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Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf
MPB-07679; No of Pages 5 Marine Pollution Bulletin xxx (2015) xxx–xxx
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Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf Abolfazl Naji a,⁎, Farhan R. Khan b, Seyed Hassan Hashemi c a b c
Department of Fisheries, Faculty of Marine Science and Technology, Hormozgan University, Bandar Abbas, Iran Department of Science and Environment, Roskilde University, Roskilde, Denmark Department of Environment, Branch of Hormozgan Province, Bandar Abbas, Iran
a r t i c l e
i n f o
Article history: Received 2 January 2016 Received in revised form 30 April 2016 Accepted 3 May 2016 Available online xxxx Keywords: Trace metals Seafood Pollution Estimated daily intake Target hazard quotient
a b s t r a c t This study was carried out to evaluate the concentration of trace metals (Cd, Cu, Ni, Pb and Zn) in the muscle of four fish species from the Persian Gulf. Trace metals were analyzed using atomic absorption spectroscopy and consumption rates advisory for minimizing chronic systemic effects in children and adults were estimated. The metals concentrations in analyzed fish samples were lower than legal limits. Cadmium target hazard quotient values suggested that the threshold to avoid the potential risk for children health is an exposure level lower than 3 meals per week. Hazard index values based on four metals (not including Pb) for the child age class were higher than those of the adult age class, suggesting that children may suffer from a higher health risk. This study provides information about the consumption limits of certain metals, in particular Cd, necessary for minimizing potential health risks resulting from human consumption. © 2015 Elsevier Ltd. All rights reserved.
In most Asian countries fish are an important dietary constituent providing protein, fatty acids as well as trace elements and vitamins (Copat et al., 2013; Hajeb et al., 2009). In Iran an estimated 380,000 tons of fish were caught in 2009, with approximately 90% belonging to southern waters of Iran (mainly Persian Gulf) (SaeiDehkordi et al., 2010). There are also reports of contamination in these fish from chemicals released into the environment, including trace metals, but to date the balance between benefits and risk due to ingestion of chemical contaminants has been poorly characterized (Copat et al., 2012, 2013; Domingo et al., 2007). Therefore, in recent years the fish consumption advisories for human populations have become increasingly important, as has the role of environmental monitoring projects that provide baselines assessments for determining the health risks to both fish species and human populations (Agah et al., 2009; Copat et al., 2013; Naji et al., 2014). Whilst some trace metals are essential (e.g. Cu or Zn) at high enough concentrations all metals can be toxic. Thus trace metals have been recognized as one of the most important pollutant groups in the aquatic environment affecting numerous eco-toxicological endpoints in various fish species, including organ specific toxicity, reduced fecundity and mortality. Trace metals are readily assimilated and bioaccumulated in aquatic organisms and can be passed between trophic levels, including humans consuming contaminated food (Copat et al., 2013; Naji and Ismail, 2012; Naji et al., 2010; Taweel et al., 2013). Whilst there are ⁎ Corresponding author. E-mail address: [email protected] (A. Naji).
studies assessing the metal concentrations in fish from the Persian Gulf (Agah et al., 2007, 2009, 2012; Saei-Dehkordi et al., 2010), to the best of our knowledge, there are no specific studies linking this to the consequences for human health. Thus the main objectives of this study were to (1) investigate metal concentrations (Cd, Cu, Ni, Pb and Zn) in local marine fish (Longtail tuna, Kluzinger's mullet, Indian mackerel, Pickhandle barracuda) and (2) estimate the potential risk for human health via their consumption. The Persian Gulf is characterized by warm and saline water with a total area of 240,000 km2. It has an average depth of 35 m which decreases from east to west with maximum depth of 90 m in the Strait of Hormuz. The average seawater temperature of the Persian Gulf is 28–30 °C, but it can rise up to 35.8 °C, and the oxygen content can vary from 4 to 7 mg l−1. High evaporation result in increasing salinity with values as high as 40 ppt (Agah et al., 2007, 2012; Naser, 2013). The Persian Gulf is considered one of the most highly anthropogenically impacted regions in the world. It is estimated that N 40% of the coasts of the Gulf has been developed (Hamza and Munawar, 2009; Naser, 2013). In terms of pollution, the water quality of the Persian Gulf is influenced by various industrial and urban outputs in which wastewater directly discharges into the sea or enters via rivers (Agah et al., 2007; Naser, 2013). Besides pollution through riverine inputs from adjacent countries (Iran, Iraq, Kuwait, Saudi Arabia, and the Emirates, Bahrain, Qatar and Oman), the Gulf has been exposed to various additional contaminants. Dredging and reclamation, hypersaline water discharges from desalination plants and oil pollution are examples of anthropogenic stresses that contribute to environmental degradation
http://dx.doi.org/10.1016/j.marpolbul.2016.05.002 0025-326X/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
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A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Table 1 Characteristics of the fish samples used in this study (presented as mean value ± standard deviation (S.D.)). Species
n
Length (cm)
Weight (g)
Feeding
Habitat
Longtail tuna (Thunnus tonggol) Kluzinger's mullet (Liza klunzingeri) Indian mackerel (Rastrelliger kanagurta) Pickhandle barracuda (Sphyraena jello)
12 10 15 10
81.32 ± 8 32.58 ± 2 21.76 ± 2 50.02 ± 5
4340.0 ± 320 338.3 ± 15 114.7 ± 7 563.6 ± 65
Carnivorous Detritivorous Carnivorous Carnivorous
Pelagic Demersal Pelagic Pelagic
Table 2 Quality assurance for trace metal analysis determined by the use of certified reference material TORT-2 lobster hepatopancreas (National Research Council, Canada). Measured concentrations (presented as mean value (μg g−1 (d.w.) ± S.D, n = 3) are compared to certified concentrations (μg g−1 (d.w.)). For each metal recovery (in %) was N90% and within acceptable limits of the certified concentrations. Instrument characteristics for each metal (elemental wavelength (nm) and limit of detection (LOD, μg l−1)) are also provided. Element
Wavelength
LOD
Measured concentration
Certified concentration
Recovery
Cd Cu Ni Pb Zn
228.6 324.8 232.0 217.0 213.9
1 1 2 2 3
28.03 ± 0.3 102.80 ± 3 2.45 ± 0.15 0.33 ± 0.05 174.60 ± 4
26.70 ± 0.6 106.00 ± 10 2.50 ± 0.19 0.35 ± 0.13 180.00 ± 6
105 ± 1 97 ± 3 98 ± 6 94 ± 12 97 ± 2
in the Persian Gulf (Sheppard et al., 2010). Being located in a major area for the petroleum industry, oil extraction, the passage of oil tankers, in addition to natural shallow depths, limited circulation, high salinity and temperature have a destructive impact on its marine ecosystem (Agah et al., 2007). The turnover and flushing time have been estimated to be in the range of 3–5 years indicating that pollutants are likely to reside in the Persian Gulf for a considerable time (Sheppard et al., 1992). The present study focused on four of the most heavily consumed and economically important fish species in Iran. A total of 47 freshly caught marine fish (n = 10–15 individuals per species, Table 1) were purchased during April and May 2015 from a major retail outlet in the Bandar Abbas (one of the most important fishing ports of the Persian Gulf). Individuals of each species had similar body length and weight. Upon purchase, fish were transported to the laboratory and rinsed four times with distilled water. Muscle tissues from each individual was dissected and placed in plastic zip-lock bags and stored at −20 °C for metal analysis. Dissected tissues were then oven-dried to a constant weight at 80 °C for 24 h, ground gently with an agate pestle and mortar, homogenized through a 100-μm nylon mesh sieve, and then stored in glass bottles (Gu et al., 2015). The moisture content of the tissue samples was determined in triplicate (Helrich, 1990). To avoid contamination, all laboratory equipment used during metal analysis was first rinsed with distilled water and left in 10% HNO3 for 24 h, then rinsed again (twice) with double-distilled water and left to dry at room temperature within a fume hood. Sample preparation for metal analysis followed the method of Hajeb et al., 2009 and Yap et al., 2015. Approximately 0.5 g of homogenized fish tissue was weighed and digested in a 10 ml combination (4:1 ratio) of concentrated HNO3 (AnalaRgrade, R&M Chemicals 65%) and HClO4 (AnalaR grade, R&M Chemicals 70%). Samples were heated first at low temperature (40 °C) for 1 h and then at 140 °C for 3 h. The digested material was filtered through a 0.22 μm acid-resistant cellulose nitrate membrane. At
the end of the digestion procedure, the solution was transferred to a 50 ml volumetric flask and diluted with double deionized water. Blank acid-only digestions and certified reference material (CRM) (Lobster Hepatopancreas Reference Material for Trace Metals, TORT-2, Canada) were similarly prepared as quality control and assurance. Samples were analyzed for Cd, Zn, Ni, Cu, and Pb using an air-acetylene flame atomic absorption spectrophotometer (FAAS, SpectrAA Model VARIAN240). Multiple-level calibration standards were used to generate calibration curves against which sample concentrations were calculated. Limits of detection (LODs) were measured using the expression 3Sblank / S, where Sblank is the standard deviation of at least five replicate measurements of blanks and S is the slope of the calibration curve (Palmieri et al., 2005). Procedural blanks were monitored every five samples during the analysis. Analysis of the certified references material was consistently comparable with the certified concentrations (N 90% recovery for all metals, Table 2). The LOD values and wavelengths of Cd, Zn, Ni, Cu and Pb are presented in Table 2. Metals levels in the fish muscle of each species are presented in Table 3 on a dry weight basis, with weight used for consumption modelling shown in parenthesis. Trace metals concentrations analyzed in the muscle tissue followed the order of Zn N Cu N Pb ≈ Ni N Cd and was consistent for all four species. The concentration of Cd in this study varied from 0.22 to 0.44 μg g−1. The highest to lowest values of Cd were observed as follows: Kluzinger's mullet N Indian mackerel N Longtail tuna N Pickhandle barracuda. The concentration of Cu measured in this study varied from 5.14 to 10.67 μg g−1. Maximum Cu values were found in Pickhandle barracuda. The lowest concentration was detected in Kluzinger's mullet. Copper was found to be the second most abundant metal in the fish species in this study. The concentration of Ni in fish tissues sampled varied from 2.49 to 5.13 μg g−1. The maximum value of Ni was present in Kluzinger's mullet followed by Pickhandle barracuda, Longtail tuna and then Indian mackerel. The maximum concentration of Pb detected in this study was in Pickhandle barracuda (6.46 μg g−1) followed by Longtail tuna (6.06 μg g−1), Kluzinger's mullet (4.73 μg g−1) and Indian mackerel (2.43 μg g−1). Zinc was the most abundant trace element in tissue samples from this study. The maximum Zn concentration was determined in Pickhandle barracuda (36.17 μg g−1), and the lowest Zn concentration observed in Kluzinger's mullet (19.58 μg g−1). The mean Zn concentration of tissue samples analyzed in this study was 30.65 μg g−1. Overall, studied metal concentrations in analyzed fish muscle samples were lower than legally defined limits. The present Cd ranges did not exceed the food safety guidelines (FSG) (1.00 mg kg−1 (w.w.)) set by WHO (1989), and the European Union (EC, 2006). The highest Cu concentration were present in Pickhandle barracuda and the lowest in Kluzinger's mullet, but again Cu concentrations were well below the FSG suggested by WHO (1996) (30 mg kg−1 (w.w.)). Similarly, the
Table 3 Trace metal concentrations found in the muscle tissue of each species presented as μg g−1 (d.w.) ± S.D. (n = 10–15, see Table 1). Wet weight concentrations used in estimated daily intake (EDIm), maximum allowable fish consumption rate (CRlim), target hazard quotient (THQ) and hazard index (HI) models are found in parenthesis and were derived using the % moisture determined for muscle tissue for each species. Species
Moisture (%)
Cd
Cu
Ni
Pb
Zn
Longtail tuna Kluzinger's mullet Indian mackerel Pickhandle barracuda
0.76 0.78 0.73 0.76
0.22 ± 0.25 (0.04) 0.44 ± 0.09 (0.09) 0.36 ± 0.05 (0.07) 0.17 ± 0.06 (0.03)
9.78 ± 0.7 (1.95) 5.14 ± 0.26 (1.02) 8.86 ± 0.86 (1.77) 10.67 ± 0.4 (2.13)
3.90 ± 0.05 (0.78) 5.13 ± 0.15 (1.03) 2.49 ± 0.16 (0.50) 4.09 ± 0.01 (0.82)
6.06 ± 0.10 (1.21) 4.73 ± 0.15 (0.94) 2.43 ± 0.08 (0.50) 6.46 ± 0.01 (1.30)
30.89 ± 2.71 (6.20) 19.58 ± 0.79 (3.9) 35.97 ± 5.33 (7.2) 36.17 ± 1.02 (7.2)
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
ranges for Ni and Pb were, respectively, lower than those set by the US Food and Drug Administration (USFDA, 2007) (80 mg Ni kg−1 (w.w.)), the FSGs set by WHO (2.00 mg Pb kg−1 (w.w.), WHO, 1996) and by the EU (1.50 mg Pb kg−1 (w.w.), EC, 2006). As expected Zn was the most abundant metal in the tissue, but concentrations were below the FSGs suggested by the Food Administration Organization (FAO) (30 mg Zn kg−1 (w.w.), FAO, 1983). According to the Priority List of Hazardous Substances and Disease Registry (ATSDR, 2013), the descending order of trace metals effecting human health is Pb N Cd N Ni N Zn N Cu. Several online databases provide information on the ingestion rate for fish by human populations. Here, we chose the U.S. Environmental Protection Agency methodology based on the estimation of risk-based consumption limits expressed in terms of real meals. All consumption limits and risk factors were calculated assuming, for adults, a meal size of 227 g and a body weight (BW) of 70 kg (USEPA, 2000), and, for children of six years old, a meal size of 114 g and a BW of 16 kg (Copat et al., 2013; Mansilla-Rivera and Rodríguez-Sierra, 2011). The estimated daily intake per meal size of seafood (EDI) was made according to Eq. (1). Where MS is the meal size, C is the metal concentration (mg kg− 1 (w.w.)) and BW is the body weight. Based on the USEPA (1989) Guidance, we assumed that the ingestion dose is equal to the adsorbed contaminant dose and that cooking has no effect on the contaminants (Chien et al., 2002). EDI ¼
C MS : BW
ð1Þ
To calculate the allowable daily consumption of fish, Eq. (2) was used. The results were expressed in kilograms of fish per day. On the assumption that no other sources of Cu, Cd, Zn, Pb and Ni exist in the diets of the consumers, the allowable daily consumption limits for fish for which no adverse health effects are expected are determined as follows: CR lim
RfD BW ¼ C
ð2Þ
where CRlim is the maximum safe daily consumption rate of fish (kg day− 1), RfD is the reference dose for each trace metal (mg kg−1 d−1), BW is the average consumer body weight (in kg) and C is the concentration of chemical in the edible portion of fish (mg kg−1). The RfD is an estimate of the daily intake of a contaminant over a lifetime that would not be expected to cause adverse health effects (USEPA, 2000). The RfD values (μg kg−1 day−1) provided by the USEPA's regional screening level were 1.0 for Cd, 40.0 for Cu, 20.0 for Ni and 300.0 for Zn (USEPA, 2015). The European Protection Agency has declined to set a RfD for Pb because it has found no evidence of a threshold below which a non-harmful intake could be allowed (USEPA, 2004; Copat et al., 2012; Yap et al., 2015). Target hazard quotients (THQ, Equation 3) provide the ratio between exposure and the reference doses. Calculations were made using the standard assumption for an integrated USEPA risk analysis (USEPA, 1989). When THQ value is above 1, meaning that THQ is higher than the reference dose, systemic toxic effects may occur. In Eq. 3, EF is
3
Table 5 Maximum allowable fish consumption rate (CRlim) for the studied metals (mg kg−1 day−1(w.w.)) in adults (A) and children (C) based on the consumption of fish muscle. Species
Metals
Metal concentrations
Longtail tuna
Cd Cu Ni Zn Cd Cu Ni Zn Cd Cu Ni Zn Cd Cu Ni Zn
0.04 1.95 0.78 6.20 0.09 1.02 1.03 3.92 0.07 1.77 0.50 7.20 0.03 2.13 0.82 7.23
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
CRlim A
C
1.75 1.43 1.79 3.40 0.78 2.74 1.36 5.36 1 1.58 2.80 2.92 2.33 1.32 1.71 2.90
0.40 0.33 0.41 0.78 0.18 0.62 0.31 1.23 0.23 0.36 0.64 0.67 0.53 0.30 0.39 0.66
the exposure frequency, or number of exposure events per year of exposure (from 365 days per year for people who eat fish seven times a week to 52 days per year for people who eat fish once a week); ED is the exposure duration (70 years in adults and 6 years in children), MS is the food meal size (0.227 kg day−1 for adults and 0.114 kg day−1 for children), C is the metal concentration in fish (μg g−1, (w.w)), RfD is the oral reference dose (μg g−1 day− 1), BW is the body weight (adults 70 kg; children 16 kg), and AT is the averaging time (equal to EF × ED). EF, ED, MS, BW and AT, are default data provided by the USEPA (USEPA, 1989; USEPA, 2000), for consumption limits calculations. THQ ¼
EF ED MS C : BW RfD AT
ð3Þ
For the risk assessment of multiple trace metals contained in fish, a total hazard index (HI, Eq. 4) was employed by summing all the calculated THQi values of trace metals (Li et al., 2013). CRlim, THQ and HI values could not be calculated for Pb because there is no reported RfD value. Where THQi is the targeted hazard quotient of an individual metals in the present study (Cd Zn, Cu, and Ni). Hazard IndexðHIÞ ¼
X THQ i ¼ THQ Cd þ THQ Zn þ THQ cu þ THQ Ni : ð4Þ
The estimated daily intake per meal size (EDI) of metals for adult and children through the consumption of the fish muscle (edible parts) are presented in Table 4. The average EDI values of metals for both adult and children through fish consumption can be ordered as follows: Zn N Cu N Pb ≈ Ni N Cd. EDI values were lower than those suggested by the Joint FAO/WHO Expert Committee on Food Additives (JECFA, 2009) for Cd, Zn and Cu for both adults and children, but for Pb the value was higher than the tolerable intake (TI in μg kg− 1 day− 1)
Table 4 Estimated daily intake per meal size (EDIm) in adults (A) and children (C) compared with tolerable intake (TI) (μg Kd−1 gd−1) suggested by Joint FAO/WHO Expert Committee on Food Additives(JECFA)based on the consumption of fish muscle. TI
1 500 – 3.57 300–1000
Metals
Cd Cu Ni Pb Zn
Longtail tuna
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
EDImA
EDImC
EDImA
EDImC
EDImA
EDImC
EDImA
EDImC
0.14 6.34 2.53 3.93 20.03
1.03 45.18 18.02 27.99 142.74
0.29 3.33 3.32 3.07 12.70
0.63 7.32 7.30 6.74 27.91
0.23 5.75 1.61 1.58 23.33
0.51 12.63 3.54 3.46 51.26
0.11 6.92 2.66 4.19 23.46
0.24 15.20 5.83 9.21 51.54
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
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A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Table 6 Target hazard quotient (THQ) and Hazard index(HI) of Cd, Zn, Cu and Ni in adults (A) and children (C) based on the consumption of fish muscle. Species
Exposure time (d)
Target hazard quotient (THQ) Cd
Longtail tuna
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
1 3 7 1 3 7 1 3 7 1 3 7
Hazard Index (HI)
Cu
Ni
Zn
A
C
A
C
A
C
A
C
0.03 0.09 0.14 0.06 0.17 0.29 0.05 0.14 0.23 0.02 0.06 0.11
0.22 0.65 1.52 0.43 1.30 3.04 0.35 1.06 2.47 0.16 0.49 1.14
0.02 0.07 0.16 0.01 0.04 0.08 0.02 0.06 0.14 0.02 0.07 0.17
0.05 0.15 0.35 0.03 0.08 0.18 0.05 0.14 0.32 0.05 0.16 0.38
0.02 0.05 0.13 0.02 0.07 0.17 0.01 0.03 0.08 0.02 0.06 0.13
0.04 0.12 0.28 0.05 0.16 0.37 0.03 0.08 0.18 0.04 0.13 0.29
0.00 0.03 0.07 0.00 0.02 0.04 0.00 0.03 0.08 0.00 0.03 0.08
0.02 0.06 0.15 0.01 0.04 0.09 0.02 0.07 0.17 0.02 0.07 0.17
suggested by JECFA, except in the case of Kluzinger's mullet for the adult age class, and Indian mackerel for the child age class. Calculated allowable fish consumption rates (CRlim kg−1 day−1) are shown Table 5. In accordance with the USEPA (2000), these risk-based consumption limits are estimated as the maximum daily consumption rates of contaminated fish and in these cases would not be expected to cause any adverse health effects for human consumers, irrespective of age. The THQ values of metals through muscle consumption for children and adults are shown in Table 6. THQ values for Zn, Cu and Ni for both age classes considered, and for Cd in adult age class were all below 1. Therefore, the daily intakes for these metals derived from a real meal at levels of assumed exposure were not likely to cause any adverse effect during a human lifetime. However, THQ values of Cd in children class in some levels of assumed exposure (7 and 3 days per week) were N1, indicating the presence of a health risk. That means that there is a potential risk of developing chronic systemic effects due to Cd intake. Therefore, THQ values for Cd indicated that the threshold to avoid the potential risk for children health was an exposure lower than 3 meals per week. HI was also employed in this study because humans are often exposed to more than one contaminant and suffer from combined or interactive effects (Li et al., 2013). HI values based on four metals (not including Pb) of child age class were higher than those of adult age class, which means that children may suffer a higher risk to their health. In conclusion, the bioaccumulation of metals in seafood is a major health concern globally. The levels of studied trace metals in the muscle of Persian fish species were generally lower than the maximum permitted concentrations recommended by food safety guidelines. With the exception of Pb, EDI values were lower than those suggested by JECFA for Cd, Cu, and Zn for both adult and children. THQ values for Cu, Ni and Zn for both adults and children, and for Cd in adults were not likely to cause any adverse effect during lifetime in population. THQ values for Cd in children at some levels of assumed exposure (7 and 3 days per week) were higher than 1, indicating the presence of a health risk. Therefore, more attention should be paid to the monitoring of Cd and Pb in fish from Persian Gulf in future which might pose potential health risks to population. Due to the increasing environmental pressure on the Persian Gulf ecosystem, a regular and on-going monitoring of trace metal levels in marine organisms is necessary to prevent any deleterious effect on the human population. References Agah, H., Leermakers, M., Elskens, M., Fatemi, S.R., Baeyens, W., 2007. Total mercury and methyl mercury concentrations in fish from the Persian Gulf and the Caspian Sea. Water Air Soil Pollut. 181 (1–4), 95–105.
A
C
0.07 0.24 0.50 0.09 0.30 0.58 0.08 0.26 0.53 0.06 0.22 0.49
0.33 0.98 2.3 0.52 1.58 3.68 0.45 1.35 3.14 0.27 0.85 1.98
Agah, H., Leermakers, M., Elskens, M., Fatemi, S.M.R., Baeyens, W., 2009. Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf. Environ. Monit. Assess. 157 (1–4), 499–514. Agah, H., Hashtroudi, M.S., Baeyens, W., 2012. Trace metals and major elements in sediments of the northern Persian gulf. J. Persian. Gulf. 3 (7), 45–58. ATSDR (Agency for Toxic Substance and Disease Rigestry), 2013. Priority List of Hazardous Substances. Atlanta, Georgia, USA. Chien, L.C., Hung, T.C., Choang, K.Y., Yeh, Ch.Y., Meng, P.J., Shieh, M.J., Han, B.C.H., 2002. Daily intake of TBT, Cu, Zn, Cd and As for fishermen in Taiwan. Sci. Total Environ. 285 (1), 177–185. Copat, Ch., Bella, F., Castaing, M., Fallico, R., Sciacca, S., Ferrante, M., 2012. Heavy metals concentrations in fish from Sicily (Mediterranean Sea) and evaluation of possible health risks to consumers. Bull. Environ. Contam. Toxicol. 88 (1), 78–83. Copat, Ch., Arena, G., Fiore, M., Ledda, C., Fallico, R., Sciacca, S., Ferrante, M., 2013. Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: consumption advisories. Food Chem. Toxicol. 53, 33–37. Domingo, J.L., Bocio, A., Falcó, G., 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 (2), 219–226. EC (European Commission), 2006. Commission Regulation (EC) No 1881/2006 of the European parliament and the council of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Communities L364 (18) (Available online at: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX: 32006R1881&from=EN). FAO (Food Administration Organization). 1983. Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fish. Circ. 764. FAO, Rome, pp. 102, (http://www.fao.org/fi/oldsite/eims_search/1_dett.asp?calling=simple_s_ result&lang=fr&pub_id=65155). Gu, Y.G., Lin, Q., Wang, X.H., Du, F.Y., Yu, Z.L., Huang, H.H., 2015. Heavy metal concentrations in wild fishes captured from the South China Sea and associated health risks. Mar. Pollut. Bull. 96 (1–2), 508–512. Hajeb, P., Jinap, S., Ismail, A., Fatimah, A.B., Jamilah, B., Rahim, M. Abdul, 2009. Assessment of mercury level in commonly consumed marine fishes in Malaysia. Food Control 20 (1), 79–84. Hamza, W., Munawar, M., 2009. Protecting and managing the Arabian Gulf: past, present and future. Aquat. Ecosyst. Health Manag. 12 (4), 429–439. Helrich, K.C., 1990. Official Methods of Analysis of the AOAC. Volume 2. Association of Official Analytical Chemists Inc. JECFA (Joint FAO/WHO Expert Committee on Food Additives), 2009. Evaluations of the Joint FAO/WHO Expert Committee on Food Additives. (Available at:http://apps. Who.int/ipsc//database/evaluations/search.aspx). Li, J., Huang, Zh.Y., Hu, Y., Yang, H., 2013. Potential risk assessment of heavy metals by consuming shellfish collected from Xiamen, China. Environ. Sci. Pollut. Res. 20 (5), 2937–2947. Mansilla-Rivera, I., Rodríguez-Sierra, C.J., 2011. Metal levels in fish captured in Puerto Rico and estimation of risk from fish consumption. Arch. Environ. Contam. Toxicol. 60 (1), 132–144. Naji, A., Ismail, A., 2012. Sediment quality assessment of Klang Estuary, Malaysia. Aquat. Ecosyst. Health Manag. 15 (3), 287–293. Naji, A., Ismail, A., Ismail, A.R., 2010. Chemical speciation and contamination assessment of Zn and Cd by sequential extraction in surface sediment of Klang River, Malaysia. Microchem. J. 95 (2), 285–292. Naji, A., Ismail, A., Kamrani, E., Sohrabi, T., 2014. Correlation of MT levels in livers and gills with heavy metals in wild tilapia (Oreochromis mossambicus) from the Klang River, Malaysia. Bull. Environ. Contam. Toxicol. 92 (6), 674–679. Naser, H.A., 2013. Assessment and management of heavy metal pollution in the marine environment of the Persian Gulf: a review. Mar. Pollut. Bull. 72 (1), 6–13. Palmieri, R.M., La Pera, L., Di Bella, G., Dugo, G., 2005. Simultaneous determination of Cd (II), Cu (II), Pb (II) and Zn (II) by derivative stripping chronopotentiometry in Pittosporum tobira leaves: a measurement of local atmospheric pollution in Messina (Sicily, Italy). Chemosphere 59 (8), 1161–1168.
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Saei-Dehkordi, S. Siavash, Fallah, Aziz A., Nematollahi, Amin, 2010. Arsenic and mercury in commercially valuable fish species from the Persian Gulf: influence of season and habitat. Food Chem. Toxicol. 48 (10), 2945–2950. Sheppard, Ch., Price, A., Roberts, C., 1992. Marine Ecology of the Arabian Region. Academic Press. Sheppard, Ch., Al-Husiani, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, Francesca, D., Eric, D., Nicholas K., Durvasula, S.R.V., 2010. The Gulf: a young sea in decline. Mar. Pollut. Bull. 60 (1), 13–38. Taweel, A., Shuhaimi-Othman, M., Ahmad, A.K., 2013. Assessment of heavy metals in tilapia fish (Oreochromis niloticus) from the Langat River and Engineering Lake in Bangi, Malaysia, and evaluation of the health risk from tilapia consumption. Ecotoxicol. Environ. Saf. 93, 45–51. USEPA (US Environmental Protection Agency), 1989. Risk Assessment Guidance for Superfund. Vol. I. Human Health Evaluation Manual (Part A), Interim Final. EPA 540/1–89/002United States Environmental Protection Agency, Washington, DC. USEPA (US Environmental Protection Agency), 2000. Guidance for Assessing Chemical Contamination Data for Use in Fish Advisories. Vol. II. Risk Assessment and Fish Consumption Limits EPA/823-B94-004United States Environmental Protection Agency, Washington, DC. USEPA (US Environmental Protection Agency), 2004. Integrated risk information system (IRIS) on lead and compounds (inorganic). National Center for Environmental
5
Assessment. Office of Research and Development, Washington, DC (Last revised 2004. Available online at: http://www.epa.gov/iris/subst/0277.htm#bib). USEPA (US Environmental Protection Agency), 2015. Human health risk assessment. Regional Screening Level (RSL)—Summary Table (Available online at: http://www.epa. gov/reg3hwmd/risk/human/rbconcentration_table/Generic_Tables/docs/master_sl_ table_run_JAN2015.pdf). USFDA (US Food and Drug Administration), 2007. National shellfish sanitation program. Guide for the control of molluscan shellfish 2007. Guidance Documents Chapter II. Growing Areas: 04. Action Levels, Tolerances and Guidance Levels for Poisonous or Deleterious Substances in Seafood (Available online at: http://www.issc.org/client_ resources/2007.pdf). WHO (World Health Organization), 1989. Heavy metals—environmental aspects. Environment Health Criteria No. 85, Geneva, 1989. WHO (World Health Organization), 1996. Health criteria other supporting information. Guidelines for Drinking Water Quality, second ed. WHO, Geneva, pp. 31–388. Yap, C.K., Jusoh, A., Leong, W.J., Karami, A., Ong, G.H., 2015. Potential human health risk assessment of heavy metals via the consumption of tilapia Oreochromis mossambicus collected from contaminated and uncontaminated ponds. Environ. Monit. Assess. 187 (9), 1–16.
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Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf Abolfazl Naji a,⁎, Farhan R. Khan b, Seyed Hassan Hashemi c a b c
Department of Fisheries, Faculty of Marine Science and Technology, Hormozgan University, Bandar Abbas, Iran Department of Science and Environment, Roskilde University, Roskilde, Denmark Department of Environment, Branch of Hormozgan Province, Bandar Abbas, Iran
a r t i c l e
i n f o
Article history: Received 2 January 2016 Received in revised form 30 April 2016 Accepted 3 May 2016 Available online xxxx Keywords: Trace metals Seafood Pollution Estimated daily intake Target hazard quotient
a b s t r a c t This study was carried out to evaluate the concentration of trace metals (Cd, Cu, Ni, Pb and Zn) in the muscle of four fish species from the Persian Gulf. Trace metals were analyzed using atomic absorption spectroscopy and consumption rates advisory for minimizing chronic systemic effects in children and adults were estimated. The metals concentrations in analyzed fish samples were lower than legal limits. Cadmium target hazard quotient values suggested that the threshold to avoid the potential risk for children health is an exposure level lower than 3 meals per week. Hazard index values based on four metals (not including Pb) for the child age class were higher than those of the adult age class, suggesting that children may suffer from a higher health risk. This study provides information about the consumption limits of certain metals, in particular Cd, necessary for minimizing potential health risks resulting from human consumption. © 2015 Elsevier Ltd. All rights reserved.
In most Asian countries fish are an important dietary constituent providing protein, fatty acids as well as trace elements and vitamins (Copat et al., 2013; Hajeb et al., 2009). In Iran an estimated 380,000 tons of fish were caught in 2009, with approximately 90% belonging to southern waters of Iran (mainly Persian Gulf) (SaeiDehkordi et al., 2010). There are also reports of contamination in these fish from chemicals released into the environment, including trace metals, but to date the balance between benefits and risk due to ingestion of chemical contaminants has been poorly characterized (Copat et al., 2012, 2013; Domingo et al., 2007). Therefore, in recent years the fish consumption advisories for human populations have become increasingly important, as has the role of environmental monitoring projects that provide baselines assessments for determining the health risks to both fish species and human populations (Agah et al., 2009; Copat et al., 2013; Naji et al., 2014). Whilst some trace metals are essential (e.g. Cu or Zn) at high enough concentrations all metals can be toxic. Thus trace metals have been recognized as one of the most important pollutant groups in the aquatic environment affecting numerous eco-toxicological endpoints in various fish species, including organ specific toxicity, reduced fecundity and mortality. Trace metals are readily assimilated and bioaccumulated in aquatic organisms and can be passed between trophic levels, including humans consuming contaminated food (Copat et al., 2013; Naji and Ismail, 2012; Naji et al., 2010; Taweel et al., 2013). Whilst there are ⁎ Corresponding author. E-mail address: [email protected] (A. Naji).
studies assessing the metal concentrations in fish from the Persian Gulf (Agah et al., 2007, 2009, 2012; Saei-Dehkordi et al., 2010), to the best of our knowledge, there are no specific studies linking this to the consequences for human health. Thus the main objectives of this study were to (1) investigate metal concentrations (Cd, Cu, Ni, Pb and Zn) in local marine fish (Longtail tuna, Kluzinger's mullet, Indian mackerel, Pickhandle barracuda) and (2) estimate the potential risk for human health via their consumption. The Persian Gulf is characterized by warm and saline water with a total area of 240,000 km2. It has an average depth of 35 m which decreases from east to west with maximum depth of 90 m in the Strait of Hormuz. The average seawater temperature of the Persian Gulf is 28–30 °C, but it can rise up to 35.8 °C, and the oxygen content can vary from 4 to 7 mg l−1. High evaporation result in increasing salinity with values as high as 40 ppt (Agah et al., 2007, 2012; Naser, 2013). The Persian Gulf is considered one of the most highly anthropogenically impacted regions in the world. It is estimated that N 40% of the coasts of the Gulf has been developed (Hamza and Munawar, 2009; Naser, 2013). In terms of pollution, the water quality of the Persian Gulf is influenced by various industrial and urban outputs in which wastewater directly discharges into the sea or enters via rivers (Agah et al., 2007; Naser, 2013). Besides pollution through riverine inputs from adjacent countries (Iran, Iraq, Kuwait, Saudi Arabia, and the Emirates, Bahrain, Qatar and Oman), the Gulf has been exposed to various additional contaminants. Dredging and reclamation, hypersaline water discharges from desalination plants and oil pollution are examples of anthropogenic stresses that contribute to environmental degradation
http://dx.doi.org/10.1016/j.marpolbul.2016.05.002 0025-326X/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
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Table 1 Characteristics of the fish samples used in this study (presented as mean value ± standard deviation (S.D.)). Species
n
Length (cm)
Weight (g)
Feeding
Habitat
Longtail tuna (Thunnus tonggol) Kluzinger's mullet (Liza klunzingeri) Indian mackerel (Rastrelliger kanagurta) Pickhandle barracuda (Sphyraena jello)
12 10 15 10
81.32 ± 8 32.58 ± 2 21.76 ± 2 50.02 ± 5
4340.0 ± 320 338.3 ± 15 114.7 ± 7 563.6 ± 65
Carnivorous Detritivorous Carnivorous Carnivorous
Pelagic Demersal Pelagic Pelagic
Table 2 Quality assurance for trace metal analysis determined by the use of certified reference material TORT-2 lobster hepatopancreas (National Research Council, Canada). Measured concentrations (presented as mean value (μg g−1 (d.w.) ± S.D, n = 3) are compared to certified concentrations (μg g−1 (d.w.)). For each metal recovery (in %) was N90% and within acceptable limits of the certified concentrations. Instrument characteristics for each metal (elemental wavelength (nm) and limit of detection (LOD, μg l−1)) are also provided. Element
Wavelength
LOD
Measured concentration
Certified concentration
Recovery
Cd Cu Ni Pb Zn
228.6 324.8 232.0 217.0 213.9
1 1 2 2 3
28.03 ± 0.3 102.80 ± 3 2.45 ± 0.15 0.33 ± 0.05 174.60 ± 4
26.70 ± 0.6 106.00 ± 10 2.50 ± 0.19 0.35 ± 0.13 180.00 ± 6
105 ± 1 97 ± 3 98 ± 6 94 ± 12 97 ± 2
in the Persian Gulf (Sheppard et al., 2010). Being located in a major area for the petroleum industry, oil extraction, the passage of oil tankers, in addition to natural shallow depths, limited circulation, high salinity and temperature have a destructive impact on its marine ecosystem (Agah et al., 2007). The turnover and flushing time have been estimated to be in the range of 3–5 years indicating that pollutants are likely to reside in the Persian Gulf for a considerable time (Sheppard et al., 1992). The present study focused on four of the most heavily consumed and economically important fish species in Iran. A total of 47 freshly caught marine fish (n = 10–15 individuals per species, Table 1) were purchased during April and May 2015 from a major retail outlet in the Bandar Abbas (one of the most important fishing ports of the Persian Gulf). Individuals of each species had similar body length and weight. Upon purchase, fish were transported to the laboratory and rinsed four times with distilled water. Muscle tissues from each individual was dissected and placed in plastic zip-lock bags and stored at −20 °C for metal analysis. Dissected tissues were then oven-dried to a constant weight at 80 °C for 24 h, ground gently with an agate pestle and mortar, homogenized through a 100-μm nylon mesh sieve, and then stored in glass bottles (Gu et al., 2015). The moisture content of the tissue samples was determined in triplicate (Helrich, 1990). To avoid contamination, all laboratory equipment used during metal analysis was first rinsed with distilled water and left in 10% HNO3 for 24 h, then rinsed again (twice) with double-distilled water and left to dry at room temperature within a fume hood. Sample preparation for metal analysis followed the method of Hajeb et al., 2009 and Yap et al., 2015. Approximately 0.5 g of homogenized fish tissue was weighed and digested in a 10 ml combination (4:1 ratio) of concentrated HNO3 (AnalaRgrade, R&M Chemicals 65%) and HClO4 (AnalaR grade, R&M Chemicals 70%). Samples were heated first at low temperature (40 °C) for 1 h and then at 140 °C for 3 h. The digested material was filtered through a 0.22 μm acid-resistant cellulose nitrate membrane. At
the end of the digestion procedure, the solution was transferred to a 50 ml volumetric flask and diluted with double deionized water. Blank acid-only digestions and certified reference material (CRM) (Lobster Hepatopancreas Reference Material for Trace Metals, TORT-2, Canada) were similarly prepared as quality control and assurance. Samples were analyzed for Cd, Zn, Ni, Cu, and Pb using an air-acetylene flame atomic absorption spectrophotometer (FAAS, SpectrAA Model VARIAN240). Multiple-level calibration standards were used to generate calibration curves against which sample concentrations were calculated. Limits of detection (LODs) were measured using the expression 3Sblank / S, where Sblank is the standard deviation of at least five replicate measurements of blanks and S is the slope of the calibration curve (Palmieri et al., 2005). Procedural blanks were monitored every five samples during the analysis. Analysis of the certified references material was consistently comparable with the certified concentrations (N 90% recovery for all metals, Table 2). The LOD values and wavelengths of Cd, Zn, Ni, Cu and Pb are presented in Table 2. Metals levels in the fish muscle of each species are presented in Table 3 on a dry weight basis, with weight used for consumption modelling shown in parenthesis. Trace metals concentrations analyzed in the muscle tissue followed the order of Zn N Cu N Pb ≈ Ni N Cd and was consistent for all four species. The concentration of Cd in this study varied from 0.22 to 0.44 μg g−1. The highest to lowest values of Cd were observed as follows: Kluzinger's mullet N Indian mackerel N Longtail tuna N Pickhandle barracuda. The concentration of Cu measured in this study varied from 5.14 to 10.67 μg g−1. Maximum Cu values were found in Pickhandle barracuda. The lowest concentration was detected in Kluzinger's mullet. Copper was found to be the second most abundant metal in the fish species in this study. The concentration of Ni in fish tissues sampled varied from 2.49 to 5.13 μg g−1. The maximum value of Ni was present in Kluzinger's mullet followed by Pickhandle barracuda, Longtail tuna and then Indian mackerel. The maximum concentration of Pb detected in this study was in Pickhandle barracuda (6.46 μg g−1) followed by Longtail tuna (6.06 μg g−1), Kluzinger's mullet (4.73 μg g−1) and Indian mackerel (2.43 μg g−1). Zinc was the most abundant trace element in tissue samples from this study. The maximum Zn concentration was determined in Pickhandle barracuda (36.17 μg g−1), and the lowest Zn concentration observed in Kluzinger's mullet (19.58 μg g−1). The mean Zn concentration of tissue samples analyzed in this study was 30.65 μg g−1. Overall, studied metal concentrations in analyzed fish muscle samples were lower than legally defined limits. The present Cd ranges did not exceed the food safety guidelines (FSG) (1.00 mg kg−1 (w.w.)) set by WHO (1989), and the European Union (EC, 2006). The highest Cu concentration were present in Pickhandle barracuda and the lowest in Kluzinger's mullet, but again Cu concentrations were well below the FSG suggested by WHO (1996) (30 mg kg−1 (w.w.)). Similarly, the
Table 3 Trace metal concentrations found in the muscle tissue of each species presented as μg g−1 (d.w.) ± S.D. (n = 10–15, see Table 1). Wet weight concentrations used in estimated daily intake (EDIm), maximum allowable fish consumption rate (CRlim), target hazard quotient (THQ) and hazard index (HI) models are found in parenthesis and were derived using the % moisture determined for muscle tissue for each species. Species
Moisture (%)
Cd
Cu
Ni
Pb
Zn
Longtail tuna Kluzinger's mullet Indian mackerel Pickhandle barracuda
0.76 0.78 0.73 0.76
0.22 ± 0.25 (0.04) 0.44 ± 0.09 (0.09) 0.36 ± 0.05 (0.07) 0.17 ± 0.06 (0.03)
9.78 ± 0.7 (1.95) 5.14 ± 0.26 (1.02) 8.86 ± 0.86 (1.77) 10.67 ± 0.4 (2.13)
3.90 ± 0.05 (0.78) 5.13 ± 0.15 (1.03) 2.49 ± 0.16 (0.50) 4.09 ± 0.01 (0.82)
6.06 ± 0.10 (1.21) 4.73 ± 0.15 (0.94) 2.43 ± 0.08 (0.50) 6.46 ± 0.01 (1.30)
30.89 ± 2.71 (6.20) 19.58 ± 0.79 (3.9) 35.97 ± 5.33 (7.2) 36.17 ± 1.02 (7.2)
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
ranges for Ni and Pb were, respectively, lower than those set by the US Food and Drug Administration (USFDA, 2007) (80 mg Ni kg−1 (w.w.)), the FSGs set by WHO (2.00 mg Pb kg−1 (w.w.), WHO, 1996) and by the EU (1.50 mg Pb kg−1 (w.w.), EC, 2006). As expected Zn was the most abundant metal in the tissue, but concentrations were below the FSGs suggested by the Food Administration Organization (FAO) (30 mg Zn kg−1 (w.w.), FAO, 1983). According to the Priority List of Hazardous Substances and Disease Registry (ATSDR, 2013), the descending order of trace metals effecting human health is Pb N Cd N Ni N Zn N Cu. Several online databases provide information on the ingestion rate for fish by human populations. Here, we chose the U.S. Environmental Protection Agency methodology based on the estimation of risk-based consumption limits expressed in terms of real meals. All consumption limits and risk factors were calculated assuming, for adults, a meal size of 227 g and a body weight (BW) of 70 kg (USEPA, 2000), and, for children of six years old, a meal size of 114 g and a BW of 16 kg (Copat et al., 2013; Mansilla-Rivera and Rodríguez-Sierra, 2011). The estimated daily intake per meal size of seafood (EDI) was made according to Eq. (1). Where MS is the meal size, C is the metal concentration (mg kg− 1 (w.w.)) and BW is the body weight. Based on the USEPA (1989) Guidance, we assumed that the ingestion dose is equal to the adsorbed contaminant dose and that cooking has no effect on the contaminants (Chien et al., 2002). EDI ¼
C MS : BW
ð1Þ
To calculate the allowable daily consumption of fish, Eq. (2) was used. The results were expressed in kilograms of fish per day. On the assumption that no other sources of Cu, Cd, Zn, Pb and Ni exist in the diets of the consumers, the allowable daily consumption limits for fish for which no adverse health effects are expected are determined as follows: CR lim
RfD BW ¼ C
ð2Þ
where CRlim is the maximum safe daily consumption rate of fish (kg day− 1), RfD is the reference dose for each trace metal (mg kg−1 d−1), BW is the average consumer body weight (in kg) and C is the concentration of chemical in the edible portion of fish (mg kg−1). The RfD is an estimate of the daily intake of a contaminant over a lifetime that would not be expected to cause adverse health effects (USEPA, 2000). The RfD values (μg kg−1 day−1) provided by the USEPA's regional screening level were 1.0 for Cd, 40.0 for Cu, 20.0 for Ni and 300.0 for Zn (USEPA, 2015). The European Protection Agency has declined to set a RfD for Pb because it has found no evidence of a threshold below which a non-harmful intake could be allowed (USEPA, 2004; Copat et al., 2012; Yap et al., 2015). Target hazard quotients (THQ, Equation 3) provide the ratio between exposure and the reference doses. Calculations were made using the standard assumption for an integrated USEPA risk analysis (USEPA, 1989). When THQ value is above 1, meaning that THQ is higher than the reference dose, systemic toxic effects may occur. In Eq. 3, EF is
3
Table 5 Maximum allowable fish consumption rate (CRlim) for the studied metals (mg kg−1 day−1(w.w.)) in adults (A) and children (C) based on the consumption of fish muscle. Species
Metals
Metal concentrations
Longtail tuna
Cd Cu Ni Zn Cd Cu Ni Zn Cd Cu Ni Zn Cd Cu Ni Zn
0.04 1.95 0.78 6.20 0.09 1.02 1.03 3.92 0.07 1.77 0.50 7.20 0.03 2.13 0.82 7.23
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
CRlim A
C
1.75 1.43 1.79 3.40 0.78 2.74 1.36 5.36 1 1.58 2.80 2.92 2.33 1.32 1.71 2.90
0.40 0.33 0.41 0.78 0.18 0.62 0.31 1.23 0.23 0.36 0.64 0.67 0.53 0.30 0.39 0.66
the exposure frequency, or number of exposure events per year of exposure (from 365 days per year for people who eat fish seven times a week to 52 days per year for people who eat fish once a week); ED is the exposure duration (70 years in adults and 6 years in children), MS is the food meal size (0.227 kg day−1 for adults and 0.114 kg day−1 for children), C is the metal concentration in fish (μg g−1, (w.w)), RfD is the oral reference dose (μg g−1 day− 1), BW is the body weight (adults 70 kg; children 16 kg), and AT is the averaging time (equal to EF × ED). EF, ED, MS, BW and AT, are default data provided by the USEPA (USEPA, 1989; USEPA, 2000), for consumption limits calculations. THQ ¼
EF ED MS C : BW RfD AT
ð3Þ
For the risk assessment of multiple trace metals contained in fish, a total hazard index (HI, Eq. 4) was employed by summing all the calculated THQi values of trace metals (Li et al., 2013). CRlim, THQ and HI values could not be calculated for Pb because there is no reported RfD value. Where THQi is the targeted hazard quotient of an individual metals in the present study (Cd Zn, Cu, and Ni). Hazard IndexðHIÞ ¼
X THQ i ¼ THQ Cd þ THQ Zn þ THQ cu þ THQ Ni : ð4Þ
The estimated daily intake per meal size (EDI) of metals for adult and children through the consumption of the fish muscle (edible parts) are presented in Table 4. The average EDI values of metals for both adult and children through fish consumption can be ordered as follows: Zn N Cu N Pb ≈ Ni N Cd. EDI values were lower than those suggested by the Joint FAO/WHO Expert Committee on Food Additives (JECFA, 2009) for Cd, Zn and Cu for both adults and children, but for Pb the value was higher than the tolerable intake (TI in μg kg− 1 day− 1)
Table 4 Estimated daily intake per meal size (EDIm) in adults (A) and children (C) compared with tolerable intake (TI) (μg Kd−1 gd−1) suggested by Joint FAO/WHO Expert Committee on Food Additives(JECFA)based on the consumption of fish muscle. TI
1 500 – 3.57 300–1000
Metals
Cd Cu Ni Pb Zn
Longtail tuna
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
EDImA
EDImC
EDImA
EDImC
EDImA
EDImC
EDImA
EDImC
0.14 6.34 2.53 3.93 20.03
1.03 45.18 18.02 27.99 142.74
0.29 3.33 3.32 3.07 12.70
0.63 7.32 7.30 6.74 27.91
0.23 5.75 1.61 1.58 23.33
0.51 12.63 3.54 3.46 51.26
0.11 6.92 2.66 4.19 23.46
0.24 15.20 5.83 9.21 51.54
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
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Table 6 Target hazard quotient (THQ) and Hazard index(HI) of Cd, Zn, Cu and Ni in adults (A) and children (C) based on the consumption of fish muscle. Species
Exposure time (d)
Target hazard quotient (THQ) Cd
Longtail tuna
Kluzinger's mullet
Indian mackerel
Pickhandle barracuda
1 3 7 1 3 7 1 3 7 1 3 7
Hazard Index (HI)
Cu
Ni
Zn
A
C
A
C
A
C
A
C
0.03 0.09 0.14 0.06 0.17 0.29 0.05 0.14 0.23 0.02 0.06 0.11
0.22 0.65 1.52 0.43 1.30 3.04 0.35 1.06 2.47 0.16 0.49 1.14
0.02 0.07 0.16 0.01 0.04 0.08 0.02 0.06 0.14 0.02 0.07 0.17
0.05 0.15 0.35 0.03 0.08 0.18 0.05 0.14 0.32 0.05 0.16 0.38
0.02 0.05 0.13 0.02 0.07 0.17 0.01 0.03 0.08 0.02 0.06 0.13
0.04 0.12 0.28 0.05 0.16 0.37 0.03 0.08 0.18 0.04 0.13 0.29
0.00 0.03 0.07 0.00 0.02 0.04 0.00 0.03 0.08 0.00 0.03 0.08
0.02 0.06 0.15 0.01 0.04 0.09 0.02 0.07 0.17 0.02 0.07 0.17
suggested by JECFA, except in the case of Kluzinger's mullet for the adult age class, and Indian mackerel for the child age class. Calculated allowable fish consumption rates (CRlim kg−1 day−1) are shown Table 5. In accordance with the USEPA (2000), these risk-based consumption limits are estimated as the maximum daily consumption rates of contaminated fish and in these cases would not be expected to cause any adverse health effects for human consumers, irrespective of age. The THQ values of metals through muscle consumption for children and adults are shown in Table 6. THQ values for Zn, Cu and Ni for both age classes considered, and for Cd in adult age class were all below 1. Therefore, the daily intakes for these metals derived from a real meal at levels of assumed exposure were not likely to cause any adverse effect during a human lifetime. However, THQ values of Cd in children class in some levels of assumed exposure (7 and 3 days per week) were N1, indicating the presence of a health risk. That means that there is a potential risk of developing chronic systemic effects due to Cd intake. Therefore, THQ values for Cd indicated that the threshold to avoid the potential risk for children health was an exposure lower than 3 meals per week. HI was also employed in this study because humans are often exposed to more than one contaminant and suffer from combined or interactive effects (Li et al., 2013). HI values based on four metals (not including Pb) of child age class were higher than those of adult age class, which means that children may suffer a higher risk to their health. In conclusion, the bioaccumulation of metals in seafood is a major health concern globally. The levels of studied trace metals in the muscle of Persian fish species were generally lower than the maximum permitted concentrations recommended by food safety guidelines. With the exception of Pb, EDI values were lower than those suggested by JECFA for Cd, Cu, and Zn for both adult and children. THQ values for Cu, Ni and Zn for both adults and children, and for Cd in adults were not likely to cause any adverse effect during lifetime in population. THQ values for Cd in children at some levels of assumed exposure (7 and 3 days per week) were higher than 1, indicating the presence of a health risk. Therefore, more attention should be paid to the monitoring of Cd and Pb in fish from Persian Gulf in future which might pose potential health risks to population. Due to the increasing environmental pressure on the Persian Gulf ecosystem, a regular and on-going monitoring of trace metal levels in marine organisms is necessary to prevent any deleterious effect on the human population. References Agah, H., Leermakers, M., Elskens, M., Fatemi, S.R., Baeyens, W., 2007. Total mercury and methyl mercury concentrations in fish from the Persian Gulf and the Caspian Sea. Water Air Soil Pollut. 181 (1–4), 95–105.
A
C
0.07 0.24 0.50 0.09 0.30 0.58 0.08 0.26 0.53 0.06 0.22 0.49
0.33 0.98 2.3 0.52 1.58 3.68 0.45 1.35 3.14 0.27 0.85 1.98
Agah, H., Leermakers, M., Elskens, M., Fatemi, S.M.R., Baeyens, W., 2009. Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf. Environ. Monit. Assess. 157 (1–4), 499–514. Agah, H., Hashtroudi, M.S., Baeyens, W., 2012. Trace metals and major elements in sediments of the northern Persian gulf. J. Persian. Gulf. 3 (7), 45–58. ATSDR (Agency for Toxic Substance and Disease Rigestry), 2013. Priority List of Hazardous Substances. Atlanta, Georgia, USA. Chien, L.C., Hung, T.C., Choang, K.Y., Yeh, Ch.Y., Meng, P.J., Shieh, M.J., Han, B.C.H., 2002. Daily intake of TBT, Cu, Zn, Cd and As for fishermen in Taiwan. Sci. Total Environ. 285 (1), 177–185. Copat, Ch., Bella, F., Castaing, M., Fallico, R., Sciacca, S., Ferrante, M., 2012. Heavy metals concentrations in fish from Sicily (Mediterranean Sea) and evaluation of possible health risks to consumers. Bull. Environ. Contam. Toxicol. 88 (1), 78–83. Copat, Ch., Arena, G., Fiore, M., Ledda, C., Fallico, R., Sciacca, S., Ferrante, M., 2013. Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: consumption advisories. Food Chem. Toxicol. 53, 33–37. Domingo, J.L., Bocio, A., Falcó, G., 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 (2), 219–226. EC (European Commission), 2006. Commission Regulation (EC) No 1881/2006 of the European parliament and the council of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Communities L364 (18) (Available online at: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX: 32006R1881&from=EN). FAO (Food Administration Organization). 1983. Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fish. Circ. 764. FAO, Rome, pp. 102, (http://www.fao.org/fi/oldsite/eims_search/1_dett.asp?calling=simple_s_ result&lang=fr&pub_id=65155). Gu, Y.G., Lin, Q., Wang, X.H., Du, F.Y., Yu, Z.L., Huang, H.H., 2015. Heavy metal concentrations in wild fishes captured from the South China Sea and associated health risks. Mar. Pollut. Bull. 96 (1–2), 508–512. Hajeb, P., Jinap, S., Ismail, A., Fatimah, A.B., Jamilah, B., Rahim, M. Abdul, 2009. Assessment of mercury level in commonly consumed marine fishes in Malaysia. Food Control 20 (1), 79–84. Hamza, W., Munawar, M., 2009. Protecting and managing the Arabian Gulf: past, present and future. Aquat. Ecosyst. Health Manag. 12 (4), 429–439. Helrich, K.C., 1990. Official Methods of Analysis of the AOAC. Volume 2. Association of Official Analytical Chemists Inc. JECFA (Joint FAO/WHO Expert Committee on Food Additives), 2009. Evaluations of the Joint FAO/WHO Expert Committee on Food Additives. (Available at:http://apps. Who.int/ipsc//database/evaluations/search.aspx). Li, J., Huang, Zh.Y., Hu, Y., Yang, H., 2013. Potential risk assessment of heavy metals by consuming shellfish collected from Xiamen, China. Environ. Sci. Pollut. Res. 20 (5), 2937–2947. Mansilla-Rivera, I., Rodríguez-Sierra, C.J., 2011. Metal levels in fish captured in Puerto Rico and estimation of risk from fish consumption. Arch. Environ. Contam. Toxicol. 60 (1), 132–144. Naji, A., Ismail, A., 2012. Sediment quality assessment of Klang Estuary, Malaysia. Aquat. Ecosyst. Health Manag. 15 (3), 287–293. Naji, A., Ismail, A., Ismail, A.R., 2010. Chemical speciation and contamination assessment of Zn and Cd by sequential extraction in surface sediment of Klang River, Malaysia. Microchem. J. 95 (2), 285–292. Naji, A., Ismail, A., Kamrani, E., Sohrabi, T., 2014. Correlation of MT levels in livers and gills with heavy metals in wild tilapia (Oreochromis mossambicus) from the Klang River, Malaysia. Bull. Environ. Contam. Toxicol. 92 (6), 674–679. Naser, H.A., 2013. Assessment and management of heavy metal pollution in the marine environment of the Persian Gulf: a review. Mar. Pollut. Bull. 72 (1), 6–13. Palmieri, R.M., La Pera, L., Di Bella, G., Dugo, G., 2005. Simultaneous determination of Cd (II), Cu (II), Pb (II) and Zn (II) by derivative stripping chronopotentiometry in Pittosporum tobira leaves: a measurement of local atmospheric pollution in Messina (Sicily, Italy). Chemosphere 59 (8), 1161–1168.
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002
A. Naji et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Saei-Dehkordi, S. Siavash, Fallah, Aziz A., Nematollahi, Amin, 2010. Arsenic and mercury in commercially valuable fish species from the Persian Gulf: influence of season and habitat. Food Chem. Toxicol. 48 (10), 2945–2950. Sheppard, Ch., Price, A., Roberts, C., 1992. Marine Ecology of the Arabian Region. Academic Press. Sheppard, Ch., Al-Husiani, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, Francesca, D., Eric, D., Nicholas K., Durvasula, S.R.V., 2010. The Gulf: a young sea in decline. Mar. Pollut. Bull. 60 (1), 13–38. Taweel, A., Shuhaimi-Othman, M., Ahmad, A.K., 2013. Assessment of heavy metals in tilapia fish (Oreochromis niloticus) from the Langat River and Engineering Lake in Bangi, Malaysia, and evaluation of the health risk from tilapia consumption. Ecotoxicol. Environ. Saf. 93, 45–51. USEPA (US Environmental Protection Agency), 1989. Risk Assessment Guidance for Superfund. Vol. I. Human Health Evaluation Manual (Part A), Interim Final. EPA 540/1–89/002United States Environmental Protection Agency, Washington, DC. USEPA (US Environmental Protection Agency), 2000. Guidance for Assessing Chemical Contamination Data for Use in Fish Advisories. Vol. II. Risk Assessment and Fish Consumption Limits EPA/823-B94-004United States Environmental Protection Agency, Washington, DC. USEPA (US Environmental Protection Agency), 2004. Integrated risk information system (IRIS) on lead and compounds (inorganic). National Center for Environmental
5
Assessment. Office of Research and Development, Washington, DC (Last revised 2004. Available online at: http://www.epa.gov/iris/subst/0277.htm#bib). USEPA (US Environmental Protection Agency), 2015. Human health risk assessment. Regional Screening Level (RSL)—Summary Table (Available online at: http://www.epa. gov/reg3hwmd/risk/human/rbconcentration_table/Generic_Tables/docs/master_sl_ table_run_JAN2015.pdf). USFDA (US Food and Drug Administration), 2007. National shellfish sanitation program. Guide for the control of molluscan shellfish 2007. Guidance Documents Chapter II. Growing Areas: 04. Action Levels, Tolerances and Guidance Levels for Poisonous or Deleterious Substances in Seafood (Available online at: http://www.issc.org/client_ resources/2007.pdf). WHO (World Health Organization), 1989. Heavy metals—environmental aspects. Environment Health Criteria No. 85, Geneva, 1989. WHO (World Health Organization), 1996. Health criteria other supporting information. Guidelines for Drinking Water Quality, second ed. WHO, Geneva, pp. 31–388. Yap, C.K., Jusoh, A., Leong, W.J., Karami, A., Ong, G.H., 2015. Potential human health risk assessment of heavy metals via the consumption of tilapia Oreochromis mossambicus collected from contaminated and uncontaminated ponds. Environ. Monit. Assess. 187 (9), 1–16.
Please cite this article as: Naji, A., et al., Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2016.05.002