banner



Is Cadmium Plated Metal Hazardous Around A Vegetable Garden?

Chemosphere. Author manuscript; available in PMC 2018 Feb 1.

Published in final edited form as:

PMCID: PMC5322861

NIHMSID: NIHMS846074

Lead and cadmium contamination and exposure risk assessment via consumption of vegetables grown in agricultural soils of five-selected regions of Pakistan

Zahir Ur Rehman

1Department of Environmental Sciences, University of Peshawar, Peshawar 25120, Pakistan

3School of Earth and Environmental Sciences, University of Arizona, USA

Sardar Khan

1Department of Environmental Sciences, University of Peshawar, Peshawar 25120, Pakistan

Mark L Brusseau

3School of Earth and Environmental Sciences, University of Arizona, USA

Mohammad Tahir Shah

2National Centre of Excellence in Geology, University of Peshawar, Peshawar 25120, Pakistan

Abstract

Rapid urbanization and industrialization result in serious contamination of soil with toxic metals such as lead (Pb) and cadmium (Cd), which can lead to deleterious health impacts in the exposed population. This study aimed to investigate Pb and Cd contamination in agricultural soils and vegetables in five different agricultural sites in Pakistan. The metal transfer from soil-to-plant, average daily intake of metals, and health risk index (HRI) were also characterized. The Pb concentrations for all soils were below the maximum allowable limits (MAL 350 mg kg−1) set by the State Environmental Protection Administration of China (SEPA), for soils in China. Conversely, Cd concentrations in the soils exceeded the MAL set by SEPA (0.6 mg kg) and the European Union (1.5 mg kg−1) by 62-74% and 4-34%, respectively. The mean Pb concentration in edible parts of vegetables ranged from 1.8-11 mgkg−1. The Pb concentrations for leafy vegetables were higher than the fruiting and pulpy vegetables. The Pb concentrations exceeded the MAL (0.3 mg kg−1) for leafy vegetables and the MAL for fruity and rooty/tuber vegetables (0.1 mg kg−1) set by FAO/WHO-CODEX.. Likewise, all vegetables except Pisum sativum (0.12 mg kg−1) contained Cd concentrations that exceeded the MAL set by SEPA. The HRI values for Pb and Cd were <1 for both adults and children for most of the vegetable species except Luffa acutangula, Solanum lycopersicum, Benincasa hispada, Momordi charantia, Aesculantus malvaceae, Cucumis sativus, Praecitrullus fistulosus, Brassica oleracea, and Colocasia esculanta for children. Based on these results, consumption of these Pb and Cd contaminated vegetables poses a potential health risk to the local consumers.

Keywords: Lead and cadmium, vegetable contamination, bioconcentration factor, average daily intake, health risks

1. Introduction

Food security and safety is of great concern throughout the world due to toxic heavy metal contamination and their associated health risks (Shaheen et al., 2016; Chen et al., 2016; Yousaf et al., 2016; Zhi et al., 2008). The impact of Pb and Cd on human health has long been and continues to be of great concern, particularly for infants and children (Cao et al., 2016; Pan et al., 2016). Heavy metals enter the environment through natural sources (e.g. volcanic-emissions, erosion of soils, and weathering of parent rocks) and human practices (e.g., agricultural activities, manufacturing, mining etc) (ATSDR, 2012). For example, it is estimated that about 25,000 to 30,000 tons per year of Cd are released into the earth ecosystem through various sources; about half from the weathering of rocks and a further proportion from forest fires and volcanoes (ATSDR, 1999). Both Pb and Cd are listed as priority hazardous elements and are considered as two of the top 20 contaminants, ranked 2nd and 7th, respectively, by the US-EPA (ATSDR, 2012). The toxic heavy metals such as Pb and Cd can have severe impacts on biological processes ranging from microbial activities to primary production of plants (Khan et al., 2016; Sinkkonen et al., 2010; Kauppi et al., 2012; Hansi et al., 2014).

Pb has a large spectrum of physical effects such as neurological and gastro-intestinal distress and oncogenic effects (Li et al., 2004). Pb is a neurotoxin that can affect almost every organ or system in the human body, reducing cognitive development and intellectual performance in children and damage kidneys and the reproductive system (e.g., Qin et al., 2010). Most of the accumulated Pb is sequestered in the bone and teeth (e.g., Todd et al., 1996), causing brittle bones and weaknesses in the wrists and fingers. Pb that is stored in bones can re-enter the blood stream during periods of increased bone mineral recycling. Mobilized Pb can be redeposited in the soft tissues of the body and can cause musculo-skeletal, renal, ocular, immunological, and developmental effects (ATSDR, 1999). Pb can also cause chronic health illnesses such as abdominal-pain, nerve damage, lung and stomach cancer, irritability, and headache (e.g., Steenland et al., 2000; Jarup, 2003). As stated above, children are greatly vulnerable to Pb toxicity and their exposure to increased levels of Pb may cause severe health complications, such as behavioral disorders, memory weakening and reduced capability to understand, while long-term Pb exposure can lead to anemia (e.g., Jarup, 2003). Multiple routes of exposure to Pb exist, including unintentional soil ingestion, intake of Pb contaminated food-stuffs, and inhalation of soil-particles containing Pb. The quantity of Pb that can be transferred via inhalation is less than other pathways (Davies et al., 1990), and food ingestion is in some cases the most significant (Cao et al., 2016; Chen et al., 2016; Lanphear and Roghmann, 1997). Pb pollution of food-crops is critical to assess as vegetables are essential sources of human nutrition (Goswami et al., 2012).

Cd exposure may cause severe health effects including lung cancer, reproductive system impacts, gastro-intestinal, osteoporosis, prostate, endocrine disorder (Henson and Chedrese, 2004), cardio-vascular impacts (Martínez-Sánchez et al., 2011; Oliveira et al., 2014), bone fracture, hypertension, (Turkdogan et al., 2003; Khan et al., 2013), anemia, injury of central nervous system, and liver disease (Prabu, 2009; Asfaw, 2013). Cd intake due to the ingestion of environmentally contaminated food-crops was related also with a potential risk of post-menopausal breast cancer (Hiroaki et al., 2013). Furthermore, there are associations between Cd soil pollution and human health risks, for instance the contamination of soils by Japan's Jinzu River and its link with the 'itai-itai' disease (Robson et al., 2014). In the area adjoining to Hunan and Guangdong states (China), decades of metal production were revealed to have contaminated river sediments and agricultural soils (Robson et al., 2014) and residents are considered at risk of chronic health effects from consuming nearby grown food-crops (Zhuang et al., 2009; Zhao et al., 2012).

Pb and Cd are persistent in the environment, and are not removed by normal cropping practices nor easily leached by rainwater because of their strong affinities with the soil solid phase (Tandi et al., 2004; Rehman et al., 2013). Thus, soil constitutes a significant reservoir of Pb and Cd in many systems (e.g., Thuy et al., 2000). Vegetables take up and accumulate toxic metals in their edible and non-edible parts not only through the root system from the soil, but also through aerial deposition of contaminated dust from the air (Li et al., 2004). The uptake of metals by plants depends on soil properties and various physiologic-factors of the plant. These factors bring considerable uncertainties to estimating potential doses through oral intake compared to other exposure pathways such as soil ingestion and dust inhalation (McKone, 1994).

The objective of this study was to determine the extent of Pb and Cd contamination in selected vegetables and associated soils of five growing areas of Khyber Pakhtunkhwa (KP) Province, Pakistan. Vegetables production is a significant profession in the selected parts of KP, Pakistan. Nevertheless, there has been to date no principal study of Pb and Cd in food crops and agricultural lands in this part of the KP. It is, therefore, critical to examine Pb and Cd accumulation in vegetable species and farmlands as well as their possible health risk. Thus, we conducted a detailed investigation of Pb and Cd concentrations in soils and vegetables grown in the study site, that may have been impacted by numerous sources, including agro-chemical fertilizers, pesticides, herbicides, sewage sludge, and waste-water irrigation.

2.0. Materials and Methods

2.1. Study site description

The proposed study sites comprise five selected vegetable growing areas, Hangu, Kohat, Bannu, Lakki Marwat and Dera Ismail Khan (DI Khan), of KP Province, Pakistan, which lies between 31° 15' 00" to 33° 35' 00" north-latitude and 70° 11' 00" to 72° 01' 00" east-longitude with total population of 1343020. The total land under cultivation is approximately 5225.71 km2, with planted with various vegetables and other food crops (Rehman et al., 2016; Waqas et al., 2014). Wheat, barley, maize, rice, sugarcane, cucumber, bitter melon, ridge gourd, onion, garlic, mint, lady finger, squash-melon, lettuce, spinach, pea, pumpkin, cabbage, cauliflower, potato, bringal, turnips, pepper, carrot, radish, tomato, yam, perslane, Chinese onion, and coriander are the most important food-crops grown in the study area. The rivers Indus and Kurram, and their tributaries, as well as tube-wells are the chief sources of irrigation. The growers sell their vegetables in the local markets and also supply to other regions of the country as a source of income generation (District Census Report (DCR), 1998a,1998b,1998c,1998d,1998e).

2.2. Sampling and pre-treatment

The sampling sites were located in the selected areas of KP, Pakistan as shown in Fig. 1. Soil samples were collected from boreholes 20 cm deep and 10 cm in diameter, drilled with a stainless-steel-auger. Each soil sample comprised 5 sub-samples collected at distances of about 10 mfrom each other in different directionsusing the quartile method, followed by bulking together tocreate a composite sample of 1 kg (Wu et al., 2010). The samples were placed into sealed plastic bags and taken to the laboratory. After air drying, the soil samples were mechanically ground and passed through a sieve of 2-mm mesh, and preserved in clean zip sealed plastic bags for further chemical analyses. Basic soil properties such as pH, electrical conductivity, total carbon, nitrogen and sulfur, dissolved organic carbon (DOC), soil texture, and bulk density are presented in our previous studies (Waqas et al., 2014; Rehman et al., 2016).

An external file that holds a picture, illustration, etc.  Object name is nihms-846074-f0001.jpg

Location map of the study area showing sampling sites in the selected region of KP, Pakistan

Vegetables grown in the study area (Table 1) were harvested from the same cultivated fields from where the soil samples were collected. The vegetable samples were packed into clean polyethylene bags and transported to the laboratory of Department of Environmental Sciences, University of Peshawar, Pakistan. The collected samples were washed with double deionized water to eliminate air borne pollutants, dirt, and dust particles, then the edible parts of the samples were dried in the oven at 65° for 72 h until constant weight. The dried vegetable samples were powdered using an electric grinder and stored in labeled paper bags for acid extraction and heavy metal analyses.

Table 1

Description (botanical and vernacular names) of vegetables grown in the study area.

English name Vernacular name Botanical name Abbreviations used
Bitter melon Kareela Momordica charantia M. charantia
Ridge gourd Tori Luffa acutangula L. acutangula
Tomato Tamator Solanum lycopersicum S. lycopersicum
Lady finger Bindhi Aesculantus malvaceae A.Malvaceae
Cucumber Keera Cucumis sativus C. sativus
Brinjal Bangan Solanum melongena S. melongena
Squash-melon Tinda Praecitrullus fistulosus P.fistulosus
Cauliflower Gobhi Brassica oleracea B. oleracea
Pumpkin Kadhu Benincasa hispada B. hispada
Pea Matter Pisum sativum P. sativum
Mint Podina Mentha arvensis M. arvensis
Lettuce Salad Lectuca sativa L. sativa
Spinach Paalak Beta vulgaris B. vulgaris
Cabbage Band gobhi Brassica olemcea B. olemcea
Coriander Dannya Coriandrum sativum C. sativum
Chinese onion Gandana Allium chinense A. chinense
Perslane Kolfeka sag Portulaca oleracea P.oleracea
Onion Pyaaz Allium cepa A. cepa
Garlic Oga Allium sativum A. sativum
Radish Molli Raphanus sativus R. sativus
Turnip Shalgham Brassica rapa B. rapa
Carrot Gajer Daucus carota D. carota
Yam Kachalu Colocasia esculanta C. esculanta
Potato Aaloo Solanum tuberosum S. tuberosum

2.3. Extraction

The fine powdered soil samples (1 g) were placed in a typhlon beaker, adding 15 mL of aqua regia (HNO3: HCl at 1:3 ratio) following the method adopted by Khan et al. (2010). The soil samples were retained overnight and then next morning heated slowly on a hot plate in a fume hood, until near to dryness. After adding HClO4 (5 ml), the samples were heated again gradually until near to dryness. Diluted acid solution was added and filtered through watt-man filter paper No. 42 into volumetric flasks (50 ml). The filtrates were diluted to 50ml with double deionized water and stored for analysis.

Dried and powdered vegetable samples (2 g) were weighed in Pyrex beakers and 10ml of high grade HNO3 was added and placed overnight at room temperature (Khan et al., 2010). The samples were digested till near to dryness at 190°C for 1.5 h on a hot plate. After cooling, 5ml HClO4 was added and the samples were heated slowly until the completion of digestion process. The samples were filtered, followed by the dilution with double deionized water to required volume (50 ml) in volumetric flasks rinsed with acidified water. The samples were sealed and stored at room temperature for further analyses.

2.4. Analytical procedures

The concentrations of Pb and Cd in soils and vegetable samples were analyzed using Atomic Absorption Spectrophotometry (AAS-700-Perkin-Elmer). Analytical-grade chemicals with a high-purity of 99.9% (Merck Darmstadt, Germany) were used for sample preparation and analysis. Pb and Cd standard solution was prepared by diluting its 1000 mg L−1 specified standard solutions (F. Kamica Busch, Switzerland). The blank reagents and standard reference soil (GBW-07406 (GSS-6) and plant (GBW-07602 (GSV-1) materials purchased from National Research Center for Certified Reference-Materials, China, were used to verify the accuracy and precision of digestion. The recovery of Cd (101±4.5%) and Pb (93±7.3%) was satisfactory from these reference materials. For data quality assurance, each digested sample was analyzed in triplicate under standard conditions within the confidence level of 95%. All analyses were accomplished in the Centralized-Resource Laboratory (CRL), University of Peshawar, Pakistan.

2.5. Data analysis

The bioconcentration factor (BCF) of metals from soil to plant was computed as the ratio of metal concentration in edible parts of vegetables with the metal concentration in soils. The BCF was determined by the following equation (1) (Cui et al., 2005):

BCF = C ( vegetable ) C ( soil )

(1)

where Cvegetable and Csoil represent the metal concentrations in the extracts of vegetables and soils on a dry weight basis, respectively.

The average daily intake of metals (DIMs) was calculated according to the following formula (2) as used by Khan et al. (2008, 2010) and Jan et al. (2010):

where Cm, Cf, IRveg, and Bw represent the metal concentrations in vegetables (mgkg−1), conversion factor (0.085) for conversion of fresh to dry weight vegetables (Jan et al., 2010), ingestion rate of vegetable, and average body weight, respectively. The average daily ingestion rate of food-crops for adults (both male and female) and child were considered to be 0.345 and 0.232 kg-person−1-day−1, respectively (Khan et al., 2008, 2010), while the average adult and child body weights were considered as 73 kg and 32.7 kg, respectively (Jan et al., 2010).

To estimate the chronic health risk, the health risk index (HRI) for Pb and Cd through contaminated food-crop consumption was determined using the following formula (3) (Khan et al., 2008; Jan et al., 2010):

Here, HRI, DIM, and RfD, represent the human health risk index, daily intake of metal, and reference dose of metal, respectively. According to US-EPA (2005) database the oral toxicity reference dose value (RfD) for Pb and Cd is 3.50E-03 and 5.0E-04 mgkg−1day−1, respectively, (US-EPA, 2005; Shah et al., 2012). The exposed population is considered to experience no significant risk when HRI < 1 (Khan et al., 2008; Muhammad et al., 2011).

The data were statistically analyzed using Microsoft Excel (2010) computer packages. The measurements were expressed in term of mean and standard deviation. The location map of the study area was prepared using Arc-Geographic Information System (Arc-GIS).

3. Results and Discussion

3.1. Pb and Cd concentrations in soil samples

The concentrations of Pb in the soil samples collected from all study areas are summarized in Fig. 2, while the detail is given in Supporting Information (SI) (Table S1). The Pb concentrations varied from 12.2 to 13.9 mg kg−1. The trend of mean Pb concentration in soils for the five locations were DI Khan >Kohat>Bannu>Hangu>Lakki Marwat. Pb concentrations for all samples are below the safe maximum allowable limits (MAL 350 mg kg−1) established by State Environmental-Protection Administration, China (SEPA), for soils in China. These limits are used as a reference as no such values have been established in Pakistan. The Pb concentrations in soils of this study were lower than those reported in the previous studies undertaken by Jie et al. (2009) in contaminated vegetable soils from the Pb/Zn mining and smelting areas in Hunan Province of China, Khan et al. (2010), in Gilgit northern Pakistan; Lu et al. (2011), Douay et al. (2013), in northern France; Zheng et al. (2013), near the edge of the Lake Eyre Basin in the semi-arid region of continental Australia; Attanayake et al. (2014), in urban community garden located in the Washington Wheatley neighborhood in Kansas City, Missouri; and greater than the results of the previous studies at Ghazipur roadside, Bangladesh (Naser et al., 2012).

An external file that holds a picture, illustration, etc.  Object name is nihms-846074-f0002.jpg

Comparison of Pb and Cd concentrations (mg kg−1) in the agricultural soils collected from the study area. The error bars indicate the standard deviations.

The results presented in Fig. 2 indicate that the mean concentration of Cd in soils collected from the five study areas varied from 1.6 to 2.3 mg kg−1. Further detail is given in SI (Table S2). The lowest Cd concentration (0.15 mg kg−1) was observed in the soils of Hangu sub-site, while the highest (3.43 mg kg−1) was in soils of DI Khan area. The Cd concentrations were higher than its MAL (0.6 mg kg−1) set by SEPA (1995) for soil in China, and higher than the MAL (1.5 mg kg−1) set by the European Union (EU) (2000). The Cd concentrations in soils were higher than those reported by Gaw et al. (2008) and Khan et al. (2010) and lower than those investigated by Shah et al. (2010), Abanuz, (2011) and Li et al. (2005) in China. The highest contents of Cd in the farm-field soils may be due to the extensive use of various agro-chemicals such as phosphate fertilizers, manures, and pesticides (Alam et al., 2003). Sabiha-Javied et al. (2009) reported that phosphate rock used for production of fertilizers can be contaminated with heavy metals such as Cd and Pb and acts as sources of heavy metal pollution of air, water, soil and food chain.

3.2. Pb and Cd concentrations in vegetables

The Pb concentrations in edible parts of various vegetable species collected from the study area are presented in Table 2 and Table S3. According to FAO/WHO (2001), the MAL of Pb is 0.3 mg kg−1 for fruits and vegetables, on a dry-weight-basis. Slight variations were observed in the concentrations of Pb in different vegetable species collected from the selected study area. The mean Pb concentration ranged between 1.8 to 11 mg kg−1, all of which exceed the MAL of FAO/WHO. The sequence of mean Pb concentration in the selected vegetable species was in the order of P. oleracea>L. sativa>S. lycopersicum>B. hispada>M. arvensis =B. olemcea>L. acutangula>C. sativum>A. chinense>S. melongena>A. cepa>P. fistulous>A. Malvaceae>C. sativus>B. vulgaris>S. tuberosum>B. rapa>B. oleracea>M. charantia>C. esculanta>D. carota>A. sativum>R. sativus>P. sativum. The highest concentration of Pb was observed in samples of P. oleracea (leafy vegetable), while the lowest was observed in A. sativum (root vegetable). The results revealed that Pb concentration was higher than those reported by Mohajer et al. (2012), in Isfahan Province, Iran, and lower than the findings of Tewari and Pande (2013) in Tarai region of Kumaun north-west Himalaya, India.

Table 2

DIM and HRI for Pb and Cd via consumption of different vegetables grown in the study area. The bold values indicate the concentrations exceeded the safe limit.

DIM
HRI
Species Individual Pb Cd Pb Cd
M. charantia Adult 7.33E-04 3.94E-04 2.09E-01 7.88E-01
Children 1.10E-03 5.92E-04 3.14E-01 1.18E+00
L. acutangula Adult 2.43E-03 4.34E-04 6.93E-01 8.69E-01
Children 3.64E-03 6.52E-04 1.04E+00 1.30E+00
S. lycopersicum Adult 3.08E-03 4.83E-04 8.81E-01 9.66E-01
Children 4.63E-03 7.25E-04 1.32E+00 1.45E+00
A. Malvaceae Adult 1.69E-03 4.26E-04 4.82E-01 8.53E-01
Children 2.53E-03 6.40E-04 7.24E-01 1.28E+00
C. sativus Adult 1.62E-03 4.79E-04 4.62E-01 9.57E-01
Children 2.43E-03 7.19E-04 6.94E-01 1.44E+00
S. melongena Adult 1.87E-03 3.26E-04 5.33E-01 6.51E-01
Children 2.80E-03 4.89E-04 8.01E-01 9.78E-01
P. fistulosus Adult 1.85E-03 4.84E-04 5.28E-01 9.68E-01
Children 2.77E-03 7.27E-04 7.93E-01 1.45E+00
B. oleracea Adult 1.25E-03 2.26E-04 3.57E-01 4.53E-01
Children 1.87E-03 3.40E-04 5.35E-01 6.80E-01
B. hispada Adult 3.17E-03 4.99E-04 9.05E-01 9.99E-01
Children 4.76E-03 7.50E-04 1.36E+00 1.50E+00
P. sativum Adult 5.49E-04 5.19E-05 1.57E-01 1.04E-01
Children 8.24E-04 7.79E-05 2.35E-01 1.56E-01
M. arvensis Adult 1.63E-03 1.55E-04 4.67E-01 3.09E-01
Children 2.45E-03 2.32E-04 7.01E-01 4.64E-01
L. sativa Adult 1.68E-03 1.99E-04 4.80E-01 3.98E-01
Children 2.52E-03 2.99E-04 7.20E-01 5.97E-01
B. vulgaris Adult 1.44E-03 2.82E-04 4.12E-01 5.63E-01
Children 2.16E-03 4.23E-04 6.18E-01 8.46E-01
B. olemcea Adult 1.39E-03 1.66E-04 3.96E-01 3.31E-01
Children 2.08E-03 2.49E-04 5.94E-01 4.98E-01
C. sativum Adult 1.37E-03 1.97E-04 3.92E-01 3.93E-01
Children 2.06E-03 2.95E-04 5.89E-01 5.90E-01
A. chinense Adult 2.20E-03 2.64E-04 6.28E-01 5.29E-01
Children 3.30E-03 3.97E-04 9.43E-01 7.94E-01
P. oleracea Adult 6.09E-04 4.12E-04 1.74E-01 8.24E-01
Children 9.15E-04 6.18E-04 2.61E-01 1.24E+00
A. cepa Adult 2.01E-03 2.54E-04 5.73E-01 5.09E-01
Children 3.01E-03 3.82E-04 8.60E-01 7.64E-01
A. sativum Adult 1.04E-03 1.60E-04 2.96E-01 3.19E-01
Children 1.55E-03 2.40E-04 4.44E-01 4.79E-01
R. sativus Adult 8.95E-04 2.02E-04 2.56E-01 4.04E-01
Children 1.34E-03 3.03E-04 3.84E-01 6.07E-01
B. rapa Adult 9.63E-04 2.31E-04 2.75E-01 4.62E-01
Children 1.45E-03 3.47E-04 4.13E-01 6.94E-01
D. carota Adult 1.10E-03 1.27E-04 3.15E-01 2.54E-01
Children 1.65E-03 1.91E-04 4.72E-01 3.82E-01
C. esculanta Adult 1.27E-03 3.41E-04 3.62E-01 6.83E-01
Children 1.90E-03 5.13E-04 5.43E-01 1.03E+00
S. tuberosum Adult 1.41E-03 2.98E-04 4.02E-01 5.96E-01
Children 2.11E-03 4.47E-04 6.03E-01 8.95E-01

The results of this study revealed that the concentrations of Cd in vegetable samples collected from the five aforementioned sites of the study were ranged from 0.2 to 1.6 mgkg−1. Cd concentrations for all vegetables, except P. sativum (0.12 mg kg−1), exceed the MAL (0.1-0.2 mg kg−1) set by SEPA, (2005). Divergence was detected in Cd accumulation in various plants species, which suggest that different vegetables have different Cd accumulation rates (Yang et al., 2009).

3.3. Bioconcentration factor (BCF)

Fig. 3 summarizes the values of BCF for Pb from soil to the edible tissues of various selected vegetables collected from the study sites. Being the key components of human exposure, BCF is essential which reflects a high accumulating potential of the metal uptake by vegetables from the soils on which they are grown. Highest BCF (> 1) for Pb was observed in P. oleracea, having maximum capability to bioaccumulate Pb content in the tissues of its edible parts as compared to all other vegetables investigated for this study, while the smallest BCF was determined for P. sativum. Among the groups, the trend of BCF was in decreasing order of leafy > fruity > rooty, which shows that leafy vegetables accumulated greater concentrations of Pb as compared to other vegetables. The BCF for Cd was higher in leafy vegetables as compared to fruity and rooty food-crops, consistent with the Pb results (Fig. 3).

An external file that holds a picture, illustration, etc.  Object name is nihms-846074-f0003.jpg

Comparison of Pb and Cd concentrations (mg kg−1) in vegetables collected from the study area.

BCF values for Pb are higher than those observed by Khan et al. (2008), in Beijing China; Garg et al. (2014), in a semi-urbanized area of Haryana state, India, and lower than the findings described by Khan et al. (2010), in Gilgit northern Pakistan. The reported Cd BCF values were lower than those observed by Khan et al. (2010), in Gilgit, northern Pakistan and by Khan et al. (2013) in Swat District, northern Pakistan. This could be attributed to the variations in soil properties as well as differences in sources of contamination.

3.4. Daily intake of metals (DIM) and health risk index (HRI)

To assess the human health risk index of a toxin, it is mandatory to estimate the level of exposure by quantifying the routes of exposure of a contaminant to the target organisms. The exposure of toxic metals to humans occurs through several pathways including inhalation, food-chain, and dermal contact. The DIM and HRI of Pb and Cd were calculated for both adults and children to evaluate the potential human health risk in the study area due to ingestion of vegetables.

Table 2 summarizes the estimated values of DIM and HRI of Pb and Cd through the ingestion of selected food-crops in the entire study area. It is observed that the DIM values were relatively high through the consumption of various selected vegetables grown in the study area. However, all the values of DIM were observed to be less than one.

The highest intake of Pb was estimated for P. oleracea, while the lowest was for P. sativum for both adults and children. The calculated values of HRI for Pb and Cd through the ingestion of various vegetables grown in selected sites for both adults and children are also shown in Table 2. The results of this study indicate that the HRI values of Pb were < 1 for most of the vegetable species. However, HRI values that exceeded the safe limit (> 1) are calculated for P. oleracea for adults, and for L. acutangula, S. lycopersicum, B. hispada, M. arvensis, L. sativa, B. olemcea, P. oleracea for children. The HRI values for Pb of this study are consistent with the results reported by Singh et al. (2010).

The HRI of Cd was ranged from 0.1 to 1.3 for adults, while it was varied from 0.002 to 1.9 for children (Table 2). The results of Table 2 show that the Cd content was not within the acceptable limits (HRI >1) for several vegetables (US-EPA, 1999), specifically A. Malvaceae, C. esculanta, L. acutangula, M. charantia, P. fistulosus, P. oleracea, S. lycopersicum for children and B. hispada and P. fistulosus for adults. HRI values exceeding 1 were reported for both Pb and Cd for a few species, namely L. acutangula, S. lycopersicum, and P. oleracea for children.

4. Conclusion

The concentrations of Pb in all soils were below the MAL (350 mg kg−1) set by SEPA for soils. There were minimal differences in Pb concentration among all the soil samples of the study area. Conversely, Cd concentrations exceeded the MALs (0.6 mg kg−1) and (1.5 mg kg−1) set by SEPA (1995) for soils in China and EU (2000), respectively. Concentrations of Pb and Cd in the vegetables grown in the study area exceeded the MALs. The highest BCF was observed for leafy vegetables followed by fruity > rooty. The values of DIM for Pb and Cd in all the selected vegetables were below one. HRI values exceeded the safe limit (>1) were reported for several vegetables. Consumption of these vegetables poses a potential health risk to the local community.

Given the results of this study, it is recommended that the farmers of the study area should be informed about the proper use of fertilizers, pesticides, and herbicides and to test the soils of their agricultural fields prior to cultivation of vegetables. It is recommended that Government departments should formulate strategies for regular monitoring of toxic metal contamination of soils and food-crops to ensure food safety and to help to prevent health problems caused by ingestion of contaminated vegetables.

An external file that holds a picture, illustration, etc.  Object name is nihms-846074-f0004.jpg

Bioconcentration factor (BCF) of Pb and Cd for collected samples of vegetables grown in the study area

Supplementary Material

SI

Acknowledgements

The financial support for sampling and analysis was partly provided by the Directorate of Science and Technology, Khyber Pakhtunkhwa, Pakistan. The first author also acknowledges the Higher Education Commission, Islamabad, Pakistan for providing Indigenous PhD fellowship. The contribution of M.L. Brusseau and Marry K Amistadi was supported by the NIEHS Superfund Research Program (ES04940).

Footnotes

Conflict of Interest

The authors declare that there are no conflicts of interest.

References

  • Abanzun GY. Heavy metal contamination of surface soil around Gebze industrial area. Turkey, Microchem. J. 2011;99:82–92. [Google Scholar]
  • Alam MGM, Snow ET, Tanaka A. Arsenic and heavy metal concentration of vegetables grown in Samta village. Bangladesh. Sci. Total Environ. 2003;111:811–815. [PubMed] [Google Scholar]
  • Asfaw A, Sime M, Itanna F. Determining the extent of contamination of vegetables affected by tannery effluent in Ejersa area of East Shoa. Ethiopia. Intern. J. Sci. Resea. Public. 2013;3(5):1–7. [Google Scholar]
  • ATSDR (Agency for Toxic Substances and Disease Registry) Toxicological Profile for Lead. Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services. Public Health service. 1999:205–93-0606. [Google Scholar]
  • Attanayake CP, Hettiarachchi GM, Harms A, Presley D, Martin S, Pierzynski GM. Field evaluations on soil plant transfer of lead from an urban garden soil. J. Environ. Qual. 2014;43:475–487. [PubMed] [Google Scholar]
  • Auda AM, Ali ES. Cadmium and zinc toxicity effects on growth and mineral nutrients of carrot (daucus carota). Pak. J. Bot. 2010;42:341–351. [Google Scholar]
  • Cambra K, Martinez T, Urzelai A, Alonso E. Risk analysis of a farm area near a lead- and cadmium-contaminated industrial site. J. Soil Contam. 1999;8:527–540. [Google Scholar]
  • Cao S, Duan X, Zhao X, Chen Y, Wang B, Sun C, Zheng B, Wei F. Health risks of children's cumulative and aggregative exposure to metals and metalloids in a typical urban environment in China. Chemosphere. 2016;147:404–411. [PubMed] [Google Scholar]
  • Chen H, Teng Y, Lu S, Wang Y, Wu J, Wang J. Source apportionment and health risk assessment of trace metals in surface soils of Beijing metropolitan, China. Chemosphere. 2016;144:1002–1011. [PubMed] [Google Scholar]
  • Chen HM. Heavy metal contamination in soil-plant system. Sc. Press; Beijing China: 1996. pp. 32–36. [Google Scholar]
  • Cui YJ, Zhu YG, Zhai R, Huang Y, Qiu Y, Liang J. Exposure to metal mixtures and human health impacts in a contaminated area in Nanning. China. Environ. Inter. 2005;31:784–790. [PubMed] [Google Scholar]
  • Cui YJ, Zhu YG, Zhai RH, Chen DY, Huang YZ, Qui Y, Liang JZ. Transfer of metals from near a smelter in Nanning. China. Environ. Int. 2004;30:785–791. [PubMed] [Google Scholar]
  • Davies DJA, Thornton I, Watt JM, Culbard EB, Harvey PG, Delves HT, Sherlock JC, Smart GA, Thomas, A. JF, M.J. Quinn. Lead intake and blood lead in two-year-old U.K. urban children. Sci. Total Environ. 1990;90:13–29. [PubMed] [Google Scholar]
  • DCR (District Census Report of Bannu) Statistic Division. Ministry of Economic Affairs and Statistic Government of Pakistan; 1998a. Population Census Organization; pp. 1–17. [Google Scholar]
  • DCR (District Census Report of Dera Ismail Khan) Population Census Organization . Ministry of Economic Affairs and Statistic, Government of Pakistan; 1998b. Statistic Division; pp. 1–17. [Google Scholar]
  • DCR (District Census Report of Hangu ) Population Census Organization, Statistic Division. Ministry of Economic Affairs and Statistic, Government of Pakistan; 1998d. pp. 1–17. [Google Scholar]
  • DCR (District Census Report of Kohat ) Population Census Organization, Statistic Division. Ministry of Economic Affairs and Statistic Government of Pakistan; 1998c. pp. 1–17. [Google Scholar]
  • DCR (District Census Report of Lakki Marwat ) Population Census Organization, Statistic Division. Ministry of Economic Affairs and Statistic Government of Pakistan; 1998e. pp. 1–17. [Google Scholar]
  • Douay F, Pelfrêne A, Pelfrêne J, Fourrier H, Richard A, Roussel H, Girondelot B. Assessment of potential health risk for inhabitants living near a former lead smelter. Part 1: metal concentrations in soils, agricultural crops, and homegrown vegetables. Environ. Monit. Assess. 2013;185:3665–3680. [PubMed] [Google Scholar]
  • Dudka S, Miller WP. Permissible concentrations of arsenic and lead in soils based on risk assessment. Water Air Soil Pollu. 1999;113:127–132. [Google Scholar]
  • European Union 2000:19. [Google Scholar] Working document on sludge, 3rd Draft, Brussels, 27 April 2000. ENV. E. 3/LM
  • FAO/WHO Food additives and contaminants. Codex Alimentarius Commission. Joint FAO/WHO Food Standards Program. 2001:1–289. ALI-NORM 01/12A. [Google Scholar]
  • FAO/WHO-CODEX [20 Aug. 2012]; Codex general standard for contaminants and toxins in food and feed: Codex standard. Revised 1995, 2006, 2008, 2009, amended 2010 . 1995 http://www.fao.org/fileadmin/user_upload/agns/pdf/CXS_193e.pdf.
  • Garg VK, Yadav P, Mor S, Singh B, Pulhani V. Heavy metals bio-concentration from soil to vegetables and assessment of health risk caused by their ingestion. Biol. Trace Elem. Res. 2014;157:256–265. [PubMed] [Google Scholar]
  • Goswami K, Gachhui R, Goswami I, Pal S. Synthetic color culprit in street food in Kolkata, India. J. Inst. Chem. (India) 2012;84:94–96. [Google Scholar]
  • Granero SD. Levels of metals in soils of Alcaa de Henares, Spain: human health risks. J. Environ. Intern. 2002:159–164. [PubMed] [Google Scholar]
  • Hansia M, Weidenhamer JD, Sinkkonen A. Plant growth responses to inorganic environmental contaminants are density-dependent: Experiments with copper sulfate, barley and lettuce. Environ. Pollu. 2014;184:443–448. [PubMed] [Google Scholar]
  • Hawley JK. Assessment of health risk from exposure to contaminated soil. Risk Anal. 1985;5:289–302. [PubMed] [Google Scholar]
  • Hiroaki I, Motoki I, Norie S, Ribeka T, Yoshio K, Shiro Y. Dietary cadmium intake and breast cancer risk in Japanese women: a case-control study. J. Hazard Mater. 2013 http://dx.doi.org/10.1016/j.jhazmat.
  • Hough RL, Young SD, Crout NM. Modeling of Cd, Cu, Ni, Pb and Zn uptake by winter wheat and forage maize from a sewage disposal farm J. Soil Use Manag. 2003;19(1):19–27. [Google Scholar]
  • Jan FA, Ishaq M, Khan S, Ihsanullah I, Ahmad I, Shakirullah M. 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. Mater. 2010;179:612–62. [PubMed] [Google Scholar]
  • Jarup L. Hazards of heavy metals concentration. Br. Med. Bull. 2003;68:166–183. [Google Scholar]
  • Jie S, Zhao-hui G, Xi-yuan X, Xu-feng M, Feng-yong W. Environmental availability and profile characteristics of arsenic, cadmium, lead and zinc in metal-contaminated vegetable soils. Trans. Nonferrous Met. Soc. China. 2009;19:765–772. [Google Scholar]
  • Jun-Yu H, Yan-Fang R, Cheng Z, De-An J. Effects of cadmium stress on seed germination, seedling growth and seed amylase activities in rice (Oryza sativa). Rice Sci. 2008;15:319–325. [Google Scholar]
  • Kauppi S, Romantschuk R, Strömmer R, Sinkkonen A. Natural attenuation is enhanced in previously contaminated and coniferous forest soils. Environ. Sci. Pollut. Res. 2012;19:53–63. [PubMed] [Google Scholar]
  • Khan A, Khan S, Alam M, Khan MA, Aamir M, Qamar Z, Rehman ZU, Perveen S. Toxic metal interactions affect the bioaccumulation and dietary intake of macro- and micro-nutrients Chemosphere. 2016;146:121–128. [PubMed] [Google Scholar]
  • Khan K, Lu Y, Khan H, Ishtiaq M, Khan S, Waqas M, Wei L, Wang T. Heavy metals in agricultural soils and crops and human health risks in Swat District, northern Pakistan. Food Chem. Toxicol. 2013;58:449–458. [PubMed] [Google Scholar]
  • Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 2008;152:686–692. [PubMed] [Google Scholar]
  • Khan S, Rehman S, Khan AZ, Khan MA, Shah MT. Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan. Ecotoxicol. Environ. Saf. 2010;73:1820–1827. [PubMed] [Google Scholar]
  • Lanphear BP, Roghmann KJ. Pathways of lead exposure in urban children. Environ. Res. 1997;74:67–73. [PubMed] [Google Scholar]
  • Li J, Zhu Y, Naidu R. Risk assessment of heavy metals contaminated soils in the vicinity of a lead/zinc mine in Shaoxing, Zhejiang, China. J. Environ. Sci. 2005;17(6):881–885. [PubMed] [Google Scholar]
  • Li X, Lee SL, Wong SC, Shi W, Thornton I. The study of metal contamination in urban soils of Hong Kong using a GIS-based approach. Environ. Pollut. 2004;129:113–124. [PubMed] [Google Scholar]
  • Li XD, Hua RM, Yue YM. Evaluation on contamination of Cr, Pb, Cd and Cu in vegetables of Hefei region China. J. Agr. Environ. Sci. 2004;31(2):143–147. [Google Scholar]
  • Liu X, Song Q, Tang Y, Li W, Xu J, Wu J, Wang F, Brookes PC. Human health risk assessment of heavy metals in soil-vegetable system: A multi-medium analysis. Sci. Total Environ. 2013:530–540. [PubMed] [Google Scholar]
  • Lu Y, Yin W, Huang L, Zhang G, Zhao Y. Assessment of bioaccessibility and exposure risk of arsenic and lead in urban soils of Guangzhou city, China. Environ. Geochem. Health. 2011;33:93–102. [PubMed] [Google Scholar]
  • Martinez-Sanchez MJ, Martinez-Lopez S, Garcia-Lorenzo ML, Martinez-Martinez LB, Perez-Sirvent C. Evaluation of arsenic in soils and plant uptake using various chemical extraction methods in soils affected by old mining activities. Geoderma. 2011;160:535–541. [Google Scholar]
  • Mohajer R, Salehi MH, Mohammadi J. Accumulation of cadmium and lead in soils and vegetables of Lenjanat Region in Isfahan Province, Iran. Int. J. Agron. Plant. Prod. 2012;3(12):576–578. [Google Scholar]
  • Muhammad S, Shah MT, Khan S. Health risk assessment of heavy metals and their source apportionment in drinking water of Kohistan region, northern Pakistan. Microchem. J. 2011;98:334–343. [Google Scholar]
  • Muller M, Anke M. Distribution of cadmium in the food chain (soil-plant-human) of a cadmium exposed area and the health risks of the general population. Sci. Total. Environ. 1994;156:151–158. [PubMed] [Google Scholar]
  • Naser HM, Sultana S, Gomes R, Noor SN. Heavy metal pollution of soil and vegetable grown near road side at Ghazipur, Bangladesh. J. oAgr. Res. 2012;37(1):9–17. [Google Scholar]
  • Naz A, Khan S, Qasim M, Khalid S, Muhammad S. Metals toxicity and its bioaccumulation in purslane seedlings grown in controlled environment. Nat. Environ. 2013;5(5):573–579. [Google Scholar]
  • Nielson FH, Robinson RK, Sadler KJ. Trace elements. In: Macrae, editor. Ency. Fd. Sc. Fd. Tech. Nutr. Academic Press; London: 1997. pp. 4593–4600. [Google Scholar]
  • Oliveira LM, Lena QM, Jorge AG, Luiz RG, Jason TL. Effects of arsenate, chromate and sulfate on arsenic and chromium uptake and translocation by arsenic hyper-accumulator Pterisvittata L. Environ. Pollu. 2014;184:187–192. [PubMed] [Google Scholar]
  • Pan L, Ma J, Wang XL, Hou H. Heavy metals in soils from a typical county in Shanxi Province, China: Levels, sources and spatial distribution. Chemosphere. 2016;148:248–254. [PubMed] [Google Scholar]
  • Qin F, Chen W. Lead and copper levels in tea samples marketed in Beijing, China. Bull. Environ. Contam. Toxicol. 2010;78:128–131. [PubMed] [Google Scholar]
  • Rehman K, Ashraf S, Rashid U, Ibrahim M, Hina S, Iftikhar T, Ramzan S. Comparison of proximate and heavy metal contents of vegetables grown with fresh and wastewater. Pak. J. Bot. 2013;45(2):391–400. [Google Scholar]
  • Rehman Zu., Khan S, Qin K, Brusseau ML, Shah MT, Din I. Quantification of inorganic arsenic exposure and cancer risk via consumption of vegetables in southern selected districts of Pakistan. Sci. Total Environ. 2016;550:321–329. [PMC free article] [PubMed] [Google Scholar]
  • Robson TC, Braungardt CB, Rieuwerts J, Worsfold P. Cadmium contamination of agricultural soils and crops resulting from sphalerite weathering. Environ. Poll. 2014;184:283–289. [PubMed] [Google Scholar]
  • Sabiha-Javied, Mehmood T, Chaudhry MM, Tufail M, Irfan N. Heavymetalpollutionfromphosphaterockusedfortheproductionoffertilizer in Pakistan. Microchem. J. 2009;91:94–99. [Google Scholar]
  • SEPA . State Environmental Protection Administration. China. GB: 1995. Environmental Quality Standards for Soils. pp. 15618–1995. [Google Scholar]
  • SEPA . State Environmental Protection Administration. China, Gb: 2005. The Limits of Pollutants in Food. pp. 2762–2005. [Google Scholar]
  • Shah MT, Ara J, Muhammad S, Khan S, Tariq S. Health risk assessment via surface water and sub-surface water consumption in the mafic and ultramafic terrain, Mohmand agency, northern Pakistan. J. Geochem. Explor. 2012;118:60–67. [Google Scholar]
  • Shah MT, Begum S, Khan S. Pedo and biogeochemical studies of mafic and ultramafic rocks in the Mingora and Kabal areas Swat, Pakistan. Environ. Earth. Sci. 2010;60:1091–1102. [Google Scholar]
  • Shaheen N, Irfan NM, Khan IN, Islam S, Islam MS, Ahmed MK. Presence of heavy metals in fruits and vegetables: Health risk implications in Bangladesh. Chemosphere. 2016;152:431–438. [PubMed] [Google Scholar]
  • Shute T, Macfie SM. Cadmium and zinc accumulation in soybean: A threat to food safety? Sci. Total Environ. 2006;371:63–73. [PubMed] [Google Scholar]
  • Sinkkonen A, Simpanen S, Romantschuk R. Plaza G, editor. An evolutionary perspective to the stimulation of bacterial activity in contaminated soil. Trends in bioremediation and phytoremediation. Research Signpost Kerala India. 2010;8:73–80. [Google Scholar]
  • Smolders E, Mertens J. Cadmium. In: Alloway BJ, editor. Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. springer, dordrecht. Nederlands: 2013. pp. 283–311. [Google Scholar]
  • Sridhar BM, Han FX, Diehl SV, Monts DL, Su Y. Effect of phyto-accumulation of arsenic and chromium on structural and ultra-structural changes of brake fern (Pteris vittata). Braz. Soc. Plant Physiol. 2011;23:285–293. [Google Scholar]
  • Steenland K, Boffetta P. Lead and cancer in humans: where are we now? Am. J. Ind. Med. 2000;38:295–299. [PubMed] [Google Scholar]
  • Tandi NK, Nyamangara J, Bangira C. Environmental and potential health effects of growing leafy vegetables on soil irrigated using sewage and effluent: a case of Zn and Cu. J. Environ. Sci. Health. 2004;39:461–471. [PubMed] [Google Scholar]
  • Tewari G, Pande C. Health risk assessment of heavy metals in seasonal vegetables from north-west Himalaya. Afr. J. of Agric. Res. 2013;8(23):3019–3024. [Google Scholar]
  • Thuy HTT, Tobschall HJ, An PV. Distribution of heavy metals in urban soils-A case study of Danang-Hoian area (vietnam). Environ. Geogr. 2000;39:603–610. [Google Scholar]
  • Todd GC. Vegetables grown in mine wastes. Environ. Toxicol. Chem. 1996;19(3):600–607. [Google Scholar]
  • Turkdogan MK, Fevzi K, Kazim K, Ilyas T, Ismail U. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ. Toxicol. Pharmacol. 2003;13:175–179. [PubMed] [Google Scholar]
  • Umoru PE. Heavy metal content in vegetables from an irrigated farm land in Kaduna Metropolis, Nigeria. Intern. J. Adv. Res. Tech. 2013;2(1):1–11. [Google Scholar]
  • UNEP . Interim review of scientific information on cadmium. United Nations Environmental Programme; 2006. [Google Scholar]
  • United State, Environmental Protection Agency Region 9, Preliminary remediation goals. 2002 Dec; http://www.epa.gov/region09/waste/sfind/prg 2006 .
  • USEPA (United States Environmental Protection Agency) Guidelines for carcinogen risk assessment. Risk Assessment Forum; Washington, DC.: 2005. EPA/630/P-03/001F. [Google Scholar]
  • Waqas M, Khan S, Chao C, Shamshad I, Qamar Z, Khan K. Quantification of PAHs and health risk via ingestion of vegetable in Khyber Pakhtunkhwa Province, Pakistan. Sci. Total Environ. 2014;497-498:448–458. [PubMed] [Google Scholar]
  • Weldemariam MM, Kahsay AW. Heavy metal (Pb, Cd, Zn, Cu, Cr and Fe) content in Almeda Textile Industry Sludge, Northern Tigrai, Ethiopia. Intern. J. Sci. Res. Pub. 2014;4(1):1–5. [Google Scholar]
  • Wong CS, Li XD, Zhang G, Qi SH, Peng XZ. Atmospheric depositions of heavy metals in the Peari River Delta, China. Atmos. Environ. 2003;37:767–776. [Google Scholar]
  • Wu YG, Xu YN, Zhang JH, Hu SH. 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. 2010;20:688–694. [Google Scholar]
  • Xiao LL, Shu ZZ. Intra specific differences in effects of co-contamination of cadmium and arsenate on early seedling growth and metal uptake by wheat. J. Environ. Sci. 2007;191:1221–1227. [PubMed] [Google Scholar]
  • Yang Y, Zhang FS, Li HF, Jiang RF. Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils. J. Environ. Manag. 2009;90(2):1117–1122. [PubMed] [Google Scholar]
  • Yousaf B, Amina, Liu G, Wang R, Imtiaz M, Rizwan MS, Zia-ur-Rehman M, Qadir A, Si Y. The importance of evaluating metal exposure and predicting human health risks in urban-periurban environments influenced by emerging industry. Chemosphere. 2016;2016;150:79–89. [PubMed] [Google Scholar]
  • Zeng G, Liang J, Guo S, Shi L, Xiang L, Li X, Du C. Spatial analysis of human health risk associated with ingesting manganese in Huangxing Town, Middle China. Chemosphere. 2009;77(3):368–375. [PubMed] [Google Scholar]
  • Zheng J, Huynh T, Gasparon M, Jack N, Noller B. Human health risk assessment of lead from mining activities at semi-arid locations in the context of total lead exposure. Environ. Sci. Pollut. Res. 2013;20:8404–8416. [PubMed] [Google Scholar]
  • Zhi LF, Wei PS, Shi RG, Zhang T.l., Zhao YJ, Zhou QX. Cadmium accumulation in soil and crops and pollution risks to human health under different land use types. J. Resour. Sci. 2008;30(12):1904–1909. [Google Scholar]
  • Zurera G, Estrada B, Rincon F, Poza R. Lead and cadmium contamination levels in the edible vegetables. Bull. Environ. Cont. Toxicol. 1987;38:805–812. [PubMed] [Google Scholar]
  • Zwarum AA. Tolerance of Escherichia Coli to Cd. Journal of Environmental Quality. 1973;2:353–355. [Google Scholar]

Is Cadmium Plated Metal Hazardous Around A Vegetable Garden?

Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322861/

Posted by: maserneash1938.blogspot.com

0 Response to "Is Cadmium Plated Metal Hazardous Around A Vegetable Garden?"

Post a Comment

Iklan Atas Artikel

Iklan Tengah Artikel 1

Iklan Tengah Artikel 2

Iklan Bawah Artikel