot of work. The amount of Hg in Engraulis encrasicolus was found to be less in the current study compared to other studies [28, 69]. The Hg levels in Trachurus mediterraneus and Sarda sarda were found to be much higher on the Bulgarian coasts [48, 50].
Although Hg levels in Merlangius merlangus were the same in this study [46, 57, 58, 62], it was higher in other studies [28, 55, 57, 63, 65].
Hg levels in Mullus barbatus were found to be high in the studies conducted by Ergül and Aksan, Özden et al. [43, 55].
Hg levels in Mugil cephalus were found to be the lowest in the present study and the highest was found in the study conducted by Stancheva et al. [53] in Varna Lake.
Hg levels in Scophthalmus maximus were found to be the lowest in the study conducted by Bat et al. [46] and the highest in the study conducted by Tüzen [28].
Cd in Fish Species
Cd is also known to be one of the most dangerous metals to people. The mean levels of Cd revealed in this study are different but low in all fish species (Fig. 2). In the scientific literature in Table 1, similar Cd values were recorded in the muscles of E. encrasicolus from the Black Sea coasts [30, 33, 35], while low levels of Cd were found in the muscles of E. encrasicolus from Rize coasts in the Black Sea [40]. On the other hand, some studies have shown high levels of Cd in the muscles of anchovy in the Black Sea coasts [28, 34, 42].
Cd levels were generally found to be low in the muscles of T. mediterraneus. The lowest values were obtained from this study, followed by the Bulgarian coasts [48, 50].
The findings of this study were found to be the least in Cd levels in the muscles of S. sarda and were similar to those of Nisbet et al. [30] and Ergül and Aksan [43]. The highest value was found in Atlantic bonito with 0.20 ± 0.01 mg/kg wet wt. on the Kastamonu coasts of the Black Sea [52].
Cd levels in the muscles of M. merlangus, which are frequently used in monitoring studies, were found to be very different in different studies. The highest value was found in whiting with 4.05 ± 0.14 mg/kg wet wt. on the coasts of Trabzon [60], followed by Giresun coasts with 0.66 ± 0.08 mg/kg wet wt. [42] and Amasra coasts with 0.40 ± 0.29 mg/kg wet wt. [56], respectively.
M. barbatus is the other fish most commonly used in monitoring studies and the highest Cd value was obtained from Trabzon coasts with 3.38 ± 0.06 mg/kg wet wt. [60], followed by Kastamonu coasts 0.28 ± 0.03 mg/kg wet wt. [52] and Samsun coasts with 0.20 ± 0.11 mg/kg wet wt. [38], respectively.
The lowest Cd level in M. cephalus was found in this study. However, the high values were determined in flathead grey mullet from Giresun and Rize coasts of the Black Sea [42].
In S. maximus, Cd levels were generally found to be very low except for a study of Tüzen [28].
Pb in Fish Species
Another important toxic metal is lead. In this study, Pb values were higher than both Cd and Hg as expected. Pb levels differ widely in other studies. Comparing the results of the present study with previous studies, Pb levels in E. encrasicolus were found to be high on the coasts of Giresun, Trabzon and Rize [42].
Although Pb levels in T. mediterraneus were below the allowed values (0.3 mg/kg wet wt.) in all studies, it was found to be the highest value (0.25 mg/kg wet wt.) in the study conducted by Alkan et al. [34].
Pb levels in S. sarda were found above the permissible values (0.3 mg/kg wet wt.) in many studies [28, 38, 42, 52]. Likewise, Pb levels in M. merlangus and M. barbatus were found to be much higher than allowed values in many studies [28, 38, 42, 52, 56, 57, 64].
Pb levels in M. cephalus were below the allowed values, except for Tüzen [28] and Türkmen and Akaydın [42]. Pb levels in S. maximus were below the accepted values (0.3 mg/kg wet wt.) in all studies (Table 3).
Conclusion
Toxic metals are among the contaminants which could pose a danger to marine coastal environments in general and fish fauna in particular. Owing to their extremely high toxicity, even at low concentrations, their sustained persistence in the environment and their propensity to bioaccumulate in fish species, these elements are very harmful because they are not biodegradable and thus concentrate large amounts of them in their tissues. Therefore, for the evaluation of the possible health risks associated with the consumption of fish from the coasts of the Black Sea, awareness of the toxic metal values in these fish is of great importance.
In this study, the toxic metal concentrations for seven commercial fish species have been analysed. The most Pb was found in all studied fish muscles, followed by Hg and Cd. The results of toxic metal levels in the fish samples did not exceed the permissible limits set for these toxic metals by the European Commission Regulation [21] and Turkish Legislation [22].
The daily intakes (EDIs) of the metals were estimated as the means of Hg, Cd and Pb in all fish samples and the mean consumption of fish per day for infants, children and adults, respectively. These results are significantly lower than the recommended values. The estimated hazarded quotients (HIs) of the considered metals were below the value of 1. Therefore, metals in fish samples do not pose an apparent threat to the population and these fishes are safe for consumption.
References
Bat L (2019) One health: the interface between fish and human health. Curr World Environ 14(3):355–357. https://doi.org/10.12944/CWE.14.3.04
EFSA Scientific Committee (2015) Statement on the benefits of fish/seafood consumption compared to the risks of methylmercury in fish/seafood. EFSA J 13(1):3982, 36 pp. https://doi.org/10.2903/j.efsa.2015.3982
Rainbow PS (1995) Biomonitoring of heavy metal availability in the marine environment. Mar Pollut Bull 31(4–12):183–192
Bryan GW (1971) The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc R Soc Lond 177(B):389–410
Bryan GW (1984) Pollution due to heavy metals and their compounds. In: Kinne O (ed) Marine ecology. John Wiley and Sons Ltd. 5(3):1290–1430
Phillips DJH, Rainbow PS (1994) Biomonitoring of trace aquatic contaminants. Environmental Management Series, Chapman & Hall, London
Bat L (2014) Heavy metal pollution in the Black Sea. In: Düzgüneş E, Öztürk B, Zengin M (eds) Turkish fisheries in the Black Sea. Published by Turkish Marine Research Foundation (TUDAV), Publication number: 40, ISBN: 987-975-8825-32-5 Istanbul, Turkey, p. 71-107
Bat L (2017) The contamination status of heavy metals in fish from the Black Sea, Turkey and potential risks to human health. In: Sezgin M, Bat L, Ürkmez D, Arıcı E, Öztürk B (eds) Black Sea marine environment: the Turkish Shelf. Turkish Marine Research Foundation (TUDAV), Publication No: 46, ISBN- 978-975-8825-38-7, Istanbul, TURKEY, pp. 322–418
Bat L, Sezgin M, Şahin F, Birinci Özdemir Z, Ürkmez D (2013) Sinop city fishery of the Black Sea. Mar Sci 3(3):55–64. https://doi.org/10.5923/j.ms.20130303.01
Bat L, Sahin F, Sezgin M, Gonener S, Erdem E, Ozsandıkcı U (2018) Fishery of Sinop coasts in the Black Sea surveys. Eur J Biol 77(1):18–25. https://doi.org/10.26650/EuroJBiol.2018.388175
Bat L, Öztekin A, Şahin F, Arıcı E, Özsandıkçı U (2018) An overview of the Black Sea pollution in Turkey. MedFAR 1(2):67–86
T.R. the Ministry of Agriculture and Forest General Directorate of Fisheries and Aquaculture (2019) Fishery products statistics. Available at: http://www.tarim.gov.tr/BSGM
Official Gazette of Republic of Turkey (2016) Notice on the organization of amateur fishing no. 4/2. (in Turkish), (Notification No: 2016/36), issue. 29800
U.S. Environmental Protection Agency, Integrated Risk Information System (2018) URL: https://www.epa.gov/risk/regional-screening-levels-rsls-generic-tables [accessed 20.11.2020]
U.S. Department of Health and Human Services Public Health Service (2007) Agency for Toxic Substances and Disease Registry. Toxicological profile for lead. Atlanta, Georgia. URL: https://www.atsdr.cdc.gov/toxprofiles/tp13.pdf [accessed 20.11.2020]
U.S. Environmental Protection Agency IRIS, Lead. Washington, DC (2005) Integrated Risk Information System. URL: http://www.epa.gov/iris/
Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Pollut 152:686–692. https://doi.org/10.1016/j.envpol.2007.06.056
Harmanescu M, Alda LM, Bordean DM, Gogoasa I, Gergen I (2011) Heavy metals health risk assessment for population via consumption of vegetables grown in old mining area; a case study: Banat County, Romania. Chem Cent J 22(5):64. https://doi.org/10.1186/1752-153X-5-64
Bat L, Arıcı E, Öztekin A, Şahin F (2020) Toxic metals in Engraulis encrasicolus (Linnaeus, 1758) from the coastal waters of Sinop in the Black Sea. Ecol Life Sci 15(1):9–14. https://doi.org/10.12739/NWSA.2020.15.1.5A0128
UNSCEAR (United Nations Scientific Committee on the Effects of Atomic Radiation) (2010) Sources and effects of ionizing radiations, UNSCAR 2008 Report to General Assembly with Scientific Annexes Volume I. United Nations, New York
EC (COMMISSION REGULATION) (2006) Setting maximum levels for certain contaminants in foodstuffs, No 1881/2006 of 19 December 2006
Official Gazette of Republic of Turkey (2009) Notifications changes to the maximum levels for certain contaminants in foodstuffs (in Turkish). (Notification No: 2009/22), Issue: 27143
Bat L, Gökkurt-Baki O (2014) Seasonal variations of sediment and water quality correlated to land-based pollution sources in the middle of the Black Sea coast, Turkey. IJMS 4(12):108–118. https://doi.org/10.5376/ijms.2014.04.0012
Bat L, Öztekin HC, Üstün F (2015) Heavy metal levels in four commercial fishes caught in Sinop coasts of the Black Sea, Turkey. TRJFAS 15(4):399–405. https://doi.org/10.4194/1303-2712-v15_2_25
Jorgensen PET, Pedersen S (1999) Spectral pairs in cartesian coordinates. J Fourier Anal Appl 5:285–302. https://doi.org/10.1007/BF01259371
Polak-Juszczak L (2000) Levels and trends of changes in heavy metal concentrations in Baltic fish, 1991 to 1997 Bull Sea Fish Inst p 27-33
FAO (2004) Human energy requirements Report of a Joint FAO/WHO/ UNU Expert Consultation. FAO Food and Nutrition Technical Report Series No.1 Food and Agriculture Organization of the United Nations: Rome
Tuzen M (2009) Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. FCT 47(8):1785–1790. https://doi.org/10.1016/j.fct.2009.04.029
Turan C, Dural M, Oksuz A, Öztürk B (2009) Levels of heavy metals in some commercial fish species captured from the Black Sea and Mediterranean coast of Turkey. Bull Environ Contam Toxicol 82(5):601–604. https://doi.org/10.1007/s00128-008-9624-1
Nisbet C, Terzi G, Pilgir O, Sarac N (2010) Determination of heavy metal levels in fish samples collected from the Middle Black Sea. Kafkas Univ Vet Fak Derg 16(1):119–125
Aygun SF, Abanoz FG (2011) Determination of heavy metal in anchovy (Engraulis encrasicolus L 1758) and whiting (Merlangius merlangus euxinus Nordman, 1840) fish in the Middle Black Sea. Kafkas Univ Vet Fak Derg 17. https://doi.org/10.9775/kvfd.2011.4058
Görür FK, Keser R, Akçay N, Dizman S (2012) Radioactivity and heavy metal concentrations of some commercial fish species consumed in the Black Sea Region of Turkey. Chemosphere 87(4):356–361. https://doi.org/10.1016/j.chemosphere.2011.12.022
Bat L, Sezgin M, Baki OG, Ustun F, Sahin F (2013) Determination of heavy metals in some commercial fish from the Black Sea coast of Turkey. WJST 10(6):581–589. https://doi.org/10.2004/wjst.v10i6.409
Alkan N, Alkan A, Gedik K, Fisher A (2013) Assessment of metal concentrations in commercially important fish species in Black Sea. Toxicol Ind Health 32(3):447–456. https://doi.org/10.1177/0748233713502840
Ergönül MB, Altindağ A (2014) Heavy metal concentrations in the muscle tissues of seven commercial fish species from Sinop coasts of the Black Sea. ROS 16:34–51
Bat L, Kaya Y, Öztekin HC (2014) Heavy metal levels in the Black Sea anchovy (Engraulis encrasicolus) as biomonitor and potential risk of human health. TRJFAS 14(4):845–851. https://doi.org/10.4194/1303-2712-v14_4_01
Rudneva II, Boldyrev DA, Skuratovskaya EN, Zav’yalov AV (2015) Some trace metals pollution of Black Sea anchovy from Crimean Coastal Region (Black Sea and Azov Sea). Adv Dent Res 3(3):341–349. https://doi.org/10.9734/AIR/2015/10756
Türkmen M, Dura N (2016) Assessment of heavy metal concentrations in fish from south western Black Sea. IJMS 45(11):2357–2360
Gundogdu A, Culha ST, Kocbas F, Culha M (2016) Heavy metal accummulation in muscles and total bodies of Mullus barbatus, Trachurus trachurus and Engraulis encrasicolus captured from the coast of Sinop, Black Sea. Pak J Zool 48(1):25–34
Baltas H, Kiris E, Sirin M (2017) Determination of radioactivity levels and heavy metal concentrations in seawater, sediment and anchovy (Engraulis encrasicolus) from the Black Sea in Rize, Turkey. Mar Pollut Bull 116(1–2):528–533. https://doi.org/10.1016/j.marpolbul.2017.01.016
Galaţchi M, Oros A, Coatu V, Costache M, Coprean D, Galaţchi LD (2017) Pollutant bioaccumulation in anchovy (Engraulis encrasicolus) tissue, fish species of commercial interest at the Romanian Black Sea coast. Ovidius Univ Ann Chem 28(1):11–17. https://doi.org/10.1515/auoc-2017-0003
Türkmen M, Akaydin A (2017) Metal levels in tissues of commercially important fish species from Southeastern Black Sea Coasts. IJMS 46(11):1552–1559
Ergül HA, Aksan S (2013) Evaluation of non-essential element and micronutrient concentrations in seafood from the Marmara and Black Seas. J Black Sea/Mediterr Environ 19(3):312–330
Bat L, Sezgin M (2015) Heavy metal levels in some commercial fish from Sinop coast of the Black Sea, Turkey, pp. 645–656. Proceedings of the Twelfth International Conference on the Mediterranean Coastal Environment MEDCOAST 2015, 10 October, Varna, Bulgaria
Bat L, Arıcı E, Sezgin M, Şahin F (2017) Heavy metal levels in commercial fishes caught in the southern Black Sea coast. IJEGEO 4(2):94–102. https://doi.org/10.30897/ijegeo.312584
Bat L, Arıcı E, Öztekin A (2019) Heavy metals health risk appraisal in benthic fish species of the Black Sea. IJMS 48(01):163–168
Bat L, Sezgin M, Üstün F, Şahin F (2012) Heavy metal concentrations in ten species of fishes caught in Sinop coastal waters of the Black Sea, Turkey. TRJFAS 12(5):371–376. https://doi.org/10.4194/1303-2712-v12_2_24
Stancheva M, Makedonski L, Peycheva K (2014) Determination of heavy metal concentrations of most consumed fish species from Bulgarian Black Sea coast. Bulg Chem Commun 46(1):195–203
Plavan G, Jitar O, Teodosiu C, Nicoara M, Micu D, Strungaru SA (2017) Toxic metals in tissues of fishes from the Black Sea and associated human health risk exposure. ESPR 24(8):7776–7787. https://doi.org/10.1007/s11356-017-8442-6
Makedonski L, Peycheva K, Stancheva M (2017) Determination of heavy metals in selected black sea fish species. Food Control 72:313–318. https://doi.org/10.1016/j.foodcont.2015.08.024
Mendil D, Demirci Z, Tuzen M, Soylak M (2010) Seasonal investigation of trace element contents in commercially valuable fish species from the Black Sea, Turkey. FCT 48(3):865–870. https://doi.org/10.1016/j.fct.2009.12.023
Sönmez AY, Kadak AE, Özdemir RC, Bilen S (2016) Establishing on heavy metal accumulation in some economically ımportant fish species captured from Kastamonu costal. Alinteri J Agric Sci 31(B):84–90
Stancheva M, Makedonski L, Petrova E (2013) Determination of heavy metals (Pb, Cd, As and Hg) in Black Sea grey mullet (Mugil cephalus). BJAS 19(1):30–34
Das YK, Aksoy A, Baskaya R, Duyar HA, Guvencn D, Boz V (2009) Heavy metal levels of some marine organisms collected in Samsun and Sinop coasts of Black Sea, in Turkey. AJAVA 8(3):496–499
Özden Ö, Erkan N, Ulusoy Ş (2010) Determination of mineral composition in three commercial fish species (Solea solea, Mullus surmuletus, and Merlangius merlangus). Environ Monit Assess 170(1–4):353–363. https://doi.org/10.1007/s10661-009-1238-5
Fındık Ö, Çiçek E (2011) Metal concentrations in two bioindicator fish species, Merlangius merlangus, Mullus barbatus, captured from the West Black Sea Coasts (Bartin) of Turkey. Bull Environ Contam Toxicol 87(4):399–403. https://doi.org/10.1007/s00128-011-0373-1
Balkis N, Aksu A, Hiçsönmez H (2012) Metal levels in biota from the Southern Black Sea. Turkey. J Black Sea/Mediterr Environ 18:134–143
Alkan N, Aktaş M, Gedik K (2012) Comparison of metal accumulation in fish species from the southeastern Black Sea. Bull Environ Contam Toxicol 88(6):807–812. https://doi.org/10.1007/s00128-012-0631-x
Alkan A, Alkan N, Akbaş U (2016) The factors affecting heavy metal levels in the muscle tissues of whiting (Merlangius merlangus) and red mullet (Mullus barbatus). JAS 22(3):349–359. https://doi.org/10.1501/Tarimbil_0000001393
Aydın D, Tokalıoğlu Ş (2015) Trace metals in tissues of the six most common fish species in the Black Sea, Turkey. Food Addit Contam B 8(1):25–31. https://doi.org/10.1080/19393210.2014.949873
Bat L, Özkan EY, Öztekin HC (2015) The contamination status of trace metals in Sinop coast of the Black Sea, Turkey. CJES 13(1):1–10
Mol S, Karakulak FS, Ulusoy S (2017) Assessment of potential health risks of heavy metals to the general public in Turkey via consumption of red mullet, whiting, turbot from the Southwest Black Sea. TRJFAS 17(6):1135–1143. https://doi.org/10.4194/1303-2712-v17_6_07
Kuplulu O, Iplıkcıoglu Cil GI, Korkmaz SD, Aykut O, Ozansoy G (2018) Determination of metal contamination in seafood from the Black, Marmara, Aegean and Mediterranean Sea metal contamination in seafood. J Hell Vet Med Soc 69(1):749–758. https://doi.org/10.12681/jhvms.16400
Elderwısh MA (2019) Seasonal investigation of heavy metal deposits of water, sediment and some economic fish species of West Black Sea Coasts. Kastamonu University Institute of Science Department of Aquaculture pHD Thesis. 70 pp
Turan H, Altan CO, Kocatepe D (2019) Black Sea whiting: assessment of potential health benefits/risks and differences based on mineral concentrations of meat and roes. TURJAF 7(12):2075–2082. https://doi.org/10.24925/turjaf.v7i12.2075-2082.2780
Harmelin-Vivien M, Cossa D, Cochet S, Bănaru D, Letourneur Y, Mellon-Duval C (2009) Difference of mercury bioaccumulation in red mullets from the north-western Mediterranean and Black seas. Mar Pollut Bull 58(5):679–685. https://doi.org/10.1016/j.marpolbul.2009.01.004
Jitar O, Teodosiu C, Oros A, Plavan G, Nicoara M (2015) Bioaccumulation of heavy metals in marine organisms from the Romanian sector of the Black Sea. New Biotechnol 32(3):369–378. https://doi.org/10.1016/j.nbt.2014.11.004
Durmuş M, Kosker AR, Ozogul Y, Aydin M, Uçar Y, Ayas D, Ozogul F (2018) The effects of sex and season on the metal levels and proximate composition of red mullet (Mullus barbatus Linnaeus 1758) caught from the Middle Black Sea. Hum Ecol Risk Assess Int J 24(3):731–742. https://doi.org/10.1080/10807039.2017.1398071
Bat L, Arici E, Öztekin A, Şahin F (2020) Toxic metals in the warty crab in the southern Black Sea: assessment of human health risk. MBJ 5(1):1–9. https://doi.org/10.21072/mbj.2020.05.1.01
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Bat, L., Şahin, F., Öztekin, A. et al. Toxic Metals in Seven Commercial Fish from the Southern Black Sea: Toxic Risk Assessment of Eleven-Year Data Between 2009 and 2019. Biol Trace Elem Res 200, 832–843 (2022). https://doi.org/10.1007/s12011-021-02684-4
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DOI: https://doi.org/10.1007/s12011-021-02684-4