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Research Article Health Risk Assessment of Heavy Metals from Smoked Corbicula fluminea Collected on Roadside Vendors at Kelantan, Malaysia Koh Han Dee , 1 Faizuan Abdullah, 2 Siti Nor Aini Md Nasir, 1 Suganthi Appalasamy, 1 Rozidaini Mohd Ghazi, 1 and Aweng Eh Rak 1 1 Department of Natural Resource and Sustainability, Universiti Malaysia Kelantan, Jeli Campus, Locked Bag No.100, 17600 Jeli, Kelantan, Malaysia 2 Department of Chemistry, Faculty of Science, Universiti Teknologi Malaysia, 81310 UTM Johor Bahru, Johor, Malaysia Correspondence should be addressed to Aweng Eh Rak; [email protected] Received 11 May 2019; Revised 27 August 2019; Accepted 6 September 2019; Published 30 September 2019 Academic Editor: Francesco Dondero Copyright © 2019 Koh Han Dee et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Corbicula fluminea serves as traditional food to the local people in Kelantan, Malaysia. Concerns regarding river contamination, smoking method, and associated adverse effects on public health had been increasing. Hence, this study aims to measure the level of heavy metals (Cd, Cu, Mn, Pb, and Zn) and assess human health risk in C. fluminea consumption at Kelantan. Heavy-metal analysis was done using flame atomic absorption spectrophotometry, while human health risk was assessed using provisional tolerable weekly intake (PTWI), target hazard quotient (THQ), and hazard index (HI). e estimated weekly intake (EWI) for all metals was found within PTWI, while THQ for Cd, Cu, Mn, Pb, and Zn was 0.12, 0.06, 0.04, 0.41, and 0.03, respectively. e HI was calculated at 0.61 which is less than 1, considered as the safe consumption level. erefore, C. fluminea consumption in this study was found safe from the health risk of noncarcinogenic effect over a lifetime. 1. Introduction Corbicula fluminea (M¨ uller, 1774) is known as “Etak” at Kelantan, Malaysia. e local people consume C. fluminea since a very long time ago, especially smoked C. fluminea as their favourite. Smoked C. fluminea is broadly sold at morningmarket,nightmarket,andinthestreetstalls.is food generates income for local Kelantanese. In average, C. fluminea sellers can generate up to 600 USD/month [1]. Different countries have different ways to cook C. flu- minea. is can be shown in the Philippines where C. fluminea is consumed raw-pickled or cooked in soup [2]. In Kelantan, the local people consume C. fluminea in many cooking methods, including the smoke method, sun-drying method, and frying method [1]. Among these cooking methods, the smoke method is the most popular method.elocalpeopleconsumethesmoked C.fluminea while they are watching television, studying, and chatting with friends. Corbicula fluminea is distributed in most of the fresh- water river in Malaysia, such as Perak River, Pahang River, Golok River, and Pergau River. is clam is mostly found in sand and gravel sediments. C. fluminea obtains the food in water column and sediment via inherent filter feeding and pedal feeding ability, respectively [3]. ey mainly feed on suspended matter, phytoplankton, bacterioplankton, zoo- plankton, diatoms, green algae, and protozoans [4, 5]. With this feeding ability, C. fluminea is important in ecosystem balance by contributing in benthic/pelagic biogeochemical coupling and enhanced oxygen penetration into the sedi- ment [6, 7]. C. fluminea is also used as a bioindicator of the heavy metals and microplastic in freshwater river [8, 9]. In Kelantan, high demand for C. fluminea is contrib- uted by a better understanding of nutrition content on seafood consumption. C. fluminea is well known for its high nutritional values of protein, omega-3 fatty acid, and pharmaceutical values including lowering cholesterol ac- cumulation, increasing antioxidant, and anticancer and Hindawi BioMed Research International Volume 2019, Article ID 9596810, 9 pages https://doi.org/10.1155/2019/9596810

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Page 1: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

Research ArticleHealth Risk Assessment of Heavy Metals from SmokedCorbicula fluminea Collected on Roadside Vendors atKelantan Malaysia

Koh Han Dee 1 Faizuan Abdullah2 Siti Nor Aini Md Nasir1 Suganthi Appalasamy1

Rozidaini Mohd Ghazi1 and Aweng Eh Rak 1

1Department of Natural Resource and Sustainability Universiti Malaysia Kelantan Jeli Campus Locked Bag No 100 17600 JeliKelantan Malaysia2Department of Chemistry Faculty of Science Universiti Teknologi Malaysia 81310 UTM Johor Bahru Johor Malaysia

Correspondence should be addressed to Aweng Eh Rak awengumkedumy

Received 11 May 2019 Revised 27 August 2019 Accepted 6 September 2019 Published 30 September 2019

Academic Editor Francesco Dondero

Copyright copy 2019 Koh Han Dee et al +is is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Corbicula fluminea serves as traditional food to the local people in Kelantan Malaysia Concerns regarding river contaminationsmoking method and associated adverse effects on public health had been increasing Hence this study aims to measure the levelof heavy metals (Cd Cu Mn Pb and Zn) and assess human health risk in C fluminea consumption at Kelantan Heavy-metalanalysis was done using flame atomic absorption spectrophotometry while human health risk was assessed using provisionaltolerable weekly intake (PTWI) target hazard quotient (THQ) and hazard index (HI) +e estimated weekly intake (EWI) for allmetals was found within PTWI while THQ for Cd Cu Mn Pb and Zn was 012 006 004 041 and 003 respectively +e HIwas calculated at 061 which is less than 1 considered as the safe consumption level +erefore C fluminea consumption in thisstudy was found safe from the health risk of noncarcinogenic effect over a lifetime

1 Introduction

Corbicula fluminea (Muller 1774) is known as ldquoEtakrdquo atKelantan Malaysia +e local people consume C flumineasince a very long time ago especially smoked C flumineaas their favourite Smoked C fluminea is broadly sold atmorning market night market and in the street stalls +isfood generates income for local Kelantanese In averageC fluminea sellers can generate up to 600 USDmonth [1]Different countries have different ways to cook C flu-minea +is can be shown in the Philippines where Cfluminea is consumed raw-pickled or cooked in soup [2]In Kelantan the local people consume C fluminea inmany cooking methods including the smoke methodsun-drying method and frying method [1] Among thesecooking methods the smoke method is the most popularmethod+e local people consume the smoked C flumineawhile they are watching television studying and chattingwith friends

Corbicula fluminea is distributed in most of the fresh-water river in Malaysia such as Perak River Pahang RiverGolok River and Pergau River +is clam is mostly found insand and gravel sediments C fluminea obtains the food inwater column and sediment via inherent filter feeding andpedal feeding ability respectively [3] +ey mainly feed onsuspended matter phytoplankton bacterioplankton zoo-plankton diatoms green algae and protozoans [4 5] Withthis feeding ability C fluminea is important in ecosystembalance by contributing in benthicpelagic biogeochemicalcoupling and enhanced oxygen penetration into the sedi-ment [6 7] C fluminea is also used as a bioindicator of theheavy metals and microplastic in freshwater river [8 9]

In Kelantan high demand for C fluminea is contrib-uted by a better understanding of nutrition content onseafood consumption C fluminea is well known for itshigh nutritional values of protein omega-3 fatty acid andpharmaceutical values including lowering cholesterol ac-cumulation increasing antioxidant and anticancer and

HindawiBioMed Research InternationalVolume 2019 Article ID 9596810 9 pageshttpsdoiorg10115520199596810

antitumor activities [10ndash13] Despite the ecological im-portance and economic benefits the heavy metals poten-tially accumulate in C fluminea soft tissue [5] +e riverpollution and popular smoking method are suspected tocontaminate C fluminea One of the most common heavymetals bioaccumulation in human body is through the foodchain and regular consumption of contaminated food [14]+e relationship between the heavy metals concentrationsin this clam and associated health risk assessment inKelantan is yet to e reported +e local people lack in-formation about the safety of C fluminea consumptionHence this research aims to determine the selected heavy-metal (cadmium copper manganese lead and zinc) levelin C fluminea soft tissue that is sold in the streets and assessthe human health risk +ese selected heavy metals andtheir effects on human health are of great concern based onthe previous studies [5 15ndash17] +e health risk assessmentis carried out on the ready-to-eat C fluminea sold along theroadside +e provisional tolerable weekly intake (PTWI)target hazard quotient (THQ) and hazard index (HI) wereused to evaluate the health risk

2 Materials and Methods

21 Study Area +e samples were collected at Pasir Mas andTumpat Kelantan (60495938N 1021693547E and61467273N 102218605E) for six months duration Six stallsofC flumineawere selected due to their availability throughoutthe year (Figure 1) +e primary source of C fluminea used inthese stalls is fromPerak River which is located close to oil palmplantations durian farms and urban area Around 1kgsmoked C fluminea was collected from each seller for theheavy-metal analysis Each sample was labelled with the datetime collection site and weather +e samples were preservedat 4degC by storing in an ice box during their transportation to thelaboratory [18] +e samples were stored in a freezer at minus 20degCbefore analysis

22 Sample Analysis +e soft tissues of C fluminea wereobtained using a blade and oven dried (60degC 72 hours) toconstant weight After that the samples were ground intohomogenous samples using a mill machine (PanasonicregMX-900M) +e samples were preserved in amber jars and storedin a desiccator before acid digestion +e digestion processwas carried out by following the standard method by Per-kinElmer Corporation [19]

Approximately 5 g of dried samples was placed in the250mL beaker in which 5mL of 95 sulfuric acid (Merck)and 5mL of 65 nitric acid (Merck) were added +esamples were covered immediately with watch glass Afterthe reaction between sample and acid was completed themixtures were heated at 60degC for 30 minutes using hot plates(IKAreg C-MAGHS 7)+e samples were allowed to cool and20mL of 65 nitric acid was added +e temperature wasincreased slowly to 150degC for two hours +en the solutionswere allowed to cool and 1mL of 30 hydrogen peroxide(Merck) was added until the colour became clear Sampleswere diluted to 50ml with deionized water +e solutions

were then filtered by filter paper (Whatmanreg No 41 filtercircles 125mm) and syringe filter (Minisartreg nylon syringefilter 25mm)

+e samples analysis was analysed by using the flameatomic absorption spectrophotometer PinAACLE 900F andmeasured in triplicates +e accuracy and validity of theapplied protocol were evaluated using the Standard Refer-ence Materials (SRM 2976 National Institute of Standardsand Technology) due to its suitability in the mussel sampleand matrix Recovery rates were found to be between9998ndash11008 for the selected metals

23 Human Health Risk Assessment (HHRA) All data ob-tained were converted into wet weight (ww) using a con-version factor of 019 +e conversion factor is based on themoisture analysis carried out in the food laboratory Uni-versiti Malaysia Kelantan by our research assistant Siti NorAini Md Nasir on 28 October 2018

(a) Maximum permissible limit (MPL) of the heavymetals for the consumers set by the European Union[20] and FAO compilation of the legal limits by FAO[21]

(b) +e estimated daily intakes (EDIs) of the consumersin order to evaluate the adverse health effects+e JECFA uses the term estimated daily intake(EDI) and provisional tolerable daily intake (PTDI)for contaminants as heavy metals that can accu-mulate in the human body [22] Estimated dailyintake (EDI) (μgkg body weight) of heavy metalsfrom C fluminea consumption was obtained usingthe following equation (1) [23 24]

EDI Cmetal times IR( 1113857

BW (1)

where EDI is estimated daily intake and Cmetal (mgkgww) is an average weighted heavy metal content in Cfluminea Ingestion rate (IR) (gramday person) is thedaily mussel consumption BW is the average bodyweight +e average IR is determined by interviewingthe local people using a simple questionnaire +eaverage IR of C fluminea for Malaysian adults is 75 gday person which is similar to the literature [2] +eaverage body weight for Malaysians was 6265 kg [25]To obtain estimated weekly intake (EWI) the EDIwill be multiplied by a factor of 7 corresponding to 7days However based on questionnaires and in-terviews the local people consume C fluminea witha frequency of three days per week Hence EWI wasobtained using the following equation

EWIthis study EDI times 7 times37 (2)

+e EWIthis study is compared to the JECFA pro-visional tolerable weekly intake (PTWI)

(c) Target hazard quotient has been recognised as auseful parameter for evaluation of risk associated

2 BioMed Research International

with the consumption of metal contaminated foodTo assess the noncarcinogenic risk due to heavymetal exposure in C uminea soft tissue the targethazard quotient (THQ) was computed using thefollowing equation [26]

THQ EFr times ED times IR timesMCRfD times BW times AT

[ ] times 10minus 3 (3)

where EFr is exposure frequency (156 days per year forthe average consumer according to the local in-terview) ED is exposure duration (70 years) equiv-alent to the average human lifespan IR is the ingestionrate (75 grams per person per day) MC is the metalconcentration in C uminea soft tissue (in mgkgww) RfD is the oral reference dose (Cd is 1mgkg wtday Cu 40mgkg wtday Zn 300mgkg wtday andMn 140mgkg wtday) [27]e reference dose (RfD)

is an estimate of the daily intake of contaminantduring a lifetime that would not cause adverse healtheects to the human [28] BW is the average bodyweight (6265 kg) AT is the averaging time fornoncarcinogens (ie 30 years or 10950 days)With the refusal to set the reference dose of Pb byEPA [29] the THQ for Pb was calculated by usingthe following equation [30]

THQ CPb

MPL (4)

where CPb is the Pb concentration in C uminea(mgkg ww) MPL maximum permissible limit Inthis study the MPL of Pb for bivalve is 150mgkgww [20]THQlt 1 indicates no obvious risk A THQ gt1 showsthat the level of exposure is higher than the oral

Scale

0 20km 40km

Sampling pointsKelantan

102deg0prime0PrimeE

6deg0prime0PrimeN

5deg0prime0PrimeN

6deg0prime0PrimeN

102deg0prime0PrimeE

Pengkalan Chepa

Tumpat

Kelantan

5deg0prime0PrimeN

N

S

EW

Figure 1 e map of the Kelantan state Malaysia e study area and sampling points of C uminea were at Pasir Mas and TumpatKelantan

BioMed Research International 3

reference dose (ORD) which assumes that a daily ex-posure at this level is likely to cause harmful healtheffects during the lifetime in a human population [31]Following EPA guidelines we assumed that the ingesteddose was equal to the absorbed contaminant dose

(d) +e hazard index (HI) calculated from THQ is thetotal of the hazard quotients [23 32]HI THQCd + THQCu + THQMn + THQPb + THQZn

(5)

If HI less than 1 there is no obvious risk

24 Statistical Analysis +e metal concentrations for sixsellers were averaged to obtain the mean Microsoft Excelwas used to tabulate all the data throughout the experimentand generate the hazard index graph SPSS 23 for Windowswas used to run the statistical analysis including the meanstandard error and one-way ANOVA with Tukey post hoctest +e statistical significance was significant whenPlt 005

3 Results and Discussions

31 Heavy-Metal Concentration in C fluminea and HumanHealth Risk Assessment +e mean concentration of Cd CrCu Mn Pb and Zn (mgkg ww) in C fluminea from theroadside stalls which are consumed by local people istabulated in Table 1 +e values in each month are the meanfrom six stalls Metal concentration in C fluminea exhibitedan order of ZngtMngtCugtPbgtCd

In this study dietary exposure to heavy metals throughconsumption of C fluminea in the studied areas was eval-uated using estimated daily intake (EDI) by considering theaverage concentration of the heavy metals and the respectiveconsumption rate for adults +en the estimated weeklyintake (EWI) was calculated and compared with PTWITable 2 shows the values of EDI EWI PTWI and EWI PTWI ratio

32 Cadmium Cd detected in C fluminea ranged from 017to 034mgkg ww and has a mean of 023plusmn 001mgkg wwNo significant difference was found between Cd levels ineach month with Pgt 005 +e Cd level is within the per-missible limit set by the European Union of 10mgkg ww[20] In EWI measurement the local people consumingC fluminea would intake 084μgkgweek or 005mg6265 kgpersonweek (084times 62651000) of the Cd +e EWI PTWIratio of the Cd was 1200 +is showed that the intake iswithin the safe level

+e current result is found to be higher than that in thestudy by Zhelyazkov et al [35] who reported the EWI ofCd for the marine mollusc (Mytilus galloprovincialis) was0002mg70 kg personweek (00032 times 70 times 71000) Be-sides Yunus et al [36] study the metal level in the cockles(Anadara granosa) from Kuala Selangor Malaysia +eyreported 596 μg70 kgdaily or 004mg70 kg personweek (596 times 71000) of Cd intake with cockle

consumption which is also lower than the EWI value of Cdin the current study Sharif et al [37] study on con-sumption of shellfish clam (Metretrix spp) scallop(Amusium pleuronectes) and conch (Strombus canarium)at Kudat Sabah +ey reported that if the local peopleconsume these shellfish every day the EWI values of Cdfor Metretrix spp Amusium pleuronectes and Strombuscanarium were 001mg6265 kg personweek(003 times 7 times 62651000) 069mg6265 kg personweek(158 times 7 times 62651000) and 0009mg6265 kg personweek (002 times 7 times 62651000) respectively

EWI of Cd (005mg6265 kg personweek) in thecurrent study is higher than that of previous studies exceptthe scallop (Amusium pleuronectes) High EWI of Cd in Cfluminea is due to high ingestion rate and high Cd con-centration in C fluminea Cd is mainly used in industriesincludes electroplating alloy production pigments andbattery production [38] +is is in agreement in the currentstudy where metal industries automobile workshops andlaptop shops can be found near to Perak River +e Cd indischarged wastewater is easily deposited into rivertransferred to aquatic life and eventually accumulated inhuman body through the food chain [39] As a filter feedingorganism C fluminea is reported susceptible to heavy-metal exposure in river and possess high metal level [5]

Cadmium is a nonessential element for human anddetrimental to our health even when ingested in smallquantities Food is the primary source of Cd exposurebesides cigarette smoking [40 41] Continuous Cd con-sumption leads to respiratory system damage lung cancerParkinsonrsquos and Wilsonrsquos diseases and estrogen receptor-positive breast cancer in postmenopausal women [42 43] InJapan consumption of Cd-contaminated rice causes oste-omalacia (bone disease) and kidney malfunction to the localpeople [44] Cd-poisoning patients need to be treated withgastrointestinal tract irrigation supportive care andchemical decontamination with chelating agents andnanoparticle-based antidotes [45]

33 Copper +e Cu detected in C fluminea ranged from264 to 1261mgkg ww and has a mean of 503plusmn 047mgkgww+ere is no significant difference between the Cu level inevery month with Pgt 005 except in April with Plt 005+eCu level is within the permissible limit of 20 to 70mgkg wwset by FAO compilation of the legal limits [21] In EWImeasurement the C fluminea consumer would intake1806 μgkgweek or around 113mg6265 kg personweek(1806times 62651000) of the copper +e EWI PTWI ratio ofthe Cu was 052 +is showed that the intake is within thesafe level +e result obtained is higher than the previousstudy carried out by Olmedo et al [46] who reported082mg60 kg personweek (0117times 7) of Cu intake throughfish and shellfish consumption in Andalusia (SouthernSpain) Bat et al [47] study the heavy metals in Mytillusgalloprovincialis from the Turkish Black Sea coasts andfound that EWI of Cu was in the range of 024 to 088mg70 kg personweek (00035times 70 to 00126times 70) with EWI PTWI ratio 01 to 036

4 BioMed Research International

By comparing the data with the mussel in the previousstudies it is notable that the Cu level in the current study washigher than that of those studies It is believed that usingcopper-based pesticide in paddy fields in Perak River anddischarge of municipal sewage increase the Cu concentra-tion in the soil [48 49] +e contaminant leached into theriver and the sediment eventually accumulated in C flu-minea soft tissue [50] +is is supported by Patrick et al [6]who reported C fluminea soft tissue had significantly greaterCu concentrations compared to river and sediment

Copper is an essential trace element for living organismswhich allows the critical enzyme to function properly andassists enzyme in transferring energy into the cells inhumans [51] +e shellfish is an excellent source of Cu forhuman needs [46] However higher copper uptake thanneeded is a double-edged sword that causes adverse effects[52] +e effects include headache vomiting liver andkidney damage and Wilsonrsquos disease [53]

34 Manganese +e Mn level in C fluminea ranged from363 to 2616mgkg ww and has a mean of 1025plusmn 192mgkg ww No significant difference was found betweenMn levelin eachmonth with Pgt 005+ere is no permissible limit formanganese In EWI measurement the C fluminea con-sumers would intake 3681 μgkgweek or around 231mg6265 kg personweek (3681times 62651000) of the manga-nese +e EWI PTWI ratio of the Mn was 376 +isshowed that Mn intake is within the safe level +e currentresult is found to be higher than that of the study by Olmedoet al [46] who reported 035mg60 kg personweek(005times 7) of Mn intake through fish and shellfish con-sumption in Andalusia+e current result is also found to beslightly higher than that of the study by Bat et al [47] whoreported that EWI of the Mn in M galloprovincialis was in

the range of 137 to 221mg70 kg personweek (00196times 70to 00315times 70)

High Mn contamination in C fluminea is associated withaccumulation from the sediment and river+is is supported byHulten et al [54] who reported that sediment is the mainsource of Mn specifically on the surface of the sedimentparticles Moreover wastewater discharged from the metalindustry flows into the river lowering its pH and facilitating thesediment dissolution into the river [55] Hence concentratedMn in river and sediment contributes to high Mn level in Cfluminea

Manganese is an essential element for living organismsTiny amounts of Mn are required to form healthy bonesregulate the blood sugar level maintain the metabolismpromote the digestion and boost the vitamin absorption [56]Overconsumption ofmanganese from food sources is rare [57]When Mn uptake exceeded the required amount it hasnegative impacts on the human body including weaknessmuscle pain less facial expression and clumsy movement ofthe limbs and neurological damage [58 59]

35 Lead Pb detected in C fluminea ranged from 017 to034mgkg ww and has a mean of 062plusmn 012mgkg ww +ePb detection in April and June is significantly different thanthat in other months with Plt 005 +e Pb level is within thepermissible limit set by the European Union of 15mgkg ww[20] In EWI measurement the local people consuming Cfluminea would intake 222μgkgweek or around 014mg6265 kg personweek (222times 62651000) of the lead+eEWI PTWI ratio of Pbwas 888+is showed that the intake rate ofPb is within the safe level

+e current finding is compared with that of the previousstudies Zhelyazkov et al [35] reported that the EWI of Pbfor the Mytilus galloprovincialis was 0001mg70 kg person

Table 1 Concentration of heavy metals (mgkg ww) in C fluminea soft tissue from February to July

Month Cd Cu Mn Pb ZnMeanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE

February 024plusmn 002a 368plusmn 022a 762plusmn 309a 045plusmn 021a 906plusmn 219aMarch 021plusmn 001a 326plusmn 018a 1218plusmn 144a 044plusmn 002ab 1503plusmn 063abApril 023plusmn 001a 897plusmn 122b 691plusmn 094a 086plusmn 004b 2982plusmn 189cMay 020plusmn 001a 494plusmn 064a 816plusmn 149a 049plusmn 005ab 1831plusmn 208bJune 024plusmn 002a 423plusmn 043a 1252plusmn 283a 088plusmn 006b 1667plusmn 145bJuly 026plusmn 001a 512plusmn 015a 1411plusmn 170a 057plusmn 035ab 1606plusmn 155abAverage 023plusmn 001 503plusmn 047 1025plusmn 192 062plusmn 012 1749plusmn 163Letters show significant differences among the months at Plt 005 +e data were presented as meanplusmn standard error

Table 2 +e comparison of the estimated daily intake and estimated weekly intake with the recommended values for C flumineaconsumption

C fluminea (mgkg ww) EDI (μgkgday) ADIa (μgkgday) EWIb (μgkgweek) PTWI (μgkgweek) EWI PTWI ratio ()Cd 023 028 1 084 7c 1200Cu 503 602 350 1806 3500c 052Mn 1025 1227 140 3681 980d 376Pb 062 074 357 222 25c 888Zn 1747 2091 1000 6273 7000c 090aAccepted daily intake which was calculated from PTWI bestimated weekly intake with a frequency of three times consumption per week cPTWI set by FAOWHO [33] dreference dose of Mn established by USEPA [34]

BioMed Research International 5

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

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Page 2: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

antitumor activities [10ndash13] Despite the ecological im-portance and economic benefits the heavy metals poten-tially accumulate in C fluminea soft tissue [5] +e riverpollution and popular smoking method are suspected tocontaminate C fluminea One of the most common heavymetals bioaccumulation in human body is through the foodchain and regular consumption of contaminated food [14]+e relationship between the heavy metals concentrationsin this clam and associated health risk assessment inKelantan is yet to e reported +e local people lack in-formation about the safety of C fluminea consumptionHence this research aims to determine the selected heavy-metal (cadmium copper manganese lead and zinc) levelin C fluminea soft tissue that is sold in the streets and assessthe human health risk +ese selected heavy metals andtheir effects on human health are of great concern based onthe previous studies [5 15ndash17] +e health risk assessmentis carried out on the ready-to-eat C fluminea sold along theroadside +e provisional tolerable weekly intake (PTWI)target hazard quotient (THQ) and hazard index (HI) wereused to evaluate the health risk

2 Materials and Methods

21 Study Area +e samples were collected at Pasir Mas andTumpat Kelantan (60495938N 1021693547E and61467273N 102218605E) for six months duration Six stallsofC flumineawere selected due to their availability throughoutthe year (Figure 1) +e primary source of C fluminea used inthese stalls is fromPerak River which is located close to oil palmplantations durian farms and urban area Around 1kgsmoked C fluminea was collected from each seller for theheavy-metal analysis Each sample was labelled with the datetime collection site and weather +e samples were preservedat 4degC by storing in an ice box during their transportation to thelaboratory [18] +e samples were stored in a freezer at minus 20degCbefore analysis

22 Sample Analysis +e soft tissues of C fluminea wereobtained using a blade and oven dried (60degC 72 hours) toconstant weight After that the samples were ground intohomogenous samples using a mill machine (PanasonicregMX-900M) +e samples were preserved in amber jars and storedin a desiccator before acid digestion +e digestion processwas carried out by following the standard method by Per-kinElmer Corporation [19]

Approximately 5 g of dried samples was placed in the250mL beaker in which 5mL of 95 sulfuric acid (Merck)and 5mL of 65 nitric acid (Merck) were added +esamples were covered immediately with watch glass Afterthe reaction between sample and acid was completed themixtures were heated at 60degC for 30 minutes using hot plates(IKAreg C-MAGHS 7)+e samples were allowed to cool and20mL of 65 nitric acid was added +e temperature wasincreased slowly to 150degC for two hours +en the solutionswere allowed to cool and 1mL of 30 hydrogen peroxide(Merck) was added until the colour became clear Sampleswere diluted to 50ml with deionized water +e solutions

were then filtered by filter paper (Whatmanreg No 41 filtercircles 125mm) and syringe filter (Minisartreg nylon syringefilter 25mm)

+e samples analysis was analysed by using the flameatomic absorption spectrophotometer PinAACLE 900F andmeasured in triplicates +e accuracy and validity of theapplied protocol were evaluated using the Standard Refer-ence Materials (SRM 2976 National Institute of Standardsand Technology) due to its suitability in the mussel sampleand matrix Recovery rates were found to be between9998ndash11008 for the selected metals

23 Human Health Risk Assessment (HHRA) All data ob-tained were converted into wet weight (ww) using a con-version factor of 019 +e conversion factor is based on themoisture analysis carried out in the food laboratory Uni-versiti Malaysia Kelantan by our research assistant Siti NorAini Md Nasir on 28 October 2018

(a) Maximum permissible limit (MPL) of the heavymetals for the consumers set by the European Union[20] and FAO compilation of the legal limits by FAO[21]

(b) +e estimated daily intakes (EDIs) of the consumersin order to evaluate the adverse health effects+e JECFA uses the term estimated daily intake(EDI) and provisional tolerable daily intake (PTDI)for contaminants as heavy metals that can accu-mulate in the human body [22] Estimated dailyintake (EDI) (μgkg body weight) of heavy metalsfrom C fluminea consumption was obtained usingthe following equation (1) [23 24]

EDI Cmetal times IR( 1113857

BW (1)

where EDI is estimated daily intake and Cmetal (mgkgww) is an average weighted heavy metal content in Cfluminea Ingestion rate (IR) (gramday person) is thedaily mussel consumption BW is the average bodyweight +e average IR is determined by interviewingthe local people using a simple questionnaire +eaverage IR of C fluminea for Malaysian adults is 75 gday person which is similar to the literature [2] +eaverage body weight for Malaysians was 6265 kg [25]To obtain estimated weekly intake (EWI) the EDIwill be multiplied by a factor of 7 corresponding to 7days However based on questionnaires and in-terviews the local people consume C fluminea witha frequency of three days per week Hence EWI wasobtained using the following equation

EWIthis study EDI times 7 times37 (2)

+e EWIthis study is compared to the JECFA pro-visional tolerable weekly intake (PTWI)

(c) Target hazard quotient has been recognised as auseful parameter for evaluation of risk associated

2 BioMed Research International

with the consumption of metal contaminated foodTo assess the noncarcinogenic risk due to heavymetal exposure in C uminea soft tissue the targethazard quotient (THQ) was computed using thefollowing equation [26]

THQ EFr times ED times IR timesMCRfD times BW times AT

[ ] times 10minus 3 (3)

where EFr is exposure frequency (156 days per year forthe average consumer according to the local in-terview) ED is exposure duration (70 years) equiv-alent to the average human lifespan IR is the ingestionrate (75 grams per person per day) MC is the metalconcentration in C uminea soft tissue (in mgkgww) RfD is the oral reference dose (Cd is 1mgkg wtday Cu 40mgkg wtday Zn 300mgkg wtday andMn 140mgkg wtday) [27]e reference dose (RfD)

is an estimate of the daily intake of contaminantduring a lifetime that would not cause adverse healtheects to the human [28] BW is the average bodyweight (6265 kg) AT is the averaging time fornoncarcinogens (ie 30 years or 10950 days)With the refusal to set the reference dose of Pb byEPA [29] the THQ for Pb was calculated by usingthe following equation [30]

THQ CPb

MPL (4)

where CPb is the Pb concentration in C uminea(mgkg ww) MPL maximum permissible limit Inthis study the MPL of Pb for bivalve is 150mgkgww [20]THQlt 1 indicates no obvious risk A THQ gt1 showsthat the level of exposure is higher than the oral

Scale

0 20km 40km

Sampling pointsKelantan

102deg0prime0PrimeE

6deg0prime0PrimeN

5deg0prime0PrimeN

6deg0prime0PrimeN

102deg0prime0PrimeE

Pengkalan Chepa

Tumpat

Kelantan

5deg0prime0PrimeN

N

S

EW

Figure 1 e map of the Kelantan state Malaysia e study area and sampling points of C uminea were at Pasir Mas and TumpatKelantan

BioMed Research International 3

reference dose (ORD) which assumes that a daily ex-posure at this level is likely to cause harmful healtheffects during the lifetime in a human population [31]Following EPA guidelines we assumed that the ingesteddose was equal to the absorbed contaminant dose

(d) +e hazard index (HI) calculated from THQ is thetotal of the hazard quotients [23 32]HI THQCd + THQCu + THQMn + THQPb + THQZn

(5)

If HI less than 1 there is no obvious risk

24 Statistical Analysis +e metal concentrations for sixsellers were averaged to obtain the mean Microsoft Excelwas used to tabulate all the data throughout the experimentand generate the hazard index graph SPSS 23 for Windowswas used to run the statistical analysis including the meanstandard error and one-way ANOVA with Tukey post hoctest +e statistical significance was significant whenPlt 005

3 Results and Discussions

31 Heavy-Metal Concentration in C fluminea and HumanHealth Risk Assessment +e mean concentration of Cd CrCu Mn Pb and Zn (mgkg ww) in C fluminea from theroadside stalls which are consumed by local people istabulated in Table 1 +e values in each month are the meanfrom six stalls Metal concentration in C fluminea exhibitedan order of ZngtMngtCugtPbgtCd

In this study dietary exposure to heavy metals throughconsumption of C fluminea in the studied areas was eval-uated using estimated daily intake (EDI) by considering theaverage concentration of the heavy metals and the respectiveconsumption rate for adults +en the estimated weeklyintake (EWI) was calculated and compared with PTWITable 2 shows the values of EDI EWI PTWI and EWI PTWI ratio

32 Cadmium Cd detected in C fluminea ranged from 017to 034mgkg ww and has a mean of 023plusmn 001mgkg wwNo significant difference was found between Cd levels ineach month with Pgt 005 +e Cd level is within the per-missible limit set by the European Union of 10mgkg ww[20] In EWI measurement the local people consumingC fluminea would intake 084μgkgweek or 005mg6265 kgpersonweek (084times 62651000) of the Cd +e EWI PTWIratio of the Cd was 1200 +is showed that the intake iswithin the safe level

+e current result is found to be higher than that in thestudy by Zhelyazkov et al [35] who reported the EWI ofCd for the marine mollusc (Mytilus galloprovincialis) was0002mg70 kg personweek (00032 times 70 times 71000) Be-sides Yunus et al [36] study the metal level in the cockles(Anadara granosa) from Kuala Selangor Malaysia +eyreported 596 μg70 kgdaily or 004mg70 kg personweek (596 times 71000) of Cd intake with cockle

consumption which is also lower than the EWI value of Cdin the current study Sharif et al [37] study on con-sumption of shellfish clam (Metretrix spp) scallop(Amusium pleuronectes) and conch (Strombus canarium)at Kudat Sabah +ey reported that if the local peopleconsume these shellfish every day the EWI values of Cdfor Metretrix spp Amusium pleuronectes and Strombuscanarium were 001mg6265 kg personweek(003 times 7 times 62651000) 069mg6265 kg personweek(158 times 7 times 62651000) and 0009mg6265 kg personweek (002 times 7 times 62651000) respectively

EWI of Cd (005mg6265 kg personweek) in thecurrent study is higher than that of previous studies exceptthe scallop (Amusium pleuronectes) High EWI of Cd in Cfluminea is due to high ingestion rate and high Cd con-centration in C fluminea Cd is mainly used in industriesincludes electroplating alloy production pigments andbattery production [38] +is is in agreement in the currentstudy where metal industries automobile workshops andlaptop shops can be found near to Perak River +e Cd indischarged wastewater is easily deposited into rivertransferred to aquatic life and eventually accumulated inhuman body through the food chain [39] As a filter feedingorganism C fluminea is reported susceptible to heavy-metal exposure in river and possess high metal level [5]

Cadmium is a nonessential element for human anddetrimental to our health even when ingested in smallquantities Food is the primary source of Cd exposurebesides cigarette smoking [40 41] Continuous Cd con-sumption leads to respiratory system damage lung cancerParkinsonrsquos and Wilsonrsquos diseases and estrogen receptor-positive breast cancer in postmenopausal women [42 43] InJapan consumption of Cd-contaminated rice causes oste-omalacia (bone disease) and kidney malfunction to the localpeople [44] Cd-poisoning patients need to be treated withgastrointestinal tract irrigation supportive care andchemical decontamination with chelating agents andnanoparticle-based antidotes [45]

33 Copper +e Cu detected in C fluminea ranged from264 to 1261mgkg ww and has a mean of 503plusmn 047mgkgww+ere is no significant difference between the Cu level inevery month with Pgt 005 except in April with Plt 005+eCu level is within the permissible limit of 20 to 70mgkg wwset by FAO compilation of the legal limits [21] In EWImeasurement the C fluminea consumer would intake1806 μgkgweek or around 113mg6265 kg personweek(1806times 62651000) of the copper +e EWI PTWI ratio ofthe Cu was 052 +is showed that the intake is within thesafe level +e result obtained is higher than the previousstudy carried out by Olmedo et al [46] who reported082mg60 kg personweek (0117times 7) of Cu intake throughfish and shellfish consumption in Andalusia (SouthernSpain) Bat et al [47] study the heavy metals in Mytillusgalloprovincialis from the Turkish Black Sea coasts andfound that EWI of Cu was in the range of 024 to 088mg70 kg personweek (00035times 70 to 00126times 70) with EWI PTWI ratio 01 to 036

4 BioMed Research International

By comparing the data with the mussel in the previousstudies it is notable that the Cu level in the current study washigher than that of those studies It is believed that usingcopper-based pesticide in paddy fields in Perak River anddischarge of municipal sewage increase the Cu concentra-tion in the soil [48 49] +e contaminant leached into theriver and the sediment eventually accumulated in C flu-minea soft tissue [50] +is is supported by Patrick et al [6]who reported C fluminea soft tissue had significantly greaterCu concentrations compared to river and sediment

Copper is an essential trace element for living organismswhich allows the critical enzyme to function properly andassists enzyme in transferring energy into the cells inhumans [51] +e shellfish is an excellent source of Cu forhuman needs [46] However higher copper uptake thanneeded is a double-edged sword that causes adverse effects[52] +e effects include headache vomiting liver andkidney damage and Wilsonrsquos disease [53]

34 Manganese +e Mn level in C fluminea ranged from363 to 2616mgkg ww and has a mean of 1025plusmn 192mgkg ww No significant difference was found betweenMn levelin eachmonth with Pgt 005+ere is no permissible limit formanganese In EWI measurement the C fluminea con-sumers would intake 3681 μgkgweek or around 231mg6265 kg personweek (3681times 62651000) of the manga-nese +e EWI PTWI ratio of the Mn was 376 +isshowed that Mn intake is within the safe level +e currentresult is found to be higher than that of the study by Olmedoet al [46] who reported 035mg60 kg personweek(005times 7) of Mn intake through fish and shellfish con-sumption in Andalusia+e current result is also found to beslightly higher than that of the study by Bat et al [47] whoreported that EWI of the Mn in M galloprovincialis was in

the range of 137 to 221mg70 kg personweek (00196times 70to 00315times 70)

High Mn contamination in C fluminea is associated withaccumulation from the sediment and river+is is supported byHulten et al [54] who reported that sediment is the mainsource of Mn specifically on the surface of the sedimentparticles Moreover wastewater discharged from the metalindustry flows into the river lowering its pH and facilitating thesediment dissolution into the river [55] Hence concentratedMn in river and sediment contributes to high Mn level in Cfluminea

Manganese is an essential element for living organismsTiny amounts of Mn are required to form healthy bonesregulate the blood sugar level maintain the metabolismpromote the digestion and boost the vitamin absorption [56]Overconsumption ofmanganese from food sources is rare [57]When Mn uptake exceeded the required amount it hasnegative impacts on the human body including weaknessmuscle pain less facial expression and clumsy movement ofthe limbs and neurological damage [58 59]

35 Lead Pb detected in C fluminea ranged from 017 to034mgkg ww and has a mean of 062plusmn 012mgkg ww +ePb detection in April and June is significantly different thanthat in other months with Plt 005 +e Pb level is within thepermissible limit set by the European Union of 15mgkg ww[20] In EWI measurement the local people consuming Cfluminea would intake 222μgkgweek or around 014mg6265 kg personweek (222times 62651000) of the lead+eEWI PTWI ratio of Pbwas 888+is showed that the intake rate ofPb is within the safe level

+e current finding is compared with that of the previousstudies Zhelyazkov et al [35] reported that the EWI of Pbfor the Mytilus galloprovincialis was 0001mg70 kg person

Table 1 Concentration of heavy metals (mgkg ww) in C fluminea soft tissue from February to July

Month Cd Cu Mn Pb ZnMeanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE

February 024plusmn 002a 368plusmn 022a 762plusmn 309a 045plusmn 021a 906plusmn 219aMarch 021plusmn 001a 326plusmn 018a 1218plusmn 144a 044plusmn 002ab 1503plusmn 063abApril 023plusmn 001a 897plusmn 122b 691plusmn 094a 086plusmn 004b 2982plusmn 189cMay 020plusmn 001a 494plusmn 064a 816plusmn 149a 049plusmn 005ab 1831plusmn 208bJune 024plusmn 002a 423plusmn 043a 1252plusmn 283a 088plusmn 006b 1667plusmn 145bJuly 026plusmn 001a 512plusmn 015a 1411plusmn 170a 057plusmn 035ab 1606plusmn 155abAverage 023plusmn 001 503plusmn 047 1025plusmn 192 062plusmn 012 1749plusmn 163Letters show significant differences among the months at Plt 005 +e data were presented as meanplusmn standard error

Table 2 +e comparison of the estimated daily intake and estimated weekly intake with the recommended values for C flumineaconsumption

C fluminea (mgkg ww) EDI (μgkgday) ADIa (μgkgday) EWIb (μgkgweek) PTWI (μgkgweek) EWI PTWI ratio ()Cd 023 028 1 084 7c 1200Cu 503 602 350 1806 3500c 052Mn 1025 1227 140 3681 980d 376Pb 062 074 357 222 25c 888Zn 1747 2091 1000 6273 7000c 090aAccepted daily intake which was calculated from PTWI bestimated weekly intake with a frequency of three times consumption per week cPTWI set by FAOWHO [33] dreference dose of Mn established by USEPA [34]

BioMed Research International 5

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

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[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

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[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

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Page 3: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

with the consumption of metal contaminated foodTo assess the noncarcinogenic risk due to heavymetal exposure in C uminea soft tissue the targethazard quotient (THQ) was computed using thefollowing equation [26]

THQ EFr times ED times IR timesMCRfD times BW times AT

[ ] times 10minus 3 (3)

where EFr is exposure frequency (156 days per year forthe average consumer according to the local in-terview) ED is exposure duration (70 years) equiv-alent to the average human lifespan IR is the ingestionrate (75 grams per person per day) MC is the metalconcentration in C uminea soft tissue (in mgkgww) RfD is the oral reference dose (Cd is 1mgkg wtday Cu 40mgkg wtday Zn 300mgkg wtday andMn 140mgkg wtday) [27]e reference dose (RfD)

is an estimate of the daily intake of contaminantduring a lifetime that would not cause adverse healtheects to the human [28] BW is the average bodyweight (6265 kg) AT is the averaging time fornoncarcinogens (ie 30 years or 10950 days)With the refusal to set the reference dose of Pb byEPA [29] the THQ for Pb was calculated by usingthe following equation [30]

THQ CPb

MPL (4)

where CPb is the Pb concentration in C uminea(mgkg ww) MPL maximum permissible limit Inthis study the MPL of Pb for bivalve is 150mgkgww [20]THQlt 1 indicates no obvious risk A THQ gt1 showsthat the level of exposure is higher than the oral

Scale

0 20km 40km

Sampling pointsKelantan

102deg0prime0PrimeE

6deg0prime0PrimeN

5deg0prime0PrimeN

6deg0prime0PrimeN

102deg0prime0PrimeE

Pengkalan Chepa

Tumpat

Kelantan

5deg0prime0PrimeN

N

S

EW

Figure 1 e map of the Kelantan state Malaysia e study area and sampling points of C uminea were at Pasir Mas and TumpatKelantan

BioMed Research International 3

reference dose (ORD) which assumes that a daily ex-posure at this level is likely to cause harmful healtheffects during the lifetime in a human population [31]Following EPA guidelines we assumed that the ingesteddose was equal to the absorbed contaminant dose

(d) +e hazard index (HI) calculated from THQ is thetotal of the hazard quotients [23 32]HI THQCd + THQCu + THQMn + THQPb + THQZn

(5)

If HI less than 1 there is no obvious risk

24 Statistical Analysis +e metal concentrations for sixsellers were averaged to obtain the mean Microsoft Excelwas used to tabulate all the data throughout the experimentand generate the hazard index graph SPSS 23 for Windowswas used to run the statistical analysis including the meanstandard error and one-way ANOVA with Tukey post hoctest +e statistical significance was significant whenPlt 005

3 Results and Discussions

31 Heavy-Metal Concentration in C fluminea and HumanHealth Risk Assessment +e mean concentration of Cd CrCu Mn Pb and Zn (mgkg ww) in C fluminea from theroadside stalls which are consumed by local people istabulated in Table 1 +e values in each month are the meanfrom six stalls Metal concentration in C fluminea exhibitedan order of ZngtMngtCugtPbgtCd

In this study dietary exposure to heavy metals throughconsumption of C fluminea in the studied areas was eval-uated using estimated daily intake (EDI) by considering theaverage concentration of the heavy metals and the respectiveconsumption rate for adults +en the estimated weeklyintake (EWI) was calculated and compared with PTWITable 2 shows the values of EDI EWI PTWI and EWI PTWI ratio

32 Cadmium Cd detected in C fluminea ranged from 017to 034mgkg ww and has a mean of 023plusmn 001mgkg wwNo significant difference was found between Cd levels ineach month with Pgt 005 +e Cd level is within the per-missible limit set by the European Union of 10mgkg ww[20] In EWI measurement the local people consumingC fluminea would intake 084μgkgweek or 005mg6265 kgpersonweek (084times 62651000) of the Cd +e EWI PTWIratio of the Cd was 1200 +is showed that the intake iswithin the safe level

+e current result is found to be higher than that in thestudy by Zhelyazkov et al [35] who reported the EWI ofCd for the marine mollusc (Mytilus galloprovincialis) was0002mg70 kg personweek (00032 times 70 times 71000) Be-sides Yunus et al [36] study the metal level in the cockles(Anadara granosa) from Kuala Selangor Malaysia +eyreported 596 μg70 kgdaily or 004mg70 kg personweek (596 times 71000) of Cd intake with cockle

consumption which is also lower than the EWI value of Cdin the current study Sharif et al [37] study on con-sumption of shellfish clam (Metretrix spp) scallop(Amusium pleuronectes) and conch (Strombus canarium)at Kudat Sabah +ey reported that if the local peopleconsume these shellfish every day the EWI values of Cdfor Metretrix spp Amusium pleuronectes and Strombuscanarium were 001mg6265 kg personweek(003 times 7 times 62651000) 069mg6265 kg personweek(158 times 7 times 62651000) and 0009mg6265 kg personweek (002 times 7 times 62651000) respectively

EWI of Cd (005mg6265 kg personweek) in thecurrent study is higher than that of previous studies exceptthe scallop (Amusium pleuronectes) High EWI of Cd in Cfluminea is due to high ingestion rate and high Cd con-centration in C fluminea Cd is mainly used in industriesincludes electroplating alloy production pigments andbattery production [38] +is is in agreement in the currentstudy where metal industries automobile workshops andlaptop shops can be found near to Perak River +e Cd indischarged wastewater is easily deposited into rivertransferred to aquatic life and eventually accumulated inhuman body through the food chain [39] As a filter feedingorganism C fluminea is reported susceptible to heavy-metal exposure in river and possess high metal level [5]

Cadmium is a nonessential element for human anddetrimental to our health even when ingested in smallquantities Food is the primary source of Cd exposurebesides cigarette smoking [40 41] Continuous Cd con-sumption leads to respiratory system damage lung cancerParkinsonrsquos and Wilsonrsquos diseases and estrogen receptor-positive breast cancer in postmenopausal women [42 43] InJapan consumption of Cd-contaminated rice causes oste-omalacia (bone disease) and kidney malfunction to the localpeople [44] Cd-poisoning patients need to be treated withgastrointestinal tract irrigation supportive care andchemical decontamination with chelating agents andnanoparticle-based antidotes [45]

33 Copper +e Cu detected in C fluminea ranged from264 to 1261mgkg ww and has a mean of 503plusmn 047mgkgww+ere is no significant difference between the Cu level inevery month with Pgt 005 except in April with Plt 005+eCu level is within the permissible limit of 20 to 70mgkg wwset by FAO compilation of the legal limits [21] In EWImeasurement the C fluminea consumer would intake1806 μgkgweek or around 113mg6265 kg personweek(1806times 62651000) of the copper +e EWI PTWI ratio ofthe Cu was 052 +is showed that the intake is within thesafe level +e result obtained is higher than the previousstudy carried out by Olmedo et al [46] who reported082mg60 kg personweek (0117times 7) of Cu intake throughfish and shellfish consumption in Andalusia (SouthernSpain) Bat et al [47] study the heavy metals in Mytillusgalloprovincialis from the Turkish Black Sea coasts andfound that EWI of Cu was in the range of 024 to 088mg70 kg personweek (00035times 70 to 00126times 70) with EWI PTWI ratio 01 to 036

4 BioMed Research International

By comparing the data with the mussel in the previousstudies it is notable that the Cu level in the current study washigher than that of those studies It is believed that usingcopper-based pesticide in paddy fields in Perak River anddischarge of municipal sewage increase the Cu concentra-tion in the soil [48 49] +e contaminant leached into theriver and the sediment eventually accumulated in C flu-minea soft tissue [50] +is is supported by Patrick et al [6]who reported C fluminea soft tissue had significantly greaterCu concentrations compared to river and sediment

Copper is an essential trace element for living organismswhich allows the critical enzyme to function properly andassists enzyme in transferring energy into the cells inhumans [51] +e shellfish is an excellent source of Cu forhuman needs [46] However higher copper uptake thanneeded is a double-edged sword that causes adverse effects[52] +e effects include headache vomiting liver andkidney damage and Wilsonrsquos disease [53]

34 Manganese +e Mn level in C fluminea ranged from363 to 2616mgkg ww and has a mean of 1025plusmn 192mgkg ww No significant difference was found betweenMn levelin eachmonth with Pgt 005+ere is no permissible limit formanganese In EWI measurement the C fluminea con-sumers would intake 3681 μgkgweek or around 231mg6265 kg personweek (3681times 62651000) of the manga-nese +e EWI PTWI ratio of the Mn was 376 +isshowed that Mn intake is within the safe level +e currentresult is found to be higher than that of the study by Olmedoet al [46] who reported 035mg60 kg personweek(005times 7) of Mn intake through fish and shellfish con-sumption in Andalusia+e current result is also found to beslightly higher than that of the study by Bat et al [47] whoreported that EWI of the Mn in M galloprovincialis was in

the range of 137 to 221mg70 kg personweek (00196times 70to 00315times 70)

High Mn contamination in C fluminea is associated withaccumulation from the sediment and river+is is supported byHulten et al [54] who reported that sediment is the mainsource of Mn specifically on the surface of the sedimentparticles Moreover wastewater discharged from the metalindustry flows into the river lowering its pH and facilitating thesediment dissolution into the river [55] Hence concentratedMn in river and sediment contributes to high Mn level in Cfluminea

Manganese is an essential element for living organismsTiny amounts of Mn are required to form healthy bonesregulate the blood sugar level maintain the metabolismpromote the digestion and boost the vitamin absorption [56]Overconsumption ofmanganese from food sources is rare [57]When Mn uptake exceeded the required amount it hasnegative impacts on the human body including weaknessmuscle pain less facial expression and clumsy movement ofthe limbs and neurological damage [58 59]

35 Lead Pb detected in C fluminea ranged from 017 to034mgkg ww and has a mean of 062plusmn 012mgkg ww +ePb detection in April and June is significantly different thanthat in other months with Plt 005 +e Pb level is within thepermissible limit set by the European Union of 15mgkg ww[20] In EWI measurement the local people consuming Cfluminea would intake 222μgkgweek or around 014mg6265 kg personweek (222times 62651000) of the lead+eEWI PTWI ratio of Pbwas 888+is showed that the intake rate ofPb is within the safe level

+e current finding is compared with that of the previousstudies Zhelyazkov et al [35] reported that the EWI of Pbfor the Mytilus galloprovincialis was 0001mg70 kg person

Table 1 Concentration of heavy metals (mgkg ww) in C fluminea soft tissue from February to July

Month Cd Cu Mn Pb ZnMeanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE

February 024plusmn 002a 368plusmn 022a 762plusmn 309a 045plusmn 021a 906plusmn 219aMarch 021plusmn 001a 326plusmn 018a 1218plusmn 144a 044plusmn 002ab 1503plusmn 063abApril 023plusmn 001a 897plusmn 122b 691plusmn 094a 086plusmn 004b 2982plusmn 189cMay 020plusmn 001a 494plusmn 064a 816plusmn 149a 049plusmn 005ab 1831plusmn 208bJune 024plusmn 002a 423plusmn 043a 1252plusmn 283a 088plusmn 006b 1667plusmn 145bJuly 026plusmn 001a 512plusmn 015a 1411plusmn 170a 057plusmn 035ab 1606plusmn 155abAverage 023plusmn 001 503plusmn 047 1025plusmn 192 062plusmn 012 1749plusmn 163Letters show significant differences among the months at Plt 005 +e data were presented as meanplusmn standard error

Table 2 +e comparison of the estimated daily intake and estimated weekly intake with the recommended values for C flumineaconsumption

C fluminea (mgkg ww) EDI (μgkgday) ADIa (μgkgday) EWIb (μgkgweek) PTWI (μgkgweek) EWI PTWI ratio ()Cd 023 028 1 084 7c 1200Cu 503 602 350 1806 3500c 052Mn 1025 1227 140 3681 980d 376Pb 062 074 357 222 25c 888Zn 1747 2091 1000 6273 7000c 090aAccepted daily intake which was calculated from PTWI bestimated weekly intake with a frequency of three times consumption per week cPTWI set by FAOWHO [33] dreference dose of Mn established by USEPA [34]

BioMed Research International 5

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

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Page 4: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

reference dose (ORD) which assumes that a daily ex-posure at this level is likely to cause harmful healtheffects during the lifetime in a human population [31]Following EPA guidelines we assumed that the ingesteddose was equal to the absorbed contaminant dose

(d) +e hazard index (HI) calculated from THQ is thetotal of the hazard quotients [23 32]HI THQCd + THQCu + THQMn + THQPb + THQZn

(5)

If HI less than 1 there is no obvious risk

24 Statistical Analysis +e metal concentrations for sixsellers were averaged to obtain the mean Microsoft Excelwas used to tabulate all the data throughout the experimentand generate the hazard index graph SPSS 23 for Windowswas used to run the statistical analysis including the meanstandard error and one-way ANOVA with Tukey post hoctest +e statistical significance was significant whenPlt 005

3 Results and Discussions

31 Heavy-Metal Concentration in C fluminea and HumanHealth Risk Assessment +e mean concentration of Cd CrCu Mn Pb and Zn (mgkg ww) in C fluminea from theroadside stalls which are consumed by local people istabulated in Table 1 +e values in each month are the meanfrom six stalls Metal concentration in C fluminea exhibitedan order of ZngtMngtCugtPbgtCd

In this study dietary exposure to heavy metals throughconsumption of C fluminea in the studied areas was eval-uated using estimated daily intake (EDI) by considering theaverage concentration of the heavy metals and the respectiveconsumption rate for adults +en the estimated weeklyintake (EWI) was calculated and compared with PTWITable 2 shows the values of EDI EWI PTWI and EWI PTWI ratio

32 Cadmium Cd detected in C fluminea ranged from 017to 034mgkg ww and has a mean of 023plusmn 001mgkg wwNo significant difference was found between Cd levels ineach month with Pgt 005 +e Cd level is within the per-missible limit set by the European Union of 10mgkg ww[20] In EWI measurement the local people consumingC fluminea would intake 084μgkgweek or 005mg6265 kgpersonweek (084times 62651000) of the Cd +e EWI PTWIratio of the Cd was 1200 +is showed that the intake iswithin the safe level

+e current result is found to be higher than that in thestudy by Zhelyazkov et al [35] who reported the EWI ofCd for the marine mollusc (Mytilus galloprovincialis) was0002mg70 kg personweek (00032 times 70 times 71000) Be-sides Yunus et al [36] study the metal level in the cockles(Anadara granosa) from Kuala Selangor Malaysia +eyreported 596 μg70 kgdaily or 004mg70 kg personweek (596 times 71000) of Cd intake with cockle

consumption which is also lower than the EWI value of Cdin the current study Sharif et al [37] study on con-sumption of shellfish clam (Metretrix spp) scallop(Amusium pleuronectes) and conch (Strombus canarium)at Kudat Sabah +ey reported that if the local peopleconsume these shellfish every day the EWI values of Cdfor Metretrix spp Amusium pleuronectes and Strombuscanarium were 001mg6265 kg personweek(003 times 7 times 62651000) 069mg6265 kg personweek(158 times 7 times 62651000) and 0009mg6265 kg personweek (002 times 7 times 62651000) respectively

EWI of Cd (005mg6265 kg personweek) in thecurrent study is higher than that of previous studies exceptthe scallop (Amusium pleuronectes) High EWI of Cd in Cfluminea is due to high ingestion rate and high Cd con-centration in C fluminea Cd is mainly used in industriesincludes electroplating alloy production pigments andbattery production [38] +is is in agreement in the currentstudy where metal industries automobile workshops andlaptop shops can be found near to Perak River +e Cd indischarged wastewater is easily deposited into rivertransferred to aquatic life and eventually accumulated inhuman body through the food chain [39] As a filter feedingorganism C fluminea is reported susceptible to heavy-metal exposure in river and possess high metal level [5]

Cadmium is a nonessential element for human anddetrimental to our health even when ingested in smallquantities Food is the primary source of Cd exposurebesides cigarette smoking [40 41] Continuous Cd con-sumption leads to respiratory system damage lung cancerParkinsonrsquos and Wilsonrsquos diseases and estrogen receptor-positive breast cancer in postmenopausal women [42 43] InJapan consumption of Cd-contaminated rice causes oste-omalacia (bone disease) and kidney malfunction to the localpeople [44] Cd-poisoning patients need to be treated withgastrointestinal tract irrigation supportive care andchemical decontamination with chelating agents andnanoparticle-based antidotes [45]

33 Copper +e Cu detected in C fluminea ranged from264 to 1261mgkg ww and has a mean of 503plusmn 047mgkgww+ere is no significant difference between the Cu level inevery month with Pgt 005 except in April with Plt 005+eCu level is within the permissible limit of 20 to 70mgkg wwset by FAO compilation of the legal limits [21] In EWImeasurement the C fluminea consumer would intake1806 μgkgweek or around 113mg6265 kg personweek(1806times 62651000) of the copper +e EWI PTWI ratio ofthe Cu was 052 +is showed that the intake is within thesafe level +e result obtained is higher than the previousstudy carried out by Olmedo et al [46] who reported082mg60 kg personweek (0117times 7) of Cu intake throughfish and shellfish consumption in Andalusia (SouthernSpain) Bat et al [47] study the heavy metals in Mytillusgalloprovincialis from the Turkish Black Sea coasts andfound that EWI of Cu was in the range of 024 to 088mg70 kg personweek (00035times 70 to 00126times 70) with EWI PTWI ratio 01 to 036

4 BioMed Research International

By comparing the data with the mussel in the previousstudies it is notable that the Cu level in the current study washigher than that of those studies It is believed that usingcopper-based pesticide in paddy fields in Perak River anddischarge of municipal sewage increase the Cu concentra-tion in the soil [48 49] +e contaminant leached into theriver and the sediment eventually accumulated in C flu-minea soft tissue [50] +is is supported by Patrick et al [6]who reported C fluminea soft tissue had significantly greaterCu concentrations compared to river and sediment

Copper is an essential trace element for living organismswhich allows the critical enzyme to function properly andassists enzyme in transferring energy into the cells inhumans [51] +e shellfish is an excellent source of Cu forhuman needs [46] However higher copper uptake thanneeded is a double-edged sword that causes adverse effects[52] +e effects include headache vomiting liver andkidney damage and Wilsonrsquos disease [53]

34 Manganese +e Mn level in C fluminea ranged from363 to 2616mgkg ww and has a mean of 1025plusmn 192mgkg ww No significant difference was found betweenMn levelin eachmonth with Pgt 005+ere is no permissible limit formanganese In EWI measurement the C fluminea con-sumers would intake 3681 μgkgweek or around 231mg6265 kg personweek (3681times 62651000) of the manga-nese +e EWI PTWI ratio of the Mn was 376 +isshowed that Mn intake is within the safe level +e currentresult is found to be higher than that of the study by Olmedoet al [46] who reported 035mg60 kg personweek(005times 7) of Mn intake through fish and shellfish con-sumption in Andalusia+e current result is also found to beslightly higher than that of the study by Bat et al [47] whoreported that EWI of the Mn in M galloprovincialis was in

the range of 137 to 221mg70 kg personweek (00196times 70to 00315times 70)

High Mn contamination in C fluminea is associated withaccumulation from the sediment and river+is is supported byHulten et al [54] who reported that sediment is the mainsource of Mn specifically on the surface of the sedimentparticles Moreover wastewater discharged from the metalindustry flows into the river lowering its pH and facilitating thesediment dissolution into the river [55] Hence concentratedMn in river and sediment contributes to high Mn level in Cfluminea

Manganese is an essential element for living organismsTiny amounts of Mn are required to form healthy bonesregulate the blood sugar level maintain the metabolismpromote the digestion and boost the vitamin absorption [56]Overconsumption ofmanganese from food sources is rare [57]When Mn uptake exceeded the required amount it hasnegative impacts on the human body including weaknessmuscle pain less facial expression and clumsy movement ofthe limbs and neurological damage [58 59]

35 Lead Pb detected in C fluminea ranged from 017 to034mgkg ww and has a mean of 062plusmn 012mgkg ww +ePb detection in April and June is significantly different thanthat in other months with Plt 005 +e Pb level is within thepermissible limit set by the European Union of 15mgkg ww[20] In EWI measurement the local people consuming Cfluminea would intake 222μgkgweek or around 014mg6265 kg personweek (222times 62651000) of the lead+eEWI PTWI ratio of Pbwas 888+is showed that the intake rate ofPb is within the safe level

+e current finding is compared with that of the previousstudies Zhelyazkov et al [35] reported that the EWI of Pbfor the Mytilus galloprovincialis was 0001mg70 kg person

Table 1 Concentration of heavy metals (mgkg ww) in C fluminea soft tissue from February to July

Month Cd Cu Mn Pb ZnMeanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE

February 024plusmn 002a 368plusmn 022a 762plusmn 309a 045plusmn 021a 906plusmn 219aMarch 021plusmn 001a 326plusmn 018a 1218plusmn 144a 044plusmn 002ab 1503plusmn 063abApril 023plusmn 001a 897plusmn 122b 691plusmn 094a 086plusmn 004b 2982plusmn 189cMay 020plusmn 001a 494plusmn 064a 816plusmn 149a 049plusmn 005ab 1831plusmn 208bJune 024plusmn 002a 423plusmn 043a 1252plusmn 283a 088plusmn 006b 1667plusmn 145bJuly 026plusmn 001a 512plusmn 015a 1411plusmn 170a 057plusmn 035ab 1606plusmn 155abAverage 023plusmn 001 503plusmn 047 1025plusmn 192 062plusmn 012 1749plusmn 163Letters show significant differences among the months at Plt 005 +e data were presented as meanplusmn standard error

Table 2 +e comparison of the estimated daily intake and estimated weekly intake with the recommended values for C flumineaconsumption

C fluminea (mgkg ww) EDI (μgkgday) ADIa (μgkgday) EWIb (μgkgweek) PTWI (μgkgweek) EWI PTWI ratio ()Cd 023 028 1 084 7c 1200Cu 503 602 350 1806 3500c 052Mn 1025 1227 140 3681 980d 376Pb 062 074 357 222 25c 888Zn 1747 2091 1000 6273 7000c 090aAccepted daily intake which was calculated from PTWI bestimated weekly intake with a frequency of three times consumption per week cPTWI set by FAOWHO [33] dreference dose of Mn established by USEPA [34]

BioMed Research International 5

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

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Page 5: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

By comparing the data with the mussel in the previousstudies it is notable that the Cu level in the current study washigher than that of those studies It is believed that usingcopper-based pesticide in paddy fields in Perak River anddischarge of municipal sewage increase the Cu concentra-tion in the soil [48 49] +e contaminant leached into theriver and the sediment eventually accumulated in C flu-minea soft tissue [50] +is is supported by Patrick et al [6]who reported C fluminea soft tissue had significantly greaterCu concentrations compared to river and sediment

Copper is an essential trace element for living organismswhich allows the critical enzyme to function properly andassists enzyme in transferring energy into the cells inhumans [51] +e shellfish is an excellent source of Cu forhuman needs [46] However higher copper uptake thanneeded is a double-edged sword that causes adverse effects[52] +e effects include headache vomiting liver andkidney damage and Wilsonrsquos disease [53]

34 Manganese +e Mn level in C fluminea ranged from363 to 2616mgkg ww and has a mean of 1025plusmn 192mgkg ww No significant difference was found betweenMn levelin eachmonth with Pgt 005+ere is no permissible limit formanganese In EWI measurement the C fluminea con-sumers would intake 3681 μgkgweek or around 231mg6265 kg personweek (3681times 62651000) of the manga-nese +e EWI PTWI ratio of the Mn was 376 +isshowed that Mn intake is within the safe level +e currentresult is found to be higher than that of the study by Olmedoet al [46] who reported 035mg60 kg personweek(005times 7) of Mn intake through fish and shellfish con-sumption in Andalusia+e current result is also found to beslightly higher than that of the study by Bat et al [47] whoreported that EWI of the Mn in M galloprovincialis was in

the range of 137 to 221mg70 kg personweek (00196times 70to 00315times 70)

High Mn contamination in C fluminea is associated withaccumulation from the sediment and river+is is supported byHulten et al [54] who reported that sediment is the mainsource of Mn specifically on the surface of the sedimentparticles Moreover wastewater discharged from the metalindustry flows into the river lowering its pH and facilitating thesediment dissolution into the river [55] Hence concentratedMn in river and sediment contributes to high Mn level in Cfluminea

Manganese is an essential element for living organismsTiny amounts of Mn are required to form healthy bonesregulate the blood sugar level maintain the metabolismpromote the digestion and boost the vitamin absorption [56]Overconsumption ofmanganese from food sources is rare [57]When Mn uptake exceeded the required amount it hasnegative impacts on the human body including weaknessmuscle pain less facial expression and clumsy movement ofthe limbs and neurological damage [58 59]

35 Lead Pb detected in C fluminea ranged from 017 to034mgkg ww and has a mean of 062plusmn 012mgkg ww +ePb detection in April and June is significantly different thanthat in other months with Plt 005 +e Pb level is within thepermissible limit set by the European Union of 15mgkg ww[20] In EWI measurement the local people consuming Cfluminea would intake 222μgkgweek or around 014mg6265 kg personweek (222times 62651000) of the lead+eEWI PTWI ratio of Pbwas 888+is showed that the intake rate ofPb is within the safe level

+e current finding is compared with that of the previousstudies Zhelyazkov et al [35] reported that the EWI of Pbfor the Mytilus galloprovincialis was 0001mg70 kg person

Table 1 Concentration of heavy metals (mgkg ww) in C fluminea soft tissue from February to July

Month Cd Cu Mn Pb ZnMeanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE Meanplusmn SE

February 024plusmn 002a 368plusmn 022a 762plusmn 309a 045plusmn 021a 906plusmn 219aMarch 021plusmn 001a 326plusmn 018a 1218plusmn 144a 044plusmn 002ab 1503plusmn 063abApril 023plusmn 001a 897plusmn 122b 691plusmn 094a 086plusmn 004b 2982plusmn 189cMay 020plusmn 001a 494plusmn 064a 816plusmn 149a 049plusmn 005ab 1831plusmn 208bJune 024plusmn 002a 423plusmn 043a 1252plusmn 283a 088plusmn 006b 1667plusmn 145bJuly 026plusmn 001a 512plusmn 015a 1411plusmn 170a 057plusmn 035ab 1606plusmn 155abAverage 023plusmn 001 503plusmn 047 1025plusmn 192 062plusmn 012 1749plusmn 163Letters show significant differences among the months at Plt 005 +e data were presented as meanplusmn standard error

Table 2 +e comparison of the estimated daily intake and estimated weekly intake with the recommended values for C flumineaconsumption

C fluminea (mgkg ww) EDI (μgkgday) ADIa (μgkgday) EWIb (μgkgweek) PTWI (μgkgweek) EWI PTWI ratio ()Cd 023 028 1 084 7c 1200Cu 503 602 350 1806 3500c 052Mn 1025 1227 140 3681 980d 376Pb 062 074 357 222 25c 888Zn 1747 2091 1000 6273 7000c 090aAccepted daily intake which was calculated from PTWI bestimated weekly intake with a frequency of three times consumption per week cPTWI set by FAOWHO [33] dreference dose of Mn established by USEPA [34]

BioMed Research International 5

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

Medicinal ChemistryInternational Journal of

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Page 6: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

week (00028times 70times 71000) Besides Sharif et al [37] re-ported that the EWI of Pb for Metretrix spp Amusiumpleuronectes and Strombus canarium were 004mg6265 kgpersonweek (010times 7times 62651000) 011mg6265 kg per-sonweek (025times 7times 62651000) and 008mg6265 kgpersonweek (019times 7times 62651000) respectively Bat et al[47] reported that the EWI of Pb inM galloprovincialis fromthe Turkish Black Sea coasts was in the range of 003 to015mg70 kg personweek (000042times 70 to 000217times 70)with the highest EWI PTWI ratio of 168 to 868 In thecurrent study the Pb intake in weekly measurement is foundto be higher than that of most of these previous studiesHowever the current result is in line with a similar study byDe la Cruz et al [2] who also studied the human health riskin C fluminea consumption in Philippines +ey reportedthat EWI for average consumers was within 076 to 12 μgkgday or 015 to 023mg65 kg personweek (076times 65times 31000 to 12times 65times 31000) assuming three times consump-tion per week as indicated in their result

High Pb contamination in C fluminea is due to fact thattheir habitat was within the vicinity of oil palm plantationthat used pesticides and herbicides [60] In Nigeria Oso-bamiro and Adewuyi [61] reported that Pb concentration inoil palm plantation soil ranged from 155 to 331mgkgwhich is significantly higher than that of arable soil +e Pb-contaminated soils leached into the river and accumulated inthe soft tissue of C fluminea [62] Besides the smokingprocess of C fluminea using firewood was also reported toincrease Pb contamination in soft tissue of C fluminea [63]

In the top 20 most poisonous heavy metals Pb is thesecond element after As Pb has no biological function inhuman body and it is highly harmful to human health evenin the smallest amount [64 65] +ere are many types of Pbexposures but inhalation and ingestion through contami-nated food is found to be the most common route [66]Excessive Pb uptake causes intellectual damage to childrensuch as cognitive and behavioural problems [67 68] +is isbecause the brain development and central nervous systemof children are susceptible to damage [69] Long-term ex-posure to Pb-contaminated food caused the metal to bedeposited into bone leading to kidney and liver diseasecardiovascular disease cancer and reproductive systemdefect [64 70]

36 Zinc +e Zn concentrations in C fluminea were foundin the range of 247 to 3376mgkg ww with a mean of1749plusmn 163mgkg ww +e Zn level in April is significantlyhigher than those in other months with Plt 005 +e Znlevel is within the permissible limit in FAO compilation ofthe legal limits of 40ndash150mgkg ww [20] +is indicated thatthe Zn is in the safe level to consume In EWI measurementthe C fluminea consumers would intake 6273 μgkgweekor around 393mg6265 kg personweek (6273times 62651000) of the zinc+e EWI PTWI ratio of the Zn was 090+e Zn intake is within the safe level +is result is inagreement with that of Olmedo et alrsquos [46] study whichfound 325mg60 kg personweek (0464times 7) of Zn intakethrough fish and shellfish consumption in Andalusia

(Southern Spain) +e current result is lower than that in[47] which reported that the EWI of the Pb in M gallo-provincialis ranged from 392 to 1323mg70 kg personweek(0056times 70 to 0189times 70) with the EWI PTWI ratio of 086to 270

+e Zn in C fluminea is believed to be due to phosphaterock fertilizer that is used for oil palm growth Zn in thetopsoil leached into the river [71] Besides Zn as a famousanticorrosive agent is widely used as antifouling paint forcommercial boats [72 73] +e leaching of boat paintcoupling with accidental spill of oils or fuel increases the Zncontamination that accumulates in C fluminea [74]

Zn is considered as an essential trace element for livingorganisms which is relatively less toxic compared to othermetals It assists in metabolism enzyme catalytic activityand immune system functioning and possesses antioxidantproperties [75] Oyster is reported as a source of Zn followedby meat and mussel [76] Excess Zn uptake damages thebrain respiratory tract gastrointestinal tract and prostategland [77] Besides high Zn intake disrupts homeostasis forother essential elements and suppresses the Cu and Feabsorption [78]

Figure 2 shows the THQ values of the heavy metals andtheir hazard index (HI) for the consumption of theC fluminea+e target hazard quotient (THQ) values of Cd Cu Zn Pband Mn were 012 006 004 041 and 003 respectively +eresults of the THQ showed the following order of levelPbgtCdgtCrgtCugtZngtMn As presented in THQ thereexists no hazard+e HI index is found to be 061 which is lessthan 1 +is suggests a relative absence of human health riskassociated with intake of heavy metal via consumption of softtissue alone However health risks to the consumers depend onthe amounts of estimated weekly intake of heavy metal In thisstudy we do not take into account the heavy-metal intake viaother sources that probably contributes to higher THQ andHIHence the present results need more attention in view of thefact that metals enter into the human body through othersources primarily through other foodstuff

+e results in current study can be used as a guideline toconsume C fluminea safely Nevertheless as reported in theliterature the heavy metals in surrounding sediment andriver water from anthropogenic activities correlate withheavy metal levels in C fluminea [79 80] Although the levelof heavy metal in C fluminea is within the permissible limit

001020304050607

Cd Cu Mn Pb Zn HI

Valu

e

THQ and HI

Figure 2 +e THQ and HI values in this study +e THQ for eachheavy metals and their hazard index (HI) were calculated fromconsumption of C fluminea soft tissue collected from Pasir Masand Tumpat Kelantan

6 BioMed Research International

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

Medicinal ChemistryInternational Journal of

Hindawiwwwhindawicom Volume 2018

ToxicologyJournal of

Hindawiwwwhindawicom Volume 2018

PainResearch and TreatmentHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Arthritis

Neurology Research International

Hindawiwwwhindawicom Volume 2018

StrokeResearch and TreatmentHindawiwwwhindawicom Volume 2018

Drug DeliveryJournal of

Hindawiwwwhindawicom Volume 2018

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Advances in Pharmacological Sciences

Tropical MedicineJournal of

Hindawiwwwhindawicom Volume 2018

AddictionJournal of

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Anesthesiology Research and Practice

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Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

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Submit your manuscripts atwwwhindawicom

Page 7: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

potential dangers emerging in the future depends uponindustrial wastewaters and domestic activities Given thevital level of C fluminea to the local people the routinebiomonitoring of the clam for consumption should be doneto ensure continuous food safety +e authority must ensurethat domestic sewage and industrial effluents are treatedbefore discharge into the rivers [81]

4 Conclusion

+e mean concentrations of metals found in C flumineawere 023 plusmn 001 503 plusmn 047 1025 plusmn 192 062 plusmn 012 and1749 plusmn 163 mgkg ww for Cd Cu Mn Pb and Zn re-spectively All EWI values were found to be less than theJECFA provisional tolerable weekly intake (PTWI) valuefor studied heavy metals +us there is no potentialhealth risk for people who consume C fluminea inKelantan +e present study showed that the consump-tion of C fluminea from Pasir Mas and Tumpat Kelantanat the rate of 75 gdayperson with the frequency of threetimes per week most probably does not pose a healthhazard of cancer to the local population

Data Availability

+e data of the heavy metals used to support the findings ofthis study are included within the article

Additional Points

Human health risk as a result of heavy metals intake due toC fluminea consumption was evaluated All metal con-centrations inC flumineawere within the permissible limitsSmoked C fluminea in Kelantan is safe for human healthwith the current consumption rate

Conflicts of Interest

+e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

We are grateful to the Universiti Malaysia KelantanMalaysia for its support for both facility and instruments+is study was supported by the Transdisciplinary ResearchGrant Scheme under Malaysia Ministry of Higher Education(funding code RTRGSA080000244A0052016000389)

Supplementary Materials

Graphical overview starting from C fluminea selling to theconsumption safety (Supplementary Materials)

References

[1] E R Aweng and A A Kutty Etak Lokan Air Tawar DewanBahasa Dan Pustaka Johor Bahru Malaysia 2018

[2] C P P De la Cruz N M De Vera L Lapie M N Catalmaand R V Bunal ldquoBioaccumulation and health risks assess-ment of lead (Pb) in freshwater Asian clams (Corbicula

fluminea Muller) from Laguna de Bay Philippinesrdquo PollutionResearch vol 36 no 2 pp 366ndash372 2017

[3] C C Hakenkamp S G Ribblett M A Palmer C M SwanJ W Reid andM R Goodison ldquo+e impact of an introducedbivalve (Corbicula fluminea) on the benthos of a sandystreamrdquo Freshwater Biology vol 46 no 4 pp 491ndash501 2001

[4] J Arapov D Ezgeta-Balic M Peharda and Z N GladanldquoBivalve feedingmdashhow and what they eatrdquo Ribarstvo vol 68no 3 pp 105ndash116 2010

[5] M Kong X Hang L Wang H Yin and Y Zhang ldquoAccu-mulation and risk assessment of heavy metals in sedimentsand zoobenthos (Bellamya aeruginosa and Corbicula flumi-nea) from Lake TaihurdquoWater Science and Technology vol 73no 1 pp 203ndash214 2016

[6] C Patrick M Waters and S Golladay ldquo+e distribution andecological role of Corbicula fluminea (Muller 1774) in a largeand shallow reservoirrdquo BioInvasions Records vol 6 no 1pp 39ndash48 2017

[7] L Zhang Q Shen H Hu S Shao and C Fan ldquoImpacts ofcorbicula fluminea on oxygen uptake and nutrient fluxesacross the sedimentndashwater interfacerdquo Water Air amp SoilPollution vol 220 no 1ndash4 pp 399ndash411 2011

[8] L Su H Cai P Kolandhasamy C Wu C M Rochman andH Shi ldquoUsing the Asian clam as an indicator of microplasticpollution in freshwater ecosystemsrdquo Environmental Pollutionvol 234 pp 347ndash355 2018

[9] B Waykar and G Deshmukh ldquoEvaluation of bivalves asbioindicators of metal pollution in freshwaterrdquo Bulletin ofEnvironmental Contamination and Toxicology vol 88 no 1pp 48ndash53 2012

[10] N Liao S Chen X Ye et al ldquoAntioxidant and anti-tumoractivity of a polysaccharide from freshwater clam Corbiculaflumineardquo Food amp Function vol 4 no 4 pp 539ndash548 2013

[11] N Liao J Zhong R Zhang et al ldquoProtein-bound poly-saccharide from Corbicula fluminea inhibits cell growth inMCF-7 and MDA-MB-231 human breast cancer cellsrdquo PLoSOne vol 11 no 12 Article ID e0167889 2016

[12] H-T Yao P-F Lee C-K Lii Y-T Liu and S-H ChenldquoFreshwater clam extract reduces liver injury by loweringcholesterol accumulation improving dysregulated choles-terol synthesis and alleviating inflammation in high-fathigh-cholesterol and cholic acid diet-induced steatohepa-titis in micerdquo Food amp Function vol 9 no 9 pp 4876ndash48872018

[13] J Pi G-pWang Z-j Lv et al ldquoAnalysis and evaluation of thenutritional components in the soft part of Corbicula flumineain Datong Lakerdquo Journal of Hydroecology vol 5 p 15 2013

[14] J E Gall R S Boyd and N Rajakaruna ldquoTransfer of heavymetals through terrestrial food webs a reviewrdquo Environ-mental Monitoring and Assessment vol 187 no 4 p 2012015

[15] T Sarkar M M Alam N Parvin et al ldquoAssessment of heavymetals contamination and human health risk in shrimpcollected from different farms and rivers at Khulna-Satkhiraregion Bangladeshrdquo Toxicology Reports vol 3 pp 346ndash3502016

[16] N S El-shenawy N Loutfy M F Soliman MM Tadros andA A A El-Azeez ldquoMetals bioaccumulation in two ediblebivalves and health risk assessmentrdquo Environmental Moni-toring and Assessment vol 188 no 3 p 139 2016

[17] C K Yap F B Edward +omas W H Cheng et al ldquoDis-tribution of heavy metals in edible bivalve Donax faba col-lected from Pasir Panjang a health risk assessmentrdquo FrontiersDrug Chemistry Clinical Research vol 2 pp 1ndash5 2019

BioMed Research International 7

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

Medicinal ChemistryInternational Journal of

Hindawiwwwhindawicom Volume 2018

ToxicologyJournal of

Hindawiwwwhindawicom Volume 2018

PainResearch and TreatmentHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Arthritis

Neurology Research International

Hindawiwwwhindawicom Volume 2018

StrokeResearch and TreatmentHindawiwwwhindawicom Volume 2018

Drug DeliveryJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in Pharmacological Sciences

Tropical MedicineJournal of

Hindawiwwwhindawicom Volume 2018

AddictionJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Emergency Medicine InternationalHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Anesthesiology Research and Practice

Journal of

Hindawiwwwhindawicom Volume 2018

Pharmaceutics

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Infectious Diseases and Medical Microbiology

Hindawiwwwhindawicom Volume 2018

Canadian Journal of

Hindawiwwwhindawicom Volume 2018

Autoimmune DiseasesScientica

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

Submit your manuscripts atwwwhindawicom

Page 8: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

[18] M Zeiner I Rezic and I Steffan ldquoAnalytical methods for thedetermination of heavy metals in the textile industryrdquo KemijaU Industriji vol 56 no 11 pp 587ndash595 2007

[19] Perkin Elmer Corporation Analytical Methods for AtomicAbsorption Spectroscopy +e Perkin-Elmer CorporationWaltham MA USA 1996

[20] European Union ldquoNo 18812006 of the European parlia-ment and the council 693 of 19 December 2006 settingmaximum levels for certain contaminants in 694 foodstuffsrdquoOfficial Journal of the European Communities pp 5ndash242006

[21] C E Nauen Compilation of Legal Limits for HazardousSubstances in Fish and Fishery Products Vol 764 FAOFisheries Circular (FAO) Rome Italy 1983

[22] JECFA Evaluation of Certain Food Additives and Contami-nants Sixty-Ninth Report of the Joint FAOWHO ExpertCommittee on Food Additives World Health OrganizationGeneva Switzerland 2009

[23] J Li Z Y Huang Y Hu and H Yang ldquoPotential risk as-sessment of heavy metals by consuming shellfish collectedfrom Xiamen Chinardquo Environmental Science and PollutionResearch vol 20 no 5 pp 2937ndash2947 2013

[24] N U Saher and N Kanwal ldquoAssessment of some heavy metalaccumulation and nutritional quality of shellfish with refer-ence to human health and cancer risk assessment a seafoodsafety approachrdquo Environmental Science and Pollution Re-search vol 26 no 5 pp 5189ndash5201 2019

[25] M Azmi R Junidah A S Mariam et al ldquoBody mass index(BMI) of adults findings of the Malaysian adult nutritionsurvey (MANS)rdquo Malaysian Journal of Nutrition vol 15no 2 2009

[26] USEPA USEPA Regional Screening Level (RSL) SummaryTable November 2011 USEPA Washington DC USA 2011

[27] USEPA Human Health Risk Assessment Regional ScreeningLevel (RSL)mdashSummary Table USEPA Washington DCUSA 2015

[28] USEPA Reference Dose (RfD) Description and Use in HealthRisk Assessments USEPA Washington DC USA 1993

[29] USEPA Integrated Risk Information System (IRIS) on Leadand Compounds (Inorganic) National Center for Environ-mental Assessment Washington DC USA 2004

[30] M Jovic and S Stankovic ldquoHuman exposure to trace metalsand possible public health risks via consumption of musselsMytilus galloprovincialis from the Adriatic coastal areardquo Foodand Chemical Toxicology vol 70 pp 241ndash251 2014

[31] G Liang W Gong B Li J Zuo L Pan and X Liu ldquoAnalysisof heavy metals in foodstuffs and an assessment of the healthrisks to the general public via consumption in Beijing ChinardquoInternational Journal of Environmental Research and PublicHealth vol 16 no 6 p 909 2019

[32] M Javed and N Usmani ldquoAccumulation of heavy metals andhuman health risk assessment via the consumption offreshwater fish Mastacembelus armatus inhabiting thermalpower plant effluent loaded canalrdquo SpringerPlus vol 5 no 1p 776 2016

[33] FAOWHO Summary of Evaluations Performed by the JointFAOWHO Expert Committe on Food Addictive (JEFCA) Firstthrough Sixtyfirst Meetings ILSI Press International LifeSciences Institute Washington DC USA 2004

[34] USEPA Manganese Compound USEPA Washington DCUSA 2008

[35] G Zhelyazkov T Yankovska-Stefanova E Mineva et alldquoRisk assessment of some heavy metals in mussels (Mytilusgalloprovincialis) and veined rapa whelks (Rapana venosa) for

human healthrdquo Marine Pollution Bulletin vol 128 pp 197ndash201 2018

[36] S M Yunus Z Hamzah N A N Ariffin and M B MuslimldquoCadmium chromium copper lead ferrum and zinc levels inthe cockles (Anadara granosa) from Kuala SelangorMalaysiardquo Malaysian Journal of Analytical Sciences vol 18no 3 pp 514ndash521 2014

[37] R Sharif E Chong and C K Meng ldquoHuman health riskassessment of heavy metals in shellfish from Kudat SabahrdquoMalaysian Journal of Nutrition vol 22 no 2 pp 301ndash3052016

[38] P B Tchounwou C G Yedjou A K Patlolla andD J Sutton ldquoHeavy metal toxicity and the environmentrdquoExperientia Supplementum vol 101 pp 133ndash164 2012

[39] International Cadmium Association Level of Cadmium in theEnvironment International Cadmium Association BrusselsBelgium 2018

[40] R Chunhabundit ldquoCadmium exposure and potential healthrisk from foods in contaminated area+ailandrdquo ToxicologicalResearch vol 32 no 1 pp 65ndash72 2016

[41] M Cejchanova K Wranova V Spevackova et al ldquoHumanbio-monitoring study-toxic elements in blood of womenrdquoCentral European Journal of Public Health vol 20 no 2p 139 2012

[42] K Ganguly B Levanen L Palmberg A Akesson andA Linden ldquoCadmium in tobacco smokers a neglected link tolung diseaserdquo European Respiratory Review vol 27 no 147Article ID 170122 2018

[43] H Itoh M Iwasaki N Sawada et al ldquoDietary cadmiumintake and breast cancer risk in Japanese women a case-control studyrdquo International Journal of Hygiene and Envi-ronmental Health vol 217 no 1 pp 70ndash77 2014

[44] R A Wuana and F E Okieimen ldquoHeavy metals in con-taminated soils a review of sources chemistry risks and bestavailable strategies for remediationrdquo ISRN Ecology vol 2011Article ID 402647 20 pages 2011

[45] M R Rahimzadeh M R Rahimzadeh S Kazemi andA-A Moghadamnia ldquoCadmium toxicity and treatment anupdaterdquo Caspian Journal of Internal Medicine vol 8 no 3pp 135ndash145 2017

[46] P Olmedo A F Hernandez A Pla P Femia A Navas-Acien and F Gil ldquoDetermination of essential elements(copper manganese selenium and zinc) in fish and shellfishsamples Risk and nutritional assessment and mercury-sele-nium balancerdquo Food and Chemical Toxicology vol 62pp 299ndash307 2013

[47] L Bat E Arici and A Oztekin ldquoHuman health risk as-sessment of heavy metals in the Black Sea evaluatingmusselsrdquo Current World Environment vol 13 no 1 p 152018

[48] T M Chiroma B I Abdulkarim and H M Kefas ldquo+eimpact of pesticide application on heavy metal (Cd Pb andCu) levels in spinachrdquo Leonardo Electronic Journal of Practicesand Technologies vol 11 pp 117ndash122 2007

[49] F M Fishel Pesticide Toxicity Profile Copper-Based PesticidesUFIFAS Extension Gainesville FL USA 2005

[50] S Giri A K Singh and M K Mahato ldquoMetal contaminationof agricultural soils in the copper mining areas of Singhbhumshear zone in Indiardquo Journal of Earth System Science vol 126no 4 p 49 2017

[51] L Prashanth K Kattapagari R Chitturi V Baddam andL Prasad ldquoA review on role of essential trace elements inhealth and diseaserdquo Journal of Dr NTR University of HealthSciences vol 4 no 2 pp 75ndash85 2015

8 BioMed Research International

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

Medicinal ChemistryInternational Journal of

Hindawiwwwhindawicom Volume 2018

ToxicologyJournal of

Hindawiwwwhindawicom Volume 2018

PainResearch and TreatmentHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Arthritis

Neurology Research International

Hindawiwwwhindawicom Volume 2018

StrokeResearch and TreatmentHindawiwwwhindawicom Volume 2018

Drug DeliveryJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in Pharmacological Sciences

Tropical MedicineJournal of

Hindawiwwwhindawicom Volume 2018

AddictionJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Emergency Medicine InternationalHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Anesthesiology Research and Practice

Journal of

Hindawiwwwhindawicom Volume 2018

Pharmaceutics

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Infectious Diseases and Medical Microbiology

Hindawiwwwhindawicom Volume 2018

Canadian Journal of

Hindawiwwwhindawicom Volume 2018

Autoimmune DiseasesScientica

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

Submit your manuscripts atwwwhindawicom

Page 9: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

[52] E Tvrda R Peer S C Sikka and A Agarwal ldquoIron andcopper in male reproduction a double-edged swordrdquo Journalof Assisted Reproduction and Genetics vol 32 no 1 pp 3ndash162015

[53] M Mahurpawar ldquoEffects of heavy metals on human healthrdquoInternational Journal of ResearchmdashGranthaalayah vol 3pp 1ndash7 2015

[54] V M Hulten J-C Dutay R Middag et al ldquoManganese in theworld ocean a first global modelrdquo Biogeosciences Discussionsvol 14 no 5 pp 1ndash38 2016

[55] V N T Ha S Takizawa K Oguma and N Van PhuocldquoSources and leaching of manganese and iron in the saigonriver basin Vietnamrdquo Water Science and Technology vol 63no 10 pp 2231ndash2237 2011

[56] A Jose ldquoEleven impressive health benefits of manganeserdquo 2018httpswwwnaturalfoodseriescom11-benefits-manganese

[57] D S Avila R L Puntel and M Aschner ldquoManganese inhealth and diseaserdquo in Interrelations between Essential MetalIons and Human Diseases pp 199ndash227 Springer BerlinGermany 2013

[58] World Health Organization Manganese in Drinking-WaterBackground Document for Development of WHO Guidelinesfor Drinking-Water Quality World Health OrganizationGeneva Switzerland 2011

[59] T R Guilarte and K K Gonzales ldquoManganese-Inducedparkinsonism is not idiopathic Parkinsonrsquos disease envi-ronmental and genetic evidencerdquo Toxicological Sciencesvol 146 no 2 pp 204ndash212 2015

[60] M Hossen S Hamdan and M Rahman ldquoReview on the riskassessment of heavy metals in Malaysian clamsrdquoGe ScientificWorld Journal vol 2015 Article ID 905497 7 pages 2015

[61] M T Osobamiro and G O Adewuyi ldquoLevels of heavy metalsin the soil effects of season agronomic practice and soilgeologyrdquo Journal of Agricultural Chemistry and Environmentvol 4 no 4 pp 109ndash117 2015

[62] T-L Pham ldquoAccumulation depuration and risk assessmentof cadmium (Cd) and lead (Pb) in clam Corbicula fluminea(OF Muller 1774) under laboratory conditionsrdquo IranianJournal of Fisheries Sciences vol 17 pp 1ndash11 2018

[63] A O Igwegbe C A Negbenebor E C ChibuzoM H Badauand G I Agbara ldquoEffects of season and fish smoking on heavymetal contents of selected fish species from three locations inBorno State of Nigeriardquo Asian Journal of Science and Tech-nology vol 6 no 2 pp 1010ndash1019 2015

[64] M A Assi M N M Hezmee A W Haron M Y Sabri andM A Rajion ldquo+e detrimental effects of lead on human andanimal healthrdquo Veterinary World vol 9 no 6 pp 660ndash6712016

[65] M Jaishankar T Tseten N Anbalagan B B Mathew andK N Beeregowda ldquoToxicity mechanism and health effects ofsome heavy metalsrdquo Interdisciplinary Toxicology vol 7 no 2pp 60ndash72 2014

[66] A Jan M Azam K Siddiqui A Ali I Choi and Q HaqldquoHeavy metals and human health mechanistic insight intotoxicity and counter defense system of antioxidantsrdquo In-ternational Journal of Molecular Sciences vol 16 no 12pp 29592ndash29630 2015

[67] R L Canfield T A Jusko and K Kordas ldquoEnvironmentallead exposure and childrenrsquos cognitive functionrdquo Ge ItalianJournal of Pediatrics vol 31 no 6 pp 293ndash300 2005

[68] A P Sanders B Claus Henn and R O Wright ldquoPerinataland childhood exposure to cadmium manganese and metalmixtures and effects on cognition and behavior a review of

recent literaturerdquo Current Environmental Health Reportsvol 2 no 3 pp 284ndash294 2015

[69] World Health Organization Lead Poisoning and HealthWorld Health Organization Geneva Switzerland 2018

[70] L H Mason J P Harp and D Y Han ldquoPb neurotoxicityneuropsychological effects of lead toxicityrdquo BioMed ResearchInternational vol 2014 Article ID 840547 8 pages 2014

[71] A Aini C Fauziah and A Samsuri ldquoCadmium and zincconcentrations in soils and oil palm tissues as affected by long-term application of phosphate rock fertilizersrdquo Soil andSediment Contamination An International Journal vol 21no 5 pp 586ndash603 2012

[72] E Ytreberg J Karlsson and B Eklund ldquoComparison oftoxicity and release rates of Cu and Zn from anti-foulingpaints leached in natural and artificial brackish seawaterrdquoScience of the Total Environment vol 408 no 12 pp 2459ndash2466 2010

[73] M A Bighiu A-K Eriksson-Wiklund and B EklundldquoBiofouling of leisure boats as a source of metal pollutionrdquoEnvironmental Science and Pollution Research vol 24 no 1pp 997ndash1006 2017

[74] A D Mustafa H Juahir K Yunus et al ldquoOil spill relatedheavy metal a reviewrdquo Malaysia Journal of Analytical Sci-ences vol 19 no 6 pp 1348ndash1360 2015

[75] P T Bhattacharya S R Misra and M Hussain ldquoNutritionalaspects of essential trace elements in oral health and diseasean extensive reviewrdquo Scientifica vol 12 2016

[76] N Bilandzic M Sedak M ETHokic et al ldquoDetermination ofzinc concentrations in foods of animal origin fish andshellfish from Croatia and assessment of their contribution todietary intakerdquo Journal of Food Composition and Analysisvol 35 no 2 pp 61ndash66 2014

[77] L M Plum L Rink and H Haase ldquo+e essential toxinimpact of zinc on human healthrdquo International Journal ofEnvironmental Research and Public Health vol 7 no 4pp 1342ndash1365 2010

[78] J Osredkar and N Sustar ldquoCopper and zinc biological roleand significance of copperzinc imbalancerdquo Journal of ClinicalToxicology vol s3 pp 2161ndash0495 2011

[79] E R Aweng and M Mohamed ldquoWater quality and shellfishrelated gastrointestinal disease cases in Kota Bharu KelantanMalaysiardquo Journal of Bioentrepreneurship vol 1 pp 9ndash132011

[80] J M Salman A R Hughes and A M Almamoori ldquoSeasonalvariations of heavy metals in water and two species of mol-luscs in Al Hilla River Iraqrdquo International Journal of GeologyEarth amp Environmental Sciences vol 4 no 2 pp 16ndash24 2014

[81] M Hussain T Saputra E Szabo and B Nelan ldquoAn overviewof seafood supply food safety and regulation in New SouthWales Australiardquo Foods vol 6 no 7 p 52 2017

BioMed Research International 9

Medicinal ChemistryInternational Journal of

Hindawiwwwhindawicom Volume 2018

ToxicologyJournal of

Hindawiwwwhindawicom Volume 2018

PainResearch and TreatmentHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Arthritis

Neurology Research International

Hindawiwwwhindawicom Volume 2018

StrokeResearch and TreatmentHindawiwwwhindawicom Volume 2018

Drug DeliveryJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in Pharmacological Sciences

Tropical MedicineJournal of

Hindawiwwwhindawicom Volume 2018

AddictionJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Emergency Medicine InternationalHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Anesthesiology Research and Practice

Journal of

Hindawiwwwhindawicom Volume 2018

Pharmaceutics

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Infectious Diseases and Medical Microbiology

Hindawiwwwhindawicom Volume 2018

Canadian Journal of

Hindawiwwwhindawicom Volume 2018

Autoimmune DiseasesScientica

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

Submit your manuscripts atwwwhindawicom

Page 10: HealthRiskAssessmentofHeavyMetalsfromSmoked ...downloads.hindawi.com/journals/bmri/2019/9596810.pdfKelantan 5 0′0″N N S W E Figure 1: •e map of the Kelantan state, Malaysia

Medicinal ChemistryInternational Journal of

Hindawiwwwhindawicom Volume 2018

ToxicologyJournal of

Hindawiwwwhindawicom Volume 2018

PainResearch and TreatmentHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Arthritis

Neurology Research International

Hindawiwwwhindawicom Volume 2018

StrokeResearch and TreatmentHindawiwwwhindawicom Volume 2018

Drug DeliveryJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Advances in Pharmacological Sciences

Tropical MedicineJournal of

Hindawiwwwhindawicom Volume 2018

AddictionJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Emergency Medicine InternationalHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Anesthesiology Research and Practice

Journal of

Hindawiwwwhindawicom Volume 2018

Pharmaceutics

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Infectious Diseases and Medical Microbiology

Hindawiwwwhindawicom Volume 2018

Canadian Journal of

Hindawiwwwhindawicom Volume 2018

Autoimmune DiseasesScientica

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

Submit your manuscripts atwwwhindawicom