Introduction

Nearly 40% of the world’s human population (2.4 billion) lives within 0–100 km of the coastal zones (UN 2017). Resources in these coastal zones are essential for trade, transportation, recreation, and, most importantly, nutrition for the people who are living in the coastal zones (Neumann et al. 2015). The decreased food production over the global climate shifts caused by unpreventable abiotic factors (drought, flood, etc.) has switched people’s interest in the consumption of aquaculture resources (FAO 2018). Accordingly, in Turkey as well, since the sea surrounds it on three sides, the country’s coastal resources are important platforms for people, providing benefits as nutrition, transportation, tourism, and recreation (PAP/RAC 2005). Coastal counties are also the areas in which a significant portion of the production and consumption of fishery products are taking place in Turkey. People mainly living in these counties benefit more from these resources and prefer fishery products more than people living far from the coastline (Cisneros-Montemayor et al. 2016). Considering the pressure of the anthropogenic pollutants in the coastal waters as a result of the coastal population in Turkey, which is around 45 million, we see those trace elements (TE) are one of the most hazardous groups of these pollutants here (Gedik 2018). The pollutants are becoming more prone to be accumulated in the coastal zones (Sundaray et al. 2011) in parallel with the population expansion (Gedik and Eryaşar 2020).

Fishery products (fish, mussels, etc.) are considered an integral part of an irreplaceable and well-balanced diet that provides a healthy energy source since they bear great nutritional value owing to high-quality proteins, lipids, minerals, and vitamins (Pieniak et al. 2010). Likewise, seafood is a food group that is recommended to be consumed at least twice a week as a critical target for promoting healthy nutrition (Tacon and Metian 2013). In the context of better nutrient intake goals, seafood consumption is also increasing to outrun bad-diet-associated health problems proportional to the improvement of living standards of the population (CIHEAM/FAO 2015). Nevertheless, seafood could overshadow all these positive aspects, being a significant source of various contaminants such as TE that can pose critical risks to consumer health (US EPA 2000; EFSA 2012). Up to now, several studies have already assessed that seafood consumption is the most crucial source of TE exposure for consumers (Traina et al. 2019; Wang et al. 2020; Liu et al. 2019). Accordingly, today, the consumption of aquatic products is indeed considered to be the primary exposure route that consumers are exposed to severe TE (US EPA 2000; EFSA 2012).

TE contaminants attributed to their non-biodegradable nature (Matta et al. 1999), not only accumulate in the aquatic organisms but also reach human beings through the food chain due to their cumulative amounts (biomagnification) and might threaten human health (Wang et al. 2020; Guendouzi et al. 2020; Yuan et al. 2020). It is well-known that bivalves accumulate TE more than any other aquatic organisms (Yuan et al. 2020). Particularly mussels, since they feed by filtering water, are adapted to accumulate large amounts of TE dissolved in the surrounding water column in their tissues. Therefore, mussels reasonably indicate the levels of TE found in the surrounding water column. Concordantly, the mussels sampled from the polluted coastal areas were reported to be accumulating more TE than mussels sampled from the unpolluted areas (Guendouzi et al. 2020; Yuan et al. 2020; Bajt et al. 2019). Hence, due to the possible interventions and impacts, guidelines setting the target TE limits regarding the protection of public health have been developed by various governmental agencies and health organizations (JECFA 1982, 2011a, b; EC 2006).

TE which might be toxic to organisms (Zhou et al. 2008) is caused by the trace elements as Cr, Pb, Cd, and As even at lower doses in the aquatic environment. However, burgeoning studies have already revealed the associated consequential carcinogenic effects of particularly As and Pb on the general public health and development in both children and adult populations under chronic exposure (US EPA 2000). Since the TE-contaminated seafood could trigger severe risks for human health, it is vital to continuously monitor the TE for frequent consumption conditions (Wang et al. 2020; Yuan et al. 2020; Guendouzi et al. 2020). Therefore, marine species especially sessile ones (e.g., mussels) consumed as seafood are also good candidates to be representatives of the environmental pollution studies as bioindicator species (Zhou et al. 2008; Baltas et al. 2017; Terzi and Isler 2019; Terzi and Civelek 2021). Therefore, several monitoring research has been performed on the Turkish coastal waters regarding TE (Baltas et al. 2017; Unsal 2001; Topcuoǧlu et al. 2002; Sunlu 2006; Cevik et al. 2008; Culha et al. 2011; Mol and Alakavuk 2011; Kucuksezgin et al. 2013; Balkis et al. 2013; Tepe et al. 2016; Belivermis et al. 2016) yet both due to the limited number of TE examined and the lack of extended sampling areas, the impact of these was bounded by local studies only. Therefore, large-scale surveys are needed to be performed in these data-scarce coastal areas promptly.

In this context, here we aimed (1) to determine essential (Cu, Cr, Ni, V, and Zn) and non-essential TE (As, Cd, and Pb) concentrations in the tissues of a bioindicator organism, Mediterranean mussel (Mytilus galloprovincialis Lamarck, 1819) sampled along coastal waters of Turkey, and (2) to evaluate potential health risks for children and adults by Mediterranean mussel consumption comparing with the toxicological limit values such as provisional tolerable weekly intake (PTWI), target risk coefficient (THQ), Hazard Index (HI), and cancer risk (CR).

Materials and methods

Study area and mussel sampling

With the seas surrounded on three sides, Turkey has a length of 8483 km of coastline. There are 28 cities along the coastal line, and approximately 55% of the total population lives in these littoral cordons (TURKSTAT 2019). Sampling stations along this coastline were selected based on two criteria: The areas where the mussel naturally spreads, and the areas with high mussel population density that was assumed to be affected by anthropogenic sources which were preferred to avoid subjective judgment. Based on these criteria, Mediterranean mussels were collected from 23 different stations: 12 from the Black Sea, 6 from the Sea of Marmara, and 5 from the Aegean Sea (Fig. 1). Approximately 20 mussels from each sampling point were obtained by either free or scuba diving at depths ranging from 0.5 to 23 m between September 2019 and March 2020. Geographical coordinates and sampling depths of the stations are provided in Supplementary Material Table 1. The collected samples were placed in the iceboxes within the Ziploc bags, transferred to the laboratory, and stored at −20 °C for posterior analyses.

Fig. 1
figure 1

Sampling stations of the Mediterranean mussel along the coastline of Turkey

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Table 1 Analysis of the certified reference material (ERM CE278k mussel tissue): standard material values versus measured values (mean±SD)
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Sample digestion

Samples were thawed at room temperature and then washed with ultrapure water. Random 5-6 (N) mussels were selected among a bulk of 20 individuals. Right after measuring the length and the weight (Supplementary Material Table 1) of the samples, soft tissues were removed by tissue dissection. The dissected tissues belonging to the specific individuals were homogenized separately and around 1.5 g (fresh weight) of the samples from each was placed in the different digestion tubes with 5 mL of HNO3 (65% Suprapur, Merck) and was covered with polypropylene caps and kept overnight. The tubes were then transferred to a block heater (Velp, Italy) and incubated at 95±3 °C (solution temperature) for 2.5 h. Afterward, the tubes were allowed to cool down to room temperature and were continued to be incubated at 95±3 °C for another 2 h with 2.5 mL of extra H2O2 (30% Suprapur, Merck). The caps were removed, and the tubes were kept in the block heater until the solution volumes were around 2 mL. Finally, the solution was diluted to 50 mL with ultrapure H2O and filtered through the polytetrafluoroethylene, 0.45-μm pore size syringe filter (US EPA 1996), then stored at +4 °C until analyses.

TE analysis and quality control

As, Cd, Cu, Cr, Ni, Pb, V, and Zn concentrations were measured using inductively coupled plasma-mass spectrometer (ICP-MS) (Agilent, 7800). To check and control the digestion processes, the exact method applied to the samples was applied to the certified reference material (ERM-CE278k Mussel Tissue) as well, the results were compared, then the accuracy of the process was determined (Table 1). Blank samples and internal standards (Indium and Scandium) were also used to detect possible interventions during both the digestion process and ICP-MS measurements.

Health risk assessment

Estimated weekly intake (EWI mg/kg/week) is defined as the multiplication of the weekly TE intake with the bioaccessibility (BAm) of TE in the people’s digestive system (Gedik 2018). We calculated EWI using the weekly average mussel consumption rate and average portion size by determined TE concentrations in the mussel. Then, we compared the data to the PTWI values declared by FAO/WHO Joint Expert Committee on Food Additives (JECFA 1982; JECFA 2011a, b). EWI calculation was performed by using the below-given formula (US EPA 2011):

$$ \mathrm{EWI}=7\times \kern0.5em \frac{C\times \mathrm{EF}\times \mathrm{ED}\times \mathrm{FCR}}{\mathrm{BW}\times \mathrm{ET}}\times \mathrm{ADAF}\times {\mathrm{BA}}_{\mathrm{m}}\times {10}^{-3} $$
(1)

where EDI is estimated daily intake, C is the average concentration of TE in the mussel (mg kg−1 wet weight); EF is the exposure frequency (365 days year−1); ED is the exposure duration; and FCR is the mussel consumption rate (g per person per day). For FCR value, with an average daily consumption amount of 1.01 g released by FAO (2013), it was used along with the 85 g and 227 g of the average portion size values for children and adults (US EPA 2000), respectively. ET is known as the average exposure time for non-carcinogens (365 days year−1 × number of exposure years), BW is the average body weight of adults: 70 kg; children: 14.5 kg (US EPA 2000). ADAF is an age-dependent adjustment factor for adults: 1, children: 3 (US EPA 2011). The values of BAm were used for Cr, Ni, Cu, Zn, Cd, Pb, and As which were 58%, 83%, 80%, 76%, 73%, 61% (Gedik 2018), and 90% (He and Wang 2013), respectively.

The target hazard quotients (THQ), calculated by the ratio of exposure to the reference dose concentrations (RfD, mg kg−1 day−1) are used to explain for long-term non-carcinogenic exposure probabilities (US EPA 2020a). People are often exposed to more than one pollutant from the foods they consume. Therefore, Hazard Index (HI) was used to predict (Newman and Unger 2002) the possible combined effects of TE here in our work. THQ and HI were calculated using the formulas below:

$$ \mathrm{THQ}=\mathrm{EDI}/\mathrm{RfD} $$
(2)
$$ \mathrm{HI}=\sum {\mathrm{THQ}}_{\mathrm{i}} $$
(3)

where EDI is the estimated daily intake, RfD is the reference dose, As =3×10−4, Cd =1×10−3, Pb =3.5×10−3, Zn= 3×10−1, Cu= 4×10−2, Ni=2×10−2, Cr=1.5, and V=5×10−3 (US EPA 2020a). The THQ and HI values >1 mean that the TE in the mussel can exert a potential non-carcinogenic health risk. To be able to estimate an individual’s lifetime probability of developing cancer caused by TE exposure, cancer risk (CR) was further calculated via the below formula (US EPA 2011):

$$ \mathrm{CR}=\mathrm{EDI}\times \mathrm{SF} $$
(4)

where SF is slope factors (SF, mg kg−1 day−1). SF: As= 1.5, Pb= 8.5×10−3 (Traina et al. 2019).

Risk factors (EWI, THQ, HI, and CR) for As were calculated using inorganic As values, which are 10% of the total As (US FDA 1993).

Data analysis

The Shapiro-Wilk and Levene tests were used to analyze normality and equal variance, respectively. Non-normally distributed and non-homogeneous data groups were transformed. One-way analysis of variance (Anova, post hoc: Tukey) test was used to determine the differences between the stations regarding TE concentrations in the mussel’s soft tissues. The relationship of the TE concentrations in mussel tissues and the mussel length was examined by linear regression analysis. To determine the contamination status at the stations, TE measurements were assigned to a concentration range as high, medium, and low in the tissue of the mussels sampled from different stations. In order to determine these ranges, cluster (statistical) classification analysis was used to separate the different groups by making use of the similarities in TE concentrations determined in the mussels at the different stations. Each classification (low, medium, high) defined according to the results obtained in this study shows the relative differences between the sampling locations. Factor analysis was performed to confirm the main source(s) of the TE, and Pearson’s correlation analysis was used to determine the relations of the TE with each other. Monte Carlo simulations were further performed to assess the probabilistic distributions of THQ and CR values for children and adult consumers related to mussel consumption. The values were calculated based on the average values of As and Pb in the mussels. The simulations were carried out through 10,000 iterations.

Results and discussion

TE concentration and spatial distribution in the mussels

TE concentrations in the soft tissues of mussels collected from all different stations throughout the Black Sea, the Sea of Marmara, and the Aegean Sea of the Turkish coastal waters were ranged between 0.565–4.202 mg kg−1, 0.565–4.202 mg kg−1, 0.012–0.186 mg kg−1, 0.112–1.865 mg kg−1, 0.169–1.503 mg kg−1, 0.383–2.350 mg kg−1, 0.046–1.865 mg kg−1, and 11.96–150.99 mg kg−1 for As, Cu, Cd, Cr, Ni, Pb, V, and Zn (Fig. 2). The average values (mg kg−1) of TE in general were found in the order of Zn (39.76)> Cu (1.95)> As (1.84)> Pb (0.99)> Ni (0.65)> Cr (0.62)> V (0.47)> Cd (0.08).

Fig. 2
figure 2

Violin plots showing the distribution of trace elements (mg kg−1 fresh weight) in edible soft tissues of Mediterranean mussels sampled along the Turkish coastline. Each dot shows the result of different samples

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TE concentrations in the soft tissues of mussels collected from 23 different stations throughout the Black Sea, the Sea of Marmara, and the Aegean Sea are given in Fig. 3. Significant differences (p<0.05) between the stations were detected in the TE concentrations (Table S1). The difference in the TE concentrations in different sampling regions may be due to the pollution levels in growth environments and several other factors such as gender, age, and size of the individual (Belabed et al. 2013). Also, the change in the TE concentrations in the soft tissues of mussels sampled from different locations is generally related to the local pollution status (Liu et al. 2017). Based on these reasons, as the sampling zones cover an area of approximately 6500 km, pollution loads in terms of TE may vary between the stations.

Fig. 3
figure 3

Trace elements concentrations (average ± standard error; fresh weight, mg kg−1) in edible soft tissues of the Mediterranean mussels sampled along the Turkish coastline. Colored circles at the stations show the cluster analysis results according to the PTEs concentrations in the tissues of the mussels sampled from the relevant station. Each classification identified (low, medium, high) indicates relative differences between the locations

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Based on the specific factors, another reason that may affect the TE accumulation in the mussel tissues might be the mussel sizes differ at sampling stations. To that end, the relationship between mussel length and TE concentrations were analyzed by linear regression analysis (Fig. 4). According to our data, a positive relationship was found between the mussels’ length and As, Cd, and Zn concentrations, while a negative relationship was detected between the Cu, Cr, Ni, Pb, and V (Fig. 4). Other researchers have also studied the relationship between the TE accumulation in the tissues of the mussels and the mussel size. Mubiana et al. (2006), for instance, stated that the TE concentrations were inversely proportional to body size. A similar result was stated by Yap et al. (2009) in their study, which was reported that the small individuals accumulate Cd, Pb, and Zn higher than large individuals. This situation was investigated in another study dealing with four different types of gastropods. In that work, a positive relation was determined between the TE concentrations and the body size (Cubadda et al. 2001). Baltas et al. (2016) further reported that the Cu accumulation was inversely proportional to the body size in their work. Newman and Unger (2002) also reported a growth decrease along with the increased TE accumulation, which was due to the dilution effect in the accumulation resulting from the growth phases. Newman and Unger (2002) stated that growth could also affect the TE elimination processes.

Fig. 4
figure 4

The relationship between the mussel size and the trace elements’ concentrations in the soft tissues of the Mediterranean mussels sampled along the Turkish coastline. Each dot shows the result of different samples

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Natural and anthropogenic TE in coastal ecosystems come from the main point and non-point sources: point-industrial and municipal discharge, and non-point-contaminated river water, agricultural and urban runoff, atmospheric transport, etc. The shares of these resources vary between the different regions. Here in our study, factor analysis and Pearson’s correlation analysis were applied to determine the potential contamination sources of the TE, and the relationship between the TE for the mussels. Factor analysis result is given in Table 2 as eigenvalues, variance (%), and cumulative variance (%). Four components (C) were extracted which explained with Eigenvalues >1. The variance of these components was calculated to be the 70.82%, with the variances being C1 (25.92%)> C2 (17.42%)> C3 (16.09)> C4 (11.39), respectively (Table 2). Thus, we can conclude that C1 was mainly dominated by V, Ni, and As. As enters the coastal waters via the natural sources by erosion, whereas Ni and vanadium enter by burning fossil fuels and mainly through rivers (ATSDR 2005; Wang and Whelmy 2009; ATSDR 2007). C2, on the other hand, was dominated by Zn and Cd. Therefore, the data show that the Zn and Cd distribution and their emerging source might be the same. Also, the discharges of the mining and metal industries are generally shown as the source of these elements (ATSDR 2012). Again, C3 was dominated by Cr and Cu. The reason that Cr and Cu show similar distribution trend might be due to the natural origin of these TE in the sampling regions. Finally, C4 was found highly dominated by Pb. Although naturally found in the earth’s crust, high levels of Pb usually enter the coastal waters by direct discharges of several anthropogenic sources such as production processes, painting, and fossil fuels. Due to the use of leaded gasoline in the past decades, Pb concentrations in the environment have also reached high levels worldwide (ATSDR 2020). Furthermore, Baltas et al. (2017) shown that the Cu, Pb, and Zn derived from the anthropogenic sources on the eastern Black Sea coasts which might be attributable to the rich mineral deposits (Cu and Zn) (Pehlivan et al. 2021) in the region.

Table 2 Results of the factor analysis
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The TE forming the components (Ni, As, and V for C1, Zn, and Cd for C2, Cr, and Cu for C3, Table 2) were found to have a significant positive correlation among TE concentrations (p<0.01). Pearson’s correlation analysis results showing this are given in Table 3. Liu et al. (2018) stated that these significant correlations might reflect that the relevant TE accumulated in the mussels come from similar pollution sources or that mussels tend to accumulate related TE with a similar trend.

Table 3 Pearson’s correlation coefficients matrix of the trace elements in the soft tissues of Mediterranean mussels sampled along the coastline of Turkey (N= 119)
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Status and trends of the TE

Cluster analysis results using the TE concentration similarities in the mussel tissues sampled from different stations along the Turkish coastline are shown in Fig. 3. Three different concentration ranges as low, medium, and high, specific to TE, were determined. Cluster values (low, medium, high) do not indicate the presence of a universal classification or classification for human health. It only indicates the status of the stations depending on the TE concentrations in mussel tissue among stations. Figure 3 shows that 13% of the stations with the highest concentrations of As was categorized as high level, 26% as medium concentration level, and the remaining stations categorized as low concentration level. Low- (0.80–2.799 mg kg−1) and medium-level concentrations (2.800–5.699 mg kg−1) of Cu in 82% and about 13% of the stations were detected, respectively, whereas high concentrations were found at 1 station only (Fig. 3). Six stations were classified as high in terms of Cd concentration, whereas 9 stations were medium, and the others were low concentration. Based on the Cr concentrations data, approximately 21% of the stations were classified as high concentration (0.800–1.300 mg kg−1), about 43% as medium (0.500–1.799 mg kg−1), and the remaining 36% stations as low in terms of Cr contamination. According to the cluster analysis results, Ni levels in the stations were classified as high (approximately 17%), medium (approx. 61%), and low (approx. 22%) concentration, respectively. The stations were classified as 21% high, 21% medium, and 58% low, based on the Pb distributions. For V, about 78% of the sites along the Turkish coasts exhibited low concentrations (0.10–0.59 mg kg−1), about 17% exhibited medium concentrations (0.600–1.299 mg kg−1), and about 5% exhibited the high concentrations (1.300–1.600 mg kg−1). For Zn concentrations in the mussels sampled from different locations, whereas 35% of stations showed low concentrations (13.00–30.99 mg kg−1), about 55% showed medium concentrations (31.00–59.99 mg kg−1), and about 9% was showing high concentrations (60.00–85.00 mg kg−1).

In order to determine the time-dependent change trends of the As, Cd, Zn, Pb, and Cu concentrations at the sampling stations, the data were compared with the works conducted in similar stations (Unsal 2001; Topcuoǧlu et al. 2002; Sunlu 2006; Cevik et al. 2008; Culha et al. 2011; Mol and Alakavuk 2011; Kucuksezgin et al. 2013; Balkis et al. 2013; Tepe et al. 2016; Belivermis et al. 2016). The resulting data of the comparisons is given in Fig. 5. Based on this comparison, As increased in 9 stations (p <0.05), and no change in trend has been detected in 3 stations. Cd concentrations of a total of 16 stations were compared, and a downward trend was observed at 15 stations, whereas no change was detected at 1 station. In the Zn concentrations, while there is a decrease in 4 stations and an increase in 1 station, no change has been identified in the other 13 stations. While no changes were observed at 8 stations for Pb concentration, noticeable increases and decreases were determined at 6 and 5 stations, respectively. While the number of stations without any change for Cu was 12, an increase was observed only at 1 station and a decrease at 3 stations (Fig. 5).

Fig. 5
figure 5

The trends of the trace elements in the soft tissues of the Mediterranean mussels sampled along the Turkish coastline. Results were presented as decreasing (˅), increasing (˄), or exhibiting no trend (-). The trends obtained in our study were compared with the literature conducted in similar stations (Unsal 2001; Topcuoǧlu et al. 2002; Sunlu 2006; Cevik et al. 2008; Culha et al. 2011; Mol and Alakavuk 2011; Kucuksezgin et al. 2013; Balkis et al. 2013; Tepe et al. 2016; Belivermis et al. 2016)

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Health risk

In order to protect the health of consumers, some institutions and countries have set guidelines on the maximum levels of TE permitted in seafood. Among these TE, Cu, Zn, Cr, V, and Ni take part in critical metabolic activities. However, high doses could easily have a toxic effect.

Conversely, As, Cd, and Pb can be toxic for humans even at very low doses. For this reason, these 3 elements were listed as the top 10 in the “Substance Priority List” declared by ATSDR 2019). The maximum permissible limits had also been determined by some international organizations for As, Cd, and Pb. For example, the European Commission (EC) stated that the Pb and Cd values in the mollusks should not exceed 1.5 and 1 mg kg−1, respectively (EC 2006). When we compared our data with these limits, the Cd value did not exceed the thresholds. However, the Pb values in the tissues of the mussels sampled from 10 different stations were found to be above the limits (Fig. S1). We calculated the estimated weekly intake values using the values obtained for As, Cu, Cd, Ni, Pb, and Zn, for the average consumption and average portion size for both children and adults (EWI). We also compared that with the provisional tolerable weekly intake (PTWI) values specified by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) (Table 4). We further determined that the EWI values calculated for children and adults were below the limit values specified by JECFA (Table 4).

Table 4 Estimated weekly intake (EWI), target hazard quotients (THQs), Hazard Index (HI), and carcinogenic risk (CR) through consumption of soft tissues of Mediterranean mussels sampled along the coastline of Turkey
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Chronic exposure to As, which is toxic to all living organisms at high concentrations, has a carcinogenic effect on animals and humans (ATSDR 2007). JECFA stated that the PTWI value for As was 0.015 mg kg−1 bw (JECFA 2011a). Average and average portion consumption of As concentrations in the mussels sampled from different stations for adults and children constitute at most 19.6% of the declared JECFA PTWI values.

Trace levels of Cu are an essential nutrient for living organisms. Accordingly, it has a vital cofactor role in several biological processes. PTWI value for Cu is 3.5 mg kg−1 bw (JECFA 1982). When the consumption-based EWI was calculated with the Cu values obtained in the current study, we found that the values varied between 0.000158 and 0.0276 mg kg−1 bw. The EWI values obtained were determined to vary between 0.005 and 0.79% of the PTWI value specified by JECFA.

The primary source of human exposure for Cd is reported to be the food for the non-smoking population (EFSA 2012). The JECFA (2011b) established a provisional tolerable weekly intake (PTWI) for Cd of 0.007 mg kg−1 bw in this regard. Based on our calculation, Cd exposure via mussels contributed to the dietary in child and adult consumers was between 0.83–2.68% and 1.21–14.57%, respectively.

Nickel is a biologically essential element as well that is widely distributed in the environment (EFSA 2015). Gastrointestinal effects and neurological symptoms were reported to be seen in humans after Ni exposure through food (EFSA 2015). EFSA determined the PTWI value for Ni as 0.0196 mg kg−1 bw. Here we calculated that the EWI values for Ni varied between the 0.000054 and 0.00942 mg kg−1 bw for child and adult consumers. Given this calculation, mussels contributed to dietary Ni exposure for child and adult consumers were between the rates of 0.27 and 48.06%.

Pb is another TE that exists naturally in the earth’s crust; however, it is not used in the biological processes of organisms because of its toxic effects. People generally are exposed to Pb through food consumption (EFSA 2010) as expected. Pb accumulation in humans affects the central nervous system, along with the possible impairment in visual abilities and psychiatric symptoms such as malfunction in information processing and manual skills (EFSA 2010). PTWI value for Pb specified by JECFA (2011b) is 0.025 mg kg−1 bw. Thus, when we calculated the EWI for Pb content in the sampled mussels in coastal waters of Turkey (Table 4), we found that the mussels contributed to the dietary exposure of Pb in child and adult consumers were between the rates of 0.24 and 42.8% depending on the consumption rates.

Zn is also an essential element and has various vital biological functions. People get Zn from food (EFSA 2014), and large amounts, unfortunately, can lead to gastrointestinal effects and hinder the homeostasis of other essential elements in the body (WHO 2001). For this reason, JECFA declared that the PTWI limit is 7 mg kg−1 bw for Zn (JECFA 1982). Average daily requirements were also reported to be 6.2–12.7 mg/day for an adult, while in children, this amount is between 2.4 and 11.8 mg/day (EFSA 2014). The weekly Zn intake, which we calculated from the average and the average portion amounts in children and adults, ranged between 0.00309 and 0.537 mg kg−1 bw (Table 4), and PTWI contribution of these amounts varied between 0.04 and 7.67%.

THQ was further calculated and is given in Table 4 to evaluate the non-carcinogenic health hazard for humans comes from each TE by the consumption of mussels taken from the sampling regions. All THQ values calculated for TE (except As) were detected <1, which shows that the average and the average portion size of mussel consumption size may not necessarily have adverse health effects for both children and adult consumers. However, for As, THQ value was 1.40, which was calculated based on the 85 g consumption per week for children. This data indicates that the As that comes from mussels might cause adverse health effects for children. When we evaluate the HI values, these values which were found lower than 1 (which is the limit value) varied between 0.0175 and 0.561 depending on the average daily consumption. However, on the basis of the average portion size, we calculated that HI values varied between 0.253 and 3.40, which was above the limit value of 1 for children. This result proves that the weekly portion size (85 g) in pediatric consumers might cause adverse health effects. The results also showed that the As, compared to the other TE, had the highest and most significant share in the non-carcinogenic risks at low and high consumption amounts both for adults and children. Some other studies on aquatic organisms have also shown that As has the most significant contribution to the HI.

An individual’s lifetime exposure to potential carcinogens is estimated with cancer risk (CR) (US EPA 2011). CR values here in our work were calculated only for As, and Pb, whose cancer slope factor is specified (Traina et al. 2019). Calculated CR values are given in Table 4. The CR value for As ranged from 3.62 × 10−6 to 1.16 × 10−4 and 5.25 × 10−5 to 6.31 × 10−4 for adults and children, respectively. CR values calculated for Pb varied between the 7.43 × 10−8 and 2.39 × 10−6 and 1.85 × 10−6 and 1.29 × 10−5 for respective individuals. According to the US EPA (2020b), CR values indicated that if it is less than 10−6, it is insignificant, if > 10−4, it is unacceptable, and if it is between 10−6 and 10−4 then it is acceptable. The CR values were calculated based on the high consumption amounts, and we detected that the As amount was higher than the limit value of 10−4, which is the unacceptable level in the recommended consumption limits for adults and children. CR values were also found to be acceptable or insignificant for Pb at all consumption rates in both adults and children (Table 4).

In addition, the probabilistic distributions of THQ and CR for adult and child consumers regarding mussel consumption were evaluated using the Monte Carlo simulation, which was performed through 10,000 iterations. Monte Carlo simulations are presented in Fig. 6. The THQ and CR values were detected higher in children, of which similar results were reported in the literature (Wang et al. 2020). The simulation of Monte Carlo exceeded the THQ uncertainty distribution limit value of 1, which was calculated from the weekly consumption amount for children, for both As and Pb. It could be concluded that 73.63% and 0.1% of child consumers may experience adverse health effects for As and Pb respectively. Besides, CR values of As showing the unacceptable limit (10−4) were exceeded by 62.98% of adults consumers and by 97.24% of children consumers (Fig. 6). This data show that consuming mussel from polluted locations (3, 18, 23) may pose a considerable carcinogenic risk to adult and childconsumers.

Fig. 6
figure 6

Monte Carlo simulation results of the target hazard quotients (THQ) and cancer risks (CR) for adults and children exposed to the As and Pb by Mediterranean mussel consumption. The blue dash line shows the threshold level of THQ (1) and CR (10−4). The percentages (%) in the graphs show the probabilities of potential risks for the As and Pb. THQ and CR were calculated using average consumption rate (7.07 g/week/person; FAO 2013), and average portion size for adults and children (227 and 85 g/week/person, respectively; US EPA 2000)

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The International Cancer Research Agency (IARC) has defined the As as a group I element. It indicates that the As is potentially carcinogenic to humans. IARC (2012) generally outlines the ways of As exposure via the consumption of contaminated drinking water and food. Several researchers have shown that the As accumulated in the aquatic organisms is way more than in quantity found in the other foodstuffs (Gedik and Ozturk 2019; Liu et al. 2018). However, it is in the organic form, which is less toxic to human. Inorganic As, on the other hand, which is toxic to humans, constitutes 10% (US FDA 1993) of the total As in the crustaceans. Although THQ and CR were calculated using this 10% of As values, it has been detected that the CR and THQ values exceeded the limits.

Conclusion

This study was designed to determine the concentration of the TE in the mussels collected from the Turkish coasts (the Black Sea, the Sea of Marmara, and the Aegean Sea) and evaluate the human health risks related to mussel consumption. Pb values were found above the EU limit values (detected in 43% of the stations) while Cd values were found to be below the limits at all 23 stations. The EWI values calculated for the child and adult consumers according to the daily average consumption and average portion size were below the PTWI limits. However, the THQ (non-carcinogenic risk) values were recorded higher than 1 for As, indicating that it may induce adverse health effects for children caused by mussel’s consumption. Furthermore, As exposure via higher amounts of mussel consumption can pose carcinogenic risks for 63% and 97% of the adult and children populations, respectively. Further research should focus on determining the clean areas along the Turkish coasts to use mussel production for safe consumption.