Water Air Soil Pollut (2019) 230: 164

https://doi.org/10.1007/s11270-019-4221-y

Sources of Soil Pollution by Heavy Metals and Their

Accumulation in Vegetables: a Review
Aneta Zwolak & Magdalena Sarzyńska &
Ewa Szpyrka & Kinga Stawarczyk

Received: 15 April 2019 / Accepted: 27 June 2019 / Published online: 6 July 2019
# The Author(s) 2019

Abstract The presence of heavy metals in food is a Apart from being influenced by the soil-related fac-
threat to human health. Exposure to heavy metals as a tors, absorption of metals differs in different types of
result of consumption of contaminated vegetables, as plants. A significant variation in metal concentrations
well as their toxicity, is a serious problem. was also found depending on their location in plant
Different branches of industry and the road traffic tissues, on plant species, or even on varieties of the same
have a significant impact on environmental pollution species.
with heavy metals. Municipal and industrial sewage also
is an important source of those substances. Furthermore, Keywords Heavy metals . Soil pollution . Vegetables .
the mineral content of vegetables depends on factors Accumulation . Contamination
such as the natural content of trace elements in the
environment, their levels in mineral fertilizers, and fer-
tilizer doses. In the soil, a natural source of these metals
is bedrock. In soils used for agricultural purposes, some 1 Introduction
quantities of metals are introduced together with fertil-
izers, both organic and mineral. Additionally, another The problem of heavy metal contamination in the envi-
sources of the metals are plant protection products. ronment is widespread. Taken up by plants, heavy metals
Heavy metal dynamics in the soil and their uptake by may enter the food chain, and therefore, humans can also
plants are influenced by soil properties, which play a key be exposed to them (Intawongse and Dean 2006). A
role in the bioavailability of these metals. Metal mobility recently published WHO/FAO report recommends con-
and assimilation are also influenced by the addition of sumption of minimum of 400 g of fruit and vegetables per
organic and inorganic matter. A significant body of evi- day (excluding potatoes and other starchy tubers) for
dence also suggest that the age of the soil plays an impor- prevention of chronic diseases such as heart diseases,
tant role in modulation of metal bioavailability to plants. cancer, diabetes, and obesity, as well as for prevention
and alleviation of several micronutrient deficiencies, es-
pecially in less developed countries (WHO 2004).
A. Zwolak (*) : M. Sarzyńska : E. Szpyrka Heavy metals are widely distributed in the environ-
University of Rzeszow, Faculty of Biotechnology, 1 Pigoń St., ment and are considered significant chemical food con-
35-310 Rzeszów, Poland taminants. The group of heavy metals includes both
e-mail: [email protected] elements essential for normal metabolic processes,
K. Stawarczyk called micronutrients (Fe, Mn, Cu, Zn, Mo), which in
Veterinary Inspectorate Mielec, Skłodowskiej 8, 39-300 Mielec, excessive quantities are more harmful to plants than to
Poland animal bodies, as well as elements such as As, Hg, Pb,
164 Page 2 of 9 Water Air Soil Pollut (2019) 230: 164

or Cd, which already at low concentrations are very that is reasonably achievable by good practices of agri-
harmful to humans and animals, while affecting plant cultural industry, and taking into account the risks asso-
growth and development to a lesser extent. ciated with food consumption. For contaminants that are
According to their toxicity to living organisms, the considered genotoxic carcinogens, or in cases where the
heavy metals can be arranged in the following order: current exposure of the population or the most vulnera-
Hg > Cu > Zn > Ni > Pb > Cd > Cr > Sn > Fe > Mn > ble population groups is close to or exceeds the tolerated
Al (Wang et al. 2003; Pueyo et al. 2004; Filipiak-Szok uptake, the highest permitted levels should be set at the
et al. 2015). lowest reasonably achievable level.
Heavy metals present in food, even in trace amounts, The exposure to cadmium, lead, and methylmercury
pose a threat to human health. In different parts of the compounds is especially dangerous during prenatal de-
world, different acceptable levels for heavy metal con- velopment and infancy, as it causes irreversible changes
tent in foodstuffs were adopted: in the central nervous system. Lead also causes cardio-
vascular diseases, disrupts heme biosynthesis and vita-
& EU Commission Regulation No 1881/2006 of 19 min D metabolism, causes kidney and liver dysfunc-
December 2006 and amending Regulation No 420/ tions and disorders of the immune and the reproductive
2011 of 29 April 2011. Setting maximum levels for systems, and disrupts iron, zinc, and copper metabolism.
certain contaminants in foodstuffs (Text with EEA Cadmium is carcinogenic, neurotoxic, and nefrotoxic,
relevance); and causes skeletal disorders, liver damage, cardiovas-
& Codex Alimentarius Commission (CODEX)-CO- cular diseases, dysfunctions of the sexual glands, and
DEX STAN 193-1995 (Amendment 2010). disrupts a mineral balance in the body. Mercury, and
Established maximum of five heavy metals: arsenic, especially the methylmercury compounds, accumulates
cadmium, lead, mercury (including methylmer- mainly in the brain tissue, causing damage to the central
cury), tin; nervous system, especially the developing fetal brain. In
& Mainland-GB 2762: Maximum levels of contami- adults, it causes hearing, speech, and visual disorders,
nants in food. Established maximum levels of six cardiovascular diseases, and limb muscle paralysis. Ar-
heavy metals: arsenic, cadmium, chromium, lead, senic has carcinogenic, neurotoxic (hearing disorders),
mercury (including methylmercury), tin; and genotoxic effects, and causes cardiovascular dis-
& US Food and Drug Administration (FDA). The US eases, peripheral vascular disorders, anemia, and dys-
Food and Drug Administration (FDA) has not functions of the reproductive system (Wojciechowska-
established regulatory limits for heavy metals in Mazurek et al. 2008; Shaheen et al. 2016).
finished food products other than bottled water. Due to their properties such as toxicity, persistence,
However, the Agency has provided guidance on and non-biodegradation, contamination with metals has
some heavy metal levels in certain foods (such as become a serious and widespread environmental threat,
candy and juice). For juice, FDA states in its “Guid- particularly in urban areas (Yang-Guang et al. 2016).
ance for Industry: Juice HACCP Hazards and Con- The problem of heavy metals stems out not only from
trols” that lead levels in juice above 50 ppb may their toxic properties but also from their ability to accu-
constitute a health hazard. With respect to candy, mulate in the body, as it is a case with all elements listed
FDA recommends a maximum lead level of 100 ppb above. At low levels of exposure to these elements,
in candy likely to be consumed by small children; clinical signs do not manifest immediately and their
& China National Standards (GB 2762-2012). effects can be observed only at the physiological or
biochemical level (Wojciechowska-Mazurek et al. 2008).
Due to differences in national legislations and the
related risk of distortion of competition, it is necessary
to introduce measures in respect of certain pollutants, 2 Sources of Contaminations with Heavy Metals
heavy metals in particular, to ensure homogeneity of the
market, with a due regard for the principle of The rapid global industrial development has resulted in a
proportionality. significantly increased risk of environmental contamina-
The maximum levels of heavy metals in foodstuffs of tion with heavy metals. Fast industrialization and disorga-
plant origin should be set at the strictest possible level nized urbanization, together with long-term use of large
Water Air Soil Pollut (2019) 230: 164 Page 3 of 9 164

amounts of fertilizers and pesticides, result in accumulation associated with vehicle wear parts, such as tires, brakes,
of toxic substances in soil, water, and air (Kishan et al. and catalysts. The re-suspension of metal-enriched road
2014; Kumar et al. 2015; Rodriguesa et al. 2017). dust caused by vehicle traffic may also be the main source
The main sources of emissions caused by human of road pollution, especially along roads with more in-
activities include: tense traffic and higher proportion of heavy vehicles
(Czarnowska and Bednarz 2000; Sternbeck et al. 2002;
& Emissions from mobile sources related to vehicle Lough et al. 2005; Wiseman et al. 2013, 2015).
transport and fuels, called linear emission A risk of heavy metal presence in vegetables culti-
& Processes of energy combustion of fuels, and indus- vated near old industrial areas is significant (Sun and
trial technological processes, discharging substances Chen 2018; Murray et al. 2011; Sung and Park 2018),
into the air through an emitter (stack) in an orga- and this kind of contamination is rather problematic.
nized manner, called point emission sources; Municipal and industrial sewage is also an important
& Emissions related to house heating in the municipal source of heavy metals. Wastewater irrigation is a com-
and household sector, called surface emission mon practice in the world, and in some metropolitan
(WIOŚ Szczecin 2015). areas, wastewater is treated biologically and used for
irrigation in agriculture. In recent years, many articles
Exposure to heavy metals resulting from consumption about soils irrigated with wastewater contaminated with
of contaminated vegetables and their toxicity is a serious heavy metals were published. On the basis of their
problem. An increased content of certain elements is studies, Mahmood and Malik (2014) showed that waste-
found particularly in vegetables grown in the vicinity of water irrigation has changed physical and chemical
industrial plants and busy roads, as well as in crops properties of the soil and led to heavy metal uptake by
exposed to municipal and agricultural wastewater. This plants, mostly vegetables. Earlier reports from Pakistan
may lead to a disrupted balance of these elements, and, in confirmed that vegetables grown in effluents accumu-
turn, significantly affect their bioavailability and interac- late higher concentrations of heavy metals than vegeta-
tion with other food ingredients, as well as other metals bles grown in groundwater (Akbar et al. 2009; Jan et al.
(Wong et al. 2006; Śmiechowska and Florek 2011). 2010; Khan et al. 2013). Similar conclusions were also
Different branches of industry, as well as road traffic, reached by Khan et al. (2008) on the basis of their
have a significant impact on environmental pollution studies conducted in China.
with heavy metals, such as the following: chrome from
metallurgical, paint, and tanning industries; nickel main-
ly from the steel industry, and burning of coal and liquid 3 Soil Factors Affecting Metal Accumulation
fuel; cadmium from metal (mostly zinc) smelters, while
along roads another source of contamination with this The mineral content of vegetables also depends on
element may be grease used in motor vehicles; and lead factors such as the natural content of trace elements in
from paint, metallurgical, and glass industries. The main the environment, their level in mineral fertilizers, and
sources of lead contamination in soils, plants, and air are fertilizer doses. In the soil, a natural source of these
the exhaust gases of motor vehicles. For many years, metals is bedrock. In soils used for agricultural pur-
lead had been added to petrol as lead tetraethyl, which poses, some quantities of metals are introduced together
was released during mechanical engine operation with fertilizers, both organic and mineral (mainly calci-
(Lityński and Jurkiewicz 1982; Nieć et al. 2013; Zhou um and phosphates). Additionally, another sources of
et al. 2016). In Poland, universal petrol (containing lead metals are plant protection products (Kabata-Pendias
tetraethyl) was withdrawn from the market in January and Pendias 1999; Antisari et al. 2015; Ye et al. 2015).
2005 and was replaced with unleaded petrol. Heavy metal dynamics in the soil and their uptake by
Numerous studies conducted in recent years found a plants depend on soil properties, which play a key role
large share of street dust in contaminants of urban soils in the bioavailability of these metals. The level of these
near traffic routes (Czarnowska and Bednarz 2000; compounds’ accumulation in plants depends on,
Sternbeck et al. 2002; Zereini et al. 2007, 2012; amongst others, soil type, pH, humidity, and
Wiseman et al. 2013, 2015). Heavy metals come from micronutrients content, as well as on the time of crop
motor vehicle exhaust emissions; their release is also harvesting (Kabata-Pendias and Pendias 1999; Järup
164 Page 4 of 9 Water Air Soil Pollut (2019) 230: 164

2003; Leitzmann 2003; Właśniewski and Hajduk be influenced by addition of organic and inorganic
2012;Yang-Guang et al. 2016; Hu et al. 2017). matter. A basic treatment restricting metal mobility is
On the basis of their research, Właśniewski and soil de-acidification by liming. Application of phos-
Hajduk (2012) associated the high cadmium content phate also affects soil heavy metal mobility and assim-
mainly with the granulometric composition of the soils, ilation by plants (Finžgar et al. 2006; Wuana and
and then with their location along busy traffic routes. Okieimen 2011; Zhang et al. 2010; Paltseva et al. 2018).
Furthermore, they showed that the cadmium content in Studies have shown that the use of phosphates stabi-
tested vegetables was, to a very small extent, associated lizes Pb by reducing its availability in the soil. However,
with the properties of the soil top layer, including a soil this effect depends on the soil type and is not sufficiently
content of total and soluble cadmium. described, similarly as plants’ ability to take up lead.
Kabata-Pendias and Pendias (1999) claimed that The researchers speculate that phosphates can mobilize
acidic soil pH is considered to be the most important As. The addition of phosphate increases soil permeabil-
factor influencing the increased absorption of heavy ity, thus contributing to arsenic migration deeper into the
metals by vegetables. This was confirmed by research soil profile and entering groundwaters. This involves
conducted by Bielecka et al. (2009), which showed that, increasing its availability and uptake by plants
in alkaline soils (pH within the range of 7.1–8.1), a risk (Scheckel et al. 2013; McBride et al. 2014; McBride
of heavy metal leaching and their bioavailability to et al. 2015; Lim and McBride 2015).
plants are lower, and the presence of organic matter Adding materials rich in organic components, such as
can inhibit metals uptake from the soil solution. By compost, sawdust, tree bark, or granulated or powdered
changing these soil properties that determine metal sol- lignite, is frequently recommended to reduce mobility
ubility in the soil, heavy metals can be immobilized in and bioavailability of metals. Some researchers suggest
its solid phase. Metal mobility and bioavailability may that regular addition of organic matter in large quantities

Table 1 Heavy metal concentration in edible parts of vegetables from China, depending on species (mg/kg). Data show mean ± standard
error of three replicates Hang et al. (2016)

Vegetable type Vegetable species Pb (mg/kg) As (mg/kg) Cd (mg/kg) Zn (mg/kg) Cu (mg/kg)

Root White radish 0.270 ± 0.057 0.099 ± 0.012 0.011 ± 0.003 4.690 ± 1.367 0.167 ± 0.073
Carrot 0.233 ± 0.001 0.188 ± 0.030 0.023 ± 0.005 1.591 ± 0.092 0.227 ± 0.011
Sweet potato 0.613 ± 0.162 0.448 ± 0.013 0.135 ± 0.007 4.674 ± 0.790 0.015 ± 0.005
National standard (China)a 0.1 0.5 0.1 – –
Stalk White caitai 0.785 ± 0.239 0.225 ± 0.043 0.239 ± 0.090 24.23 ± 5.541 0.456 ± 0.033
Red caitai 0.939 ± 0.327 0.396 ± 0.076 0.176 ± 0.038 20.95 ± 2.993 0.478 ± 0.089
National standard (China) a
0.3 0.5 0.1 – –
Solanaceous Eggplant 0.429 ± 0.001 0.072 ± 0.004 0.289 ± 0.027 2.786 ± 0.588 0.937 ± 0.199
Tomato 0.078 ± 0.023 0.014 ± 0.003 0.028 ± 0.005 1.419 ± 0.185 0.468 ± 0.036
National standard (China)a 0.1 0.5 0.05 – –
Melon Pumpkin 0.121 ± 0.031 0.073 ± 0.015 0.005 ± 0.001 2.883 ± 0.749 0.647 ± 0.104
Cucumber 0.004 ± 0.001 0.039 ± 0.014 0.004 ± 0.001 1.206 ± 0.107 0.284 ± 0.047
National standard (China)a 0.1 0.5 0.05 – –
Leafy Lettuce 1.162 ± 0.540 0.660 ± 0.086 0.460 ± 0.207 11.79 ± 1.688 0.775 ± 0.170
Spinach 0.971 ± 0.194 0.310 ± 0.064 0.513 ± 0.055 20.81 ± 4.543 0.966 ± 0.288
Cabbage 0.671 ± 0.277 0.211 ± 0.014 0.036 ± 0.022 9.926 ± 2.226 0.314 ± 0.043
National standard (China) a
0.3 0.5 0.2 – –
Legume Kidney bean 0.033 ± 0.036 0.050 ± 0.010 0.010 ± 0.017 5.669 ± 0.236 1.310 ± 0.085
Asparagus bean 0.070 ± 0.014 0.047 ± 0.014 0.013 ± 0.011 6.682 ± 1.550 1.999 ± 1.247
National standard (China)a 0.2 0.5 0.1 – –
a
The tolerance limit for contaminants specified in foodstuffs in the China National Standards (GB 2762-2012)
Water Air Soil Pollut (2019) 230: 164 Page 5 of 9 164

may inhibit metal uptake from the soil solution, and thus wet ditches and reclaimed wetlands, levels of some
would be advantageous (Brown et al. 2012; Attanayake heavy metals, such as Pb, Cd, and Zn, are much higher
et al. 2014, 2015). Defoe et al. (2014) and Karczewska in wetlands in a young region because these wetlands
et al. (2010) confirmed that organic matter stabilizes are richer in mangrove soils. Higher toxic levels of
trace elements in the soil, while Murray et al. (2011) heavy metals in flat wetlands and recovered wetlands
showed that the addition of compost may lead to in- in an old region are observed because of their long
creased accumulation of metals in cultivated plants. history of reclamation, when compared with lowland
McBride et al. (2015), on the other hand, found that wetlands (Bai et al. 2011).
Pb and As levels in vegetables were strongly correlated Apart from being influenced by the soil-related fac-
with a total content of these metals in the soil, and not tors, absorption of metals differs in different types of
with organic matter content in the soil or a level of plants. A significant variation in metal concentrations
compost addition. was also found depending on their location in plant
Bai et al. (2011) and Wiseman et al. (2015) provided tissues, on plant species and even on varieties of the
evidence that the soil age also plays an important role in same species (Szatanik-Kloc 2004; Karami et al. 2011;
modulation of metal bioavailability in plants. A higher Zhou et al. 2016).
content of heavy metals was found in old flat wetlands On a basis of her research, Szatanik-Kloc (2004)
due to long-term discharges of municipal and industrial reported that she did not observe any relevant correla-
wastewater. A multivariate analysis shows that bedrock tion between the concentration of Cr, Ni, and Cd in the
is a source of Fe and Mn, while Cu, Zn, Cd, Cr, Ni, and soil and in the plant (only Pb content in leaves showed a
Pb are of anthropogenic origin. When compared with large dependence on its contents in the topsoil).

Table 2 Concentrations of heavy metals in edible parts of vegetables from UK, depending on species and cultivar (mg/kg) Alexander et al.
(2006)

Vegetable species Vegetable cultivar Cd Pb Zn Cu

(mg/kg) (mg/kg) (mg/kg) (mg/kg)

Carrot Amsterdam 2.521 6.310 52.590 5.770

Nantes 1.812 5.010 19.020 4.43
Wlewek 2.298 7.230 33.380 4.43
European standardsb 0.1 0.1 – –
Spinach Bloomsdale 4.24 1.74 334.9 9.01
G. Thick Leaved 5.13 1.68 341.8 6.05
Grodane 6.94 1.78 380.2 10.08
European standardsb 0.3 0.3 – –
Pea Douce P 0.4282 1.399 47.99 5.163
Feltham 0.2615 0.547 36.82 5.727
Pilot 0.1785 0.508 59.9 6.722
European standardsb 0.05 0.2 – –
Onion Buffalo 4.0229 6.486 50.45 2.374
Express 3.5566 8.745 60.94 3.078
Shenshyu 3.7283 7.77 31.0 2.693
European standardsb 0.2 0.3 – –
Lettuce Corsair 9.033 11.73 160.69 12.55
Little Gem 8.173 19.68 172.17 9.97
Paris island 7.948 9.97 142.57 6.73
European standards b
0.3 0.3 – –
b
Maximum levels for certain contaminants in foodstuffs on the basis of Commission Regulation (EC) No 1881/2006 of 19 December 2006
and amending Regulation No 420/2011 of 29 April 2011
164 Page 6 of 9 Water Air Soil Pollut (2019) 230: 164

Table 3 Concentrations of heavy metals in edible parts of vegetables from Germany, depending on species (mg/kg). Data show mean ±
standard error of three replicates Säumel et al. (2012)

Vegetable type Vegetable species Pb (mg/kg) Cd (mg/kg) Cr (mg/kg) Ni (mg/kg) Cu (mg/kg) Zn (mg/kg)

Stem Kohlrabi 0.1–3.1 0.03–0.15 0.07–0.54 0.29–0.67 3.2–11.7 20.6–50.3

European standardsb 0.3 0.1 – – – –
Root Carrot 1.3–28.5 0.06–0.41 0.1–2.39 0.07–1.93 5.4–23.2 23.3–122.8
Potato 0.3–31.3 0.02–0.42 0.03–4.69 0.03–3.25 3.4–20.1 11.7–78.2
European standardsb 0.1 0.1 – – – –
Solanaceous Tomato 0.1–6.7 0.01–0.79 0.11–0.63 0.03–0.70 3.5–16.0 15.8–84.7
European standardsb 0.1 0.05 – – – –
Legume Green beans 0.1–3.5 0.01–0.04 0.08–0.46 0.27–1.3 3.5–10.5 32.4–44.2
European standardsb 0.2 0.05 – – – –
Leafy White Cabbage 0.6–2.6 0.06–0.41 0.025–0.81 0.01–1.0 3.2–6.6 26.4–46.5
European standardsb 0.3 0.2 – – – –
b
Maximum levels for certain contaminants in foodstuffs on the basis of Commission Regulation (EC) No 1881/2006 of 19 December 2006
and amending Regulation No 420/2011 of 29 April 2011

However, she found that, in the studied plants, concen- Zhong et al. (2017) reached similar conclusions on
trations of nickel, chromium, and cadmium were the the basis of tests conducted on three types of vegetables.
highest in roots, while lead levels were the highest in They have found that the concentration of heavy metals
leaves. Only in the case of cadmium acidic soil signif- in edible parts was the highest in leaf vegetables, lower
icantly contributed to an increase in its content in the in root vegetables, and the lowest in fruit vegetables.
studied plants. For the remaining studied metals, this Kabata-Pendias and Pendias (1999), Kabata-Pendias
effect was small. (2000) included root vegetables in plants particularly
Zhou et al. (2016) reported that there are clear differ- susceptible to cadmium accumulation. Furthermore,
ences in heavy metal concentrations in edible parts of they reported that cadmium is uptaken extremely easily,
various vegetables. The ability to uptake and accumu- both by the root system and leaves, generally in propor-
late heavy metals was the highest in leafy vegetables and tion to its concentration in the environment, regardless
the lowest in melon vegetables (Table 1). of the soil properties. However, acidic soil is considered
Alexander et al. (2006) reported that Cd, Cu, to be the most important factor influencing its increased
and Zn accumulated to the largest extent in lettuce phyto-assimilation. Cadmium is characterized by a high
and spinach, while the highest accumulation of Pb (up to 10) bioaccumulation index, and its content in
was noted in lettuce and onions. They also dem- plants is frequently directly proportional to its content
onstrated that vegetables of the same species ac- in the ground.
cumulated different amounts of heavy metals de-
pending on a cultivar (Table 2).
Yang et al. (2009) found that cucumber, radish, and
tomato had lower concentrations of Cd in their edible 4 Conclusions
parts than pak choi, Chinese leek, and carrots. Accumu-
lation of Cd by different plant species increases in the & Cultivation of vegetables in regions characterized by
following order: legumes vegetables < melon vegetables high density of industrial factories, or near busy
< alliums vegetables < root vegetables < solanaceous roads results in significant contamination of crops
vegetables < leafy vegetables. with heavy metals.
Säumel et al. (2012) reported that the concen- & Irrigation of agricultural fields with wastewater
tration of heavy metals in leafy vegetables is leads to their significant contamination with heavy
higher than in potato, carrot, tomato, kohlrabi, metals and, thereby, to accumulation of metals in
and green bean seeds (Table 3). vegetables cultivated there.
Water Air Soil Pollut (2019) 230: 164 Page 7 of 9 164

& It is necessary to maintain a reasonable approach to allotments). Environmental Protection and Natural
Resources., 40, 209–216 In polish.
fertilizing and the use of plant protection products,
Brown, S. L., Clausen, I., Chappell, M. A., Scheckel, K. G.,
because they also increase accumulation of these Newville, M., & Hettiarachchi, G. M. (2012). High-iron
metals in plants. biosolids compost–induced changes in lead and arsenic spe-
& Leafy vegetables and root vegetables have the ciation and bioaccessibility in co-contaminated soils. Journal
of Environmental Quality, 41, 1612. https://doi.org/10.2134
greatest ability to accumulate heavy metals; there-
/jeq2011.0297.
fore, they are not suitable for growing on contami- Czarnowska, K., & Bednarz, I. (2000). Metale ciężkie w pyle
nated soils. ulicznym Warszawy (Heavy metals in street dust from
Warsaw). Roczniki Gleboznawcze – Soil Science Annual,
51, 29–36.
Defoe, P. P., Hettiarachchi, G. M., Benedict, C., & Martin, S.
Open Access This article is distributed under the terms of the (2014). Safety of gardening on lead- and arsenic-
Creative Commons Attribution 4.0 International License (http:// contaminated urban brownfields. Journal of Environmental
creativecommons.org/licenses/by/4.0/), which permits unrestrict- Quality, 43, 2064–2078. https://doi.org/10.2134
ed use, distribution, and reproduction in any medium, provided /jeq2014.03.0099.
you give appropriate credit to the original author(s) and the source, Filipiak-Szok, A., Kurzawa, M., & Szlyk, E. (2015).
provide a link to the Creative Commons license, and indicate if Determination of toxic metals by ICP-MS in Asiatic and
changes were made. European medicinal plants and dietary supplements.
Journal of Trace Elements in Medicine and Biology, 30,
54–58. https://doi.org/10.1016/j.jtemb.2014.10.008.
Finžgar, N., Kos, B., & Leštan, D. (2006). Bioavailability and
References mobility of Pb after soil treatment with different remediation
methods. Plant, Soil and Environment, 52, 25–34. https://doi.
Akbar, F., Ishaq, M., Ihsanullah, I., & Asim, S. M. (2009). org/10.17221/3342-PSE.
Multivariate statistical analysis of heavy metals pollution in Hu, B., Jia, X., Hu, J., Xu, D., Xia, F., & Li, Y. (2017). Assessment
industrial area and its comparison with relatively less polluted of heavy metal pollution and health risks in the soil-plant-
area: a case study from the City of Peshawar and District Dir human system in the Yangtze River Delta, China.
Lower. Journal of Hazardous Materials, 176, 609–616. International Journal of Environmental Research and
https://doi.org/10.1016/j.jhazmat.2009.11.073. Public Health, 14, 1042. https://doi.org/10.3390
/ijerph14091042.
Alexander, P. D., Alloway, B. J., & Dourado, A. M. (2006).
Intawongse, M., & Dean, J. R. (2006). Uptake of heavy metals by
Genotypic variations in the accumulation of Cd, Cu, Pb and
vegetable plants grown on contaminated soil and their bio-
Zn exhibited by six commonly grown vegetables.
availability in the human gastrointestinal tract. Food
Environmental Pollution, 144, 736–745. https://doi.
Additives and Contaminants, 23, 36–48. https://doi.
org/10.1016/j.envpol.2006.03.001.
org/10.1080/02652030500387554.
Antisari, L. V., Orsini, F., Marchetti, L., Vianello, G., & Jan, F. A., Ishaq, M., Khan, S., Ihsanullah, I., Ahmad, I., &
Gianquinto, G. (2015). Heavy metal accumulation in vege- Shakirullah, M. (2010). A comparative study of human
tables grown in urban gardens. Agronomy for Sustainable health risks via consumption of food crops grown on waste-
Development, 35, 1139–1147. https://doi.org/10.1007 water irrigated soil (Peshawar) and relatively clean water
/s13593-015-0308-z. irrigated soil (lower Dir). Journal of Hazardous Materials,
Attanayake, C. P., Hettiarachchi, G. M., Harms, A., Presley, D., 179, 612–621. https://doi.org/10.1016/j.
Martin, S., & Pierzynski, G. M. (2014). Field evaluations on jhazmat.2010.03.047.
soil plant transfer of lead from an urban garden soil. Journal Järup, L. (2003). Hazards of heavy metal contamination. British
of Environmental Quality, 43, 475. https://doi.org/10.2134 Medical Bulletin, 68, 167–182. https://doi.org/10.1093
/jeq2013.07.0273. /bmb/ldg032.
Attanayake, C. P., Hettiarachchi, G. M., Martin, S., & Pierzynski, Kabata-Pendias, A. (2000). Biogeochemia kadmu. Kadm w
G. M. (2015). Potential bioavailability of lead, arsenic, and środowisku - problemy ekologiczne i metodyczne. Zeszyty
polycyclic aromatic hydrocarbons in compost-amended ur- Naukowe Komitetu Człowiek i środowisko PAN, 26, 17–24 In
ban soils. Journal of Environmental Quality, 44, 930–944. polish.
https://doi.org/10.2134/jeq2014.09.0400. Kabata-Pendias, A., & Pendias, H. (1999). Biogeochemia
Bai, J., Xiao, R., Cui, B., Zhang, K., Wang, Q., Liu, X., Gao, H., & pierwiastków śladowych. Warsaw: PWN In polish.
Huang, L. (2011). Assessment of heavy metal pollution in Karami, N., Clemente, R., Moreno-Jiménez, E., Lepp, N. W., &
wetland soils from the young and old reclaimed regions in the Beesley, L. (2011). Efficiency of green waste compost and
Pearl River Estuary, South China. Environmental Pollution, biochar soil amendments for reducing lead and copper mo-
159, 817–824. https://doi.org/10.1016/j.envpol.2010.11.004. bility and uptake to ryegrass. Journal of Hazardous
Bielecka, A., Ryłko, E., & Bojanowska, I. (2009). Zawartość Materials, 191, 41–48. https://doi.org/10.1016/j.
pierwiastków metalicznych w glebach i warzywach z jhazmat.2011.04.025.
ogrodów działkowych Gdańska i okolic (Contents of metals Karczewska, A., Lewińska, K., Agata, M., & Krysiak, A. (2010).
in soils and vegetables from Gdansk and Straszyn Soil pollution by arsenic within the allotment gardens in
164 Page 8 of 9 Water Air Soil Pollut (2019) 230: 164

Zloty Stok. Ecological Chemistry and Engineering A, 17, przedszkoli z obszaru Górnego Śląska. Journal of Ecology
927–933. and Health, 2, 55–62 In polish.
Khan, S., Cao, Q., Zheng, Y. M., Huang, Y. Z., & Zhu, Y. G. Paltseva, A., Cheng, Z., Deeb, M., Groffman, P. M., Shaw, R. K.,
(2008). Health risks of heavy metals in contaminated soils & Maddaloni, M. (2018). Accumulation of arsenic and lead
and food crops irrigated with wastewater in Beijing, China. in garden-grown vegetables: factors and mitigation strategies.
Environmental Pollution, 152, 686–692. https://doi. The Science of the Total Environment, 640-641, 273–283.
org/10.1016/j.envpol.2007.06.056. https://doi.org/10.1016/j.scitotenv.2018.05.296.
Khan, K., Khan, Y., Lu, H., Ishtiaq, M., Khan, S., Waqas, M., Wei, Pueyo, M., Lopez-Sanchez, J. F., & Rauret, G. (2004). Assessment
L., & Wang, T. (2013). Heavy metals in agricultural soils and of CaCl2, NaNO3, and NH4NO3 extraction procedures for
crops and their health risks in Swat District, northern the study of Cd, Cu, Pb and Zn extractability in contaminated
Pakistan. Food and Chemical Toxicology, 58, 449–458. soils. Analytica Chimica Acta, 504, 217–225.
https://doi.org/10.1016/j.fct.2013.05.014. Rodriguesa, A. A. Z., De Queiroz, M. E. L. R., Oliveira, A. F.,
Kishan, P. S., Bhattacharya, S., & Sharma, P. (2014). American- Heleno, A. A. F. F., Zambolim, L., Freitasa, J. F., & Morais,
Eurasian assessment of heavy metal contents of some Indian E. H. C. (2017). Pesticide residue removal in classic domestic
medicinal plants. Journal of Agricultural & Environmental processing of tomato and its effects on product quality.
Sciences, 14, 1125–1129. https://doi.org/10.5829/idosi. Journal of Environmental Science and Health. Part. B, 52,
aejaes.2014.14.10.12447. 1–8. https://doi.org/10.1080/03601234.2017.1359049.
Kumar, N., Kumar, S., Bauddh, K., Dwivedi, N., Shukla, P., Säumel, I., Kotsyuk, I., Hölscher, M., Lenkereit, C., Weber, F., &
Singh, D. P., & Barman, S. C. (2015). Toxicity assessment Kowarik, I. (2012). How healthy is urban horticulture in high
and accumulation of metals in radish irrigated with battery traffic areas? Trace metal concentrations in vegetable crops
manufacturing industry effluent. International Journal of from plantings within inner city neighbourhoods in Berlin,
Vegetable Science, 00, 1–13. https://doi.org/10.1080 Germany. Environmental Pollution, 165, 124–132.
/19315260.2014.880771. https://doi.org/10.1016/j.envpol.2012.02.019.
Leitzmann, C. (2003). Nutrition ecology: the contribution of veg- Scheckel, K. G., Diamond, G. L., Burgess, M. F., Klotzbach, J. M.,
etarian diets. The American Journal of Clinical Nutrition, 78, Maddaloni, M., Miller, B. W., Partridge, C. R., & Serda, S.
657S–659S. https://doi.org/10.1093/ajcn/78.3.657S. M. (2013). Amending soils with phosphate as means to
Lim, M. P., & McBride, M. B. (2015). Arsenic and lead uptake by mitigate soil lead hazard: a critical review of the state of the
Brassicas grown on an old orchard site. Journal of science. Journal of Toxicology and Environmental Health,
Hazardous Materials, 299, 656–663. https://doi. Part B: Critical Reviews, 16, 337–380. https://doi.
org/10.1016/j.jhazmat.2015.07.082. org/10.1080/10937404.2013.825216.
Lityński, T., & Jurkiewicz, H. (1982). Żyzność gleby i odżywianie Shaheen, N., Irfan, N. M., Khan, I. N., Islam, S., Islam, M. S., &
się roślin. Warszawa: PWN In polish. Ahmed, M. K. (2016). Presence of heavy metals in fruits and
Lough, G., Schauer, J. J., Park, J. S., Shafer, M. M., Deminter, J. vegetables: health risk implications in Bangladesh.
T., & Weinstein, J. (2005). Emissions of metals associated Chemosphere, 152, 431–438. https://doi.org/10.1016/j.
with motor vehicle roadways. Environmental Science & chemosphere.2016.02.060.
Technology, 39, 826–836. https://doi.org/10.1021/es048715f. Śmiechowska, M., & Florek, A. (2011). Content of heavy metals
Mahmood, A., & Malik, R. N. (2014). Human health risk assess- in selected vegetablesfrom conventional, organic and allot-
ment of heavy metals via consumption of contaminated ment cultivation. Journal of Research and Applications in
vegetables collected from different irrigation sources in Agricultural Engineering, 56, 152–156.
Lahore, Pakistan. Arabian Journal of Chemistry, 7, 91–99. Sternbeck, J., Sjödin, A., & Andréasson, K. (2002). Metal emis-
https://doi.org/10.1016/j.arabjc.2013.07.002. sions from road traffic and the influence of resuspension—
McBride, M.B., Shayler, H.A., Spliethoff, H.M., Mitchell, R.G., results from two tunnel studies. Atmospheric Environment,
Marquez-Bravo, L.G., Ferenz, G.S., Russell-Anelli, J.M., 36, 4735–4744. https://doi.org/10.1016/S1352-2310(02
Casey, L., Bachman, S. (2014). Concentrations of lead, cad- )00561-7.
mium and barium in urban garden-grown vegetables: the Sun, Z., & Chen, J. (2018). Risk assessment of potentially toxic
impact of soil variables. Environmental Pollution, 194, elements (PTEs) pollution at a rural industrial wasteland in an
254–261. https://doi.org/10.1016/j.envpol.2014.07.036. abandoned metallurgy factory in North China. International
McBride, M. B., Shayler, H. A., Russell-Anelli, J. M., Spliethoff, Journal of Environmental Research and Public Health, 15,
H. M., & Marquez-Bravo, L. G. (2015). Arsenic and lead 85. https://doi.org/10.3390/ijerph15010085.
uptake by vegetable crops grown on an old orchard site Sung, C. Y., & Park, C. B. (2018). The effect of site- and
amended with compost. Water, Air, & Soil Pollution, 226, landscape-scale factors on lead contamination of leafy vege-
265–279. https://doi.org/10.1007/s11270-015-2529-9. tables grown in urban gardens. Landscape and Urban
Murray, H., Pinchin, T. A., & Macfie, S. M. (2011). Compost Planning, 177, 38–46. https://doi.org/10.1016/j.
application affects metal uptake in plants grown in urban landurbplan.2018.04.013.
garden soils and potential human health risk. Journal of Szatanik-Kloc, A. (2004). Wpływ pH i stężenie wybranych metali
Soils and Sediments, 11, 815–829. https://doi.org/10.1007 ciężkich w glebie na ich zawartość w roślinach. Acta
/s11368-011-0359-y. Agrophysica, 4, 177–183 In polish.
Nieć, J., Baranowska, R., Dziubanek, G., & Rogala, D. (2013). Wang, Q., Cui, Y., Liu, X., Dong, Y., & Christie, P. (2003). Soil
Narażenie środowiskowe dzieci na metale ciężkie zawarte w contamination and plant uptake of heavy metals at polluted
glebach z placów zabaw, boisk, piaskownic i terenów sites in China. Journal of Environmental Science and Health,
Water Air Soil Pollut (2019) 230: 164 Page 9 of 9 164

Part A, 38, 823–838. https://doi.org/10.1081/ESE- implications in southern China’s largest city, Guangzhou.
120018594. Journal of Cleaner Production, 115, 122–129. https://doi.
WHO. 2004. Fruit and Vegetables for Health -Report of a Joint org/10.1016/j.jclepro.2015.12.031.
FAO/WHO Workshop, 1–3 September 2004, http://www. Ye, X., Xiao, W., Zhang, Y., Zhao, S., Wang, G., Zhang, Q., &
fao.org/3/a-y5861e.pdf, Accesed January 2019. Wang, Q. (2015). Assessment of heavy metal pollution in
WIOŚ Szczecin. 2015. Stan środowiska w województwie vegetables and relationships with soil heavy metal distribu-
zachodniopomorskim Wojewódzki Inspektorat Ochrony tion in Zhejiang province, China. Environmental Monitoring
Środowiska w Szczecinie. Report 2015. Accesed January and Assessment, 187, 378. https://doi.org/10.1007/s10661-
2019. www.wios.szczecin.pl/bip/files/.../VII_Ochrona_ 015-4604-5.
powietrza.pdf. In polish. Zereini, F., Wiseman, C. L. S., & Püttmann, W. (2007). Changes in
Wiseman, C. L., Zereini, S. F., & Püttmann, W. (2013). Traffic- palladium, platinum, and rhodium concentrations, and their
related trace element fate and uptake by plants cultivated in spatial distribution in soils along a major highway in
roadside soils in Toronto, Canada. The Science of the Total Germany from 1994 to 2004. Environmental Science &
Environment, 442, 86–95. https://doi.org/10.1016/j. Technology, 41, 451–456. https://doi.org/10.1021/es061453s.
scitotenv.2012.10.051. Zereini, F., Alsenz, H., Wiseman, C. L. S., Püttmann, W., Reimer,
Wiseman, C. L., Zereini, S. F., & Püttmann, W. (2015). Metal and E., Schleyer, R., Bieber, E., & Wallasch, M. (2012). Platinum
metalloid accumulation in cultivated urban soils: a medium- group elements (Pt, Pd, Rh) in airborne particulate matter in
term study of trends in Toronto, Canada. The Science of the rural vs. urban areas of Germany: concentrations and spatial
Total Environment, 15, 564–572. https://doi.org/10.1016/j. patterns of distribution. The Science of the Total
scitotenv.2015.08.085. Environment, 416, 261–268. https://doi.org/10.1016/j.
Właśniewski, S., & Hajduk, E. (2012). Akumulacja kadmu w scitotenv.2011.11.070.
glebach i wybranych warzywach uprawianych w ogrodach Zhang, M. K., Liu, Z. Y., & Wang, H. (2010). Use of single
działkowych Rzeszowa. Roczniki Gleboznawcze – Soil extraction methods to predict bioavailability of heavy metals
Science Annual, 48, 55–60. In polish. in polluted soils to rice. Communications in Soil Science and
Wojciechowska-Mazurek, M., Starska, K., Brulińska-Ostrowska, Plant Analysis, 41, 820–831. https://doi.org/10.1080
E., Plewa, M., Biernat, U., & Karłowski, K. (2008). /00103621003592341.
Monitoring of contamination of foodstuffs with elements
Zhong, T., Xue, D., Zhao, L., & Zhang, X. (2017). Concentration
noxious to human health. Part I. Wheat cereal products,
of heavy metals in vegetables and potential health risk as-
vegetable products, confectionery and products for infants
sessment in China. Environmental Geochemistry and Health,
and children (2004 year). Rocznik PZH, 59, 251–266.
40, 313–322. https://doi.org/10.1007/s10653-017-9909-6.
Wong, C. S. C., Li, X., & Thornton, I. (2006). Urban environmen-
tal geochemistry of trace metals. Environmental Pollution, Zhou, H., Yang, W. T., Zhou, X., Liu, L., Gu, J. F., Wang, W. L.,
142, 1–16. https://doi.org/10.1016/j.envpol.2005.09.004. Zou, J. L., Tian, T., Peng, P. Q., & Liao, B. H. (2016).
Wuana, R. A., & Okieimen, F. E. (2011). Heavy metals in con- Accumulation of heavy metals in vegetable species planted
taminated soils: a review of sources, chemistry, risks and best in contaminated soils and the health risk assessment.
available strategies for remediation. ISRN Ecology, 1–20. International Journal of Environmental Research and
https://doi.org/10.5402/2011/402647. Public Health, 13, 289. https://doi.org/10.3390
Yang, Y., Zhang, F. S., Li, H. F., & Jiang, R. F. (2009). /ijerph13030289.
Accumulation of cadmium in the edible parts of six vegetable
species grown in Cd-contaminated soils. Journal of Publisher’s Note Springer Nature remains neutral with regard to
Environmental Management, 90, 1117–1122. https://doi. jurisdictional claims in published maps and institutional
org/10.1016/j.jenvman.2008.05.004. affiliations.
Yang-Guang, G., Qin, L., & Yan-Peng, G. (2016). Metals in
exposed-lawn soils from 18 urban parks and its human health