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Microelements and Heavy Metals Content in Frequently Utilized Medicinal Plants Collected from the Power Plant Area

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Natural Product Communications
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  • Institute for Plant Protection and Environment, Belgrad, Serbia

Abstract and Figures

The effectiveness of medicinal plants is mainly associated with their active constituents, but one of the major quality problems frequently encountered is their high trace metals content that can be associated to extensive pollution of the environment where medicinal plants grow. Therefore the aim of this research was to evaluate the content of Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn and As in selected and frequently used medicinal plants, including chicory, broadleaf, common comfrey and dandelion. The plant material was collected from their wild habitats in the area of highly developed power plant activity during the summer of 2015. Plant analyses were done according to ICP methodology, using ICAP 6300 ICP optical emission spectrometer. The obtained results showed that the content of As, Cd, Co, Mn, Ni and Zn in the investigated medicinal plant species was below the maximum permissible concentration, while in all parts of all studied plants the concentration of Cr was toxic. The toxic concentrations of Cu were determined in root and aerial parts of chicory and common comfrey, and the toxic concentrations of Fe in root and aerial parts of dandelion and broadleaf plantain, and in aerial parts of common comfrey. However, high but not toxic content of Pb was found in aerial parts of chicory. It can be concluded that medicinal plants from the studied growing site are not appropriate for use in alternative medicine and that a determination of trace metals content in these plants must become a standard criterion for evaluation of their quality.
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Microelements and Heavy Metals Content in Frequently Utilized
Medicinal Plants Collected from the Power Plant Area
Aleksandra Stanojković-Sebića*, Jelena Maksimovića, Zoran Dinića, Dobrivoj Poštićb, Renata Iličićc,
Aleksandar Stanojkovićd and Radmila Pivića
aDepartment for Soil Reclamation, Institute of Soil Science, 11000 Belgrade, Serbia
bInstitute for Plant Protection and Environment, 11000 Belgrade, Serbia
cFaculty of Agriculture, University of Novi Sad, 21000 Novi Sad, Serbia
dInstitute for Animal Husbandry, 11080 Belgrade-Zemun, Serbia
astanojkovic@yahoo.com
Received: May 30th, 2016; Accepted: November 24th, 2016
The effectiveness of medicinal plants is mainly associated with their active constituents, but one of the major quality problems frequently encountered is their
high trace metals content that can be associated to extensive pollution of the environment where medicinal plants grow. Therefore the aim of this research was
to evaluate the content of Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn and As in selected and frequently used medicinal plants, including chicory, broadleaf, common
comfrey and dandelion. The plant material was collected from their wild habitats in the area of highly developed power plant activity during the summer of
2015. Plant analyses were done according to ICP methodology, using ICAP 6300 ICP optical emission spectrometer. The obtained results showed that the
content of As, Cd, Co, Mn, Ni and Zn in the investigated medicinal plant species was below the maximum permissible concentration, while in all parts of all
studied plants the concentration of Cr was toxic. The toxic concentrations of Cu were determined in root and aerial parts of chicory and common comfrey, and
the toxic concentrations of Fe in root and aerial parts of dandelion and broadleaf plantain, and in aerial parts of common comfrey. However, high but not toxic
content of Pb was found in aerial parts of chicory. It can be concluded that medicinal plants from the studied growing site are not appropriate for use in
alternative medicine and that a determination of trace metals content in these plants must become a standard criterion for evaluation of their quality.
Keywords: Heavy metals, Chicory, Broadleaf, Common comfrey, Dandelion, Power plant.
For the majority of the world population medicinal plants represent
the primary source of the health care. An effectiveness of medicinal
plants is mainly associated with their constituents such as essential
oils and secondary metabolites. As it was reported by the World
Health Organization (WHO), about 80% of people in peripheral
communities use only medicinal herbs for the treatment of many
diseases [1]. When the herbs are used in the treatment of certain
illnesses, it should be known that, besides the pharmacological
effect they have, the medicinal plants could be toxic if the content
of heavy metals in them is elevated. This can be associated to
extensive pollution of the environment where medicinal plants grow
since the plants can be easily contaminated by heavy metals in the
course of cultivation or later during the processing stage [2]. Along
with other pollutants, heavy metals can be added into the
environment through industrial activities, municipal wastes,
automobile exhaust, pesticides and fertilizers used in agriculture [3].
Several heavy metals such as Fe, Mn, Zn, Cu, Ni and Mo, in low
concentrations, are considered to be essential micronutrients for
plants. However, a high concentration of heavy metals causes
several problems, including toxicity of plants, animals and humans
[4]. As heavy metals pose a hazard to human and animal health,
their content in plants used for consumption or medicinal purposes
must be limited [5]. Therefore, controlling the heavy metal
concentrations in both medicinal plants and their products should be
made to ensure safety and effectiveness of herbal products.
Regarding the preceding comments, the main purpose of this
research was to evaluate the content of cadmium (Cd), cobalt (Co),
chromium (Cr), copper (Cu), iron (Fe), manganese (Mn), nickel
(Ni), lead (Pb), zinc (Zn) and arsenic (As) in selected and frequently
used medicinal plants, including chicory (Cichorium intybus L.),
broadleaf (Plantago major L.), common comfrey (Symphytum
officinale L.) and dandelion (Taraxacum officinale F. H. Wigg.).
The behavior of heavy metals and microelements in the soil is
conditioned by many factors that may affect their mobility and
accumulation by plants, and the most important are soil reaction,
organic matter content and the percentage of colloidal clay [6].
Table 1 displays the data on total concentrations of the
microelements and heavy metals in the study soil. The overall
concentrations of Cd, Co, Cr, Cu, Fe, Mn, Pb, Zn and As in the soil
samples correspond to the usual levels in agricultural soils and were
within the permissible limits, except for the content of Ni which
exceeds the maximum permissible concentrations (MPC) [7-10].
This may be the result of anthropogenic activity, where Ni enters
the soil mostly due to atmospheric deposition by the coal, oil and
diesel burning. In addition, the concentrations of Cr and Cu are
high but do not exceed the MPC. Cr is mainly found in the soil in
basic and ultrabasic rocks, which is the main source of geochemical
origin of this metal in the soil. As for Ni, in industrial regions Cu
mainly enters the soil by deposition from the atmosphere, so its high
concentration in the soil is usually of anthropogenic origin [9].
Nevertheless, the impact of flood waters containing heavy metals
may also be the reason for increased content of some trace metals in
the soil from the study area which is characterized by highly
developed power plant activities and affected by the great floods in
May, 2014.
An analytical determination of heavy metals in medicinal plants is a
significant part of quality control in order to establish the plants
purity, safety and efficacy since human activities, such as industry
and agriculture, promote trace metals release into the environment
[11]. Figures 1-4 show the concentrations of microelements and
heavy metals in the root and aerial parts of the studied medicinal
plants compared to the the reference values for plants normal and
toxic concentrations (Table 2).
NPC Natural Product Communications 2017
Vol. 12
No. 2
185 - 188
186 Natural Product Communications Vol. 12 (2) 2017 Stanojković-Sebić et al.
Table 1: Total content of trace elements (mg kg-1) in soil under studied plants.
Trace
elements
Plant species MPC
(mg kg-1)
C. intybus P. major S. officinale T. officinale
Cd 0.56±0.02*
0.54-0.58**
0.57±0.03
0.55-0.60
0.55±0.02
0.53-0.57
0.48±0.02
0.46-0.50 3a
Co 19.11±0.34
18.78-19.45
15.75±0.22
15.54-15.98
16.96±0.17
16.78-17.12
19.37±0.24
19.21-19.65 30b
Cr 78.71±0.23
78.56-78.97
82.11±0.34
81.78-82.45
84.61±0.42
84.15-84.98
81.21±0.66
80.56-81.87 100a
Cu 92.05±0.56
91.45-92.15
91.35±0.20
91.12-91.49
89.98±0.45
89.56-90.45
93.81±0.34
93.45-94.12 100a
Fe 29920±684
29150-30457
31345±579
30978-32012
30160±711
29457-30879
34491±612
33897-35120 50000d
Mn 724.67±5.03
720-730
428.67±9.29
421-439
481.00±7.55
474-489
749.33±16.92
735-768
1500-
3000c
Ni 76.37±0.55
75.78-76.87
69.25±0.47
68.87-69.78
71.86±0.22
71.69-72.11
81.86±0.40
81.45-82.24 50a
Pb 21.81±0.42
21.41-22.24
20.68±0.32
20.34-20.98
19.93±0.29
19.65-20.23
14.16±0.35
13.78-14.48 100a
Zn 94.38±0.38
94.02-94.78
111.55±0.38
111.23-111.97
111.75±0.45
111.23-112.05
91.37±0.41
90.97-91.78 300a
As 8.60±0.37
8.23-8.97
3.46±0.37
3.04-3.94
3.80±0.21
3.59-4.01
9.86±0.38
9.48-10.24 25a
*means ± standard deviation; ** intervals; MPC - maximum permissible concentrations:
a[7], b[8], c[9], d[10].
Table 2: Reference values for trace elements normal and toxic concentrations in plants.
Element Normal concentrations Toxic concentrations
(mg kg-1)
Cu 3-15a 20
b
Ni 0.1-5a 30
b
Pb 1-5a 20
b
Cr <0.1-1a 2
b
Cd <0.1-1a 10
b
Mn 15-100e 400
b
Zn 15-150a 200
b
Co 0.05-0.5e 30-40d
Fe 50-250
f
(>500)
f
As 10-60c* <2
c
*µg kg-1; reference values: a[12], b[13], c[14], d[9], e[15], f[16].
One of the most important role of Mn in plants is its involvement in
the breakdown of water molecules with the releasing of oxygen,
although, for its full metabolic activity, Mn is only required at low
concentration [17].
Zn and Cu are considered to be an essential elements for
humans, animals and plants growth and play a significant role in
various metabolic processes [18]. The normal Zn concentration
in plants ranges from 15 to 150 mg kg-1 [12], while the plant
toxic concentrations of this element is 200 mg kg-1 [13]. The
concentrations of Cu in many plant species varies between 20
and 30 mg kg-1 on dry weight basis. If its concentration in dry
plant material is higher than 20-100 mg kg-1, it becomes
phytotoxic [19].
The appropriate concentration of Fe in all plant species is
essential both for the health of plants and for the nutrient supply
to humans and animals. The normal Fe concentration in plants
used for animal nutrition ranges from 50 to about 250 mg kg-1,
while the nutritional requirements of grazing animals for this
element are generally present at concentrations within the range
of 50-100 mg kg-1 [9, 16]. Pb and Cd are trace metals which are
not essential for either humans, animals or plants, and in humans
could easily induce toxic effects at low concentrations. Pb as a
pollutant can be detected in all environmental and biological
systems. Sources of Pb contamination are the products of
combustion in the metallurgical and chemical industry,
transportation, industrial waste waters and landfills [20]. Similarly
to Pb, Cd is a widespread metal in nature characterized as toxic
industrial pollutant with expressed mobility [21]. The maximum
permissible concentration of Cd in edible plants is as low as 1 μg
kg-1 [22]. Hence, low levels of Cd in the studied plants is a highly
desirable outcome.
Figure 1: Concentrations of zinc (Zn), manganese (Mn), iron (Fe) and copper (Cu) in
the plants root (mg kg-1).
Figure 2: Concentrations of zinc (Zn), manganese (Mn), iron (Fe) and copper (Cu) in
the plants aerial parts (mg kg-1).
Figure 3: Concentrations of cobalt (Co), cadmium (Cd), arsenic (As), nickel (Ni),
chromium (Cr) and lead (Pb) in the plants root (mg kg-1).
Figure 4: Concentrations of cobalt (Co), cadmium (Cd), arsenic (As), nickel (Ni),
chromium (Cr) and lead (Pb) in the plants aerial parts (mg kg-1).
The compounds of As are highly toxic and after Pb they represent
the highest toxicological risk to humans and domestic animals [23].
As for most plant species, it is their common constituent and could
be passively taken up by them with the water flow. Concentrations
of As in edible plants vary highly, most commonly in the range
from 10 to 60 μg kg-1, while the tolerance for this element in plants
is established as 2 mg kg-1 [14, 24]. As for Cd and Pb, the
0.0 200.0 400.0 600.0 800.0 1,000.0
Cu
Fe
Mn
Zn
Concentration (mg kg
-1
)
Trace elements
T. offic inale
C. intybu s
P. m a jo r
S. officinale
0.0 100.0 200.0 300.0 400.0 500.0 600.0 700.0 800.0
Cu
Fe
Mn
Zn
Concen tration (mg kg
-1
)
Trace elements
T. officinale
C. intybu s
P. m a jo r
S. officinale
0.0 1.0 2.0 3.0 4.0 5.0
Co
Cd
As
Ni
Cr
Pb
Concentration (mg kg
-1
)
Trace elements
T. o ff ic in a le
C. intybus
P. m a jo r
S. officinale
0.0 2.0 4.0 6.0 8.0 10.0 12.0 14.0 16.0
Co
Cd
As
Ni
Cr
Pb
Concentration (mg kg
-1
)
Trace elements
T. officinale
C. intybu s
P. m a jo r
S
. officina le
Medicinal plants and trace metals Natural Product Communications Vol. 12 (2) 2017 187
undetectably low levels of As in tested medicinal plants in this
study is highly acceptable because of its high toxicity to both
humans and animals.
Ni is an essential element required for growth and absorption of Fe,
but its presence in high concentrations can disturb the life processes
causing chlorosis, intercostal necrosis and reduced root growth. The
average Ni content in plants is 0.1-5.0 mg kg-1 of dry matter [13].
Cr is an essential element for humans as a nutritional enhancement
to glucose metabolism, and for animals due to its essential role in
normal metabolism of carbohydrates and lipids. As for the plant
growth, Cr was never considered as an essential element, but some
of its stimulative effects were reported. Toxic effects in plants is
manifested in the form of chlorosis [23, 25]. The phytotoxic
concentrations of Cr in tops of plants were as follows: 18 to 24 (mg
kg-1) in tobacco, 4 to 8 (mg kg-1) in corn and 10 (mg kg-1) in barley
seedlings [9].
Cobalt is essential to humans and animals as the vital trace mineral
and the main constituent of cobalamin, also known as vitamin B12,
but required in small amounts for daily body growth and
maintenance. For plants Co is not classified as an essential element,
however, it is usually described as “beneficial”. This trace element
can be a contaminant in soils due to agricultural additives or metal
refineries [26]. Regarding its toxicity in plants, commonly reported
critical Co levels range from 30 to 40 mg kg-1 [9].
Results concerning the concentrations of Zn, Mn, Fe and Cu in the
plants root and aerial parts (Figures 1 and 2) showed the following:
Mn and Zn concentrations were below the maximum permissible
[12-13, 15] in all the analyzed parts of the tested plant species; the
toxic concentrations of Cu [13] were determined in root and aerial
parts of chicory and common comfrey; the toxic concentrations of
Fe [16] were registered in root and aerial parts of dandelion and
broadleaf plantain, and in aerial parts of common comfrey.
Results on the content of Pb, Cr, Ni, Cd, Co and As in the plants
root and aerial parts (Figures 3 and 4) showed the following:
concentrations of As, Cd, Co and Ni were below the maximum
permissible [9, 13-14] in all the analyzed parts of the tested plant
species; the toxic concentrations of Cr [13] were determined in all
parts of all studied plants; high but not toxic content of Pb [12-13]
was found in aerial parts of chicory.
Accessibility, adoption and phytotoxicity of heavy metals are not
only conditioned by their total content in the soil, but also by
chemical form, affinity of plant, and individual or interactive effect
of different soil properties. A dominant influence on increased and
toxic content of trace metals determined in the studied plant species
has a pH value of soil. Generally, in soils with low pH, the mobility
of metal cations is increased, whereas in soils with high pH the
mobility is decreased [9].
Floodwater could also be an important source of determined high
and toxic levels of heavy metals in plants. The plants that were in or
near flooded areas, should not be used in alternative medicine.
Further control of trace metals content in the plants from the studied
area is necessary in order to prevent their entry into the food chain
and to ensure the healthy food production.
Experimental
Study area: The investigation was conducted at wild habitats in the
city of Obrenovac, located about 30 km southwest of Belgrade in
Serbia, during the summer of 2015. The study area is characterized
by highly developed industrial activities since it is located in the
middle of the power plants A and B (TENT A and TENT B), at the
distance of about 5 km from each of them. Obrenovac is also known
as a city mostly affected by the floods during May, 2014. The
studied soil type, under all plant species sampled, was Calcic
Gleysol [27]. This soil is a hydromorphic black soil, developed
under the influence of groundwater and classified in A-G class. It is
characterized with both humic and gleyic horizons which give this
soil its name [28]. It is clayey soil with the following granulometric
composition: the content of sand fractions (>0.02 mm) - 38.0%, the
content of silt fractions (0.02-0.002 mm) - 25.4%, the content of
clay fraction (<0.002 mm) - 36.6% [29]. According to the reference
values [30], the soil analyzed in this study is characterized as
slightly acid in reaction, having high levels of available potassium,
low levels of available phosphorus, containing medium levels of
SOM and medium to well provided with total nitrogen.
Sampling, preparation and analysis of the soil and plant material:
Four soil samples, in triplicates, were taken from the rhizosphere of
the tested species, from the depth of 0-30 cm. The soil samples were
air-dried, crushed and passed through a sieve (≤ 2 mm). In order to
provide the representative subsampling for analysis, soil fractions
smaller than 2 mm were crushed into dust by hand. The total
contents of Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn and As in soil
samples were determined by inductively coupled plasma-atomic
emission spectrometry - THERMO iCAP 6300 Duo (radial/axial
view versions) ICP-OES, after the digestion of the samples with
aqua regia [31-32]. For checking the accuracy of analytical results,
the Certified European Reference Material ERM® - CC141 for loam
soil was used. The following plant species, both aerial parts and
root, were sampled: C. intybus, P. major, S. officinale and T.
officinale. The sampled plant material were dried at 105oC for a
period of 2 hours, using gravimetric method for determination of
dry matter contents of plant tissues [33]. Plant material was then
ground to 0.5 to 1.0 mm particle size to ensure homogeneity and to
facilitate organic matter digestion. The contents of Cd, Co, Cr, Cu,
Fe, Mn, Ni, Pb, Zn and As in aerial parts and root of the selected
medicinal plants were determined in triplicates with THERMO
iCAP 6300 Duo (radial/axial view versions) ICP-OES after the
digestion of the samples with concentrated HNO3 and redox
reaction with H2O2 for total forms extraction [34].
Calibration standards for both soil and plant material were in the
range of 0-10 ppm, except for iron (0-25 ppm). The ICP detection
limits (LOD) for soil and plant material are given in Table 3.
Table 3: The ICP detection limits for soil and plant material.
Trace elements LOD for soil (mg kg-1) LOD for plant material (mg kg-1)
Cd 0.0111 0.013
Co 0.0201 0.041
Cr 0.0931 0.053
Cu 0.1483 0.088
Fe 3.4387 0.430
Mn 0.1902 0.025
Ni 0.1493 0.029
Pb 0.0731 0.062
Zn 0.1987 0.060
As 0.0499 0.055
LOD - low limits of detection
Data analysis: The obtained data on microelements and heavy
metals concentration in the soil studied represent the arithmetic
means of three replicates of each sampling, their ranges and
standard deviations values. The data on microelements and heavy
metal concentrations in the studied plant species are presented by
figures as the bar charts with standard deviation values.
Acknowledgments - The study was financially supported by the
Ministry of Education, Science and Technological Development of
Republic of Serbia, Project TR-37006.
188 Natural Product Communications Vol. 12 (2) 2017 Stanojković-Sebić et al.
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... Symphytum officinale (comfrey). Studies qualitatively described the composition of comfrey 73,74 , and the in vitro modelling of Pb-tannin chelation in planta 75 . In a cluster containing coltsfoot too, comfrey demonstrated measurably higher Fe levels than other medicinal plants, as well as Zn and Cr 73 . ...
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... The most frequent contaminants of medicinal plants are pesticide residues, heavy metals, mycotoxins, polycyclic aromatic hydrocarbons and pyrrolizidine alkaloids [18]. Pollution of the environment with heavy metals causes these metals to penetrate plants growing on contaminated soils [19,20]. The European Pharmacopeia sets limits for some popular heavy metals, including cadmium, lead, mercury, arsenic, cobalt, nickel, vanadium and thallium, which can be found in plant materials [21,22]. ...
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Chapter
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