E-ISSN 2310-9599
Foods and Raw Materials, 2020, vol. 8, no. 1 .„..,,,.. .„._
ISSN 230o-405/
Research Article Open Access
^ Check for updates
DOI: http://doi.org/10.21603/2308-4057-2020-1-115-124 Available online at http://jfrm.ru/en/
Health risk assessment: heavy metals in fish from the southern Black Sea
Levent Bat* , Ay§ah Oztekin , Elif Arici , Fatih §ahin
Sinop University, Sinop, Turkey * e-mail: [email protected]
Received December 27, 2019; Accepted in revised form January 20, 2020; Published February 25, 2020
Abstract:
Introduction. The coastal contamination of the Black Sea has been an important issue for several decades. Heavy metals are the most harmful contaminants which affect people health. The research objective of the present study was to determine the amounts of Cd, Hg, Pb, Cu, and Zn found in the whiting (M. merlangus L.) and the red mullet (M. barbatus L.). These Black Sea bottom fish species have the highest commercial value. The obtained data were used to assess the risk which the fish represents for human consumers. Study objects and methods. The elements were detected using an inductively coupled plasma mass spectrometer (ICP-MS). The amounts of the metals arranged in the following order: Zn > Cu > Pb > Hg > Cd.
Results and discussion. The mean values of Cd, Hg, Pb, Cu, and Zn in the edible tissues were 0.013, 0.024, 0.07, 0.195, and 9.05 mg/kg wet wt. for whiting and 0.017, 0.036, 0.05, 0.29, and 6.4 mg/kg wet wt. for red mullet, respectively. These levels proved lower than the permitted values set by the Ministry of Agriculture, Forestry, and Fisheries of the UK (MAFF), Turkish Food Codex (TFC), and EU Commission Regulation. The target hazard quotient (THQ) for all the elements via consumption of whiting and red mullet were also low.
Conclusion. Hazard index (HI) was < 1, which means that the fish caused no health problems in people who consumed whiting and red mullet caught in the southern Black Sea during the fishing seasons of 2017-2018. The carcinogenic risk index (CRI) for whiting and red mullet was also considered insignificant.
Keywords: Heavy metals, Black Sea, fish, risk assessment, target hazard quotient, carcinogenic risk index
Please cite this article in press as: 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.
INTRODUCTION
Fish is usually located at the top of the food chain in the marine ecosystem. It accumulates contaminants from water, food, bottom sediment, and suspended particles in the water column. Even though available and accessible literature shows that heavy metals accumulated in the Black Sea commercial fish have no detrimental effect on human health [1], this issue remains a matter of public concern. However, the present research confirmed the fact that Black Sea fish is unaffected by environmental situation and is safe to eat.
A review conducted by Bat et al. showed some concern about the increase of unregulated settlements and anthropogenic activities along the marine coastal area of the Black Sea [2]. The growing urbanization and industrialization, as well as the fast development of agriculture, tourism, and fishery, increase the concentration of heavy metals discharged by major
rivers into the coastal waters of the Black Sea. The resulting increase in heavy metals adversely affects the coastal ecosystem.
The contaminants eventually accumulate in marine biota, particularly in fish [3, 4]. Subsequently, metals pass on to people that consume contaminated fish, thus threatening their health [5]. As a result, the environmental issues related to heavy metal contamination of the Black Sea are relevant to all countries along the Black Sea coast. After Romania and Bulgaria entered the European Union, the problem affected the whole of Europe.
The Marine Environment Policy of the Marine Strategy Framework Directive (MSFD) concerns the matters of monitoring chemical elements in edible tissues of seafood and avoiding heavy metal transfer from sea biota to human body via food chain [6]. The MSFD targets the
Copyright © 2020, 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.
subject of sea contamination in Descriptor 8 "Concentrations of contaminants are at levels not giving rise to pollution effect" and Descriptor 9 "Contaminants in fish and other seafood for human consumption do not exceed levels established by Community legislation or other relevant standards" [6]. The objective of the MSFD with concern to Descriptors 8 and 9 is to ensure that contaminants are represented in foods in safe amounts.
According to the main guideline of the European Union, European seas are to obtain the Good Environmental Status (GES) by 2020. The abovementioned facts make studies of chemical elements in commercial fish extremely relevant.
The current study featured two commercial demersal fish species and assessed the heavy metal contamination, as well as the risk that the detected heavy metals represent for human health. The current study concentrated on the effect of Cd, Hg, Pb, Cu, and Zn on consumers' health. The concentrations of the metals were measured in the muscle tissues of whiting and red mullet caught along the Sinop coast of the southern Black Sea and sold on fish markets. The research also included a thorough analysis of scientific literature on the amounts of Cd, Hg, Pb, Cu, and Zn in Black Sea whiting and red mullet. The obtained results could help in achieving the goals set by MSFD 2008/56/EC [6].
STUDY OBJECTS AND METHODS
Sample Collection. Twenty specimens of whiting and red mullet were purchased on fish markets. The sampling was conducted during the fishing seasons of
2017 and 2018 on the Sinop coast of the Black Sea (Fig. 1). The fish samples were processed according to the method depicted by Bernhard and UNEP [6-8]. The edible tissues of M. merlangus L. and M. barbatus L. were dissolved with Suprapur® HNO3 (nitric acid) using a microwave digestion system. The elemental concentrations (Cd, Hg, Pb, Cu, and Zn) of the digested edible samples of whiting and red mullet were studied using the methods recognized by the Environmental Food Analysis Lab Industry and Trade Inc.
Fish tissues were prepared using an inductively coupled plasma mass spectrometer (ICP-MS), based on m-AOAC 999.10 (Association of Official Analytical Chemists with TS EN ISO IEC 17025 AB-0364-T references number) and CSN EN 15763 European Standards. The presence and quantity of the metals were detected according to the instrumental reaction of the equipment. The results were given as mgkg-1 wet weight (wt.).
Health risk assessment. The risk assessment for infants, children, and adults was performed to estimate the possible hazard associated with the consumption of heavy metals contained in the Black Sea fish. The risk exposure demands taking the mean daily intake of the heavy metals (mg/kg/day). The estimated daily intake (EDI) is subjected to the element levels and the amount of ingestion of fish. The EDI of heavy metals was calculated according to the equation below:
C x W EDI = meta'BW fish (1)
where C t, is the amounts of elements in edible tissues;
metal
34°50'0''E 34°55'0''E 35°0'0"E 35°5'0"E 35°10'0"E 35°15'0"E
42°5'0''N "
42°0'0''N -
41°55'0''N .
Figure 1 Fishing area
ii'|Wi represents the daily mean ingestion of fish given as 0.013, 0.027, and 0.041 kg/day for infants, children, and adults, respectively [10]; BW is the body weight of 10 kg for infants, 30 kg for children, and 70 kg for adults.
The target hazard quotient (THQ) has been used in many studies to analyze the potential non-carcinogenic effect of the metals in the edible tissues of fish. The EDI (mg/kg of body wt. per day) of each heavy metal was related with the reference dose (Rf. D, mg/kg/day) as described in the equation below [11-13]:
EDI
THQ =
(2)
Rf.D.
Rf. D. is the oral reference dose for Zn, Cu, Pb, Hg, and Cd as suggested by the US Environmental Protection Agency, i.e. 0.3, 0.04, 0.004, 0.0005, and 0.001 mg/kg/day, respectively [14, 15]. However, in the Risk Assessment Information System (RAIS), the mercury inorganic salts Rf. D. value is 0.0003, and there is no Rf. D. value for lead and compounds [15]. In contrast, oral slope factor is given only for lead and compounds as 0.0085 mg/kg/day [16]. The hazard index (HI) was defined as the sum of the THQs as described in the equation below:
HI= THQ (Zn) + THQ (Cu) + THQ (Pb) +
+ THQ (Hg) + THQ (Cd) (3)
The HI was used in this study to describe the cumulative non-carcinogenic effect. If HI > 1.0, then the EDI of a specific element exceeds the Rf. D, showing that there is a potential risk associated with that element.
The risk index (RI) represents the probability of developing any type of cancer over a lifetime. It is calculated by integrating the EDI with the respective oral slope factors (SF) for heavy metals. Slope factors (SF) are used to reckon the risk of cancer along with exposure to a carcinogenic or probably carcinogenic matter [17]. The description is presented in the equation below:
RI= EDI x SF
(4)
The RI was considered insignificant if the RI was < 10 the RI was considered allowable or tolerable if RI was 106 < RI < 104; the RI was considered significant if the RI was > 10 '.
RESULTS AND DISCUSSION
The average amounts of the heavy metals in Black Sea whiting and red mullet are given in Fig. 2. The amounts of heavy metals in both M. merlangus L. and M. barbatus L. decreased in the following order: Zn > Cu > Pb > Hg > Cd. The essential metals Zn and Cu were represented in higher amounts due to their biological functions, whereas the toxic metals Pb, Hg, and Cd have no biological functions, and their amounts in fish tissues were considerably lower.
0.016
0.012
^ 0.008
0.004
0.04
0.03
0.02
0.01
0.08
^ 0.06
op 0.04
0.02
0.3
0.2
a o.i
10
2017
2018
MM. merlangus M. barbatus
Figure 2 Heavy metal amounts with standard deviation for Cd, Hg, Pb, Cu, and Zn in the edible tissues of M. merlangus L. andM. barbatus L. from the Black Sea coasts caught in 2017 and 2018
0
U
U
U
8
6
4
2
0
Table 1 Estimated daily intakes (EDI) of elements in the edible tissues ofMerlangius merlangus L. from the southern Black Sea
Heavy metals EDI (2017), mg/day/kg body wt. EDI (2018), mg/day/kg body wt.
Infants Children Adults Infants Children Adults
Cd 0.0000156 0.0000108 0.0000070 0.0000182 0.0000126 0.0000082
Hg 0.0000273 0.0000189 0.0000123 0.0000351 0.0000243 0.0000158
Pb 0.0000780 0.0000540 0.0000351 0.0001040 0.0000720 0.0000468
Cu 0.0002730 0.0001890 0.0001230 0.0002340 0.0001620 0.0001054
Zn 0.0114400 0.0079200 0.00515428 0.0120900 0.0083700 0.0054471
Table 2 Estimated daily intakes (EDI) of elements in edible tissues of Mullus barbatus L. from the southern Black Sea
Heavy EDI (2017), mg/day/kg body wt. EDI (2018), mg/day/kg body wt.
metals Infants Children Adults Infants Children Adults
Cd 0.0000234 0.0000162 0.0000105 0.0000208 0.0000144 0.00000937
Hg 0.0000494 0.0000342 0.0000222 0.0000442 0.0000306 0.0000199
Pb 0.0000585 0.0000405 0.0000263 0.0000715 0.0000495 0.0000322
Cu 0.0004030 0.0002790 0.0001815 0.0003510 0.0002430 0.00015814
Zn 0.0093600 0.0064800 0.0042171 0.0072800 0.0050400 0.0032800
Table 3 Target hazard quotients (THQ) and hazard index (HI) of elements consumed with Merlangius merlangus L. caught near the southern coast of the Black Sea in 2017 and 2018
Heavy _THQ (2017)_THQ (2018)
metals Infants Children Adults Infants Children Adults
Cd 0.0156000 0.0108000 0.00702857 0.0182000 0.0126000 0.0082000
Hg 0.0546000 0.0378000 0.0246000 0.0702000 0.0486000 0.03162857
Pb 0.0195000 0.0135000 0.008785714 0.0260000 0.0180000 0.011714286
Cu 0.0068250 0.0047250 0.0030750 0.0058500 0.0040500 0.00263571
Zn 0.0381330 0.0264000 0.01718095 0.0403000 0.0279000 0.01815714
HI 0.1346580 0.0932250 0.060670238 0.1605500 0.1111500 0.072335714
Table 4 Target hazard quotients (THQ) and hazard index (HI) of elements consumed with Mullus barbatus L. caught near the southern coast of the Black Sea in 2017 and 2018
Heavy _THQ (2017)_
metals_Infants_Children Adults
Cd 0.0234000 0.0162000
Hg 0.0988000 0.0684000
Pb 0.0146250 0.0101250
Cu 0.0100750 0.0069750
Zn 0.0312000 0.0216000
HI 0.1781000 0.1233000
THQ (2018)
Infants Children Adults
0.0208000 0.0144000 0.009371429
0.0884000 0.0612000 0.039828571
0.0178750 0.0123750 0.008053571
0.0087750 0.0060750 0.003953571
0.0242666 0.0168000 0.010933333
0.160116667 0.1108500 0.072140476
0.010542857 0.044514286 0.006589286 0.004539286 0.014057143 0.080242857
In this study, the heavy metal amounts in edible tissues varied according to the species. Cd, Hg, and Cu were high in M. barbatus, whereas M. merlangus proved rich in Pb and Zn. These differences may be related to habitat and feeding habits. The red mullet is demersal fish found near sand, gravel, and mud bottoms of the continental shelf. It feeds on small benthic mollusks, crustaceans, and worms. The whiting is benthopelagic fish found mostly near gravel and mud bottoms. Less frequently, it can be found on rock and sand. The whiting feeds on crabs, shrimps, mollusks, polychaetes, and small fish [17].
Cu and Zn are relatively safe for living biota. Therefore, the permissible values of such essential heavy metals as Cu and Zn are not available in the
current European Union and TFC regulations. However, they can be harmful if consumed in large amounts. According to the Ministry of Agriculture, Forestry, and Fisheries of the UK (MAFF), the maximal tolerable limits of Cu and Zn are 20 and 50 mg/kg wet wt., respectively [18]. In this study, the amount of heavy metal detected in whiting and red mullet was found to be significantly lower than these values.
Similarly, the present study revealed that toxic metal values (Cd, Hg and Pb) in edible tissues of whiting and red mullet were below the permissible values (0.05, 0.5, and 0.3 mg/kg wet wt.) set by European Union Commission Regulation and Turkish Food Codex [19, 20]. The Global Agriculture Information Network (GAIN) Report of the Russian Federation defined the
Table 5 Carcinogenic concentration of consumed fish (CDI), hazard quotient (HQ), risk index (RI), and hazard risk (HI) of elements in Merlangius merlangus L. caught near the southern coast of the Black Sea in 2017 and 2018
Heavy _2017_2018_
metals_CDI, mg/kg/day HQ_RI_CDI, mg/kg/day HQ_RI_
Cd 0.0000026 0.0070290 0.0000030 0.0082000
Hg 0.0000045 0.0246000 0.0000058 0.0316290
Pb 0.0000130 - 0.00000011 0.0000170 - 0.00000014
Cu 0.0000450 0.0030750 0.0000390 0.0026360
Zn 0.0019144 0.0171810 0.0020232 0.0181570
HI 0.0518850 0.00000011 0.0606220 0.00000014
Table 6 Carcinogenic concentration of consumed fish (CDI), hazard quotient (HQ), risk index (RI), and hazard risk (HI) of elements in Mullus barbatus L. caught near the southern coast of the Black Sea in 2017 and 2018
Heavy _2017_2018_
metals_CDI, mg/kg/day HQ_RI_CDI, mg/kg/day HQ_RI
Cd 0.0000039 0.0105430 0.0000034 0.0093710
Hg 0.0000082 0.0445140 0.0000082 0.0398290
Pb 0.0000097 - 0.000000083 0.0000119 - 0.0000001
Cu 0.0000670 0.0045390 0.0000580 0.0039540
Zn 0.0015663 0.0140570 0.0012182 0.0109330
HI 0.0736530 0.000000083 0.0640870 0.0000001
permissible amounts of Cd, Hg, and Pb as 0.2, 0.5, and 1 mg/kg wet wt., respectively [21].
Tables 1 and 2 present the EDI values for whiting and red mullet caught near the Sinop coast of the Black Sea in 2017 and 2018 for infants, children, and adults. Tables 3 and 4 feature the THQ and HI values.
The EDI levels of Cd, Hg, Pb, Cu, and Zn were very low for both whiting and red mullet. These values were observed to be lower than their Rf. D. values. Likewise, THQ levels of these elements were very low. The HI values for infants were observed to be higher than those for children and adults. This result suggests that, at a relatively high level of exposure, infants will be more likely at risk than children and adults. Obviously, infants weigh much less than children and adults. However, the total non-carcinogenic indices (HI), which is the sum of THQ values for all the heavy metals studied for each sampling year, were lower than the threshold value of 1.0. Therefore, there were no health risks for infants, children, and adults who consumed whiting and red mullet caught near the southern coast of the Black Sea during the fishing seasons of 2017 and 2018.
In the Risk Assessment Information System, the SP value is given for Pb and its compounds only. The lifetime of a person is stated to be 70 years on average, while the exposure duration is assumed to be 26 years [16]. Tables 5 and 6 show carcinogenic concentration of consumed fish (CDI), hazard quotient (HQ), risk index (RI), and hazard risk (HI) of heavy metals in M. merlangus and M. barbatus caught near the southern coast of the Black Sea. The carcinogenic risk for whiting and red mullet was lower than 10-6 and is considered insignificant. The lowest RI was found in red mullet in 2017.
The results of this study were compared with the studies that featured Merlangius merlangus and Mullus barbatus from the Black Sea. They are presented in Tables 7 and 8, respectively.
In general, the amount of heavy metal found in both Merlangius merlangus and Mullus barbatus proved to be lower than that in other studies. Likewise, Zn is the heaviest metal found in both species. It is followed by Cu, Pb, Cd, and Hg. When compared, Zn, Cu, and Pb were found in high amounts in the whiting collected near the Amasra coasts of the southern Black Sea [31]. Hg was the highest in the whiting caught near the shores of Istanbul in the Black Sea [30]. Cd was detected in both fish species caught near the Trabzon shores. The highest Hg level species was obtained from M. barbatus caught near the shores of Istanbul and Kocaeli in the Black Sea [37]. The highest Pb value was found in the red mullet fished near the Kastamonu shores of the Black Sea [45].
The differences in the amounts of heavy metals found in these fish species may be due to the fact that they were caught during different fishing seasons and in different areas of the Black Sea. Metabolism, physiology, and feeding habits of the fish are different in different seasons. The pollution load also varies in different areas of the Black Sea coast [2]. Similarly, one should not dismiss different applications in heavy metal measurements, equipment accuracy, and human error. Although there are some exceptions, the amounts of heavy metals in these fish species proved to be low. Therefore, they posed no threat to human health.
CONCLUSION
The research featured the effect of Cd, Hg, Pb, Cu, and Zn on the health of infants, children, and adults who
Table 7 Comparison of the amounts (ppm) of heavy metals in the edible tissues ofMerlangius merlangus L. caught near various areas of the Black Sea coast
Location dw/ww Metals Ref.
Zn Cu Pb Cd Hg
Black Sea d.w. 48.6 ± 3.9 1.25 ± 0.10 0.93 ± 0.07 0.55 ± 0.04 - [22]
Black Sea d.w. 8.86-163.28 0.91-8.95 - - - [23]
Trabzon w.w. 8.62 ± 0.54 0.88 ± 0.12 0.25 ± 0.07 0.01 ± 0.00 - [24]
Sinop 12.9 ± 4.14 2.90 ± 0.78 0.46 ± 0.08 0.04 ± 0.01 -
Bartin 5.73 ± 0.37 0.77 ± 0.07 0.18 ± 0.04 0.02 ± 0.00 -
Istanbul d.w. 6.03 ± 0.55 0.50 ± 0.10 0.19 ± 0.02 - [25]
Black Sea w.w. 65.4 ± 4.2 1.32 ± 0.11 0.53 ± 004 0.21 ± 0.02 84 ± 5 ^gkg-1 [26]
Sinop d.w. - - < 0.05 < 0.02 < 0.05 [27]
Samsun - - < 0.05 < 0.02 < 0.05
Samsun, Ordu, Trabzon, Rize d.w 20.6 ± 2.1 1.8 ± 0.2 0.46 ± 0.05 0.18 ± 0.02 - [28]
Samsun, Sinop, Terme, Fatsa d.w. 31.34 ± 1.61 3.72 ± 0.59 0.58 ± 0.03 0.002 ± 0.000 not detect [29]
Ordu
Istanbul w.w. 4.248-30.842 0.001-4.915 0.004-1.581 0.001-0.151 0.003-0.491 [30]
Amasra-West Black Sea w.w. 77.99 ± 46.91 8.53 ± 2.14 6.80 ± 5.88 0.40 ± 0.29 - [31]
Samsun- Turkey d.w. 58 ± 3.5 2.3 ± 0.7 0.9 ± 0.2 0.2 ± 0.03 - [32]
28.3 ± 1 2.7 ± 0.7 not detect not detect
Terkos d.w. - - 15 0.35 0.07 [33]
Sakarya - - 12 0.24 < 0.01
Bafra - - 15 0.07 0.09
Ordu - - 13 0.22 0.5
Trabzon-Turkey d.w. 22.76 ± 2.01 1.02 ± 0.05 0.08 ± 0.03 0.04 ± 0.01 0.05 ± 0.01 [34]
Black Sea d.w. 8.49 0.51 0.01 - - [35]
Sinop d.w. 22.82-34.33 2.85-5.26 0.02 0.08-0.18 - [36]
Black Sea d.w. 18 ± 1.4 2.5 ± 0.06 0.05 ± 0.01 0.03 ± 0.01 0.33 ± 0.02 [37]
Eastern Black Sea, Turkey d.w. 21.5 1.56 0.024 0.031 - [38]
Ordu-Samsun
West Black Sea w.w. 18.1 ± 0.3 1.28 ± 0.07 - - - [39]
Sinop d.w. 16.34 ± 3.83 1.20 ± 0.31 0.69 ± 0.34 0.027 ± 0.012 - [40]
Trabzon-Turkey w.w. - - 0.02 ± 0.00 4.05 ± 0.14 - [41]
Sinop w.w. 3.4 < 0.5 < 0.05 < 0.02 < 0.05 [42]
Sinop w.w. 43 ± 6 0.41 ± 0.02 0.88 ± 0.006 0.075 ± 0.006 not detect [43]
Samsun w.w. 5.04 ± 0.58 1.28 ± 0.09 1.41 ± 0.23 0.06 ± 0.02 - [44]
Sinop 3.47 ± 0.27 0.92 ± 0.08 0.63 ± 0.06 0.05 ± 0.003 -
Kocaeli 3.99 ± 0.5 1.46 ± 0.18 0.69 ± 0.12 0.06 ± 0.01 -
Kastamonu w.w. 5.45 ± 1.12 4.52 ± 0.70 6.12 ± 1.45 0.24 ± 0.02 - [45]
Giresun w.w. 3.77 ± 0.22 2.40 ± 0.25 0.05 ± 0.00 0.66 ± 0.08 - [46]
Trabzon 5.65 ± 0.58 1.62 ± 0.25 1.30 ± 0.31 0.12 ± 0.03 -
Rize 4.08 ± 0.36 1.65 ± 0.26 1.29 ± 0.21 0.08 ± 0.02 -
Southwestern Black Sea w.w. 23.54 ± 6.77 2.44 ± 0.54 0.36 ± 0.42 0.02 ± 0.01 0.01 ± 0.01 [47]
Black Sea w.w. - - 0.099 0.013 0.081 [48]
Sinop w.w. 7.11-17.88 0.18-0.33 0.03-0.09 0.007-0.0085 0.01-0.017 [49]
Sinop w.w. 9.70 ± 1.9 2.90 ± 0.99 1.17 ± 1.01 0.02 ± 0.01 - [50]
Kastamonu 6.74 ± 1.63 2.35 ± 0.36 1.18 ± 0.45 0.03 ±0.01 -
Zonguldak 6.24 ± 0.8 2.25 ± 0.25 0.86 ± 0.34 0.03 ± 0.01 -
Sinop w.w. 12.63 ± 0.22 0.59 ± 0.06 0.19 ± 0.02 0.03 ± 0.00 0.13 ± 0.01 [51]
18.52 ± 0.60 2.10 ± 0.67 0.90 ± 0.28 0.22 ± 0.03 0.23 ± 0.00
Western Black Sea w.w. - - - - 0.01 ± 0.01 [52]
d.w.= dry wt.; w.w. = wet wt.
Table 8 Comparison of the amounts (ppm) of heavy metals in the edible tissues of Mullus barbatus L. caught near various areas of the Black Sea coast
Location dw/ Metals Ref.
ww Zn Cu Pb Cd Hg
Black Sea d.w. 106 ± 9.1 0.98 ± 0.07 0.84 ± 0.07 0.45 ± 0.04 - [22]
Black Sea d.w. 1.424-63.290 0.380-2.714 - - - [23]
Trabzon w.w. 8.26 ± 0.77 1.30 ± 0.13 0.22 ± 0.08 0.02 ± 0.00 - [24]
Sinop 10.5 ± 2.03 0.87 ± 0.09 0.39 ± 0.03 0.03 ± 0.00 -
Istanbul d.w. 7.573 ± 0.389 - 0.727 ± 0.141 0.208 ± 0.017 - [25]
Black Sea w.w. 75.5 ± 5.3 0.96 ± 0.08 0.36 ± 0.03 0.17 ± 0.02 36 ± 2 №-kg-1 [26]
Sinop d.w. - - 0.0525 < 0.02 < 0.05 [27]
Samsun - - 0.0815 < 0.02 < 0.05
Samsun, Ordu, Trabzon, Rize d.w. 17.8 ± 1.8 1.4 ± 0.1 0.40 ± 0.04 0.23 ± 0.02 - [28]
Samsun, Sinop, Terme, Fatsa Ordu d.w. 23.71 ± 0.71 3.14 ± 0.31 0.92 ± 0.12 0.020 ± 0.002 - [29]
Amasra Trabzon-Turkey w.w. d.w. 16.03 ± 14.05 (3.48-40.72) 27.36 4.08 ± 2.79 (1.23-9.21) 1.12 1.11 ± 1.60 (0.09-7.00) 0.10 0.11 ± 0.13 (0.02-0.55) 0.02 0.11 [31] [32]
Sinop d.w. 6.95-18.43 4.93-7.74 0.09-0.31 0.02 - [53]
Black Sea (Istanbul and Kocaeli) d.w. 14.6 ± 1.3 1 ± 0.18 0.02 ± 0.01 0.02 ± 0.01 0.47 ± 0.02 [37]
Eastern Black Sea, Turkey Ordu-Samsun d.w. 19.7 1.36 0.020 0.018 - [38]
West Black Sea d.w. 36.4 ± 3.2 2.28 ± 0.03 - - - [39]
Sinop d.w. 17.15 ± 3.78 0.95 ± 0.41 0.82 ± 0.34 0.035 ± 0.018 - [40]
Trabzon-Turkey w.w. - - < LOD 3.38 ± 0.06 - [41]
Sinop d.w. 3.2 < 0.5 < 0.05 < 0.02 < 0.05 [42]
Sinop d.w. 10.64-19.53 2.79-5.45 0.11-0.45 0.03-0.19 - [54]
Samsun w.w. 4.95 ± 0.6 1.27 ± 0.19 1.76 ± 0.40 0.20 ± 0.11 - [44]
Sinop 9.49 ± 0.38 2.38 ± 0.12 2.94 ± 0.81 0.07 ± 0.02 -
Kocaeli 5.71 ± 0.88 1.4 ± 0.12 0.88 ± 0.12 0.06 ± 0.005 -
Kastamonu w.w. 6.14 ± 1.46 2.35 ± 0.38 7.21 ± 1.56 0.28 ± 0.03 - [45]
Giresun w.w. 6.02 ± 0.45 1.99 ± 0.18 0.45 ± 0.05 0.04 ± 0.00 - [46]
Trabzon 7.15 ± 0.64 1.74 ± 0.13 1.03 ± 0.10 0.12 ± 0.03 -
Rize 5 ± 0.31 1.81 ± 0.15 1.30 ± 0.16 0.09 ± 0.02 -
Southwestern Black Sea w.w. 20.80-34.94 1.36-11.85 0.03-1.70 0.02-0.05 0.01-0.03 [47]
Ordu d.w. 44.85 ± 7.11 83.13 ± 8.4 1.64 ± 0.37 3.95 ± 0.74 0.81 ± 0.04 1.54 ± 0.36 0.8 ± 0.02 0.91 ± 0.02 - [55]
Black Sea w.w. - - 0.165 0.016 0.032 [48]
Sinop w.w. 5.61-11.8 0.27-0.49 0.025-0.06 0.007-0.011 0.015-0.021 [49]
Romania w.w. - 3.486 ± 2.45 0.32 ± 0.25 0.026 ± 0.001 - [56]
Romania West Black Sea w.w. w.w. 0.035 ± 0.01 (0.021-0.072) 0.03 ± 0.02 [57] [52]
d.w.= dry wt.; w.w. = wet wt.
consumed whiting (M. merlangus L.) and red mullet (M. barbatus L.) caught near the southern coast of the Black Sea in 2017 and 2018. For all age groups, the EDI values for each heavy metal decreased in the following order: Zn > Cu > Pb > Hg > Cd. The mean values of Cd, Hg, Pb, Cu, and Zn in the edible tissues were 0.013, 0.024, 0.07, 0.195, and 9.05 mg/kg wet wt. for whiting and 0.017, 0.036, 0.05, 0.29, and 6.4 mg/kg wet wt. for red mullet, respectively. The differences might have been caused by the fact that the samples were caught
during different fishing seasons and in different areas of the Black Sea.
In all cases, HI values for each metal were < 1, suggesting no health risk. The concentrations also met the standards set up by regulatory bodies of Turkey and the European Union. The RI values for whiting and red mullet did not exceed the insignificant limit (10-6). In addition, these two commercial species caught near the Sinop coast showed no carcinogenic potential.
CONTRIBUTION
CONFLICT OF INTEREST
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors were equally involved in writing the manuscript and are equally responsible for plagiarism.
REFERENCES
1. Bat L, Oztekin A, §ahin F, Anci E, Ozsandikçi U. An overview of the Black Sea pollution in Turkey. Mediterranean Fisheries and Aquaculture Research. 2018;1(2):66-86.
2. Zhelyazkov G, Yankovska-Stefanova T, Mineva E, Stratev D, Vashin I, Dospatliev L, et al. Risk assessment of some heavy metals in mussels (Mytilus galloprovincialis) and veined rapa whelks (Rapana venosa) for human health. Marine Pollution Bulletin. 2018;128:197-201. DOI: https://doi.org/10.10167j.marpolbul.2018.01.024.
3. Plavan G, Jitar O, Teodosiu C, Nicoara M, Micu D, Strungaru SA. Toxic metals in tissues of fishes from the Black Sea and associated human health risk exposure. Environmental Science and Pollution Research. 2017;24(8):7776-7787. DOI: https://doi.org/10.1007/s11356-017-8442-6.
4. Omar S, Muhamad MS, Chuan LT, Hadibarata T, Teh ZC. A review on lead sources, occurrences, health effects, and treatment using hydroxyapatite (HAp) adsorbent made from fish waste. Water, Air, & Soil Pollution. 2019;230(12). DOI: https://doi.org/10.1007/s11270-019-4312-9.
5. Directives Directive 2008/56/Ec of The European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union. 2008;164:19-40.
6. Bernhard M. Manual of methods in the aquatic environment research. FAO fisheries technical paper FIRI/T № 158. Rome: Food and Agriculture Organisation; 1976. 124 p.
7. Determination of total Cd, Zn, Pb and Cu in selected marine organisms by flameless AAS. Reference methods for marine pollution studies. UNEP; 1984.
8. GESAMP: Cadmium, lead and tin the Marine Environment. UNEP Regional Seas Reports and Studies № 56. UNEP; 1985.
9. Sources and effects of ionizing radiation: United Nations Scientific Committee on the Effect of Atomic Radiation (UNSCEAR) Report to the General Assembly, with Scientific Annexes. New York: United Nations Pubns; 2010. 658 p.
10. Kaya G, Turkoglu S. Bioaccumulation of heavy metals in various tissues of some fish species and green tiger shrimp (Penaeus semisulcatus) from iskenderun Bay, Turkey, and risk assessment for human health. Biological Trace Element Research. 2017;180(2):314-326. DOI: https://doi.org/10.1007/s12011-017-0996-0.
11. 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. DOI: https://doi.org.10.21603/2308-4057-2019-2-329-338.
12. Miao X, Hao Y, Tang X, Xie Z, Liu L, Luo S, et al. 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. 2020;243. DOI: https:// doi.org/10.1016/j.chemosphere.2019.125337.
13. Risk assessment guidance for superfund. Human health evaluation manual (Part A). Washington: US Environmental Protection Agency; 1989. 291 p.
14. Guidance for assessing chemical contamination data for use in fish advisories. Volume 2. Risk assessment and fish consumption limits. Washington: US Environmental Protection Agency; 2000. 383 p.
15. The risk assessment information system [Internet]. [cited 2019 Nov 27]. Available from: https://rais.ornl.gov/index. html.
16. FishBase [Internet]. [cited 2019 Nov 27]. Available from: www.fishbase.org.
17. Jones J, Franklin A. Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities regulating the disposal of wastes at sea, 1993. Great Britain: Centre for Environment, Fisheries and Aquaculture Science; 1993. 92 p.
18. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union. 2006.
19. Communiqué on maximum limits of contaminants in foodstuffs. Official Gazette. 2008. (In Turkish).
20. Agricultural Ministry sets procedure for examining Russian. GAIN Report. 2010.
21. Uluozlu OD, Tuzen M, Mendil D, Soylak M. Trace metal content in nine species of fish from the Black and Aegean Seas, Turkey. Food Chemistry. 2007;104(2):835-840. DOI: https://doi.org/10.1016/j.foodchem.2007.01.003.
22. Turk Culha S, Bat L, Culha M, Efendioglu A, Andac MB, Bati B. Heavy metals levels in some fishes and molluscs from Sinop, Peninsula of the Southern Black Sea, Turkey. 38th CIESM congress proceedings. 2007. DOI: https://doi. org/10.13140/2.1.4328.6400.
23. Tepe Y, Turkmen M, Turkmen A. Assessment of heavy metals in two commercial fish species of four Turkish seas. Environmental Monitoring and Assessment. 2008;146(1-3):277-284. DOI: https://doi.org/10.1007/s10661-007-0079-3.
24. Turan C, Dural M, Oksuz A, Ozturk B. Levels of heavy metals in some commercial fish species captured from the Black Sea and Mediterranean coast of Turkey. Bulletin of Environmental Contamination and Toxicology. 2009;82(5):601-604. DOI: https://doi.org/10.1007/s00128-008-9624-1.
25. Tuzen M. Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. Food and Chemical Toxicology. 2009;47(8):1785-1790. DOI: https://doi.org/10.1016/jiet.2009.04.029.
26. Das YK, Aksoy A, Baskaya R, Duyar HA, Guvenc D, Boz V Heavy metal levels of some marine organisms collected in Samsun and Sinop coasts of Black Sea, in Turkey. Journal of Animal and Veterinary Advances. 2009;8(3):496-499.
27. Mendil D, Demirci Z, Tuzen M, Soylak M. Seasonal investigation of trace element contents in commercially valuable fish species from the Black sea, Turkey. Food and Chemical Toxicology. 2010;48(3):865-870. DOI: https://doi. org/10.1016/j.fct.2009.12.023.
28. Nisbet C, Terzi G, Pilgir O, Sarac N. Determination of heavy metal levels in fish samples collected from the middle Black Sea. Kafkas Universitesi Veteriner Fakultesi Dergisi. 2010;16(1):119-125.
29. Ozden O, Erkan N, Ulusoy S. Determination of mineral composition in three commercial fish species (Solea solea, Mullus surmuletus, and Merlangius merlangus). Environmental Monitoring and Assessment. 2010;170(1-4):353-363. DOI: https://doi.org/10.1007/s10661-009-1238-5.
30. Findik O, Cicek E. Metal concentrations in two bioindicator fish species, Merlangius merlangus, Mullus Barbatus, captured from the west Black Sea coasts (Bartin) of Turkey. Bulletin of Environmental Contamination and Toxicology. 2011;87(4):399-403. DOI: https://doi.org/10.1007/s00128-011-0373-1.
31. Aygun SF, Abanoz FG. Determination of heavy metal in anchovy (Engraulis encrasicolus L 1758) and whiting (Merlangius merlangus euxinus Nordman, 1840) fish in the middle Black Sea. Kafkas Universitesi Veteriner Fakultesi Dergisi. 2011;17:S145-S152.
32. Balkis N, Aksu A, Hissonmez H. Metal levels in biota from the Southern Black Sea, Turkey. Journal of the Black Sea/ Mediterranean Environment. 2012;18(2):134-143.
33. Alkan N, Aktas M, Gedik K. Comparison of metal accumulation in fish species from the Southeastern Black Sea. Bulletin of Environmental Contamination and Toxicology. 2012;88(6):807-812. DOI: https://doi.org/10.1007/ s00128-012-0631-x.
34. Gorur FK, Keser R, Akcay N, Dizman S. Radioactivity and heavy metal concentrations of some commercial fish species consumed in the Black Sea region of Turkey. Chemosphere. 2012;87(4):356-361. DOI: https://doi.org/10.1016/j. chemosphere.2011.12.022.
35. Bat L, Sezgin M, Baki OG, Ustun F, §ahin F. Determination of heavy metals in some commercial fish from the Black Sea coast of Turkey. Walailak Journal of Science and Technology. 2013;10(6):581-589.
36. Ergul HA, Aksan S. Evaluation of non-essential element and micronutrient concentrations in seafood from the Marmara and Black Seas. Journal of the Black Sea/Mediterranean Environment. 2013;19(3):312-331.
37. Alkan A, Alkan N, Akbas U. The factors affecting heavy metal levels in the muscle tissues of whiting (Merlangius merlangus) and red mullet (Mullus barbatus). Tarim Bilimleri Dergisi - Journal of Agricultural Sciences. 2016;22(3):349-359.
38. Kupeli T, Altundag H, Imamoglu M. Assessment of trace element levels in muscle tissues of fish species collected from a river, stream, lake, and sea in Sakarya, Turkey. Scientific World Journal. 2014. DOI: https://doi. org/10.1155/2014/496107.
39. Ergonul MB, Altindag A. Heavy metal concentrations in the muscle tissues of seven commercial fish species from Sinop coasts of the Black Sea. Rocznik Ochrona Srodowiska. 2014;16:34-51.
40. Aydin D, Tokalioglu S. Trace metals in tissues of the six most common fish species in the Black Sea, Turkey. Food Additives and Contaminants: Part B. 2015;8(1):25-31. DOI: https://doi.org/10.1080/19393210.2014.949873.
41. Bat L, Oztekin HC, Ustun F. Heavy metal levels in four commercial fishes caught in Sinop coasts of the Black Sea, Turkey. Turkish Journal of Fisheries and Aquatic Sciences. 2015;15:393-399. DOI: https://doi.org/10.4194/1303-2712-v15 2 25.
42. Bat L, Arisi E. Heavy metal levels in tissues of Merlangius merlangus (Linnaeus, 1758) from the Black Sea coast of Turkey and potential risks to human health. International Journal of Marine Science. 2016;6(10):1-8. DOI: https://doi. org/10.5376/ijms.2016.06.0010.
43. Turkmen M, Dura N. Assessment of heavy metal concentrations in fish from South Western black sea. Indian Journal of Geo - Marine Sciences. 2016;45(11):1552-1559.
44. Sonmez AY, Kadak AE, Ozdemir RC, Bilen S. Kastamonu kiyilarindan yakalanan bazi ekonomik balik turlerinde agir metal birikiminin tespiti [Some economic captures from Kastamonu coasts detection of heavy metal accumulation in its types]. Alinteri Journal of Agriculture Sciences. 2016;31(2):84-90. (In Turkish).
45. Turkmen M, Akaydin A. Metal levels in tissues of commercially important fish species from Southeastern Black Sea Coasts. Indian Journal of Geo - Marine Sciences. 2017;46(11):2357-2360.
46. Mol S, Karakulak FS, Ulusoy S. 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. Turkish Journal of Fisheries and Aquatic Sciences. 2017;17(6):1135-1143. DOI: https:doi.org/10.4194/1303-2712-v17_6_07.
47. Kuplulu O, Cil GI, Korkmaz SD, Aykut O, Ozansoy G. Determination of metal contamination in seafood from the Black, Marmara, Aegean and Mediterranean sea metal contamination in seafood. Journal of the Hellenic Veterinary Medical Society. 2018;69(1):749-758.
48. 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.
49. Elderwish M. A Bati Karadeniz Kiyilarinin Su, sediment ve bazi ekonomik balik turlerinin agir metal birikimlerinin mevsimsel olarak incelenmesi [Seasonal investigation of heavy metal accumulation of water, sediment and some economic fish species of West Black Sea coast]. Dr. eng. sci. diss. Kastamonu: Kastamonu Universitesi; 2019. 70 p.
50. Turan H, Altan CO, Kocatepe D. Black Sea whiting: assessment of potential health benefits/risks and differences based on mineral concentrations of meat and roes. Turkish Journal of Agriculture. 2019;7(12):2075-2082. DOI: https://doi. org/10.24925/turjaf.v7i12.2075-2082.2780.
51. Ulusoy S, Mol S, Karakulak FS, Kahraman AE. Selenium-mercury balance in commercial fish species from the Turkish waters. Biological Trace Element Research. 2019;191(1):207-213. DOI: https://doi.org/10.1007/s12011-018-1609-2.
52. Bat L, Sezgin M, Ustun F, Sahin F. Heavy metal concentrations in ten species of fishes caught in Sinop coastal waters of the Black Sea, Turkey. Turkish Journal of Fisheries and Aquatic Sciences. 2012;12:371-376. DOI: https://doi. org/10.4194/1303-2712-v12_2_24.
53. Gundogdu A, Culha ST, Kocbas F, Culha M. Heavy metal accummulation in muscles and total bodies of Mullus barbatus, Trachurus trachurus and Engraulis encrasicolus captured from the coast of Sinop, Black Sea. Pakistan Journal of Zoology. 2016;48(1):25-34.
54. Durmus M, Kosker AR, Ozogul Y, Aydin M, Ucar Y, Ayas D, et al. 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. Human and Ecological Risk Assessment. 2018;24(3):731-742. DOI: htps://doi.org/10.1080/10807039.2017.1398071.
55. Jitar O, Teodosiu C, Oros A, Plavan G, Nicoara M. Bioaccumulation of heavy metals in marine organisms from the Romanian sector of the Black Sea. New Biotechnology. 2015;32(3):369-378. DOI: https://doi.org/10.1016/j. nbt.2014.11.004.
56. Harmelin-Vivien M, Cossa D, Crochet S, Banaru D, Letourneur Y, Mellon-Duval C. Difference of mercury bioaccumulation in red mullets from the north-western Mediterranean and Black seas. Marine Pollution Bulletin. 2009;58(5):679-685. DOI: https://doi.org/10.1016/j.marpolbul.2009.01.004.
57. Bat L. One health: the interface between fish and human health. Current World Environment. 2019;14(3):355-357. DOI: https://doi.org/10.12944/CWE.143.04.
ORCID IDs
Levent Bat https://orcid.org/0000-0002-2289-6691 Ay§ah Oztekin https://orcid.org/0000-0002-3726-7134 Elif Arici https://orcid.org/0000-0001-6359-9194 Fatih §ahin https://orcid.org/0000-0003-0605-2672