Bioaccumulation and human health implications of essential and toxic metals in freshwater products of Northeast China

Science of the Total Environment 673 (2019) 768–776

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Bioaccumulation and human health implications of essential and toxic metals in freshwater products of Northeast China Lei Fu a,b, Xianbo Lu a,⁎, Kai Niu a,b, Jun Tan a, Jiping Chen a,⁎ a

b

CAS Key Laboratory of Separation Science for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, China University of Chinese Academy of Sciences, Beijing 100049, China

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• EDI of metals from freshwater products of N. China were below their limits. • Species-specific bioaccumulation for different metals was quite different. • Methyl mercury and Mn could pose potential noncarcinogenic risk to human. • Inorganic arsenic would cause potential carcinogenic risk at the 1/100,000 level. • Bioaccumulation of toxic metals in E. sinensis and C. auratus was most serious.

a r t i c l e

i n f o

Article history: Received 4 February 2019 Received in revised form 4 April 2019 Accepted 8 April 2019 Available online 09 April 2019 Editor: Jay Gan Keywords: Bioaccumulation Human health risks Heavy metals ICP-MS Freshwater products Northeast China

a b s t r a c t Bioaccumulation and human health risks of essential and toxic metals in ten species of freshwater products from Northeast China were investigated in this study. The concentrations (mg/kg wet weight) of target metals in aquatic products were: Fe (4.6–165.4), Zn (4.1–33.4), Mn (0.28–80.0), Cu (0.24–15.8), Cr (0.074–0.80), As (0.0068–0.72), Hg (0.016–0.58), Ni (0.019–0.58), Pb (0.017–0.27) and Cd (0.0004–0.058). There was no significant regional difference of target metal levels in fish samples between Liaoning province and Inner Mongolia Autonomous Region according to matched sample t-test. Every daily intakes (EDI) of target metals from freshwater products were far below their corresponding limits. However, health risk assessment of individual metal in freshwater products showed methyl mercury (MeHg) and Mn could pose potential noncarcinogenic risk to human, and inorganic arsenic (iAs) would cause potential carcinogenic risk to consumers at the level of 1 in 100,000. Furthermore, freshwater product species-specific bioaccumulation characteristics for different metals are quite different. The total hazard quotients of target metals in different aquatic product species demonstrated that coexposure of target metals by consumption of these six species (C. auratus, E. sinensis, C. erythropterus, C. carpio, M. anguillicaudatus and O. cantor) from Northeast China could cause potential noncarcinogenic risk to human, and the pollution of toxic metals in E. sinensis and C. auratus were most serious among all investigated aquatic species. © 2019 Elsevier B.V. All rights reserved.

1. Introduction ⁎ Corresponding authors. E-mail addresses: [email protected] (X. Lu), [email protected] (J. Chen).

https://doi.org/10.1016/j.scitotenv.2019.04.099 0048-9697/© 2019 Elsevier B.V. All rights reserved.

Aquatic products are important nutrient sources to human, as they are abundant of proteins, omega-3 fatty acid, microelements and

L. Fu et al. / Science of the Total Environment 673 (2019) 768–776

vitamins (Cutting, 1961). Due to their rich nutrients and delicious tastes, the consumption of aquatic products is increasing greatly in China during recent decades (Golden et al., 2016; FAO, 2016). Even though aquatic products provide numerous nutrients for human, they also contain environmental contaminants which can cause adverse effects on human health. Aquatic products are the important source of essential metals for human, while they also are the significant source of toxic metals. The levels of toxic metals in aquatic products are increasing due to industrial, agricultural and mining activities. Iron, copper, zinc, nickel and manganese are regarded as essential metals in human body as they play an important role in the maintenance of human health. Lack or excess of essential metals in human body can have hazard effects on human health (Chale, 2002). Mercury, arsenic, cadmium, chromium and lead are toxic metals which can induce a series of cancers, embryotoxicity, neurotoxicity and genetic alteration of cells to human even exposure at extremely low dose (Jarup, 2003; Jomova and Valko, 2011). It has been demonstrated that consumption of aquatic products is the main pathway of human intake of trace metals (CEC, 2006; Jarup, 2003), and toxic metals in aquatic products can pose significant risks on human health (Gu et al., 2017; Jayaprakash et al., 2015; Sapkota et al., 2008; Yi et al., 2011). Therefore, information about the bioaccumulation of essential metals and toxic metals in aquatic products are important both from ecological and human health perspectives. A large number of researches about the levels of toxic metals in aquatic products from famous rivers, lakes and reservoirs had been reported (Ahmed et al., 2015; Arulkumar et al., 2017; Jayaprakash et al., 2015; Kaya and Turkoglu, 2017; Liu et al., 2018; Ragi et al., 2017; Varol and Sunbul, 2017; Yi et al., 2017; Yi et al., 2011). These researches indicated that aquatic products were contaminated by toxic metals in varying degrees and pollution of toxic metals in aquatic products is a common problem in many countries. Although there are some researches about toxic metals in aquatic products from China, investigated regions of these studies are usually limited to only one city, one lake or one reservoir, and these investigations are limited to only a few species of aquatic products. Besides, few researches evaluated the human health risk of both essential metals and toxic metals in freshwater products systematically. Northeast China, including Liaoning, Jilin, Heilongjiang province and Inner Mongolia Autonomous Region, is very rich in natural resources, especially mineral and petroleum resources. As a traditional agricultural production and industrial base in China, agricultural, industrial and mining activities leaded to large amounts of heavy metals releasing into aquatic ecosystem (Gao et al., 2014; Li et al., 2017; Zhu et al., 2017). Northeast China has a significant potential in terms of fisheries and aquaculture production, and its area accounts for 21% of China's territorial area, while its output of freshwater products in this area was about 1.9 million tons in 2015 (National Bureau of statistics of China, 2015). Up to now, there is no systematic study on bioaccumulation and human health risk of heavy metals in aquatic products from Northeast China. The present study aimed to systematically investigate the levels, regional distributions, species-specific differences of essential metals and toxic metals in aquatic products from Northeast China, and to assess potential human health risks caused by metals exposure via aquatic products consumption. Ten metals including essential metals (Fe, Zn, Cu, Ni, Mn) and toxic metals (As, Pb, Cd, Cr, Hg), in ten species of freshwater products from Northeast China were investigated in this study, and the selected freshwater product species are all popular and favored by consumers. 2. Materials and methods 2.1. Chemicals and reagents 68% concentrated nitric acid (guaranteed reagent) was purchased from CNW (Germany). 30% hydrogen peroxide solution (Guaranteed

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reagent) was from Sinopharm (Shanghai, China). Deionized water was prepared with a Milli-Q purifier (Millipore, St. Quentin en Yvelines, France). Multi-Element Standard Solution came from Perkin-Elmer (Massachusetts, USA). Certified reference materials GBW10018 (Element analysis standard material in Chicken muscle) for method verification was obtained from the National Research Center for Certified Reference Materials (Beijing, China). Other reagents were analytical grade and the blank levels of metal contents were confirmed to guarantee free of target metals. 2.2. Information about industries development and aquatic environment in Northeast China Northeast China is a main production region of agricultural products and an old industrial base in China, and these agricultural and industrial activities have resulted in larger amounts of contaminants releasing into the environment. Northeast China is rich in petroleum, coal and metal mineral resources, which has been China's most important energy and steel base. There are a large number of industries in Northeast China, such as Liaohe Oilfield and Ansteel. With the discovery, exploration and development of mineral deposits, metal pollution in aquatic environment of Northeast China is worrying, especially in resource-based cities, such as Panjin, Benxi, Anshan, Fushun, Batou, Wuhai, Chifeng, Hulun Buir, Ordos and so on (Li et al., 2014). There are several famous aquatic products from Northeast China, such as freshwater fishes in Dahuofang reservoir, crabs from Panjin and rainbow trout from Benxi. Some researchers found there was metal pollution in these aquatic environments. For example, Dahuofang is the biggest reservoir of Liaoning Province, which provides drinking water for thirty million citizens, as well as industrial and agricultural water for dozens of cities and rural areas. Researches revealed that Dahuofang reservoir was polluted by several kinds of heavy metals (Pb, Cr, Hg and As) (Wu et al., 2012). In addition, the pollution level and potential eco-risk intensity of Cd in sediment from Taizi River, one of the largest rivers in Liaoning Province, were worrying (Shao and Zhao, 2012). In another study, investigation showed Cd and As in sediment of Hulun Lake, the biggest lake in Inner Mongolia autonomous region, demonstrated an increasing trend during recent years (Sun et al., 2018). 2.3. Sample collection 106 individual aquatic products representing ten species were onsite collected from the main production areas of freshwater products in Liaoning province and Inner Mongolia autonomous region in 2015. The economy of Liaoning province is dominated by heavy industry and crop farming, and Inner Mongolia is typically based on animal husbandry and mining industry (Fu et al., 2018). Besides, the sum area of these two regions accounts for about 67.5% of the total area of Northeast China. Therefore, Liaoning and Inner Mongolia are chosen as representative areas of Northeast China, and aquatic products sampled from these two areas can be sufficiently representative of the overall aquatic products in Northeast China. The whole process of aquatic product sample collection was carried out according to the Chinese sampling regulation for contaminant monitoring in fishery products (Ministry of Agriculture of China, 2004). The detailed information of sampling locations is presented in Fig. 1, and the information about freshwater product species is summarized in Table S1 in the Supporting information. With the help of fishermen, N106 aquatic products were on-spot sampled. The tissues of aquatic products for analysis were homogenized by grinder and stored in polythene self-sealing bag under −10 °C in freezer. To make the sample more representative, each sample for analysis is a mixture muscle from three aquatic products of the same species collected from the same sampling site. A total of 33 representative samples were made from 99 aquatic product samples that were on-spot sampled. The

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Fig. 1. The map of the investigated region with the sampling points ( ) and the output percentage of freshwater products in each province accounting for the total output in Northeast China.

investigated ten species of aquatic products include silver carp (H. molitrix), rainbow trout (O. mykiss), common carp (C. carpio), river crab (E. sinensis), crucian (C. auratus), grass crap (C. idellus), predatory carp (C. erythropterus), snake head (O. cantor), bighead carp (A. nobilis) and loach (M. anguillicaudatus). The output of these investigated aquatic product species accounts for the main part of the total production of aquatic products in the Northeast China. Furthermore, these investigated species of aquatic products are living in different habitats and have different feeding habits. 2.4. Sample preparation The digestion was performed in Anton Paar microwave digestion system (Anton Paar GmBH, Austria). Samples of aquatic products (0.300 g dry weight) were directly weighted into acid-washed polytetrafluoroethylene microwave digestion tube, then 10 mL of concentrated HNO3 (68%) and 2.0 mL of H2O2 (30%) were added to each tube before microwave digestion. Each digestion batch contained a reagent blank, and a certified reference material (GBW10018) was used to ensure the accuracy of measurement (the certified values and recoveries were provided in Table S2 of the Supporting information). The

procedure of microwave digestion was as follows: the temperature of microwave digestion system heated up to 175 °C in 10 min and kept this temperature for 30 min. After the digestive solution cooling down to room temperature, the solution was transferred into a volumetric flask and the volume was made up to 50 mL with ultrapure water.

2.5. Instrumentation and analysis The concentrations of Fe and Zn were determined by 7300DV ICPOES (PerkinElmer, USA, Massachusetts), and the concentrations of Mn, Cu, Cr, As, Hg, Ni, Pb and Cd were measured using NexION 300D ICPMS (PerkinElmer, USA, Massachusetts). Results were quantified through calibration curves which were generated from responses obtained from multiple dilutions of a multi-element calibration standard. The correlation coefficients of calibration curves of metals were all N0.999. Analytical quality control included the procedural blank and certified reference material of a similar matrix. The concentrations of target metals in blanks were extremely low to be negligible, and the measured values of target metals in certified reference material were consistent with the certified values as shown in Table S2.

L. Fu et al. / Science of the Total Environment 673 (2019) 768–776

2.6. Evaluating bioaccumulation levels of different aquatic product species Metal pollution index (MPI) is an index to compare the accumulation levels of metals among different aquatic product species. The higher the MPI value of freshwater product is, the higher the accumulation level of metals is. MPI is calculated according to Eq. (1) (Usero et al., 1997). MPI ¼ ðC1  C2  C3  …  Cn Þ1=n

ð1Þ

where Cn is the concentration of metal n in aquatic product samples. 2.7. Human exposure and health risk assessment The target hazard quotient (THQ) is an index to assess noncarcinogenic risk of metal through aquatic product consumption. It can be calculated according to the following equations recommended by EPA (EPA, 2000).

Table 1 Concentrations of metals in aquatic products and their corresponding maximum residue limits (mg/kg wet weight). Range

Fe Zn Mn Cu Ni Cr As iAsa Hg MeHgb Pb Cd a b c d

THQ ¼ EDI=RfDo

ð2Þ

EDI ¼ ðR  Cn Þ=BW

ð3Þ

where RfDo represents oral reference dose of pollutant recommended by EPA, EDI is every daily intake of metals through aquatic products consumption, R is the per capita aquatic product consumption, BW is adult's average body weight. R was 134 g day−1 for Chinese in 2015, reported by National Statistics Bureau of China in 2015. BW was considered as 60 kg in this study. Actually, human is exposed to metals mixture during the consumption of freshwater products, and co-exposure to a cocktail of metals could result in synergistic toxicities on organism (Cobbina et al., 2015; Lin et al., 2016). So, the total THQ (TTHQ) is applied to evaluate the noncarcinogenic risk on human body caused by co-exposure to metal mixture from aquatic products consumption, which is the arithmetic sum of each metal THQ value (Chien et al., 2002). TTHQ ¼ THQ 1 þ THQ 2 þ THQ 3 þ … þ THQ n

ð4Þ

where THQn represents the THQ of metal n in aquatic product samples. It is necessary to evaluate the carcinogenic risk of inorganic arsenic (iAs) via consuming aquatic products as inorganic arsenic is a proven human carcinogen (EPA, 1993; CAC, 2017). The target cancer risk (TR) is applied to estimate the carcinogenic risk, calculated as the following equation. TR ¼ EDI  CSF

ð5Þ

where CSF (1.5/mg kg−1 day−1) is cancer slope factor recommended by EPA (EPA, 2000). 3. Results and discussion 3.1. Concentration of essential metals in aquatic products Fe, Zn, Mn, Cu and Ni were analyzed in present study, and the concentration ranges, average values of target metals in freshwater products and corresponding limits of metals recommended by China (Food and Administration, 2012) and international organizations (CEC, 2006; CAC, 2017) are shown in Table 1. The mean concentrations of metals in samples decreased in the order: Fe N Zn N Mn N Cu N Ni, and Fe was the most abundant metal with median values of 12.7 mg/kg ww. These values in present study were compared with those in other regions as shown in Table 2. The concentrations obtained in present study were much higher than researches carried in Northeast China a few years ago (Qin et al., 2015) and Xiang River (Jia et al., 2017) for

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4.6–165.4 4.1–33.4 0.28–80.0 0.24–15.8 0.019–0.58 0.074–0.80 0.0068–0.72 0.0002-0.022 0.016–0.58 0.014-0.52 0.017–0.27 0.0004–0.058

Mean

19.4 12.6 6.6 1.8 0.10 0.35 0.17 0.005 0.13 0.12 0.062 0.0047

Median

12.7 9.1 0.65 0.67 0.039 0.28 0.076 0.002 0.071 0.064 0.040 0.0012

MRL China

EUc

CACd

– – – – – 2.0

– – – – – – –

– – – – – – –

0.5 0.3 0.05

0.5 0.3 –

0.1 0.5 0.5 0.1

Represented inorganic arsenic. Represented methylmercury. EU (CEC, 2006). (CAC, 2017).

Fe, Zn, Mn and Cu, and were similar with those in fishes from The Yangtze River (Yi et al., 2017) for Fe, Zn, Mn and Cu. 3.2. Concentration of toxic metals in aquatic products The levels of Cr, As, Hg, Pb and Cd in present study were shown in Table 1. The concentrations of Cr and Pb in all samples were all far below their corresponding maximum residue limits (MRLs) recommended by China and other international organizations. iAs is a wellknown carcinogen which is the most toxic form of arsenic, and oral exposure to iAs is responsible for a series of cancers (Waalkes et al., 2004). According to Chinese national standard, the MRL for iAs in aquatic product is 0.1 mg/kg ww. The content of iAs was assumed to be 3% of total As in aquatic product (EPA, 1993), iAs concentrations in present study were all far below its corresponding limit. Methylmercury (MeHg) is the chemical form of most concern and can make up N90% of the total mercury in aquatic products (CEC, 2006), and ingestion of contaminated aquatic products is the primary source of MeHg exposure (Mergler et al., 2007; Ramon et al., 2011; Vieira et al., 2015; Xu and Newman, 2015). MeHg is widely recognized as a potent neurotoxicant in humans since it can affect both the developing and the mature central nervous systems (World Health Organization, 2007). The MRL for MeHg in aquatic products recommended by China and international organizations are 0.5 mg/kg ww. The concentration of MeHg was assumed as 90% of the total Hg, and the results of this study showed that the levels of MeHg in most samples were far below the MRLs established by China, EU and CAC, except one Cyprinus carpio sample from Tongliao, Inner Mongolia with concentration of 0.52 mg/kg ww. The MRLs recommended by EU and China for Cd in aquatic products were 0.05 mg/kg (CEC, 2006) and 0.1 mg/kg respectively, while the concentration of Cd in an Eriocheir sinensis sample from Panjin, Liaoning (0.058 mg/kg ww) slightly exceeded the MRL of EU. Overall, all mean concentrations of toxic metals in this study were less than their corresponding MRLs. The concentrations of toxic elements in our study were compared with those in previous literatures as shown in Table 2. The average levels for Cr, As and Hg in present study were 0.35, 0.17 and 0.13 mg/kg respectively, which were much higher than previous research carried in Northeast China a few years ago (0.121, 0.096, 0.013 mg/kg), while the levels for Pb and Cd in present study (0.062 and 0.0047 mg/kg) were obviously lower than the reported values in Northeast China (0.172 and 0.011 mg/kg) (Qin et al., 2015). Compared with other area in China, the concentrations of As and Hg in this study were higher than those in fishery products from The Yangtze River (0.095 and 0.043 mg/kg), while the values for Cr, Pb and Cd in present study were much lower than those in fishes from The Yangtze River

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Table 2 Average concentrations of metals in aquatic products of the present study and other literatures (mg/kg ww). Region

Fe

Zn

Mn

Cu

Cr

As

Hg

Ni

Pb

Cd

Present study Northeast China (Qin et al., 2015) Xiang river (Jia et al., 2017) The Yangtze River (Yi et al., 2017) Niger Delta (Moslen and Miebaka, 2017) Turkey (Varol and Sunbul, 2017)

19.4 6.71 3.137 25.421 –a –

12.6 7.90 4.69 12.193 –a 12.33

6.6 0.136 0.215 –a –a –

1.8 0.293 0.118 1.020 12.94 0.78

0.35 0.121 –a 0.420 2.32 –

0.17 0.096 0.042 0.095 –a 0.12

0.13 0.013 –a 0.043 –a –

0.10 0.119 –a –a 2.76 –

0.062 0.172 0.056 0.117 5.67 0.018

0.0047 0.011 0.021 0.062 0.73 0.0013

a

It was not analyzed in the literature.

(Yi et al., 2017). Compared to other countries, the concentration determined for Cu, Cr, Ni, Pb and Cd in this study were much lower than those in aquatic products from Niger Delta (12.94, 2.32, 2.76, 5.67 and 0.73 mg/kg) (Moslen and Miebaka, 2017), while the values for As, Pb and Cd were higher than those in aquatic products from Turkey (0.12, 0.018, 0.0013 mg/kg) (Varol and Sunbul, 2017). 3.3. Species-specific bioaccumulation characteristics for different metals In order to discover the bioaccumulation characteristic of metals among different aquatic product species, mean concentrations of target metals in different species were compared and showed in Fig. 2. The levels of Mn, Cu, Fe, Cd, and Ni in E. sinensis were the highest, and the average concentrations of Zn, Cr, Pb and Hg in C. auratus were the highest

among all investigated species. It indicated the higher bioaccumulation potential of metals in E. sinensis and C. auratus than in other aquatic species. For example, the concentration of Cd and Mn in E. sinensis reached 0.129 mg/kg (ww) and 219 mg/kg (ww), which was about 30 times and 45 times higher than that in C. carpio, respectively. In addition, the highest average concentration of As in O. mykiss was found to be 2.27 mg/kg ww, which was about 6 times higher than that in C. carpio. Bioaccumulation process of metals in organism is influenced by many factors, such as habitats, dietary habits, growth rate and so on (Liu et al., 2018). E. sinensis and C. auratus are benthic organism, and their habitat are sludge and lower layer of water body, which usually contains higher metal concentrations than in other part of water body (Jayaprakash et al., 2015). As a result, metals are likely more easily to accumulate in E. sinensis and C. auratus compared with other investigated

Fig. 2. Average concentration of essential metals and toxic metals in different aquatic product species.

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species. As for O. mykiss, it is a carnivorous fish living in cold water, meanwhile its metabolism is very slow. In previous studies, it was found that organochlorine pesticides and polychlorinated biphenyl levels in O. mykiss were obviously higher than in other aquatic products (Fu et al., 2018). In fact, most of the As (about 97%) in aquatic products are organic arsenic. It was deduced that the dietary habits and slow metabolism rate of O. mykiss might result in the high bioaccumulation potential of organic arsenic. The principal components analysis (PCA) was performed on the Logarithmic transformation of individual concentration of target analytes in each sample, and the PCA score plot and loading plot are shown in Fig. 3. Combining the PCA score plot and the PCA loading plot for analysis, Fe, Cu, Cd, Mn, As and Ni preferred to enrich in E. sinensis among all investigated species. The result was consistent with above analysis result that these concentrations of Fe, Cu, Cd, Mn and Ni in E. sinensis were the highest, as shown in Fig. 2. Besides, the position of Zn and Pb in PCA loading plot was close, it implied that these two elements shared a certain similarity on metals bioaccumulation in aquatic products. MPI is an index to evaluate the contaminated level of different aquatic products, and MPIs of essential and toxic metals in different aquatic products species are shown in Fig. 4. MPIs of essential and toxic metals in E. sinensis were the highest among all species, and MPIs of C. auratus were the second highest. The results showed E. sinensis and C. auratus could not only provide high levels of essential metals, but also bring high levels of toxic metals for human body. O. mykiss is one of the most popular aquatic products in all over the world due to its good taste. It was noteworthy that MPI of essential metals in O. mykiss was the lowest, while MPI of toxic metals in O. mykiss were the third highest, which demonstrated that O. mykiss supplied relatively low content of essential metals and relatively higher content of toxic metals for human body. 3.4. Characteristics of metal concentrations in aquatic products from different sampling regions The concentrations of target metals in aquatic products from different sampling sites were presented in Fig. 5. Mixed breeding of Rice and Crab is the biggest feature of Panjin area. The total concentrations of essential and toxic metals in samples from Panjin were the highest and the second highest among all samples respectively, which should be attributed to that the samples collected from Panjin were crabs, as above

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mentioned that crabs are easier to accumulate metals than other species of aquatic products. The total concentration of toxic metals in samples from Huludao and Benxi were higher while their essential metals' concentrations were lower. There is a Zinc plant in Huludao city, which is the largest zinc smelting plant in Asia. Some literature had reported that there were potential ecological risk of As, Hg, Pb, Cd and Cr in soil, sediment, water and vegetables around Huludao zinc plant (Zhang et al., 2008; Zheng et al., 2008; Zheng et al., 2007). Benxi is one of the important bases for steel production and raw material industry, and this industrial structure has a certain effect on the high concentrations of heavy metals in aquatic products. In general, as shown in Fig. 5B, the total concentrations of toxic metals in aquatic product from Liaoning were higher than those from Inner Mongolia. These results may be mainly attributed to the differences in agricultural and industrial structures. Overall, the heavy industry is much more developed in Liaoning than in Inner Mongolia, as the economy of Liaoning Province is typically based on heavy industry and crop farming, whereas animal husbandry is dominant in the Inner Mongolia Autonomous Region (Fu et al., 2018). The concentration ranges and mean concentrations of all target analytes in samples from Liaoning province and Inner Mongolia Autonomous Region were presented in Table 3. The mean concentrations of all metals except Hg in aquatic products from Liaoning were obviously higher than those in samples from Inner Mongolia. Significant differences of all target metals between these two regions were analyzed according to matched sample t-test. The results indicated that there was no significant difference of target metals contents except As in aquatic products between Liaoning and Inner Mongolia (P N 0.05), showing similarity in spatial distribution of these metals between these two regions. It should be noted that significant difference of As concentrations in aquatic products was observed between Liaoning and Inner Mongolia (P b 0.05), and the former presented 3 times higher content than the latter. The samples from Liaoning included fishes and crabs, while the samples from Inner Mongolia were all fishes. As discussed in above Section 3.2, the concentrations of metals in crabs were significantly different with those in fishes. So, the concentration of target metals in fishes (excluding crabs) from Liaoning and Inner Mongolia are compared. The levels of ten metals in fishes from Liaoning and Inner Mongolia are shown in Table S3. There was no significant difference of heavy metal concentrations in fish samples between Liaoning and

Fig. 3. The PCA score plot and loading plot of the Logarithmic transformation of individual metal concentrations in freshwater products from Northeast China. In score plot, red symbols represent samples from Liaoning and green symbols represent samples from Inner Mongolia. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Fig. 4. MPI of essential metals (A) and toxic metals (B) in different freshwater product species from Northeast China.

Inner Mongolia, which suggested that aquatic product species had a greater influence on metals bioaccumulation characteristics than regional difference between Liaoning and Inner Mongolia.

3.5. Human exposure and health risk assessment through aquatic product consumption Aquatic products contaminated by excessive essential element and toxic element would cause negative effects for human health (Korashy et al., 2017; Morcillo et al., 2016; Park et al., 2007). For the purpose to assess the potential human health risks of metals in aquatic products from Northeast China through consumption of aquatic products, EDI, THQ, HI and TR are used as indexes to evaluate the potential risks induced by target metals. EDI of metals via the consumption of aquatic products were calculated via Eq. (3). As shown in Table 4, EDI50th and EDI95th of Cu, As, Cd, Hg, Fe and Zn were all far below their corresponding Provisional Maximum Tolerable Daily Intake (PMTDI) recommended by The Joint FAO/ WHO Expert Committee on Food Additives (JECFA, 2017). It should be pointed out, because diet exposure of lead at 0.6 μg/kg bw/day corresponding to a decrease of 1 IQ point, JECFA concluded that it was not possible to establish PMTDI for Pb that would be considered health protective. Besides, by far JECFA have not established PMTDI for Cr, Mn and Ni to protect human heathy. THQ is an index of assessing the potential noncarcinogenic risk to human caused by individual metal exposure via aquatic product consumption. If the value of THQ is equal or above 1, indicating that metal exposure via fishery products consumption poses noncarcinogenic risk for human body. If THQ is b1, suggesting there is no obvious risk. As shown in Table 4, the THQ50th for individual metal decreased in the

Table 3 Concentrations of metals in freshwater products from Liaoning and Inner Mongolia (mg/kg ww). Liaoning

Fig. 5. Concentration of metals in aquatic products from different sampling sites (mg/kg ww; A: essential metals; B: toxic metals).

Cr Mn Ni Cu As Cd Hg Pb Fe Zn

Inner Mongolia

Min

Max

Mean

Min

Max

Mean

0.14 0.28 0.028 0.47 0.056 0.0004 0.03 0.021 4.57 4.12

0.77 80.28 0.58 15.81 0.72 0.058 0.28 0.27 165.35 27.49

0.418 15.82 0.136 3.37 0.30 0.01 0.095 0.08 30.71 14.04

0.074 0.30 0.019 0.24 0.0068 0.0004 0.016 0.017 6.55 4.75

0.80 1.67 0.29 2.10 0.41 0.0039 0.58 0.23 22.97 33.45

0.31 0.69 0.076 0.71 0.092 0.0012 0.15 0.051 12.00 11.60

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Table 4 Estimated daily intake (EDI, μg kg−1 day−1) and target hazard quotients (THQ) for individual metals through aquatic products consumption. EDI50th

EDI95th

RfDo (μg kg−1 day−1)

THQ50th

THQ95th

PMTDI (μg kg−1 d−1)

1500 140 20 40 – 0.3 1 – 0.1 4 700 300

0.0004 0.010 0.004 0.037 – 0.017 0.003 – 1.43 0.025 0.041 0.068

0.0012 1.18 0.042 0.67 – 0.15 0.094 – 9.95 0.15 0.29 0.22

– – – 500 2.1 – 0.83 0.57 – – 800 1000

TR50th

TR95th

– – – – – 7.5 × 10−6 – – – – – –

– – – – – 6.5 × 10−5 – – – – – –

(μg kg−1 day−1) Cr Mn Ni Cu As iAs Cd Hg MeHg Pb Fe Zn

0.6 1.5 0.09 1.50 0.17 0.005 0.003 0.16 0.14 0.09 28.4 20.3

1.8 164.9 0.83 26.79 1.49 0.045 0.094 1.11 1.00 0.53 201.0 65.5

following sequence: Cr b Cd b Ni b Mn b iAs b Pb b Cu b Fe b Zn b 1 b MeHg, while the THQ95th for individual metal decreased as following sequence: MeHg N Mn N 1 N Cu N Fe N Zn N Pb N iAs N Cd N Ni N Cr. The THQ50th of all metals except MeHg were lower than 1, and the THQ95th of MeHg and Mn were 3.69 and 1.18, respectively. It indicated that exposure to Hg and Mn via aquatic product consumption from Northeast China would cause potential noncarcinogenic risk for human health when exposure at upper-bound level (THQ95th). TTHQ is applied to as an index of assessing total noncarcinogenic risk of all target metals in different aquatic product species which is calculated via Eq. (4). As presented in Fig. 6, the TTHQ of different aquatic product species decreased as following sequence: C. auratus N E. sinensis N C. erythropterus N C. carpio N M. anguillicaudatus N O. cantor N 1 N H. molitrix N H. nobilis N O. mykiss N C. idellus. The TTHQ of the top six species were N1, suggesting that co-exposure of the target metal mixture by consumption of these six aquatic product species from Northeast China would cause noncarcinogenic risk for human. Among all target metals, iAs was identified as human carcinogen by EPA. As shown in Table 4, the TRs of iAs at lower-bound and upperbound concentrations were 7.5 × 10−6 and 6.5 × 10−5, respectively. TR50th fell in the acceptable risk range (10−6 to 10−5) recommended by many regulatory agencies, while TR95th was out of the safety threshold range. It suggested that consumption of aquatic products from Northeast China would cause potential carcinogenic risk to consumers at 10−5 level based on 95th percentile concentration of iAs. 4. Conclusions In present study, a systematic survey of essential metals and toxic metals in freshwater products from Northeast China were performed.

The contents of all target metals were below their responding permittable limits recommended by China, except for the concentration of Cd in one C. carpio sample slightly exceeded the limit established by EU. The results indicated that the levels of target metals in freshwater products from Northeast China were generally in an acceptable range. Excluding the data from E. sinensis, there was no significant regional difference of heavy metal concentrations in fish samples between Liaoning and Inner Mongolia according to matched sample t-test. However, the species-specific bioaccumulation characteristics for different metals are quite significant. The results indicated the higher bioaccumulation potential of metals in E. sinensis and C. auratus than in other aquatic species. Furthermore, human health risks via exposure to target metals through aquatic products consumption were assessed. EDI of individual metal was all far below its corresponding PMTDI. Among all investigated ten metals, the THQ50th of all metals except MeHg were lower than 1, indicating the potential noncarcinogenic risk to human caused by individual metal exposure via aquatic product consumption from Northeast China were generally negligible, although the potential noncarcinogenic risk caused by individual exposure to MeHg should be given more attention. The total noncarcinogenic risk of all target metals co-exposure (TTHQ) in different freshwater product species showed that daily consumption of these six kinds of fishery products (including C. auratus, E. sinensis, C. erythropterus, C. carpio, M. anguillicaudatus and O. cantor, their TTHQ N 1) from Northeast China would cause potential noncarcinogenic risks to human. It should be pointed out that the TR50th of iAs (7.5 × 10−6) fell in the acceptable risk range (10−6 to 10−5) recommended by many regulatory agencies, while the TR95th (6.5 × 10−5) of iAs indicated that it would cause potential carcinogenic risk to consumers at the level of 1 in 100,000. Overall, the potential human health risk from MeHg and iAs via consumption of freshwater products from Northeast China should be paid more attention. Acknowledgments This work was financially supported by the Special Fund for Agroscientific Research in the Public Interest of China (Grant No. 201503108), and the National Natural Science Foundation of China (No. 21577139). Statement The authors declare no competing interests. Appendix A. Supplementary data

Fig. 6. The TTHQ of different freshwater product species from Northeast China.

Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2019.04.099.

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