Residual levels of rare earth elements in freshwater and marine fish and their health risk assessment from Shandong, China

Marine Pollution Bulletin 107 (2016) 393–397

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Residual levels of rare earth elements in freshwater and marine fish and their health risk assessment from Shandong, China Luping Yang a,b, Xining Wang a,b, Hongqian Nie a,b, Lijun Shao a,b, Guoling Wang a,b, Yongjun Liu c,⁎ a b c

Shandong Center for Food Safety Risk Assessment, Shandong Center for Disease Control and Prevention, Jinan, People's Republic of China Academy of Preventive Medicine, Shandong University, Jinan, People's Republic of China Institute of Materia Medica, Shandong Academy of Medical Sciences, Jinan, People's Republic of China

a r t i c l e

i n f o

Article history: Received 4 February 2016 Received in revised form 14 March 2016 Accepted 16 March 2016 Available online 24 March 2016 Keywords: Rare earth elements China Marine Freshwater Fish

a b s t r a c t The total concentrations of rare earth elements (ΣREE) were quantified in 251 samples from 10 common species of freshwater and marine fish in seventeen cities of Shandong, China. ΣREE obtained from the freshwater fish ranged from 34.0 to 37.9 ngg−1 (wet weight) and marine fish from 12.7 to 37.6 ngg−1. The ratio of LREE to HREE was 13.7:1 and 10:1 for freshwater and marine fish, respectively. This suggests that freshwater fish exhibit greater REE concentrations than marine fish and the biological effects of LREE are higher than HREE. Results revealed a similar REE distribution pattern between those fish and coastal sediments, abiding the “abundance law”. The health risk assessment demonstrated the EDIs of REEs in fish were significantly lower than the ADI, indicating that the consumption of these fish presents little risk to human health. © 2016 Elsevier Ltd. All rights reserved.

Elements from lanthanum (La; Z = 57) to lutetium (Lu; Z = 71) are commonly referred to as rare earth elements (REEs). REEs are utilized in various different fields; acting as petrogenetic tracers in geochemistry, fertilizers in agriculture, and superconductors and supermagnets in the industry (Celik et al., 2015). Due to their metallurgical, optical and electronic properties, they are of great importance for industrial applications. However, the broad usage of REEs has gradually increased the pollution of the environment which in turn has caused an accumulation in organisms, therefore making it possible to enter the food chain (Kumar et al., 2011). Fish constitutes a prominent part of the human diet, thus its quality and safety aspects are of particular interest. People worldwide consume fish for their health benefits such as high protein, low saturated fat content and omega fatty acids (Cirillo et al., 2010; Storelli et al., 2007; Xia et al., 2013). On the other hand, reports show that seafood consumption can lead to humans being exposed to a variety of chemical contaminants, such as REEs, that can cause harm to the human body (Storelli, 2008). Over the past decades, concentrations of heavy metals in fish have been extensively studied in various places around the world. (Leung et al., 2014; Makedonski et al., 2015; Qiu, 2015; Scheuhammer et al., 2015; Storelli et al., 2007; Wu et al., 2014). Relative to common metals (e.g., arsenic, copper, lead, mercury, and zinc), fewer studies were published regarding the aquatic toxicity or bioaccumulation ⁎ Corresponding author at: Institute of Materia Medica, Shandong Academy of Medical Sciences. No.18877 Jingshi Road, Jinan, Shandong, China. E-mail address: [email protected] (Y. Liu).

http://dx.doi.org/10.1016/j.marpolbul.2016.03.034 0025-326X/© 2016 Elsevier Ltd. All rights reserved.

characteristics of REEs. REEs are less prominent environmental contaminants unlike ubiquitous heavy metals (e.g., As, Cd, and Pb). These can induce adverse health effects and stimulate crystallization of urinary stones (Bernstein et al., 2012; Cui et al., 2012; Hongyan et al., 2002; Pagano et al., 2015a, b). Previous studies have focused on REE contents in several environmental samples such as lakes, oceans, and the atmosphere (Costas et al., 2010; Jiang et al., 2012; Tranchida et al., 2011). Currently, there is only a limited amount of study and research material in regards to the content of REEs in fish (Huimin et al., 2009; Mayfield and Fairbrother, 2015; Weidong et al., 2003; Xiaorong et al., 1991, 1993; Yatawara et al., 2010). In addition, no publications have been found to report the current REE pollution levels. This issue underlines the importance of establishing a baseline data for future references. The aim of this paper is to document concentrations of total and individual REEs in fish sold in the Shandong Province. The major objectives of this study were; (1) to examine the extent of bioaccumulation of REEs in freshwater and marine fish available in local markets of the Shandong Province and (2) to assess the potential health risks based on REE concentrations in fish muscle. Based on our knowledge, this is the first study to compare REEs in freshwater and marine fish. Located in eastern China, Shandong Province is the largest center for fishery production and processing in the country. Its fishery output value and total output of aquatic products is also ranked first in the country (Xiumei et al., 2007). A total of 251 samples were selected from ten fish species collected in the Shandong province. This includes four freshwater fish and six marine fish collected from local markets and supermarkets within 17 cities of Shandong. These fish species

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Table 1 Fish species obtained from local markets of the Shandong province, China. Common name Freshwater fish Grass carp Crucian Big head Carp Carp

Latin name

Mean size Feeding (gram/cm) mode

Number tested

Ctenopharyngodon Carassius auratus Aristichthys nobilis Cyprinus carpio

895/25.4 403/20.6 387/30.2 945/29.4

Herbivorous Herbivorous Filter feeder Herbivorous

29 26 10 50

Platycephalus indicus 476/35.8 Scophthalmusmaximus 426/34.6 Trichiurus lepturus 452/58.4

Carnivorous Carnivorous Carnivorous

10 11 34

Marine fish Flathead fish Turbot Largehead hairtail Japanese sea perch Sphyraenus

Perca fluviatilis

764/42.8

Carnivorous

30

Chelon haematocheilus

378/28.6

30

Yellow croaker

Larimichthys polyactis

157/15.8

Bottom feeder Bottom feeder

21

currently hold the greatest economic importance and are the most commonly consumed amongst the Shandong residents. At least 5 individual samples were taken from each fish species with similar body weights. All biological characteristics of fish samples are shown in Table 1. The specimens were wrapped in aluminum foil, preserved in ice and brought to the laboratory on the same day of collection. Before analysis, the muscular tissue (edible part) from each fish was homogenized with a blender and stored in closed polyethylene vessels inside a refrigerator at −20 °C. The microwave digestion system was used for analysis where approximately 0.50 g of the sample was weighed and digested with 8 ml of concentrated nitric acid (65%) in a PTFE digestion vessel. The solution was then poured into a volumetric flask and diluted to 10 ml with ultra-high purity water after cooling for roughly 40 min. The inductively-coupled plasma mass spectrometry (ICPMS) determined the Pr, Sm, Lu, Nd, Gd, Dy, Nd, Ce, Ho, Tb, Er, Tm, Yb, and Eu in the muscle samples (Thermo iCAP Q, Thermo Fisher Scientific, Bremen, Germany). Concentrations were expressed in REE nanogram per wet weight of tissue samples (ngg− 1). The limits of detection (LOD) and quantification (LOQ) of each analyte were calculated through the analyte concentration that corresponded to three and ten times the standard deviation of ten independent blank measurements respectively. The result is then divided by the slope of the calibration curve. The current ICP-MS system accurately determines extremely low REE concentrations in fish samples. This is illustrated through the results of the LOD (0.001 ~ 0.255 ngg− 1) values. The correlation coefficient of

the REEs ranged from R2 = 0.9994 to R2 = 0.9999, with the calibration curves displaying great linearity in the concentration range from 1 to 100 ngg− 1. The Quality Assurance/Quality Control (QA/QC) procedures involved the use of standard reagents and the analysis of two certified reference materials: GBW10024(GSB-15) pectinid, GBW10050(GSB-28) prawn (Institute of Geophysical and Geochemical Prospecting, LangFang, China). The results of the analysis are presented in Table 2. Concentrations of REE in fish meat collected from Shandong markets are tabulated (Table 3). The concentrations of light REEs (LREEs; La to Eu), heavy REEs (HREEs; Gd to Lu), and the total concentration of REEs (ΣREEs) at each sampling are as shown in Table 4. The REE levels were determined through the sampling of 251 samples from six marine and four freshwater fish species. ΣREEs obtained ranged from 34.0 to 37.9 ngg−1 (wet weight) for freshwater fish and 12.7 to 37.6 ngg−1 (wet weight) for marine fish. The Largehead hairtail (12.7 ngg−1) was found to have the lowest ΣREE concentration amongst marine fish samples while the carp (37.9 ngg− 1) had the highest for the freshwater samples. The average concentration of REEs for freshwater fish and marine fish were 35.8 and 21.0 ngg−1 respectively. In general, freshwater fish meat contains relatively greater levels of total REEs contents compared to those of marine fish meat. Fewer amounts of REEs contents in marine fish meat may be due to dilution and microbial degradation (Miceli et al., 2009). This REE distribution pattern is similar to the distribution of other contaminants in freshwater and marine fishes (Wei et al., 2011a, b). Coherent with previous research and reports, REE concentrations in fish meat of the benthic feeding species (Sphyraenus and Yellow croaker) were greater than the pelagic feeding species (turbot and Largehead hairtail species) (Mayfield and Fairbrother, 2015). The law of distribution is the same in other metals, evident as benthic fish exhibited higher heavy metal concentrations than fishes inhabiting in the upper water column. This is because they are in direct contact with the sediments and can uptake greater amounts of heavy metal concentrations from benthic organisms (El-Moselhy et al., 2014; Gu et al., 2015; Wei et al., 2014). The ΣREEs (35.8 ngg−1) of REEs in freshwater fish is dominated by LREEs (33.3 ngg− 1), LREEs (33.3 ngg−1) being 13.7 times that of HREEs (2.44 ngg− 1). The patterns of REE concentrations in marine and freshwater fish muscles were relatively similar. For the marine fish samples, the ΣREE was 21.0 ngg−1 and the ratio of LREE to HREE was 10.0 with the LREEs and HREES contents being 19.1 and 1.90, respectively. The variation of ΣREEs closely matched that of LREEs, reflecting the determination of LREEs to ΣREEs. The ratio of LREEs to HREEs falls within the range of the freshwater fish tissues from a reservoir in the Washington State (9.0) (Mayfield and Fairbrother, 2015) and higher than the fish of Shenzhen coastal region (2.37) (Huimin et al., 2009) and Xiamen Bay (1.39) (Weidong et al., 2003). This shows that

Table 2 Analysis of reference materials (GBW10024, GBW10050) (mean ± SD,n = 6). Element

La Ce Pr Nd Sm Eua Gd Tb Dy Ho Er Tm Yb Lu a

GBW10024(GSB-15)

GBW10050(GSB-28)

Certified μgkg−1

Determined μgkg−1

Recovery %

Certified μgkg−1

Determined μgkg−1

Recovery %

37 ± 8 53 ± 13 6.0 ± 0.8 25 ± 7 4.8 ± 1.5 0.9 ± 0.3 5.2 ± 1.2 0.84 ± 0.19 5.3 ± 1.2 1.2 ± 0.3 3.3 ± 0.7 0.52 ± 0.10 3.2 ± 0.9 0.49 ± 0.11

33.3 ± 5.07 49.5 ± 7.28 5.85 ± 0.57 22.8 ± 3.42 4.24 ± 0.80 0.87 ± 0.17 4.80 ± 0.71 0.77 ± 0.12 4.96 ± 0.73 1.09 ± 0.17 3.13 ± 0.51 0.48 ± 0.07 2.86 ± 0.46 0.45 ± 0.07

90.1 93.4 97.5 91.2 88.4 96.2 92.4 91.7 93.6 90.7 94.9 93.2 89.4 91.4

66 ± 5 130 ± 30 14.5 ± 1.1 56 ± 6 10.7 ± 1.8 2.5 ± 0.3 10.5 ± 1.2 1.5 ± 0.2 7.9 ± 0.5 1.5 ± 0.2 4.4 ± 0.4 0.69 ± 0.18 4.1 ± 0.8 0.64 ± 0.21

64.6 ± 3.75 124 ± 5.70 13.3 ± 0.77 52.3 ± 3.56 9.68 ± 0.49 2.24 ± 0.20 9.75 ± 0.76 1.30 ± 0.09 7.02 ± 0.32 1.32 ± 0.12 4.00 ± 0.22 0.61 ± 0.03 3.78 ± 0.22 0.60 ± 0.04

97.9 95.3 91.7 93.4 90.5 89.6 92.9 86.4 88.9 88.2 91.0 87.8 92.1 93.4

Corrected for interference from BaO.

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Table 3 Concentrations of REEs in four kinds of freshwater fish and six kinds of marine fish. Unit is ngg−1 for all elements. La

Ce

Pr

Nd

Sm

Eu

Gd

Tb

Dy

Ho

Er

Tm

Yb

Lu

Freshwater fish Grass carp Crucian Big head carp Cyprinus Carpio Average of freshwater fish

16.7 15.7 19.1 14.8 16.6

9.28 12.0 10.0 9.54 10.2

1.00 1.09 1.12 1.45 1.16

3.63 4.11 4.07 4.91 4.18

0.897 0.999 0.800 1.04 0.933

0.256 0.231 0.320 0.247 0.264

0.985 0.926 1.18 1.19 1.07

0.089 0.102 0.095 0.111 0.099

0.475 0.518 0.518 0.553 0.516

0.089 0.099 0.107 0.107 0.100

0.290 0.315 0.329 0.353 0.322

0.039 0.044 0.045 0.044 0.043

0.227 0.270 0.231 0.260 0.247

0.037 0.042 0.045 0.041 0.041

Marine fish Flathead fish Turbot Largehead hairtail Japanese sea perch Sphyraenus Yellow croaker Average of marine fish

13.2 4.65 4.87 4.71 14.7 10.8 8.81

6.15 4.79 3.92 3.88 11.7 6.67 6.19

0.646 0.500 0.452 0.390 1.32 0.709 0.670

2.41 1.99 1.76 1.53 5.04 2.76 2.58

0.456 0.782 0.424 0.687 1.21 0.683 0.706

0.132 0.136 0.091 0.128 0.267 0.177 0.155

0.550 0.602 0.455 0.448 1.16 0.692 0.652

0.060 0.091 0.052 0.060 0.158 0.096 0.086

0.317 0.557 0.315 0.372 0.891 0.544 0.499

0.053 0.117 0.058 0.072 0.172 0.106 0.096

0.174 0.346 0.191 0.223 0.493 0.318 0.291

0.011 0.039 0.018 0.024 0.052 0.034 0.030

0.130 0.275 0.149 0.171 0.366 0.244 0.222

0.012 0.029 0.016 0.023 0.050 0.031 0.027

there is more bioaccumulation of LREEs in fish than HREEs, strongly relating to the light and heavy REE crystal chemical properties (Xiong-yi et al., 2014). Simultaneously, it also demonstrates the biological effects of LREEs on fish and other organisms that are stronger than that of HREEs (Weidong et al., 2003). The REE distribution characteristics in fish tissues can be graphically represented. The abundance coefficient curve of REEs was established with the normalized ratio of REE contents in sediments and in chondrite. This could eliminate the abundant changes between odd and even atomic numbers. The curve mapped the geochemical differentiation of the fish tissues to the original rare earth composition (Shakeri et al., 2015; Wood, 2006). Although the abundances of REEs were vastly different, the REE distribution patterns in all fish species were consistent and had obvious regularities, as shown in Fig. 1. The LREEs had apparent negative slopes, proving that the degree of LREEs was higher than that of HREEs, this may be due to the fractionation of LREE and HREE. The La–Eu curve is steep, while the Eu–Lu curve is gradual, with the enrichment of LREE relative to HREE and slightly negative Eu anomalies. This indicates that the REEs in fish are related to the marine sediments in the sea area and that the utilization of REEs in marine fish generally follows the law of abundance. The correlation analysis results are consistent with the existing research result (Huimin et al., 2009; Weidong et al., 2003). The estimated daily intake (EDI) of REEs through fish consumption was calculated by the following equation (EPA, 2000): EDI ¼

Cfish  CR BW

EDI (ng kg−1 body weight (bw) day−1) is an estimated point where REEs could be exposed to humans. Cfish is the fish consumption rate. In order to deduce low and high exposures to REE concentrations for people with varied fish consumption, Cfish was estimated to be 11 g day−1 per capita for the low fish consumption group and 119 g day−1 per capita for the high consumption group (Fung et al., 2004). Based on the statistics of 158,666 Chinese people from all provinces compiled by Gu et al., the average body weight (BW) for Chinese adults is 58.1 kg, (Gu et al., 2006). This was certificated from the human health survey in REE mining areas and animal experimentation results. From this data, Zhu et al. have proposed a daily allowable intake (DAI) of 4.2 mg for rare earth oxides (REOs) (Weifang et al., 1997). The EDIs of REE for both the low and high fish consumption group indicates that all fish consumption would result in far less than that of the EDI found to be damaging to human health (70 μg/kg/day for REOs) (Weifang et al., 1997). However, the EDIs of REE for the fish species including Big head Carp and Sphyraenus were much higher than the other species as evident in Table 5. The daily intake dose for both the low and high fish consumption groups of the ten fishes declined in the order of: Big head Carp N Sphyraenus N Crucian N Carp N Grass carp N Flathead fish N Yellow croaker N Turbot N Largehead hairtail N Japanese sea perch. The EDIs of the total rare earth oxides (ΣREOs) of both Freshwater and Marine fish consumption are significantly lower than the established ADI, despite the high fish consumption along the coast. Therefore, based on these results, the human health risk assessment indicated that the harm of REE exposure to human body through the consumption of these Freshwater and Marine fishes are negligible.

Table 4 Concentration of total REEs (ΣREEs), light REEs (LREE:La to Eu) and Heavy REEs (HREE:Gd to lu)(in ngg−1). LREE/HREE concentration ratio, normalized La/Yb and La/Sm concentration ratios and values of δEu and δCe in fishs collected from market of Shandong province, China. ∑REE

LREE

HREE

LREE/HREE

δEu

δCe

(La/Yb)N

(La/Sm)N

(Gd/Yb)N

Freshwater fish Grass carp Crucian Big head Carp Cyprinus carpio Average of freshwater fish

34.0 36.4 37.9 34.7 35.8

31.8 34.1 35.4 32.0 33.3

2.23 2.32 2.55 2.66 2.44

14.2 14.7 13.9 12.0 13.7

0.84 0.74 1.02 0.69 0.82

0.53 0.68 0.51 0.48 0.54

48.7 38.4 54.5 37.7 44.3

11.4 9.63 14.6 8.78 10.9

3.49 2.76 4.09 3.68 3.48

Marine fish Flathead fish Turbot Largehead hairtail Japanese sea perch Sphyraenus Yellow croaker Average of marine fish

24.3 14.9 12.8 12.7 37.6 23.8 21.0

23.0 12.8 11.5 11.3 34.2 21.8 19.1

1.31 2.06 1.25 1.39 3.35 2.06 1.90

17.6 6.25 9.19 8.14 10.2 10.5 10.0

0.82 0.62 0.64 0.72 0.70 0.80 0.71

0.49 0.74 0.62 0.67 0.62 0.56 0.60

66.9 11.2 21.7 18.2 26.5 29.2 26.2

17.8 3.64 7.04 4.21 7.45 9.66 7.65

3.38 1.76 2.46 2.10 2.56 2.28 2.35

(La/Sm)N and (Gd/Yb)N mean the internal differentiation status of LREE and HREE, respectively; δEu, and δCe mean abnormality degree of Ce, and Eu. The subscript N refers to the relative abundance after chondrite was standardized: δCe = CeN/(LaN × PrN)0.5,δEu = EuN/(SmN × GdN)0.5.

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Fig. 1. Chondrite-normalized REE distribution patterns for freshwater and marine fish. The surface sediments from the coastal Bahai Bay (Zhang and Gao, 2015) and the Huanghe river are also presented (Yang et al., 2002).

Concentrations of total and individual REEs in freshwater and marine fish samples in the Shandong Province were documented with freshwater fish having a relatively higher ΣREE than marine fish. The abundance of REEs in both freshwater and marine fish was different while their REE distribution patterns were consistent with LREEs are higher than HREEs. This consistency was also found when comparing REE content patterns in fish to those of coastal sediments; evidently complying the abundance law. Results of the health risk assessment found that EDIs of REEs for the low and high fish consumption groups are significantly lower than the ADI, thus can be assumed a trivial issue to damaging the human health.

Acknowledgments This study was supported by the Medical and Health Technology Project of Shandong Province (2015WS0273).

Table 5 Estimated daily intake (EDI) of total REOs via fish consumption for the low and high fish consumption group in Shandong Province (μg/kg/day). Species

REEs

REOs

Low fish consumption group

High fish consumption group

(μg/kg)

(μg/kg)

EDI(μg/kg/day)

EDI(μg/kg/day)

Freshwater fish Grass carp Crucian Big head Carp Carp

34 36.4 37.9 34.7

40.3 43.3 45 41.1

0.00764 0.00821 0.00851 0.00779

0.0826 0.0887 0.0921 0.0843

Marine fish Flathead fish Turbot Largehead hairtail Japanese sea perch Sphyraenus Yellow croaker

24.3 14.9 12.8 12.7 37.6 23.8

28.8 17.7 15.2 15.1 44.6 28.2

0.00546 0.00335 0.00287 0.00286 0.00844 0.00534

0.0593 0.0362 0.0312 0.0309 0.0913 0.0578

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