Environ Monit Assess (2018) 190:505
https://doi.org/10.1007/s10661-018-6881-2
Concentrations, dietary exposure, and human health risk
assessment of heavy metals in market vegetables of Peshawar,
Pakistan
Mehboob Alam & Maaz Khan & Anwarzeb Khan &
Shah Zeb & Muhammad Amjad Khan & Noor ul Amin &
Muhammad Sajid & Abdul Mateen Khattak
Received: 16 March 2018 / Accepted: 25 July 2018
# Springer Nature Switzerland AG 2018
Abstract The present study was carried out to assess
heavy metal concentrations in ready-to-eat vegetables
(RTEs) collected from open markets. Samples of RTEs
including lettuce, coriander, and carrot were collected
from five different local markets of Peshawar, Pakistan
including Industrial estate, Board, Agriculture University,
Firdos, and Hashtnaghri on four different dates, i.e., 21st
March, 04th April, 19th April, and 05th May, 2016. The
samples were analyzed through atomic absorption spec-
trophotometer to see the amount of heavy metals present
in them. The elements studied were cadmium (Cd), chro-
mium (Cr), copper (Cu), nickel (Ni), and lead (Pb). Max-
imum Cd, Cr, Cu, Ni, and Pb concentrations in samples
collected from different markets were 0.68, 5.28, 12.31,
7.61, and 25.04 mg kg−1, respectively, whereas maximum
Cd, Cr, Cu, Ni, and Pb concentrations in RTEs collected at
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s10661-018-6881-2) contains
supplementary material, which is available to authorized users.
M. Alam (*) : M. Khan : S. Zeb : N. u. Amin : M. Sajid : carbohydrates, minerals, and fibers, along with other
A. M. Khattak
Department of Horticulture, The University of Agriculture
Peshawar, Peshawar, KP, Pakistan
e-mail: mehboobalam@aup.edu.pk
A. Khan (*)
Department of Environmental and Conservation Sciences,
University of Swat, Swat, KP, Pakistan
e-mail: khan.anwarzeb@yahoo.com
M. A. Khan
Department of Environmental Sciences, University of Peshawar,
Peshawar, KP, Pakistan
different dates were 0.59, 4.08, 14.85, 7.23, and
21.97 mg kg−1, respectively. The mean Cd, Cr, and Pb
concentrations exceeded the permissible limits, while Cu
and Ni were found within the limits set by FAO/WHO in
all studied RTEs. The daily dietary intake and hazard
quotient (HQ) showed great variations. The HQ was
found > 1 for Pb in all studied vegetables, while it was
< 1 for Cd, Cr, Cu, and Ni with few exceptions. It can be
concluded from the study that heavy metal concentrations
were above the permissible toxicity levels and their con-
tinuous consumption may cause several health issues.
Keywords Dietary intake . Hazard quotient . Heavy
metals . Markets . Ready-to-eat vegetables
Introduction
Vegetables are important part of the human diet as they
provide essential nutrients, such as vitamins, proteins,
essential micronutrients and trace metals (Khanna
2011; Yang et al. 2011; Khan et al. 2015, 2016). Human
beings require varying amount of essential nutrients
(i.e., nitrogen (N), phosphorus (P), potassium (K), sodi-
um (Na), iron (Fe), manganese (Mn), magnesium (Mg),
and zinc (Zn)) for biochemical processes, and excessive
level of these elements may be harmful (Onsanit et al.
2010). Beside the essential elements, vegetables are
capable of bioaccumulating other elements including
arsenic (As), cadmium (Cd), copper (Cu), chromium
(Cr), nickel (Ni), and lead (Pb) in their edible and non-
505 Page 2 of 15
edible tissues (Singh et al. 2010). Some of the heavy
metals are harmful to humans and a little amount can
cause health disorders, while others including Cu, Ni,
etc. are required by living organisms, but can be harmful
in excessive amount. Higher concentrations of heavy
metals in soil have deleterious effects on plant nutrition-
al components as they replace essential elements (Khan
et al. 2016).
Ready-to-eat vegetable (RTE) contamination by tox-
ic metals has become a serious global issue during
recent decades, because of their potential bioaccumula-
tion through contaminated soil and water (Khan et al.
2016). Globally, consumers are concerned about food
safety due to increase in pollution, which accelerates the
demand for safe food. Heavy metals are serious envi-
ronmental concern posing health risk through contami-
nated food ingestion (Cui et al. 2005). Rapid industrial-
ization and urbanization in developing countries have
contributed to the high level of heavy metal pollution
(Wang et al. 2005). Human body mechanisms are inca-
pable of detoxifying heavy metals, which
bioaccumulate in their vital organs such as kidneys,
liver, bones, and muscles (Naseri et al. 2015). Heavy
metals are of particular concern, because in human
body, vital minerals are substituted by these heavy
metals, interrupting their normal functions (Malayeri
et al. 2008).
Generally, heavy metals originate from two main
sources including natural and anthropogenic (Zhang
2006). Natural sources of contamination include
weathering of parent materials, erosion of bed rocks,
volcanic activities, forest fires, and ore deposits, while
anthropogenic sources include irrigation with wastewa-
ter or sewage sludge, application of fertilizers (Frost and
Ketchum 2000), industrial discharge, mining and min-
eral processing (Khan et al. 2017), electroplating,
smelting, and atmospheric deposition (Wuana and
Okieimen 2011). Rapid growth in population and in-
creased need for food resulted in excessive use of fertil-
izers and metal-based pesticides for producing more and
more food (Pourang and Noori 2012). The RTEs culti-
vated in metal-contaminated soil are either consumed by
the farmers itself or transported to urban markets for sale
posing health risks to the consumers (Zhou et al. 2016).
Peshawar is the most populated city of Khyber
Pakhtunkhwa province of Pakistan. Pollution in the city
is a major issue relating to public health. The condition
of markets in Peshawar region is not satisfactory and
transportation and handling of vegetables are not up to
Environ Monit Assess (2018) 190:505
the standards. Moreover, the quality of RTEs vended in
open air on roadside is further deteriorated by the fumes
and dust generated by the heavy traffic. These RTEs are
directly exposed to vehicular, industrial, and brick kiln
emissions in and around the city. Likewise, limited
activities of municipality in lifting waste materials, poor
sanitation, and the presence of dumping yards in the
vicinity are also the contributing factors to heavy metal
concentration.
Food chain contamination by heavy metals re-
quires more consideration due to its impact on all
living organisms. Heavy metal bioaccumulation and
toxicity have been studied extensively during the
present and previous decades. The prime focus was
given to mining impacted or wastewater-contaminated
soils. However, less attention has been given to mar-
ket RTEs and their impact on human health. There-
fore, it was necessary to conduct a comprehensive
survey of heavy metals in market RTEs and their
impact on public health (Song et al. 2009). Keeping
in view the issues and consequences of heavy metal
contamination, the present study was conducted to
assess heavy metal concentrations in RTEs, including
lettuce, coriander, and carrots, collected from different
markets of Peshawar and correlate that with the con-
sumer’s health risk. The vegetables were mainly se-
lected based on their consumption as RTEs, since
they are consumed fresh and no processing is done
before its consumption. The RTEs in this study rep-
resent both leafy and rooted vegetables.
Materials and methods
Study area
The present study was carried out in Peshawar district of
Khyber Pakhtunkhwa (Fig. 1). Peshawar is the provin-
cial capital of Khyber Pakhtunkhwa, Pakistan. Accord-
ing to 2017 population census, the total population of
Khyber Pakhtunkhwa is 30,523,371, while the popula-
tion of Peshawar is composed of 1,970,042 individuals.
The markets selected for the present study comprised
well-established markets that provide food items to the
residents of Peshawar as well as other parts of the
Khyber Pakhtunhwa. These markets are located in the
center of the city and vicinity of industrial estates and
heavy traffic zones.
Environ Monit Assess (2018) 190:505
Fig. 1 Location map of the study area showing sampling sites
Sample collection
During March–May, 2016, commonly consumed
RTE samples including lettuce (Lactuca sativa),
coriander (Coriandrum sativum), and carrot
(Daucus carota subsp. sativus) were collected on
Page 3 of 15 505
four various dates from five different markets of
Peshawar, Pakistan. The RTE samples were col-
lected on 21st March, 04th April, 19th April, and
05th May 2016 from Industrial estate, Board, Ag-
riculture University, Firdos, and Hashtnaghri mar-
kets. Each sample consisted of 100 g of fresh
505 Page 4 of 15
RTE, collected in clean polythene bag and labeled
properly. From all the markets, 60 samples were
collected for each RTE separately with a total of
180 samples for the three RTEs per sampling date.
The samples were then brought to the laboratory
of Soil and Environmental Sciences Department,
The University of Agriculture Peshawar, Pakistan
for further analysis.
Sample preparation and analysis
In laboratory, the samples were first washed with
running tap water and then distilled water. These
were then oven-dried for 48 h at 72 °C to get a
constant weight. After complete drying, the sam-
ples were ground to fine powder with electric
mortal. The powdered samples were then analyzed
for selected heavy metals, following the modified
procedure of Liu et al. (2008). Briefly, 1 g of
ground plant sample was heated with 20 ml of
concentrated HNO3 and 4 ml of analytical grade
perchloric acid (HClO4) on a hot plate till the
volume reached to 3–4 ml. The solutions were
then left to cool, filtered, and the final volume
was adjusted to 50 ml with deionized water in
corning tubes. The heavy metals were then deter-
mined using atomic absorption spectrophotometer
(AAS, Perkin Elmer).
Quality control
All the chemicals, used in this experiment, were of
analytical grade. All the solutions were prepared
with deionized water obtained from Department of
Soil and Environmental Sciences, The University
of Agriculture Peshawar, Pakistan. For quality as-
surance, all the samples were analyzed in tripli-
cate; blanks and standards were run after each
batch of 10 samples.
Data analysis
Average daily intake
The average daily intake (ADI) of metals was cal-
culated following Eq. 1 previously adopted by
Khan et al. (2016) and Rehman et al. (2016). The
total ADI was calculated with the help of Eq. 2,
Environ Monit Assess (2018) 190:505
which is the sum of ADI for different RTEs as
suggested by Uddh-Söderberg et al. (2015) and
Rehman et al. (2016).
ADI ¼ Cm  Cf  Dfood intake =Bw ð1Þ
Total ADI ¼ ADILettuce þ ADICoriander þ ADICarrot ð2Þ
In Eq. 1, Cm, Cf, Dfood intake, and Bw represent the
heavy metal concentrations in RTEs (mg kg−1), conver-
sion factor, daily food intake, and average body weight
of individuals, respectively.
Exposure and risk assessment
The estimated daily dose (EDD) was calculated based
on average heavy metal concentrations in selected RTE
following formula shown in Eq. 3 (USEPA 2011;
Rehman et al. 2016),
EDD ¼ Cm  IRveg  C f  EF  ED=LE  Bw ð3Þ
In Eq. 3, IRveg EF, LE, and ED represent ingestion
rate of vegetables, exposure frequency, life expectancy
(25,550 days), and exposure duration, respectively
(Rehman et al. 2016). The values of average body
weight, conversion factor, daily food intake, exposure
duration, exposure frequency, life expectancy, and oral
reference doses (RfD) selected from literature are given
in Table 1.
Hazard quotient
The hazard quotient (HQ) was calculated using Eq. 4, so
as to estimate the extent of toxicity. HQ is the ratio of
ADI to the reference dose (RfD).
HQ ¼ ADI=RfD ð4Þ
Statistical analysis
Completely randomized design (CRD) was used with
two factors replicated three times. Factor A consisted of
five markets including Industrial Estate, Board, Agri-
culture University, Firdos, and Hashtnaghri, while factor
B was the sampling dates, i.e., 21st March, 04th April,
19th April, and 05th May.
Microsoft Excel was used to calculate the concentra-
tions (mg kg−1) and health risk index for each heavy
Environ Monit Assess (2018) 190:505 Page 5 of 15 505

Table 1 Heavy metal permissible limits and values used to calculate EDI, EDD, and HQ

Parameters Symbol Units Value References

Metal concentration Cm mg kg−1 Presented in Table 2 This study

Daily food intake Dfood intake g day−1 232 and 345 for children Khan et al. 2016
and adults
Conversion factor CF 0.085 Khan et al. 2015, 2016
Exposure frequency EF Days year−1 365 Khan et al. 2016
Exposure duration ED Years 70 Khan et al. 2016
Life expectancy LE Days 25,550 Rehman et al. 2016
Body weight BWavg kg 25, 76 for children and Khan et al. 2016
adults, respectively
Oral reference dose RfD mg kg−1 USEPA 2012; Khan et al. 2010
Permissible limits and RfD values
Lead Cadmium Chromium Nickel Copper
−3 −3 −2
RfD 3.5 × 10 -3a
1 × 10 3.0 × 10 4.0 × 10 2.0 × 10−2
a b
GB 2762–2017 0.1–0.3 0.1–0.2 0.5 10 10c
FAO/WHO 2001 0.1 0.05 2.3 10 40
a
Korre et al. (2002)
a
National Standard for Food Safety; limit of heavy metals in vegetables (GB 2762–2017) (CFDA 2017)
b
State Environmental Protection Administration, China (GB 2762–2005)
c
National Standard for Food Safety: Limit of heavy metals in Foods (GB2762–2012)

metal in the RTEs. All data were then subjected to
analysis of variance (ANOVA) using statistical package,
Statistix version 8.1. When data were found significant-
ly different, then least significant difference test at 5%
level of significance was performed. Location and
heavy metal distribution maps were prepared using
Arc-GIS software.
Results and discussion
Heavy metal concentrations in RTEs
The study area comprises open markets having high
traffic zones with less plantation and management facil-
ities. Therefore, dust and smoke released in the atmo-
sphere can easily settle down on vegetables vended in
open, manmade objects and shopkeeper’s clothing etc.
Sprinkling of water on RTEs for fresh look may further
increase the risk of heavy metal contamination.
Furthermore, the RTEs used in this experiment do not
go through any process before consumption; therefore,
consumption of such vegetables may further enhance the
health risk. Earlier, it has been suggested that cooking
process may severely affect the non-essential element
concentrations in vegetables (Somsub et al. 2008).

Heavy metal contamination of RTEs is one of the

major issues associated with human health. However,
less attention has been given to RTEs from open
markets compared to the ones grown in other envi-
ronmental conditions. Heavy metal concentrations in
RTEs collected from local markets of Peshawar are
shown in Table 2, while the mean concentrations of
these RTEs are given in Figs. 2 and 3. The analyzed
data were compared with FAO/WHO (2001) and
Chinese standards (GB2762—2017). Results indicated
that most of the heavy metals were found above the
permissible limits, particularly Pb and Cr.
Cadmium
Cadmium (Cd) is one of the most toxic metals found
ubiquitously in the environment (Khan et al. 2016, 2017).
Cd concentrations in RTE samples collected from differ-
ent markets showed significant variation among different
sampling points, while sampling dates have no significant
effects (Table 2). The highest Cd concentrations in lettuce
were recorded in samples collected from industrial estate
market (0.47 mg kg−1), which were also at par with
Firdos market (0.36 mg kg−1) and Hashtnaghri market
 505

Table 2 Heavy metal concentrations (mg kg−1) in ready-to-eat vegetables collected from different markets on various sampling dates

Sampling Ind. Board Agri. Firdos Hashtnaghari Ind. Board Agri. Firdos Hashtnaghari Ind. Board Agri. Firdos Hashtnaghari
dates Estate market Uni. market market Estate market Uni market market Estate market Uni market market
Page 6 of 15

Lettuce Coriander Carrot

Pb 21st 18.47 18.40 16.10 20.47 9.30 20.17 21.90 15.00 4.07 22.97 22.83 12.60 5.93 10.87 11.50
March
04th April 22.30 15.57 14.97 33.27 23.73 28.80 7.83 27.60 29.43 9.00 26.90 17.43 17.50 10.63 16.00
19th April 15.97 23.33 23.20 10.73 11.00 17.97 21.60 6.93 26.43 15.40 23.07 10.47 15.17 12.13 11.20
05th May 16.87 23.53 17.47 35.70 15.17 25.43 11.07 15.77 18.63 20.53 21.83 11.60 16.40 15.50 9.33
Mean 18.40 20.21 17.94 25.04 14.80 23.09 15.60 16.33 19.64 16.98 23.66 13.03 13.75 12.28 12.01
Cd 21st 0.57 0.27 0.17 0.53 0.23 0.30 0.67 0.30 0.33 0.37 0.17 0.47 0.40 0.20 0.50
March
04th April 0.53 0.20 0.23 0.27 0.30 0.23 0.70 0.43 0.63 0.97 0.07 0.87 0.53 0.53 0.47
19th April 0.37 0.13 0.33 0.37 0.30 0.47 0.10 0.53 0.20 0.57 0.37 0.47 0.20 0.37 0.53
05th May 0.40 0.30 0.13 0.27 0.47 0.30 1.00 0.27 0.63 0.77 0.20 0.93 0.63 0.33 0.17
Mean 0.47 0.23 0.22 0.36 0.33 0.33 0.62 0.38 0.45 0.67 0.20 0.69 0.44 0.36 0.42
Cr 21st 3.10 3.53 2.37 5.33 3.43 4.20 2.67 2.00 4.17 1.87 3.33 3.07 1.47 3.13 2.67
March
04th April 3.90 2.13 2.20 6.23 2.27 2.23 1.80 5.60 2.27 2.50 1.67 2.83 3.10 3.30 1.37
19th April 1.03 4.20 1.63 5.73 1.57 3.10 3.67 3.07 3.33 3.70 1.57 3.27 3.17 1.47 3.03
05th May 3.60 4.97 4.70 3.83 2.87 4.23 3.73 5.33 3.83 3.27 3.30 3.10 1.63 2.70 4.17
Mean 2.91 3.71 2.73 5.28 2.54 3.44 2.97 4.00 3.40 2.84 2.47 3.07 2.34 2.65 2.81
Ni 21st 8.50 7.63 5.03 8.50 4.30 5.13 7.93 7.30 5.23 10.57 2.30 4.17 7.07 7.10 3.13
March
04th April 7.83 7.13 3.83 4.07 5.63 1.60 7.50 3.13 6.53 4.83 2.47 2.70 4.70 2.87 2.93
19th April 3.63 4.97 8.90 6.83 2.10 8.87 7.20 4.17 5.70 7.10 2.43 3.27 3.70 4.07 6.47
05th May 6.13 6.13 6.17 6.00 2.87 6.33 5.93 5.57 3.73 7.93 3.07 3.40 2.40 3.87 3.27
Mean 6.52 6.47 5.98 6.35 3.73 5.48 7.14 5.04 5.30 7.61 2.57 3.39 4.47 4.48 3.95
Cu 21st 10.17 14.03 6.70 5.70 7.40 16.17 13.03 12.60 20.10 12.33 3.87 4.17 3.47 6.20 4.47
March
04th April 10.43 7.53 9.73 11.27 12.17 8.93 7.97 8.77 12.37 11.37 12.70 6.23 6.77 11.23 8.70
19th April 8.23 8.20 10.73 11.33 5.43 8.43 6.80 9.17 10.07 6.33 8.17 4.13 6.83 6.50 5.40
05th May 7.13 4.03 6.13 6.40 6.57 10.20 7.60 10.23 6.70 8.33 8.20 5.43 3.93 3.87 5.50
Environ Monit Assess (2018) 190:505

Mean 8.99 8.45 8.32 8.68 7.89 10.93 8.85 10.19 12.31 9.59 8.24 4.99 5.25 6.95 6.02

Ind estate Industrial Estate Market, Agri. Uni. Agriculture University Market
Environ Monit Assess (2018) 190:505 Page 7 of 15 505

30.00 Ind. State

25.00 Board market
Lettuce Coriander 20.0
20.00 Agri. Uni
Concentraons (mg kg-1)

Concentraons (mg kg-1)

Firdos market 15.0
15.00
Hashtnaghari market
10.00 10.0

5.00 5.0

0.6
0.20 0.5

0.15 0.4
0.3
0.10
0.2
0.05 0.1

0.00 0.0
Carrot Cd Cr Cu Ni Pb
20.0
Concentraons (mg kg-1)

Metals
15.0
10.0
5.0
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
Cd Cr Cu Ni Pb
Metals
Fig. 2 Mean heavy metal concentrations in ready-to-eat vegetables collected from different markets

25.0 21st March Lettuce Coriander

04th April 20.0
20.0
Concentrations (mg kg-1)

Concentrations (mg kg-1)

19th April 15.0
15.0 05th May
10.0 10.0
5.0 5.0
0.4 0.6
0.5
0.3
0.4
0.2 0.3
0.2
0.1
0.1
0.0 0.0
Carrot Cd Cr Cu Ni Pb
15.0
Concentrations (mg kg-1)

Metals
10.0

5.0
0.5
0.4
0.3
0.2
0.1
0.0
Cd Cr Cu Ni Pb
Metals
Fig. 3 Mean heavy metal concentrations in ready-to-eat vegetables collected on different sampling dates
505 Page 8 of 15
(0.33 mg kg − 1 ), while lowest concentrations
(0.22 mg kg−1) were observed in RTEs collected from
Agriculture University market (Table 2 and Figs. 2 and
3). The analysis of variance for data showed that market,
sampling date, and their interaction for Cd concentrations
in coriander were found significant (Table S1), while
sampling dates were found non-significant for carrot
(Table S1). Comparative analysis of collected data
showed that the highest Cd concentrations in coriander
and carrot were recorded in samples collected from
Hashtnaghri market (0.67 mg kg−1) and Board market
(0.68 mg kg−1), while the lowest concentrations in cori-
ander and carrot were recorded in samples collected from
industrial estate market (0.33 and 0.20 mg kg−1, respec-
tively) (Table 2 and Figs. 2 and 3). Similarly, samples
collected on 4th April and 5th May showed the highest
Cd (0.59 mg kg−1) concentrations, while minimum
(0.37 mg kg−1) concentrations were recorded in samples
collected on 19th April (Table 2 and Figs. 2 and 3). The
interaction among markets and sampling dates was sig-
nificant for samples collected from Board market on 5th
May, where the highest Cd concentrations in coriander
and carrots (1.00 and 0.93 mg kg−1, respectively) were
observed, while less significant at industrial estate market
on 4th April (0.07 mg kg−1) and Board market on 19th
April (0.10 mg kg−1) (Table 2), respectively. All the
samples were found above the maximum permissible
limits as per FAO/WHO (2001) (0.05 mg kg−1) and
Chinese Standards (GB2762—2017) (0.2 and 0.1 for leaf
and non-leafy vegetables, respectively).
Among the selected RTEs, leafy vegetables have
higher concentration of Cd. The higher Cd concentra-
tions in leafy vegetables were obvious, since higher
concentration of essential and non-essential elements
translocates to leaves, being the main site of photosyn-
thesis and transpiration (Zhou et al. 2016). Furthermore,
elevated levels of Cd in RTEs might be due to pollution
in urban environment, poor sanitary conditions and
contamination during transport to urban region
(Mahdavian and Somashekar 2008), the use of fungi-
cides, and most likely cheap phosphatic fertilizers that
are contaminated with cadmium (Booth 2005; Stephens
and Calder 2005). The excessive uses of phosphate
fertilizers by the farmers significantly increase Cd con-
centrations in plants as traces of Cd have been reported
in phosphates and phosphatic rocks (Alam et al. 2003).
Higher Cd concentrations in samples collected from
different markets (Industrial estate and Board) were
obvious as industrial activities are among the major
Environ Monit Assess (2018) 190:505
sources of air, water, and soil pollution. Furthermore,
heavy traffic on road, wastes release during industrial
activities and RTEs vended in open air on ground near
the road may also contribute to high levels of Cd in
RTEs. These results were in agreement with the findings
of Rashed et al. (2003). Ali and Al-Qahtani (2012)
reported high level of Cd (4.2 mg kg−1) in spinach and
carrot (1.20 mg kg−1) due to industrial activities and
polluted air in production and market area. Labhade
(2013) also found average Cd concentrations
(1.98 μg g−1) in coriander when samples were collected
from different sites and proposed that elevated levels
were because of urbanization and industrialization.
Similarly, Mahmood and Malik (2014) obtained 0.13–
0.61 mg kg−1 of Cd in coriander grown on soil irrigated
with untreated industrial and urban wastewater.
Chromium
Chromium (Cr) is among the toxic metals that is found
everywhere in the environment particularly in areas of
excessive mining. In this case, the results were akin to
Cd, where Cr concentrations showed significant varia-
tion among different market sites, while sampling dates
and the interaction between markets and sampling dates
were insignificant (Table S1).
Maximum Cr concentration (5.28 mg kg−1) in lettuce
was observed in samples collected from Firdos market,
while the lowest (2.53 mg kg−1) concentration was
observed in samples collected from Hashtnaghri market
(Table 2 and Figs 2 and 3). The analysis of variance
showed that Cr concentrations in coriander were found
non-significant for markets, sampling dates, and the
interaction between the two. Similarly, analysis of the
data for Cr concentrations in carrot indicated that inter-
action between markets and sampling dates was signif-
icant, while the differences among the markets and
sampling dates were non-significant (Table S1). The
data revealed that the highest Cr concentrations in cori-
ander and carrot were reported in the samples collected
from Agriculture University market on 4th April and
Hashtnaghri market collected on 5th May, while the
lowest concentrations were observed in samples from
Board and Hashtnaghri markets, collected on 4th April
(Figs. 2 and 3). All the mean values were found above
the maximum permissible levels according to Chinese
standards (GB2762—2017) (0.5 mg kg−1) and FAO/
WHO (2001) (2.3 mg kg−1) standards with a few ex-
ceptions (Tables 1 and 2).
Environ Monit Assess (2018) 190:505
This elevated Cr contamination in RTEs could be due
to several human-related activities, such as municipal
wastewater sludge deposition, urban compost
(Boularbah et al. 2006), and tanning industrial waste.
Another reason of this raised Cr concentration in RTEs
could be the use of wastewater for irrigation that affects
food chain (Rattan et al. 2002). High level of Cr in
Hashtnaghri and Board markets may be due to poor
and unhygienic conditions of these markets, as well as,
sprinkling of dirty, contaminated water on RTEs to give
them a fresh look. Kananke et al. (2014) analyzed Cr
concentrations in green leafy vegetables, which ranged
from 0.18 to 5.05 mg kg−1 around Piliyandala area of
Colombo District, Sri Lanka, due to hasty urbanization,
industrialization, and automobile activities. Similar
results of Cr concentrations were recorded in spinach
by Malik et al. (2013) where the crop was irrigated with
wastewater.
Our results are in close agreement with Khan et al.
(2013), who observed 3.4 mg kg−1 Cr concentration in
carrot due to wastewater irrigation practice. Mahmood
and Malik (2014) also found similar results of Cr con-
centration (0.98–3.01 mg kg−1) in carrot when irrigated
with wastewater.
Copper
The levels of copper (Cu) in analyzed RTEs are present-
ed in Table 2 and Figs. 2 and 3. In the present study, Cu
concentrations ranged from 4.03 to 12.17 mg kg−1 in
lettuce samples collected from different markets on var-
ious sampling dates (Table 2 and Figs. 2 and 3). The
highest Cu concentration in lettuce was recorded in
samples collected on 4th April, while the lowest was
recorded in samples collected on 5th May (Fig. 3).
Similarly, among different markets, both the highest
and lowest concentrations were reported in Board mar-
ket on different sampling dates. In coriander and carrot,
the highest Cu concentrations were observed in samples
collected from Firdos and Industrial estate markets,
while the lowest Cu concentrations were recorded in
Hashtnaghri and Agriculture University markets. Fur-
thermore, the highest Cu concentrations in coriander
and carrot were recorded in samples collected on 21st
March and 4th April, while the lowest concentrations
were recorded in samples collected on 21st March and
19th April (Table 2 and Fig. 3). The analysis of variance
showed that Cu concentrations in lettuce were found
significant for sampling dates, whereas the differences
Page 9 of 15 505
among the markets and the interaction between markets
and sampling dates were non-significant (Table S1).
Similarly, in coriander and carrot, the differences among
the sampling dates were significant, while no differ-
ences were observed among the different markets and
the interaction between markets and sampling date was
also non-significant. Cu concentrations in the studied
RTEs were within permissible limits of FAO/WHO
(2001), whereas they exceeded the limit of national food
safety standards, China (10 mg kg−1) (GB2762— 2012)
in some of the studied samples (Table 1).
High levels of Cu in green leafy vegetables could be
attributed to polluted atmosphere around the market and
use of metal-based fertilizers (Nankishore 2014), differ-
ent metals electronic repairing shops and the use of Cu-
based pesticides. Results of the present study are in line
with those of Nankishore (2014) who reported a signif-
icant higher Cu concentration in lettuce collected from
various markets of Guyana, grown on soil irrigated with
contaminated wastewater and fertilized with metal-
based fertilizers. Similarly, Mahmood and Malik
(2014) recorded 2.14–10.94 mg kg−1 Cu concentrations
in spinach grown on soil irrigated with wastewater.
The higher concentrations of Cu could be due to the
use of poor quality irrigation water, excessive use of
fertilizers, and other agricultural practices, which in turn
affect the quality of irrigation water and might accumu-
late heavy metals in higher amounts in RTEs and other
field crops (Khan et al. 2008; Hua et al. 2013).
Nickel
The result of nickel (Ni) concentrations in lettuce
showed great variation among different sampling dates
and markets, whereas the interaction between markets
and sampling dates was not significant. The highest Ni
concentration was reported in samples of Agriculture
University market, while the lowest was recorded in
Hashtnaghari market (Fig. 2). Similarly, at different
sampling dates, the highest and lowest concentrations
were reported on 19th April, depending upon type of
markets (Fig. 3).
Analysis of collected data regarding Ni concentra-
tions in coriander showed that the differences among
different markets, sampling dates as well as their inter-
action were non-significant (Table S1). In case of carrot,
the Ni concentrations varied substantially both among
the sampling dates and the markets. However, their
interaction was also significant. The results revealed that
505 Page 10 of 15
for different sampling sites and dates, maximum Ni
concentrations in coriander and carrot were observed
in samples collected from Hashtnaghri and Firdos mar-
kets, whereas minimum Ni concentrations were found
in samples collected from Agriculture University and
Industrial estate markets (Table 2 and Fig. 2). Similarly,
the highest Ni concentration was noted in samples col-
lected on 21st March, while the lowest was found in
those collected on 4th April (Table 2 and Fig. 3). All the
samples of coriander for Ni concentrations were found
below the toxicity limit proposed by FAO/WHO (2001),
except samples collected from Hashtanghri market,
which gave 10.57 mg kg−1 Ni concentration (Table 2).
Ni concentrations in RTEs, according to the current
observations, are in safe range. However, these concen-
trations might increase in future due to combustion of
coal, fuel oil, tobacco smoke, industrial and agricultural
emissions. Mahmood and Malik (2014) reported similar
results and observed high Ni concentrations in carrot
irrigated with ground water and wastewater.
Lead
Lead (Pb) concentrations in lettuce samples collected
from different markets are given in Table 2 and Figs. 2
and 3. Among different heavy metals, Pb showed the
highest concentrations in lettuce. The mean Pb concen-
trations showed significant variation among different
markets but the differences among sampling dates were
found non-significant. On the other hand, the interaction
between the markets and sampling dates was also signif-
icant (Table 2 and Figs. 2 and 3). The highest
(25.04 mg kg−1) Pb concentration was found in lettuce
samples collected from Firdos market, while the lowest
(14.80 mg kg −1 ) was reported in samples from
Hashthnagri market (Fig. 2). Analysis of data collected
on different sampling dates showed that the highest
(35.70 mg kg−1) Pb concentration was noted in samples
collected from Firdos market on 5th May, whereas lowest
Pb (9.30 mg kg−1) concentration was obtained in samples
collected from Hashtnaghri market on 21st March
(Table 2). Other RTEs, i.e., coriander and carrot, also
showed significant variations for Pb concentrations col-
lected from different markets on various sampling dates
(Figs. 2 and 3). The analysis of the collected data for
coriander showed no differences in terms of different
markets or sampling dates but the interaction between
them was significant, while in carrot, the analysis indi-
cated substantial differences among the markets but the
Environ Monit Assess (2018) 190:505
differences in sampling dates and their interaction were
non-significant (Table S1). The highest (29.43 mg kg−1)
Pb concentration in coriander was observed in samples
collected from Firdos market on 4th April, whereas the
lowest (4.07 mg kg−1) Pb concentration was recorded in
samples from Firdos and industrial estate markets on 21st
March (Table 2). Similarly, maximum (23.66 mg kg−1)
Pb concentration in carrot was recorded in samples col-
lected from Industrial estate market, while minimum
(12.01 mg kg−1) concentration was found in carrots of
Hashtnaghri market. Although great variations were ob-
served among different sampling points, all the samples
exceeded the permissible limits set by FAO/WHO (2001)
and Chinese standards (GB2762—2017) (Table 1). The
results indicated that various markets showed significant
variations in Pb concentrations, which might be attributed
to the impact of various environmental factors including
industrial emission, leaded gasoline exhaust from auto-
mobiles, unorganized urbanization (Duzgoren-Aydin
2007; Sharma et al. 2008), and excessive use of fertil-
izers, pesticides, and wastewater (Bradl 2005) for high
yield in crop production. Greater concentrations of Pb in
samples collected from Firdos and industrial estate mar-
kets could be due to heavy traffic load on road, poor
sewerage system, and atmospheric deposition as RTEs
vended in open are exposed to contaminated dust and dirt
that accumulates on surface of RTEs (AL Jassir et al.
2005). Similarly, Achakzai et al. (2011) and Perveen et al.
(2012) reported Pb concentrations in lettuce and cauli-
flower to a level of 6.32 and 50 mg kg−1 due to sewage
water. Firdos market is very crowded and dirty with huge
traffic load due to which contamination is frequent in
food items especially RTEs marketed in open air. These
results are in line with Khan et al. (2010) who determined
Pb concentrations up to 18 mg kg−1 in spinach due to
weathering of parent rocks and enrichment of soil with
metals. Similarly, Gupta et al. (2008) also reported high
concentrations (31.13 mg kg−1) of Pb in coriander due to
municipal wastewater irrigation.
Average daily intake and hazard quotient
The ADI and HQ of the selected heavy metals through
consumption of contaminated RTEs are given in Figs 4
and 5. The ADI of the selected heavy metals were in
order of Pb > Cu > Ni > Cr > Cd, while the HQ were in
order of Pb > Cr > Cu > Cd > Ni. The highest ADI were
observed for Pb, while the lowest were reported for Cd.
Similarly, the highest HQ values were reported for Pb
Environ Monit Assess (2018) 190:505 Page 11 of 15 505

0.07
Pb 21st March Cd
0.06 4th April
19th April
0.05 5th May

0.04
ADI

0.03

0.02

0.01
Markets/age groups
0.00
Cr Ni
0.010

0.008

0.006
ADI

0.004

0.002

0.000
Cu

n
ult

Adult

llt

dult

Adult
ildren

dren

n
Childre

Childre

Childre
ni./Adu
tate/Ad
0.025

arket/A
ni./Chil
market/

market/
tate/Ch

market/

market/

market/
Agri. U
Ind. Es

0.020

Firdose
Agri. U
Ind. Es

Board

aghari
ADI

Firdos

aghari
Board

0.015

Hashtn
Hashtn
0.010
Location/Age Groups

0.005

0.000
n

n
ult

Adult

llt

dult

Adult
ildren

dren

n
Childre

Childre

Childre
ni./Adu
tate/Ad

arket/A
ni./Chil
market/

market/
tate/Ch

market/

market/

market/
Agri. U
Ind. Es

Firdose
Agri. U
Ind. Es

Board

aghari
Firdos

aghari
Board

Hashtn
Hashtn

Location/Age Groups

Fig. 4 Average daily intake (ADI) of heavy metals through consumption of contaminated ready-to-eat vegetables

and lowest were reported for Ni. Among the selected
RTEs, the highest DIM and HQ values were recorded
for lettuce, followed by coriander and carrot. The high
HQ values were obvious because lettuce and coriander
are green leafy vegetables and are considered as the
hyper accumulators (Khan et al. 2015, 2016). The ADI
values for all the heavy metals were < 1 (Fig. 4).
Although the growing areas of the studied RTEs are
unknown as they are transported from all over the coun-
try to various markets in Peshawar, the high level of
toxic metals in these RTEs can be linked with poor
hygienic conditions of markets, RTEs vended in open
and unhygienic transport systems. The HQ values of Pb
in all samples collected from different markets on
505 Page 12 of 15 Environ Monit Assess (2018) 190:505

6
Pb Cd
0.5
5
0.4
4

THQ
0.3
THQ

0.2
2

1 0.1

0 0.0
Ind. Estate Ni 0.16
1.4 Cr
Board market
Agri. Uni. 0.14
1.2 Fridos market
Hashtnaghari maret 0.12
1.0
0.10

THQ
THQ

0.8
0.08
0.6
0.06
0.4
0.04
0.2 0.02

0.0 0.00
Cu

lts
ildren

ildren
lt

lts
0.45
du

dre

/Adu

/Adu
0.40
ce/A

/Chil
h

ot/Ch
ce/C

nder

t
Carro
0.35
Lettu

nder

Carr
0.30
Lettu

Coria
THQ

Coria

0.25
0.20
0.15
Vegetables / Age groups
0.10
0.05
0.00
n

re n
dult

lts

lts
ildren
hildre

/Adu

t/Adu
d
ce/A

/Chil
h
ce/C

der/C

nder

Carro
Lettu

ot
Carr
Lettu

Coria
n
Coria

Vegetables / Age groups

Fig. 5 Hazard quotient (HQ) of heavy metals through consumption of contaminated ready-to-eat vegetables

different sampling dates were > 1 posing great threats to organizations. In the present study, the ADI value was
the consumers. Similarly, the HQ of Cd, Cr, Cu, and Ni higher than RfD for Pb and Cr in some cases that
were < 1 for some RTEs while > 1 for others depending resulted in high HQ value. Among different age groups,
upon markets and type of vegetables. The HQ were < 1 children have higher ADI and HQ values than adults
for Cd, Cu, and Ni in all RTE samples, while for Cr, the and are more at risk. The higher HQ values (> 1) of
HQ were found > 1 in some samples collected from heavy metals for special group of population including
Firdos and Agriculture University markets, while other those with weak health, pregnancy, birth disorder, and
samples had HQ < 1. The mean HQ values were < 1 for compromised immune system are potentially more at
lettuce and coriander (Fig. 5). The HQ value of a par- risk than normal individuals (Li et al. 2017).
ticular metal depends on daily intake of metal and oral Human beings are exposed to heavy metal toxicity
reference dose (RfD) values suggested by different through a variety of exposure pathways depending upon
Environ Monit Assess (2018) 190:505
particular media of contamination. Among these expo-
sure pathways, RTE contamination with heavy metals is
the major exposure pathway for human beings (Khan
et al. 2015). As expressed from the results, RTEs were
tainted with toxic metals that may pose great threat to
local consumers. These results are in consistence with
the findings of Khan et al. (2010), who reported health
risk value of > 1 for Pb and < 1 for Cd, Cu, and Ni. The
significant variation observed in ADI and HQ for chil-
dren and adults might be associated with factors includ-
ing differences in body weight, exposure time, and
duration as well as metal intake (Zhou et al. 2016; Li
et al. 2017). The results showed great variation among
different RTE species across different sampling points
and dates. The findings of ADI and HQ suggest that
consumption of contaminated RTEs, purchased from
markets with unhygienic conditions, may result in
various health disorders. Furthermore, the RTEs are
consumed, as fresh vegetables, without any
postharvest processing, which may further enhance the
risk to human health.
Conclusions
Results revealed that heavy metals collected from dif-
ferent markets of Peshawar at different time showed
great variation for different RTEs and sampling dates.
Some of the heavy metals in all studied RTEs exceeded
the permissible levels set by FAO/WHO (2001) and
Chinese standards (GB2762—2017) standards. High
heavy metal concentrations were found in industrial
estate market, while low concentrations were observed
in Hashtnaghri market. Similarly, maximum heavy met-
al concentrations were observed on 4th April, while the
lowest were recorded on 21st March. Among different
RTEs, maximum heavy metal concentrations were re-
ported in lettuce. The ADI and HQ values showed great
variations. The highest HQ (> 1) values were reported
for Pb followed by Cr, while other heavy metals had
HQ < 1. The findings of this study showed that due to
unhygienic conditions of the markets and unavailability
of resources to properly handle RTEs from harvesting to
market supply may pose great risks to consumers.
Therefore, it is suggested that government authorities
should prepare guidelines and regularly visit vegetable
markets to minimize the chances of heavy metal con-
tamination. Furthermore, the government authorities
must insure regular monitoring of industries for their
Page 13 of 15 505
heavy metals discharge in environment, evaluation of
fertilizers and pesticides for metal contents and proper
disposal of industrial and municipal waste materials in
and around the city. Further studies are suggested to
observe RTEs in field conditions during their harvest
and then after transportation to the market. This will
enable us to know whether the contamination was only
due to field conditions or the transportation process and
the market conditions also had an impact.
Acknowledgments Our thanks to the support staff at the De-
partment of Soil and Environmental Sciences, The University of
Agriculture Peshawar, for their skillful technical assistance.
Funding This study was funded through a project from Higher
Education Commission (HEC) Pakistan (Project # 21-65/SRGP/
R&D/HEC/2014), which is gratefully acknowledged.
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