Polychlorinated biphenyls (PCBs) concentration in demersal fish and ...

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Selangor, Malaysia, 3 Institute for Environmental and Development (LESTARI), Universiti Kebangsaan Malaysia, ... PCBs were present in sufficient concentrations to lead to cancer ... argentimaculatus (Malabar red snapper), Sepia officinalis.
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Journal of Food, Agriculture & Environment Vol.11 (1): 1094-1098. 2013

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Polychlorinated biphenyls (PCBs) concentration in demersal fish and shellfish from West Coast of Peninsular Malaysia Alina Mohamad 1, Azrina Azlan 1, 2 *, Muhammad Rizal Razman 3, Nor Azam Ramli 4 and Aishah A. Latiff 5 Department of Nutrition and Dietetics, Faculty of Medicine and Health Sciences, 43400 UPM Serdang, Selangor, Malaysia. 2 Laboratory of Halal Science Research, Halal Products Research Institute, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia, 3 Institute for Environmental and Development (LESTARI), Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia. 4 Sustainable and Environmental Section, School Of Civil Engineering, Engineering Campus, Universiti Sains Malaysia, 14300 Nibong Tebal, Penang, Malaysia. 5 Doping Control Centre, Universiti Sains Malaysia, 11800 Penang, Malaysia. *e-mail: [email protected] 1

Received 18 September 2012, accepted 19 January 2013.

Abstract Fish is a good source of high-quality protein, vitamins and other essential nutrients, especially essential fatty acids (EFAs), known as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). Nutritionists have suggested an intake of 35g or more of fish daily and two fatty fish-meals per week as to reduce the relative risk of death from coronary heart diseases. However, fish consumption also has been identified as one of the primary route of exposure to polychlorinated biphenyls (PCBs). This study has identified the type and level of 12 congeners of PCBs that are the most toxic to humans. The maximum permitted level of PCBs is 4 pg/g for muscles meat of fish and fishery products by World Health Organization (WHO) using 2005 WHO-TEFs. The highest amount of PCBs concentration was in Anadara granosa (cockles) with level of 2.61pg/g wet weight. Other species such as Psettodes erumei (large-scale tongue sole), Plotosus spp. (gray eel-catfish), Sepia officinalis (cuttle fish), and Macrobrachium rosenbergi (prawn) contained relatively low concentration of PCBs in their tissue collected from West Coast of Peninsular Malaysia. Therefore, it can be concluded that these demersal fish and shellfish are safe to consume. Key words: Fish, shellfish, polychlorinated biphenyls.

Introduction Fish can be classified depending on the environment they live whether from freshwater or marine, pelagic or demersal. Demersal fish live in the bottom of the sea and examples of local species from this habitat are such as long-tailed butterfly ray, Japanese threadfin bream, and large-scale tongue sole 1. The fat contents of fish also are depending on its habitats. Besides that, fish also are commonly classified as white fish and oily fish depending on where they store their body fat. The white fish store their fat in liver while oily fish store their fat in liver and throughout their bodies 2. Fish is a good source of high-quality protein (17% of total animal protein and 6% of all protein consumed by humans), vitamins and other essential nutrients 3, 4. Nutritionists have suggested intake of 35 g or more fish daily 5 and two fatty fishmeals per week 6 as to reduce the relative risk of death from coronary heart diseases. Besides protein, fish is also high in essential fatty acids (EFA), known as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) that are important to the diet. Although, fish is high in protein and other beneficial components, it also may contain mercury and organochlorine compounds such as polychlorinated biphenyls (PCBs) that give negative effects for health. The PCBs are synthetic organic chemicals comprising 209 individual chlorinated biphenyl compounds known as congeners. Among these congeners, only 13 were considered toxic to human health. These most toxic congeners were separated by the different types which are non-ortho, mono-ortho, and di-ortho 7. The 1094

highest toxic equivalent factors for PCB congeners are 126 and 169 8. The PCBs would bio-accumulate in the fatty tissues of exposed animals and human and this exposure is believed to be responsible for the wide variety of negative health effects 9. The PCBs when present in sufficient concentrations exceeding the level often considered acceptable for environmental exposure may lead to chronic disease like cancer 4. Gagnon et al. 10 in their assessment on chemical risk associated with consumption of seafood products in Canada, found that inorganic arsenic and PCBs were present in sufficient concentrations to lead to cancer risks exceeding the level often considered acceptable for environmental exposure. The maximum level of PCBs is 4 pg/g for muscles meat of fish and fishery products and products thereof with the exception of eel, according to World Health Organization (WHO) toxic equivalents using the WHO-TEFs 11. There were varied levels of polychlorinated compounds (PCBs together with dioxins and furans) in various fish and shellfish species have been widely published from different countries including Tunisia 12, Spain 8, Ireland 13 and the U. S. 14. However, in Asia reported data on these contaminants are still lacking and sparse. Therefore, this study was carried out to obtain data on type and level of PCBs in fish and shellfish from this region especially Malaysia. The west coastal region of Peninsular Malaysia also known as Straits of Malacca is one of the busiest business routes in the world. Therefore, the level of PCBs in aquatic Journal of Food, Agriculture & Environment, Vol.11 (1), January 2013

organisms including fish of this vicinity could be potentially high due to the various industrial and shipping activities along the coastal region. This study is important as to identify and quantify the type and amount of polychlorinated biphenyls (PCBs) in commonly consumed marine fish and shellfish caught along the strait.

Psettodes erumei (large-scale tongue sole), Lutianus argentimaculatus (Malabar red snapper), Sepia officinalis (cuttle fish), Anadara granosa (cockles), and Macrobrachium rosenbergi (prawn). The selection of the fish samples was based on Osman et al. 15, most of the species are those preferred by local consumers.

Materials and Methods Chemical and instrumentation: The reagents used were hexane, dichloromethane, toluene from Fisher Scientific, Leicestershire, UK with pesticide residue grade and the equipment used was accelerated solvent extraction (ASE200, Dionex Corp., Sunnyvale, CA, USA), fluid management system (FMS, Inc, Waltham, MA, USA), high-resolution gas chromatography/high-resolution mass spectrometry (MAT 95 XL, Agilent 6890 Series, USA) and rotary evaporator (BUCHI Labortechnik, Flawil, Switzerland).

Sample preparation: Upon arrival in the laboratory, the collected samples were measured for their length and weight individually. Fish samples were gutted, viscera removed, beheaded, washed and filleted before frozen. Shellfish samples were also prepared by removing inedible parts, washed and frozen. All samples were kept at -75oC without any prior treatment. Before analysis, composite sample of each species in different regions was prepared by mixing and grinding homogenously the prepared samples using food processor (National, Petaling Jaya, Malaysia). All composite samples were packed into polyethylene (PE) covered cup, stored in freezer at -20oC and analyzed within a week.

Sample collection: Stratified sampling method was used to collect fish and shellfish samples. Fresh fish and shellfish were collected from 10 identified fish landing areas along the Straits of Malacca that was divided into 3 regions (Fig. 1); North (Kuala Perlis, Kuala Kedah, Teluk Bahang and Batu Maung), South (Port Dickson, Malacca and Muar) and Middle (Kuala Selangor, Manjung Utara and Matang). Collection of samples at each region was carried out twice from August to November 2008. All samples were immediately dipped in a mixture of water and ice to block any digestive and unfavorable changes. From collection site to laboratory, samples were transferred in polystyrene boxes containing ice and transported at refrigerated temperature (4oC). Fish samples: There were 6 species of fish and 3 species of shellfish collected: Gymnura spp. (long-tailed butterfly ray), Plotosus spp. (gray eel-catfish), Nemipterus janonicus (Japanese threadfin bream), Epinephulus sexfasciatus (sixbar grouper), Perlis Langkawi Island

PeninsularMalaysia Kedah

NorthRegion

Penang

Perak

MiddleRegion Selangor

Straitsof Malacca

Kuala Lumpur

Negeri Sembilan Malacca

SouthRegion Johor Bahru

Figure 1. Location of sampling sites at Straits of Malacca. Journal of Food, Agriculture & Environment, Vol.11 (1), January 2013

Fat extraction and sample clean-up: Ten gram of homogenized wet muscle tissue was injected with 20µl of 4937 PCBs internal standard (Cambridge Isotope Laboratories, Inc., Andover, MA, USA) and extracted by accelerated solvent extraction (ASE) 200 (Dionex Corp., Sunnyvale, CA, USA). About 7 g of hydromatrix was added and mixed together with the sample. After that, the sample mixture was put in microwave oven (Khind, Petaling Jaya, Malaysia) for drying for about 2 min. The dried sample was put into ASE extraction cell (size 33) and extraction process was carried out for 20 min. After ASE extraction, solvents used were removed by means of a rotary evaporator (Büchi Labortechnik, Flawil, Switzerland) that was set at 500 Mbar, 40-50oC for 20-30 min. The fat fraction extracted was determined gravimetrically. After fat extraction, eluents (fat and hexane) were cleaned up using acid/base modified silica gel, alumina, and graphitized carbon column chromatography for about 1 hour. Later, hexane was removed from the PCBs eluent using rotary evaporator (Büchi Labortechnik, Flawil, Switzerland). Then, 20µl of 4798 PCBs external standard (Cambridge Isotope Laboratories, Inc., Andover, MA, USA) was added into the sample in a small vial and mixed well. The process was continued with drying the mixture of sample on heating block at 70oC with nitrogen gas until the amount of sample was about 10 µl. After that, sample was analyzed using high-resolution gas chromatography/high resolution mass spectrometry (HRGC/HRMS). The samples were analyzed for 12 dioxin like co-planar PCBs; PCBs 77, 81, 105, 114, 118, 123, 126, 156, 157, 167, 169 and 189. The sample preparation procedures, analytical techniques, and quality control strategies described are as defined in US EPAs Method 1613 16, 17. Calculation of toxicity equivalents (TEQ Values) for PCBs compounds: Toxicity equivalent (TEQ values) was calculated using the procedure developed by World Health Organization11. The toxicity of PCB congeners are expressed using toxic equivalence factors (TEFs) representing the relative toxicity of the compound being measured to the most toxic PCB (PCB 126) with TEF value of 0.1. The TEQ of PCBs was calculated by multiplying the analytical determined concentration of each congener by its corresponding TEF. 1095

Results and Discussion Table 1 shows the level of fat and PCBs in demersal fish and shellfish samples. The fat content and total PCBs were expressed as g/100 g and total WHO-iTEQ in pg/g wet weight of samples, respectively. There were 12 congeners of PCBs determined in the muscle tissue of 28 samples (9 species) from different regions. WHO toxic equivalent factors 11 were used to calculate the TEQ of each sample. The fat content varied from one species to another. In this study, gray eel-catfish contained the highest fat at 5.70 g/100 g compared to other species. The second highest fat content obtained was in Malabar red snapper at 5.45 g/100 g of wet weight sample. While, the lowest fat content was observed in large-scale tongue sole with total fat of 0.80 g/100 g. The fat contents for Japanese threadfin bream and long-tailed butterfly ray were 2.30 g/100 g and 1.05-1.20 g/100 g, respectively. For shellfish species, cuttlefish contained the highest fat content, 2.15- 3.05 g/100 g. Other species of shellfish showed lower fat content at 1.15- 1.35 g/100 g and 2.95 g/100 g for prawn and cockles, respectively. For smaller shellfish such as shrimp, it was reported that the fat content (%) of 0.70 ± 0.40, which is much lower than amount observed in prawn of the present study 18 . Study by Osman et al. 15 has reported the fat content of Gymnura spp. of 1.95 g/100 g which was higher than the value obtained from this study. Other species of Plotosus spp. such as striped sea catfish, however, contained lower fat at 2.79 g/100 g than the value obtained in this study. Data from Tee et al. 19 stated that fat content of Malabar red snapper of 2.3 g/100 g was lower than fat content in the sample of the present study. Generally, the values obtained from this study were higher in all fish and shellfish species compared to Tee et al. 19. The variation in the fat content of the 9 species ranged 6.7-53% between trip 1 and trip 2. Fat content of fish is influenced by species, season, geographical region, age and maturity 15. Determination of fat content gives the important factors even though lipid likely had little effect on the magnitude of bioaccumulation of PCBs. However, tissue lipid may be the factor in determining the toxic response 20. In the North region, large-scale tongue sole contained the highest amount of PCBs at 1.05 pg/g wet weight while sixbar grouper contained the lowest amount of PCBs at 0.38 pg/g wet weight. For the South region, higher level of PCBs was in Plotosus spp. (gray eel-catfish) at 1.07 pg/g wet weight and

lower amount was detected in prawn and cuttlefish at 0.35 pg/g wet weight, respectively. For Middle region, higher level of PCBs was obtained in Sepia officinalis (cuttlefish), in the amount of 1.81 pg/g wet weights, followed by cockles at 1.48 pg/g wet weights. The lowest amount of PCBs was in long-tailed butterfly ray at 0.35 pg/g wet weight. In the present study, the level of PCB contamination varies greatly between trip 1 and trip 2 as variation ranged from 0 to 108% between different species across all regions. Intra species, it can be clearly seen that Psettodes erumei (large-scale tongue sole), Plotosus spp. (gray eel-catfish), and Anadara granosa (cockles) were the most sensitive species as variation existed up to more than 90%. This finding also suggests that different time of sample collection results in difference levels of PCBs depending on the surrounding human activities and industrial waste releases. Based on Table 1, the highest amount of PCB concentration was in cockles with level of PCBs at 2.61pg/g wet weight in the first trip of collection. This could be due to the fact that the habitat of Anadara granosa (cockles) that are living at the bottom of the sea, nearly to the sediment. According to Boscolo et al. 21, the bivalve mollusc species had a high capacity and propensity to concentrate pollutants. Furthermore, environmental conditions and seasonal fluctuations of lipids may influence the PCBs accumulation. Besides that, Sepia officinalis (cuttlefish) also showed higher levels of PCBs in trip 1 which was at 2.08 and 0.91pg/g from Middle and North region, respectively. Bocio et al.8 showed that the sole species of fish contain low level of PCBs at 0.24 pg/g of wet weight, which was much lower than the value obtained (1.05 pg/g) in the present study. Similarly, for the cuttlefish, the level was 0.02 pg/g of wet weight, which was also much lower than observed in the present study. For catfish, the level of total PCBs (1.07pg/g wet weight) obtained from this study was much lower than the reported value for catfish in Mississippi, USA (15.19 ng/ g wet weight) 22. Generally, in sample collection of trip 1, the Middle region showed higher level of PCBs contamination compared to the North and the South regions. This may be due to the geographical area of the region that can be categorized as highly industrial with Selangor and Perak states having many factories and busiest port ship landing (Port Klang, Selangor) 23, 24. Table 2 shows the distribution of PCB families (non-ortho and mono-ortho PCBs) of the PCBs. Generally, the non-ortho PCBs dominated more than 85% of the total PCBs leaving to less than

Table 1. Fat content (g/100 g) and total PCB (WHO-iTEQ pg/p wet weight) in demersal fish and shellfish from different regions of West Coast of Peninsular Malaysia. Regions

North

South

Middle

Species (common name) Psettodes erumei (Large-scale tongue sole) Nemipterus janonicus (Japanese threadfin bream) Gymnura spp. (Long-tailed butterfly ray) Epinephulus sexfasciatus (Sixbar Grouper) Sepia officinalis (cuttle fish) Plotosus spp. (Gray eel-catfish) Sepia officinalis (cuttle fish) Macrobrachium rosenbergi (prawn) Gymnura spp. (Long-tailed butterfly ray) Epinephulus sexfasciatus (Sixbar Grouper) Lutianus argentimaculatus (Malabar red snapper) Sepia officinalis (cuttle fish) Macrobrachium rosenbergi (prawn) Anadara granosa (cockles)

Fat (g/100g) T1 T2 0.5 1.1 3.0 1.6 1.0 1.4 1.7 0.8 1.5 3.1 5.4 6.0 2.6 1.7 0.9 1.4 1.0 1.1 6.1 3.1 3.8 7.1 3.3 2.8 1.1 1.6 3.2 2.7

Mean 0.80 2.30 1.20 1.25 2.30 5.70 2.15 1.15 1.05 4.60 5.45 3.05 1.35 2.95

Variation (%) 53.03 43.04 23.57 50.91 49.19 7.44 29.60 30.74 6.73 46.12 42.82 11.59 26.19 11.98

WHO-iTEQ (pg/g) T1 T2 0.35 1.74 0.35 0.65 0.54 0.67 0.41 0.35 0.91 0.57 0.38 1.76 0.35 0.35 0.35 0.35 0.35 0.35 0.88 0.36 0.67 0.43 2.08 1.54 0.35 0.65 2.61 0.35

Mean 1.05 0.50 0.61 0.38 0.74 1.07 0.35 0.35 0.35 0.62 0.55 1.81 0.50 1.48

Variation (%) 94.06 42.43 15.19 11.16 32.49 91.20 0.00 0.00 0.00 59.31 30.86 21.10 42.43 107.98

% variation was calculated based on the following formula: (SD/Mean) × 100 TI is Trip 1 (12 August 2008 until 9 September 2008) T2 is Trip 2 (15 October 2008 until 12 November 2008)

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Conclusions In the study, the type and level of 12 congeners of PCBs were identified. The most toxic congener, PCB 126 was detected in relatively low concentration in muscle tissue. Generally, in all the studied species, PCBs concentration varied. However, the levels of these contaminants were well below the permitted level as shown in Fig. 3. Among the studied species, cockles contained the highest PCBs level (2.61 pg/g) but still below the permitted level of 4 pg/g for muscles meat of fish and fishery products 11. Other species

Species of demersal and shellfish

pg/g (wet weight)

pg/g (wet weight)

pg/g (wet weight)

pg/g (wet weight)

pg/g (wet weight)

pg/g (wet weight)

Cuttlefish Gray eel-catfish 10% in most samples to the mono-ortho families. The 2.00 0.35 profile of polychlorinated congeners in fish samples 0.30 1.50 0.25 caught from the Straits of Malacca was dissimilar with 0.20 1.00 12 fishes caught in Mediterranean waters of Tunisia 0.15 0.10 0.50 and farmed rainbow trouts in Southern Finland 25. 0.05 0.00 0.00 For the cuttlefish, it was found to contain an amount ) ) 7 1 5) 4) 8) 3) 6) 6) 7) 7) 9) 9) 7) 1) 5) 4) 8) 3) 6) 6) 7) 7) 9) 9) B7 CB8 B10 B11 B11 B12 B12 B15 B15 B16 B16 B18 B7 CB8 B10 B11 B11 B12 B12 B15 B15 B16 B16 B18 of PCBs concentration at 1.79±0.59 and 0.51±0.38 pg/ C C (P (P (PC (PC (PC (PC (PC (PC (PC (PC (PC (PC (P (P (PC (PC (PC (PC (PC (PC (PC (PC (PC (PC g for non-ortho and mono-ortho PCBs, respectively Type of congeners Type of congeners 26 . The amount of non-ortho PCBs was lower than the level obtained from the present study (1.94 pg/ Cockles Sixbar grouper 3.00 g) but higher in mono-ortho PCBs than the present 0.80 0.70 2.50 study (0.14 pg/g). Differences of PCBs profile 0.60 between areas clearly indicate the influence of 2.00 0.50 surrounding human activities as PCBs are synthetic 1.50 0.40 chemical compounds commonly used in industrial 0.30 1.00 activities, composite of some electrical equipments 0.20 0.50 and ship paint as well as product of plastics and 0.10 0.00 0.00 paper mill industries 27. ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) 77 B81 105 114 118 123 126 156 157 167 169 189 77 81 105 114 118 123 126 156 157 167 169 189 B Besides determining total PCBs and its related C C B B B B B B B B B B CB CB B B B B B B B B B B (P (P (PC (PC (PC (PC (PC (PC (PC (PC (PC (PC (P (P (PC (PC (PC (PC (PC (PC (PC (PC (PC (PC families, this study also determined the amount of Type of congeners Type of congeners each congener of PCBs. All of the studied species had their own congeners profile (Fig. 2). According Prawn 0.70 Malabar red snapper to Bocio et al. 8, the predominant PCB congeners 0.70 0.60 0.60 are PCB 118 and 126. PCBs 126 is the most toxic 0.50 0.50 (WHO-TEF = 0.1) to human, and is accounted for the 0.40 0.40 largest contribution of PCBs to the TEQs for each 0.30 0.30 0.20 species 26. In the present study, all the studied 0.20 0.10 0.10 species contained 2-6 congeners in each sample with 0.00 0.00 PCB 126 being present in the all samples. For fish ) ) ) ) ) ) ) ) ) ) ) ) 77 81 105 114 118 123 126 156 157 167 169 189 7) 81) 05) 14) 18) 23) 26) 56) 57) 67) 69) 89) 7 1 1 1 1 1 1 1 1 1 1 B CB B B B B B B B B B B with more than 2% fat, the PCB 126 was found to be CB PCB CB CB CB CB CB CB CB CB CB CB P C ( ( (P (P (P (P (P (P (P (P (P (P (P (P (PC (PC (PC (PC (PC (PC (PC (PC (PC (PC highest in gray eel-catfish sample at the amount of Type of congeners Type of congeners 1.26 pg/g while the lowest was in Malabar red snapper Figure 2. Type of congeners in demersal fish and shellfish species. at 0.56 pg/g. For shellfish samples, PCB 126 was highest in cockles at 2.46 pg/g, followed by 1.90 pg/ permitted level g in cuttlefish and only 0.58 pg/g in prawn. Although PCBs 118 Cockles was considered toxic to humans but the amount of this congeners Prawn was negligible in samples. Generally, other PCB congeners such Cuttlefish Malabar red snapper as PCBs 77, 81, 105, 123, 156 157 and 189 were not detected in the Sixbar grouper samples. PCBs 169 was detected in all samples at very low Long-tailed butterfly ray trip 2 concentration (0.03-0.11 pg/g) while PCB 114 was present in gray Prawn trip 1 eel-catfish, prawn, sixbar grouper and cuttlefish samples. Cuttlefish Gray eel-catfish Cuttlefish Sixbar grouper Long-tailed butterfly ray Japanese threadfin bream Large-scale tongue sole 0 1 2 3 4 5 Concentration of PCBs (WHO-iTEQ pg/g wet sample)

Figure 3. Total PCBs in demersal fish species and shellfish (WHOiTEQ pg/g wet weight).

Table 2. Polychlorinated biphenyls (four non-ortho-PCBs and eight mono-ortho-PCBs congeners) and toxic equivalents (WHO-iTEQ) as pg/g in fish and shellfish species. Fish and shellfish Analytes Non-ortho PCBs Mono-ortho PCBs WHO-iTEQ (pg/g)

Malabar red snapper 0.66 0.01 0.67

Sixbar grouper 0.75 0.13 0.88

Large-scale tongue sole 1.62 0.12 1.74

Cuttlefish

Cockles

Prawn

1.94 0.14 2.08

2.57 0.04 2.61

0.61 0.04 0.65

Long-tailed butterfly ray 0.66 0.01 0.67

Gray eelcatfish 1.65 0.11 1.76

Japanese threadfin bream 0.6 0.05 0.65

Non-ortho PCBs include (PCBs 77, 81, 126 and 169) Mono-ortho PCBs include (PCBs 105, 114, 118, 123, 156, 157, 167 and 189)

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(except for cuttlefish, gray eel catfish, and large-scale tongue sole) contained relatively low level of PCBs. Therefore, these fish and shellfish are safe to consume in term of PCBs level. Even though the levels are not high they still can cause the adverse health effect among the resident who consume excessive amount of fish, especially fatty fish. So, it is important to set limits for PCBs in fish and shellfish species to better estimate the risk of exposure to human through dietary intake especially fatty fish to meet nutritional requirement for long-chain n-3 polyunsaturated fatty acids. Acknowledgements This work was supported by a research grant from Ministry of Science, Technology and Innovation, Malaysia (MOSTI), Vote No. 5450400. The authors also acknowledged the assistance of staff from the Department of Nutrition and Dietetics, UPM and Doping Control Center, USM throughout the research project. They also extend the thanks to the Lembaga Kemajuan Ikan Malaysia (LKIM) and Persatuan Nelayan Kawasan (PNK) for their support and cooperation during the collection of the samples. References Abdul Majid, A. R. 2004. Field Guide to Selected Commercial Marine Fishes of Malaysian Waters. Fisheries Research Institute, Malaysia, 132 p. 2 Brown, A. 2008. Understanding Food: Principle and Preparation. 3rd edn. Thompson, Wardsworth, USA, 654 p. 3 Torpy, J. M., Lynm, C. and Glass, R. M.2006. Eating fish: Health benefits and risk. JAMA 296(15):1926. 4 Domingo, J. L., Bocio, A., Falco, G. and Llobet, J. M. 2007. Benefits and risks of fish consumption Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology 230:219-226. 5 Daviglus, M. L., Stamler, J. and Orencia, A. J. 1997. Fish consumption and the 30-year risk of fatal myocardial infarction. N. Engl. J. Med. 336:1046-1053. 6 Siscovick, D. S., Raghunathan, T. E. and King, I. 1995. Dietary intake and cell membrane levels of long-chain n-3 polyunsaturated fatty acids and the risk of primary cardiac arrest. JAMA 274:1363-1367. 7 Kannan, N., Tanabe, S., Ono, M. and Tatsukawa, R. 1989. Critical evaluation of polychlorinated biphenyl toxicity in terrestrial and marine mammals: Increasing impact of non-ortho and mono-ortho coplanar polychlorinated biphenyls from land to ocean. Arch. Environ. Contam. Toxicol. 18:850-857. 8 Bocio, A., Domingo, J. L., Falco, G. and Llobet, J. M. 2007. Concentrations of PCDD/PCDFs and PCBs in fish and seafood from Catalan (Spain) market: Estimated human intake. Environ. Int. 33:170175. 9 Fiedler, H. 1997. Polychlorinated Biphenyls (PCBs): Uses and Environmental Releases. Electronic references. Available at: http:// www.chem.unep.ch/pops/ POPs_Inc/proceedings/bangkok/ FIEDLER1 .html (Retrieved on 25 February 2009). 10 Gagnon, F., Trembaly, T., Rouette, J. and Cartier, J. F. 2004. Chemical risks associated with consumption of shellfish harvested on the north shore of the St. Lawrence Rivers lower estuary. Environ. Health Perspect. 112:883-888. 11 Van den Berg, M., Birnbaum, L. S., Denison, M., De Vito, M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L.,Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N. and Peterson, R. E. 2006. The 2005 World Health Organization re-evaluation of human and mammalian toxic equivalent factors for dioxins and dioxin-like compounds. Toxicol. Sci. 93(2):223-241. 1

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Journal of Food, Agriculture & Environment, Vol.11 (1), January 2013