Environ Sci Pollut Res DOI 10.1007/s11356-016-6918-4

RESEARCH ARTICLE

Trace metal contamination in commercial fish and crustaceans collected from coastal area of and health risk assessment

Mohammad Raknuzzaman1,2 & Md Kawser Ahmed3 & Md Saiful Islam4 & Md Habibullah-Al-Mamun1,2 & Masahiro Tokumura1 & Makoto Sekine1 & Shigeki Masunaga 1

Received: 25 January 2016 /Accepted: 17 May 2016 # Springer-Verlag Berlin Heidelberg 2016

Abstract Trace metals contamination in commercial fish and intake (EDI) and target cancer risk (TR) revealed high dietary crustaceans have become a great problem in Bangladesh. This intake of As and Pb, which was obviously a matter of severe study was conducted to determine seven trace metals concen- public health issue of Bangladeshi coastal people which should tration (Cr, Ni, Cu, Zn, As, Cd, and Pb) in some commercial not be ignored and concentrate our views to solve this problem fishes and crustaceans collected from coastal areas of with an integrated approaches. Thus, continuous monitoring of Bangladesh. Trace metals in fish samples were in the range of these toxic trace elements in seafood and immediate control Cr (0.15 − 2.2), Ni (0.1 − 0.56), Cu (1.3 − 1.4), Zn (31 − 138), measure is recommended. As (0.76 − 13), Cd (0.033 − 0.075), and Pb (0.07 − 0.63 mg/kg wet weight (ww)), respectively. Arsenic (13 mg/kg ww) and Zn Keywords Bangladesh . Trace metals . Fish . Crustaceans . (138 mg/kg ww) concentrations were remarkably high in fish Health risk of Cox’s Bazar due to the interference of uncontrolled huge hatcheries and industrial activities. The elevated concentrations of Cu (400), Zn (1480), and As (53 mg/kg ww) were also observed in crabs of Cox’s Bazar which was considered as an Introduction absolutely discrepant aquatic species with totally different bio- accumulation pattern. Some metals in fish and crustaceans In recent, substantial considerations are being compensated to exceeded the international quality guidelines. Estimated daily the environmental pollution by a variety of chemical contam- inants including the trace metals (Orecchio and Amorello 2010). Accumulation of trace metals in aquatic ecosystems Responsible editor: Philippe Garrigues have upstretched public apprehension to all over the world Electronic supplementary material The online version of this article due to their high potential to enter and accumulate in food (doi:10.1007/s11356-016-6918-4) contains supplementary material, chains (Ivan et al. 2011; Erdoğrul and Erbilir 2007). Trace which is available to authorized users. metals are environmentally ubiquitous, freely dissolved and transported by water, and readily taken up by fish and other * Mohammad Raknuzzaman aquatic organisms (Jordao et al. 2002). Fishes are often at the [email protected] top of the aquatic food chain, and their normal metabolism may accumulate some trace metals from food, water, or sedi- 1 Graduate School of Environment and Information Sciences, ment (Yilmaz et al. 2007; Mansour et al. 2002). Thus, fishes Yokohama National University, Yokohama, Japan are often used for many years as excellent biomarkers to in- 2 Department of Fisheries, University of , Dhaka 1000, vestigate metal levels in their living environments and to as- Bangladesh sess ecological and health risks posed by anthropogenic waste 3 Department of Oceanography, University of Dhaka, discharges (Muiruri et al. 2013;Zhouetal.2008;Oostetal. Dhaka 1000, Bangladesh 2003). Metal accumulation in fish has been evidenced to be 4 Department of Soil Science, Patuakhali Science and Technology pretentious by several factors, e.g., metabolic activities, swim- University, Dumki, Patuakhali 8602, Bangladesh ming patterns, ecological needs, and living environments. Environ Sci Pollut Res

Among these factors, living environment is frequently consid- the coastal water pollution that might contaminate the ered to be more important due to its complicated nature and fish, crustaceans and others aquatic biota which eventu- the heterogeneous tendency of metal distribution (Mustafa ally threaten human health through fish and seafood con- and Gülüzar 2003). Besides, accumulation patterns of contam- sumption. About five million people are engaged in inants in fish and other aquatic organisms also depend both on commercial fishing while fish and crustaceans are the uptake and elimination rates (Hakanson et al. 1988;Guven major protein and earning source of the coastal people. et al. 1999). Compared with fishes, crustaceans particularly TheHilsa(Tenualosa ilisha), Rupchanda (Pampus crabs, may be considered as an absolutely discrepant aquatic argentius), Long tongue sole (Cynoglossus lingua), species and act as a typical benthic organism and might also be Indian shrimp (Penaeus indicus), and Mud crab (Scylla good indicators reflecting the contamination levels in surface serrata) are commercially important edible fishes and sediment (Ololade et al. 2011). However, metals from natural crustaceans which are widely consumed by the common and anthropogenic sources incessantly enter into the aquatic people. The contaminated fish and crustaceans from the environment where they pose a serious threat as a conse- coastal environment may become a public health con- quence of their toxicity, long persistence, bioaccumulation, cern in future. and biomagnification in the food chain (Papagiannis et al. But, in the Bangladesh context, the concerned author- 2004). Thus, trace metal residues in contaminated habitats ities and general people have not been aware and no may accumulate in microorganisms, fishes, crustaceans, and complete study has been carried out so far regarding this other aquatic animals which may enter into the human food issue. So, it is important to determine the concentrations chain and result in health problems (Cook et al. 1990; Gupta of trace metals in commercial fishes and crustaceans con- et al. 2009). sidering possible health risk of coastal people through We are not free from health risks. Modern economic fish consumption. Furthermore, it is important to observe development has been accelerating environmental pollu- the level of trace metals in consumed fishes to get some tion which, in turn, becomes a threat to human health. concepts regarding the safety of fish and seafood protein Health risk concerning with trace metals contamination supplied to the consumers. Thus, the objective of this is regarded as a global crisis. The accumulation of these study is extensively involved on health risk assessment trace elements can cause severe damage to liver, kidney, of coastal people of Bangladesh, based on certain trace central nervous system, mucus tissues, intestinal tract, metals (Cr, Ni, Cu, Zn, As, Cd, and Pb) contamination and reproductive systems. Furthermore, to the toxic and and their spatial and temporal distribution in some com- carcinogenic effects of some metals in humans and ani- mercial fishes, crustaceans along with environmental mals, they also play vital role in mediating a balanced media. biological functioning of cells (Sharma et al. 2014). Therefore, the concern is growing more and more seri- ous globally especially in developing countries like Materials and methods Bangladesh (Chen et al. 2011;Wuetal.2008). Currently, trace metals contamination in fish and crusta- Study area and sampling location ceans have become a severe issue to the public health of Bangladesh. Bangladesh is a riverine country with a Four sampling sites (Cox’s Bazar, Chittagong, Meghna large marshy jungle coastline of 580 km in the Bay of Estuary, and Sunderbans) with three different locations . The river and have been one of of each were investigated in the southeast and southwest the major recipients of industrial effluents from India coastal area of Bangladesh (Fig. 1). The first site (St 1) (Gupta et al. 2009) entering into Bangladesh as Padma is located at the southeast coastal area in Cox’s Bazaar and Jamuna. The river Padma and the river Jamuna are which lies between latitudes 21° 27′ 02″ N to 21° 26′ joined together in Chandpur forming the 33″ N and longitudes 91° 58′ 16″ E to 91° 57′ 01″ E. which dumping up the waste materials through Bhola Cox’s Bazar was a seaside tourist town with an unbroken estuary to the Bay of Bengal. Besides, the rapid inadver- 125 km world’s longest natural sandy sea beach. Coastal tent industrialization, urban expansion, enormous popu- shrimp culture has been widely practiced in this coast lation growth, and overall trans-boundary water issue since a couple of decades where more than 53 shrimp contribute massive amounts of domestic wastewater hatcheries and aquafarms, big fish landing centers can be and untreated industrial effluents into the coastal area foundinverycloserelationto the sea beach. Besides, through rivers. These contaminants can be deposited into these sampling areas were mostly influenced by un- aquatic organisms by the effects of bioconcentration, planned industries, huge hotels for tourists, and munici- bioaccumulation, and the food chain process. The con- pal sewages. The second site (St 2) is located near the taminants coming through these rivers are accelerating Chittagong port and ship breaking area which lies Environ Sci Pollut Res

Source- http://bluegoldbd.org/more-information/maps/ Fig. 1 Map showing sampling sites in the coastal area of Bangladesh

between latitudes 22° 13′ 27″ Nto22°38′ 22″ Nand activities like cement factories, export processing zone, longitudes 91° 48′ 14″ Eto91°32′ 45″ E. This is the sea port, paper industries, oil refinery industries, steel southeastern principal seaport region of the country, rerolling, fertilizer industry, hatcheries, aquafarms, fish straddling the hills at the estuary of the processing industries, leather industries, dyeing indus- River which are regarded as industrial and commercial tries, and paint industries. The basic information of sam- hubs. There are more than 8542 industrial establishments pling sites is presented in Table S1. dealing with cement clinker, fertilizers, steel rerolling, paper and pulp, rubber and plastic, oil refinery, bever- Sample collection and preparation ages, sugar, pharmaceuticals, tobacco, jute, textiles, fish processing, tannery, paint, rechargeable batteries, jewel- Threemostlyconsumedfish(Hilsa(Tenualosa ilisha), ry, plating, automobile engine, electronic industries, and Rupchanda (Pampus argentius), Long tongue sole ship breaking yard (BOBLME, 2011). The third site (St (Cynoglossus lingua)) and crustacean species (Indian shrimp 3) is located near the Meghna Estuary in Bhola which (Penaeus indicus)andMudcrab(Scylla serrata)) were col- lies between latitudes 22° 28′ 07″ N to 22° 20′ 39″ N lected from the sampling sites. Immediately after collection, and longitudes 90° 49′ 41″ E to 90° 50′ 31″ E. This is an fish and crustacean samples were kept in airtight insulating estuarine area where the main rivers mix together to the box and thereafter transported to the laboratory of the Bay of Bengal containing the industrial effluents through Department of Fisheries, University of Dhaka, Bangladesh. inland rivers from the country and trans-boundary coun- After transportation, fish and crustaceans samples were rinsed tries. The last site (St 4) is located near the southwest in deionized water to remove surface adherents. Nonedible part of the coastal area of Sundarbans that is regarded as parts were removed with the help of a steam cleaned stainless a large mangrove ecosystem in Bangladesh which lies steel knife. The edible portion of the samples was cut into between latitudes 22° 34′ 43″ Nto22°18′ 02″ Nand small pieces. A composite of at least 9 samples of each fish longitudes 89° 32′ 48″ Eto89°36′ 26″ E. This sampling and crabs, and 18 for shrimps was prepared and homogenized area is also mostly influenced by different industrial in a food processor and 100 g test portions were stored at Environ Sci Pollut Res

−20 °C in the Laboratory of Fisheries Department, Dhaka evaluated using an internal quality approach and validated if University. Then, all samples were freeze-dried for 48 h until they satisfied the defined Internal Quality Controls (IQCs). constant weight was attained. The all processed samples were For each batch experiment, one blank, one certified reference brought to Yokohama National University, Japan, for chemi- material (CRM) and several samples were analyzed in dupli- cal analysis under the permission of Yokohama Plant cate to eliminate any batch-specific error. Finally, the concen- Protection Station. tration of trace metals were quantified by calibration based on internal standards. Sample digestion and metal extraction Quality control and quality assurance A microwave digestion was used to digest the samples for analysis. All chemicals were analytical grade reagents, and The quality of total acid digestion of the fish and crustaceans Milli-Q (Elix UV5 and Milli-Q Adv.A10, Millipore, USA) was checked by using a certified reference material (NMIJ water was used for each solution preparation. The CRM 7402-a, Cod fish tissue) purchased from the National polytetrafluoroethylene (PTFE) digestion vessels and poly- Institute of Advanced Industrial Science and Technology propylene containers were cleaned, soaked in 5 % HNO3 for (AIST) and yielded a good accuracy of the analysis. The cer- more than 24 h, then rinsed with Milli-Q water and dried. For tified and analyzed values of trace metals of CRM 7402-a are metal analysis, 0.2 g of fish and crustaceans samples of each shown in Table 2. The comparison is made with the certified were treated with 5 mL 69 % HNO3 acid (Kanto Chemical values, which in both cases confirmed that the sample prepa- Co., Tokyo, Japan) and 2 mL 30 % H2O2 (Wako Chemical ration and instrumentation conditions provided good levels of Co., Tokyo, Japan) in closed digestion vessels. After mixing accuracy and precision. for 20 min, the vessels containing samples were placed in a microwave digestion system (Berghof-MWS2, Berghof Health risk calculations speedwave®, Germany). The following microwave program was applied: 10 min at 180 °C with 800 W, 10 min at 190 °C Estimated daily intakes with 900 W, and as a last step 10 min at 100 °C with 400 W. After digestion, acid solutions with samples were transferred Estimated daily intakes (EDIs) for the analyzed trace metals into a Teflon graduated cylinder and total volume was made were calculated by multiplying the respective average concen- up to 50 mL with Milli-Q water. The digested acid solutions tration in composite fish and crustaceans samples by the av- were then filtered by using syringe filter (DISMIC®-25HP erage weight of consumption per day dividing by the average μ PTFE, pore size = 0.45 m; Toyo Roshi Kaisha, Ltd., Tokyo body weight of Bangladeshi coastal people (which was ob- Japan) and stored in 50 mL polypropylene tubes (Nalgene, tained from survey data). Metal concentration in fish was ob- NY, USA). tained on the basis of wet weight (ww). EDI were calculated by the following equation: Instrumental analysis . . X FIR Â C EDI μg kg‐bw day ¼ i i For trace metals, samples were analyzed using inductively i WAB coupled plasma mass spectrometer (ICP-MS, Agilent 7700 series, USA, Table 1). Multi-element Standard XSTC-13 where FIRi is the food (fish and crustaceans) ingestion rate (SPEX CertiPrep®, USA) solutions were used to prepare a (77 and 21 g/person/day for adults respectively); Ci is the calibration curve. The calibration curves with R2 > 0.999 were metal concentration in fish and crustaceans (μg/g ww); WAB accepted for concentration calculation. Before starting the se- is the average body weight (59 kg for adults); and i is the food quence, relative standard deviation (RSD < 5 %) was checked item (fish and crustaceans). by using tuning solution (1 μg/L each of Li, Y,Ce, Tl, Mg, and

Co in 2 wt % HNO3) purchased from Agilent Technologies. Carcinogenic health hazard Internal calibration standard solution containing 1.0 mg/L each of beryllium (Be) and tellurium (Te), and 0.5 mg/L each In this study, the carcinogenic health risks related with the of indium (In), yttrium (Y), cobalt (Co), and thallium (TI) was consumption of fish and crustacean’s species were measured purchased from SPEX CertiPrep®, USA, and it was added based on the target cancer risk (TR) or the risk of cancer over a into each sample. Working standards (0, 10, 20, 50, and lifetime. For carcinogens, risks were estimated as the incre- 100 μg/L) were prepared by dilution of a multi-element stock mental probability of an individual to develop cancer over a solution (Custom Assurance Standard, SPEX CertiPrep®, lifetime exposure to that potential carcinogen (i.e., incremen- USA), then the concentrations of trace metals were deter- tal or excess individual lifetime cancer risk) (USEPA 1989). mined by an internal standard method. All test batches were Acceptable risk levels for carcinogens range from 10−4 (risk of Environ Sci Pollut Res

Table 1 Operating conditions for ICP-MS and parameters for metal Operating conditions analysis Nebulizer pump (rps) 0.1 Radio frequency (RF) power (W) 1550 Radio frequency (RF) 27.12 MHz Sample depth (mm) 9 mm from load coil Plasma gas flow rate (L/min) 15 Make up gas flow rate Ar 0 L/min Carrier gas (Ar) flow rate (L/min) 1.0 (optimized daily) Collision gas mode He 4.0 mL/min Measurement parameters Scanning mode Peak hop Resolution (amu) 0.7 Readings/replicate 1 No. of replicates 3 Correction equations for interferences Li [6]: [6]*1 − [7]*0.082 In [115]: (115)*1 − [118]*0.014 Pb [208]: [208]*1 + [206]*1 + [207]*1 Isotopes 52Cr, 60Ni, 63Cu, 65Zn, 75As, 111Cd, 208Pb

developing cancer over a human lifetime is 1 in 10,000) to Results and discussion 10−6 (risk of developing cancer over a human lifetime is 1 in 1, 000,000). The equation used for estimating the target cancer Trace metals concentration in fish and crustaceans risk (lifetime cancer risk) is as follows (USEPA 1989), X In this study, the trace metal concentrations were determined EF  ED  FIRi  Ci  CSFo on a wet weight basis in the composite commercially impor- ¼ i  : tant fishes and crustacean species which were widely con- TR  0 001 WAB TA sumed by Bangladeshi coastal people. Mean metal concentra- where TR represents the target cancer risk or the risk of cancer tions in fishes and crustaceans are shown in Table 3. over a lifetime (dimensionless); EF is the exposure frequency (365 days/year); ED is the exposure duration (60 years for Trace metals concentration in fish Bangladesh), equivalent to the average lifetime; FIR is the fish and crustaceans ingestion rate (77 and 21 g/person/ day for Awide range of metal concentrations were observed among the adults, respectively); C is the metal concentration in fish and sampling sites. Trace metals in fish were ranged over following crustaceans (μg/g ww); i is the food item (fish and crusta- intervals: Cr 0.15–2.2; Ni 0.1–0.6; Cu 1.3 − 14; Zn 31–138; As ceans); WAB is the average body weight (59 kg for adults); 0.8–13; Cd 0.03–0.09; Pb 0.07–0.63 mg/kg ww. The mean TA is the averaging exposure time (365 days/year × ED); and concentration of studied metals in fish followed a decreasing CSFo is the oral carcinogenic slope factor from the Integrated order of Zn>Cu>As>Cr>Pb>Ni>Cd. Mostfish samples Risk Information System (USEPA 2010)database(1.5(mg/ showed highest mean concentration of metals at Cox’s Bazar − − kg/day) 1 for As and 0.0085 (mg/kg/day) 1 for Pb). site while the samples of fish collected at Sundarbans and

Table 2 Analysis of trace metals from certified reference materials Metal Certified value (mg/kg dw) Measured value (mg/kg dw) Average recovery (%) (NMIJ CRM 7402-a cod fish (n =3) tissue) by ICP-MS (mean ± SD, mg/kg dw) Cr 0.72 ± 0.09 0.76 ± 0.08 106 Ni 0.38 ± 0.05 0.40 ± 0.02 105 Cu 1.25 ± 0.07 1.14 ± 0.05 91 Zn 21.3 ± 1.50 20.5 ± 1.94 96 As 36.7 ± 1.80 38.3 ± 1.73 104 Environ Sci Pollut Res

Table 3 Mean (± SD) metal concentrations (mg/kg ww) in fish and crustaceans (composite samples) collected from Bangladeshi coast

Sampling sites Sample Cr Ni Cu Zn As Cd Pb

Cox’s Bazar Fish Mean 2.2 0.56 14 138 13 0.075 0.63 SD 1.80 0.57 16.2 87.3 15.5 0.05 0.46 Shrimp Mean 1.1 1.3 13 131 2.5 0.086 0.38 SD 0.04 0.06 1.1 3.60 1.4 0.01 0.12 Crabs Mean 29 43 400 1480 53 8.27 67.84 SD 12 15.3 28.8 24.3 4.6 2.19 6.87 Chittagong port Fish Mean 1.1 0.51 5.9 53 2.7 0.06 0.51 SD 1.2 0.48 6.7 27.3 1.5 0.06 0.34 Shrimp Mean 1.0 1.4 22 107 2.0 0.12 0.31 SD 0.3 0.4 3.0 1.4 1.1 0.02 0.17 Crabs Mean 14 34 305 902 34 4.2 78.54 SD 3.0 9.12 4.7 14.3 7.3 2.20 12.12 Sunderbans Fish Mean 0.15 0.1 1.3 31 1.1 0.033 0.07 SD 0.05 0.04 1.07 9.2 0.95 0.05 0.09 Shrimp Mean 0.34 0.49 63 53 0.92 0.022 0.10 SD 0.20 0.10 20.0 11.2 0.22 0.01 0.09 Crabs Mean 0.48 1.4 80 157 1.3 0.094 0.49 SD 0.18 0.4 12.5 13.9 0.20 0.02 0.18 Meghna estuary, Bhola Fish Mean 0.32 0.28 1.6 34 0.76 0.051 0.25 SD 0.16 0.11 0.44 8.8 0.78 0.06 0.19 Shrimp Mean 0.17 0.77 52 114 0.30 0.097 0.13 SD 0.06 0.11 14.00 8.6 0.17 0.02 0.05 Crabs Mean 0.29 0.81 111 137 1.5 0.19 0.24 SD 0.10 0.12 1.73 6.0 0.27 0.09 0.06

Composite samples: For each site, 9 samples of each fish and crabs and 18 for shrimps were homogenized in a food processor to prepare composite samples having three replicates of each mg/kg ww milligrams/kilogram wet weight basis Bhola showed lowest metals concentration. Among the metals, Zinc is known to be involved in most metabolic pathways the highest mean concentrations of Zn (138) and As (13 mg/kg in humans, and its deficiency can lead to loss of appetite, ww) were observed at Cox’s Bazar site which exceeded the growth retardation, skin changes, and immunological abnor- international quality guideline values (Table 4). malities (Tuzen 2009). The lowest and highest Zn content in

Table 4 Standard levels of metals in fish in (mg/kg ww) described in the literature and range of concentrations found in fishes and crustaceans in coastal area of Bangladesh

Cr Ni Cu Zn As Cd Pb References

Bangladesh coast Fish 0.15–2.2 0.1–0.6 1.3–14 31–138 0.8–13 0.03–0.09 0.07–0.63 Present study Shrimp 0.32–1.1 0.28–1.4 13–63 53–131 0.3–2.5 0.02–0.12 0.1–0.38 Present study Crab 0.29–29 0.49–43 80–400 137–1480 1.3–53 0.084–8.3 0.24–79 Present study Guidelines New Zealand 30 40 1 1 2 CEPA,1995-97a Hong Kong 1.4 2 6 CEPA,1995-97a Zambia 100 100 5 10 CEPA,1995-97a Tolerance level in fish 50 0.1 0.5 FAO/WHO, 1989 Turkish 20 50 0.1 0.3 Turkish Food Codex (Anonymous, 2008) mg/kg ww milligrams/kilogram wet weight basis a California Environmental Protection Agency, State Water Resources Control Environ Sci Pollut Res fish were found as 31 mg/kg ww in Sundarbans and 138 mg/ Chronic exposure to arsenic can lead to dermatitis, mild pig- kg ww in Cox’s Bazar site. Zinc contents in the literature have mentation keratosis of the skin, decreased nerve conduction been reported in the range of 42.8–418 mg/kg ww in some velocity, and lung cancer (Occupational Safety and Health edible fishes in Bangladesh (Rahman et al. 2012) and 38.8– Administration 2004). However, as only about 10 % of the 93.4 mg/kg ww in some fish species from the Black Sea, As present in fish is in inorganic form, only this percentage Turkey (Tuzen 2009). Other literatures have been reported in was used to calculate hazard (Buchet et al. 1996). The lowest the range of 0.60–11.57 mg/kg ww in fish species which were concentration of arsenic in fish was observed as 0.76 mg/kg collected from the Iskenderun Bay, Turkey (Turkmen et al. ww in Bhola site while the highest concentration was ob- 2005). The high Zn concentration at Cox’s Bazar site might served as 13 mg/kg ww in Cox’s Bazar site which has been be attributed to the discharge of different salts and chemicals exceeded the international quality guideline values (Table 4). from hatcheries and fish processing industries where zinc ox- In some literature, the arsenic concentration has been reported ide (ZnO) was broadly used for the oxygen supply to fry and in the range of 1.01–15.2 mg/kg ww in Bangladeshi freshwa- fingerlings (Shamsuzzaman and Biswas 2012). Besides, most ter fish species (Shah et al. 2009). According to Tuzen (2009), of the domestic sewages of Cox’s Bazar city were incorporat- the range of As level was found as 0.11–0.32 mg/kg ww in ed to the Bakkhali River through different uncontrolled canals fish species from the Black Sea, Turkey. Other literatures have to the Sea. The biggest fishery landing center was located in been reported in the range of 12.6–190 mg/kg ww in fish and this site and all poisonous effluents were directly discharged shellfish samples proposed by Lavilla et al. (2008). The con- into the river without treatment. Along the banks of this river, centration range 0.02–0.04 mg/kg ww was also found in fish a dock yard has been recently developed to repair fishing and sample which was proposed by Das et al. (2004). Compared trawling boats. Waste discharge and chemical spills associated with published data, the total As was found in muscles ranging with boat repairing industries represent an additional source of from 0.39 to 12.58 mg/kg ww in fish collected from the south- pollutants to the water and sediments. Moreover, galvanizing east Spain (Delgado-Andrade et al. 2003). De Rosemond et al. steel, ship repairing, painting, textile and dyeing, and rubber (2008) observed a range of 0.57 to 1.15 mg/kg ww for total industries also contribute significant amount of Zn in this area. arsenic in muscles of five freshwater fish species collected Considering ship repairing, painting, and coating, a huge from the Back Bay near Yellowknife, NT, Canada. amount of commercial paints containing zinc oxide (ZnO) According to the New Zealand food safety standard and zinc sulfide (ZnS) have long been used as anticorrosive (Table 4), the maximum arsenic level permitted for fish sam- coatings in different type of boats, fishing trawlers, and ships ples is of 1.0 mg/kg ww. Food and Agriculture Organization in Cox’s Bazar and Chittagong coast to protect wood and steel (FAO), especially the Regional Office for Asia and the Pacific, structures under normal atmospheric conditions, as well as to has recommended a concentration of 0.126 mg/day as a pro- underwater steel surfaces of these water vehicles. Zinc oxide visional maximum tolerable daily intake for ingested arsenic is also used to retain their flexibility and adherence on such (FAO 2006). surfaces for many years and using component in many formu- Copper is essential for good health, but very high intake lations of durables and protective paints. Besides, the rubber can cause adverse health problems such as liver and kidney industry in general, and tire manufacturers in particular, are damage (Ikem and Egiebor 2005). The highest concentration the largest users of ZnO. It is utilized to activate the organic of copper was found in fish as 14 mg/kg ww at Cox’s Bazar accelerator, serves as an effective co-accelerator in the vulca- site while lowest content was found as 1.3 mg/kg ww in nization process, and inhibits the growth of fungi, with suffi- Sundarbans site. Copper levels in the literature have been cient stability, as part of the production process of latex foam reported in the range of 5.17–9.45 mg/kg ww in fish from rubber products. Dhaleshwari River, Bangladesh (Ahmed et al. 2009). In the Arsenic is particularly difficult to characterize as a single other literature, copper levels have been reported in the range element because its chemistry is really complex. Arsenic oc- of 0.11–0.97 mg/kg ww in Northeast Atlantic (Celik and curs in three oxidation states: trivalent arsenite (As(III)), pen- Oehlenschlager 2004) and 0.04–5.43mg/kgwwinthe tavalent arsenate (As(V), and elemental. Arsenite is ten times Iskenderun Bay, Turkey (Turkmen et al. 2005). In this study, more toxic than arsenate; elemental arsenic is nontoxic in comparison to the international guideline, the concentration (Sharma et al. 2014). Naturally, As in seafood exists in two of copper was within safe limit (Table 4). forms: inorganic and organic (arsenobetaine, arsenocholine, The range of Cr level was found as 0.15–2.2 mg/kg ww and organoarsenicals). Although seafood contains a high con- which is within the legal limits. The lowest content was found centration of organic arsenic, it is much less toxic than inor- as 0.15 mg/kg ww in Sundarbans site while the highest con- ganic arsenic (Han et al. 1998, Sharma et al. 2014) and can be tent was found as 2.2 mg/kg ww in Cox’s Bazar. Chromium efficiently and rapidly excreted in urine without transforma- contents in the literature have been reported in the range of tion (Han et al. 1998). Conversely, it is suspected that inor- 0.07–6.46 mg/kg ww in fish species from Iskenderun Bay, ganic As present in fish consumed by humans is carcinogenic. Turkey (Turkmen et al. 2005). The range of Cr level was also Environ Sci Pollut Res found as 0.04–1.75 mg/kg ww in seafood from Marmara, other synthetics (Sharma et al. 2014). Cadmium is a highly Aegean, and Mediterranean seas in Turkey (Turkmen et al. toxic metal with a natural occurrence in the soil, but it is also 2008). Besides, the range of Cr as 0.47–2.07 mg/kg ww in spread in the environment due to human activities. Cadmium some edible Bangladeshi fishes were also reported (Rahman may accumulate in the human body and may give rise to renal, et al. 2012). Other authors also found some Cr concentrations pulmonary, hepatic, skeletal, reproductive effects, and cancer in edible tissue of Silurus glanis which was in the range of (Zhu et al. 2011). It also causes osteoporosis, anemia, 0.80–1.40 mg/kg ww (Mendil and Uluzlu 2007)and0.11– nonhypertrophic emphysema, irreversible renal tubular injury, 0.23 mg/kg ww (Matasin et al. 2011), respectively. eosinophilia, anosmia, and chronic rhinitis (Sharma et al. However, the content of chromium in food is of great impor- 2014). The highest cadmium content in fish species were tance as it is involved in insulin function and lipid metabolism found as 0.075 mg/kg ww which is close to the literature of the body (Bratakos et al. 2002). reported concentrations of 0.05 mg/kg ww in fish (Tuzen Lead is another ubiquitous toxic metal detectable practical- et al. 2009). In the literature, cadmium levels in fish have been ly in all phases of the inert environment and biological sys- reported in the range of 0.51–0.73 mg/kg dw in fish samples tems. It is frequently used in the production of batteries, metal from Dhaleshwari River, Bangladesh (Ahmed et al. 2009). products, ammunition, and devices to shield X-rays (Sharma The European Community legislation has recommended a et al. 2014). Lead is a nonessential element, and it is well maximum Cd level of 0.05 mg/kg ww in fish (EC documented that it can cause neurotoxicity, nephrotoxicity, Regulation 2001). Besides, the Codex Committee on Food and many other adverse health effects (Garcia-Leston et al. Additives and Contaminants recommends 0.5 mg/kg ww in 2010). This neurotoxicity was later found to be associated fish (Ikem and Egilla 2008). with lead-induced production of ROS which caused increase or decrease in the levels of lipid peroxidation or antioxidant Trace metal concentration in crustaceans defense mechanisms in the brain (Sharma et al. 2014). However, in this experiment, the lowest concentration of Pb The concentration ranges of trace metals in crustaceans (shrimp) in fish was observed as 0.07 mg/kg ww in Sundarbans site were as follows: Cr 3.2–1.1; Ni 0.28–1.4; Cu 13–63; Zn 53–131; while the highest concentration was observed as 0.63 mg/kg As 0.3–2.5; Cd 0.02–0.12; Pb 0.1–0.38 mg/kg ww. According to ww in Cox’s Bazar which was close to the literature reported these data in shrimp, zinc had the highest concentration and concentrations of 0.026–0.481 mg/kg ww (Morgano et al. followed by copper, arsenic, nickel, chromium, cadmium, and 2011). Lead content in the literature has been reported in the lead. Otherwise, trace metals in crustaceans (crabs) ranged over range of 0.09–6.95 mg/kg dw in fish species from Iskenderun following intervals: Cr 0.29–29;Ni0.49–43; Cu 80–400; Zn Bay, Turkey (Turkmen et al. 2005). Moreover, another litera- 137–1480; As 1.3–53; Cd 0.084–8.3; Pb 0.24–79 mg/kg ww. ture has been reported in the range of 1.76–10.27 mg/kg ww The mean concentrations of studied metals in crabs followed a in some edible fishes of Bangladesh (Rahman et al. 2012). decreasing order of Zn > Cu > Pb > As > Ni > Cr > Cd. Regarding Pb, the maximum concentration limit of Pb was Remarkably, most of the studied metals in crustaceans showed proposed by the European Community as 0.2 mg/kg ww in the highest mean concentration at Cox’s Bazar site which fish (EC Regulation 2001). exceeded the international quality guideline (Table 4). Nickel normally occurs at very low levels in the environ- Comparing crustaceans, crab had the higher mean contents of ment, and it can cause a variety of pulmonary adverse health most metals. Crab is a typical benthic organism that resides effects, such as lung inflammation, fibrosis, emphysema, and above or in the sediment that might be good indicators reflecting tumors (Forti et al. 2011). The highest nickel concentration in the contamination levels in surface sediment (Ololade et al. fish was found as 0.56 mg/kg ww in Cox’s Bazar which was 2011). Unlike fish skin, crab legs are often buried in surficial within the guideline limits. Nickel concentration in the litera- sediments and might adsorb metals from sediment more easily. ture has been reported in the range of 0.02–3.97 mg/kg ww in Thus, it is more susceptible to sediment and is expected to pos- seafood from Marmara, Aegean, and Mediterranean seas sess high metal levels (Zhao et al. 2012). Besides, crabs has (Turkmen et al. 2008). Other literature showed the range of capability of accumulating more trace metals by the hepatopan- 0.11–12.88 mg/kg ww in fish species from the Iskenderun creas, one of the most important organs that play important roles Bay (Turkmen et al. 2005). A concentration range of 2.94– in metal detoxification (Reinecke et al. 2003;Wangetal.2001). 46 mg/kg ww in fish and shellfish samples were also reported Mean concentrations of most metals in crabs were significantly by Lavilla et al. (2008). The World Health Organization has higher than those in fishes, indicating that high metal levels in recommended a range of 100–300 mg/kg bw/day for daily sediment might have resulted in the enrichment of metals in nickel intake (WHO 1994). crabs. Moreover, crab is known as a scavenger that tends to feed Cadmium poisoning is an occupational hazard associated on detritus which is the most contributing factor to the high with industrial processes such as metal plating and the pro- pollution in crabs (Ip et al. 2005). Unlike benthic fishes, crabs duction of nickel-cadmium batteries, pigments, plastics, and often bury themselves in the sediments, making them closer to Environ Sci Pollut Res sediments and thus expose to higher concentration and more during a lifetime. It is useful as a reference point from which to metal species (Zhao et al. 2012). It can be seen that perceptibly gauge the potential effects of the chemical at other doses. elevated levels of Zn (1480 mg/kg ww) and Cu (400 mg/kg ww) Usually, doses less than the RfD are not likely to be associated were found in crabs (Table 3) which can be explained by the facts with adverse health risks and are therefore less likely to be of that the two metals are necessary elements to meet crab’s phys- regulatory concern. As the frequency and/or magnitude of the iological needs and most of crab’s food (e.g., debris or small exposures exceeding the RfD increase, the probability of ad- benthic organism) had high accumulation of these metals. verse effects in a human population increases. However, it However, crab gill is an organ responsible for breathing and should not be categorically concluded that all doses below regulating permeation pressure and ionic equilibrium. Because the RfD are Bacceptable^ (or will be risk free) and that all of its functional characteristics and large surface area, it often doses in excess of the RfD are Bunacceptable^ (or will result contains high concentrations of metals (Zhao et al. 2012). in adverse effects) (US EPA 2008). There are several ap- However, it is difficult to conclude which pathways (e.g., dermal proaches of human exposure to trace metals such as breathing exposure or breathing or complicated food sources) are contrib- and dermal exposure. However, food consumption is often uting more bioaccumulation and biotransformation in crabs’ regarded as one of the most important approaches. body as few literatures are mentioned in this regard. Some studies Considering fish, except for As, the average EDIs of metals reported that the dermal contact through appendages and chest in fish was below the RfDs (Fig. 2) indicating that average region contribute higher metal concentration in crabs’ body as consumption of fish in the coastal area would not result in legs and chest are often submerged in upper part of sediments health risk. But, dietary intakes of As exceeded the RfDs (Falusi and Olanipekun 2007). through consumption of fish which was mainly ascribed to the fact that high concentrations of As can produce toxic Health risk assessment effects. Hence, excessive ingesting of fish should be avoided to Estimated daily intakes minimize the harmful effects caused by As accumulation. Besides, except for Zn and Ni, the average EDIs of most EDIs of selected toxic trace metals from fish and crustaceans metals (As, Pb, Cu, Cr, and Cd) in crustaceans exceeded the consumption by average Bangladeshi coastal adults are pre- RfDs (Fig. 2) indicating that average consumption of crusta- sented in Tables 4 and 5. The oral reference dose (RfD) was ceans would result in severe health risk. In Bangladesh con- used in this study to evaluate the EDIs of metals in fishes. text, shrimp is very popular, expensive, and emblematic of RfDs are based on 3, 20, 40, 300, 0.3,1 and 3.5 μg/kg bw/ Bangladeshi cuisine. Coastal people are used to consume day for Cr, Ni, Cu, Zn, As, Cd, and Pb, respectively (USEPA more as it is readily available in local area. Besides, due to 2008). The RfD represents an estimate of the daily exposure to religious prohibition, eating crabs is not so popular in all over which the human population may be continually exposed over the country even though they have high commercial value in a lifetime without a considerable risk of deleterious effects. In the world market to earn foreign exchange (Azam et al. 1998). general, the RfD represents an estimate (with uncertainty Nevertheless, millions of poor coastal fishers, traders, and spanning perhaps an order of magnitude) of a daily exposure rural ethnic people are directly or indirectly dependent on this to the human population (including sensitive subgroups) that crab fishery (Zafar 2004; Patterson and Sainuel 2005). is likely to be without an appreciable risk of deleterious effects Therefore, excessive consumption of crustaceans in this

Table 5 Estimated daily intake (EDI) and target cancer risk (TR) of trace elements due to consumption of some commercial fishes and crustaceans collected from Bangladeshi coast

Metals Mean concentration (μg/g ww) Estimated daily intake (EDI) (**μg/kg-bw/day) RfD (μg/kg bw/day) Estimated target cancer risk (TR)

Fish Crustaceans Fish Crustaceans Total seafoods Total seafoods

Cr 0.93 11.6 1.2 4.1 5 3 Ni 0.36 20.8 0.5 7.4 8 20 Cu 5.70 261.4 7.4 93 100 40 Zn 64.1 770.2 83.6 274 358 300 As 4.25 23.6 5.6 8.4 14 0.3 0.02 Cd 0.05 3.3 0.07 1.2 1 1 Pb 0.36 37.0 0.5 13 14 3.5 0.0001

RfD oral reference dose (RfD) proposed by USEPA 2008, μg/kg bw/day micrograms/kilogram body weight/day basis Environ Sci Pollut Res

-Blue dot lines (------) are marked as RfD.

Fig. 2 Bar graph showing estimated daily intake (EDI) of selected toxic trace metals from fish and crustaceans (seafood) consumption by average Bangladeshi coastal adults in comparison with oral reference dose (RfD) (USEPA 2008) Environ Sci Pollut Res coastal area should be avoided to prevent the detrimental ef- exposure in men can damage the organs responsible for fects triggered by As, Pb, Cu, Cr, and Cd accumulation. In sperm production (Martin and Griswold 2009). In pregnant addition, a difference of metal levels and EDI among the areas women, lead may cause miscarriage. Therefore, the poten- should be considered. For example, the EDI levels of most tial health risk for the coastal people due to metal exposure metals specially Cr, Zn, and As in fish and crustaceans from through fish and crustaceans (seafood) consumption should Cox’s Bazar site were higher than those from Sundarbans and not be ignored. Moreover, there are also other cradles of Bhola and sometime Chittagong area (Table 6). Therefore, metal exposures, such as consumption of other contaminat- people in Cox’s Bazar may be exposed to higher levels of ed foods and dust inhalation, which were not encompassed some metal contaminations than people living in the other area in this study. It is thus proposed that continuous monitoring of Bangladeshi coast. of these toxic trace elements in all foodstuffs are needed to evaluate if any impending health risks of the study area do exist. Carcinogenic health hazard

The target lifetime carcinogenic risk (TR) of As and Pb due to exposure from seafood consumption are listed in Table 5. Conclusions The TR values for As and Pb from seafood consumption were 2 × 10−2 and 1 × 10−4, respectively. In general, the ex- This study was developed to provide baseline information cess cancer risk lower than 10−6 are considered to be negli- on the concentrations of some toxic trace metals in com- gible, cancer risk above 10−4 are considered unacceptable, mercial fish and crustaceans of coastal areas of and risks lying between 10−6 and 10−4 are generally consid- Bangladesh. Among the four sites studied, fishes of ered an acceptable range (USEPA 1989; 2010). The carci- Cox’s Bazar site were more contaminated by trace metals. nogenic risk for Pb was close to the unacceptable range, Arsenic and Zn concentration were remarkably high in whereas that of As was higher than the unacceptable value fishes and crabs collected from Cox’s Bazar. Crabs were (10−4). According to the USFDA (1993), about 90 % of the more susceptible to possess higher metal accumulation As exposure occurs from the seafood. Multiple health im- than other fishes due to its absolute different bioaccumu- plications have been associated with As exposure. Inorganic lation pattern. Some metals in fish and crustaceans arsenic is a known carcinogen and can cause cancer of the exceeded the international quality guidelines. Estimated skin, lungs, liver, and bladder. Cardiovascular disease daily intake (EDI) and target cancer risk (TR) revealed (CVD) for instance, is observed in the areas of endemic high dietary intake of As and Pb, which was obviously As exposures (Cheng et al. 2010). Besides, EPA has deter- a matter of severe public health issue of Bangladeshi mined that lead is a probable human carcinogen. Long-term coastal people which should not be ignored and concen- exposure can result in decreased performance of nervous trate our views to solve this problem with an integrated system. Exposure to high lead levels can severely damage approaches. Thus, continuous monitoring of these toxic the brain, liver, and kidneys and ultimately cause death (Lee trace elements in seafood and immediate control measure et al. 2011; Luckey and Venugopal 1977). High-level is recommended.

Table 6 Site-specific estimated daily intake (EDI) of selected toxic trace metals from fish and crustaceans (seafood) consumption by average Bangladeshi coastal adults in comparison with oral reference dose (RfD) (USEPA, 2008) (μg/kg bw/day)

Sampling sites EDI Cr Ni Cu Zn As Cd Pb

Cox’s Bazar Fish 3.1 0.8 20.0 199.1 18.0 0.11 0.9 Crustaceans 10.7 15.9 146.9 573.3 19.6 2.97 24.3 Chittagong port Fish 1.5 0.7 8.2 73.3 3.7 0.08 0.7 Crustaceans 5.7 13.5 124.8 384.2 13.6 1.65 30.0 Meghna estuary, Bhola Fish 0.4 0.3 2.0 41.7 0.9 0.06 0.3 Crustaceans 0.3 0.6 46.6 68.7 0.7 0.04 0.2 Sunderbans Fish 0.2 0.1 1.6 37.4 1.3 0.04 0.1 Crustaceans 0.2 0.5 54.2 83.9 0.6 0.10 0.1 RfD (USEPA 2008) 3 20 40 300 0.3 1 3.5

Consumption of seafood—Average fish and crustacean’s (seafood) ingestion rate of Bangladeshi coastal people of were 77 and 21 g/person/day for adults, respectively, which was obtained from survey data. Metal concentration data of fish and crustaceans were adopted from Table 3 Environ Sci Pollut Res

Acknowledgments The authors would like to acknowledge the Program Data Report.AppendixV,http://www.swrcb.ca.gov/ Graduate School of Environment and Information Sciences, Yokohama programs/smw/smw9597.html. National University, Japan, for providing research grant through the Erdoğrul Ö, Erbilir F (2007) Heavy metal and trace elements in various International Environmental Leadership Program in Sustainable Living fish samples from Sir Dam Lake, Kahramanmaraş, Turkey. Environ with Environmental Risk (SLER) and through research cooperation pro- Monit Assess 130:373–379 gram for Ph. D students. The authors also would like to convey special EU, European Union. Commission of the European Communities (2001) thanks and gratitude to the Setsutaro Kobayashi Memorial Fund by Fuji Commission regulation (EC) n. 221/2002 of the 6 February 2002 Xerox Co., Ltd., Japan, for the financial assistance of this research. The amending regulation (EC) n. 466/2002 setting maximum levels for authors also thankfully acknowledge the Yokohama Plant Protection au- certain contaminants in foodstuffs, Official Journal of the European thority of Japan for the import permission of the sediment samples from Communities. Brussels (2002), 6 February Bangladesh (MAFF Directive Import Permit No. 25Y324, date of issue: Falusi BA, Olanipekun EO (2007) Bioconcentration factors of heavy June 11, 2013). metals in tropical crab (Carcinus sp.) from River Aponwe, Ado- Ekiti, Nigeria. J Appl Sci Environ Man 11(4):51–54 Compliance with ethical standards FAO (2006) Arsenic contamination of irrigation water, soil and crops in Bangladesh: Risk implications for sustainable agriculture and food Conflict of interest The authors declare that they have no conflict of safety in Asia. . Food and Agriculture Organization of the United interest. 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