Heavy Metal Levels in Tissues of Merlangius merlangus (Linnaeus, 1758) from the Black Sea Coast of Turkey and Potential Risks to Human Health  

Levent Bat , Elif Arıcı
University of Sinop Fisheries Faculty Department of Hydrobiology, Akliman 57000 Sinop, Turkey
Author    Correspondence author
International Journal of Marine Science, 2016, Vol. 6, No. 10   doi: 10.5376/ijms.2016.06.0010
Received: 20 Jan., 2016    Accepted: 24 Mar., 2016    Published: 24 Mar., 2016
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Bat L., and Arıcı E., 2016, 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, 6(10): 1-8 (doi: 10.5376/ijms.2016.06.0010)


In this study, heavy metal concentrations (Fe, Zn, Mn, Co, Cu, Cr, Pb, Cd, Ni, Al and Hg) were analysed in muscle, liver, eggs and gills of Merlangius merlangus caught from the Sinop coast of the Black Sea between September 2014 and February 2015. Al, Ni and Hg in all tissues were below the detection limits. Cd and Pb were not detected in the edible parts of M. merlangus. Gill and liver tissues showed higher metal concentrations than edible tissues including eggs. The highest concentrations were found in gills (Fe: 57±9 mg/kg wet wt., Mn: 2.4±0.2 mg/kg wet wt., Cr: 0.65±0.05 mg/kg wet wt. and Pb: 0.88±0.006 mg/kg wet wt.) and in liver (Zn: 43±6 mg/kg wet wt., Co: 0.88±0.03 mg/kg wet wt., Cu 0.41±0.02 mg/kg wet wt. and Cd: 0.075±0.006 mg/kg wet wt.). The lowest metal levels were determined in muscle tissues of whiting followed eggs. Thus the concentration of heavy metals in edible part of whiting did not exceed the permissible limits proposed by European Union and Turkish regulations, MAFF, EFSA. The average weekly intakes of heavy metals studied per body weight values not exceeded the Provisional Tolerable Weekly Intake (PTWI) established. Therefore, it may be concluded that these 11 heavy metals should not pose any health threat to the consumers resulting from the consumption of M. merlangus.

Heavy metals; Merlangius merlangus; Sinop coast; Black Sea; Provisional Tolerable Weekly Intake (PTWI); Estimated Daily Intake (EDI); Estimated Weekly Intake (EWI); Legal thresholds, Commission Regulation (EC)

1 Introduction

The harmful effects of heavy metals in fish on human health are of great interest in Marine Strategy Framework Directive (Official Journal of the European Union, 2008). Some of these metals are toxic to living organisms even at low concentrations when ingested over a long time period, whereas others are biologically essential and become toxic when their intake is excessive (Phillips and Rainbow, 1994). Heavy metals may enter the Black Sea from different natural and human activities, including industrial and domestic wastewater, shipping, harbour and touristic activities, inorganic fertilizers, storm runoff, leaching from landfills and geological weathering of the earth crust and atmospheric deposition (Bat, 2014; Bat and Özkan, 2015; Bat et al., 2015). When metals enter the marine ecosystem can be accumulated in biota through the effects of bioaccumulation via the food chain process and become toxic when accumulation reaches substantially high concentrations. Fish are generally at the top of the aquatic food chain and may concentrate high levels of some metals via skin, gills, oral consumption of water, food and non-food particles (Heath, 1991). Therefore it is highly important to determine and monitor heavy metal levels in fish because of their easily accumulation in such food compared and course harmful effect on human health by their consumptions. It is well known that fish is one of the most important seafood to be eaten for a healthy life because it has a high protein quality and unsaturated fatty acids.

M. merlangus is highly commercial fish and frequently consumed in Sinop of the Black Sea (Bat et al., 2013a). They are utilized fresh, dried or salted, smoked and frozen; eaten steamed, broiled and baked (Murua and Saborido-Rey, 2003). They feed on mainly shrimps, crabs, molluscs, small fish and polychaetes (Cohen et al., 1990). Quantity of caught whiting from the Turkish Black Sea waters is 9,555.1 metric tons in 2014 (TUIK, 2015).
This study has been conducted to determine Fe, Zn, Mn, Co, Cu, Cr, Pb, Cd, Ni, Al and Hg concentrations in the liver, gill, muscle and eggs of M. merlangus from the Sinop coast of the Turkish Black Sea. Liver and gills are chosen as target organs whereas muscles and eggs are chosen as edible tissues for assessing metal accumulation. 
2 Materials and Methods
Preparation fish samples and determination of heavy metals
The accumulation of heavy metals was studied in liver, gills, eggs and muscle of M. merlangus collected from Sinop coasts of the Black Sea. The samples were collected during September 2014 and February 2015 from the important fishing port in Sinop. Fish samples of uniform size were collected in order to avoid the possible mistake due to size differences. The location of the sampling areas is shown in Figure 1.

Figure 1 Location of sampling area


After capturing, fish specimens were transferred in an ice box immediately to the laboratory. Each specimen was dissected with corrosion-resistant stainless steel knife, removing liver, gills, eggs and muscle tissues according to a method of Bernhard (1976), UNEP (1984 and 1985). Each dissected organ was homogenized to form a composite sample and placed in a polyethylene bag then stored at −21ºC before digestion.


Metal analysis in tissues of whiting was performed using m-AOAC 999.10- ICP/MS (Inductively Coupled Plasma – Mass Spectrometer) method by accredited ÇEVRE Industrial Analysis Laboratory Services Trade Company (TÜRKAK Test TS EN ISO IEC 17025 AB-0364-T). EN 15763 European Standard methods was applied. The detection limits (µg/l) used for analysis of Fe, Zn, Mn, Co, Cu, Cr, Pb, Cd, Ni, Al and Hg were 0.5, 0.5, 0.5, 0.166, 0.5, 0.787, 0.05, 0.02, 0.15, 0.5 and 0.05, respectively.


Intake Levels Calculation
The average heavy metal weekly intake was calculated according to the following formula:
Heavy metals intake level = average heavy metal content X consumption of fish per person/ body weight
The annual quantity of fish consumed is 6.3 kg / person in 2013 (TUIK, 2014), which is equivalent to 17.3 g/day
for Turkey. This is equivalent to 121.1 g/week. The body weight of adult person is 70 kg.
Statistical analysis
Results were allowed to relate the heavy metal levels with the tissue type, examined to determinate descriptive parameters such as mean and standard deviation and compared using variance analysis (ANOVA) and a comparison of means test, setting a significance level of 0.05 (Zar, 1984). Comparisons were performed using the statistical software IBM SPSS Statistics version 21.

Figure 2 2A-H. Mean levels and standard deviation of Fe, Zn, Cu, Cd, Pb, Cr, Mn and Co found in different tissues of M. merlangus individuals collected from the southern of the Black Sea. Values with different letters represent significant differences (p<0.05) between the mean values of the levels of each heavy metal in each of the tissues.


3 Results and Discussion
The result obtained for the determination of the concentration of heavy metals in liver, gills, eggs and muscle tissues from Sinop coasts of the Black Sea were given in Figures 2A-H. There are high levels of Zn and Fe at a significant level (P<0.05) in M. merlangus when compared with other metals, followed by the Mn, Co and Cu. However, there is no significant variation (P>0.05) observed among the heavy metal levels in the muscles and eggs.
Al, Ni and Hg in all tissues were below the detection limits. Cd and Pb were not detected in the edible parts of M. merlangus. Gill and liver tissues showed higher metal concentrations than edible tissues including eggs. The highest concentrations were found in gills (Fe: 57±9 mg/kg wet wt., Mn: 2.4±0.2 mg/kg wet wt., Cr: 0.65±0.05 mg/kg wet wt. and Pb: 0.88±0.006 mg/kg wet wt.) and in liver (Zn: 43±6 mg/kg wet wt., Co: 0.88±0.03 mg/kg wet wt., Cu 0.41±0.02 mg/kg wet wt. and Cd: 0.075±0.006 mg/kg wet wt.). The lowest metal levels were determined in muscle tissues of whiting followed eggs.
The result shows that Zn has the highest concentration in liver than those in other tissues. However the highest concentration of Fe was in the gills than the other tissues, an indication of its availability in the environment. Cu has the least of the heavy metals in edible tissues of M. merlangus analyzed.
The lowest concentration (0.05±0.003 mg/kg wet wt.) of Mn was observed in the muscles, while the highest concentration of 0.52±0.05 mg Mn/kg wet wt. Mn was detected in gill. Mn is an essential and deficiencies of the result in severe skeletal and reproductive abnormalities in mammals (Akan et al., 2012). Cr is also an essential and the biologically usable form plays vital role in glucose metabolism (Akan et al., 2012). In this study the lowest concentration (0.06±0.003 mg/kg wet wt.) of Cr was observed in the muscles, while the highest concentration of 0.65±0.1 mg Cr/kg wet wt.
Noreña et al. (2012) indicated that Ni accumulation in fish is not common in research related to environmental pollution because of its low uptake and rapid elimination. In this study Ni levels in all tissues of M. merlangus were below detection limit.
Non-essential metals such as Hg, Pb and Cd, among others, have taken great importance, because their toxic properties through different levels along the food chain. Fish is the main source of metals like Hg in human diet (Hosseini et al., 2015).
Zeri et al. (2000) show that the Black Sea is rich in Cd, Co, Cu and Ni, as compared to other regional seas. However, a comparison of mean concentrations of heavy metals in tissues of some fish species from the Romanian and Bulgarian coasts of the Black Sea demonstrates that the metal levels in fish tissues are variable and reflect the level of contamination in the sampling areas (Jitar et al., 2013). Ni levels were slightly higher in anchovies, bluefish and sprat (Oros et al., 2010).
Large differences in heavy metal concentrations were observed between different tissues. Cd and Pb levels in eggs and muscle tissues were below detection limits. Regarding these metals significant differences (p<0.05) are distinguished in the accumulated levels in gills and liver of fish samples. Cd levels in liver (0.74±0.2 mg/kg wet wt.) were higher than those in gills (0.48±0.1 mg/kg wet wt.) suggesting that liver as the major reservoir of this metal in the fish organ. Noreña et al., (2012) agreed that Cd binds to metallothionein in cells which is more toxic to renal tubules than the Cd itself whereas Pb levels (0.61±0.15 mg/kg wet wt.) in gills were higher than those in liver (0.28±0.03 mg/kg wet wt.) in this study. Similar results were found by Akan et al., (2012). It is highlighted that the gills are a major organ of accumulation of heavy metals, since they are in direct contact with the water and therefore are the first barrier of defense (Noreña et al., 2012). The fish gills tend to accumulate critical concentrations of heavy metal than other tissues (Akan et al., 2012). In general it is approved that if the main entry route of the xenobiotic is via the water, the high concentrations would be in gills, yet the intake is mainly for food contaminated with metals, the accumulation would take place in the digestive system tract tissues or organs (Noreña et al., 2012). The liver plays vital role in accumulation and detoxification of heavy metals and the liver tissue is next in terms of metals tissue accumulation after gills (Akan et al., 2012).
In many studies (Noreña et al., 2012; Akan et al., 2012; Hosseini et al., 2015) gills and liver are also chosen as target organs for assessing metal accumulation. Abdolahpur Monikh et al., (2013) indicated that the metal concentrations in gills reflect the concentrations of metals in waters where the fish species live, whereas the liver is the main tissues of accumulation, biotransformation and excretion of metals in fish. Recently, Bat (2014) pointed out that in previous studies on metal levels in fish from the Black Sea coasts show that bioaccumulation of metals was more in the liver than those in other tissues.
Benthic fishes are nearby sediment and receive more sediment-associated metals than pelagic fishes (Abdolahpur Monikh et al., 2013; Hosseini et al., 2015). M. merlangus is benthopelagic fish and occurs on sand, mud and gravel sea beds at depths down to about 100 m (Fishbase, 2016).  Bat et al. (2015) demonstrated the distribution of heavy metals in sediments of Sinop coast in the Black Sea shows a variable pattern. Although high metal levels were found in some regions of the Black Sea coast, the level of most often of the heavy metals were not extremely enriched in these surface sediments of Sinop coast and did not present a serious threat to the local fauna and flora (Bat et al., 2015). Moreover pelagic fish are very high metabolic rates, and consequently high food intake rates, a property that accentuates the exposure to heavy metals (Kojadinovic et al., 2007). Topping (1973) suggested that mainly plankton feeding fish contain much higher concentrations of some heavy metals than bottom feeding fish. Abdolahpur Monikh et al., (2013) were surprised that Euryglossa orientalis, which are flatfish, bottom feeders and are associated with sediment species, did not show the highest metals concentrations. Accumulations of heavy metals were generally found to be species specific and may be related to their feeding habits and the bioconcentration capacity of each species (Bustamante et al., 2003; Bat et al., 2013b; Abdolahpur Monikh et al., 2013; Bat, 2014). Bat et al. (2013b) found that whiting feed on anchovy as well. In the present study it may be suggested that metals might have been taken up from prey in the pelagic zone and on sea bed and upper layer of the water. Abdolahpur Monikh et al. (2013) found no significant correlation between metal concentrations in sediment and fish tissues and argued that demersal species, Johnius belangerii and Euryglossa orientalis were not suitable biomonitors for heavy metal contamination in the Persian Gulf.
M. merlangus is of great commercial importance because they are more consumed fish in Turkey and one of the most dominates species in the Black Sea. However, the eggs of M. merlangus are the parts of fish that are consumed by human; it has not been studied in previous works in this region. The present study indicated that Cu, Mn and Co concentrations were higher (p<0.05) in eggs samples than in the muscle samples, whereas the others were no significant differences (p>0.05). Fish eggs of M. merlangius are hardly consumed by people, this tissue is very important for transferring contamination to the next fish generations, resulting in diseases (Terra et al., 2007). The results of this study are also in agreement with the many studies which have indicated that gonads have a higher tendency to accumulate heavy metals than those in muscles. Yilmaz (2003) found that gonads showed higher metal concentrations than muscle for Mugil cephalus and Trachurus meditterraneus from Iskenderun Bay, Turkey. Similarly Wong et al. (2001) found the highest metal concentrations in liver and gonads compared with edible muscle tissues tended to accumulate less heavy metal. Terra et al. (2007) also found the highest Zn values in gonads for three fish species, suggested that it might be also associated to reproductive processes. Jezierska et al. (2009) pointed out that waterborne metals might be accumulated in the gonads and adversely affected gamete production and viability. The egg shell does not provide full protection the embryo against heavy metal influence, especially during the swelling phase so; metals may accumulate in the egg (Jezierska et al., 2009).
With regard to health risk, the tolerable weekly intakes were estimated by means of references for edible tissues of fishes consumed by people. The annual quantity of fish consumed is 6.3 kg/person in 2013 (TUIK, 2014), which is equivalent to 17.3 g/day for Turkey. The EWI (Estimated Weekly Intake) and EDI (Estimated Daily Intake) values presented in Table 1 were estimated by assuming that a 70-kg person will consume 17.3 g fish/day which is equal to 121.1 g fish/week. The tolerable weekly intake of heavy metals as PTWI (Provisional Tolerable Weekly Intake), are set by the Food and Agriculture Organization/World Health Organization (FAO/WHO) Joint Expert Committee on Food Additives (JECFA). PTWI is the maximum amount of a contaminant to which a person can be exposed per week over a lifetime without an unacceptable risk of health effects (National Academy of Sciences, 1989; WHO, 1996; Council of Europe, 2001; FAO/WHO, 2010; EFSA 2010, 2012a,b). EWI values of metals for an adult (mg/70 kg body weight) consuming 121.1 g fish/week were estimated using the mean ±SD metal levels in Figures 2A-H for M. merlangus. Intake estimates were expressed as per unit body weight (mg/kg body wt. /weekly and daily). EDI values were calculated from EWI values (Türkmen et al., 2008; 2009).

Table 1 Estimated Weekly Intakes (EWI) and Estimated Daily Intakes (EDI) of heavy metals in edible tissues of whiting from Sinop Coastal waters of the Black Sea, Turkey.


It can be seen from Table 1 that the estimated EWIs and EDIs of heavy metals in this study are far below the recommended PTWIs and/or PTDIs and indicated no adverse effects to the consumers.


4 Conclusions
The highest levels of all the heavy metals in this study were measured in gills and liver, while muscle and eggs show the lowest levels. The reason for high metal concentrations in the gills and liver it is suggested that they should be removed completely and washed well before cook.  In view of the results it was indicated that Fe, Zn, Mn, Co, Cu, Cr, Pb, Cd, Ni, Al and Hg levels in the edible tissues of whiting (M. merlangus) from Sinop coasts of the southern Black Sea during September 2014 and February 2015 were considerably lower than the maximum levels set by the national (Turkish Food Codex, 2002) and international (MAFF, 1995; Cunocil of Europe, 2001; Commission Regulation, 2006 and 2015) standards. Therefore it could be concluded that there is no risk in consumption of M. merlangus collected from Sinop coast of the Black Sea. Further research is therefore suggested to determine the concentration of heavy metal from other regions of the Black Sea.
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