Abstract
Muscle tissues of squid (Loligo vulgaris), cuttlefish (Sepia officinalis) and prawn (Penaeus semisulcatus) marketed for consumption were analyzed for their Fe, Cu, Zn, Cd and Pb levels. Metal analysis were carried out using Inductively Coupled Plasma-Mass Spectroscopic (ICP-MS) methods. Muscle levels of Fe, Cu, Zn and Pb ranged between 0.50–19.82, 0.53–8.57, 6.80–32.12 and <0.003–1.60 mg/kg w.w., respectively whereas Cd level was below detection limits in the species studied. Mean muscle levels of metals in samples for consumption were compared with provisional tolerable daily (PTDs) and weekly (PTWs) limits. It was shown that the levels of metals in tissues analyzed were below PTDs and PTWs. Mean metal levels of all samples were also below the upper limits set by Turkish Food Codex (TFC) and European Union (EU) Commission. Hence it was shown that levels of the selected 5 metals in muscle tissues of squid, cuttlefish and prawns marketed in Mersin were in accordance with the quality standards set by TFC and EUC and concluded that they do not pose any health problems for human consumption.
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Introduction
Various human activities in the environment release toxic substances which eventually end up in water columns, sediments and indeed in living organisms of the oceans where they make marine pollution as a global problem (Maanan 2008). The level of pollution increased drastically due to ever increasing human population, agricultural and industrial developments, increasing diversity in raw materials and changing climate which began to threat environment and human health (Bailey et al. 1999). Heavy metals are one of the first ranked chemicals that cause pollution in aquatic environments (Bettini et al. 2006). As their concentrations reaches above certain levels heavy metals tend to accumulate in tissues of aquatic organisms and cause metabolic, physiologic and pathologic changes effecting reproduction and development of organisms (Levesque et al. 2002). These metals also can be transferred to upper levels of food web through ingestion.
Edible aquatic organisms are considered as an important protein source and consumed in increasing amounts for their trace element contents (Burger and Gochfeld 2005). Mollusks and crustaceans are considered as bioindicator and biomonitoring organisms (Lau et al. 1998; Jimoh et al. 2011) because they are widely distributed in aquatic environments, can be sampled easily and can tolerate high levels of heavy metal accumulation (Lau et al. 1996).
In addition to its quantity, it is rather important to keep quality of food in certain limits hence increasing numbers of studies are carried out on level of toxic substances in edible organisms (Korkmaz et al. 2017).
Present study was undertaken to determine the levels of Fe, Cu, Zn, Cd and Pb in muscle tissues of L.vulgaris, S. officinalis and P. semisulcatus marketed in Mersin. Samples were obtained from different marketing points and the metal levels were measured in their muscle tissues. Results were compared with different food codex after statistical analysis to determine whether they are in acceptable limits for consumption.
Material and Methods
Research Material and Sampling
Research material L. vulgaris, S. officinalis and P. semisulcatus were obtained from 3 large fish point of sale including Mersin fish market in 2016 by random sampling method. Eight samples were collected from each species at each point of sale totaling to 72 specimens. Samples were brought to laboratory in cold chain and 0.5 g muscle tissue was dissected from each and the tissues were kept at -4 °C until analysis. The length and weight of experimental materials used are given in Table 1.
Metal Analysis
Muscle samples were transferred to petri dishes and oven dried at 150 °C for 72 h and brought to a constant weight. After determining their dry weights, they were transferred to experimental tubes and 2 ml nitric acid (HNO3, % 65, S.G.: 1.40, Merck) and 1 ml perchloric acid (HClO4, % 60, S.G.: 1.53, Merck) was added on to each sample and they were wet burned at 120 °C for 8 h. They were then transferred to polyethylene tubes and their volumes were made up to 10 ml with deionized water (Muramoto 1983). Samples were passed through a 0.45 μm membrane filter before analysis. Metal levels in tissues were determined using an ICP-MS (Agilent 7500ce, Octopole Reaction System, Agilent Technologies, Japan) on three replicates. Operating conditions of the ICP-MS are given in Table 2.
Metal content of the tissues were calculated on dry weight basis (mg kg−1 d.w.) and converted to wet weight (mg kg−1 w.w.) taking the water content of each tissue into account (El-Moselhy et al. 2014). Samples with known metal contents were prepared for regaining purposes and regaining percentages for Fe, Cu, Zn, Cd and Pb were found as 96.29%, 93.63%, 93.06%, 97.20 and 96.59% respectively. Validation parameters of the analytical method are given in Table 3.
Calculation of Weekly Intakes of the Metals Analyzed (EWI)
The following formula was used to calculate the amount of metal intake by consuming fish tissues;
C (Concentration); metal content of fish tissue (mg kg−1 w.w.).
FIR (Feeding rate); According to FAO (2005), fish consumption per capita per day is 20 g/person/day. Hence weekly consumption can be calculated by multiplying with seven.
Data obtained from the tissues were analyzed statistically a series of variance analysis (ANOVA) and Student-Newman Keul’s tests (SNK) using SPSS 16.0 software package.
Results and Discussion
Heavy metal levels in muscle tissues of L.vulgaris, S. officinalis and P. semisulcatus samples are given in Table 4. Metal levels in muscle samples ranged between the following values; Fe: 0.50–19.82; Cu:0.53–8.57; Zn: 6.80–32.12; Cd: < 0.0004; Pb: < 0.0003–1.60 mg/kg.w.w.
According to the result of muscle analysis, two specimens belonging to L.vulgaris and P. semisulcatus and three specimens belonging to S. officinalis had higher levels of Pb than the accepted by TFC. Cd levels were below detection limits of the ICP-MS at all the samples analyzed.
Iron
World Health Organization (WHO) reported that provisional tolerable weekly intake limit (PTWI) for iron is about 5600 μg/kg/week and intake above this value cause health problems in humans (FAO/WHO 2004). Higher levels of iron intake were also reported to cause heart attack, cancer, fibrosis in liver, Parkinson and Alzheimer diseases (Killilea et al. 2003).
Iron levels in muscle tissues of L.vulgaris, P. semisulcatus ve S. officinalis ranged between 0.50–19.82, 1.28–15.11, 1.42–19.47 mg kg−1 w.w. respectively. Highest level of Fe was measured in muscle of L. vulgaris and lowest in P. semisulcatus. Mean levels of Fe in squid, cuttlefish and prawn species in France were reported as 4.57, 1.27 and 15.80 mg kg−1 w.w. (Guérin et al. 2011) and mean Fe levels in squid and prawn species marketed in Greece were reported as 6.00 and 56.00 mg kg−1 w.w. respectively (Kalogeropoulos et al. 2012). Mean levels of Fe in muscle tissues of Penaeus japonicus caught from different stations in Mediterranean were shown to be between 52.30–113.40 mg kg−1 d.w. (Canlı et al. 2001) whereas mean Fe in muscle of P. semisulcatus differed between 8.70–16.90 mg kg−1 d.w. (Çoğun et al. 2005).
Mean levels of Fe in fish species from Mediterranean were reported to change between 29.70–56.70 mg kg−1 d.w. (Çoğun et al. 2006), 32.20–129.00 mg kg−1 d.w. (Kalay et al. 1999) and 0.21–3.59 mg kg−1 w.w. (Ersoy and Çelik 2010). Mean levels of iron in muscle tissue of mollusk and crustacean species determined in the present study were lower when compared with fish species marketed in Mersin (Turkey), which contained 10.03–13.52 mg Fe kg−1 w.w. (Korkmaz et al. 2017). Higher Fe levels in muscle tissues of fish compared with invertebrates could be related with the presence of iron in fish blood as a structural part of hemoglobin for transporting oxygen.
Copper
It was reported that the PTWI value of copper is 3500 μg/kg/week (FAO/WHO 2004) above which result in liver and kidney damages in humans (Ikem and Egiebor 2005; Türkmen et al. 2009).
Copper levels in muscle tissues of L.vulgaris, S. officinalis and P. semisulcatus ranged between 0.5–3.73, 0.59–8.57, 1.09–7.43 mg kg−1 w.w. respectively. The highest level of copper was determined in muscle tissue of S. officinalis and the lowest in L.vulgaris. Squid, cuttlefish and prawn species marketed in France was reported to have mean copper levels of 2.56, 2.57 and 9.22 mg kg−1 w.w. (Guérin et al. 2011). Kalogeropoulos et al. (2012) reported that squid and prawn marketed in Greece had mean 4.7 and 9.5 mg Cu kg-1 w.w in their edible tissues. Mean copper levels ranged between 15.71–18.88 mg kg−1 d.w. in P. japonicus (Canlı et al. 2001) and between 27.9–41.9 mg kg−1 d.w. in P. semisulcatus (Çoğun et al. 2005) obtained from different stations in Mediterranean.
Mean levels of copper determined in marketed fish species were determined as 8.30–17.50 mg kg−1 d.w. (Çoğun et al. 2006), 0.77–9.20 mg kg−1 d.w. (Karayakar et al. 2017), 2.26–6.15 mg kg−1 d.w. (Kalay et al. 1999), 1.06–3.41 mg kg−1 d.w. (Karayakar et al. 2010) and 1.06–2.09 mg kg−1 w.w. (Ersoy and Çelik 2010).
Korkmaz et al. (2017) reported that mean Cu levels in fish species marketed in Mersin (Turkey) ranged between 0.35–0.72 mg kg-1 w.w. which seems to be lower than the Cu levels measured in muscle tissue of the mollusk and crustacean species studied in the present study. Mollusks and crustaceans store copper in their tissues, a structural part in synthesizing blood pigment hemocyanin for gas exchange which may be associated with high levels of copper found in muscle tissues of invertebrates in this study.
Zinc
Oral reference concentration (RfC) of Zn was given as 2100 μg/kg/week (EPA 2005) and reproductive and developmental disorders result in Zn intake over this level (Ikem and Egiebor 2005; Türkmen et al. 2009).
Zn levels in muscle tissues of L.vulgaris, S. officinalis and P. semisulcatus marketed in Mersin ranged between 9.14–32.12, 8.18–22.76 and 6.80–25.05 mg kg−1 w.w. Highest levels of Zn was detected in muscle tissue of L.vulgaris, and the lowest in P. semisulcatus. It was reported that squid, cuttlefish and prawn marketed in France had mean Zn levels of 6.69, 15.1 and 13.4 mg kg−1 w.w. (Guérin et al. 2011) and the mean Zn levels in squid and prawn marketed in Greece was gives as 9.7 and 12 mg/kg−1 w.w. (Kalogeropoulos et al. 2012). P.japonicus and P.semiculcatus caught from different stations in Mediterranean had Zn levels ranging between 18.00–24.70 mg kg-1 d.w. (Canlı et al. 2001) and 50.10–63.10 mg kg-1 d.w. (Çoğun et al. 2005).
Fish species marketed in Saudi Arabia had mean Zn levels differing between 4.22–6.99 mg kg−1 w.w. in their muscle tissues (Al-Bader 2008). Various fish species caught from Mediterranean Sea had mean zinc levels ranging between 21.50–34.50 mg kg−1 d.w. (Çoğun et al. 2006), 24.32–67.65 mg kg−1 d.w. (Karayakar et al. 2017), 16.10–33.60 mg kg−1 d.w. (Kalay et al. 1999), 2.36–15.78 mg kg−1 d.w. (Karayakar et al. 2010) and 1.76–5.19 mg kg−1 w.w. (Ersoy and Çelik 2010).
In a recent study mean Zn levels were reported to vary between 11.75–23.58 mg kg−1 w.w. in fish marketed in Mersin (Korkmaz et al. 2017) being about the same levels found in the muscle tissues of invertebrates studied in the present study.
Cadmium
Cadmium is known to have no biological function in living organisms and is toxic even at trace amounts. Its oral RfC is given as 1 μg/kg/day by US EPA and stated that intakes over this dose can result in kidney, liver, skeleton and reproductive system disorders (EPA 2000). The main intake route for Cd intake is food for non-smokers.
The levels of Cd in muscle tissues of L.vulgaris, S. officinalis ve P. semisulcatus were below the detection limit of ICP-MS. Kalogeropoulos et al. (2012) reported mean Cd levels in squid and prawn species as 0.23 and 0.14 mg kg−1 w.w respectively. Mean Cd levels in cephalopods including squid and cuttlefish marketed in Italy reported as 0.006 mg kg−1 w.w. (Cirillo et al. 2010), whereas Miedico et al. (2015) stated that mean Cd levels ranged between 0.004–8.470 mg kg−1 w.w. for his group of organisms in Italian markets. Mean levels of Cd in tissues of prawn and squid species markets in Spain were reported as 0.23 and 0.34 mg kg−1 w.w. (Yusa et al. 2008). Al-Bader stated that mean Cd levels in muscle tissues of fish species marketed in Saudi Arabia ranged between 0.002–0.008 mg/kg-1 w.w. Cadmium in tissues of prawn species caught from different stations of Mediterranean were recorded as 0.64–0.91 mg kg−1 d.w. for P. japonicus (Canlı et al. 2001) and 2.70–5.00 mg kg−1 d.w. for P. semisulcatus (Çoğun et al. 2005).
Mean levels of Cd in Mediterranean fish species were reported to change between 1.10–3.10 mg kg−1 d.w., (Çoğun et al. 2006), 0.61–1.43 mg kg−1 d.w. (Kalay et al. 1999), 0.20–0.73 mg kg−1 d.w. (Karayakar et al. 2010) and 0.03–0.20 mg kg−1 w.w. (Ersoy and Çelik 2010) whereas Karayakar et al. (2017) claimed that Cd was below detection limits in muscle tissues of fish caught from Mersin Bay.
As mentioned in a previous study (Korkmaz et al. 2017), Cd levels in muscle tissues of fish marketed in Mersin were below detection limits, the same was true for the invertebrate animals studied in the present study.
Lead
PTWI value of lead, which is another toxic element which has no biological function, is 25 μg/kg/week and intakes above this level cause memory loss, mental retardation, instable neurotransmission, cardiovascular complications, liver and kidney damages (Ikem and Egiebor 2005).
Lead levels in muscle tissues of L.vulgaris, S. officinalis ve P. semisulcatus were calculated as ranging between <0.003–1.25, <0.003–1.60, <0.003–0.84 mg kg−1 w.w. respectively. The highest Pb level was measured in L.vulgaris and lowest in P. semisulcatus. Squid, cuttlefish and prawn species marketed in France was reported to have 0.008, 0.01 and 0.01 mg kg−1 w.w. mean Pb levels in their muscle tissues (Guérin et al. 2011). Cirillo et al. (2010) and Miedico et al. (2015) reported mean Pb levels in muscle tissues of cephalopods squid and cuttlefish, as 0.22 mg kg−1 w.w. and 0.01–0.92 mg kg−1 w.w. respectively. Pb level was 0.0001 mg kg-1 w.w. in prawn species and undetectable in squid sold in Greek markets (Kalogeropoulos et al. 2012). Two species of prawn caught from different stations in Mediterranean had mean Pb levels ranging between 3.70–5.40 mg kg−1 d.w. in P. japonicus (Canlı et al. 2001) and between 15.40–28.60 mg kg−1 d.w. in P. semisulcatus (Çoğun et al. 2005).
Al-Bader (2008), reported that fish species marketed in Saudi Arabia had mean Pb levels of 0.02–0.03 mg kg−1 d.w. in their muscle tissues. Mean Pb levels of fish species from Mediterranean were reported as between 5.80–9.40 mg kg−1 d.w. (Çoğun et al. 2006), 4.43–9.11 mg kg−1 d.w. (Kalay et al. 1999) and 0.12–0.58 mg kg−1 w.w. (Ersoy and Çelik 2010). Karayakar et al. (2017), however, stated that the level of Pb was below detection limits in fish caught from Mersin Bay.
Some fish species marketed in Mersin was shown to have mean Pb levels ranging between 0.16–0.91 mg kg- w.w. (Korkmaz et al. 2017). Hence the mean levels of lead determined in the muscle of mollusk and crustacean species in the present study is similar to those measured in fish species.
Risk Evaluation of Human Health in Regard to Fish Consumption in Mersin
A number of organizations brought restrictions to some heavy metals that can be present in food stuff and set maximum acceptable limits for these metals. Present results were evaluated in the light of upper limits recommended and are given in Table 5.
Mean levels of metals detected in muscle tissues of L.vulgaris, S. officinalis ve P. semisulcatus were below the accessible upper limits given by TFC and by EU. However, the levels in 8.33% of L.vulgaris and P. semisulcatus samples and 12.5% of S. officinalis samples were not in accordance with the recommended values.
Mean levels detected in the present study were compared with the tolerable upper limits and risk evaluation by fish consumption was made for Mersin and the results are given in Table 6.
Amount of tolerable daily intake is the amount of material that can be consumed without taking any risk throughout the life of an organism and expressed by taking the body weight as a base value. Amount of tolerable daily intake depends on the amount of metal concentration in food and on the amount of food consumed. According to FAO values the daily mean consumption of fish is 20 g per capita which is equal to 140 g weekly intake. Considering a person of 70 kg in weight who consumes 20 g daily and 140 g weekly fish meat, the amount of mean metal level that can be taken into body was calculated and the data obtained were compared with the PTDI and PTWI values (Table 6). The amount of metal in muscle of the species studied were found to be considerably below the PTDI and PTWI and concluded that consumption of fish species studied would not pose any risk as far as human health is concerned.
Conclusion
L.vulgaris, S. officinalis ve P. semisulcatus are economically important and frequently consumed species in Turkey. The results revealed that the mean heavy metal levels in muscle tissues of the species studied do not pose any threat as far as human health is concerned. It was also shown that 8.33% of L.vulgaris and P. semisulcatus and 12.5% of S. officinalis were not in accordance with TFC and EU standards. It was concluded that heavy metal analysis should be carried out as frequent as possible in edible parts of aquatic organisms for a healthy natural environment and for human health purposes.
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Korkmaz, C., Ay, Ö., Çolakfakıoğlu, C. et al. Heavy Metal Levels in some Edible Crustacean and Mollusk Species Marketed in Mersin. Thalassas 35, 65–71 (2019). https://doi.org/10.1007/s41208-018-0086-x
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DOI: https://doi.org/10.1007/s41208-018-0086-x