- Email: [email protected]
Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan
Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Contents lists available at ScienceDirect
Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv
Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan Sardar Khan a,n, Shafiqur Rehman a, Anwar Zeb Khan a, M. Amjad Khan a, M. Tahir Shah b a b
Department of Environmental Sciences, University of Peshawar, Peshawar 25120, Pakistan National Center of Excellence in Geology, University of Peshawar, Peshawar 25120, Pakistan
a r t i c l e in f o
a b s t r a c t
Article history: Received 3 September 2009 Received in revised form 2 August 2010 Accepted 13 August 2010
This study was conducted to investigate the concentrations of heavy metals in soil and vegetables, and human health risks through ingestion of contaminated vegetables. Soil and vegetable samples were collected from different locations in Gilgit, northern Pakistan, and analyzed for Cd, Cu, Ni, Pb and Zn. Plant transfer factors (PTF), daily intake of metals (DIM) and health risk index (HRI) were also calculated. The concentrations of Cd, Cu and Zn exceeded their respective permissible limits in soil samples. The highest concentrations of Cu, Ni, Pb and Zn were observed in the edible parts of Malva neglecta, Brassica oleracea, Mintha sylvestris and Brassica campestris, respectively. PTF values were lower for all the selected heavy metals, except for Cd. Furthermore, the HRI values were within the safe limit ( o 1) except for Pb; therefore, the health risks of metals through ingestion of vegetables were of great concern in the study area. & 2010 Elsevier Inc. All rights reserved.
Keywords: Daily intake Heavy metals Health risk Natural sources Soil and vegetable contamination Transfer factor
1. Introduction Soil pollution is an undesirable change in the physical, chemical and/or biological characteristics, which reduces the amount of land for cultivation and habitation. Human health is closely related to the quality of soil and especially to its degree of pollution (Romic and Romic, 2003; Velea et al., 2009). Soil acts as a sink and also as a source of pollution with the capacity to transfer pollutants to groundwater and food chain, and then to the human and/or animals. Soil provides the critical interface environment where the interaction of rock, air and water takes place and can be a source of pollution to surface and groundwater, living organisms, sediments and oceans (Facchinelli et al., 2001). Heavy metal enrichment/contamination of the soil has attracted a great deal of attention worldwide due to their non-biodegradable nature and long biological half-lives for elimination from the body (Raghunath et al., 1999; Li et al., 2004). Generally, both natural and anthropogenic sources are responsible for soil enrichment/contamination with heavy metals and its contamination level varies from place to place (Khan et al., 2008a; Shah et al., 2010; Kashem et al., 2006). Previous research works have shown the natural sources of heavy metal enrichment of soil ecosystem and the plants grown on it (Del Rı´o et al., 2002; + osi + et al., 2009). The basic chemical properties of soil depend Szoll
n
Corresponding author. Fax: + 92 91 9218401. E-mail address: [email protected] (S. Khan).
0147-6513/$ - see front matter & 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ecoenv.2010.08.016
on the types of weathered rocks of the concerned areas. Particularly, the mafic and ultramafic rocks are generally enriched in heavy metals such as Fe, Cr, Ni and Cd, leading to elevated level in both soil and standing plants (Kafayatullah et al., 2001; Shah et al., 2010). Heavy metals can be harmful due to their potential to accumulate in different body parts of the human being. Even in low concentrations, they have adverse health effects (Ikeda et al., 2000), because these are non-biodegradible and persistent in nature (Duruibe et al., 2007). Many food plants accumulate heavy metals and result in the rise in the metal contents of farm’s production (Khan et al., 2008a, 2008b). Food chain translocation of heavy metals is one of the consequences of soil contaminated with heavy metals, and excessive intake of metals through consumption of contaminated vegetables and other plants is associated with human health risks (Khan et al., 2008b; Nasreddine and Parent-Massin, 2002; Turkdogan et al., 2003). Furthermore, the ingestion of heavy metals (Cd, Cu, Ni, Pb, Zn, etc.) can seriously cause depletion of some essential nutrients in the body, which in turn causes a decrease in immunological defenses, intrauterine growth retardation (caused by Al, Cd, Mn and Pb), psychosocial dysfunctions, disabilities associated with malnutrition and a high prevalence of upper gastrointestinal cancer (Iyengar and Nair, 2000; Turkdogan et al., 2003). Heavy metals such as Cd and Pb have shown carcinogenic effects (Trichopoulos, 1997). Similarly, high concentrations of Cd, Cu and Pb in vegetables and fruits were related to high prevalence of upper gastrointestinal cancer (Turkdogan et al., 2003).
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Furthermore, Ni at high concentration can cause cancer, skin rashes, fatigue, headache, heart problems, dizziness and respiratory illness. It is a fact that different serious systemic health diseases can develop as a result of excessive dietary accumulation of these heavy metals in human beings (Oliver, 1997). According to Satarug et al. (2000) Cd causes bone fracture, cancer, kidney dysfunction and hypertension. High concentration of Pb has chronic adverse health effects including respiratory and dermatogenic problems caused by ingestion and dermal contacts of contaminated soil and/or dusts (Oliver, 1997; Wang et al., 2006). This requires knowledge of different heavy metals accumulation in different vegetable species and cultivars, as well as soil factors that control bioavailability of heavy metals to plants. In order to produce vegetables with low heavy metals and adopt the best suitable forming/agriculture practices, a better knowledge of heavy metals accumulation in different vegetables species will be required. This study was aimed to investigate soil and vegetable enrichment with heavy metals, originating from natural sources such as weathering of rocks and contribution from underground geology and soil-to-plant transfer factor and human health risks due to ingestion of heavy metals enriched vegetables.
2. Material and methods 2.1. Area description
1821
The meta-sedimentary rocks of the Gilgit Complex are greenshist facies slates, phyllites and psammite, having local mineralization of base metal sulfides. The soil is sandy and neutral with a slightly acidic nature in some regions (Naltar). Land use in the region includes agriculture and orchids, and most of cultivation is generally focused on green leafy vegetable and other edible crops. The cultivated areas have been developed on alluvial fans and to a lesser extent from the reclamation of old rivers terraces. Soil is generally low in clay contents, high in silt and sand fraction and low in organic matter (usually less than 1%). The soil is freely drained with only moderate water retention capacity and is generally shallow. 2.2. Soil sampling and preparation In the study area, five sites were selected for soil sampling and eleven samples were collected from each sampling site (total of 55 samples) at a depth of 0–25 cm with stainless steel auger. Each sample was collected in the form of sub-samples at a distance of about 20 m each from the first sub-sample in different directions, at each sampling site. These sub-samples were thoroughly mixed to a composite sample (Wu et al., 2010). The samples were brought to laboratory in polyethylene bags and air-dried covered with cloth to prevent contamination. After drying, the soil samples were mechanically ground and passed through a sieve of 2 mm and properly stored for analysis. 2.3. Vegetable sampling and preparation The vegetable samples (Table 1) were collected from the same sites from where the soil samples were collected and the total number of vegetable samples was 60. The vegetables were taken out along with their roots and cut into roots and shoots. The root and shoot tissues were washed with double deionised water to remove the soil particles and then placed in separate paper bags properly marked.
Table 1 English, local and botanical names of the vegetables collected from study area.
The study area is located within the administrative capital (Gilgit) Baltistan, northern Pakistan (Fig. 1). The Gilgit region covers an area of about 16 800 km2 with latitude from 351 31! to 361 09! N and longitude from 731 24! to 741 54! E. The climate of the study area is moderate with average maximum temperature 35.9 and minimum 16 1C. The monsoon winds are blocked by the high mountains of Nanga Parbat and clouds cannot reach Gilgit, which make it dry and rugged. The annual rainfall in the region is 136.2 with maximum 28.3 mm in April and minimum 2.1 mm in November. The total agricultural land consists of 36 769 ha, usually cultivated with cereals, vegetables, fruits and fodder (IUCN, 2003). The Gilgit area is generally composed of fluvial plain deposits. It is mostly surrounded by volcanic rocks and the rocks of the Kohistan batholith in the north, northeast and northwest while its southern, southeastern and southwestern parts are covered by the meta-sedimentary rocks of the Gilgit Complex. The volcanic rocks are mainly basaltic andesites, rhyolites and pyroclastic flows. The Kohistan batholith is composed of a variety of diorites, granodiorites and granites.
English name
Local name
Botanical name
Spinach Lettuce Cauliflower Trifolium Mustard Zebra mallow Common chicory Mint Slender amaranth Common purslane Common mallow (button weed)
Palak Salad Kamshah Shaftal Isgar Swanchal Ishkanachi Philil Ganhari Pichili Shani
Spinecia oleracea Lectuca sativa Brassica oleracea Trifolium repenus Brassica campestris Malva sylvestris Cichorium intybus Mentha sylvestris Amaranthus viridis Portulaca oleracea Malva neglecta
Fig. 1. Location map of the study area (Gilgit) Biltastan, northern Pakistan.
1822
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
The vegetable samples were kept in oven at 70 1C till complete dryness. Dried vegetable samples, both roots and shoots, were powdered using clean electronic grinder and then stored in paper bags at room temperature for further analysis. 2.4. Analytical procedures Physical properties of soil were measured according to standard procedures as shown in Table 2. The soil fraction of o 2 mm was used to determine pH (1:3.5 soil water extract) using a pH meter. The soil organic matter was determined using the Walkley–Black procedure (Bai et al., 2010), while the soil moisture content was determined using the Australian standard method (SAA, 1977). Particle size analyses were performed on Fritsch Analysette 3 PRO sieve machine.
represent the heavy metal concentrations in plants (mg kg 1), conversion factor (fresh vegetable weight into dry vegetable weight), daily intake of vegetables and average body weight, respectively. The average daily vegetable intake for adults and children was considered to be 0.345 and 0.232 kg person 1 day 1, respectively, while the average adult and child body weights were considered as 73 (FAO, 2000) and 32.7 kg, respectively (Ge, 1992; Wang et al., 2005). 2.10. Health risk index The health risk index (HRI) for the inhabitants through the consumption of contaminated vegetables was assessed based on the food chain and the reference oral dose (RfD) for each metal such as HRI ¼DIM/RfD (US-EPA, 2002). HRI o 1 indicates the exposed population is assumed to be safe.
2.5. Soil digestion 2.11. Statistical analysis Soil samples were digested according to the method adopted by FAO/SIDA (1983). 1 g air-dried and powdered soil sample was taken into a pyrex beaker and 15 mL of aqua regia was added. It was kept overnight and then heated on the hot plate until no brown fumes were produced. Then concentrated HClO4 (5 mL) was added and heated again on low heat until the solution was evaporated near to dryness. The extracts were filtered and the final volume of 50 mL was made with double de-ionized water.
Data were statistically analyzed using SPSS (11.5) Statistical software. The measurements were expressed in term of means with standard deviation; also the figure is represented with the mean values. Microsoft excel software (Microsoft 2003) was used to evaluate the results graphically. ANOVA and cluster analysis (CA) statistical techniques were used determine significant differences.
2.6. Vegetable digestion
3. Results
Powdered vegetable sample (2 g) was taken into a pyrex beaker, 10 mL of concentrated HNO3 was added to it and kept overnight without heating. It was then heated on a hot plate, and after evaporation near to dryness, the sample was cooled and 5 mL HClO4 was added and heated again. After digestion was complete, the sample was filtered into a clean volumetric flask and diluted to 50 mL with double de-ionized water.
3.1. Heavy metals in soil
2.7. Heavy metal analysis In the acid extracts, the concentrations of heavy metals including Cd, Cu, Ni, Pb and Zn were determined using atomic absorption spectrophotometer (AAS 700) in the Geochemistry laboratory of National Center of Excellence in Geology, University of Peshawar. The analyses were performed in triplicates under standard optionizing conditions. The blank reagent and standard reference soil (NIST, 2709 San Joaquin) and plant materials (NIST, 1547 Peach leave) of National Institute and Technology were included in each sample batch to verify the accuracy and precision of the digestion procedure and for subsequent analyses. The analyses were within the confidence limit of 95%.
Mean values of the physical characteristics of soil samples are shown in Table 2. A wide range of heavy metal concentrations was observed across the study area (Table 3). The results indicated that the concentrations of Cd in soil samples ranged from 0.30 to 2.30 mg kg 1. The highest Cd concentration (2.30 mg kg 1) was detected in the soil sample of Naltar. Similarly, the mean concentrations of Cu ranged from 55 to 147 mg kg 1 as given in Table 3. The highest concentration of Ni (57 mg kg 1) was detected in the samples of Jageer baseen. The concentrations of Pb ranged from 29 to 138 mg kg 1 as given in Table 3. Zn concentrations were highly variable throughout the study area and ranged from 173 to 1194 mg kg 1. 3.2. Heavy metals in vegetables
2.8. Soil-to-plant transfer factor Metal concentrations in the extracts of soils and plants were calculated on the basis of dry weight. The soil-to-plant transfer factor (PTF) was calculated as PTF¼ Cplants/Csoil (Cui et al., 2005), where Cplant and Csoil represent the heavy metal concentration in extracts of plants and soils on dry weight basis, respectively. 2.9. Daily intake of metals The daily intake of metals (DIM) was determined using the equation DIM¼ Cmetal Cfactor Dfood intake/BWaverage weight. Cmetal, Cfactor, Dfood intake and BWaverage weight
The mean concentrations of heavy metals in various vegetable species collected from the study area were compared with the standards set by China, India and FAO/WHO for vegetables and fruits (Table 4). The mean concentrations of Cd ranged from 0.24 to 2.10 mg kg 1. The highest Cd concentration was detected in S. oleracea, while the lowest concentration in M. sylvestris (Table 4). The mean concentrations of Cu ranged from 9 to 48 mg kg 1, in all the vegetable samples with the highest Cu concentration in C. intibus. The mean concentrations of Ni ranged
Table 2 Basic properties of soil samples collected from the study area. Parameters
pH MCa (%) SOMb (%) Clay (%) (o 2 mm) Silt (%) (2–20 mm) Fine sand (%) (20–200 mm), Coarse sand (%) (4200 mm), 7 Standard deviation. a b
Moisture contents. Soil organic matter.
Sampling sites
Mean
Konadas
Dainyor
Nagirl
Jageer Baseen
Naltar
7.77 22.70 5.98 1.30 18.10 42.29 38.32
7.57 10.45 1.25 0.69 25.78 43.85 29.64
7.74 9.50 1.65 0.503 13.61 41.13 44.75
7.53 12.40 2.00 1.21 12.44 29.54 56.81
6.60 20.26 4.62 0.25 11.80 36.96 51.00
7.44 7 0.48 15.06 7 0.06 3.107 0.02 0.797 0.45 16.35 7 5.82 38.75 7 5.75 44.10 7 10.63
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
1823
Table 3 Mean concentrations (mg kg 1) of heavy metals in soil samples (n ¼11 for each site) of the study area are compared with the permissible limits set by various countries. Heavy metals
Cd Cu Ni Pb Zn
Sampling sites
Standards
Konadas
Dainyor
Nagirl
Jageer baseen
Naltar
SEPAa (1995)
Indian standardsb
EUc (2000)
1.00 7 0.7 147 7 37 52 7 15 35 7 29 590 7 350
0.85 7 0.25 99 7 29 31 7 13 36 7 31 1193 7 449
0.37 0.15 55 7 36 36 7 16 43 7 18 172 7 82
0.75 7 0.66 72 7 38 57 7 10 29 7 22 210 7 147
2.3 7 0.90 71 7 33 24 7 11 138 7 46 460 7 447
0.6 100 60 350 300
NAd 135–270 75–150 250–500 300–600
1.5 100 70 100 200
7 Standard deviation. a
State Environmental Protection Administration China. Indian standards (Awashti, 2000). EU (European Union, 2000). d Not available. b c
from 4 to 24 mg kg 1. However, the highest Ni concentration was observed in B. oleracea (Table 4). Similarly, the mean concentrations of Pb in the studied vegetable samples ranged from 9 to 44 mg kg 1, the highest mean concentration of Pb was observed in M. sylvestris. Similarly, the mean concentrations of Zn ranged from 7 to 350 mg kg 1 with highest concentrations in M. sylvestris, C. intibus and B. campestris. Comparison with SEPA (2005) limits indicated that the enrichment trend of heavy metals in the vegetables of the study area was in the order of Cd 4Pb4 Zn4Cu 4Ni.
3.3. Plant transfer factor The mean PTF values for Cd, Cu, Ni, Pb and Zn ranged from 0.58 to 2.01, 0.16 to 0.55, 0.19 to 1.62, 0.22 to 1.35 and 0.15 to 0.90, respectively. Cd transfer factor was the highest for P. oleracea, B. oleracea, T. repenus, A. viridis, S. oleracea, M. Sylvestris, L sativa and M. neglecta. Similarly the highest PTF was found for Ni in B. compestris and M. sylvestris, while for Pb it was found in C. intibus. The trend of transfer factor of heavy metals for different vegetables was in the order of Cd4Ni4Pb4Zn 4Cu.
3.4. Values of DIM and HRI of heavy metals Table 6 shows the values of DIM for both children and adults based on average daily consumption of different vegetables. The DIM values were considerably high through the consumption of selected vegetables grown in the study area. However, all the values were below one; the highest intake of Zn, Cu and Pb was noted in most of the vegetables for children and the lowest for Cd and Ni. The values of HRI for selected heavy metals through the consumption of vegetables for both adults and children were also calculated and the values are given in Table 7. The HRI of Cd, Cu, Ni, Pb and Zn ranged from 8.4 10 1 to 1.0 10 1, 7.5 10 1 to 8.4 10 2, 4.9 10 1 to 8.4 10 2, 5.1 to 1.1 and 3.6 10 1 to 9.3 10 3, respectively, for adults, while it ranged from 1.3 100 to 1.4 10 1, 1.1 to 1.4 10 1, 7.3 10 1 to 1.3 10 1, 7.6 to 1.6 and 5.5 10 1 to 1.4 10 2, respectively, for children. The highest HRI value was obtained for M. sylvestris for both adults and children, while the lowest was for M. neglecta. The results were compared with those reported by Singh et al. (2010) where the HRI value was more than one for Cd, Pb and Ni. The high values of HRI may be due to the higher proportion of leafy vegetables in diet, which consequently increased the health risk index.
4. Discussion In the study area, the parent rocks (mafic and ultramafic) are enriched with heavy metals, leading to contamination of both soil and plants (Kafayatullah et al., 2001; Shah et al., 2010). An attempt was, therefore, made to link the heavy metals in soil and vegetables with the source rocks in the region. During the field visit and sampling, it was found that the soils of the study area are generally the transported soil. The local geology of the area, therefore, may influence the soils of the area. Transportation and release of minerals from their source rocks are very complicated process and involve so many variables that it makes it impossible to correctly guess the distance a particular mineral can travel. Therefore, to locate the source rocks for minerals, great efforts and investigation are needed; during which all tributaries, channels and soils must be checked for the concerned minerals, which is not an easy job (Khaliq et al., 2008). Moreover, during the flood season farmers tend to use the muddy water for irrigation and other agricultural activities. This muddy water generally has high concentrations of suspended solids, which carry high concentrations of heavy metals. These heavy metals, after settling down in the soils, may have caused the contamination. In the study area, the physical properties of soil indicated that the soil was alkaline except in Naltar, which was slightly acidic. Naltar shows the highest concentration of Cd among the selected sites, which may be due to the moderate acidic pH of the area because soil pH has great influence on the mobility and bioavailability of heavy metals (Nigam et al., 2001; Jan et al., 2010). Kashem et al. (2006) have also reported high Cd concentration at low pH. Similarly, increased availability of heavy metals is also reported with lowering pH by Sukreeyapongse et al. (2002). In some sites of the study area, Cd, Cu, Ni, Pb and Zn were higher than their respective permissible limits. The Cd, Cr, Pb and Zn concentrations in soil were lower than those reported in the previous study at Hunan, southern China mines (Lei et al., 2008), which might be due to the difference in the soil properties, particularly the pH, organic matter and enrichment source. However, the Cd concentrations were higher than those reported by Gaw et al. (2008). Heavy metal concentrations were not consistent with those reported by Rodrıguez et al. (2009) around the Pb–Zn mine in Spain and Krishna and Govil (2008) around the Manali industrial area, Chennai, India. In the study area, all the samples, except from Nagril, exceeded the permissible limit (0.6 mg kg 1) set by SEPA (1995) for soil in China (Table 3). Cu concentration in the sample collected from Konadas exceeded the permissible limit, set by SEPA, India and European Union (EU), while its concentration in the remaining sites was within the limits; Ni concentrations, however, were
50 9.4 100
2.5 0.3 9
NA 66.9 10
30 73.3 20
1.5 NAd 0.1-0.2
1.55 7 1.30 75 78 15 71 10 7 7.1 7 74 0.84 7 0.02 24 7 15 11 7 0.65 15 7 0.43 54 7 21 0.72 70.45 17 71.7 24 72.5 35 722 115 7103 0.94 70.66 9 75 10 72 16 74 96 764 0.79 7 0.29 17 79 11 72 16 78 50 7 10 0.86 70.08 15 71.5 12 74 18 78 50 73 0.81 70.18 48 721 12 710 42 722 240 7164 0.67 70.18 28 72 20 719 44 719 78 771
c
b
a
7 Standard deviation.
Zn
Pb
Ni
Cu
SEPA (2005). FAO/WHO (2001). Indian standards (Awashti 2000). d Not available.
2.10 70.75 11 71.1 7 75.7 18 710 40 75 0.62 7 0.32 17 79 4 7 1.3 17 7 1.7 271 7 31.4 0.24 7 0.06 20 77 10 74 20 79 247 7 35
L. sativa B. oleracea P. oleracea A. viridis T. repenus C. intibus M. sylvestris S. oleracea B. campestris Heavy metals
Table 4 Mean concentrations (mg kg 1) of heavy metals in vegetables (n¼5 for each species) of the study area and permissible limits set by various countries.
Cd
SEPAa (2005) M. sylvestris
M. neglecta
Standards Plant species
Indianc
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
FAOb
1824
found within the permissible limits set by SEPA India and EU. Throughout the study area, the concentrations of Pb were within the permissible limits set by SEPA and India (Table 3), while its concentration exceeded the limit of EU (100 mg kg 1) at Naltar. Similarly, the Zn concentrations were high throughout the study area and its concentration in soil samples collected from Nagril, Jageer baseen and Naltar was within the permissible limit, while those from Konodas and Dainyor exceeded the permissible limit of SEPA, India and EU (Table 3). The mean concentrations of Cd in the vegetables samples exceeded the permissible limits set by SEPA. The mean concentrations of Cu exceeded the SEPA permissible limit (20 mg kg 1) in M. sylvestris, Chicorium intibus, Lectuca sativa, M. sylvestris and M. neglecta (Table 4), while that of Ni exceeded the SEPA limit (10 mg kg 1) in M. sylvestris, C. intibus, Trifolium repenus, B. oleracea and M. neglecta. However, the mean concentrations of Ni in all the vegetables were found within the FAO/WHO limits (67 mg kg 1). Similarly, the mean concentrations of Pb in the studied vegetable samples exceeded the permissible limits set by SEPA, FAO, India and EU and of Zn exceeded the SEPA limit (100 mg kg 1) in the samples of M. sylvestris, C. intibus, B. campestris and B. oleracea. The vegetables grown on contaminated soils accumulate high concentrations of heavy metals in their edible parts (Khan et al., 2008b; Mapanda et al., 2007). The green vegetables, particularly leafy vegetables, uptake high amounts of heavy metals from the soil ecosystem. Once these metals are taken by plants, they then accumulate in their different tissues; therefore, this continuous uptake and translocation can increase the concentrations of metals in plant tissues instead of soil that has low metal concentrations. In this study, the highest enrichment factor was found for Cd. The high enrichment factor for Cd in leafy vegetables was also reported by Fytianos et al. (2001). Similarly, Chary et al. (2008) have reported the highest enrichment factor for heavy metals in leafy vegetables. High transpiration rate may result in high uptake of heavy metals in leafy vegetables to retain the moisture content and growth of these plants (Tani and Barrington, 2005). In a majority of the selected vegetables Cd, Cu, Ni, Pb and Zn partially or totally exceeded the permissible limits set by SEPA, India, EU/UK and/or FAO/WHO. These results are consistent with the findings reported by Intawongse and Dean (2005). The variation in heavy metal concentrations in the vegetables can be attributed to the heavy metal concentrations in soils. The soil Cd concentrations greatly varied (from 0.3 to 2.3 mg kg 1) throughout the selected sampling areas and similar variation (0.24–2.10 mg kg 1) was also present in the Cd concentrations of vegetables. Like Cd, other heavy metals also showed the same variation in soil and vegetables (Tables 3 and 4). Metals enrichment trends in the vegetables of the area were in order of Cd4Pb4Cu4Zn4Ni. Concentrations of all heavy metals exceeded their respective SEPA limits in C. intibus samples (Table 4). Soil-to-plant transfer factor is one of the key components of human exposure to metals through the food chain. In order to investigate the human HRI for naturally enriched soils, it is essential to assess the PTF (Cui et al., 2004). The PTF were higher for Ni, Cd and Pb than other metals and varied widely among the plants species and also with sampling sites (Table 5). The highest Cd PTF was found in P. oleracea, Ni in B. compestris and M. sylvestris, while Pb in C. intibus. This indicated a strong accumulation of the respective metals by food crops, particularly by leafy vegetables. The results showed that the PTF values were lower for Cu, Ni and Zn and higher for Cd and Pb than those reported by Khan et al. (2008b) at China and Jan et al. (2010) at Peshawar and Lower Dir. This could be due to the difference in soil properties and contaminated source. Results from present and previous studies demonstrated that the vegetables grown on heavy metals enriched soil contain high concentrations of heavy metals (Mapanda et al., 2007).
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
1825
Table 5 Mean PTF of heavy metals for different selected vegetables. Plants species
Cd
Cu
Ni
Pb
Zn
M. sylvestris B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta
0.58 7 0.37 0.87 7 0.04 1.26 7 0.99 1.19 7 1.0 0.907 0.10 1.70 7 1.27 1.63 7 1.49 2.01 7 1.89 1.70 7 1.27 1.07 7 0.08 1.05 7 0.04
0.24 70.14 0.17 70.03 0.26 70.19 0.25 70.12 0.55 70.12 0.26 70.13 0.21 70.04 0.16 70.11 0.19 70.14 0.33 70.14 0.32 70.12
1.367 1.0 1.627 0.82 0.237 0.09 1.627 1.2 0.247 0.13 0.347 0.07 0.327 0.10 0.227 0.03 0.767 0.11 0.197 0.12 0.657 0.20
0.517 0.16 0.427 0.06 0.577 0.45 0.427 0.17 1.35 7 0.88 0.457 0.14 0.437 0.26 0.437 0.20 0.947 0.92 0.497 0.21 0.227 0.15
0.90 70.47 0.57 70.39 0.21 70.13 0.15 70.1 0.90 70.12 0.17 70.08 0.17 70.11 0.53 70.41 0.20 70.06 0.25 70.04 0.65 70.11
7 Standard deviation.
Table 6 DIM for individual heavy metals caused by the consumption of different selected vegetables grown in northern areas, Gilgit. Plants M. sylvestris B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta RfD (US-EPA IRIS, 2006) a
Individual Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children
Cd
Cu 4
1.0 10 1.4 10 4 2.5 10 4 3.7 10 4 8.4 10 4 1.3 10 3 2.7 10 4 4.0 10 4 3.3 10 4 4.9 10 4 3.5 10 4 5.2 10 4 3.2 10 4 4.8 10 4 3.8 10 4 5.7 10 4 2.9 10 4 4.3 10 4 3.4 10 4 5.1 10 4 6.2 10 4 9.3 10 4 1.0 10 3
Ni 3
8.1 10 1.2 10 2 6.7 10 3 1.0 10 2 4.5 10 3 6.7 10 3 1.1 10 2 1.7 10 2 1.9 10 2 2.9 10 2 6.0 10 3 9.0 10 3 6.7 10 3 1.0 10 2 3.7 10 3 5.6 10 3 6.7 10 3 1.0 10 2 9.6 10 3 1.4 10 2 3.0 10 2 4.5 10 2 4.0 10 2
Pb 3
4.0 10 5.9 10 3 1.7 10 3 2.5 10 3 2.8 10 3 4.2 10 3 8.0 10 3 1.2 10 2 4.7 10 3 7.0 10 3 4.7 10 3 7.0 10 3 4.3 10 3 6.5 10 3 4.1 10 3 6.2 10 3 9.7 10 3 1.5 10 2 4.2 10 3 6.3 10 3 5.9 10 3 8.9 10 3 2.0 10 2
Zn 3
8.0 10 1.2 10 2 6.6 10 3 1.0 10 2 7.3 10 3 1.1 10 2 1.8 10 2 2.7 10 2 1.7 10 2 2.5 10 2 7.3 10 3 1.1 10 2 6.5 10 3 9.8 10 3 6.3 10 3 9.4 10 3 1.4 10 2 2.1 10 2 5.9 10 3 8.9 10 3 3.8 10 3 5.7 10 3 3.5 10 3a
9.9 10 2 1.5 10 1 1.1 10 1 1.6 10 1 1.6 10 2 2.4 10 2 3.1 10 2 4.7 10 2 9.6 10 2 1.4 10 1 2.0 10 2 3.0 10 2 2.0 10 2 3.0 10 2 3.9 10 2 5.8 10 2 4.6 10 2 6.9 10 2 2.2 10 2 3.2 10 2 2.8 10 3 4.2 10 3 0.3 100
Korre et al. (2002).
In order to assess the health risk of heavy metals, it is essential to estimate the level of exposure of any organism to that particular heavy metal, by quantifying the routes of exposure of a pollutant to the target organisms. For each of the metal there exist several exposure pathways that depend on the particular contaminated media of soil and food on the receptor population (Caussy et al., 2003). The local residents use these heavy metal enriched food crops and vegetables certainly ingest heavy metals at high concentrations. Once these metals enter the human body they can lead to high health risks (Khan et al., 2008b). As mentioned earlier, the vegetables were enriched with heavy metals and the consumption of such vegetables can lead to human health risks. In the study area, the vegetables were produced by the local community and sold in the local market; therefore, the average metal concentrations of vegetables were used for calculation of the HRI. The HRI results of this study were compared with Singh et al. (2010) and were found to be consistent for Pb ( 41), Cu ( o1) and Zn ( o1). The data indicated that the HRI values were o1 for all the studied heavy metals except for Pb. Typically, HRI values depend on DIM and RfD given by different organizations/authors and the calculated DIM value for Pb was higher than the RfD value; therefore, HRI exceeded the
safe limit. In this study area, the health risks of heavy metal exposure through the food chain was of great concern and generally assumed to be unsafe, particularly through consumption of heavy metal enriched vegetables. In general, the RfD is an estimated daily exposure to the human population that is likely to be without a substantial risk of harmful effects during a lifetime (US-EPA IRIS, 2006). The daily heavy metal intake for both adults and children through the consumption of vegetables in this study was less than the RfD limit set by the US-EPA, IRIS, except for Pb. From the findings of this study regarding DIM and HRI it can be suggested that the consumption of vegetables grown in the study area can cause severe health hazards, particularly due to ingestion of Pb by adults, while Cd, Cu and Pb by children, as these metals show high health risk ratio in children and adults of the study area.
5. Conclusion The present study revealed that there were high concentrations of heavy metals in soil and vegetables released from parent rocks and the extent of enrichment was in the order of
1826
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Table 7 HRI for individual heavy metals caused by the consumption of different selected vegetables grown in northern areas, Gilgit. Plants
Individual
Cd
Cu
Ni
Pb
Zn
M. sylvestris
Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children
1.0 10 1 1.4 10 1 2.5 10 1 3.7 10 1 8.4 10 1 1.3 2.7 10 1 4.0 10 1 3.3 10 1 4.9 10 1 3.5 10 1 5.2 10 1 3.2 10 1 4.8 10 1 3.8 10 1 5.7 10 1 2.9 10 1 4.3 10 1 3.4 10 1 5.1 10 1 6.2 10 1 9.3 10 1
2.0 10 1 3.0 10 1 1.7 10 1 2.5 10 1 1.1 10 1 1.7 10 1 2.8 10 1 4.2 10 1 4.8 10 1 7.2 10 1 1.5 10 1 2.3 10 1 1.7 10 1 2.5 10 1 9.0 10 2 1.4 10 1 1.7 10 1 2.5 10 1 2.4 10 1 3.6 10 1 7.5 10 1 1.1
2.0 10 1 3.0 10 1 8.4 10 2 1.3 10 1 1.4 10 1 2.1 10 1 4.0 10 1 6.0 10 1 2.4 10 1 3.5 10 1 2.3 10 1 3.5 10 1 2.2 10 1 3.3 10 1 2.1 10 1 3.1 10 1 4.9 10 1 7.3 10 1 2.1 10 1 3.2 10 1 3.0 10 1 4.5 10 1
2.3 3.4 1.9 2.8 2.1 3.1 5.1 7.6 4.8 7.2 2.1 3.1 1.9 2.8 1.8 2.7 4.0 6.0 1.7 2.5 1.1 1.6
3.3 10 1 5.0 10 1 3.6 10 1 5.5 10 1 5.3 10 2 8.0 10 2 1.0 10 1 1.6 10 1 3.2 10 1 4.8 10 1 6.7 10 2 1.0 10 1 6.7 10 2 1.0 10 1 1.3 10 1 1.9 10 1 1.5 10 1 2.3 10 1 7.2 10 2 1.1 10 1 9.3 10 3 1.4 10 2
B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta
Cd4Pb4Zn 4Cu4Ni. This research indicated that the leafy vegetables were highly enriched with heavy metals because of their greater capability to accumulate heavy metals from soil. However, this study determined that there were potential health risks for the local residents that regularly consume heavy metals enriched vegetables. It is the responsibility of the government as well as the non-government organization to raise awareness about the severe health hazards of heavy metals in the study area. It is further suggested that the former are needed to be trained and special awareness campaign should be conducted for their training and education. This study was a minor effort to estimate the heavy metal contamination of vegetables from natural sources and further study is needed to evaluate the heavy metal concentrations in human beings (blood and urine) and animals of the area.
Acknowledgments We acknowledge the financial support provided by the Department of Environmental Science, University of Peshawar. The authors thank the Director, National Center of Excellence in Geology, University of Peshawar, for providing analytical facility.
References Awashti, S.K., 2000. Prevention of Food Adulteration act no. 37 of 1954. Central and State Rules as Amended for 1999 3rd Edition Ashoka Law House, New Delhi. Bai, J., Yang, Z., Cui, B., Gao, H., Ding, Q., 2010. Some heavy metals distribution in wetland soils under different land use types along a typical plateau lake, China. Soil Tillage Res. 106, 344–348. Caussy, D., Gochfeld, M., Gurzan, E., Neagu, C., Ruedel, H., 2003. Lessons from case studies of metals investigating exposure, bioavailability and risk. Ecotoxicol. Environ. Saf. 56, 45–51. Cui, Y.J., Zhu, Y.G., Zhai, R.H., Huang, Y., Qiu, Y., Liang, J., 2005. Exposure to metal mixtures and human health impacts in a contaminated area in Nanning, China. Environ. Int. 31, 784–790. Cui, Y.J., Zhu, Y.G., Zhai, R.H., Chen, D.Y., Huang, Y.Z., Qiu, Y., Ling, J.Z., 2004. Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environ. Int. 30, 785–791. Chary, N.S., Kamala, C.T., Raj, D.S.S., 2008. Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicol. Environ. Saf. 69, 513–524.
Del Rı´o, M., Font, R., Almela, C., Ve´lez, D., Montoro, R., Bailo´n, A.D.H., 2002. Heavy metals and arsenic uptake by wild vegetation in the Guadiamar river area after the toxic spill of the Aznalco´llar mine. J. Biotech. 98, 125–137. Duruibe, J.O., Ogwuegbu, M.D.C., Egwurugwu, J.N., 2007. Heavy metal pollution and human biotoxic effects. Int. J. Phys. Sci. 2 (5), 112–118. European Union, 2000. Working Document on sludge, 3rd Draft. Brussels, 27 April 2000. ENV.E.3/LM, pp.19. Facchinelli, A., Sacchi, E., Mallen, I., 2001. Multivariate statistical and GISbased approach to identify heavy metal sources in soils. Environ. Pollut. 114, 245–276. FAO/SIDA, 1983. Manual of methods in aquatic environment research. Part 9. Analysis of metals and organochlorine in fish. FAO Fish Technical Paper 212. (FAO, Rome) Section 2, pp. 30–61. FAO/WHO, 2001. Food additives and contaminants. Codex Alimentarius Commission. Joint FAO/WHO Food Standards Program, ALI-NORM 01/12A, pp. 1–289. FAO, 2000. Food Balance Sheet, Rome. National Institute of Health (1988) National Nutrition Survey, Islamabad. Fytianos, K., Katsianis, G., Triantafyllou, P., Zachariadis, G., 2001. Accumulation of heavy metals in vegetables grown in an industrial area in relation to soil. Bull. Environ. Contamin. Toxicol. 67, 423–430. Gaw, S.K., Kim, N.D., Northcott, G.L., Wilkins, A.L., Robinson, G., 2008. Uptake of SDDT, arsenic, cadmium, copper, and lead by lettuce and radish grown in contaminated horticultural soils. J. Agric. Food Chem. 56, 6584–6593. Ge, K.Y., 1992. The Status of Nutrient and Meal of Chinese in the 1990s. Beijing People’s Hygiene Press, pp. 415–434. Ikeda, M., Zhang, Z.W., Shimbo, S., Watanabe, T., Nakatsuka, H., Moon, C.S., MatsudaInoguchi, N., Higashikawa, K., 2000. Urban population exposure to lead and cadmium in east and south-east Asia. Sci. Total Environ. 249, 373–384. Intawongse, M., Dean, J.R., 2005. Uptake of heavy metals by vegetable plants grown on contaminated soil and their bioavailability in the human gastrointestinal tract. Food Addit. Contam. 23, 36–48. IUCN, 2003. Northern Area State of Environment and Development. International Union for Conservation of Nature Pakistan Country Office, Karachi-75530, Pakistan, pp. 8–55. Iyengar, V., Nair, P., 2000. Global outlook on nutrition and the environment: meeting the challenges of the next millennium. Sci. Total Environ. 249, 331–346. Jan, F.A., Ishaq, M., Khan, S., Ihsanullah, I., Ahmad, I., Shakirullah, M., 2010. A comparative study of human health risks via consumption of food crops grown on wastewater irrigated soil (Peshawar) and relatively clean water irrigated soil (Lower Dir). J. Hazard. Mat. 179, 612–621. Kafayatullah, Q., Shah, M.T., Irfan, M., 2001. Biogeochemical and environmental study of the chromite-rich ultramafic terrain of Malakand area, Pakistan. Environ. Geol. 40, 1482–1486. Kashem, M.D.A., Singh, B.R., Kawai, S., 2006. Mobility and distribution of cadmium, nickel and zinc in contaminated soil profiles from Bangladesh. Nutr. Cycl. Agroecosyst. 77, 187–198. Khan, S., Lin, A., Zhang, S., Hu, Q., Zhu, Y.G., 2008a. Accumulation of polycyclic aromatic hydrocarbons and heavy metal in lettuce grown in the soils contaminated with long-term waste water irrigation. J. Hazard. Mat. 152, 506–515. Khan, S., Cao, Q., Zheng, Y.M., Huang, Y.Z., Zhu, Y.G., 2008b. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 152, 686–692.
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Khaliq, A., Khan, S., Moon, C.J., Ahmad, J., 2008. Heavy metal concentrations and mineral grains in soils and sands of Hindu Kush ranges, Asian plate, northern Pakistan. In: Proceedings of the 14th International Conference on Heavy Metals in the Environment (November 16–23, 2008), Taipei, Taiwan, pp. 118–122. Krishna, A.K., Govil, P.K., 2008. Assessment of heavy metal contamination in soils around Manali industrial area, Chennai, Southern India. Environ. Geol. 54, 1465–1472. Korre, A., Durucan, S., Koutroumani, A., 2002. Quantitative-spatial assessment of the risks associated with high Pb loads in soils around Lavrio, Greece. Appl. Geochem. 17, 1029–1045. Lei, M., Liao, B., Zeng, Q., Qin, P., Khan, S., 2008. Fraction distributions of lead, cadmium, copper, and zinc in metal-contaminated soil before and after extraction with disodium ethylenediaminetetraacetic acid. Commun. Soil Sci. Plant Anal. 39 (13), 1963–1978. Li, X.D., Lee, S.L., Wong, S.C., Shi, W.Z., Thornton, I., 2004. The study of metal contamination in urban soil of Hong Kong using a GIS base approach. Environ. Pollut. 129, 113–124. Mapanda, F., Mangwayana, E.N., Nyamangara, J., Giller, K.E., 2007. Uptake of heavy metals by vegetables irrigated using wastewater and the subsequent risks in Harare, Zimbabwe. Phys. Chem. Earth 32, 1399–1405. Nasreddine, L., Parent-Massin, D., 2002. Food contamination by metals and pesticides in the European Union. Should we worry? Toxicol. Lett. 127 29–41. Nigam, R., Srivastava, S., Prakash, S., Srivastava, M.M., 2001. Cadmium mobilization and plant availability—the impact of organic acids commonly exuded from roots. Plant Soil 230, 107–113. Oliver, M.A., 1997. Soil and human health: a review. Eur. J. Soil Sci. 48, 573–592. Rodrıguez, L., Ruiz, E., Alonso-Azca´rate, J., Rincon, J., 2009. Heavy metal distribution and chemical speciation in tailings and soils around a Pb–Zn mine in Spain. J. Environ. Manage. 90, 1106–1116. Raghunath, R., Tripathi, R.M., Kumar, A.V., Sathe, A.P., Khandekar, R.N., Nambi, K.S.V., 1999. Assessment of Pb, Cd, Cu and Zn exposures of 6 to 10 year-old children in Mumbai. Environ. Res. 80, 215–221. Romic, M., Romic, D., 2003. Heavy metals distribution in agricultural top soils in urban area. Environ. Geol. 43, 795–805. SAA, 1977. Determination of the moisture content of a soil: oven drying method (standard method). Standards Association of Australia. AS 1289 B1.1-1977. Satarug, S., Haswell-Elkins, M.R., Moore, M.R., 2000. Safe levels of cadmium intake to prevent renal toxicity in human subjects. Br. J. Nutr. 84, 791–802. SEPA, 1995. Environmental Quality Standards for Soils. State Environmental Protection Administration, China. GB15618-1995.
1827
SEPA, 2005. The Limits of Pollutants in Food. State Environmental Protection Administration, China. GB 2762-2005. Shah, M.T., Begum, S., Khan, S., 2010. Pedo and biogeochemical studies of mafic and ultramafic rocks in the Mingora and Kabal areas, Swat, Pakistan. Environ. Earth Sci. 60, 1091–1102. Singh, A., Sharma, R.K., Agrawal, M., Marshall, F.M., 2010. Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food Chem. Toxic. 48, 611–619. Sukreeyapongse, O., Holm, P.E., Strobel, B.W., Panichsakpatana, S., Magid, J., Hansen, H.C.B., 2002. pH dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J. Environ. Qual. 31, 1901–1909. + + Szollosi, R., Sz Varga, I., Erdei, L., Mihalik, E., 2009. Cadmium-induced oxidative stress and antioxidative mechanisms in germinating Indian mustard (Brassica juncea L.) seeds. Ecotoxicol. Environ. Saf. 72, 1337–1342. Tani, F.H., Barrington, S., 2005. Zinc and copper uptake by plants under two transpiration ratios Part I. Wheat (Triticum aestivum L.). Environ. Pollut. 138, 538–547. Trichopoulos, D., 1997. Epidemiology of cancer. In: DeVita, V.T. (Ed.), Cancer: Principles and Practice of Oncology. Lippincott Company, Philadelphia, pp. 231–258. Turkdogan, M.K., Fevzi, K., Kazim, K., Ilyas, T., Ismail, U., 2003. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ. Toxic. Pharm. 13, 175–179. US-EPA, 2002. Region 9, Preliminary remediation goals. /http://www.epa.gov/ region09/waste/sfind/prgS. US-EPA IRIS, 2006. United States, Environmental Protection Agency, Integrated Risk Information System. /http://www.epa.gov/iris/substS. Velea, T., Gherghe, L., Predica, V., Krebs, R., 2009. Heavy metal contamination in the vicinity of an industrial area near Bucharest. Environ. Sci. Pollut. Res. 10.1007/ s11356-008-0073-5. Wang, X., Sato, T., Xing, B., Tao, S., 2005. Health risks of heavy metals to the general public in Tianjin, China via consumption of vegetables and fish. Sci. Total Environ 350, 28–37. Wang, G., Su, M.Y., Chen, Y.H., Lin, F.F., Luo, D., Gao, S.F., 2006. Transfer characteristics of cadmium and lead from soil to the edible parts of six vegetable species in southeastern China. Environ. Pollut. 144, 127–135. Wu, Y.G., Xu, Y.N., Zhang, J.H., Hu, S.H., 2010. Evaluation of ecological risk and primary empirical research on heavy metals in polluted soil over Xiaoqinling gold mining region, Shaanxi, China. Trans. Nonferrous Met. Soc. China 20, 688–694.
Contents lists available at ScienceDirect
Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv
Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan Sardar Khan a,n, Shafiqur Rehman a, Anwar Zeb Khan a, M. Amjad Khan a, M. Tahir Shah b a b
Department of Environmental Sciences, University of Peshawar, Peshawar 25120, Pakistan National Center of Excellence in Geology, University of Peshawar, Peshawar 25120, Pakistan
a r t i c l e in f o
a b s t r a c t
Article history: Received 3 September 2009 Received in revised form 2 August 2010 Accepted 13 August 2010
This study was conducted to investigate the concentrations of heavy metals in soil and vegetables, and human health risks through ingestion of contaminated vegetables. Soil and vegetable samples were collected from different locations in Gilgit, northern Pakistan, and analyzed for Cd, Cu, Ni, Pb and Zn. Plant transfer factors (PTF), daily intake of metals (DIM) and health risk index (HRI) were also calculated. The concentrations of Cd, Cu and Zn exceeded their respective permissible limits in soil samples. The highest concentrations of Cu, Ni, Pb and Zn were observed in the edible parts of Malva neglecta, Brassica oleracea, Mintha sylvestris and Brassica campestris, respectively. PTF values were lower for all the selected heavy metals, except for Cd. Furthermore, the HRI values were within the safe limit ( o 1) except for Pb; therefore, the health risks of metals through ingestion of vegetables were of great concern in the study area. & 2010 Elsevier Inc. All rights reserved.
Keywords: Daily intake Heavy metals Health risk Natural sources Soil and vegetable contamination Transfer factor
1. Introduction Soil pollution is an undesirable change in the physical, chemical and/or biological characteristics, which reduces the amount of land for cultivation and habitation. Human health is closely related to the quality of soil and especially to its degree of pollution (Romic and Romic, 2003; Velea et al., 2009). Soil acts as a sink and also as a source of pollution with the capacity to transfer pollutants to groundwater and food chain, and then to the human and/or animals. Soil provides the critical interface environment where the interaction of rock, air and water takes place and can be a source of pollution to surface and groundwater, living organisms, sediments and oceans (Facchinelli et al., 2001). Heavy metal enrichment/contamination of the soil has attracted a great deal of attention worldwide due to their non-biodegradable nature and long biological half-lives for elimination from the body (Raghunath et al., 1999; Li et al., 2004). Generally, both natural and anthropogenic sources are responsible for soil enrichment/contamination with heavy metals and its contamination level varies from place to place (Khan et al., 2008a; Shah et al., 2010; Kashem et al., 2006). Previous research works have shown the natural sources of heavy metal enrichment of soil ecosystem and the plants grown on it (Del Rı´o et al., 2002; + osi + et al., 2009). The basic chemical properties of soil depend Szoll
n
Corresponding author. Fax: + 92 91 9218401. E-mail address: [email protected] (S. Khan).
0147-6513/$ - see front matter & 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ecoenv.2010.08.016
on the types of weathered rocks of the concerned areas. Particularly, the mafic and ultramafic rocks are generally enriched in heavy metals such as Fe, Cr, Ni and Cd, leading to elevated level in both soil and standing plants (Kafayatullah et al., 2001; Shah et al., 2010). Heavy metals can be harmful due to their potential to accumulate in different body parts of the human being. Even in low concentrations, they have adverse health effects (Ikeda et al., 2000), because these are non-biodegradible and persistent in nature (Duruibe et al., 2007). Many food plants accumulate heavy metals and result in the rise in the metal contents of farm’s production (Khan et al., 2008a, 2008b). Food chain translocation of heavy metals is one of the consequences of soil contaminated with heavy metals, and excessive intake of metals through consumption of contaminated vegetables and other plants is associated with human health risks (Khan et al., 2008b; Nasreddine and Parent-Massin, 2002; Turkdogan et al., 2003). Furthermore, the ingestion of heavy metals (Cd, Cu, Ni, Pb, Zn, etc.) can seriously cause depletion of some essential nutrients in the body, which in turn causes a decrease in immunological defenses, intrauterine growth retardation (caused by Al, Cd, Mn and Pb), psychosocial dysfunctions, disabilities associated with malnutrition and a high prevalence of upper gastrointestinal cancer (Iyengar and Nair, 2000; Turkdogan et al., 2003). Heavy metals such as Cd and Pb have shown carcinogenic effects (Trichopoulos, 1997). Similarly, high concentrations of Cd, Cu and Pb in vegetables and fruits were related to high prevalence of upper gastrointestinal cancer (Turkdogan et al., 2003).
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Furthermore, Ni at high concentration can cause cancer, skin rashes, fatigue, headache, heart problems, dizziness and respiratory illness. It is a fact that different serious systemic health diseases can develop as a result of excessive dietary accumulation of these heavy metals in human beings (Oliver, 1997). According to Satarug et al. (2000) Cd causes bone fracture, cancer, kidney dysfunction and hypertension. High concentration of Pb has chronic adverse health effects including respiratory and dermatogenic problems caused by ingestion and dermal contacts of contaminated soil and/or dusts (Oliver, 1997; Wang et al., 2006). This requires knowledge of different heavy metals accumulation in different vegetable species and cultivars, as well as soil factors that control bioavailability of heavy metals to plants. In order to produce vegetables with low heavy metals and adopt the best suitable forming/agriculture practices, a better knowledge of heavy metals accumulation in different vegetables species will be required. This study was aimed to investigate soil and vegetable enrichment with heavy metals, originating from natural sources such as weathering of rocks and contribution from underground geology and soil-to-plant transfer factor and human health risks due to ingestion of heavy metals enriched vegetables.
2. Material and methods 2.1. Area description
1821
The meta-sedimentary rocks of the Gilgit Complex are greenshist facies slates, phyllites and psammite, having local mineralization of base metal sulfides. The soil is sandy and neutral with a slightly acidic nature in some regions (Naltar). Land use in the region includes agriculture and orchids, and most of cultivation is generally focused on green leafy vegetable and other edible crops. The cultivated areas have been developed on alluvial fans and to a lesser extent from the reclamation of old rivers terraces. Soil is generally low in clay contents, high in silt and sand fraction and low in organic matter (usually less than 1%). The soil is freely drained with only moderate water retention capacity and is generally shallow. 2.2. Soil sampling and preparation In the study area, five sites were selected for soil sampling and eleven samples were collected from each sampling site (total of 55 samples) at a depth of 0–25 cm with stainless steel auger. Each sample was collected in the form of sub-samples at a distance of about 20 m each from the first sub-sample in different directions, at each sampling site. These sub-samples were thoroughly mixed to a composite sample (Wu et al., 2010). The samples were brought to laboratory in polyethylene bags and air-dried covered with cloth to prevent contamination. After drying, the soil samples were mechanically ground and passed through a sieve of 2 mm and properly stored for analysis. 2.3. Vegetable sampling and preparation The vegetable samples (Table 1) were collected from the same sites from where the soil samples were collected and the total number of vegetable samples was 60. The vegetables were taken out along with their roots and cut into roots and shoots. The root and shoot tissues were washed with double deionised water to remove the soil particles and then placed in separate paper bags properly marked.
Table 1 English, local and botanical names of the vegetables collected from study area.
The study area is located within the administrative capital (Gilgit) Baltistan, northern Pakistan (Fig. 1). The Gilgit region covers an area of about 16 800 km2 with latitude from 351 31! to 361 09! N and longitude from 731 24! to 741 54! E. The climate of the study area is moderate with average maximum temperature 35.9 and minimum 16 1C. The monsoon winds are blocked by the high mountains of Nanga Parbat and clouds cannot reach Gilgit, which make it dry and rugged. The annual rainfall in the region is 136.2 with maximum 28.3 mm in April and minimum 2.1 mm in November. The total agricultural land consists of 36 769 ha, usually cultivated with cereals, vegetables, fruits and fodder (IUCN, 2003). The Gilgit area is generally composed of fluvial plain deposits. It is mostly surrounded by volcanic rocks and the rocks of the Kohistan batholith in the north, northeast and northwest while its southern, southeastern and southwestern parts are covered by the meta-sedimentary rocks of the Gilgit Complex. The volcanic rocks are mainly basaltic andesites, rhyolites and pyroclastic flows. The Kohistan batholith is composed of a variety of diorites, granodiorites and granites.
English name
Local name
Botanical name
Spinach Lettuce Cauliflower Trifolium Mustard Zebra mallow Common chicory Mint Slender amaranth Common purslane Common mallow (button weed)
Palak Salad Kamshah Shaftal Isgar Swanchal Ishkanachi Philil Ganhari Pichili Shani
Spinecia oleracea Lectuca sativa Brassica oleracea Trifolium repenus Brassica campestris Malva sylvestris Cichorium intybus Mentha sylvestris Amaranthus viridis Portulaca oleracea Malva neglecta
Fig. 1. Location map of the study area (Gilgit) Biltastan, northern Pakistan.
1822
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
The vegetable samples were kept in oven at 70 1C till complete dryness. Dried vegetable samples, both roots and shoots, were powdered using clean electronic grinder and then stored in paper bags at room temperature for further analysis. 2.4. Analytical procedures Physical properties of soil were measured according to standard procedures as shown in Table 2. The soil fraction of o 2 mm was used to determine pH (1:3.5 soil water extract) using a pH meter. The soil organic matter was determined using the Walkley–Black procedure (Bai et al., 2010), while the soil moisture content was determined using the Australian standard method (SAA, 1977). Particle size analyses were performed on Fritsch Analysette 3 PRO sieve machine.
represent the heavy metal concentrations in plants (mg kg 1), conversion factor (fresh vegetable weight into dry vegetable weight), daily intake of vegetables and average body weight, respectively. The average daily vegetable intake for adults and children was considered to be 0.345 and 0.232 kg person 1 day 1, respectively, while the average adult and child body weights were considered as 73 (FAO, 2000) and 32.7 kg, respectively (Ge, 1992; Wang et al., 2005). 2.10. Health risk index The health risk index (HRI) for the inhabitants through the consumption of contaminated vegetables was assessed based on the food chain and the reference oral dose (RfD) for each metal such as HRI ¼DIM/RfD (US-EPA, 2002). HRI o 1 indicates the exposed population is assumed to be safe.
2.5. Soil digestion 2.11. Statistical analysis Soil samples were digested according to the method adopted by FAO/SIDA (1983). 1 g air-dried and powdered soil sample was taken into a pyrex beaker and 15 mL of aqua regia was added. It was kept overnight and then heated on the hot plate until no brown fumes were produced. Then concentrated HClO4 (5 mL) was added and heated again on low heat until the solution was evaporated near to dryness. The extracts were filtered and the final volume of 50 mL was made with double de-ionized water.
Data were statistically analyzed using SPSS (11.5) Statistical software. The measurements were expressed in term of means with standard deviation; also the figure is represented with the mean values. Microsoft excel software (Microsoft 2003) was used to evaluate the results graphically. ANOVA and cluster analysis (CA) statistical techniques were used determine significant differences.
2.6. Vegetable digestion
3. Results
Powdered vegetable sample (2 g) was taken into a pyrex beaker, 10 mL of concentrated HNO3 was added to it and kept overnight without heating. It was then heated on a hot plate, and after evaporation near to dryness, the sample was cooled and 5 mL HClO4 was added and heated again. After digestion was complete, the sample was filtered into a clean volumetric flask and diluted to 50 mL with double de-ionized water.
3.1. Heavy metals in soil
2.7. Heavy metal analysis In the acid extracts, the concentrations of heavy metals including Cd, Cu, Ni, Pb and Zn were determined using atomic absorption spectrophotometer (AAS 700) in the Geochemistry laboratory of National Center of Excellence in Geology, University of Peshawar. The analyses were performed in triplicates under standard optionizing conditions. The blank reagent and standard reference soil (NIST, 2709 San Joaquin) and plant materials (NIST, 1547 Peach leave) of National Institute and Technology were included in each sample batch to verify the accuracy and precision of the digestion procedure and for subsequent analyses. The analyses were within the confidence limit of 95%.
Mean values of the physical characteristics of soil samples are shown in Table 2. A wide range of heavy metal concentrations was observed across the study area (Table 3). The results indicated that the concentrations of Cd in soil samples ranged from 0.30 to 2.30 mg kg 1. The highest Cd concentration (2.30 mg kg 1) was detected in the soil sample of Naltar. Similarly, the mean concentrations of Cu ranged from 55 to 147 mg kg 1 as given in Table 3. The highest concentration of Ni (57 mg kg 1) was detected in the samples of Jageer baseen. The concentrations of Pb ranged from 29 to 138 mg kg 1 as given in Table 3. Zn concentrations were highly variable throughout the study area and ranged from 173 to 1194 mg kg 1. 3.2. Heavy metals in vegetables
2.8. Soil-to-plant transfer factor Metal concentrations in the extracts of soils and plants were calculated on the basis of dry weight. The soil-to-plant transfer factor (PTF) was calculated as PTF¼ Cplants/Csoil (Cui et al., 2005), where Cplant and Csoil represent the heavy metal concentration in extracts of plants and soils on dry weight basis, respectively. 2.9. Daily intake of metals The daily intake of metals (DIM) was determined using the equation DIM¼ Cmetal Cfactor Dfood intake/BWaverage weight. Cmetal, Cfactor, Dfood intake and BWaverage weight
The mean concentrations of heavy metals in various vegetable species collected from the study area were compared with the standards set by China, India and FAO/WHO for vegetables and fruits (Table 4). The mean concentrations of Cd ranged from 0.24 to 2.10 mg kg 1. The highest Cd concentration was detected in S. oleracea, while the lowest concentration in M. sylvestris (Table 4). The mean concentrations of Cu ranged from 9 to 48 mg kg 1, in all the vegetable samples with the highest Cu concentration in C. intibus. The mean concentrations of Ni ranged
Table 2 Basic properties of soil samples collected from the study area. Parameters
pH MCa (%) SOMb (%) Clay (%) (o 2 mm) Silt (%) (2–20 mm) Fine sand (%) (20–200 mm), Coarse sand (%) (4200 mm), 7 Standard deviation. a b
Moisture contents. Soil organic matter.
Sampling sites
Mean
Konadas
Dainyor
Nagirl
Jageer Baseen
Naltar
7.77 22.70 5.98 1.30 18.10 42.29 38.32
7.57 10.45 1.25 0.69 25.78 43.85 29.64
7.74 9.50 1.65 0.503 13.61 41.13 44.75
7.53 12.40 2.00 1.21 12.44 29.54 56.81
6.60 20.26 4.62 0.25 11.80 36.96 51.00
7.44 7 0.48 15.06 7 0.06 3.107 0.02 0.797 0.45 16.35 7 5.82 38.75 7 5.75 44.10 7 10.63
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
1823
Table 3 Mean concentrations (mg kg 1) of heavy metals in soil samples (n ¼11 for each site) of the study area are compared with the permissible limits set by various countries. Heavy metals
Cd Cu Ni Pb Zn
Sampling sites
Standards
Konadas
Dainyor
Nagirl
Jageer baseen
Naltar
SEPAa (1995)
Indian standardsb
EUc (2000)
1.00 7 0.7 147 7 37 52 7 15 35 7 29 590 7 350
0.85 7 0.25 99 7 29 31 7 13 36 7 31 1193 7 449
0.37 0.15 55 7 36 36 7 16 43 7 18 172 7 82
0.75 7 0.66 72 7 38 57 7 10 29 7 22 210 7 147
2.3 7 0.90 71 7 33 24 7 11 138 7 46 460 7 447
0.6 100 60 350 300
NAd 135–270 75–150 250–500 300–600
1.5 100 70 100 200
7 Standard deviation. a
State Environmental Protection Administration China. Indian standards (Awashti, 2000). EU (European Union, 2000). d Not available. b c
from 4 to 24 mg kg 1. However, the highest Ni concentration was observed in B. oleracea (Table 4). Similarly, the mean concentrations of Pb in the studied vegetable samples ranged from 9 to 44 mg kg 1, the highest mean concentration of Pb was observed in M. sylvestris. Similarly, the mean concentrations of Zn ranged from 7 to 350 mg kg 1 with highest concentrations in M. sylvestris, C. intibus and B. campestris. Comparison with SEPA (2005) limits indicated that the enrichment trend of heavy metals in the vegetables of the study area was in the order of Cd 4Pb4 Zn4Cu 4Ni.
3.3. Plant transfer factor The mean PTF values for Cd, Cu, Ni, Pb and Zn ranged from 0.58 to 2.01, 0.16 to 0.55, 0.19 to 1.62, 0.22 to 1.35 and 0.15 to 0.90, respectively. Cd transfer factor was the highest for P. oleracea, B. oleracea, T. repenus, A. viridis, S. oleracea, M. Sylvestris, L sativa and M. neglecta. Similarly the highest PTF was found for Ni in B. compestris and M. sylvestris, while for Pb it was found in C. intibus. The trend of transfer factor of heavy metals for different vegetables was in the order of Cd4Ni4Pb4Zn 4Cu.
3.4. Values of DIM and HRI of heavy metals Table 6 shows the values of DIM for both children and adults based on average daily consumption of different vegetables. The DIM values were considerably high through the consumption of selected vegetables grown in the study area. However, all the values were below one; the highest intake of Zn, Cu and Pb was noted in most of the vegetables for children and the lowest for Cd and Ni. The values of HRI for selected heavy metals through the consumption of vegetables for both adults and children were also calculated and the values are given in Table 7. The HRI of Cd, Cu, Ni, Pb and Zn ranged from 8.4 10 1 to 1.0 10 1, 7.5 10 1 to 8.4 10 2, 4.9 10 1 to 8.4 10 2, 5.1 to 1.1 and 3.6 10 1 to 9.3 10 3, respectively, for adults, while it ranged from 1.3 100 to 1.4 10 1, 1.1 to 1.4 10 1, 7.3 10 1 to 1.3 10 1, 7.6 to 1.6 and 5.5 10 1 to 1.4 10 2, respectively, for children. The highest HRI value was obtained for M. sylvestris for both adults and children, while the lowest was for M. neglecta. The results were compared with those reported by Singh et al. (2010) where the HRI value was more than one for Cd, Pb and Ni. The high values of HRI may be due to the higher proportion of leafy vegetables in diet, which consequently increased the health risk index.
4. Discussion In the study area, the parent rocks (mafic and ultramafic) are enriched with heavy metals, leading to contamination of both soil and plants (Kafayatullah et al., 2001; Shah et al., 2010). An attempt was, therefore, made to link the heavy metals in soil and vegetables with the source rocks in the region. During the field visit and sampling, it was found that the soils of the study area are generally the transported soil. The local geology of the area, therefore, may influence the soils of the area. Transportation and release of minerals from their source rocks are very complicated process and involve so many variables that it makes it impossible to correctly guess the distance a particular mineral can travel. Therefore, to locate the source rocks for minerals, great efforts and investigation are needed; during which all tributaries, channels and soils must be checked for the concerned minerals, which is not an easy job (Khaliq et al., 2008). Moreover, during the flood season farmers tend to use the muddy water for irrigation and other agricultural activities. This muddy water generally has high concentrations of suspended solids, which carry high concentrations of heavy metals. These heavy metals, after settling down in the soils, may have caused the contamination. In the study area, the physical properties of soil indicated that the soil was alkaline except in Naltar, which was slightly acidic. Naltar shows the highest concentration of Cd among the selected sites, which may be due to the moderate acidic pH of the area because soil pH has great influence on the mobility and bioavailability of heavy metals (Nigam et al., 2001; Jan et al., 2010). Kashem et al. (2006) have also reported high Cd concentration at low pH. Similarly, increased availability of heavy metals is also reported with lowering pH by Sukreeyapongse et al. (2002). In some sites of the study area, Cd, Cu, Ni, Pb and Zn were higher than their respective permissible limits. The Cd, Cr, Pb and Zn concentrations in soil were lower than those reported in the previous study at Hunan, southern China mines (Lei et al., 2008), which might be due to the difference in the soil properties, particularly the pH, organic matter and enrichment source. However, the Cd concentrations were higher than those reported by Gaw et al. (2008). Heavy metal concentrations were not consistent with those reported by Rodrıguez et al. (2009) around the Pb–Zn mine in Spain and Krishna and Govil (2008) around the Manali industrial area, Chennai, India. In the study area, all the samples, except from Nagril, exceeded the permissible limit (0.6 mg kg 1) set by SEPA (1995) for soil in China (Table 3). Cu concentration in the sample collected from Konadas exceeded the permissible limit, set by SEPA, India and European Union (EU), while its concentration in the remaining sites was within the limits; Ni concentrations, however, were
50 9.4 100
2.5 0.3 9
NA 66.9 10
30 73.3 20
1.5 NAd 0.1-0.2
1.55 7 1.30 75 78 15 71 10 7 7.1 7 74 0.84 7 0.02 24 7 15 11 7 0.65 15 7 0.43 54 7 21 0.72 70.45 17 71.7 24 72.5 35 722 115 7103 0.94 70.66 9 75 10 72 16 74 96 764 0.79 7 0.29 17 79 11 72 16 78 50 7 10 0.86 70.08 15 71.5 12 74 18 78 50 73 0.81 70.18 48 721 12 710 42 722 240 7164 0.67 70.18 28 72 20 719 44 719 78 771
c
b
a
7 Standard deviation.
Zn
Pb
Ni
Cu
SEPA (2005). FAO/WHO (2001). Indian standards (Awashti 2000). d Not available.
2.10 70.75 11 71.1 7 75.7 18 710 40 75 0.62 7 0.32 17 79 4 7 1.3 17 7 1.7 271 7 31.4 0.24 7 0.06 20 77 10 74 20 79 247 7 35
L. sativa B. oleracea P. oleracea A. viridis T. repenus C. intibus M. sylvestris S. oleracea B. campestris Heavy metals
Table 4 Mean concentrations (mg kg 1) of heavy metals in vegetables (n¼5 for each species) of the study area and permissible limits set by various countries.
Cd
SEPAa (2005) M. sylvestris
M. neglecta
Standards Plant species
Indianc
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
FAOb
1824
found within the permissible limits set by SEPA India and EU. Throughout the study area, the concentrations of Pb were within the permissible limits set by SEPA and India (Table 3), while its concentration exceeded the limit of EU (100 mg kg 1) at Naltar. Similarly, the Zn concentrations were high throughout the study area and its concentration in soil samples collected from Nagril, Jageer baseen and Naltar was within the permissible limit, while those from Konodas and Dainyor exceeded the permissible limit of SEPA, India and EU (Table 3). The mean concentrations of Cd in the vegetables samples exceeded the permissible limits set by SEPA. The mean concentrations of Cu exceeded the SEPA permissible limit (20 mg kg 1) in M. sylvestris, Chicorium intibus, Lectuca sativa, M. sylvestris and M. neglecta (Table 4), while that of Ni exceeded the SEPA limit (10 mg kg 1) in M. sylvestris, C. intibus, Trifolium repenus, B. oleracea and M. neglecta. However, the mean concentrations of Ni in all the vegetables were found within the FAO/WHO limits (67 mg kg 1). Similarly, the mean concentrations of Pb in the studied vegetable samples exceeded the permissible limits set by SEPA, FAO, India and EU and of Zn exceeded the SEPA limit (100 mg kg 1) in the samples of M. sylvestris, C. intibus, B. campestris and B. oleracea. The vegetables grown on contaminated soils accumulate high concentrations of heavy metals in their edible parts (Khan et al., 2008b; Mapanda et al., 2007). The green vegetables, particularly leafy vegetables, uptake high amounts of heavy metals from the soil ecosystem. Once these metals are taken by plants, they then accumulate in their different tissues; therefore, this continuous uptake and translocation can increase the concentrations of metals in plant tissues instead of soil that has low metal concentrations. In this study, the highest enrichment factor was found for Cd. The high enrichment factor for Cd in leafy vegetables was also reported by Fytianos et al. (2001). Similarly, Chary et al. (2008) have reported the highest enrichment factor for heavy metals in leafy vegetables. High transpiration rate may result in high uptake of heavy metals in leafy vegetables to retain the moisture content and growth of these plants (Tani and Barrington, 2005). In a majority of the selected vegetables Cd, Cu, Ni, Pb and Zn partially or totally exceeded the permissible limits set by SEPA, India, EU/UK and/or FAO/WHO. These results are consistent with the findings reported by Intawongse and Dean (2005). The variation in heavy metal concentrations in the vegetables can be attributed to the heavy metal concentrations in soils. The soil Cd concentrations greatly varied (from 0.3 to 2.3 mg kg 1) throughout the selected sampling areas and similar variation (0.24–2.10 mg kg 1) was also present in the Cd concentrations of vegetables. Like Cd, other heavy metals also showed the same variation in soil and vegetables (Tables 3 and 4). Metals enrichment trends in the vegetables of the area were in order of Cd4Pb4Cu4Zn4Ni. Concentrations of all heavy metals exceeded their respective SEPA limits in C. intibus samples (Table 4). Soil-to-plant transfer factor is one of the key components of human exposure to metals through the food chain. In order to investigate the human HRI for naturally enriched soils, it is essential to assess the PTF (Cui et al., 2004). The PTF were higher for Ni, Cd and Pb than other metals and varied widely among the plants species and also with sampling sites (Table 5). The highest Cd PTF was found in P. oleracea, Ni in B. compestris and M. sylvestris, while Pb in C. intibus. This indicated a strong accumulation of the respective metals by food crops, particularly by leafy vegetables. The results showed that the PTF values were lower for Cu, Ni and Zn and higher for Cd and Pb than those reported by Khan et al. (2008b) at China and Jan et al. (2010) at Peshawar and Lower Dir. This could be due to the difference in soil properties and contaminated source. Results from present and previous studies demonstrated that the vegetables grown on heavy metals enriched soil contain high concentrations of heavy metals (Mapanda et al., 2007).
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
1825
Table 5 Mean PTF of heavy metals for different selected vegetables. Plants species
Cd
Cu
Ni
Pb
Zn
M. sylvestris B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta
0.58 7 0.37 0.87 7 0.04 1.26 7 0.99 1.19 7 1.0 0.907 0.10 1.70 7 1.27 1.63 7 1.49 2.01 7 1.89 1.70 7 1.27 1.07 7 0.08 1.05 7 0.04
0.24 70.14 0.17 70.03 0.26 70.19 0.25 70.12 0.55 70.12 0.26 70.13 0.21 70.04 0.16 70.11 0.19 70.14 0.33 70.14 0.32 70.12
1.367 1.0 1.627 0.82 0.237 0.09 1.627 1.2 0.247 0.13 0.347 0.07 0.327 0.10 0.227 0.03 0.767 0.11 0.197 0.12 0.657 0.20
0.517 0.16 0.427 0.06 0.577 0.45 0.427 0.17 1.35 7 0.88 0.457 0.14 0.437 0.26 0.437 0.20 0.947 0.92 0.497 0.21 0.227 0.15
0.90 70.47 0.57 70.39 0.21 70.13 0.15 70.1 0.90 70.12 0.17 70.08 0.17 70.11 0.53 70.41 0.20 70.06 0.25 70.04 0.65 70.11
7 Standard deviation.
Table 6 DIM for individual heavy metals caused by the consumption of different selected vegetables grown in northern areas, Gilgit. Plants M. sylvestris B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta RfD (US-EPA IRIS, 2006) a
Individual Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children
Cd
Cu 4
1.0 10 1.4 10 4 2.5 10 4 3.7 10 4 8.4 10 4 1.3 10 3 2.7 10 4 4.0 10 4 3.3 10 4 4.9 10 4 3.5 10 4 5.2 10 4 3.2 10 4 4.8 10 4 3.8 10 4 5.7 10 4 2.9 10 4 4.3 10 4 3.4 10 4 5.1 10 4 6.2 10 4 9.3 10 4 1.0 10 3
Ni 3
8.1 10 1.2 10 2 6.7 10 3 1.0 10 2 4.5 10 3 6.7 10 3 1.1 10 2 1.7 10 2 1.9 10 2 2.9 10 2 6.0 10 3 9.0 10 3 6.7 10 3 1.0 10 2 3.7 10 3 5.6 10 3 6.7 10 3 1.0 10 2 9.6 10 3 1.4 10 2 3.0 10 2 4.5 10 2 4.0 10 2
Pb 3
4.0 10 5.9 10 3 1.7 10 3 2.5 10 3 2.8 10 3 4.2 10 3 8.0 10 3 1.2 10 2 4.7 10 3 7.0 10 3 4.7 10 3 7.0 10 3 4.3 10 3 6.5 10 3 4.1 10 3 6.2 10 3 9.7 10 3 1.5 10 2 4.2 10 3 6.3 10 3 5.9 10 3 8.9 10 3 2.0 10 2
Zn 3
8.0 10 1.2 10 2 6.6 10 3 1.0 10 2 7.3 10 3 1.1 10 2 1.8 10 2 2.7 10 2 1.7 10 2 2.5 10 2 7.3 10 3 1.1 10 2 6.5 10 3 9.8 10 3 6.3 10 3 9.4 10 3 1.4 10 2 2.1 10 2 5.9 10 3 8.9 10 3 3.8 10 3 5.7 10 3 3.5 10 3a
9.9 10 2 1.5 10 1 1.1 10 1 1.6 10 1 1.6 10 2 2.4 10 2 3.1 10 2 4.7 10 2 9.6 10 2 1.4 10 1 2.0 10 2 3.0 10 2 2.0 10 2 3.0 10 2 3.9 10 2 5.8 10 2 4.6 10 2 6.9 10 2 2.2 10 2 3.2 10 2 2.8 10 3 4.2 10 3 0.3 100
Korre et al. (2002).
In order to assess the health risk of heavy metals, it is essential to estimate the level of exposure of any organism to that particular heavy metal, by quantifying the routes of exposure of a pollutant to the target organisms. For each of the metal there exist several exposure pathways that depend on the particular contaminated media of soil and food on the receptor population (Caussy et al., 2003). The local residents use these heavy metal enriched food crops and vegetables certainly ingest heavy metals at high concentrations. Once these metals enter the human body they can lead to high health risks (Khan et al., 2008b). As mentioned earlier, the vegetables were enriched with heavy metals and the consumption of such vegetables can lead to human health risks. In the study area, the vegetables were produced by the local community and sold in the local market; therefore, the average metal concentrations of vegetables were used for calculation of the HRI. The HRI results of this study were compared with Singh et al. (2010) and were found to be consistent for Pb ( 41), Cu ( o1) and Zn ( o1). The data indicated that the HRI values were o1 for all the studied heavy metals except for Pb. Typically, HRI values depend on DIM and RfD given by different organizations/authors and the calculated DIM value for Pb was higher than the RfD value; therefore, HRI exceeded the
safe limit. In this study area, the health risks of heavy metal exposure through the food chain was of great concern and generally assumed to be unsafe, particularly through consumption of heavy metal enriched vegetables. In general, the RfD is an estimated daily exposure to the human population that is likely to be without a substantial risk of harmful effects during a lifetime (US-EPA IRIS, 2006). The daily heavy metal intake for both adults and children through the consumption of vegetables in this study was less than the RfD limit set by the US-EPA, IRIS, except for Pb. From the findings of this study regarding DIM and HRI it can be suggested that the consumption of vegetables grown in the study area can cause severe health hazards, particularly due to ingestion of Pb by adults, while Cd, Cu and Pb by children, as these metals show high health risk ratio in children and adults of the study area.
5. Conclusion The present study revealed that there were high concentrations of heavy metals in soil and vegetables released from parent rocks and the extent of enrichment was in the order of
1826
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Table 7 HRI for individual heavy metals caused by the consumption of different selected vegetables grown in northern areas, Gilgit. Plants
Individual
Cd
Cu
Ni
Pb
Zn
M. sylvestris
Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children Adults Children
1.0 10 1 1.4 10 1 2.5 10 1 3.7 10 1 8.4 10 1 1.3 2.7 10 1 4.0 10 1 3.3 10 1 4.9 10 1 3.5 10 1 5.2 10 1 3.2 10 1 4.8 10 1 3.8 10 1 5.7 10 1 2.9 10 1 4.3 10 1 3.4 10 1 5.1 10 1 6.2 10 1 9.3 10 1
2.0 10 1 3.0 10 1 1.7 10 1 2.5 10 1 1.1 10 1 1.7 10 1 2.8 10 1 4.2 10 1 4.8 10 1 7.2 10 1 1.5 10 1 2.3 10 1 1.7 10 1 2.5 10 1 9.0 10 2 1.4 10 1 1.7 10 1 2.5 10 1 2.4 10 1 3.6 10 1 7.5 10 1 1.1
2.0 10 1 3.0 10 1 8.4 10 2 1.3 10 1 1.4 10 1 2.1 10 1 4.0 10 1 6.0 10 1 2.4 10 1 3.5 10 1 2.3 10 1 3.5 10 1 2.2 10 1 3.3 10 1 2.1 10 1 3.1 10 1 4.9 10 1 7.3 10 1 2.1 10 1 3.2 10 1 3.0 10 1 4.5 10 1
2.3 3.4 1.9 2.8 2.1 3.1 5.1 7.6 4.8 7.2 2.1 3.1 1.9 2.8 1.8 2.7 4.0 6.0 1.7 2.5 1.1 1.6
3.3 10 1 5.0 10 1 3.6 10 1 5.5 10 1 5.3 10 2 8.0 10 2 1.0 10 1 1.6 10 1 3.2 10 1 4.8 10 1 6.7 10 2 1.0 10 1 6.7 10 2 1.0 10 1 1.3 10 1 1.9 10 1 1.5 10 1 2.3 10 1 7.2 10 2 1.1 10 1 9.3 10 3 1.4 10 2
B. campestris S. oleracea M. sylvestris C. intibus T. repenus A. viridis P. oleracea B. oleracea L. sativa M. neglecta
Cd4Pb4Zn 4Cu4Ni. This research indicated that the leafy vegetables were highly enriched with heavy metals because of their greater capability to accumulate heavy metals from soil. However, this study determined that there were potential health risks for the local residents that regularly consume heavy metals enriched vegetables. It is the responsibility of the government as well as the non-government organization to raise awareness about the severe health hazards of heavy metals in the study area. It is further suggested that the former are needed to be trained and special awareness campaign should be conducted for their training and education. This study was a minor effort to estimate the heavy metal contamination of vegetables from natural sources and further study is needed to evaluate the heavy metal concentrations in human beings (blood and urine) and animals of the area.
Acknowledgments We acknowledge the financial support provided by the Department of Environmental Science, University of Peshawar. The authors thank the Director, National Center of Excellence in Geology, University of Peshawar, for providing analytical facility.
References Awashti, S.K., 2000. Prevention of Food Adulteration act no. 37 of 1954. Central and State Rules as Amended for 1999 3rd Edition Ashoka Law House, New Delhi. Bai, J., Yang, Z., Cui, B., Gao, H., Ding, Q., 2010. Some heavy metals distribution in wetland soils under different land use types along a typical plateau lake, China. Soil Tillage Res. 106, 344–348. Caussy, D., Gochfeld, M., Gurzan, E., Neagu, C., Ruedel, H., 2003. Lessons from case studies of metals investigating exposure, bioavailability and risk. Ecotoxicol. Environ. Saf. 56, 45–51. Cui, Y.J., Zhu, Y.G., Zhai, R.H., Huang, Y., Qiu, Y., Liang, J., 2005. Exposure to metal mixtures and human health impacts in a contaminated area in Nanning, China. Environ. Int. 31, 784–790. Cui, Y.J., Zhu, Y.G., Zhai, R.H., Chen, D.Y., Huang, Y.Z., Qiu, Y., Ling, J.Z., 2004. Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environ. Int. 30, 785–791. Chary, N.S., Kamala, C.T., Raj, D.S.S., 2008. Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicol. Environ. Saf. 69, 513–524.
Del Rı´o, M., Font, R., Almela, C., Ve´lez, D., Montoro, R., Bailo´n, A.D.H., 2002. Heavy metals and arsenic uptake by wild vegetation in the Guadiamar river area after the toxic spill of the Aznalco´llar mine. J. Biotech. 98, 125–137. Duruibe, J.O., Ogwuegbu, M.D.C., Egwurugwu, J.N., 2007. Heavy metal pollution and human biotoxic effects. Int. J. Phys. Sci. 2 (5), 112–118. European Union, 2000. Working Document on sludge, 3rd Draft. Brussels, 27 April 2000. ENV.E.3/LM, pp.19. Facchinelli, A., Sacchi, E., Mallen, I., 2001. Multivariate statistical and GISbased approach to identify heavy metal sources in soils. Environ. Pollut. 114, 245–276. FAO/SIDA, 1983. Manual of methods in aquatic environment research. Part 9. Analysis of metals and organochlorine in fish. FAO Fish Technical Paper 212. (FAO, Rome) Section 2, pp. 30–61. FAO/WHO, 2001. Food additives and contaminants. Codex Alimentarius Commission. Joint FAO/WHO Food Standards Program, ALI-NORM 01/12A, pp. 1–289. FAO, 2000. Food Balance Sheet, Rome. National Institute of Health (1988) National Nutrition Survey, Islamabad. Fytianos, K., Katsianis, G., Triantafyllou, P., Zachariadis, G., 2001. Accumulation of heavy metals in vegetables grown in an industrial area in relation to soil. Bull. Environ. Contamin. Toxicol. 67, 423–430. Gaw, S.K., Kim, N.D., Northcott, G.L., Wilkins, A.L., Robinson, G., 2008. Uptake of SDDT, arsenic, cadmium, copper, and lead by lettuce and radish grown in contaminated horticultural soils. J. Agric. Food Chem. 56, 6584–6593. Ge, K.Y., 1992. The Status of Nutrient and Meal of Chinese in the 1990s. Beijing People’s Hygiene Press, pp. 415–434. Ikeda, M., Zhang, Z.W., Shimbo, S., Watanabe, T., Nakatsuka, H., Moon, C.S., MatsudaInoguchi, N., Higashikawa, K., 2000. Urban population exposure to lead and cadmium in east and south-east Asia. Sci. Total Environ. 249, 373–384. Intawongse, M., Dean, J.R., 2005. Uptake of heavy metals by vegetable plants grown on contaminated soil and their bioavailability in the human gastrointestinal tract. Food Addit. Contam. 23, 36–48. IUCN, 2003. Northern Area State of Environment and Development. International Union for Conservation of Nature Pakistan Country Office, Karachi-75530, Pakistan, pp. 8–55. Iyengar, V., Nair, P., 2000. Global outlook on nutrition and the environment: meeting the challenges of the next millennium. Sci. Total Environ. 249, 331–346. Jan, F.A., Ishaq, M., Khan, S., Ihsanullah, I., Ahmad, I., Shakirullah, M., 2010. A comparative study of human health risks via consumption of food crops grown on wastewater irrigated soil (Peshawar) and relatively clean water irrigated soil (Lower Dir). J. Hazard. Mat. 179, 612–621. Kafayatullah, Q., Shah, M.T., Irfan, M., 2001. Biogeochemical and environmental study of the chromite-rich ultramafic terrain of Malakand area, Pakistan. Environ. Geol. 40, 1482–1486. Kashem, M.D.A., Singh, B.R., Kawai, S., 2006. Mobility and distribution of cadmium, nickel and zinc in contaminated soil profiles from Bangladesh. Nutr. Cycl. Agroecosyst. 77, 187–198. Khan, S., Lin, A., Zhang, S., Hu, Q., Zhu, Y.G., 2008a. Accumulation of polycyclic aromatic hydrocarbons and heavy metal in lettuce grown in the soils contaminated with long-term waste water irrigation. J. Hazard. Mat. 152, 506–515. Khan, S., Cao, Q., Zheng, Y.M., Huang, Y.Z., Zhu, Y.G., 2008b. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 152, 686–692.
S. Khan et al. / Ecotoxicology and Environmental Safety 73 (2010) 1820–1827
Khaliq, A., Khan, S., Moon, C.J., Ahmad, J., 2008. Heavy metal concentrations and mineral grains in soils and sands of Hindu Kush ranges, Asian plate, northern Pakistan. In: Proceedings of the 14th International Conference on Heavy Metals in the Environment (November 16–23, 2008), Taipei, Taiwan, pp. 118–122. Krishna, A.K., Govil, P.K., 2008. Assessment of heavy metal contamination in soils around Manali industrial area, Chennai, Southern India. Environ. Geol. 54, 1465–1472. Korre, A., Durucan, S., Koutroumani, A., 2002. Quantitative-spatial assessment of the risks associated with high Pb loads in soils around Lavrio, Greece. Appl. Geochem. 17, 1029–1045. Lei, M., Liao, B., Zeng, Q., Qin, P., Khan, S., 2008. Fraction distributions of lead, cadmium, copper, and zinc in metal-contaminated soil before and after extraction with disodium ethylenediaminetetraacetic acid. Commun. Soil Sci. Plant Anal. 39 (13), 1963–1978. Li, X.D., Lee, S.L., Wong, S.C., Shi, W.Z., Thornton, I., 2004. The study of metal contamination in urban soil of Hong Kong using a GIS base approach. Environ. Pollut. 129, 113–124. Mapanda, F., Mangwayana, E.N., Nyamangara, J., Giller, K.E., 2007. Uptake of heavy metals by vegetables irrigated using wastewater and the subsequent risks in Harare, Zimbabwe. Phys. Chem. Earth 32, 1399–1405. Nasreddine, L., Parent-Massin, D., 2002. Food contamination by metals and pesticides in the European Union. Should we worry? Toxicol. Lett. 127 29–41. Nigam, R., Srivastava, S., Prakash, S., Srivastava, M.M., 2001. Cadmium mobilization and plant availability—the impact of organic acids commonly exuded from roots. Plant Soil 230, 107–113. Oliver, M.A., 1997. Soil and human health: a review. Eur. J. Soil Sci. 48, 573–592. Rodrıguez, L., Ruiz, E., Alonso-Azca´rate, J., Rincon, J., 2009. Heavy metal distribution and chemical speciation in tailings and soils around a Pb–Zn mine in Spain. J. Environ. Manage. 90, 1106–1116. Raghunath, R., Tripathi, R.M., Kumar, A.V., Sathe, A.P., Khandekar, R.N., Nambi, K.S.V., 1999. Assessment of Pb, Cd, Cu and Zn exposures of 6 to 10 year-old children in Mumbai. Environ. Res. 80, 215–221. Romic, M., Romic, D., 2003. Heavy metals distribution in agricultural top soils in urban area. Environ. Geol. 43, 795–805. SAA, 1977. Determination of the moisture content of a soil: oven drying method (standard method). Standards Association of Australia. AS 1289 B1.1-1977. Satarug, S., Haswell-Elkins, M.R., Moore, M.R., 2000. Safe levels of cadmium intake to prevent renal toxicity in human subjects. Br. J. Nutr. 84, 791–802. SEPA, 1995. Environmental Quality Standards for Soils. State Environmental Protection Administration, China. GB15618-1995.
1827
SEPA, 2005. The Limits of Pollutants in Food. State Environmental Protection Administration, China. GB 2762-2005. Shah, M.T., Begum, S., Khan, S., 2010. Pedo and biogeochemical studies of mafic and ultramafic rocks in the Mingora and Kabal areas, Swat, Pakistan. Environ. Earth Sci. 60, 1091–1102. Singh, A., Sharma, R.K., Agrawal, M., Marshall, F.M., 2010. Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food Chem. Toxic. 48, 611–619. Sukreeyapongse, O., Holm, P.E., Strobel, B.W., Panichsakpatana, S., Magid, J., Hansen, H.C.B., 2002. pH dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J. Environ. Qual. 31, 1901–1909. + + Szollosi, R., Sz Varga, I., Erdei, L., Mihalik, E., 2009. Cadmium-induced oxidative stress and antioxidative mechanisms in germinating Indian mustard (Brassica juncea L.) seeds. Ecotoxicol. Environ. Saf. 72, 1337–1342. Tani, F.H., Barrington, S., 2005. Zinc and copper uptake by plants under two transpiration ratios Part I. Wheat (Triticum aestivum L.). Environ. Pollut. 138, 538–547. Trichopoulos, D., 1997. Epidemiology of cancer. In: DeVita, V.T. (Ed.), Cancer: Principles and Practice of Oncology. Lippincott Company, Philadelphia, pp. 231–258. Turkdogan, M.K., Fevzi, K., Kazim, K., Ilyas, T., Ismail, U., 2003. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ. Toxic. Pharm. 13, 175–179. US-EPA, 2002. Region 9, Preliminary remediation goals. /http://www.epa.gov/ region09/waste/sfind/prgS. US-EPA IRIS, 2006. United States, Environmental Protection Agency, Integrated Risk Information System. /http://www.epa.gov/iris/substS. Velea, T., Gherghe, L., Predica, V., Krebs, R., 2009. Heavy metal contamination in the vicinity of an industrial area near Bucharest. Environ. Sci. Pollut. Res. 10.1007/ s11356-008-0073-5. Wang, X., Sato, T., Xing, B., Tao, S., 2005. Health risks of heavy metals to the general public in Tianjin, China via consumption of vegetables and fish. Sci. Total Environ 350, 28–37. Wang, G., Su, M.Y., Chen, Y.H., Lin, F.F., Luo, D., Gao, S.F., 2006. Transfer characteristics of cadmium and lead from soil to the edible parts of six vegetable species in southeastern China. Environ. Pollut. 144, 127–135. Wu, Y.G., Xu, Y.N., Zhang, J.H., Hu, S.H., 2010. Evaluation of ecological risk and primary empirical research on heavy metals in polluted soil over Xiaoqinling gold mining region, Shaanxi, China. Trans. Nonferrous Met. Soc. China 20, 688–694.