DSpace at VNU: Accumulation and potential health risks of cadmium, lead and arsenic in vegetables grown near mining sites in Northern Vietnam

DSpace at VNU: Accumulation and potential health risks of cadmium, lead and arsenic in vegetables grown near mining site...

Accumulation and potential health risks of cadmium, lead

and arsenic in vegetables grown near mining sites in Northern

Vietnam

Anh T K Bui&Ha T H Nguyen&Minh N Nguyen&

Tuyet-Hanh T Tran&Toan V Vu&Chuyen H Nguyen&

Heather L Reynolds

Received: 17 February 2016 / Accepted: 9 August 2016

# Springer International Publishing Switzerland 2016

Abstract The effect of environmental pollution on the

safety of vegetable crops is a serious global public

health issue This study was conducted to assess heavy

metal concentrations in soil, irrigation water, and 21

local vegetable species collected from four sites near

mining activities and one control site in Northern

Viet-nam Soils from vegetable fields in the mining areas

were contaminated with cadmium (Cd), lead (Pb), and

arsenic (As), while irrigation water was contaminated

with Pb Average concentrations of Pb and As in fresh

vegetable samples collected at the four mining sites

exceeded maximum levels (MLs) set by international

food standards for Pb (70.6 % of vegetable samples) and

As (44.1 % of vegetable samples), while average Cd

concentrations in vegetables at all sites were below the

MLs of 0.2 The average total target hazard quotient (TTHQ) across all vegetable species sampled was higher than the safety threshold of 1.0, indicating a health risk Based on the weight of evidence, we find that cultivation of vegetables in the studied mining sites

is an important risk contributor for local residents’ health

Keywords Heavy metal Vegetable Mining site Health risk Northern Vietnam

Introduction

The toxicities of heavy metals such as cadmium (Cd), lead (Pb), and arsenic (As) are recognized as major human health risks worldwide (Krejpcio et al 2005;

Hu et al.2013; Chang et al.2014) Cadmium exposure has been linked to lung and prostate cancers (Fraser

et al.2013; Oteef et al.2015) in addition to kidney and bone diseases (Järup and Åkesson 2009; Oteef et al

2015) Lead impairs the hematological, cardiovascular, and neurological systems (Jooste et al.2015; Oteef et al

2015) Based on evidence of kidney and brain tumors in animal studies, lead is also likely to be a human carcin-ogen (U.S 2003) Arsenic compounds are associated with many forms of skin, lung, bladder, kidney, and liver cancers (U.S 2003) Food consumption is the main source of human exposure to Cd and Pb which provides

up to 80–90 % of daily doses (Krejpcio et al 2005) Vegetables may account for substantial fractions of total exposures to Cd, Pb, and As, since vegetables are an

DOI 10.1007/s10661-016-5535-5

Institute of Environmental Technology, Vietnam Academy of

Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam

e-mail: buianh7811@gmail.com

VNU University of Science, Vietnam National University, 334

Nguyen Trai, Hanoi, Vietnam

Hanoi School of Public Health, Environmental Health, Hanoi,,

Vietnam

T V Vu

Thuyloi University, 175 Tay Son Street, Hanoi, Vietnam

H L Reynolds

Department of Biology, Indiana University, Bloomington, IN

47405, USA

important part of the human diet and vegetable crops

can uptake heavy metals from contaminated

environ-ments (Hu et al.2013; Chang et al.2014)

Mining and smelting activities have released heavy

metals to the surrounding environment (Navarro et al

2008; Zhuang et al.2009) Vietnam has a total of 73 Pb–

Zn mines, distributed mainly in the northern

mountain-ous provinces including Bac Kan, Ha Giang, Tuyen

Quang, and Thai Nguyen (DREBK2012)

Concentra-tion of Cd, Pb, and As is very high in soil and water

affected by Pb–Zn mining activities in Thai Nguyen and

Bac Kan provinces (Bui et al 2011; Ha et al 2011)

Vegetables were reported to accumulate high

concentra-tions of heavy metals if they grew on

mining-contaminated soil (Hu et al.2013) For example, leafy

vegetables can accumulate substantial amounts of heavy

metals in their leaves (Kananke et al.2014) There are,

however, still a limited number of studies on heavy

metal contents in vegetables in Vietnam (Ngo2007)

Maximum permitted levels (MLs) for contaminants

and toxins in foods are specified by international food

standards (Codex2014; Dijk et al.2015; Oteef et al

2015) Vietnam’s standards for Cd, Pb, and As

contam-ination in food follow international standards (QCVN

8.2-BYT2011) Additionally, the target hazard quotient

(THQ) developed by USEPA (1989) has been used to

evaluate potential non-cancer health risks associated

with long-term exposure to chemical pollutants in

food-stuffs (Chien et al.2002; Hu et al.2013) The aims of

this study were (1) to determine the concentrations of

Cd, Pb, and As in leafy vegetables cultivated around

several mining sites in Northern Vietnam and assess

potential health risks to the exposed local people and

(2) to provide a comparison of MLs versus the THQ in

assessing heavy metal safety concerns in vegetable

crops

Materials and methods

Study area

A monitoring program for vegetable metal

contamina-tion was set up in Cho Don district, BacKan province in

North Vietnam (Fig.1) In this area, mining activities

have been operating since the eighteenth century (Ha

et al.2011), involving wastewater release into the

sur-rounding environment without treatment (DREBK

2012) Use of potentially contaminated stream water

may enhance the heavy metal concentrations in vegeta-bles produced near the mining areas Vegetable tissue and associated soil samples were taken from crop fields cultivated by local households at four streamside sites near Pb–Zn mines: site 1 (105° 34′ 17″ E, 22° 8′ 58″ N), site 2 (105° 34′ 13″ E, 22° 8′ 50″ N), site 3 (105° 34′ 22″

E, 22° 8′ 22″ N), and site 4 (105° 34′ 22″ E, 22° 8′ 18″ N) and from one upstream control site (Una, 105° 34′

26″ E, 22° 9′ 58″ N; Fig.1)

Sampling and analysis

Vegetable, soil, and water samples were collected from February to April of 2015 A total of 21 vegetable species were sampled across the five sites, with six replicates per species per site (sites differed in which species were grown; site 1: 8 species, site 2: 12 species, site 3: 7 species, and site 4: 7 species, yielding 228 total samples) All the collected samples were leafy vegeta-bles (except string beans) Plant samples were collected approximately 40 days after sowing

Approximately 200 g of soil was collected around the sampled plants at the five study sites (90 samples total; 9 samples per site × 2 times × 5 sites) The collection steps for soil samples followed Chang et al (2014): Soil samples were taken from the surface layer (0–20 cm), using a bamboo shovel to uproot each vegetable plant and gently shake soil from the roots All samples were sealed in polyethylene bags and were transported to the Institute of Environmental Technology within 6 h of collection Fifty water samples were collected near the mine area, mine drainage, and at five streamside loca-tions at each site using a PVC tube column sampler at depth of half meter from the water surface The samples

at each position were mixed in a plastic bucket, and a sample of 1 liter was contained in a polyethylene bottle Water samples were acidified with nitric acid to pH <2 after collecting and transferred on ice to the laboratory for analysis Ten milliliters of each sample was filtered through a 0.45-μm Whatman pore-size disposable cap-sule filter before elemental determination

Sample preparation and digestion methods for vege-tables followed Ha et al (2011); methods for soil followed Bui et al (2011) with some modifications The vegetable samples were washed with tap water to remove dust, rinsed with deionized water, and oven dried at 80 °C for 2 days The dried samples were ground into fine powder using a mortar mill After grinding, samples (200 mg per each) were digested with

0.4 ml H2O2(Merck, 30 %), 1 ml HF (Merck, 40 %),

and 2 ml HNO3(Merck, 65 %) using the Multiwave

PRO (Anton Paar) microwave The microwave was set

to 8 min ramping to 140 °C, then held at this

tempera-ture for 15 min Soil samples were oven dried at 80 °C

for 2 days, crushed to pass through a 1-mm sieve, and

stored at 4 °C in dark plastic bags until analysis Dried

samples (1 g ± 1 mg) were digested with HNO365 %

(2.35 ml) and HCl 37 % (7 ml) using the microwave as

described above After cooling to room temperature, in

both soil and vegetable samples, the content of the

vessel was transferred into acid-washed plastic bottles

diluted to 10 ml with ultra-pure water and analyzed for

elemental concentrations Soil pHKClwas measured on a

1:2 ratio of soil/KCl(1N)by Lab 850 pH meter (Schott

Instruments, Germany)

Total (inorganic + organic) heavy metal

concentra-tions in plant, soil, and water samples were measured

using an inductively coupled plasma-mass spectrometer

(ICP-MS, ELAN 9000, PerkinElmer, USA) The

accu-racy and precision in elemental analyses by ICP-MS

were assessed using reagent blanks and internal

stan-dards (Ha et al.2011) We used standard reference soil

material (NIST SRM 2587) from the National Institute

of Standard and Technology, USA, standard reference plant material (NIES CRM No 1) from the National Institute for Environmental Studies, Japan, and standard reference solutions of 1000 mg l−1for As, Pb, and Cd from Merck, Germany

Heavy metal concentrations of vegetables were de-termined on a dry weight (dw) basis and converted to a fresh weight (fw) basis for comparison with the MLs for contaminants and toxins in foods The water content and the ratio of fresh to dry weight (F/D) of vegetables were calculated by their biomass before and after oven drying (Table1) Dry to fresh weight conversions were made using the respective F/D factor for each vegetable sample

Bioconcentration factor and the target hazard quotient

The bioconcentration factor (BCF) is defined as the ratio of metal concentration in shoots to that in the soil (Bui et al 2011; Ha et al 2011; Chang et al

2014) The THQ is the ratio of the body intake dose

of a pollutant to the reference dose at which no non-cancer health risks are expected, and total target hazard quotient (TTHQ) is the sum of each Fig 1 Map showing the location of the sampling sites

individual THQ (Chang et al 2014; Hu et al.2013)

(Eq.1):

BW AT  RfD  10−3; TTHQ

where C is the mean concentration of a particular

metal in a fresh vegetable (mg kg−1); Mvegetableis the

daily local leaf vegetable intake by the local

resi-dents, including local and extraneous vegetables

(Chang et al 2014); EF is the exposure frequency;

ED is the exposure duration; BW is the average

body weight of a local resident; AT is the average

exposure time for non-carcinogens; RfD is the oral

reference dose (mg kg−1 per day); and 10−3 is the

unit conversion factor If THQ > 1, there is a

poten-tial risk associated with the pollutant (Chien et al

2002; Yang et al.2011; Chang et al 2014)

We calculated THQs and TTHQs using the heavy

metal concentrations measured in our study and

esti-mates for other parameters as follows: The daily local

leaf vegetable intake by the local residents (Mvegetable) was estimated to be 200 g; the ratio of local vegetable/ total vegetable consumption was set to 0.8; the ratio of leafy vegetable/local vegetable was set to 0.7 (DARD

2010); EF = 365 (days per year), and ED was set at

70 years (Hu et al.2013; Chang et al.2014) BW was estimated from the average weight of adults in Vietnam (50 kg; VMH2015) AT was set to 365 days × 70 years (Hu et al 2013; Chang et al 2014) RfD was set to

1 × 10−3, 3.6 × 10−3, and 3 × 10−4mg kg−1per day for

Cd, Pb, and As, respectively (USEPA2014)

Statistical analysis

Statistical analyses of data were performed using the SPSS 15.0 package for Windows Data normality and homogeneity of variance were tested using a Kolmogorov-Smirnow test Evaluation of significant differences among sampling sites were determined using one-way ANOVA followed by Tukey’s post hoc test

Table 1 The ratio of fresh weight

(F) and dry weight (D) for the

vegetable species studied (n = 3)

Results and discussion

Quality of measurements

Recovery values of 91–104 % were obtained for Cd, Pb,

and As (Table2) These recovery values compare

favor-ably to those reported in the literature for the analysis of

metals in plants (Ha et al.2011; Hu et al.2013; Oteef

et al.2015), in soil (Zhuang et al.2009; Ha et al.2011),

and in water (Arora et al.2008; Ha et al.2011)

Soil pH and heavy metals in soil and irrigation water

samples

Soil pH across sites was slightly alkaline and ranged

relatively narrowly between pH 7.5– 7.9 (Table3)

Av-erage concentrations of Cd, Pb, and As in soil samples

collected at the four sites near mining activities ranged

between 1.9– 3.8, 118.2 – 160.8, and 28.9 – 39.3

(mg kg−1), respectively, all significantly higher than in

samples collected at the control site at Una (Table 3)

Sites 2 and 4 tended to have the highest levels of heavy

metals (with the exception that As concentrations were

higher at site 3 compared to site 2) The maximum

acceptable levels (MLs) for Cd, Pb, and As in

agricul-tural soil of Vietnam (QCVN.01.132.BNNPTNT2013)

are 2, 70, and 12 mg kg−1dw, respectively Thus, the Cd,

Pb, and As concentrations at the four mining sites were

1.5– 1.9 times, 1.7 – 2.3 times, and 2.4 – 3.3 times

higher than the maximum allowable limits, respectively

The high heavy metal concentrations in these soil

sam-ples may result from continuous dispersal downstream

from the tailings and wastewater of the large-scale

min-ing and smeltmin-ing operations (Ha et al 2011; Li et al

2015) These results corroborate other studies of mining

areas, which also reported that elevated levels of heavy

metals in soils were ubiquitous in the vicinities of mines

and smelters (Kachenko and Singh2006; Zhuang et al

2009; Luo et al 2011) For soil samples at the control

site at Una, the heavy metal concentrations were lower

than the permitted levels The concentrations of heavy

metals in the soil samples collected at different sites

were significantly correlated (p < 0.05) This finding

may indicate that all these heavy metals were derived

from similar sources

Average concentrations of Cd, Pb, and As in

irriga-tion water at the four mining sites ranged between

0.91– 1.92, 103.6 – 198.1, and 19.3 – 72.1 μg l−1,

re-spectively, all significantly higher than concentrations

measured at the control site at Una (p < 0.05, Table3) The highest mean concentrations were recorded for Pb

at all sites, followed by As, with lowest concentrations observed for Cd The MLs of Cd, Pb, and As in irriga-tion water according to the Vietnam standard (QCVN.01.132.BNNPTNT 2013) are 10, 50, and

50μg l−1, respectively The concentrations of Pb at site

1, site 2, site 3, and site 4 averaged 2.4, 4, 2.6, and 2.1 times higher than the ML according to Vietnam stan-dards for irrigation water, respectively The As level at site 2 was 1.4 times higher than the ML, while As concentrations were lower than the ML at the other sites Cadmium levels in irrigation water met the Vietnam standard at all sites These results suggest that stream water used by local residents for irrigation at the sites near mining activities is consistently contaminated with

Pb and contaminated with As at site 2 Therefore, these sites did not meet the standards for soil management and irrigation water of Vietnamese Good Agricultural Prac-tices (VietGAP2008)

Heavy metals in vegetables grown in the vicinity

of the mining sites in Bac Kan province

The concentrations of Cd, Pb, and As (mg kg−1dw) in leafy vegetables collected from the four Bac Kan mining areas varied between 0.02 ± 0.01–1.52 ± 0.56, 0.05 ± 0.02– 8.87 ± 1.57, and 0.17 ± 0.05 – 2.66 ± 1.03 mg kg−1dw, respectively (Table4) Signif-icantly lower levels of Cd, Pb, and As were found in vegetable samples collected at the control site at Una, ranging between 0.04– 0.06, 0.03 – 0.08, and 0.03– 0.07 mg kg−1dw, respectively The average concentra-tions of heavy metals across vegetable samples were the highest for Pb, followed by As and then Cd

The highest concentrations of Cd (mg kg−1dw) were found in mustard greens (1.52 ± 0.56, 1.44 ± 0.47, 1.04 ± 0.08, and 1.03 ± 0.04 at site 2, site 3, site 4, and site 1, respectively), kale (1.43 ± 0.09), Indian sorrel (1.39 ± 0.56), vine spinach (1.3 ± 0.32), and water spinach (1.25 ± 0.09) (Table 4) Similarly high Cd concentrations were found in leafy vegetables sampled

at Dabaoshan mine (Zhuang et al.2009) Other studies have found lower (Krejpcio et al 2005; Osma et al

2012; Chang et al 2014) and higher (Maleki and Zarasvand2008; Li et al 2015) Cd concentrations in vegetables compared to those found in our study

We observed maximum concentrations of Pb (mg kg−1dw) in water spinach (8.87 ± 1.57), mustard

greens (8.17 ± 1.09), Indian sorrel (8.07 ± 1.34), katuk

(6.57 ± 1.35), and centella (6.18 ± 1.05) Levels of Pb in

vegetables found in this study were comparable to those

found by Mohamed et al (2003) Other studies have

found lower (Krejpcio et al.2005; Kananke et al.2014;

Chang et al.2014; Chopra and Pathak2015; Oteef et al

2015) and higher (Abdullahi et al 2009; Osma et al

2012; Li et al.2015) levels of Pb contamination

Fertil-izer and other agrochemicals, atmospheric deposition,

and irrigation with contaminated water have been

im-plicated in Pb contamination of crops (Oteef et al.2015)

In our study, high levels of Pb in local vegetables appear

to be caused by soil and irrigation water that have

become contaminated by nearby Pb–Zn mining

activities

We observed the highest concentrations of As

(mg kg−1 dw) in kale (2.66 ± 1.03), amaranth

(1.61 ± 0.25), mustard greens (1.54 ± 0.06), and Indian

sorrel (1.22 ± 0.56) There have been very few studies

that explored As content in vegetables, and our results

were much higher than those reported in another study

conducted in Pearl River Delta, South China (Chang

et al.2014) Also of note, the fern Pteris vittata, known

as an As hyperaccumulator (Bui et al.2011; Ha et al

2011), was abundant at the four mining sites included in

our study and was rarely at the control site

The ratio of F/D ranged from 6.23 to 10.47,

depend-ing on water content in different leafy vegetables

(Table 1) On a fresh weight basis, levels of Cd, Pb,

and As in our vegetable samples ranged between

0.002 ± 0.001– 0.16 ± 0.06, 0.006 ± 0.002 –

1.09 ± 0.19, and 0.02 ± 0.01– 0.18 ± 0.11 mg kg−1,

respectively (Tables1and4) The maximum acceptable

levels of Cd, Pb, and As in leafy vegetables to protect

public health are 0.2, 0.3, and 0.1 mg kg−1f.w (QCVN

8.2-BYT 2011; Codex 2014) The average cadmium

concentrations in vegetables at all sites were below the

ML of 0.2 However, 70.6 and 44.1 % of leafy

vegetables collected at the four mining sites had average

Pb and As concentrations, respectively, that exceeded MLs (up to 3.63 and 1.8 times higher for Pb and As, respectively) (Table4)

Our results suggest that the stream used as irrigation water for vegetable crop production was contaminated

by wastewater from mining activities, resulting in ele-vated heavy metal concentrations in soil and vegetables

of receiving areas Lead concentrations in irrigation water, soil, and vegetables exceeded permissible stan-dard levels There was, however, significant variation among vegetable species in heavy metal content at the four affected sites Heavy metal accumulation in vege-tables depends on various factors In our case, the nature

of the plant appears to have been an important factor, since different levels of heavy metal concentrations were observed in vegetable leaves of different species grown with the same nutrient and soil properties Soil-to-plant transfer is one of the key components of human exposure to metals through the food chain (Khan

et al.2008) The BCF is an important indicator of metal transfer from soil into plants (Ha et al.2011; Chang et al

2014) In our study, BCF values differed significantly between sites, heavy metals, and vegetables (Table 4) BCF values of vegetables were the highest for Cd, rang-ing from 0.01 to 0.75, 13 to 33 times higher than for Pb (BCF: 0.003– 0.059) and 1.7 to 8.2 times higher than for

As (BCF: 0.006– 0.074) Our results indicate that Cd has a higher capacity for transferring from soil to leafy vegetable compared with Pb and As BCF values found

in this study were comparable to those observed by Chang et al (2014), although other research has ob-served higher BCF values (Álvarez-Ayuso et al.2012) The BCF of Cd in vegetables of the Brassicaceae family, including mustard greens, kohlrabi, kale, and cab-bage, were higher than those in the other vegetables sam-pled in this study The Brassicaceae includes 87 different metal hyperaccumulating plant species, and mustard

Table 2 Measurements of certified reference standards (mean concentrations ± SD, n = 5)

Certified

value

Measured value

Mean recovery (%)

Certified value

Measured value

Mean recovery (%)

Certified value

Measured value

Mean recovery (%)

1 dw

greens were previously demonstrated to be Cd and Pb

hyperaccumulators in polluted soil (Anjum et al.2013)

BCF levels of Cd and Pb in some commonly consumed

local vegetables such as Indian sorrel, katuk, perilla, purs-lane, amaranth, and mugwort were also notably high The highest BCF values of Cd and As were found at site 1,

Allowable limits of Cd, Pb and As in leafy vegetables recommended by the WHO / FAO, Codex and Vietnam National Technical Regulation

= 6 per species per site

even though Cd concentrations in soil and water of this

area were lower than in the other areas Heavy metals such

as Cd enter vegetable tissues mainly through root uptake

and absorption by foliage, of which root uptake is the

dominant pathway (Chang et al 2014) Metals can be

transferred from soil pore water into plants though the

roots in the form of dissolved ions (McLaughlin et al

2011) Our results suggest that Cd and As in site 1 may

be present in more dissolved ionic form for plant uptake

than at other sites Soil pH and other properties (salinity,

soil structure, water content, adsorption-desorption,

com-plexation-dissociation, oxidation reduction, ion exchange,

and other carrier transport role) can contribute to

differ-ences in BCF between sites (Chang et al.2014; Balkhair

and Ashraf2015) Since soil pH was very similar across

sites, we rule out pH as a significant driver of BCF

differences in our study

Potential health risks associated with the consumption

of local leafy vegetables

Many studies use THQ as a more complex parameter for

health risk assessment of heavy metals compared to

sim-pler parameters such as MLs (Chien et al.2002; Song et al

2009; Li and Zhang2010; Yang et al.2011; Chandorkar

and Deota2013; Chang et al.2014) Across all vegetable

species combined, the mean THQs of Cd, Pb, and As were

less than 1 at all sites, indicating no health risk (Fig.2)

Likewise, when calculated on a per-species basis across all

sites, THQ values of Cd, Pb, and As were also lower than

1, ranging between 0.01– 0.25, 0.004 – 0.39, and 0.04 –

0.9, respectively Given that MLs for Pb and As exceeded

in 70.6 and 44.1 %, respectively, of leafy vegetables

collected at the four mining sites, MLs are a less

conser-vative indicator of risk than THQ However, THQs of As

in five vegetable species were higher than 1 at certain sites:

mustard green (site 1 = 1.33, 3 = 1.23); kale (site 1 = 1.15);

katuk, amaranth, and Indian sorrel (site 2 = 1.28, 1.30, and

2.65, respectively) Given that As concentrations in all of

these species also exceeded MLs, there is strong evidence

of health risk for these vegetable species These results

suggest that, to protect against heavy metal toxicity, local

residents need vegetable-specific and site-specific

informa-tion and should pay atteninforma-tion to the kinds and amounts of

vegetables consumed (Hu et al.2013)

Across vegetable species, average TTHQ values of

Cd, Pb, and As at sites 1–4 varied between 1.00 – 1.44,

compared to 0.06 for the control site at Una (Fig 2)

These values indicate a health risk from a diet that

includes all the vegetables cultivated at the mining sites Arsenic was the major risk contributor at all mining sites, contributing from 49 to 73 % of TTHQ Lead was an important contributor to TTHQ at sites 2 and 4 (Fig.2) In contrast, Cd contributed the least to TTHQ at the mining sites (13.6–24.9 %) (Fig.2)

Total THQ has been used in recent public studies as a reliable way to compare the combined toxicity risks from different foods and types of chemicals (e.g., As,

Cu, Ni, Cr, Hg, Zn, Fe, Mn) (Song et al.2009; Li and Zhang2010; Chang et al.2014) Still, it should be noted that TTHQ is a highly conservative index (Yang et al

2011; Chang et al.2014) Furthermore, leafy vegetables contribute only a part of the total daily intake of heavy metals; other sources of intake include drinking water, inhalation of dust, and consumption of local meat such

as pork, chicken, ducks, and freshwater fish

Conclusions and recommendations

Our results indicate that soils exceed ML safety stan-dards for Cd, Pb, and As, irrigation water from the area exceeds ML safety standards for Pb and As, and sub-stantial percentages of leafy vegetable crops cultivated

in the area exceed ML safety standards for Pb and As Likewise, based on THQ, certain vegetable crops pose risks for As contamination at certain sites And based on TTHQ, a diet that includes all vegetables poses health risks, especially due to As, regardless of which mining site they were cultivated at

Fig 2 The target hazard quotient (THQ) and total THQ of three heavy metals at different study sites, calculated across all vegetable crops

Considering all available evidence, we do not

recom-mend field cultivation of vegetables in these types of

mining sites If vegetables are grown, we recommend

those with low BCF values, such as lolot, celery, and

string beans and caution against cultivating vegetables

belonging to the Brassicaceae family The use of

irriga-tion water from unpolluted sources (water wells,

proc-essed surface water), the use of organic fertilizers, and

growth of crops in greenhouses are recommended in

these polluted areas Replacing cultivation of leafy

veg-etables with fruit tree crops should also be explored,

because fruits retain lower concentrations of heavy

metals than leaves The relevant national authorities

should be informed about actual and potential vegetable

contamination problems, take measures to enhance the

safety of vegetable cultivation, institute crop-specific

and site-specific monitoring to check product safety

before marketing, and consider employing

eco-labeling to indicate safe products

National Foundation for Science and Technology Development

(NAFOSTED) under grant number 105.08-2014.12.

References

Abdullahi, M S., Uzairu, A., & Okunota, O J (2009).

Quantitative determination of heavy metal concentrations in

onion leaves International Journal of Environmental

Research, 3, 271–274.

Álvarez-Ayuso, E., Otones, V., Murciego, A., García-Sánchez, A.,

& Regina, I S (2012) Antimony, arsenic and lead

distribu-tion in soils and plants of an agricultural area impacted by

former mining activities Science of the Total Environment,

Anjum, A N., Ahmad, I., Peduarda, M E., Duarte, C A., & Umar,

S (2013) The plant family brassicaceae-contribution

to-wards phytoremediation Springer, 171 pages.

Arora, M., Kiran, B., Rani, S., Rani, A., Kaur, B., & Mittal, N.

(2008) Heavy metal accumulation in vegetables irrigated

with water from different sources Food Chemistry, 111(4),

Balkhair, K S., & Ashraf, M A (2015) Field accumulation risks

of heavy metals in soil and vegetable crop irrigated with

sewage water in western region of Saudi Arabia Saudi

sjbs.2015.09.023

Bui, T K A., Dang, D K., Tran, V T., Nguyen, T K., & Do, T A.

(2011) Phytoremediation potential of indigenous plants from

Thai Nguyen province, Vietnam Journal of Environmental

Chandorkar, S., & Deota, P (2013) Heavy metal content of foods and health risk assessment in the study population of

Chang, C Y., Yu, H Y., Chen, J J., Li, F B., Zhang, H H., & Liu,

C P (2014) Accumulation of heavy metals in leaf vegetables from agricultural soils and associated potential health risks in the Pearl River Delta, South China Environmental

doi: 10.1007/s10661-013-3472-0 Chien, L C., Hung, T C., Choang, K Y., Yeh, C Y., Meng, P J., Shieh, M J., & Han, B C (2002) Daily intake of TBT, Cu,

Zn, Cd and as for fishermen in Taiwan Science of the Total

Chopra, A K., & Pathak, C (2015) Accumulation of heavy metals in the vegetables grown in wastewater irrigated areas

of Dehradun, India with reference to human health risk.

CODEX (2014) Working document for information and use in discussions related to contaminants and toxins in the GSCTFF Joint FAO/WHO Food Standards Programme (CF/8 INF/1).

DARD (2010) Synthesis report on the vegetable consumption of Cho Don district, Bac Kan province, department of agricul-ture and rural development of Bac Kan, Portal of Bac Kan Province Retrieved May 20, 2010(in Vietnamese) Dijk, V C., Wim, V D., & Bert, V A (2015) Long term plant biomonitoring in the vicinity of waste incinerators in the

chemosphere.2014.11.002 DREBK (2012) Department of Resources and Environment Bac Kan, Portal of Bac Kan Province Retrieved November 15, 2012(in Vietnamese).

Fraser, M., Surette, C., & Vaillancourt, C (2013) Fish and seafood availability in markets in the Baie des Chaleurs region, New Brunswick, Canada: a heavy metal contamination baseline study Environmental Science and Pollution Research

Ha, N T H., Sakakibara, M., Sano, S., & Nhuan, M T (2011).

zinc mine area, northern Vietnam Journal of Hazardous

jhazmat.2010.12.020

Hu, J., Wu, F., Wu, S., Cao, Z., Lin, X., & Wong, M H (2013) Bioaccessibility, dietary exposure and human risk assessment

of heavy metals from market vegetables in Hong Kong revealed with an in vitro gastrointestinal model.

chemosphere.2012.11.066 Järup, L., & Åkesson, A (2009) Current status of cadmium as an environmental health problem Toxicology and Applied

taap.2009.04.020 Jooste, A., Marr, S M., Addo-Bediako, A., & Luus-Powell, W J (2015) Sharptooth catfish shows its metal: a case study of metal contamination at two impoundments in the Olifants River, Limpopo river system, South Africa Ecotoxicology

ecoenv.2014.10.033 Kachenko, A., & Singh, B (2006) Heavy metals contamination in vegetables grown in urban and metal smelter contaminated