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https://doi.org/10.1007/s12011-020-02072-4
Abstract
This study evaluates essential and toxic element contents in dragon (Hylocereus undatus (Haworth) Britton and Rose) and
pomegranate (Punica granatum L.) and possible health risks through the consumption of these fruits. Total concentrations of
15 chemical elements (Al, Br, Ca, Cd, Cl, Cr, Cu, Fe, Hg, K, Mn, Na, Ni, Pb, and Zn) were determined by instrumental neutron
activation analysis (INAA) and atomic absorption spectrometry (AAS) techniques. This study indicates that these fruits are a vital
source of essential elements for human health. It is observed that Pb concentrations were higher in both fruits whereas Cd
concentrations were slightly higher than WHO/FAO tolerable levels only in pomegranate. The estimated daily intake (EDI) of the
chemical elements was within the maximum tolerable daily intake (MTDI) values. Furthermore, target hazard quotient (THQ)
values were also within the safe level (THQ < 1). However, the calculated target carcinogenic risk (TCR) values of Cd for
pomegranate and Cr for dragon fruit were higher than the maximum limit (1.0 × 10−4) for children. Finally, this study will create
public awareness about micronutrient contents as well as metal contaminations of the studied fruits.
Keywords Essential elements . Toxic elements . Fruits . Dietary intake . Health risks . Instrumental neutron activation analysis .
Atomic absorption spectrometry
(Hylocereus undatus (Haworth) Britton and Rose) is consid- TRIGA MARK-II research reactor (neutron flux of 1.70 ×
ered as a popular and attractive fruit all over the world. 1013 cm−2 s−1) of Bangladesh Atomic Energy Commission
Currently, it is cultivated in tropical and subtropical regions (BAEC). The activities of the irradiated samples and standards
of the world. Bangladesh has also started to cultivate this fruit were measured using a high-resolution HPGe detector (reso-
about 5 years ago. Previous research has shown that dragon lution of FWHM is 1.88 keV at 1332.5 keV of 60Co) coupled
fruit has significant health benefits like treatments for memory with a digital gamma spectrometry system. For processing of
losses, prevention of cancer, control of blood cholesterol and the gamma-ray spectra and spectra analysis, Genie 2000 and
glucose level in diabetic patients, prevention of oxidation [16], Hypermet PC 5.12, respectively, softwares were used.
and additionally a potential source of micronutrients [17].
Although several researches on these two fruits have been
done, however, most of these studies are on their pharmaceu- Atomic Absorption Spectrometry
tical and mutagenic properties [9, 18]. The aims of this re-
search are, firstly, to evaluate essential and toxic element con- In the spectrometry analysis, the chemical reagents were an
tents in the H. undatus L. and P. granatum L and, secondly, to analytical grade (E. Merck, Germany) and the double deion-
assess the dietary intake values and potential health risks ized water also used for the preparation of all solutions. The
through the consumption of these two fruits. standard solutions for calibrations of each element were pre-
pared by diluting stock solutions of 1000 mg/l. One gram of
each fruit and standard materials (SRM-1547 and SRM-1515)
Materials and Methods were placed in digested Teflon vessels with 10 ml of 65%
HNO3 (Kanto Chemical Corp., Tokyo, Japan) and 2 ml of
Study Area and Sample Collection 30% H2O2 (Kanto Chemical Corp., Tokyo, Japan) in a micro-
wave digestion system [21]. After digestion, the sample solu-
A total of 7 dragon fruits and 7 pomegranate samples of the tions were filtered by Whatman No. 42 filter papers and ac-
same species from each type were collected from the local customed to a desired volume with double deionized water.
market of Dhaka city of Bangladesh in January 2019. The The samples were analyzed for Cu and Ni by a flame atomic
samples were initially washed by deionized water, and the absorption spectrometry (FAAS), and for Pb and Cd using a
peels were removed and cut into the desired size in the clean graphite furnace atomic absorption spectrometry (GFAAS).
dishes. Moreover, the samples were heated separately at 60 °C Mercury concentrations were measured by cold vapor atomic
in the microwave oven until constant weight. The dried sam- absorption spectrometry (CVAAS). In this study, performance
ples were crushed in a mortar and passed through a 2-mm of the instrument and quality of the data were checked by
nylon sieve. Composite samples of dragon fruit and pome- using replicate samples, spiked samples, and method blanks.
granate were prepared by homogeneously mixing each type The spike recoveries were from 85 to 99%.
of samples together for elemental analysis. Samples were kept
frozen in labeled plastic bags in the laboratory until analysis.
Three replicate samples from each fruit were analyzed in this Quality Control and Quality Assurance
study to get elemental concentration.
The quality control of the analyses was checked by analyzing
Instrumental Neutron Activation Analysis SRM-1547 and SRM-1515 in this investigation. The Z score
was defined as [19]:
The sample analysis procedure by neutron activation analysis X lab−X ref
(NAA) and atomic absorption spectrometry (AAS) is exactly Z−score ¼
σref
same as by Rahman et al. [19]. However, a brief description is
given here. About 200 mg of each dried powder sample and where, Xlab, Xref, and σref are the laboratory result, the refer-
standard reference materials (SRM) was used to determine the ence value, and uncertainty with the reference value, respec-
element concentration by instrumental neutron activation tively. The laboratory performance is evaluated as satisfactory
analysis (INAA). In this study, there were two SRMs, SRM- if |Z| score ≤ 2, questionable for 2 < |Z| score < 3, and unsatis-
1547 (peach leaves) and SRM-1515 (apple leaves), and one factory for |Z| score ≥ 3 [19].
certified reference material IAEA-336 (Lichen powder), Accuracy and precision of the reported data by replicate
which were analyzed with the fruit samples. For relative stan- analyses (n = 3) of SRM-1547 and SRM-1515 by INAA and
dardization approach of INAA, IAEA-336 was used as the AAS are presented in Table S1 (Supplementary data). The
standard, while SRM-1547 and SRM-1515 were used as the analytical results of the elements in reference materials indi-
control samples [20]. The samples and standards were irradi- cate laboratory performance as satisfactory based on Z score
ated using pneumatic transfer (rabbit) system of 3 MW values.
Assessment of Essential and Potentially Toxic Elements and Possible Health Risks in Hylocereus undatus...
Estimated Daily Intake of Chemical Elements concentrations of essential elements in pomegranate and drag-
on fruits are in a descending order of K > Na > Ca > Fe > Zn >
The estimated daily intakes (EDI) of chemical elements (Cd, Al > Mn > Cu and K > Ca > Na > Fe > Zn > Al > Mn > Cu,
Cr, Cu, Fe, Mn, Ni, Pb, and Zn) for children and adults were respectively. In this study, the concentrations of Ca in pome-
calculated in the following equation [19]: granate and dragon fruit are 3390 and 2390 mg/kg, respective-
ly (Table 1). Calcium is an important element to prevent bone
MC CF FIR
EDI ¼ loss and essential for teeth and bones formation. Additionally,
BW 1000 high level of Ca is needed for women (1000 mg/day, when age
where, MC is average concentration in metals in the samples is > 18 years; 1300 mg/day, when age range is 14–18 years)
(mg/kg), CF represents the conversion factor (0.208), FIR is during the period of pregnancy [25]. It is observed that K
daily food ingestion rate (g/person/day), and BW is the aver- contents in the studied pomegranate and dragon fruits are
age body weight (adult = 60 kg and children = 16 kg), respec- 6250 and 6600 mg/kg. The minimum required average dietary
tively. To calculate the EDI values, the food ingestion rate intake of K is 2300 mg/day for adult women and 3100 mg/day
(g/person/day) were found from the report of the household for adult men [26]. Therefore, from this investigation, it is
income and expenditure survey 2010 [22] for Bangladeshi observed that K contents were found higher than the intake
population as 50.59 (for adults) and 25.33 (for children) in values. The K is an important element to prevent the stroke
fruits samples, respectively. and coronary heart disease as well as reduction of hyperten-
sion and diabetes in the human body [27]. Therefore, the stud-
Target Hazard Quotient ied fruits can be a good source of K for human body. The Na is
also an important element to maintain the physiological pro-
The target hazard quotient (THQ) values were calculated by cess and function of various organs in the body [28, 29]. The
the following equation: Na contents in the pomegranate and dragon fruits are 2550
and 3270 mg/kg (Table 1). Therefore, according to this study,
EDI studied two fruits can be considered as a vital source of Na, K,
THQ ¼
RfD and Ca.
In this study, Cu concentrations in pomegranate and dragon
Here, the oral reference doses (RfD) are 0.003, 1.5, 0.0035,
fruits were found to be 3.17 mg/kg and < 0.60 mg/kg, but
0.04, 0.14, and 0.3 mg/kg/day for Cd, Cr, Pb, Cu, Mn, and Zn,
according to WHO/FAO, the acceptable limit of Cu concen-
respectively [23]. The THQ plays a vital role in identifying the
tration is 4.5 mg/kg for fruit samples [24]. According to the
non-carcinogenic health risks.
result of this study, the concentrations of Cu in pomegranate
and dragon fruit do not exceed the acceptable level. The Fe is
Target Carcinogenic Risk
one of the essential mineral and it is used for blood production,
body growth, development, and DNA synthesis [30]. The Fe
Target carcinogenic risk (TCR) values were also calculated by
concentrations in pomegranate and dragon fruits were found
the following equation:
to be 201 mg/kg and 134 mg/kg (Table 1). From previous
TCR ¼ CSF1 EDI studies, Fe concentrations in Pakistani dried fruits were found
in the range of 19.0–45.0 mg/kg [31] and 3.89–40.7 mg/kg
where, CSF1 and EDI are the carcinogenic slop factor and [30]. Therefore, pomegranate and dragon fruits are a rich
estimated daily intake of elements in the body, respectively. source of Fe. Zinc is also considered as a vital element for
The slop factors of Cr, Cd, and Pb were 0.41, 6.1, and 8.5 × growth and development in plant and human body [32]. In this
10−3 (mg/kg/day)−1 [23]. study, Zn concentrations in pomegranate and dragon fruits
were found to be 79 mg/kg and 57 mg/kg, respectively
(Table 1). From the previous study, the range of Zn concen-
Results and Discussion trations in Bangladeshi fruits was 0.235–1.19 mg/kg [1].
According to the result of this study, pomegranate and dragon
Concentration of Essential Elements in the Fruits fruits are also considered as major source of Zn.
The concentrations of fifteen chemical elements (Al, Br, Ca, Concentration of Toxic Elements in the Fruits
Cd, Cl, Cr, Cu, Fe, Hg, K, Mn, Na, Ni, Pb, and Zn) in
P. granatum L. and H. undatus L. were determined and given The concentrations of six toxic chemical elementals (Br, Cd,
in Table 1. Moreover, the determined elemental concentra- Cr, Hg, Ni, and Pb) are determined and presented in Table 1.
tions in pomegranate and dragon fruits are compared with The determined mean concentrations of toxic chemical ele-
available WHO/FAO standard values. The obtained mean ments were found in pomegranate and dragon fruits are in
Rahman et al.
descending order of Br > Pb > Cr > Cd and Br > Pb > Cr > Cd, values, the range of concentrations (mg/kg) in Bangladeshi
respectively. The concentrations of the toxic elements Ni and fruits was found as Cd 0.010–0.030, Cr 0.17–2.1 [35]; Cd
Hg were found below the detection limit in the samples. Toxic 0.16–0.58, Cr 1.2–1.4 [36]; and Cd 0.583–3.023, Cr 0.513–
elements are harmful because of their toxicity, non- 2.502 [37]. The Pb concentrations were detected as 2.55 mg/kg
biodegradable nature, and long biological half-life, as well in pomegranate and 1.85 in dragon fruit (Table 1) but the
as their negative effects on sensitive organs of human body maximum tolerable limit is 0.1 mg/kg [24]. Therefore, Pb
like heart, bones, intestines, kidneys, and nervous systems concentrations in the studied pomegranate and dragon fruit
[19, 33]. In this study, the concentrations of Cd, Br, and Cr samples are higher than the maximum tolerable limit.
in pomegranate were 0.060 mg/kg, 37.5 mg/kg, and
0.10 mg/kg, respectively, whereas in dragon fruits, the con- Comparison of our Data with Literature Values
centrations were < 0.050 mg/kg, 15.0 mg/kg, and 0.88 mg/kg,
respectively (Table 1). According to WHO/FAO, the maxi- The elemental concentrations obtained from this study are
mum tolerable limit of Cd is 0.05 mg/ kg [24]; therefore, the compared with available published literature data from differ-
obtained result was found slightly higher than the tolerable ent countries (Turkey, Iran, and China) and presented in
limit in pomegranate. However, Cd levels were found below Table 2. There is no, so far, available elemental concentration
the tolerable limit in dragon fruit samples. Bromine is also data of dragon fruits so that only pomegranate data are com-
considered as a toxic element and excess Br may cause brain pared with published literature values in this study. From the
damage [34]. Similarly, Cr levels were assessed within the previous study, Na concentrations in pomegranate were found
safe limit of WHO/FAO values [24]. From the literature 591.5 mg/kg and 96 mg/kg in Turkey samples, whereas in
Table 2 Comparison of chemical elements (mg/kg) our data with literature data (pomegranate)
Na K Fe Ca Mn Mg Zn Cu Pb Cd Ni References
3270 6600 134 2390 2.73 – 57.0 < 0.60 1.85 < 0.050 < 0.80 This study (dragon)
2550 6253 201 3392 14.2 – 79 3.17 2.55 0.06 < 0.80 This study (pomegranate)
591.5 1650 20.3 – ND 41.6 4.58 2.26 0.16 ND – Turkey samples [38]
– – 14.5 – 6.0 – 11.7 8.0 – – – Iran samples [13]
96 1283 1.81 108 0.96 67.2 0.04 0.10 0.003 ND 0.04 Turkey samples [39]
– – 489 – 277 – 1511 85.9 – – – China samples [40]
ND not detected
Assessment of Essential and Potentially Toxic Elements and Possible Health Risks in Hylocereus undatus...
Bangladeshi pomegranate samples, concentrations were 10−4 for children, respectively (Table 3). In this investigation,
2550 mg/kg. Similarly, K concentrations were found about the decreasing orders of the elements based on dietary intake
four and five times higher in Bangladeshi samples compared via pomegranate consumption are Cd < Cr < Zn < Fe < Pb <
with those of Turkey samples (Table 2). The Fe concentrations Cu < Mn for both adult and children are in the same level.
of China samples (489 mg/kg) were found twenty-four times Similarly, for the dragon fruit orders of the chemical elements
higher than those of Turkey samples (20.3 mg/kg) and thirty- are Cr < Fe < Pb < Mn < Zn for adult and Zn < Cr < Fe < Pb <
four times higher than those of Iran samples (14.5 mg/kg), but Mn for children. The maximum tolerable daily intake (MTDI)
in Bangladeshi samples, it was 201 mg/kg. The Ca concentra- of Cd, Cr, Cu, Mn, Pb, and Zn are 0.021, 0.2, 30, 2.0–5.0,
tions of Bangladeshi samples were found more than thirty 0.21, and 60, respectively [1, 35]. In this study, the EDI values
times higher than those of Turkey samples. The Mn concen- for pomegranate and dragon fruit were found less than MTDI
trations in pomegranate were found significantly higher in values.
China samples when compared with Bangladesh, Turkey,
and Iran samples. Moreover, the Zn concentrations of China Target Hazard Quotient Values
samples were found a hundred times higher than those of
Turkey and Iran samples but more than nineteen times higher From this study, the total target hazard quotient (TTHQ)
than those of Bangladeshi samples. The Pb concentrations of values of pomegranate samples were found 1.65 × 10−1 for
Bangladeshi samples (2.55 mg/kg) were found about sixteen adult and 3.06 × 10−1 for children, whereas for dragon sam-
times higher than those of Turkey samples (0.16 mg/kg). ples 9.76 × 10−2 for adult and 1.82 × 10−1 for children as given
Previous studies on Bangladeshi fruit samples have shown in Table 4. If the values of THQ were found less than 1.0, it
that the average Pb concentration in fruits are 0.969 mg/kg indicates that no non-carcinogenic risk to consume these fruits
[37], 0.003–0.642 mg/kg [1], and 0.74 mg/kg [35]. Therefore, [35, 37]. From this study, it is clear that the calculated target
Pb concentrations obtained in the studied fruits are higher than hazard quotient values were found lower than the risk levels.
the previous Pb concentrations in Bangladeshi fruits. The Cd
concentration was not detected (ND) in Turkey samples but Target Carcinogenic Risk Values
0.06 mg/kg were found in Bangladeshi samples which is
slightly higher concentration than the WHO/FAO limit [24]. In this study, calculated TCR values for the elements Cd, Cr,
and Pb in pomegranate and dragon fruit samples are given in
Health Risk Assessments Table 4. The overall range of TCR values of pomegranate for
the elements was 7.38 × 10−6 to 6.71 × 10−5 for adult and
Estimated Dietary Intake Values 7.14 × 10−6 to 1.22 × 10−4 for children, whereas for dragon
fruit samples 2.75 × 10−6 to 6.15 × 10−5 for adult and 5.18 ×
The EDI values of pomegranate and dragon fruit samples 10−6 to 1.19 × 10−4 for children. From the literature study, the
were calculated and presented in Table 3. The overall EDI values of TCR above 1.0 × 10−4 indicate carcinogenic risk to
(mg/kg-bw/day) values of Cd, Cr, Cu, Fe, Mn, Pb, and Zn in consume the fruits [1, 19]. From this study, it is observed that
pomegranate samples were found in the range of 1.1 × 10−5 to the TCR values of Cd (1.22 × 10−4) in pomegranate samples
2.5 × 10−3 for adults and 2.0 × 10−5 to 4.7 × 10−3 for children, and Cr (1.19 × 10−4) in dragon fruit samples are higher than
respectively. Similarly, EDI values of Cd, Cr, Cu, Fe, Mn, Pb, 1.0 × 10−4 for children. From the previous study, Cd and Cr
and Zn in dragon fruit samples were found in the range of concentrations were found higher in the Bangladeshi fruits
1.5 × 10−4 to 10 × 10−4 for adults and 1.9 × 10−4 to 9.0 × and vegetables due to some major reasons such as excess
Table 4 Target hazard quotient (THQ) and target carcinogenic risk (TCR) values of the elements for consuming pomegranate and dragon fruit
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