RESEARCH ARTICLE

Trace metal contamination in commercial fish and crustaceanscollected from coastal area of Bangladesh and health riskassessment

Mohammad Raknuzzaman1,2& Md Kawser Ahmed3

& Md Saiful Islam4&

Md Habibullah-Al-Mamun1,2& Masahiro Tokumura1 & Makoto Sekine1 &

Shigeki Masunaga1

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

Abstract Trace metals contamination in commercial fish andcrustaceans have become a great problem in Bangladesh. Thisstudy was conducted to determine seven trace metals concen-tration (Cr, Ni, Cu, Zn, As, Cd, and Pb) in some commercialfishes and crustaceans collected from coastal areas ofBangladesh. Trace metals in fish samples were in the range ofCr (0.15−2.2), Ni (0.1−0.56), Cu (1.3−1.4), Zn (31−138),As (0.76−13), Cd (0.033−0.075), and Pb (0.07−0.63 mg/kgwet weight (ww)), respectively. Arsenic (13mg/kgww) and Zn(138 mg/kg ww) concentrations were remarkably high in fishof Cox’s Bazar due to the interference of uncontrolled hugehatcheries and industrial activities. The elevated concentrationsof Cu (400), Zn (1480), and As (53 mg/kg ww) were alsoobserved in crabs of Cox’s Bazar which was considered as anabsolutely discrepant aquatic species with totally different bio-accumulation pattern. Some metals in fish and crustaceansexceeded the international quality guidelines. Estimated daily

intake (EDI) and target cancer risk (TR) revealed high dietaryintake of As and Pb, which was obviously a matter of severepublic health issue of Bangladeshi coastal people which shouldnot be ignored and concentrate our views to solve this problemwith an integrated approaches. Thus, continuous monitoring ofthese toxic trace elements in seafood and immediate controlmeasure is recommended.

Keywords Bangladesh . Tracemetals . Fish . Crustaceans .

Health risk

Introduction

In recent, substantial considerations are being compensated tothe environmental pollution by a variety of chemical contam-inants including the trace metals (Orecchio and Amorello2010). Accumulation of trace metals in aquatic ecosystemshave upstretched public apprehension to all over the worlddue to their high potential to enter and accumulate in foodchains (Ivan et al. 2011; Erdoğrul and Erbilir 2007). Tracemetals are environmentally ubiquitous, freely dissolved andtransported by water, and readily taken up by fish and otheraquatic organisms (Jordao et al. 2002). Fishes are often at thetop of the aquatic food chain, and their normal metabolismmay accumulate some trace metals from food, water, or sedi-ment (Yilmaz et al. 2007; Mansour et al. 2002). Thus, fishesare often used for many years as excellent biomarkers to in-vestigate metal levels in their living environments and to as-sess ecological and health risks posed by anthropogenic wastedischarges (Muiruri et al. 2013; Zhou et al. 2008; Oost et al.2003). Metal accumulation in fish has been evidenced to bepretentious by several factors, e.g., metabolic activities, swim-ming patterns, ecological needs, and living environments.

Responsible editor: Philippe Garrigues

Electronic supplementary material The online version of this article(doi:10.1007/s11356-016-6918-4) contains supplementary material,which is available to authorized users.

* Mohammad Raknuzzamanmohammad-raknuzzaman-jc@ynu.jp

1 Graduate School of Environment and Information Sciences,Yokohama National University, Yokohama, Japan

2 Department of Fisheries, University of Dhaka, Dhaka 1000,Bangladesh

3 Department of Oceanography, University of Dhaka,Dhaka 1000, Bangladesh

4 Department of Soil Science, Patuakhali Science and TechnologyUniversity, Dumki, Patuakhali 8602, Bangladesh

Environ Sci Pollut ResDOI 10.1007/s11356-016-6918-4

Among these factors, living environment is frequently consid-ered to be more important due to its complicated nature andthe heterogeneous tendency of metal distribution (MustafaandGülüzar 2003). Besides, accumulation patterns of contam-inants in fish and other aquatic organisms also depend both onuptake and elimination rates (Hakanson et al. 1988; Guvenet al. 1999). Compared with fishes, crustaceans particularlycrabs, may be considered as an absolutely discrepant aquaticspecies and act as a typical benthic organism andmight also begood indicators reflecting the contamination levels in surfacesediment (Ololade et al. 2011). However, metals from naturaland anthropogenic sources incessantly enter into the aquaticenvironment where they pose a serious threat as a conse-quence of their toxicity, long persistence, bioaccumulation,and biomagnification in the food chain (Papagiannis et al.2004). Thus, trace metal residues in contaminated habitatsmay accumulate in microorganisms, fishes, crustaceans, andother aquatic animals which may enter into the human foodchain and result in health problems (Cook et al. 1990; Guptaet al. 2009).

We are not free from health risks. Modern economicdevelopment has been accelerating environmental pollu-tion which, in turn, becomes a threat to human health.Health risk concerning with trace metals contaminationis regarded as a global crisis. The accumulation of thesetrace elements can cause severe damage to liver, kidney,central nervous system, mucus tissues, intestinal tract,and reproductive systems. Furthermore, to the toxic andcarcinogenic effects of some metals in humans and ani-mals, they also play vital role in mediating a balancedbiological functioning of cells (Sharma et al. 2014).Therefore, the concern is growing more and more seri-ous globally especially in developing countries likeBangladesh (Chen et al. 2011; Wu et al. 2008).Currently, trace metals contamination in fish and crusta-ceans have become a severe issue to the public health ofBangladesh. Bangladesh is a riverine country with alarge marshy jungle coastline of 580 km in the Bay ofBengal. The river Ganges and Yamuna have been one ofthe major recipients of industrial effluents from India(Gupta et al. 2009) entering into Bangladesh as Padmaand Jamuna. The river Padma and the river Jamuna arejoined together in Chandpur forming the Meghna riverwhich dumping up the waste materials through Bholaestuary to the Bay of Bengal. Besides, the rapid inadver-tent industrialization, urban expansion, enormous popu-lation growth, and overall trans-boundary water issuecontribute massive amounts of domestic wastewaterand untreated industrial effluents into the coastal areathrough rivers. These contaminants can be deposited intoaquatic organisms by the effects of bioconcentration,bioaccumulation, and the food chain process. The con-taminants coming through these rivers are accelerating

the coastal water pollution that might contaminate thefish, crustaceans and others aquatic biota which eventu-ally threaten human health through fish and seafood con-sumption. About five million people are engaged incommercial fishing while fish and crustaceans are themajor protein and earning source of the coastal people.The Hilsa (Tenualosa ilisha), Rupchanda (Pampusargentius), Long tongue sole (Cynoglossus lingua),Indian shrimp (Penaeus indicus), and Mud crab (Scyllaserrata) are commercially important edible fishes andcrustaceans which are widely consumed by the commonpeople. The contaminated fish and crustaceans from thecoastal environment may become a public health con-cern in future.

But, in the Bangladesh context, the concerned author-ities and general people have not been aware and nocomplete study has been carried out so far regarding thisissue. So, it is important to determine the concentrationsof trace metals in commercial fishes and crustaceans con-sidering possible health risk of coastal people throughfish consumption. Furthermore, it is important to observethe level of trace metals in consumed fishes to get someconcepts regarding the safety of fish and seafood proteinsupplied to the consumers. Thus, the objective of thisstudy is extensively involved on health risk assessmentof coastal people of Bangladesh, based on certain tracemetals (Cr, Ni, Cu, Zn, As, Cd, and Pb) contaminationand their spatial and temporal distribution in some com-mercial fishes, crustaceans along with environmentalmedia.

Materials and methods

Study area and sampling location

Four sampling sites (Cox’s Bazar, Chittagong, MeghnaEstuary, and Sunderbans) with three different locationsof each were investigated in the southeast and southwestcoastal area of Bangladesh (Fig. 1). The first site (St 1)is located at the southeast coastal area in Cox’s Bazaarwhich lies between latitudes 21° 27′ 02″ N to 21° 26′33″ N and longitudes 91° 58′ 16″ E to 91° 57′ 01″ E.Cox’s Bazar was a seaside tourist town with an unbroken125 km world’s longest natural sandy sea beach. Coastalshrimp culture has been widely practiced in this coastsince a couple of decades where more than 53 shrimphatcheries and aquafarms, big fish landing centers can befound in very close relation to the sea beach. Besides,these sampling areas were mostly influenced by un-planned industries, huge hotels for tourists, and munici-pal sewages. The second site (St 2) is located near theChittagong port and ship breaking area which lies

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between latitudes 22° 13′ 27″ N to 22° 38′ 22″ N andlongitudes 91° 48′ 14″ E to 91° 32′ 45″ E. This is thesoutheastern principal seaport region of the country,straddling the hills at the estuary of the KarnaphuliRiver which are regarded as industrial and commercialhubs. There are more than 8542 industrial establishmentsdealing with cement clinker, fertilizers, steel rerolling,paper and pulp, rubber and plastic, oil refinery, bever-ages, sugar, pharmaceuticals, tobacco, jute, textiles, fishprocessing, tannery, paint, rechargeable batteries, jewel-ry, plating, automobile engine, electronic industries, andship breaking yard (BOBLME, 2011). The third site (St3) is located near the Meghna Estuary in Bhola whichlies between latitudes 22° 28′ 07″ N to 22° 20′ 39″ Nand longitudes 90° 49′ 41″ E to 90° 50′ 31″ E. This is anestuarine area where the main rivers mix together to theBay of Bengal containing the industrial effluents throughinland rivers from the country and trans-boundary coun-tries. The last site (St 4) is located near the southwestpart of the coastal area of Sundarbans that is regarded asa large mangrove ecosystem in Bangladesh which liesbetween latitudes 22° 34′ 43″ N to 22° 18′ 02″ N andlongitudes 89° 32′ 48″ E to 89° 36′ 26″ E. This samplingarea is also mostly influenced by different industrial

activities like cement factories, export processing zone,sea port, paper industries, oil refinery industries, steelrerolling, fertilizer industry, hatcheries, aquafarms, fishprocessing industries, leather industries, dyeing indus-tries, and paint industries. The basic information of sam-pling sites is presented in Table S1.

Sample collection and preparation

Three mostly consumed fish (Hilsa (Tenualosa ilisha),Rupchanda (Pampus argentius), Long tongue sole(Cynoglossus lingua)) and crustacean species (Indian shrimp(Penaeus indicus) and Mud crab (Scylla serrata)) were col-lected from the sampling sites. Immediately after collection,fish and crustacean samples were kept in airtight insulatingbox and thereafter transported to the laboratory of theDepartment of Fisheries, University of Dhaka, Bangladesh.After transportation, fish and crustaceans samples were rinsedin deionized water to remove surface adherents. Nonedibleparts were removed with the help of a steam cleaned stainlesssteel knife. The edible portion of the samples was cut intosmall pieces. A composite of at least 9 samples of each fishand crabs, and 18 for shrimps was prepared and homogenizedin a food processor and 100 g test portions were stored at

Source- http://bluegoldbd.org/more-information/maps/

Fig. 1 Map showing sampling sites in the coastal area of Bangladesh

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−20 °C in the Laboratory of Fisheries Department, DhakaUniversity. Then, all samples were freeze-dried for 48 h untilconstant weight was attained. The all processed samples werebrought to Yokohama National University, Japan, for chemi-cal analysis under the permission of Yokohama PlantProtection Station.

Sample digestion and metal extraction

A microwave digestion was used to digest the samples foranalysis. All chemicals were analytical grade reagents, andMilli-Q (Elix UV5 and Milli-Q Adv.A10, Millipore, USA)water was used for each solution preparation. Thepolytetrafluoroethylene (PTFE) digestion vessels and poly-propylene containers were cleaned, soaked in 5 % HNO3 formore than 24 h, then rinsed with Milli-Q water and dried. Formetal analysis, 0.2 g of fish and crustaceans samples of eachwere treated with 5 mL 69 % HNO3 acid (Kanto ChemicalCo., Tokyo, Japan) and 2 mL 30 % H2O2 (Wako ChemicalCo., Tokyo, Japan) in closed digestion vessels. After mixingfor 20 min, the vessels containing samples were placed in amicrowave digestion system (Berghof-MWS2, Berghofspeedwave®, Germany). The following microwave programwas applied: 10 min at 180 °C with 800 W, 10 min at 190 °Cwith 900 W, and as a last step 10 min at 100 °C with 400 W.After digestion, acid solutions with samples were transferredinto a Teflon graduated cylinder and total volume was madeup to 50 mL with Milli-Q water. The digested acid solutionswere then filtered by using syringe filter (DISMIC®-25HPPTFE, pore size=0.45 μm; Toyo Roshi Kaisha, Ltd., TokyoJapan) and stored in 50 mL polypropylene tubes (Nalgene,NY, USA).

Instrumental analysis

For trace metals, samples were analyzed using inductivelycoupled plasma mass spectrometer (ICP-MS, Agilent 7700series, USA, Table 1). Multi-element Standard XSTC-13(SPEX CertiPrep®, USA) solutions were used to prepare acalibration curve. The calibration curves with R2 >0.999 wereaccepted for concentration calculation. Before starting the se-quence, relative standard deviation (RSD<5 %) was checkedby using tuning solution (1μg/L each of Li, Y, Ce, Tl,Mg, andCo in 2 wt % HNO3) purchased from Agilent Technologies.Internal calibration standard solution containing 1.0 mg/Leach of beryllium (Be) and tellurium (Te), and 0.5 mg/L eachof indium (In), yttrium (Y), cobalt (Co), and thallium (TI) waspurchased from SPEX CertiPrep®, USA, and it was addedinto each sample. Working standards (0, 10, 20, 50, and100 μg/L) were prepared by dilution of a multi-element stocksolution (Custom Assurance Standard, SPEX CertiPrep®,USA), then the concentrations of trace metals were deter-mined by an internal standard method. All test batches were

evaluated using an internal quality approach and validated ifthey satisfied the defined Internal Quality Controls (IQCs).For each batch experiment, one blank, one certified referencematerial (CRM) and several samples were analyzed in dupli-cate to eliminate any batch-specific error. Finally, the concen-tration of trace metals were quantified by calibration based oninternal standards.

Quality control and quality assurance

The quality of total acid digestion of the fish and crustaceanswas checked by using a certified reference material (NMIJCRM 7402-a, Cod fish tissue) purchased from the NationalInstitute of Advanced Industrial Science and Technology(AIST) and yielded a good accuracy of the analysis. The cer-tified and analyzed values of trace metals of CRM 7402-a areshown in Table 2. The comparison is made with the certifiedvalues, which in both cases confirmed that the sample prepa-ration and instrumentation conditions provided good levels ofaccuracy and precision.

Health risk calculations

Estimated daily intakes

Estimated daily intakes (EDIs) for the analyzed trace metalswere calculated bymultiplying the respective average concen-tration in composite fish and crustaceans samples by the av-erage weight of consumption per day dividing by the averagebody weight of Bangladeshi coastal people (which was ob-tained from survey data). Metal concentration in fish was ob-tained on the basis of wet weight (ww). EDI were calculatedby the following equation:

EDI μg.kg‐bw

.day

� �¼

Xi

FIRi � Ci

WAB

where FIRi is the food (fish and crustaceans) ingestion rate(77 and 21 g/person/day for adults respectively); Ci is themetal concentration in fish and crustaceans (μg/g ww); WABis the average body weight (59 kg for adults); and i is the fooditem (fish and crustaceans).

Carcinogenic health hazard

In this study, the carcinogenic health risks related with theconsumption of fish and crustacean’s species were measuredbased on the target cancer risk (TR) or the risk of cancer over alifetime. For carcinogens, risks were estimated as the incre-mental probability of an individual to develop cancer over alifetime exposure to that potential carcinogen (i.e., incremen-tal or excess individual lifetime cancer risk) (USEPA 1989).Acceptable risk levels for carcinogens range from 10−4 (risk of

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developing cancer over a human lifetime is 1 in 10,000) to10−6 (risk of developing cancer over a human lifetime is 1 in 1,000,000). The equation used for estimating the target cancerrisk (lifetime cancer risk) is as follows (USEPA 1989),

TR ¼EF � ED�

Xi

FIRi � Ci � CSFo

WAB� TA� 0:001

where TR represents the target cancer risk or the risk of cancerover a lifetime (dimensionless); EF is the exposure frequency(365 days/year); ED is the exposure duration (60 years forBangladesh), equivalent to the average lifetime; FIR is the fishand crustaceans ingestion rate (77 and 21 g/person/ day foradults, respectively); C is the metal concentration in fish andcrustaceans (μg/g ww); i is the food item (fish and crusta-ceans); WAB is the average body weight (59 kg for adults);TA is the averaging exposure time (365 days/year×ED); andCSFo is the oral carcinogenic slope factor from the IntegratedRisk Information System (USEPA 2010) database (1.5 (mg/kg/day)−1 for As and 0.0085 (mg/kg/day)−1 for Pb).

Results and discussion

Trace metals concentration in fish and crustaceans

In this study, the trace metal concentrations were determinedon a wet weight basis in the composite commercially impor-tant fishes and crustacean species which were widely con-sumed by Bangladeshi coastal people. Mean metal concentra-tions in fishes and crustaceans are shown in Table 3.

Trace metals concentration in fish

Awide range of metal concentrations were observed among thesampling sites. Trace metals in fish were ranged over followingintervals: Cr 0.15–2.2; Ni 0.1–0.6; Cu 1.3−14; Zn 31–138; As0.8–13; Cd 0.03–0.09; Pb 0.07–0.63 mg/kg ww. The meanconcentration of studied metals in fish followed a decreasingorder of Zn>Cu>As>Cr>Pb>Ni>Cd. Most fish samplesshowed highest mean concentration of metals at Cox’s Bazarsite while the samples of fish collected at Sundarbans and

Table 1 Operating conditions forICP-MS and parameters for metalanalysis

Operating conditions

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]*0.082In [115]: (115)*1− [118]*0.014Pb [208]: [208]*1+ [206]*1+ [207]*1

Isotopes 52Cr, 60Ni, 63Cu, 65Zn, 75As, 111Cd, 208Pb

Table 2 Analysis of trace metalsfrom certified reference materials(NMIJ CRM 7402-a cod fishtissue) by ICP-MS (mean± SD,mg/kg dw)

Metal Certified value (mg/kg dw) Measured value (mg/kg dw) Average recovery (%)(n= 3)

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

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Bhola showed lowest metals concentration. Among the metals,the highest mean concentrations of Zn (138) and As (13 mg/kgww) were observed at Cox’s Bazar site which exceeded theinternational quality guideline values (Table 4).

Zinc is known to be involved in most metabolic pathwaysin humans, and its deficiency can lead to loss of appetite,growth retardation, skin changes, and immunological abnor-malities (Tuzen 2009). The lowest and highest Zn content in

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 compositesamples having three replicates of each

mg/kg ww milligrams/kilogram wet weight basis

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 incoastal 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 basisa California Environmental Protection Agency, State Water Resources Control

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fish were found as 31 mg/kg ww in Sundarbans and 138 mg/kg ww in Cox’s Bazar site. Zinc contents in the literature havebeen reported in the range of 42.8–418 mg/kg ww in someedible fishes in Bangladesh (Rahman et al. 2012) and 38.8–93.4 mg/kg ww in some fish species from the Black Sea,Turkey (Tuzen 2009). Other literatures have been reported inthe range of 0.60–11.57 mg/kg ww in fish species which werecollected from the Iskenderun Bay, Turkey (Turkmen et al.2005). The high Zn concentration at Cox’s Bazar site mightbe attributed to the discharge of different salts and chemicalsfrom hatcheries and fish processing industries where zinc ox-ide (ZnO) was broadly used for the oxygen supply to fry andfingerlings (Shamsuzzaman and Biswas 2012). Besides, mostof the domestic sewages of Cox’s Bazar city were incorporat-ed to the Bakkhali River through different uncontrolled canalsto the Sea. The biggest fishery landing center was located inthis site and all poisonous effluents were directly dischargedinto the river without treatment. Along the banks of this river,a dock yard has been recently developed to repair fishing andtrawling boats. Waste discharge and chemical spills associatedwith boat repairing industries represent an additional source ofpollutants to the water and sediments. Moreover, galvanizingsteel, ship repairing, painting, textile and dyeing, and rubberindustries also contribute significant amount of Zn in this area.Considering ship repairing, painting, and coating, a hugeamount of commercial paints containing zinc oxide (ZnO)and zinc sulfide (ZnS) have long been used as anticorrosivecoatings in different type of boats, fishing trawlers, and shipsin Cox’s Bazar and Chittagong coast to protect wood and steelstructures under normal atmospheric conditions, as well as tounderwater steel surfaces of these water vehicles. Zinc oxideis also used to retain their flexibility and adherence on suchsurfaces for many years and using component in many formu-lations of durables and protective paints. Besides, the rubberindustry in general, and tire manufacturers in particular, arethe largest users of ZnO. It is utilized to activate the organicaccelerator, serves as an effective co-accelerator in the vulca-nization process, and inhibits the growth of fungi, with suffi-cient stability, as part of the production process of latex foamrubber products.

Arsenic is particularly difficult to characterize as a singleelement because its chemistry is really complex. Arsenic oc-curs in three oxidation states: trivalent arsenite (As(III)), pen-tavalent arsenate (As(V), and elemental. Arsenite is ten timesmore toxic than arsenate; elemental arsenic is nontoxic(Sharma et al. 2014). Naturally, As in seafood exists in twoforms: inorganic and organic (arsenobetaine, arsenocholine,and organoarsenicals). Although seafood contains a high con-centration of organic arsenic, it is much less toxic than inor-ganic arsenic (Han et al. 1998, Sharma et al. 2014) and can beefficiently and rapidly excreted in urine without transforma-tion (Han et al. 1998). Conversely, it is suspected that inor-ganic As present in fish consumed by humans is carcinogenic.

Chronic exposure to arsenic can lead to dermatitis, mild pig-mentation keratosis of the skin, decreased nerve conductionvelocity, and lung cancer (Occupational Safety and HealthAdministration 2004). However, as only about 10 % of theAs present in fish is in inorganic form, only this percentagewas used to calculate hazard (Buchet et al. 1996). The lowestconcentration of arsenic in fish was observed as 0.76 mg/kgww in Bhola site while the highest concentration was ob-served as 13 mg/kg ww in Cox’s Bazar site which has beenexceeded the international quality guideline values (Table 4).In some literature, the arsenic concentration has been reportedin the range of 1.01–15.2 mg/kg ww in Bangladeshi freshwa-ter fish species (Shah et al. 2009). According to Tuzen (2009),the range of As level was found as 0.11–0.32 mg/kg ww infish species from the Black Sea, Turkey. Other literatures havebeen reported in the range of 12.6–190 mg/kg ww in fish andshellfish samples proposed by Lavilla et al. (2008). The con-centration range 0.02–0.04 mg/kg ww was also found in fishsample which was proposed by Das et al. (2004). Comparedwith published data, the total As was found inmuscles rangingfrom 0.39 to 12.58 mg/kg ww in fish collected from the south-east Spain (Delgado-Andrade et al. 2003). De Rosemond et al.(2008) observed a range of 0.57 to 1.15 mg/kg ww for totalarsenic in muscles of five freshwater fish species collectedfrom the Back Bay near Yellowknife, NT, Canada.According to the New Zealand food safety standard(Table 4), the maximum arsenic level permitted for fish sam-ples is of 1.0 mg/kg ww. Food and Agriculture Organization(FAO), especially the Regional Office for Asia and the Pacific,has recommended a concentration of 0.126 mg/day as a pro-visional maximum tolerable daily intake for ingested arsenic(FAO 2006).

Copper is essential for good health, but very high intakecan cause adverse health problems such as liver and kidneydamage (Ikem and Egiebor 2005). The highest concentrationof copper was found in fish as 14 mg/kg ww at Cox’s Bazarsite while lowest content was found as 1.3 mg/kg ww inSundarbans site. Copper levels in the literature have beenreported in the range of 5.17–9.45 mg/kg ww in fish fromDhaleshwari River, Bangladesh (Ahmed et al. 2009). In theother literature, copper levels have been reported in the rangeof 0.11–0.97 mg/kg ww in Northeast Atlantic (Celik andOehlenschlager 2004) and 0.04–5.43 mg/kg ww in theIskenderun Bay, Turkey (Turkmen et al. 2005). In this study,in comparison to the international guideline, the concentrationof copper was within safe limit (Table 4).

The range of Cr level was found as 0.15–2.2 mg/kg wwwhich is within the legal limits. The lowest content was foundas 0.15 mg/kg ww in Sundarbans site while the highest con-tent was found as 2.2 mg/kg ww in Cox’s Bazar. Chromiumcontents in the literature have been reported in the range of0.07–6.46 mg/kg ww in fish species from Iskenderun Bay,Turkey (Turkmen et al. 2005). The range of Cr level was also

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found as 0.04–1.75 mg/kg ww in seafood from Marmara,Aegean, and Mediterranean seas in Turkey (Turkmen et al.2008). Besides, the range of Cr as 0.47–2.07 mg/kg ww insome edible Bangladeshi fishes were also reported (Rahmanet al. 2012). Other authors also found some Cr concentrationsin edible tissue of Silurus glanis which was in the range of0.80–1.40 mg/kg ww (Mendil and Uluzlu 2007) and 0.11–0.23 mg/kg ww (Matasin et al. 2011), respectively.However, the content of chromium in food is of great impor-tance as it is involved in insulin function and lipid metabolismof the body (Bratakos et al. 2002).

Lead is another ubiquitous toxic metal detectable practical-ly in all phases of the inert environment and biological sys-tems. It is frequently used in the production of batteries, metalproducts, ammunition, and devices to shield X-rays (Sharmaet al. 2014). Lead is a nonessential element, and it is welldocumented that it can cause neurotoxicity, nephrotoxicity,and many other adverse health effects (Garcia-Leston et al.2010). This neurotoxicity was later found to be associatedwith lead-induced production of ROS which caused increaseor decrease in the levels of lipid peroxidation or antioxidantdefense mechanisms in the brain (Sharma et al. 2014).However, in this experiment, the lowest concentration of Pbin fish was observed as 0.07 mg/kg ww in Sundarbans sitewhile the highest concentration was observed as 0.63 mg/kgww in Cox’s Bazar which was close to the literature reportedconcentrations of 0.026–0.481 mg/kg ww (Morgano et al.2011). Lead content in the literature has been reported in therange of 0.09–6.95 mg/kg dw in fish species from IskenderunBay, Turkey (Turkmen et al. 2005). Moreover, another litera-ture has been reported in the range of 1.76–10.27 mg/kg wwin some edible fishes of Bangladesh (Rahman et al. 2012).Regarding Pb, the maximum concentration limit of Pb wasproposed by the European Community as 0.2 mg/kg ww infish (EC Regulation 2001).

Nickel normally occurs at very low levels in the environ-ment, and it can cause a variety of pulmonary adverse healtheffects, such as lung inflammation, fibrosis, emphysema, andtumors (Forti et al. 2011). The highest nickel concentration infish was found as 0.56 mg/kg ww in Cox’s Bazar which waswithin the guideline limits. Nickel concentration in the litera-ture has been reported in the range of 0.02–3.97 mg/kg ww inseafood from Marmara, Aegean, and Mediterranean seas(Turkmen et al. 2008). Other literature showed the range of0.11–12.88 mg/kg ww in fish species from the IskenderunBay (Turkmen et al. 2005). A concentration range of 2.94–46 mg/kg ww in fish and shellfish samples were also reportedby Lavilla et al. (2008). The World Health Organization hasrecommended a range of 100–300 mg/kg bw/day for dailynickel intake (WHO 1994).

Cadmium poisoning is an occupational hazard associatedwith industrial processes such as metal plating and the pro-duction of nickel-cadmium batteries, pigments, plastics, and

other synthetics (Sharma et al. 2014). Cadmium is a highlytoxic metal with a natural occurrence in the soil, but it is alsospread in the environment due to human activities. Cadmiummay accumulate in the human body andmay give rise to renal,pulmonary, hepatic, skeletal, reproductive effects, and cancer(Zhu et al. 2011). It also causes osteoporosis, anemia,nonhypertrophic emphysema, irreversible renal tubular injury,eosinophilia, anosmia, and chronic rhinitis (Sharma et al.2014). The highest cadmium content in fish species werefound as 0.075 mg/kg ww which is close to the literaturereported concentrations of 0.05 mg/kg ww in fish (Tuzenet al. 2009). In the literature, cadmium levels in fish have beenreported in the range of 0.51–0.73 mg/kg dw in fish samplesfrom Dhaleshwari River, Bangladesh (Ahmed et al. 2009).The European Community legislation has recommended amaximum Cd level of 0.05 mg/kg ww in fish (ECRegulation 2001). Besides, the Codex Committee on FoodAdditives and Contaminants recommends 0.5 mg/kg ww infish (Ikem and Egilla 2008).

Trace metal concentration in crustaceans

The concentration ranges of trace metals in crustaceans (shrimp)were as follows: Cr 3.2–1.1; Ni 0.28–1.4; Cu 13–63; Zn 53–131;As 0.3–2.5; Cd 0.02–0.12; Pb 0.1–0.38mg/kg ww. According tothese data in shrimp, zinc had the highest concentration andfollowed by copper, arsenic, nickel, chromium, cadmium, andlead. Otherwise, trace metals in crustaceans (crabs) ranged overfollowing intervals: Cr 0.29–29; Ni 0.49–43; Cu 80–400; Zn137–1480; As 1.3–53; Cd 0.084–8.3; Pb 0.24–79 mg/kg ww.The mean concentrations of studied metals in crabs followed adecreasing order of Zn > Cu > Pb > As > Ni > Cr > Cd.Remarkably, most of the studied metals in crustaceans showedthe highest mean concentration at Cox’s Bazar site whichexceeded the international quality guideline (Table 4).Comparing crustaceans, crab had the higher mean contents ofmost metals. Crab is a typical benthic organism that residesabove or in the sediment that might be good indicators reflectingthe contamination levels in surface sediment (Ololade et al.2011). Unlike fish skin, crab legs are often buried in surficialsediments and might adsorb metals from sediment more easily.Thus, it is more susceptible to sediment and is expected to pos-sess high metal levels (Zhao et al. 2012). Besides, crabs hascapability of accumulating more trace metals by the hepatopan-creas, one of the most important organs that play important rolesin metal detoxification (Reinecke et al. 2003; Wang et al. 2001).Mean concentrations of most metals in crabs were significantlyhigher than those in fishes, indicating that high metal levels insediment might have resulted in the enrichment of metals incrabs. Moreover, crab is known as a scavenger that tends to feedon detritus which is the most contributing factor to the highpollution in crabs (Ip et al. 2005). Unlike benthic fishes, crabsoften bury themselves in the sediments, making them closer to

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sediments and thus expose to higher concentration and moremetal species (Zhao et al. 2012). It can be seen that perceptiblyelevated levels of Zn (1480mg/kg ww) and Cu (400mg/kg ww)were found in crabs (Table 3)which can be explained by the factsthat the two metals are necessary elements to meet crab’s phys-iological needs and most of crab’s food (e.g., debris or smallbenthic organism) had high accumulation of these metals.However, crab gill is an organ responsible for breathing andregulating permeation pressure and ionic equilibrium. Becauseof its functional characteristics and large surface area, it oftencontains high concentrations of metals (Zhao et al. 2012).However, it is difficult to conclude which pathways (e.g., dermalexposure or breathing or complicated food sources) are contrib-uting more bioaccumulation and biotransformation in crabs’body as few literatures arementioned in this regard. Some studiesreported that the dermal contact through appendages and chestregion contribute higher metal concentration in crabs’ body aslegs and chest are often submerged in upper part of sediments(Falusi and Olanipekun 2007).

Health risk assessment

Estimated daily intakes

EDIs of selected toxic trace metals from fish and crustaceansconsumption by average Bangladeshi coastal adults are pre-sented in Tables 4 and 5. The oral reference dose (RfD) wasused in this study to evaluate the EDIs of metals in fishes.RfDs are based on 3, 20, 40, 300, 0.3,1 and 3.5 μg/kg bw/day for Cr, Ni, Cu, Zn, As, Cd, and Pb, respectively (USEPA2008). The RfD represents an estimate of the daily exposure towhich the human population may be continually exposed overa lifetime without a considerable risk of deleterious effects. Ingeneral, the RfD represents an estimate (with uncertaintyspanning perhaps an order of magnitude) of a daily exposureto the human population (including sensitive subgroups) thatis likely to be without an appreciable risk of deleterious effects

during a lifetime. It is useful as a reference point fromwhich togauge the potential effects of the chemical at other doses.Usually, doses less than the RfD are not likely to be associatedwith adverse health risks and are therefore less likely to be ofregulatory concern. As the frequency and/or magnitude of theexposures exceeding the RfD increase, the probability of ad-verse effects in a human population increases. However, itshould not be categorically concluded that all doses belowthe RfD are Bacceptable^ (or will be risk free) and that alldoses in excess of the RfD are Bunacceptable^ (or will resultin adverse effects) (US EPA 2008). There are several ap-proaches of human exposure to trace metals such as breathingand dermal exposure. However, food consumption is oftenregarded as one of the most important approaches.Considering fish, except for As, the average EDIs of metalsin fish was below the RfDs (Fig. 2) indicating that averageconsumption of fish in the coastal area would not result inhealth risk. But, dietary intakes of As exceeded the RfDsthrough consumption of fish which was mainly ascribed tothe fact that high concentrations of As can produce toxiceffects.

Hence, excessive ingesting of fish should be avoided tominimize the harmful effects caused by As accumulation.Besides, except for Zn and Ni, the average EDIs of mostmetals (As, Pb, Cu, Cr, and Cd) in crustaceans exceeded theRfDs (Fig. 2) indicating that average consumption of crusta-ceans would result in severe health risk. In Bangladesh con-text, shrimp is very popular, expensive, and emblematic ofBangladeshi cuisine. Coastal people are used to consumemore as it is readily available in local area. Besides, due toreligious prohibition, eating crabs is not so popular in all overthe country even though they have high commercial value inthe world market to earn foreign exchange (Azam et al. 1998).Nevertheless, millions of poor coastal fishers, traders, andrural ethnic people are directly or indirectly dependent on thiscrab fishery (Zafar 2004; Patterson and Sainuel 2005).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 crustaceanscollected 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

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-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 averageBangladeshi coastal adults in comparison with oral reference dose (RfD) (USEPA 2008)

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coastal area should be avoided to prevent the detrimental ef-fects triggered by As, Pb, Cu, Cr, and Cd accumulation. Inaddition, a difference of metal levels and EDI among the areasshould be considered. For example, the EDI levels of mostmetals specially Cr, Zn, and As in fish and crustaceans fromCox’s Bazar site were higher than those from Sundarbans andBhola and sometime Chittagong area (Table 6). Therefore,people in Cox’s Bazar may be exposed to higher levels ofsomemetal contaminations than people living in the other areaof Bangladeshi coast.

Carcinogenic health hazard

The target lifetime carcinogenic risk (TR) of As and Pb dueto exposure from seafood consumption are listed in Table 5.The TR values for As and Pb from seafood consumptionwere 2 × 10−2 and 1 × 10−4, respectively. In general, the ex-cess cancer risk lower than 10−6 are considered to be negli-gible, cancer risk above 10−4 are considered unacceptable,and risks lying between 10−6 and 10−4 are generally consid-ered an acceptable range (USEPA 1989; 2010). The carci-nogenic risk for Pb was close to the unacceptable range,whereas that of As was higher than the unacceptable value(10−4). According to the USFDA (1993), about 90 % of theAs exposure occurs from the seafood. Multiple health im-plications have been associated with As exposure. Inorganicarsenic is a known carcinogen and can cause cancer of theskin, lungs, liver, and bladder. Cardiovascular disease(CVD) for instance, is observed in the areas of endemicAs exposures (Cheng et al. 2010). Besides, EPA has deter-mined that lead is a probable human carcinogen. Long-termexposure can result in decreased performance of nervoussystem. Exposure to high lead levels can severely damagethe brain, liver, and kidneys and ultimately cause death (Leeet al. 2011; Luckey and Venugopal 1977). High-level

exposure in men can damage the organs responsible forsperm production (Martin and Griswold 2009). In pregnantwomen, lead may cause miscarriage. Therefore, the poten-tial health risk for the coastal people due to metal exposurethrough fish and crustaceans (seafood) consumption shouldnot be ignored. Moreover, there are also other cradles ofmetal exposures, such as consumption of other contaminat-ed foods and dust inhalation, which were not encompassedin this study. It is thus proposed that continuous monitoringof these toxic trace elements in all foodstuffs are needed toevaluate if any impending health risks of the study area doexist.

Conclusions

This study was developed to provide baseline informationon the concentrations of some toxic trace metals in com-mercial fish and crustaceans of coastal areas ofBangladesh. Among the four sites studied, fishes ofCox’s Bazar site were more contaminated by trace metals.Arsenic and Zn concentration were remarkably high infishes and crabs collected from Cox’s Bazar. Crabs weremore susceptible to possess higher metal accumulationthan other fishes due to its absolute different bioaccumu-lation pattern. Some metals in fish and crustaceansexceeded the international quality guidelines. Estimateddaily intake (EDI) and target cancer risk (TR) revealedhigh dietary intake of As and Pb, which was obviouslya matter of severe public health issue of Bangladeshicoastal people which should not be ignored and concen-trate our views to solve this problem with an integratedapproaches. Thus, continuous monitoring of these toxictrace elements in seafood and immediate control measureis recommended.

Table 6 Site-specific estimated daily intake (EDI) of selected toxic trace metals from fish and crustaceans (seafood) consumption by averageBangladeshi 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 foradults, respectively, which was obtained from survey data. Metal concentration data of fish and crustaceans were adopted from Table 3

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Acknowledgments The authors would like to acknowledge theGraduate School of Environment and Information Sciences, YokohamaNational University, Japan, for providing research grant through theInternational Environmental Leadership Program in Sustainable Livingwith Environmental Risk (SLER) and through research cooperation pro-gram for Ph. D students. The authors also would like to convey specialthanks and gratitude to the Setsutaro Kobayashi Memorial Fund by FujiXerox Co., Ltd., Japan, for the financial assistance of this research. Theauthors also thankfully acknowledge the Yokohama Plant Protection au-thority of Japan for the import permission of the sediment samples fromBangladesh (MAFF Directive Import Permit No. 25Y324, date of issue:June 11, 2013).

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict ofinterest.

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