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The Concentration of Potentially Toxic Elements (Ptes) in Fruit Juices: A Global Systematic Review, Meta-Analysis and Probabilistic Health Risk Assessment
The Concentration of Potentially Toxic Elements (Ptes) in Fruit Juices: A Global Systematic Review, Meta-Analysis and Probabilistic Health Risk Assessment
Chemistry
Salman Khazaei , Elaheh Talebi Ghane , Saeid Bashirian & Fereshteh Mehri
To cite this article: Salman Khazaei , Elaheh Talebi Ghane , Saeid Bashirian & Fereshteh
Mehri (2021): The concentration of potentially toxic elements (PTEs) in fruit juices: a global
systematic review, meta-analysis and probabilistic health risk assessment, International Journal of
Environmental Analytical Chemistry, DOI: 10.1080/03067319.2021.1873309
Article views: 17
1. Introduction
Fruits are the main part of the human’s food basket, which are mainly cultivated differently
in different regions of the world; the processes of production of the fruits are dependent to
a number of parameters like the cultivable conditions of crops and the environmental
properties of each region [1]. In this study, in addition to the fruits, their products like
different juices have popularity in many countries, and the tendency to consume these
products is growing different compounds such as fibre, trace elements, vitamin C, minerals,
and various noticeably [2]. The statistics show that the worldwide consumption of fruit
juices and fruit nectars by region in 2017 and 2018 was 35 billion litres, almost 9.1 billion
litres of which were consumed in EU countries [3].The recorded per capita consumption of
fruit products including fruit juices has increased by about 56.1% since the late 1960s, and
71.5% since the late 1930s, so that 95.5% of the children of 2–4 years and 92% of the
children of 5–12 years consume the minimum recommended intake of fruit juice in each day
[4]. These drinks commonly have kinds of antioxidants which are essential for human health
and reducing disease risk as cancer and cardiovascular diseases [5]. In spite of the important
role of these compounds in the humans’ diet, one of the biggest concerns is the contam
ination of fruit juices with impurities and farming-related substances such as metals and
pesticides. Potentially toxic elements (PTEs) including heavy metals and trace elements are
substances which naturally present in the environment and human activities can change
their concentrations and lead to harmful effects on the health of both humans and animals
[6]. According to former studies, more than 90% of the human’s exposure to PTEs is related
to the consumption of contaminated foods [7]. PTEs’ toxicity can be diverse based on the
type and other criteria including duration, intensity, frequency of their exposure, and
exposure routes of metals. To date, different kinds of guidelines have been set by a huge
number of countries for monitoring the levels of toxic metals in food products, confirming
their safety for human’s consumption [8]. Owing to the accumulation of toxic metals in food
crops in high concentrations, fruits contamination is considered as an important problem
for humans’ health [9]. Metals are categorised into essential and non-essential classes.
Essential metals such as Cu, Ni and Zn are considered vital for humans’ health, because
these metals are of important coenzymes in body and play an important role in growth and
respiration. In contrast, other metals like As, Pb and Cd have been identified as toxic or non-
essential metals which have not biological activity and resulting in nutritional problems and
serious risk for human’s health [10]. Based on previous studies, Pb can occupy the Zn site in
erythrocytes and bind to δ-aminolevulinic acid dehydratase and leads to inhibition of its
function in the body [11]. Cd is considered as a carcinogenic metal which can induce
diseases such as thyroid and pancreatic cancer in the body [12]. Exposure to As via
contaminated crops can result in diabetes, neurologic and neurobehavioral disorders,
hearing loss, and haematologic disorders [13]. There are several sources of contaminating
metals which can be derived from nature and influence the quality of fruits. In another
words, contamination of agricultural soil [14] and water for irrigation with these metals [15],
the amount and type of pesticides and chemical fertilisers during fruit planting, the
contamination of water source that applied during the fruit juices production [16], as well
as the contamination during packaging and processing technologies can be factors which
cause toxicity in fruit juices. The contamination of heavy metals in different fruit juices such
as apple, grape, mango, orange, peach, and pineapple has been widely studied in a number
of countries like Poland [8, Romania [17], Ghana [18] and Nigeria [19]. Meta-analysis is
defined as an approach to integrate data from individual studies, which can be highly
advantageous and may allow new conclusions to be made [20,21]. Given that no systematic
review has been done in the field of concentration of PTEs in the fruit juices, and because of
increasing trends of fruit juice consumption in all around the world and their adverse effects
on human’s health as a result of contamination with PTEs [22], we conducted the current
research, for the first time, in order to estimate the concentration of PTEs (Pb, Cd, As, Fe, Zn,
Ni and Cu) in different fruit juices including apple, grape, mango, orange, peach, and
INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 3
1. Experimental
1.1. Study protocol
The present systematic review focussed on estimating the concentration of PTEs in fruit
juices according to the PRISMA guidelines for systematic review and meta-analysis [23].
papers including year, country, type of fruit juices, average concentration, standard deviation
of measurements, sample size and concentration range of toxic metals. In order to unify the
units in the studied papers, all units of concentration such as μg/kg, ppb and ng/g, which have
been for the heavy metals, were changed to mg/kg-dry-weight.
Where TTHQ indicates the sum of each THQ for the whole metal analysed in the fruit juice
samples [26,27]. TTHQ values lower than 1 indicate acceptable health hazard for health
human [28].
based on metal type. Heterogeneity was calculated among the studies by Q and I2 tests.
Cochran Q test (Q statistic, p < 0.10) shows statistically significant heterogeneity and I2
statistic (I2 > 50%) indicates a large heterogeneity. Statistical analysis and data analysis were
performed using the second version of the comprehensive meta-analysis software. The
significance level was considered to be less than 0.05. The data were analysed by the Stata
software, version 14 (StataCorp, College Station, TX, USA) at a significance level of 0.05.
2.3. PTEs level in fruit juices based on fruit types and continents
Our Meta-analysis regarding the concentration of PTEs in fruit juices based on fruit types
and continents have been presented in Tables 1 and Tables 2. The ranking of metals
concentration was Fe> Zn> Cu> Pb > Ni> Cd> As in apple and orange, Cu> Zn> Pb in
grape, Fe> Zn> Cu> Ni> Cd> Pb in mango, Fe> Zn> Cu> Ni > Pb> Cd in peach and Cu> Zn>
Cd> Ni> As in pineapple.
6 S. KHAZAEI ET AL.
Idenficaon
Records idenfied through
database searching
(n = 701)
Duplicates removed
(n = 244)
Screening
(n = 169)
According to the results, the concentration of PTEs in the investigated fruit juices was
greatly diverse which can be related to the several factors such as the characteristics of
metals, nature of the fruit, composition of the irrigation water and soil, the weather
conditions, agricultural activities such as the types and amounts of fertilisers used, as
well as, storage condition and processing technologies [31].
It is clearly seen that the higher concentration of Fe Zn, Cu and Ni as compared with
other investigated elements such as Pb, Cd and As in most examples can be related to this
fact that essential elements have higher transfer factors than toxic metals leading to
higher accumulation of them in fruits [32]. We observed that the concentrations of Pb and
Cd were in the lowest level in peach (0.016 mg/kg and 0.011 mg/kg) and in level in orange
and pineapple, respectively (0.075 mg/kg and 0.204 mg/kg). The concentration of As in
INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 7
Table 1. Meta-analysis of concentration of toxic metal (PTEs) (mg/kg) in juice based on fruit juice.
Heterogeneity
Metal Fruit juice N of studies ES (95% CI) weight Statistics df P.Value I2 (%)
Pb Apple 15 0.076 (0.067, 0.085) 24.38 11,732.04 14 <0.001 99.9
Grape 5 0.071 (0.049, 0.093) 7.23 289.20 4 <0.001 98.6
Mango 6 0.050 (0.040, 0.060) 11.57 2227.95 5 <0.001 99.8
Orange 18 0.076 (0.058, 0.094) 28.68 61,265.85 17 <0.001 100.0
Peach 7 0.016 (0.010, 0.021) 11.55 587.15 6 <0.001 99.0
Pineapple 11 0.035 (0.029, 0.040) 16.58 1306.59 10 <0.001 99.2
Cd Apple 11 0.041 (0.039, 0.043) 21.35 19,765.50 10 <0.001 99.9
Mango 6 0.068 (0.040, 0.096) 15.19 4956.97 5 <0.001 99.9
Orange 12 0.015 (0.011, 0.020) 32.38 3329.34 11 <0.001 99.7
Peach 6 0.011 (−0.001, 0.022) 18.20 5130.04 5 <0.001 99.9
Pineapple 7 0.204 (0.117, 0.291) 12.88 17,697.26 6 <0.001 100.0
As Apple 6 0.003 (0.001, 0.004) 65.73 163.41 5 <0.001 96.9
Orange 4 0.003 (0, 0.007) 34.27 66.5 3 <0.001 95.5
Fe Apple 14 1.794 (1.452, 2.137) 28.90 4.3E+05 13 <0.001 100.0
Mango 13 3.216 (1.535, 4.897) 24.57 3.6E+05 12 <0.001 100.0
Orange 15 2.083 (1.777, 2.390) 30.01 4228.01 14 <0.001 99.7
Peach 7 2.45 (0.82, 4.08) 14.52 14,175.8 6 <0.001 100.0
Pineapple 5 16.712 (14.906, 18.518) 2.00 5.12 4 0.275 21.9
Zn Apple 16 0.431 (0.318, 0.543) 23.12 3.5E+05 15 <0.001 100.0
Grape 5 0.447 (0.358, 0.537) 7.11 484.44 4 <0.001 99.2
Mango 11 0.562 (0.403, 0.721) 14.92 1.6E+05 10 <0.001 100.0
Orange 21 0.466 (0.371, 0.562) 27.30 52,046.47 20 <0.001 100.0
Peach 11 0.561 (0.403, 0.718) 14.82 1.9E+05 10 <0.001 100.0
Pineapple 9 0.256 (0.139, 0.372) 12.74 69,226.38 8 <0.001 100.0
Cu Apple 17 0.272 (0.230, 0.313) 22.63 9457.18 16 <0.001 99.8
Grape 6 0.458 (0.313, 0.603) 8.10 11,870.11 5 <0.001 100.0
Mango 9 0.206 (0.174, 0.238) 12.16 9681.99 8 <0.001 99.9
Orange 23 0.379 (0.240, 0.518) 30.60 2.1E+05 22 <0.001 100.0
Peach 10 0.508 (0.303, 0.713) 13.15 27,792.34 9 <0.001 100.0
Pineapple 10 0.282 (0.194, 0.371) 13.37 15,471.46 9 <0.001 99.9
Ni Apple 14 0.047 (0.034, 0.059) 25.11 2987.28 13 <0.001 99.6
Mango 10 0.164 (0.116, 0.213) 19.45 3358.75 9 <0.001 99.7
Orange 15 0.046 (0.035, 0.058) 26.61 3206.66 14 <0.001 99.6
Peach 6 0.188 (0.100, 0.276) 11.79 6354.39 5 <0.001 99.6
Pineapple 9 0.178(0.122, 0.235) 17.04 3360.87 8 <0.001 99.8
apple and orange juices was similar (0.003 mg/kg). Moreover, the lowest and the highest
concentrations of Fe were found in apple juice and pineapple juice (1.794 mg/kg and
16.712 mg/kg). For Cu, Ni and Zn, the highest concentration belonged to peach and
mango (0.508 mg/kg, 0.188 mg/kg and 0.562 mg/kg) and the lowest one belonged to
mango, orange and pineapple (0.206 mg/kg, 0.046 mg/kg and 0.256 mg/kg), respectively.
It should bear in mind that the difference that was observed in kind and content of
metals between different fruit juices can be related to physicochemical characteristics as
the bioavailability of metals and plant species [33]. Metals like Fe and Cu have high-
mobility and quickly move from soil into an aerial plant, while other metals such as Pb
have low-mobility accumulating with a high concentration in plant’s root [34]. Although
metals have similar bioavailability, other sources of contamination in fruit juices are
probably included among these differences [35]. According to the study conducted by
Mahugija et al., (2018) the mean concentrations of Cu in the pineapple juices were greater
than those of mango juices. They explained that various concentrations in these two
plants may be related to properties of them. Since the mango tree has the taller size than
the pineapple tree, thus, the location of it, than to the soil, is higher compared to
pineapple tree therefore the uptake of Cu metals from the soil is slower [36]. In the meta-
8 S. KHAZAEI ET AL.
Table 2. Meta-analysis of concentration of toxic metal (PTEs) (mg/kg) in juice based on WHO regions.
WHO Heterogeneity
Metal Region N of studies ES (95% CI) weight Statistics df P.Value I2 (%)
Pb AFRO 22 0.048 (0.042, 0.054) 31.61 8332.56 21 <0.001 99.7
EMRO 16 0.206 (0.179, 0.234) 23.75 42,207.71 15 <0.001 100.0
PAHO 10 0.006 (0.004, 0.008) 19.95 327.04 9 <0.001 97.2
EURO 14 0.010 (0.008, 0.012) 24.7 803.13 13 <0.001 98.4
Cd AFRO 13 0.128 (0.101, 0.156) 25.79 15,766.07 12 <0.001 99.9
EMRO 11 0.075 (0.059, 0.090) 25.86 9471.43 10 <0.001 99.9
PAHO 6 0.017 (0.006, 0.029) 20.67 5225.93 5 <0.001 99.9
EURO 13 0.013 (0.012, 0.014) 27.69 14,639.44 12 <0.001 99.9
As EMRO 4 0.003 (−0.001, 0.007) 33.57 68.28 3 <0.001 95.6
PAHO 1 0.008 (0.006, 0.010) 13.24 – 0 – –
EURO 5 0.002 (0, 0.003) 53.19 106.86 4 <0.001 96.7
Fe AFRO 19 4.903 (3.693, 6.113) 29.78 4.3E+05 18 <0.001 100.0
EMRO 15 1.771 (1.559, 1.982) 30.44 8220.94 14 <0.001 99.8
PAHO 11 1.565 (1.376, 1.754) 21.24 14,511.79 10 <0.001 99.9
EURO 8 2.714 (1.021, 4.406) 16.43 15,629.12 7 <0.001 100.0
SEARO 1 0.500 (0.412, 0.588) 2.11 – 0 – –
Zn AFRO 23 0.351 (0.270, 0.431) 32.43 2.1E+05 22 <0.001 100.0
EMRO 15 0.687 (0.446, 0.927) 20.16 66,717.44 14 <0.001 100.0
PAHO 20 0.455 (0.380, 0.529) 26.44 1.7E+05 19 <0.001 100.0
EURO 15 0.319 (0.251, 0.386) 19.52 63,706.44 14 <0.001 100.0
WPRO 1 0.820 (0.786, 0.854) 1.44 – 0 – –
Cu AFRO 23 0.320 (0.247, 0.393) 30.26 40,582.84 22 <0.001 99.9
EMRO 16 0.539 (0.362, 0.716) 21.31 1.8E+05 15 <0.001 100.0
PAHO 18 0.260 (0.210, 0.311) 24.27 81,000.48 17 <0.001 100.0
EURO 15 0.268 (0.144, 0.391) 20.12 31,460.19 14 <0.001 100.0
SERO 2 0.310 (−0.158, 0.779) 2.69 361.24 1 <0.001 99.7
WPRO 1 0.700 (0.666, 0.734) 1.34 – 0 <0.001 –
Ni AFRO 18 0.168 (0.135, 0.201) 30.48 3711.96 17 <0.001 99.5
EMRO 14 0.158 (0.128, 0.187) 26.23 10,735.65 13 <0.001 99.9
PAHO 12 0.071 (0.055, 0.088) 23.65 2209.17 11 <0.001 99.5
EURO 10 0.098 (−0.005, 0.201) 19.63 330,000 9 <0.001 100.0
INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 9
change can occur via irrigation of soil with wastewater and cultivation of plants with
different species. Therefore, this issue can lead to forming carbonates and hydroxides and
increased organic matter of soil [7]. Yaylali-Abanuz and Tuysuz in their study indicated that
there was a significant negative relation between soil pH and uptake of metals by tea plants
[40]. Al-Busaidi et al. (2005), reported that the soil which was irrigated by wastewater had
higher pH and metal concentration as compared with the soil which was irrigated by
ground water [41]. In two separate studies conducted in India and China, the results showed
irrigation by wastewater compared to clean water and groundwater led to a significant
increase in metal content into the soil and the following various crops [42]. Clearly, long and
frequent irrigation with wastewater has incremental effects on organic total content,
bioavailability and concentration of metals in irrigated crops [43]. Moreover, domestic and
industrial sewages can directly affect the transfer rate (bioavailability) and subsequently
accumulation of metals in crops [44]. Using modern and high-efficiency technologies in
irrigating by wastewater can result in removing large amounts of harmful metals [45].
According to the research conducted by Al-Busaidi et al, in 2015, those fruits irrigated by
groundwater had lower concentrations of Fe, Cu, Cd and Ni (0.017, 0.008, 0.142 and
0.001 mg/L), respectively [46] in comparison with other ones irrigated by wastewater
(0.018, 0.024, 0.431, and 0.039 mg/L), respectively.
Likewise, in another similar study, it was indicated that the concentrations of Pb, Zn,
Cu, Co, Cr, As, Cd, Fe, Mn and Ni in sewage effluents were higher than those in clean water,
which, in turn, were found in irrigated crops by these two water resources [47].
Table 3. Uncertainty analysis for TTHQ of metals in an adult due to consumption of fruit juice in
various countries.
Percentile 95%
Country AS Cd Cu Fe Ni Pb Zn TTHQ
Australia – – 0.0146 – – – 0.0023 0.013
Bangladesh – – 0.0015 – – – – 0.001
Brazil – 0.0120 0.0045 0.0166 0.0051 0.0014 0.0042 0.025
Egypt – 0.0179 0.0119 0.0132 0.0079 0.0250 0.0029 0.062
Ghana – 0.0364 – – – 0.0107 – 0.031
India – – 0.0119 0.0007 – – – 0.009
Iran 0.0004 0.0128 0.0146 – 0.0024 0.0347 – 0.059
Iraq – 0.0204 0.0011 0.0050 – – – 0.021
Latvia – – 0.0030 0.0011 0.0020 – 0.0006 0.004
Nigeria – 0.1328 0.0074 0.0194 0.0081 0.0168 0.0017 0.140
Northern Jordan – 0.1249 0.0186 – 0.0273 0.0004 0.0018 0.137
Pakistan 0.1943 0.0150 0.0042 0.0008 0.0140 – 0.0010 0.098
Poland – 0.0558 – – – 0.0042 – 0.048
Romania 0.0004 0.0241 0.0032 – 0.0028 0.0014 0.0009 0.025
Saudi Arabia – – 0.0144 0.0010 0.0009 0.0557 0.0018 0.070
Serbia – 0.0573 0.0139 0.0088 0.0085 – 0.0011 0.072
Spain – 0.0092 – – – – 0.0027 0.008
Tanzania – – 0.0022 – – – 0.002
Turkey 0.0041 0.0021 0.0028 0.0014 0.0032 0.0093 0.0008 0.020
USA 0.0034 0.0281 0.0054 0.0016 0.0016 0.0111 0.0011 0.052
Venezuela – – – 0.0009 – – 0.0010 0.001
3. Conclusion
In the current study, the concentrations of PTEs in the fruit juices such as apple, grape, mango,
orange, peach and pineapple were meta-analysed, and non-carcinogenic health risk in the
adults was evaluated. According to the results, the pattern of PTEs contamination was
different among fruit juices among countries. It was clear that the concentration of Fe Zn,
Cu and Ni were higher compared to other investigated elements such as Pb, Cd and As in
most fruit juices. Among heavy metals, Cd and essential elements, Fe had a higher concentra
tion of contamination (0.204 and 16.712 mg/kg), respectively, which was related to pineapple
INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 11
juice. The health risk assessment indicated that the amount of TTHQ of PTEs in fruit juices was
lower. Therefore, consumers at different ages were not at considerable non-carcinogenic risk
due to consuming fruit juices. Several factors such as physicochemical characteristics of PTEs,
the type and species of plant, as well as characteristics of soil and water used for cultivation,
various processes involved in fruit juice production play a basic role in the uptake of PTEs by
fruits. Therefore, in order to reduce the concentration of PTEs in fruit juices, there are some
preventive approaches including monitoring of soil and water used during fruit cultivation like
irrigation with clean water and appropriate techniques, which should be considered by
governments as well as farmers.
Acknowledgments
The authors would appreciate the Deputy of Research and Technology, Hamadan University of
Medical Sciences, for financial support of the study.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Conflict interest
All authors express that they have any conflict of interest.
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