Heavy Metals in Cereals and Pulses - ACS Publications - American

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Heavy Metals in Cereals and Pulses: Health Implications in Bangladesh Md. Saiful Islam,*,†,‡ Md. Kawser Ahmed,§ and Md. Habibullah-Al-Mamun‡,§ †

Department of Soil Science, Patuakhali Science and Technology University, Dumki, Patuakhali, 8602, Bangladesh Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Kanagawa-240-8501, Japan § Department of Fisheries, University of Dhaka, Dhaka-1000, Bangladesh ‡

ABSTRACT: This research was conducted to evaluate the concentration of seven common heavy metals (Cr, Ni, Cu, Zn, As, Cd, and Pb) in cereals and pulses and associated health implications in Bangladesh. USEPA deterministic approaches were followed to assess the carcinogenic risk (CR) and noncarcinogenic risk which was measured by target hazard quotient (THQ) and hazard index (HI). Total THQ values for As and Pb were higher than 1, suggesting that people would experience significant health risks if they ingest As and Pb from cereals and pulses. However, the estimated HI value of 1.7 × 101 (>1) elucidates a potential noncarcinogenic risk to the consumers. Also, the estimation showed that the carcinogenic risk of As (5.8 × 10−3) and Pb (4.9 × 10−5) exceeded the USEPA accepted risk level of 1 × 10−6. Thus, the carcinogenic risk of As and Pb with nutritional deficiency of essential elements for Bangladeshi people is a matter of concern. KEYWORDS: heavy metals, cereals, pulses, health risks, Bangladesh

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INTRODUCTION Heavy metals are ubiquitous in the environment either naturally or anthropogenically, and their occurrence in the environment occurs mainly through waste disposal, smelter stacks, atmospheric deposition, fertilizer and pesticide use, and the application of sewage sludge in cultivable lands.1,2 Heavy metals such as Cr, Ni, Cd, Pb, and As have been considered as the most toxic elements in the environment and included in the list of priority pollutants declared by US Environment Protection Agency (USEPA).3,4 Therefore, it is undoubtedly important to know the metal concentrations in soil and foods that are grown for human consumption. Soil behaves as a sink for heavy metals through the aerial deposition of particles emitted by urban and industrial activities as well as agricultural practices.5,6 High metal levels in soil can lead to phytotoxicity and finally enter into the human diet through crop uptake or soil ingestion.7 Concentration of heavy metals in different foods depends on the soil composition, water, nutrient balance, and metal permissibility, selectivity, and absorption ability of the species.8 In addition, direct foliar uptake of heavy metals from the atmosphere can also occur during plant growth. Cultivation of cereals and pulses on the contaminated soil can potentially lead to the transfer of metals into the edible parts, which may result in human health risks.9 Although the relative contribution has not yet been clearly established, consumption of food crops is considered as one of the important sources of human exposure to heavy metals in the contaminated areas.10 Sharma et al.11 have demonstrated that, except for occupational exposure, dietary intake through contaminated food has become an important route for human intake of metals. In this context, Food and Agriculture Organization (FAO), World Health Organization (WHO), European Commission (EC), and other regulatory bodies in the world strictly regulate the allowable concentrations or maximum permitted concentrations of toxic metals in foodstuffs.12 The health risk associated © XXXX American Chemical Society

with the intake of toxic metals can be evaluated by carcinogenic and noncarcinogenic means. Cereals have been the staple human diet since prehistoric times because of their wide cultivation, good keeping qualities, blend flavor, and great variety.13 Heavy metal intake through food consumption is of interest because of their essential or toxic nature. For example, Fe, Zn, Cu, and Cr are essential, while Pb, As, Cd, and Ni are toxic at certain levels.14 The presence of heavy metals in cereals, especially arsenic in rice, is a global issue impacting the lives of billions of rice consumers worldwide, especially when considering that rice is often exported from one country to another.15 Moreover, rice is a staple food for daily consumption in many countries, especially for South and South East Asia, and as a result, consumption of metal contaminated rice may contribute a major part to the daily dietary intake. Therefore, there is an increasing requirement for the investigation of heavy metals in rice and other frequently consumed cereals and pulses.16 It has been demonstrated that rice can become enriched with lead,16 in excess of the common safety threshold of 0.2 mg/kg for rice grain.17 In recent decades, the determination of trace and toxic metals in foodstuff attracted the attention of modern environmental scientists. In order to delineate the scope of the environmental contamination by heavy metals, extent of human exposure, and potential health consequences, an exposure assessment was conducted. Little attention is given to the concentrations of heavy metals in grain crops and their possible deleterious effects on human health in Bangladesh. The present study was aimed to assess the safety of human diet from grain crops that is consumed by a significant proportion of Received: May 27, 2014 Revised: October 6, 2014 Accepted: October 12, 2014

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dx.doi.org/10.1021/jf502486q | J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Journal of Agricultural and Food Chemistry

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Figure 1. Map of the study area of agricultural fields in Bogra district situated at the northern part of Bangladesh. recorded using a Horiba U-23 instrument with the calibration of pH 4.0, pH 7.0, and pH 9.0 standards. For electrical conductivity (EC) determination, 5.0 g of sediment was taken in 50 mL polypropylene tubes. Then, 30 mL of distilled water was added to the tube. The lid was closed properly and was shaken for 5 min. After that, EC was measured using an EC meter (Horiba D-52).20 Percent organic carbon of soil was measured using an elemental analyzer (model type: Vario EL III, Elenemtar, Germany). The catalytic combustion was carried out at a permanent temperature of up to 1200 °C. The element concentration from the detector signal and the sample weight based on stored calibration curves were measured. Particle size distribution was determined using the hydrometer method.21 The soils were classified using the United States Department of Agriculture (USDA) classification system (gravel [>2 mm], sand [2−0.05 mm], silt [0.05−0.002 mm], and clay [ lentil > wheat > rice. The observed variation in metal concentrations for analyzed foodstuffs might be due to variable capabilities of absorption and accumulation of metals by the cereal crops.31 An elevated level of Cr was found in black gram (2.4 mg/kg) followed by lentil, maize, rice, and wheat (Table 3). The mean Cr concentration in rice was 1.8 mg/kg (range, 0.26−4.2 mg/ kg, n = 32). A previous study by Fu et al.16 reported mean Cr concentration in Chinese rice of 0.20 mg/kg (range, 0.062− 0.42 mg/kg, n = 4), which is lower than in the present study. In the present study, the highest mean concentration of Ni was found in black gram, 1.4 mg/kg (range, 0.047−4.0 mg/kg). In rice, Ni concentration was observed (mean, 1.0; range, 0.03− 2.6 mg/kg). However, Ni concentration in all rice samples of the present study was considerably lower than those of Chinese rice (mean, 0.48 mg/kg; range, 0.20−0.82 mg/kg, n = 4)16 and Indian state of West Bengal (mean, 0.87 mg/kg; range, 0.0002−1.8 mg/kg).32 Among the studied metals, significant difference of Zn concentration was observed in the studied foods (Table 3), therefore, Zn measured in the current study is more likely to be having a micronutrient effect rather than

75 (24−205) 75 (50−116) 115 (103−123) 122 (92−142) 689 (63−7120) 18 (4.5−93) 112 (33−733) 140 720 200 200

Zn Cu Ni

45 (15−95) 64 (37−93) 58 (36−74) 8.83 (7.04−10.3) 171 (69−465) 14 (5.1−31) 45 (16−217) 35 210 50 60

Cr

41 (6.6−87)b 29 (18−46) 54 (34−68) 12.3 (9.66−19) 164 (66−279) 18 (10−60) 29 (17−81) 100 380 64 50

district (country)

Bogra (Bangladesh) Noakhali (Bangladesh) Dhaka (Bangladesh) Guandong (China) Maharashtra (India) Murcia (Spain) Kayseri (Turkey) Dutch soil quality standard (Target Value) Dutch soil quality standard (Intervention Value) Canadian Environmental Quality Guidelines Department of Environmental Protection, Australia

Table 2. Comparison of Metal Concentration in Soil of Present Study with Other Studies and Guideline Valuesa

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42 (6.4−107) 22 (13−63) 39 (31−45) 324 (210−450) 155 (52−373) 11 (3.8−65) 37 (12−144) 36 190 63 60

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Table 3. Heavy Metals (mg/kg) in Cereals and Pulses Collected from Agricultural Fields of Bogra District, Bangladesh name common rice (n = 32)a

wheat (n = 32)

maize (n = 32)

lentil (n = 24)

black gram (n = 24)

scientific Oryza sativa range mean ± SDb Triticum aestivum range mean ± SD Zea mays range mean ± SD Lens culinaris range mean ± SD Vigna mungo range mean ± SD

a

Cr

Ni

Cu

Zn

As

Cd

Pb

0.26−4.2 1.8 ± 1.4 ac

0.028−2.6 1.0 ± 0.73 a

0.50−3.3 1.7 ± 0.68 a

0.55−3.5 2.1 ± 0.64 b

0.06−1.6 0.47 ± 0.39 a

0.001−0.073 0.045 ± 0.017 a

0.07−1.3 0.71 ± 0.29 a

0.24−3.4 1.3 ± 0.92 a

0.095−3.6 1.3 ± 1.1 a

0.52−4.3 1.9 ± 0.91 a

1.1−6.0 2.9 ± 1.2 a

0.08−1.5 0.57 ± 0.39 a

0.0010−0.66 0.16 ± 0.19 b

0.028−1.1 0.26 ± 0.30 b

0.39−4.0 1.9 ± 0.99 a

0.24−2.8 1.4 ± 0.66 a

0.87−4.5 2.3 ± 0.94 a

1.5−7.3 3.6 ± 1.6 c

0.08−1.7 0.64 ± 0.44 a

0.018−0.53 0.10 ± 0.11 ab

0.044−1.3 0.31 ± 0.31 bc

0.39−6.5 2.3 ± 1.8 a

0.036−4.0 1.1 ± 1.0 a

0.61−4.5 2.3 ± 1.1 a

1.5−3.9 2.3 ± 0.71 ab

0.10−1.8 0.66 ± 0.45 a

0.018−0.13 0.044 ± 0.037 a

0.14−1.6 0.60 ± 0.38 a

0.29−6.5 2.4 ± 2.0 a

0.047−4.0 1.4 ± 1.0 a

0.43−4.1 2.1 ± 1.2 a

0.61−3.9 2.5 ± 0.81 ab

0.06−1.6 0.62 ± 0.44 a

0.0012−0.13 0.046 ± 0.041 a

0.08−1.6 0.55 ± 0.37 ac

n = number of samples analyzed for this study. bSD = standard deviation. cDifferent letter (a, b, c) indicates statistical significance (p < 0.05).

posing a significant risk of toxicity. However, the highest Zn concentration was found in maize (mean, 3.6 mg/kg; range, 1.5−7.3 mg/kg, n = 32) (Table 3). The mean concentration of As in rice was 0.47 mg/kg, which was higher than in the previous study conducted by Williams et al.,33 where As concentration in Bangladeshi rice was 0.13 mg/kg. The elevated As concentration in rice was attributed to the higher accumulation of As from soil to grain in the anaerobic paddy soil systems for rice production and uncontrolled application of As enriched fertilizers and pesticides.34 Cadmium is a metallic element that occurs naturally at low levels in the environment. Food, rather than air or water, represents the major source of cadmium exposure.35 The highest Cd concentration was observed in wheat (mean, 0.16; range, 0.001−0.66 mg/kg). Transfer Factor of Metals. The accumulation of metals in the edible parts of cereals and pulses could have a direct impact on human health through the food chain. Metals with high TF are more easily transferred from soil to the edible parts of

Figure 2. Transfer factor of metals from soil to cereals and pulses collected from agricultural fields of Bogra district, Bangladesh (bars represent standard error at 95% CI).

Table 4. Food Intake and Intake of Heavy Metals (mg/day) through the Diet of Cereals and Pulses of the Present Study (Mean ± SD) estimated daily intake (EDI) (mg/day)

foods rice wheat maize lentil black gram total intake from foods maximum tolerable daily intake (MTDI)

consumption rate (g/day/ person)18

Cr

Ni

Cu

Zn

As

44538 26.09 26.09 14.3 14.3 0.95

0.79 ± 0.62 0.035 ± 0.024 0.050 ± 0.026 0.033 ± 0.026 0.034 ± 0.028 0.57

0.46 ± 0.32 0.033 ± 0.028 0.036 ± 0.017 0.016 ± 0.014 0.020 ± 0.015 0.95

0.78 ± 0.30 0.050 ± 0.024 0.061 ± 0.025 0.033 ± 0.016 0.030 ± 0.016 1.2

0.95 ± 0.28 0.077 ± 0.030 0.095 ± 0.042 0.033 ± 0.010 0.035 ± 0.012 0.26

0.21 ± 0.17 0.015 ± 0.010 0.017 ± 0.012 0.009 ± 0.006 0.009 ± 0.006 0.028

0.020 0.004 0.003 0.001 0.001 0.35

0.246

0.347

3048

6047

0.1323

0.02149

0.2150

E

Cd ± ± ± ± ±

Pb 0.01 0.005 0.003 0.001 0.001

0.32 ± 0.13 0.007 ± 0.008 0.008 ± 0.008 0.009 ± 0.005 0.008 ± 0.005


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plants than the ones with low TF. As seen from Figure 2, large variations in TFs were observed among different samples and metals. The average TF of metals in all crops was in the following order: As > Cr > Cu > Zn > Ni > Cd > Pb. In rice, average values of TF were 0.084, 0.044, 0.086, 0.051, 0.11, 0.024, and 0.034, in wheat, average values of TF were 0.078, 0.060, 0.093, 0.070, 0.12, 0.12, and 0.014, and in maize, average values of TF were 0.11, 0.064, 0.11, 0.086, 0.14, 0.054, and 0.014 for Cr, Ni, Cu, Zn, As, Cd, and Pb, respectively. The TF of Cd in wheat was higher than those of any other metals examined. It was noticeable that Cd was considered as a very dangerous substance for human health by the long-term effects.36 Therefore, the risks of Cd for health should be highlighted by its high toxicity and mobility from soil to wheat grain. In lentil, average values of TF were 0.13, 0.066, 0.12, 0.053, 0.12, 0.023, and 0.024, and in black gram, average values of TF were 0.14, 0.059, 0.11, 0.055, 0.11, 0.021, and 0.022 for Cr, Ni, Cu, Zn, As, Cd, and Pb, respectively. The major pathway for Pb to enter the above-ground tissues of plants is through atmospheric deposition.37 Therefore, the factual TF of Pb should be lower than the calculated value. In this study, the soil-to-plant TF for various metals and for most common cereals and pulses consumed by local residents were calculated (Figure 2), and our data showed that TF values slightly varied among metals within the same crop. The difference in TFs between metals and species might be related to soil properties, nutrient management, crop genetic features, and physicochemical properties of pollutants.22 For instance, soils from S2, S3, S15, and S16 were generally higher in organic matter and clay content might be responsible for higher metal transfer from soil to plants. Estimated Daily Intakes (EDIs). The EDIs of seven metals (Cr, Ni, Cu, Zn, As, Cd, and Pb) were evaluated according to the average concentration of each metal in each food crop from each site and the respective consumption rates. The EDI and maximum tolerable daily intake (MTDI) of studied metals from consumption of grain crops are shown in Table 4. Total daily intake of Cr, Ni, Cu, Zn, As, Cd, and Pb were 0.95, 0.57, 0.95, 1.2, 0.26, 0.28, and 0.35 mg/day, respectively (Table 4). The maximum contribution of daily intake of studied metals came from rice; this is due to the highest consumption rate of rice (445 g/person/day).38 The total EDIs of Cr, Ni, As, Cd, and Pb from all examined food items were higher than the MTDI values recommended by the international regulatory bodies (Table 4), indicating that these foods might pose health risks to consumers. Noncarcinogenic Risk. Risk assessment is the process that evaluates the potential health effects from doses to humans of one contaminant received through one or more exposure pathways. The health risks from consumption of cereals and pulses by adult populations were assessed based on the target hazard quotients (THQs). The THQ is a ratio of determined dose of a pollutant to a reference dose level. If the ratio is greater than 1, the exposed population is likely to experience obvious adverse effects.25 The methodology for estimation of THQs does not provide a quantitative estimate on the probability of an exposed population experiencing a reverse health effect, but it offers an indication of the risk level due to contaminant exposure. The estimated THQs of studied metals are shown in Table 5, indicating that THQ values of As and Pb were above 1 through consumption of rice, suggesting that people would experience significant health risks if they only ingest these two metals from rice. The consumption of rice per

a The total metals THQs (TTHQ, sum of individual metal THQs). bCarcinogenic risk for As was calculated based on 90% inorganic As in cereals and pulses. cHI: the sum of THQ values of heavy metals due to consuming the diet.

10−5 10−6 10−6 10−6 10−6 10−5 × × × × × × 0.39 ± 0.27 0.027 ± 0.023 0.030 ± 0.014 0.013 ± 0.012 0.017 ± 0.012 0.47 0.009 ± 0.007 0.0004 ± 0.0003 0.0006 ± 0.0003 0.0004 ± 0.0003 0.0004 ± 0.0003 0.011 rice wheat maize lentil black gram total

0.32 ± 0.13 0.021 ± 0.010 0.025 ± 0.010 0.014 ± 0.007 0.013 ± 0.007 0.40

0.05 ± 0.02 0.004 ± 0.002 0.005 ± 0.002 0.002 ± 0.001 0.002 ± 0.001 0.066

12 ± 10 0.83 ± 0.56 0.93 ± 0.64 0.52 ± 0.36 0.49 ± 0.35 14

0.11 ± 0.04 0.023 ± 0.028 0.014 ± 0.016 0.003 ± 0.003 0.004 ± 0.003 0.16

1.5 ± 0.61 0.033 ± 0.037 0.038 ± 0.038 0.041 ± 0.026 0.037 ± 0.026 1.7

14 0.94 1.0 0.59 0.56 17 (HI)c

4.7 3.4 3.8 2.1 2.0 5.8

× × × × × ×

10 10−4 10−4 10−4 10−4 10−3

4.5 1.1 1.1 1.2 1.1 4.9

Pb

−3

Asb

carcinogenic risk (CR)

TTHQa Pb Cd As target hazard quotients (THQs)

Zn Cu Ni Cr foods

Table 5. Target Hazard Quotients (Noncarcinogenic) and Carcinogenic Risk (CR) of Heavy Metals (Mean ± SD) Due to Food Consumption in Bogra District Urban Area, Bangladesh


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capita in Bangladesh is 445 g/day.38 Therefore, consuming rice containing high As and Pb might put pregnant women at a higher risk. Among all the metals studied, the TTHQ through consuming rice was 14, suggesting that Bangladeshi people might have significant noncarcinogenic health risk through only consuming rice. However, the total target hazard quotient (TTHQ) values through consuming other cereals and pulses were equal to or less than 1, indicating that there were no potential significant health risks in terms of these food items. The hazard index (HI) value expresses the combined noncarcinogenic effects of multiple elements. In Table 5, the HI value through selected food consumption was 17, indicating that consumers of the studied foodstuffs may experience adverse health effects. Carcinogenic Risk of As and Pb. Concerning the carcinogenic risk, the CR values of As were 4.7 × 10−3, 3.4 × 10−4, 3.8 × 10−4, 2.1 × 10−4, and 2.0 × 10−4 (assuming 90% of inorganic As39) and of Pb were 4.5 × 10−5, 1.1 × 10−6, 1.1 × 10−6, 1.2 × 10−6, and 1.1 × 10−6 for rice, wheat, maize, lentil, and black gram, respectively, which were clearly higher than the USEPA threshold level (10−6) or residual level (10−4) for causing cancer,24 indicating carcinogenic risks for all adults of the study area. The concentrations of heavy metals widely varied among the samples. Among cereals and pulses, rice contributes the highest intake of the studied metals. Considering the transfer factor of metals from soil to cereals and pulses, As showed higher TF values than the other metals. Total intake of Cr, Ni, As, Cd, and Pb for the exposed people was slightly higher than that recommended as the MTDI (for a person weighing 60 kg), indicating that people would experience significant risks. From the human health point of view, the THQ values for As and Pb were higher than 1, suggesting that people would experience significant health risks if they ingest these two vital metals through consuming the studied foodstuffs. However, consumption of all foodstuffs could lead to a potential health risk to the consumers since HI value was higher than 1. Concerning the carcinogenic risk, the total CR values of As and Pb were clearly higher than the USEPA threshold level (1 × 10−6). However, health risks associated with food consumption are not negligible and the sources of metal pollution should be controlled to achieve safe foodstuffs. The present study is of great interest in terms of toxicology and food safety for the Bogra district urban population, given the absence of previous studies to determine dietary intake of heavy metals, not only for the district urban population but also at the national level.

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Chancellor, PSTU), for his valuable suggestions and cooperation to carry out this research.

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AUTHOR INFORMATION

Corresponding Author

*Department of Soil Science, Patuakhali Science and Technology University, Dumki, Patuakhali, 8602, Bangladesh. Phone: +88-01717372057. Fax: +88-04427-56009. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank the authority of Patuakhali Science and Technology University, Bangladesh, and Yokohama National University, Japan, for providing laboratory facilities. The authors are also delighted to express their gratefulness and sincerest thanks to Professor Dr. Md. Shams-Ud-Din (Vice G



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Heavy Metals in Cereals and Pulses - ACS Publications - American

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