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

Environ Monit Assess (2016) 188:525
DOI 10.1007/s10661-016-5535-5

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 Vietnam. 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
A. T. K. Bui (*) : C. H. Nguyen
Institute of Environmental Technology, Vietnam Academy of
Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam
e-mail:
H. T. H. Nguyen : M. N. Nguyen

VNU University of Science, Vietnam National University, 334
Nguyen Trai, Hanoi, Vietnam
T.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

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 carcinogen (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


525

Page 2 of 11

important part of the human diet and vegetable crops
can uptake heavy metals from contaminated environments (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 mountainous provinces including Bac Kan, Ha Giang, Tuyen
Quang, and Thai Nguyen (DREBK 2012). Concentration 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 concentrations of heavy metals if they grew on miningcontaminated 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 (Ngo 2007).
Maximum permitted levels (MLs) for contaminants

and toxins in foods are specified by international food
standards (Codex 2014; Dijk et al. 2015; Oteef et al.
2015). Vietnam’s standards for Cd, Pb, and As contamination in food follow international standards (QCVN
8.2-BYT 2011). 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 foodstuffs (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 contamination 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 surrounding environment without treatment (DREBK
2012). Use of potentially contaminated stream water

Environ Monit Assess (2016) 188:525

may enhance the heavy metal concentrations in vegetables 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 vegetables (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 locations 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 capsule filter before elemental determination.

Sample preparation and digestion methods for vegetables 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


Environ Monit Assess (2016) 188:525

Page 3 of 11 525

Fig. 1 Map showing the location of the sampling sites

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 temperature 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 HNO3 65 %
(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 pHKCl was measured on a
1:2 ratio of soil/KCl(1N) by Lab 850 pH meter (Schott
Instruments, Germany).

Total (inorganic + organic) heavy metal concentrations in plant, soil, and water samples were measured
using an inductively coupled plasma-mass spectrometer
(ICP-MS, ELAN 9000, PerkinElmer, USA). The accuracy and precision in elemental analyses by ICP-MS
were assessed using reagent blanks and internal standards (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−1 for As, Pb, and Cd
from Merck, Germany.
Heavy metal concentrations of vegetables were determined 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
(Table 1). 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 noncancer health risks are expected, and total target
hazard quotient (TTHQ) is the sum of each


525

Environ Monit Assess (2016) 188:525

Page 4 of 11

Table 1 The ratio of fresh weight
(F) and dry weight (D) for the
vegetable species studied (n = 3)

Vegetable name

Latin name

F (g)

D (g)

Mustard green

Brassica juncea

20

2.15

9.30

89.25

Kohlrabi

Brassica oleracea

20

2.43

8.23

87.85

Gourd

Benincasa hispida

20

2.85

7.02

85.75

Lolot

Piper lolot

20

2.31

8.66

88.45

Centella

Centella asiatica

20

2.12

9.43

89.40

Katuk

Sauropus androgynus

20

3.21

6.23

83.95

Water spinach

Ipomoea aquatica

20

2.45

8.16

87.75

Kale

Brassica integrifolia

20

2.33

8.58

88.35

String beans

Phaseolus vulgaris

20

2.98

6.71

85.10

Celery

Apium graveolens

20

2.45

8.16

87.75

Vine spinach

Basella alba

20

2.74

7.30

86.30

Purple onion

Allium ascalonicum

20

1.92

10.42

90.40

Cabbage

Brassica oleracea

20

2.52

7.94

87.40

Lettuce

Lactuca sativa

20

1.91

10.47

90.45

Sweet potato

Ipomoea batatas

20

2.36

8.47

88.20

Cauliflower

Brassica oleracea

20

2.34

8.55

88.30

Mugwort

Artemisia vulgaris

20

2.87

6.97

85.65

Perilla

Perilla frutescens

20

2.56

7.81

87.20

Purslane

Portulaca oleracea

20

2.24

8.93

88.80

Amaranth

Amaranthus tricolor

20

2.17

9.22

89.15

Indian sorrel

Oxalis corniculata

20

2.43

8.23

87.85

individual THQ (Chang et al. 2014; Hu et al. 2013)
(Eq. 1):

THQ ¼

C  M vegetable  EF  ED
 10−3 ; TTHQ
BW Â AT Â RfD

¼ ∑THQ ðsingle pollutantÞ

ð1Þ

where C is the mean concentration of a particular
metal in a fresh vegetable (mg kg−1); Mvegetable is the
daily local leaf vegetable intake by the local residents, 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 potential 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 estimates for other parameters as follows: The daily local

F/D

Water (%)

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; VMH 2015). 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 × 10−4 mg kg−1 per day for
Cd, Pb, and As, respectively (USEPA 2014).

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.


Environ Monit Assess (2016) 188:525

Results and discussion
Quality of measurements
Recovery values of 91–104 % were obtained for Cd, Pb,
and As (Table 2). These recovery values compare favorably 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 (Table 3). Average 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 agricultural soil of Vietnam (QCVN.01.132.BNNPTNT 2013)
are 2, 70, and 12 mg kg−1 dw, 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 samples may result from continuous dispersal downstream
from the tailings and wastewater of the large-scale mining and smelting 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 Singh 2006; 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 irrigation water at the four mining sites ranged between
0.91 – 1.92, 103.6 – 198.1, and 19.3 – 72.1 μg l−1, respectively, all significantly higher than concentrations

Page 5 of 11 525

measured at the control site at Una (p < 0.05, Table 3).
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 irrigation water according to the Vietnam standard
(QCVN.01.132.BNNPTNT 2013) are 10, 50, and
50 μg 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 standards 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 Practices (VietGAP 2008).
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−1 dw) 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−1 dw, respectively (Table 4). Significantly 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−1 dw, respectively. The average concentrations of heavy metals across vegetable samples were the
highest for Pb, followed by As and then Cd.

The highest concentrations of Cd (mg kg−1 dw) 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
Zarasvand 2008; Li et al. 2015) Cd concentrations in
vegetables compared to those found in our study.
We observed maximum concentrations of Pb
(mg kg−1 dw) in water spinach (8.87 ± 1.57), mustard


525

Environ Monit Assess (2016) 188:525

Page 6 of 11

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

NIST SRM 2587
Certified
value
(mg kg−1)

Measured
value
(mg kg−1)

As

13.7 ± 2.3

12.9 ± 1.8

Cd

1.92 ± 0.23

1.84 ± 0.34

Pb

3242 ± 57

3339 ± 86

NIES CRM No. 1
Mean
recovery
(%)

Merck

Certified

value
(mg kg−1)

Measured
value
(mg kg−1)

Mean
recovery
(%)

94

2.3 ± 0.3

2.4 ± 0.2

104

50

48.5 ± 1.1

97

96

6.7 ± 0.5

6.8 ± 0.7

101

5

4.55 ± 0.67

91

103

5.5 ± 0.8

5.4 ± 0.5

98

100

102 ± 6.3

102

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 Pathak 2015; Oteef et al.
2015) and higher (Abdullahi et al. 2009; Osma et al.

2012; Li et al. 2015) levels of Pb contamination. Fertilizer and other agrochemicals, atmospheric deposition,
and irrigation with contaminated water have been implicated 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, depending 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 (Tables 1 and 4). 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−1 f.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

Certified

value
(μg l−1)

Measured
value
(μg l−1)

Mean
recovery
(%)

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) (Table 4).
Our results suggest that the stream used as irrigation
water for vegetable crop production was contaminated
by wastewater from mining activities, resulting in elevated heavy metal concentrations in soil and vegetables
of receiving areas. Lead concentrations in irrigation
water, soil, and vegetables exceeded permissible standard levels. There was, however, significant variation
among vegetable species in heavy metal content at the
four affected sites. Heavy metal accumulation in vegetables 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, ranging 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 observed higher BCF values (Álvarez-Ayuso et al. 2012).
The BCF of Cd in vegetables of the Brassicaceae
family, including mustard greens, kohlrabi, kale, and cabbage, were higher than those in the other vegetables sampled in this study. The Brassicaceae includes 87 different
metal hyperaccumulating plant species, and mustard


7.9 (7.6–8.1)

7.5 (7.4–7.7)

Site 4

Unaa

a

Unaffected site

n = 18 for soil and n = 10 for water

7.7 (7.5–7.9)

7.6 (7.4–7.7)

Site 2

Site 3

7.5 (7.4–7.6)

pH

Site 1

Sites

0.9 (0.78–1.12)

3.7 (3.15–4.26)

2.9 (2.68–3.12)

3.8 (3.23–4.17)

1.9 (1.57–1.93)

Cd

Soil (mg kg−1 dw)

64.3 (60.1–67.6)

150 (141.2–158.5)

128.3 (121.4–132.6)

160.8 (152.7–169.4)

118.2 (111.3–122.7)

Pb

3.8 (3.67–4.48)

28.9 (27.4–31.7)

34.1 (28.6–37.8)

39.3 (31.2–45.5)

29.2 (25.3–32.4)

As

Table 3 Mean (range) concentrations of Cd, Pb, and As in soil and irrigation water and of pH in soil

0.31 (0.27–0.35)

0.91 (0.61–1.13)

1.43 (0.34–2.36)

1.92 (1.23–2.51)

1.32 (0.45–2.07)

Cd

Irrigation water (μg l−1)

1.7 (1.62–1.75)

103.6 (93.4–111.5)

129 (115.7–142.1)

198.1 (182.3–219.2)

117.4 (106.5–124.8)

Pb

1.41 (1.23–1.54)

20.1 (13.9–24.5)

19.3 (14.5–23.1)

72.1 (67.1–78.9)

45.1 (41.2–47.3)

As

Environ Monit Assess (2016) 188:525
Page 7 of 11 525


525

Environ Monit Assess (2016) 188:525

Page 8 of 11

Table 4 Concentration (mg kg−1 dw ± SD) of heavy metals in vegetables and associated BCF values
Area

Vegetable

Cd

BCF

Pb

BCF

As

BCF

Site 1

Mustard green

1.43 ± 0.09

0.75

4.17 ± 1.09a

0.035

1.66 ± 1.03a

0.057

Kohlrabi

1.12 ± 0.07

0.59

2.04 ± 0.08

0.017

1.03 ± 0.06a

0.035

Gourd

0.24 ± 0.03

0.13

1.80 ± 0.09

0.015

0.81 ± 0.03

0.028

Kale

1.03 ± 0.04

0.54

0.09 ± 0.03

0.0008

1.32 ± 0.06a

0.045

String beans

0.07 ± 0.01

0.04

0.53 ± 0.12

0.005

0.73 ± 0.22

0.025

Site 2

Site 3

Celery

0.23 ± 0.05

0.12

1.12 ± 0.53

0.01

0.34 ± 0.11

0.012

Vine spinach

0.41 ± 0.12

0.22

1.18 ± 0.87

0.010

0.44 ± 0.06

0.015

Purple onion

0.33 ± 0.14

0.17

3.21 ± 1.12a

0.027

0.63 ± 0.32

0.022

Mustard green

1.52 ± 0.56

0.40

5.38 ± 1.13a

0.034

1.05 ± 0.17a

0.027

Celery

0.93 ± 0.11

0.24

2.25 ± 1.07

0.014

0.31 ± 0.06

0.008

Cauliflower

0.19 ± 0.07

0.05

4.12 ± 1.16a

0.026

0.37 ± 0.19

0.009

Katuk

0.59 ± 0.18

0.16

6.57 ± 1.35a

0.041

1.07 ± 0.32a

0.027

Kale

0.37 ± 0.22

0.10

3.44 ± 1.27a

0.021

0.62 ± 0.18

0.016

Mugwort

0.62 ± 0.31

0.16

4.67 ± 1.73a

0.029

0.51 ± 0.10

0.013

a

Perilla

0.53 ± 0.16

0.14

3.44 ± 1.07

0.021

0.98 ± 0.16

0.025

Purslane

0.56 ± 0.23

0.15

4.09 ± 1.15a

0.025

1.16 ± 0.63a

0.030

Amaranth

0.36 ± 0.14

0.09

5.81 ± 1.21a

0.036

1.61 ± 0.25a

0.041

Indian sorrel

1.39 ± 0.56

0.37

8.57 ± 1.34a

0.053

2.92 ± 0.56a

0.074

Sweet potato

1.27 ± 0.08

0.33

3.34 ± 1.05a

0.021

0.63 ± 0.22

0.016

Centella

0.33 ± 0.12

0.09

4.75 ± 1.01a

0.030

0.42 ± 0.03

0.011

Mustard green

1.44 ± 0.47

0.50

3.38 ± 0.71a

0.026

1.53 ± 0.67a

0.045

Celery

0.98 ± 0.15

0.34

1.01 ± 0.23

0.008

0.53 ± 0.09

0.016

Vine spinach

0.82 ± 0.15

0.28

1.19 ± 0.07

0.032

0.54 ± 0.08

0.016

1.3 ± 0.32

0.45

4.12 ± 1.05a

0.009

0.56 ± 0.12

0.016
0.013

Cabbage

Site 4

b

Una

a

Lettuce

0.84 ± 0.18

0.29

0.78 ± 0.13

0.006

0.46 ± 0.13

Sweet potato

1.07 ± 0.06

0.37

3.10 ± 1.02a

0.024

0.89 ± 0.23a

0.026

Cauliflower

0.21 ± 0.07

0.07

0.09 ± 0.02a

0.0007

0.41 ± 0.13

0.012

Mustard green

1.04 ± 0.08

0.28

8.12 ± 1.01a

0.054

1.06 ± 0.04a

0.037

a

0.028

0.34 ± 0.09

0.012

Kohlrabi

0.53 ± 0.12

0.14

4.23 ± 1.14

Gourd

0.77 ± 0.02

0.21

5.37 ± 1.15a

0.036

0.64 ± 0.08

0.022

Lolot

0.02 ± 0.01

0.01

0.05 ± 0.02

0.0003

0.17 ± 0.05

0.006

Centella

0.22 ± 0.10

0.06

6.18 ± 1.05a

0.041

0.55 ± 0.12

0.019

Katuk

0.13 ± 0.03

0.04

3.18 ± 1.02a

0.021

0.35 ± 0.06

0.012

Water spinach

1.25 ± 0.09

0.34

8.87 ± 1.57a

0.059

0.94 ± 0.21a

0.033

Mustard green

0.06 ± 0.03

0.07

0.03 ± 0.01

0.0005

0.07 ± 0.03

0.018

Celery

0.04 ± 0.01

0.04

0.08 ± 0.03

0.0012

0.05 ± 0.17

0.013

Purple onion

0.05 ± 0.02

0.06

0.04 ± 0.02

0.0006

0.06 ± 0.06

0.016

Indian sorrel

0.05 ± 0.02

0.06

0.07 ± 0.04

0.0011

0.03 ± 0.01

0.008

Allowable limits of Cd, Pb and As in leafy vegetables recommended by the WHO / FAO, Codex and Vietnam National Technical Regulation
are 0.2, 0.3, and 0.1 mg kg-1 f.w., respectively; (a): The heavy metal concentrations are higher than permitted standard; (b): Unaffected site; n
= 6 per species per site

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, purslane, amaranth, and mugwort were also notably high. The
highest BCF values of Cd and As were found at site 1,


Environ Monit Assess (2016) 188:525

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, complexation-dissociation, oxidation reduction, ion exchange,
and other carrier transport role) can contribute to differences in BCF between sites (Chang et al. 2014; Balkhair
and Ashraf 2015). 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 simpler parameters such as MLs (Chien et al. 2002; Song et al.
2009; Li and Zhang 2010; Yang et al. 2011; Chandorkar
and Deota 2013; 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 conservative 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 information and should pay attention 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

Page 9 of 11 525

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

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
Zhang 2010; 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 standards for Cd, Pb, and As, irrigation water from the area
exceeds ML safety standards for Pb and As, and substantial 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.


525

Page 10 of 11

Considering all available evidence, we do not recommend 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 irrigation water from unpolluted sources (water wells, processed surface water), the use of organic fertilizers, and
growth of crops in greenhouses are recommended in
these polluted areas. Replacing cultivation of leafy vegetables 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 ecolabeling to indicate safe products.
Acknowledgments This research was funded by the Vietnam
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 distribution in soils and plants of an agricultural area impacted by
former mining activities. Science of the Total Environment,
439, 35–43. doi:10.1016/j.scitotenv.2012.09.023.
Anjum, A. N., Ahmad, I., Peduarda, M. E., Duarte, C. A., & Umar,
S. (2013). The plant family brassicaceae-contribution towards 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),
811–815. doi:10.1016/j.foodchem.2008.04.049.
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
Jour nal o f Biologic al S ciences . d o i :1 0. 10 16 / j .
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
Biology, 32, 257–262.

Environ Monit Assess (2016) 188:525
Chandorkar, S., & Deota, P. (2013). Heavy metal content of foods
and health risk assessment in the study population of

Vadodara. Current World Environment, 8(2), 291–297.
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
Monitoring and Assessment, 186(3), 1547–1560.
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
Environment, 285, 177–185.
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.
Environmental Monitoring and Assessment, 187, 1–8.
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 agriculture 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
Netherlands. Chemosphere, 122, 45–51. doi:10.1016/j.
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
International, 20, 761–770.
Ha, N. T. H., Sakakibara, M., Sano, S., & Nhuan, M. T. (2011).
Uptake of metals and metalloids by plants growing in a lead–
zinc mine area, northern Vietnam. Journal of Hazardous
Materials, 186(2–3), 1384–1391. doi:10.1016/j.
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.
C h e m o s p h e re , 9 1 ( 4 ) , 4 5 5 – 4 6 1 . d o i : 1 0 . 1 0 1 6 / j .
chemosphere.2012.11.066.
Järup, L., & Åkesson, A. (2009). Current status of cadmium as an
environmental health problem. Toxicology and Applied
Pharmacology, 238(3), 201–208. doi:10.1016/j.
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
and Environmental Safety, 112, 96–104. doi:10.1016/j.
ecoenv.2014.10.033.
Kachenko, A., & Singh, B. (2006). Heavy metals contamination in
vegetables grown in urban and metal smelter contaminated


Environ Monit Assess (2016) 188:525

sites in Australia. Water, Air, and Soil Pollution, 169(1–4),
101–123. doi:10.1007/s11270-006-2027-1.
Kananke, T., Wansapala, J., & Gunaratne, A. (2014). Heavy metal
contamination in green leafy vegetables collected from selected market sites of Piliyandala area, Colombo District,
SriLanka. American Journal of Food Science and
Technology, 2, 139–144.
Khan, S., Cao, Q., Zheng, Y. M., Huang, Y. Z., & Zhu, Y. G.
(2008). Health risks of heavy metals in contaminated soils
and food crops irrigated with wastewater in Beijing, China.
Environmental Pollution, 152(3), 686–692. doi:10.1016/j.
envpol.2007.06.056.
Krejpcio, Z., Sionkowski, S., & Bartela, J. (2005). Safety of fresh
fruits and juices available on the polish market as determined
by heavy metal residues. Polish Journal of Environmental
Studies, 16(6), 877–881.
Li, S., & Zhang, Q. (2010). Risk assessment and seasonal variations of dissolved trace elements and heavy metals in the
upper Han River, China. Journal of Hazardous Materials,
181(1–3), 1051–1058. doi:10.1016/j.jhazmat.2010.05.120.
Li, N., Kang, Y., Pan, W., Zeng, L., Zhang, Q., & Luo, J. (2015).
Concentration and transportation of heavy metals in vegetables and risk assessment of human exposure to bioaccessible
heavy metals in soil near a waste-incinerator site, South
China. Science of the Total Environment, 521–522, 144–
151. doi:10.1016/j.scitotenv.2015.03.081.
Luo, C., Liu, C., Wang, Y., Liu, X., Li, F., Zhang, G., & Li, X.
(2011). Heavy metal contamination in soils and vegetables
near an e-waste processing site, South China. Journal of
Hazardous Materials, 186(1), 481–490. doi:10.1016/j.
jhazmat.2010.11.024.
Maleki, A., & Zarasvand, M. A. (2008). Heavy metals in selected
edible vegetables and estimation of their daily intake in

Sanandaj, Iran. The Southeast Asian Journal of Tropical
Medicine and Public Health, 39, 335–340.
McLaughlin, M. J., Smolders, E., Degryse, F., & Rietra, R. (2011).
Uptake of metals from soil into vegetables. In F. A. Swartjes
(Ed.), Dealing with contaminated sites: from theory towards
practical application. Heidelberg: Springer. doi:10.1007/97890-481-9757-6_8.
Mohamed, A., Rashed, M., & Mofty, A. (2003). Assessment of
essential and toxic elements in some kinds of vegetables.
Ecotoxicology and Environmental Safety, 55, 251–260.
Navarro, M. C., Pérez-Sirvent, C., Martínez-Sánchez, M. J., Vidal,
J., Tovar, P. J., & Bech, J. (2008). Abandoned mine sites as a
source of contamination by heavy metals: a case study in a
semi-arid zone. Journal of Geochemical Exploration, 96(2–
3), 183–193. doi:10.1016/j.gexplo.2007.04.011.
Ngo, T. L. P. (2007). The affect of water and soil environment to
vegetable quality. Vietnam Journal of Agriculture and Rural
Development, 17, 15–20 in Vietnamese.

Page 11 of 11 525
Osma, E., Serin, M., Leblebici, Z., & Aksoy, A. (2012). Heavy
metals accumulation in some vegetables and soils in Istanbul.
Ekoloji, 21(82), 1–8.
Oteef, M. D., Fawy, K. F., Abd-Rabboh, H. S., & Idris, A. M.
(2015). Levels of zinc, copper, cadmium, and lead in fruits
and vegetables grown and consumed in Aseer region, Saudi
Arabia. Environmental Monitoring and Assessment,
187(676).
QCVN.01.132.BNNPTNT (2013). Vietnam national technical
regulation on fresh vegetable, fruit and tea—conditions for
ensuring food safety in production and packing.

Retrieved 22
Jan 2013.
QCVN8.2-BYT (2011). Vietnam national technical regulation on
the limits of heavy metals contamination in food. http://www.
fsi.org.vn/pic/files/qcvn-8-2_2011-byt-gioi-han-o-nhiemkim-loai-nang.pdf. Retrieved 13 Jan 2011.
Song, B., Lei, M., Chen, T., Zheng, Y., Xie, Y., Li, X., & Gao,
D. (2009). Assessing the health risk of heavy metals in
vegetables to the general population in Beijing, China.
Journal of Environmental Sciences, 21(12), 1702–1709.
doi:10.1016/S1001-0742(08)62476-6.
U.S (2003). The booklet from Department of Health and Human
Services, USA.NIH Publication No. 03–2039. from:
/>environment_508.pdf.
USEPA (1989). Guidance manual for assessing human health risks
from chemically contaminated, fish and shellfish EPA-503/889-002. US Environmental Protection Agency (US EPA),
Washington DC.
USEPA (2007). Microwave assisted acid digestion of sediments,
sludges, soils and oils. Revision 1.
USEPA (2014). EPA Region 3 Risk-based Concentration Table.
September 12, 2014, .
gov/ncea/iris/search/index.cfm.
VietGAP (2008). The Vietnamese Good Agricultural Practices
Ministry of Agriculture and Rural Development.Retrieved
October 15, 2008 from: />VMH (2015). Vietnam ministry of health, the report of the census
of nutrition 2009–2012 of households the Youth
newspaper(in Vietnamese).
Yang, Q. W., Xu, Y., Liu, S. J., He, J. F., & Long, F. Y. (2011).
Concentration and potential health risk of heavy metals in
market vegetables in Chongqing, China. Ecotoxicology and
Environmental Safety, 74, 1664–1669.

Zhuang, P., Zou, B., Li, N. Y., & Li, Z. A. (2009). Heavy metal
contamination in soils and food crops around Dabaoshan
mine in Guangdong, China: implication for human health.
Environmental Geochemistry and Health, 31, 707–715.