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Foods and Raw Materials, 2021, vol. 9, no. 2
E-ISSN 2310-9599 ISSN 2308-4057
Research Article https://doi.org/10.21603/2308-4057-2021-2-317-323
Open Access Available online at http:jfrm.ru/en
Farmed Turkish salmon: Toxic metals and health threat
Levent Bat* , Elif Arici , Ay§ah Oztekin , Fatih §ahin
University of Sinop"®, Sinop, Turkey * e-mail: leventbat@gmail.com Received June 20, 2021; Accepted in revised form July 12, 2021; Published online September 09, 2021
Abstract:
Introduction. Toxic metals in fish, even at low levels, have negative consequences for human health. Even essential metals pose a health threat if consumed in certain quantities. Mercury, cadmium, and lead are the most frequent metals containing in fish. The research objective was to inspect the quality of aquaculture fish found in most major grocery chains across Turkey. Study objects and methods. The present research featured the quantities of Zn, Fe, Cu, Al, Pb, Hg, and Cd in Turkish salmon. The sampling took place between February and June 2019. The cumulative carcinogenic and non-carcinogenic risk for consumers was evaluated based on trace element levels in a prospective health risk assessment using the U.S. EPA model of lifetime exposure. Results and discussion. Fe proved to be the most abundant element in fish fillets, followed by Zn and Cu. Other elements appeared to be far below the permissible values, namely Al < 0.5, Cd < 0.02, Pb, and Hg < 0.05. All the trace elements detected in Turkish salmon were below the reference dose values. The percent contribution to total risk by Fe, Cu, and Zn were 34.20, 24.80, and 41.01%, respectively. The hazard index was < 1. The contamination of aquaculture fish fillet proved insignificant, and the carcinogenic risk was entirely negligible.
Conclusion. The research revealed no hazardous trace elements, and their cumulative effects were not indicated in the hazardous index.
Keywords: Salmon, heavy metals, estimated daily intake, hazard index
Please cite this article in press as: Bat L, Arici E, Oztekin A, §ahin Fa. Farmed Turkish salmon: Toxic metals and health threat. Foods and Raw Materials. 2021;9(2):317-323. https://doi.org/10.21603/2308-4057-2021-2-317-323.
INTRODUCTION
Rainbow trout from North America is one of the most profitable members of the family in Turkish freshwater farming. Black Sea trout, also known as Turkish salmon, has now taken its place on the Turkish fish market, following the decision of the General Directorate of Fisheries and Aquaculture of the Ministry of Agriculture and Forestry. Turkish salmon grows in dam lakes until its weight reaches 180-220 g. After that, it is put into farms in the cold-water areas of the Black Sea. It is harvested when it weighs 3-4 kg.
In 2019, fish farms produced 116 053 tons of Turkish Salmon in inland waters and 9692 tons in sea farms [1]. This amount is constantly increasing compared to previous years. Farmed trout from Turkey's southern Black Sea littoral proved to be a rich nutritional source of fatty and amino acids, which normalize atherogenicity and thrombogenicity indices of blood [2].
Trout is mobile and prefers clean and oxygen-rich waters. As a result, even a slight contamination affects this fish, long before the water quality deteriorates.
Even at low concentrations, metals in contaminated foods have harmful effects on human health [3]. Metal contamination occurs in nature; nevertheless, human activities, such as mining and heavy industry, have severe consequences for ecosystems and aquatic environment. Despite advancements in sewage effluent technology, sewage discharge remains a major challenge in many developing countries [4].
Metals have a strong impact on marine environment and make their way into human food chains. Such toxicants as Hg, Cd, and Pb are associated with fish consumption. Methyl Hg poisoning induced by prenatal ingestion of contaminated fish causes infant mortality and severe birth defects, such as mental retardation, cerebral palsy, and various neurological disorders [5-7]. When Cd is deposited in the proximal tubular cells of the kidney, it causes renal failure because of the decreasing glomerular filtration rates [8]. Pb poisoning affects renal, hematological, cardiovascular, gastrointestinal, and reproductive systems. Moreover, skeletal abnormalities may occur as a result of renal dysfunction and Pb accumulation in the bones [9-11].
Copyright © 2021, Bat et al. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.
Even though some metals are necessary, when their level in the tissues exceeds a certain threshold, they damage both individual organs and the entire organism.
Fish, as an essential aquatic food in the human food chain, has often been tested for metal contamination [3, 12-14]. Several studies have identified metal residues in various fish species, including trout. Rainbow trout has also been subjected to toxicological studies, which detected accumulation in tissues and liver even at low concentrations of Zn [15].
The current research dealt with both cancer and non-cancer hazards associated with trace elements (Fe, Zn, Cu, Al, Pb, Hg, and Cd) in Turkish salmon. Despite the fact that wellness threat assessment models were predominantly created in Europe and the United States, the European model is still in development, getting ever more complex [16]. The American model, according to Grzetic and Ghariani, is detailed and accurate [16]. It is accessible through the Risk Assessment Information System (RAIS), which is backed up by chemical characteristic established and gathered by the U.S. Environmental Protection Agency (U.S. EPA) Integrated Risk Information System [17]. Following [18-22], this research was based on the American model produced by the U.S. EPA [23, 24].
SRUDY OBJECTS AND METHODS
Turkish salmon samples collection. The object of the study was Turkish salmon collected from the Yakakent farm between February and June 2019 (three individual samples per month). The samples were randomly picked from fish offered for sale (Fig. 1). The samples were washed, stored in iceboxes, and transported to the Hydrobiology Laboratory, the Department of Fisheries, to be tested for Fe, Zn, Cu, Al, Pb, Hg, and Cd. Prior to the analysis, the fish samples were documented for the required biological parameters, e.g. wet body weight and total length. The measurements were based on the European Parliament's Animal Care and Use Directive on the Protection of Animals Used for Scientific Purposes [25]. After that, the samples were filleted (Fig. 2), put into polyethylene bags, and stored at 21°C.
Analytical procedures. The trace elements in the Turkish salmon fillets were determined by
inductively coupled plasma mass spectrometry (ICP-MS) after applying the pressure digestion method at an environmental food analysis laboratory accredited in Turkey (TURKAK Test TS EN ISO IEC 17025 AB-0364-T). European Standard method EN 15763 was used to determine trace elements using acid, wet digestion, and standard reference material. The outputs were presented as mg/kg wet wt.
Daily trace elements intake. Risk evaluations for infants, children, and adults were conducted in order to determine the potential hazards that may arise as a result of consuming heavy metals with Turkish salmon. The risks were defined by calculating the probability of health hazard based on potential exposure. The risk exposure depended on the daily consumption of elements (mg/kg body weight per day). The estimated daily intake (EDI) was calculated using element levels and the amount of the fish consumed. The EDI of trace elements was calculated using the following equation:
EDI =
Cmetal (%)x Wfish(||)
BW (kg)
(1)
where C
is trace elements levels in the fillet;
Wfish is the daily mean consumption ofthe fillet, which was reported as 0.041, 0.027, and 0.013 kg/day for adults, children, and infants, respectively [26]; and BW refers to an average adult's body weight of 70 kg, a child's weight of 30 kg, and an infant's weight of 10 kg.
Carcinogenic and non-carcinogenic risks. The incremental lifetime cancer risk (ILCR) model was used to predict the likelihood of cancer risks in the fish caused by exposure to carcinogenic trace elements:
ILCR = CDI x SF
(2)
where CDI stands for chronic daily consumption of a carcinogen in mg/kg of body weight per day, and refers the lifetime mean diurnal dose of exposure to the carcinogen. The cancer risk connected with the exposure
Figure 1 Turkish salmon
Figure 2 Fillet of Turkish salmon
to a carcinogenic or potentially carcinogenic material was calculated using slope factors (SF) [17].
If the ILCR was < 10-6, it was regarded negligible; if it was 10-6 < ILCR < 10-4, it was assessed as permissible
where CDI is the chronic daily intake of carcinogen; Cis the trace element concentrations in the fillet;
fish '
EF is the exposure frequency; ED is the exposure duration; FIR is the fish ingestion rate for adults; AT is the averaging exposure time for non-carcinogenic effects and 70 years of lifetime (LT) for carcinogenic effect; AT is the averaging exposure time for non-carcinogenic effects and 26 years of exposure for carcinogenic effect; BW is the body weight.
Many recent studies used the Target Hazard Quotient (THQ) to peruse the potential non-carcinogenic effect of elements in the edible tis sues of fish. In the present study, THQ was computed esing the following equation to assess non-carcinogenic risks for trac eelements in the fillet for adults [27-33]:
THQ = ^- (5)
^ Rf.D.
where Rf.D. is an estimate of daily exposure that is unlikely to have significant adverse effects over the lifetime.
The U.S. EPA oral reference doses for Fe, Zn, Cu, Al, and Cd are 0.7, 0.3, 0.04, 1.00, and 0.001 mg/kg/day, respectively [23, 24]. The Rf.D. value for Hg inorganic salts is 0.0003 in the Risk Assessment Information System (RAIS). However, there is no Rf.D. value for Pb and its compounds [17]. The oral slope factor, on the other hand, is only indicated for Pb and its compounds as 0.0085 mg/kg/day [17]. The Hazard Index (HI) was found by summing up the THQs, as illustrated by the equation below:
HI= THQ (Fe) + THQ (Zn) + THQ (Cu) + THQ (Al) + + THQ (Pb) + THQ (Hg) + THQ (Cd) (6)
or tolerated; if the ILCR > 10-4, it was acknowledged as substantial. The carcinogenic and non-carcinogenic CDI values were obtained using the following formula [17]:
(3)
(4)
In the current study, the term "non-carcinogenic effect" (HI) describes the cumulative non-carcinogenic effect. If HI > 1.0, the CDI of a certain element exceeds Rf.D, which indicates that the element poses a potential risk.
Statistical analysis. The statistical analysis was performed using the statistical software SPSS Version 21.0. The one-way analysis of variance (ANOVA) was used to examine the difference in trace element quantities in the fish samples across months, followed by Duncan's post hoc test. The threshold for significance wasset at P < 0.05.
RESULTS AND DISCUSSION
Fifteen Turkish salmon were purchased for trace element analysis. The fish had an average length of 51 cm and a weight of 2.90 kg.
Trace elements in the Turkish salmon. The concentrations of the trace elements observed in the samples of Turkish salmon were generally low (Table 1). Fe appeared to be the most abundant element, followed by Zn and Cu. As long as they do not exceed certain concentrations, such essential elements as Fe, Zn, and Cu are not harmful to biota, including fish.
No Al, Pb, Hg, and Cd concentrations were determined in the fillet samples. In both the European Union Commission Regulation and Turkish Food Codex, the maximum allowable values of carcinogenic Pb, Hg, and Cd are 0.3, 0.5, and 0.05 mg/kg wet wt., respectively [34, 35]. However, neither the European Union Commission Regulation nor the Turkish Food Codex gives any permissible values for Fe, Zn, Cu, and Al [34, 35]. These elements were far below the
CDI Cfish (mg> EF x ED (26 years) x F^C^ f
Dcar. AT /365 days
V year
CDI
AT (t6yeaieS t LT(nc years)) t BW (nc hg) - /mg\ ^/tie Says\ „„ , * ^T„/-ssss mg\ ss-6 kg
Cfish bf)p EF HeiSS p ED (26 yeais) p FIR(-ssssr^)t -TET
n0n-Cai. ATa (f2 t ED (26 year s)) t BW (nc hg)
Table 1 Trace elements content in the fillet of Turkish salmon
Content, mg/kg wet wt.
Fe Zn Cu Al Pb Hg Cd
February 3.9a 2.2a 0.13a < 0.5a < 0.05a < 0.05a < 0.02a
March 4.2a 2.3a 0.11a < 0.5a < 0.05a < 0.05a < 0.02a
April 4.8b 2.7b 0.23b < 0.5a < 0.05a < 0.05a < 0.02a
May 5.5c 2.6b 0.24b < 0.5a < 0.05a < 0.05a < 0.02a
June 6.7d 3.1c 0.33c < 0.5a < 0.05a < 0.05a < 0.02a
Mean ± SD 5.02 ± 1.12 2.58 ± 0.35 0.21 ± 0.08 < 0.5 < 0.05 < 0.05 < 0.02
Letters a, b, c, and d show statistically significant differences (P < 0.05)
Table 2 Estimated daily intake (EDI) of trace elements in Turkish salmon farmed in Yakakent
Trace Rf.D. EDI (2019) mg/day/ kg body wt.
elements Values Infants Children Adults
Fe 0.7 0.006526 0.004518 0.00294029
Zn 0.3 0.003354 0.002322 0.00151114
Cu 0.04 0.0002704 0.000187 0.00012183
Al 1.00 - - -
Pb - - - -
Hg 0.0003 - - -
Cd 0.001 - - -
permissible values, namely Al < 0.5, Cd < 0.02, and Pb and Hg < 0.05.
The sequence of trace elements according to contamination was Fe > Zn > Cu > Al > Pb = Hg > Cd. The reason for the low amounts of Al, Pb, Hg, and Cd could be that the fish farms are located in areas not contaminated by urban or rural sewage. The toxic quantities of Fe, Zn, Cu, Al, Pb, Hg, and Cd in seafood may have a negative impact on consumers' health. As a result, fish farms in coastal areas may be heavily contaminated with non-carcinogenic and carcinogenic hazardous materials that pose a substantial risk to human health. Thus, trace element levels in fish from this area should be regularly monitored and assessed.
In fact, the toxic elements in fish depend on water, food, and sediment. However, accumulation of these elements in food and water usually depends on other factors, e.g. metabolic rate, physiology, ecology, contamination tendency of food, sediment, and the temperature, salinity, and solubility of water, as well as on the interaction of these parameters.
In this study, food intake and uncontaminated water column had an important effect on the amount of trace elements in Turkish salmon, which resulted in a considerable decrease in the toxic elements in question. As metabolic activity decreases with growth and a proportionally lower food intake, the accumulation of
elements decreases quite naturally. The trace elements in Turkish salmon farmed in Yakakent appeared to be below the permissible thresholds set by international and national organizations, confirming the results obtained by other researchers who studied trace element accumulation in trout [31, 36].
Estimated daily intake of trace elements. Table 2 illustrates the EDI values of Turkish salmon farmed in the Black Sea of Yakakent in 2019 for adults, children, and infants.
The toxicity of trace elements in humans is determined by their daily intake. In Turkey, the average fish consumption per adult is still low and remains at 15-20 g/day, compared to the recommended amount of 41 g/day [1, 26]. However, people who live near the coast consume far more fish than those who live in continental Turkey. As a result, the research relied on the data approved by the UN Scientific Committee on the Effects of Atomic Radiation [26]. The consumption of these contaminated fish parts puts the health of the local population at risk.
The EDI calculated for all chemical elements in the fish samples was compared with the toxicologically acceptable level and the oral reference dosage (Rf.D. values). The intake of all the trace elements was below the Rf.D. limits. Thus, the trace elements in Turkish salmon pose no threat for the population of the region.
Human health risks. The Risk Assessment Information System classifies Cd, Hg, and Pb as carcinogenic agents [17]. Chronic exposure to even low levels of Cd, Hg, and Pb could lead to a variety of cancers. If it exceeds a certain threshold value, it can have a carcinogenic effect. Table 3 demonstrates a lifetime risk analysis for Turkish salmon consumers.
Percent contribution to total risk by Fe, Cu, and Zn was determined as 34.20, 24.80, and 41.01%, respectively. According to U.S. EPA, at ILCR 10-6, cancer threat is insignificant, the threshold risk limit of ILCR > 10-4 requires preventive medical measures, while ILCR > 10-3 signals that local public health is under threat. In the present study, the samples of Turkish
Table 3 Chronic Rf. D values, oral slope factor (SP), non-carcinogenic and carcinogenic chronic daily intake (CDI), target hazard quotient (THQ), hazard index (HI), and incremental lifetime cancer risk (ILCR) of trace elements in Turkish salmon in 2019
Elements Chronic Rf.D., Oral slope factor (SF), Noncarcinogenic CDI, Carcinogenic CDI, THQ ILCR
mg/kg/day mg/kg/day mg/kg/day mg/kg/day
Fe 7.00E-01 - 2.82E-03 1.05E-03 4.03E-03
Zn 3.00E-01 - 1.45E-03 5.38E-04 4.83E-03
Cu 4.00E-02 - 1.17E-04 4.34E-05 2.92E-03
Al 1.00E+00
Pb - 8.5E-03
Hg 3.00E-04
Cd 1.00E-03 - - - -
HI 1.18E-02 ~
salmon posed no cancer risk. Since none of the cancer-causing trace elements were detected, Turkish salmon consumption can be considered beneficial. However, a regular control the contamination levels of farmed fish is essential.
Chemicals can be either non-carcinogenic or carcinogenic in health risk assessments. Non-carcinogenic trace elements have a threshold limit. Therefore, they are regarded as having no adverse health effects at doses below the threshold level computed using the dose-response assessment method based on the specific reference dose for each element. Carcinogenic substances, on the other hand, are believed to have no effective threshold limits. This assumption implies that even low doses of the chemicals mean a low risk of cancer developing over time. As a result, there is no such thing as a safe level of exposure to carcinogenic substances [21]. In this sense, risk analysis and regular follow-ups are essential for human health.
The research also featured non-cancer risks of the trace elements in Turkish salmon. The risk level of hazard quotients (HQ) for adults was monitored for Fe, Zn, Cu, Al, Pb, Hg, and Cd. It revealed that consuming these trace elements through a fish-based diet posed a significant non-cancer risk. Individual ingestion of these trace elements from Turkish salmon in this region, on the other hand, is safe (HQ < 1) for the local population. Bat et al. and Yardim and Bat have obtained similar results [31, 35]. The cumulative HI, which is the sum of individual trace element THQs, was also used to describe the non-cancer hazards posed by Turkish salmon. Since the total of hazard quotients was < 1, Turkish salmon revealed no potential risk for human health.
CONCLUSION
The hazard index was < 1, so the concentrations of trace elements (Fe, Zn, Cu, Al, Pb, Hg, and Cd) proved to pose no health threat via consumption. Adults, children, and infants had the same risk ranking, although infants were at a higher risk due to their low body weight. However, since Turkish salmon revealed no carcinogenic trace elements, and the non-carcinogenic trace elements were quite low, no consumer in any group is at risk. Risk within the non-carcinogenic trace elements in Turkish salmon was as follows: Zn (41.01°%) > Fe (34.20%) > Cu (24.80%).
Food safety requires an intensive study program and longitudinal studies on the health risk of trace elements in aquaculture products cultivated in Turkey's coastal waters, regardless of how safe the current results are. The practice of health management, according to Bassey et al., begins with routine monitoring by regulatory bodies, toxicologically assessment of wastewater using conventional procedures, and raising public awareness of health consequences [21].
CONTRIBUTION
The authors were equally involved in writing the manuscript and are equally responsible for plagiarism.
CONFLICT OF INTEREST
The authors declare no conflict of interests regarding the publication of this article.
ACKNOWLEDGEMENTS
The authors wish to acknowledge the Department of Hydrobiology, Fisheries Faculty, University of Sinop, for providing laboratory facilities.
REFERENCES
1. Republic of Turkey Ministry of Agriculture and Forestry General Directorate of Fisheries and Aquaculture. Fishery Statistics [Internet]. [cited 2021 May 10]. Available from: https://www.tarimorman.gov.tr/BSGM.
2. Kaya Öztürk D, Baki B, Öztürk R, Karayücel S, Uzun Gören G. Determination of growth performance, meat quality and colour attributes of large rainbow trout (Oncorhynchus mykiss) in the southern Black Sea coasts of Turkey. Aquaculture Research. 2019;50(12):3763-3775. https://doi.org/10.1111/are.14339.
3. Bat L. 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, Arici E, Öztürk B, editors. Black Sea marine environment: The Turkish shelf. Istanbul: Turkish Marine Research Foundation; 2017. pp. 322-418.
4. Bat L, Gökkurt Baki O. Seasonal variations of sediment and water quality correlated to land-based pollution sources in the middle of the Black Sea coast, Turkey. International Journal of Marine Science. 2014;4(12):108-118.
5. Toxicological profile for mercury. Atlanta: U.S. Department of Health and Human Services; 1999. 20 p.
6. Cadmium dietary exposure in the European population. EFSA Journal. 2012;10(1). https://doi.org/10.2903/j. efsa.2012.2551.
7. Statement on the benefits of fish/seafood consumption compared to the risks of methylmercury in fish/seafood. EFSA Journal. 2015;13(1). https://doi.org/10.2903Zj.efsa.2015.3982.
8. Scientific opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA Journal. 2012;10(12). https://doi.org/10.2903/j.efsa.2012.2985.
9. Toxicological profile for lead. Atlanta: U.S. Department of Public Health and Human Services; 2007. 573 p.
10. Scientific opinion on lead in food. EFSA Journal. 2010;8(4). https://doi.org/10.29037j.efsa.2010.1570.
11. Lead dietary exposure in the European population. EFSA Journal. 2012;10(7). https://doi.org/10.2903/j.efsa.2012.2831.
12. Bat L. One health: The interface between fish and human health. Current World Environment. 2019;14(3):355-357. https://doi.org/10.12944/CWE.14.3.04.
13. Bat L, Arici E. Heavy metal levels in fish, molluscs, and crustacea from turkish seas and potential risk of human health. In: Holban AM, Grumezescu AM, editors. Food quality: Balancing health and disease. A volume in handbook of food bioengineering. Academic Press; 2018. pp. 159-196. https://doi.org/10.1016/B978-0-12-811442-1.00005-5.
14. Bat L, Oztekin A, Arici E, §ahin F. Health risk assessment: heavy metals in fish from the southern Black Sea. Foods and Raw Materials. 2020;8(1):115-124. DOI: http://doi.org/10.21603/2308-4057-2020-1-115-124.
15. Gundogdu A, Yardim O, Bat L, Qulha ST. Accumulation of zinc in liver and muscle tissues of Rainbow trout (Onchorhyncus mykiss Walbaum 1792). Fresenius Environmental Bulletin. 2009;18(1):40-44.
16. Grzetic I, Ghariani ARH. Potential health risk assessment for soil heavy metal contamination in the central zone of Belgrade (Serbia). Journal of the Serbian Chemical Society. 2008;73(8-9):923-934. https://doi.org/10.2298/ JSC0809923G.
17. The Risk Assessment Information System [Internet]. [cited 2021 May 10]. Available from: https://rais.ornl.gov/index. html.
18. Wu B, Zhao DY, Jia HY, Zhang Y, Zhang XX, Cheng SP. Preliminary risk assessment of trace metal pollution in surface water from Yangtze River in Nanjing Section, China. Bulletin of Environmental Contamination and Toxicology. 2009;82(4):405-409. https://doi.org/10.1007/s00128-008-9497-3.
19. Li S, Zhang Q. Risk assessment and seasonal variations of dissolved trace elements and heavy metals in the Upper Han River, China. Journal of Hazardous Materials. 2010;181(1-3):1051-1058. https://doi.org/10.1016/j. jhazmat.2010.05.120.
20. Tepanosyan G, Maghakyan N, Sahakyan L, Saghatelyan A. Heavy metals pollution levels and children health risk assessment of Yerevan kindergartens soils. Ecotoxicology and Environmental Safety. 2017;142:257-265. https://doi. org/10.1016/j.ecoenv.2017.04.013.
21. Bassey OB, Chukwu LO, Alimba GC. Cytogenetics of Chrysichthys nigrodigitatus as bioindicator of environmental pollution from two polluted lagoons, South-Western Nigeria. Journal of Genetics and Genome Research. 2019;6. https://doi.org/10.23937/2378-3648/1410047.
22. Mohammadi AA, Zarei A, Majidi S, Ghaderpoury A, Hashempour Y, Saghi MH, et al. Carcinogenic and non-carcinogenic health risk assessment of heavy metals in drinking water of Khorramabad, Iran. MethodsX. 2019;6:1642-1651. https://doi.org/10.1016Zj.mex.2019.07.017.
23. Risk assessment guidance for superfund. Volume I. Human health evaluation manual (Part A). Interim Final. Washington: U.S. Environmental Protection Agency; 1989. 291 p.
24. Guidance for assessing chemical contamination data for use in fish advisories. Volume 2. Risk assessment and fish consumption limits. Washington: U.S. Environmental Protection Agency; 2000. 383 p.
25. Directive 2010/63/EU of the European parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union. 2010:33-76.
26. Sources and effects of ionizing radiation: United Nations Scientific Committee on the Effects of Atomic Radiation. 2008 Report. Volume I. New York: United Nations; 2010. 683 p.
27. Bat L, Arici E, Sezgin M, §ahin F. Heavy metal levels in commercial fishes caught in the southern Black Sea coast. International Journal of Environment and Geoinformatics. 2017;4(2):94-102.
28. Bat L, Oztekin A, §ahin F. Trace metals amounts and health risk assessment of Alosa immaculate Bennett, 1835 in the southern Black Sea. Discovery Science. 2018;14:109-116.
29. Bat L, Arici E, Oztekin A. Heavy metals health risk appraisal in benthic fish species of the Black Sea. Indian Journal of Geo-Marine Sciences. 2019;48(1):163-168.
30. Bat L, Oztekin A, Arici E, §ahin F. Health risk assessment: heavy metals in fish from the southern Black Sea. Foods and Raw Materials. 2020;8(1):115-124. https://doi.org/10.21603/2308-4057-2020-1-115-124.
31. Yardim O, Bat L. Human health risk assessment of heavy metals via dietary intake of Rainbow trout from Samsun fish markets. Journal of Anatolian Environmental and Animal Sciences. 2020;5(2):260-263. https://doi.org/10.35229/ jaes.702810.
32. Bat L, §ahin F, Oztekin A, Arici E. Toxic metals in seven commercial fish from the southern Black Sea: Toxic risk assessment of eleven-year data between 2009 and 2019. Biological Trace Element Research. 2021. https://doi. org/10.1007/s12011-021-02684-4.
33. Majlesi M, Malekzadeh J, Berizi E, Toori MA. Heavy metal content in farmed rainbow trout in relation to aquaculture area and feed pellets. Foods and Raw Materials. 2019;7(2):329-338. https://doi.org/10.21603/2308-4057-2019-2-329-338.
34. Commission Regulation (EC) No 1881/2006. Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union. 2006;364:5-24.
35. Communiqué on maximum limits of contaminants in foodstuffs. Official Gazette. 2008;(26879). (In Turkish).
36. Bat L, Oztekin A, Yardim O. Metal levels in large sea trout from Sinop fish market. Fresenius Environmental Bulletin. 2018;27(12):8505-8508.
ORCID IDs
Levent Bat http://orcid.org/0000-0002-2289-6691 ElifArici https://orcid.org/0000-0001-6359-9194 Ayçah Oztekin https://orcid.org/0000-0002-3726-7134 Fatih Çahin https://orcid.org/0000-0003-0605-2672
