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Assessment of heavy metal pollution transfer and h

Environmental Science and Pollution Research
Assessment of heavy metal pollution transfer and human exposure
risks from the consumption of chicken grown
in mining-surrounding areas
Sameh Elkribi-Boukhris 1,2 & Naceur M’hamdi 3 & Iteb Boughattas 1 & Sondes Helaoui 1 & Cecile Coriou 4 & Sylvie Bussiere 4 &
Valerie Sappin-Didier 4 & Mohamed Banni 1
Received: 4 May 2021 / Accepted: 12 August 2021
# The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
The purpose of this study was to assess heavy metal contamination in soil, plants, earthworms, and chicken in farmlands adjacent
to an old mining site and to evaluate the potential exposure risks to humans through the consumption of chicken. For this purpose,
soil, earthworms, plant, chickens, and eggs were sampled from 5 sites following a gradient of contamination. All samples were
analyzed for heavy metals (Pb, Cd, Cu, and Zn). A food chain model was used in order to characterize heavy metal transfer
between soil-plant-earthworm and chicken organs. Furthermore, target hazard quotient (THQ), estimated daily intake (EDI), and
hazard index (HI) were employed to assess human health risks posed by heavy metal contamination. Despite the higher level of
Pb, our data related to the calculation of EDI and THQ suggested that local consumers are more at risk of Cd contamination. The
calculated HI showed values ranging from 2.58 to 4.74 for adults, and up to 12.34 for children, indicating a considerable risk to
the health of local inhabitants, especially children. This study highlighted the crucial role of diets based on chickens grown in
contaminated areas, on health risks especially for children.
Keywords Estimated daily intake (EDI) . Hazard index (HI) . Heavy metals . Old mine . Target hazard quotient (THQ)
Heavy metals are characterized by their non-biodegradability and
long biological half-life, (Tlili et al. 2010; Sobhan 2017).
Consequently, they can be accumulated within soil-plant-food
chains in a considerable amount, which presents a potential
health risk for humans (Rezaei Raja et al. 2016; Boughattas
et al. 2017; Rezvan et al. 2019). For example, deficits in intelligence quotient development of physiological abnormalities, and
Responsible Editor: Lotfi Aleya
* Iteb Boughattas
[email protected]
Laboratory of Agrobiodiversity and Ecotoxicology, Higher Institute
of Agronomy, Chott-Mariem, 4040 Chott-Mariem, Tunisia
Department of Biological Sciences, Faculty of Science of Tunis,
University of Tunis El Manar, Tunis, Tunisia
Department of Animal Sciences, National Agronomic Institute of
Tunisia, University of Carthage, 1082 Tunis, Tunisia
UMR ISPA, INRAE, 33140, Villenave-d’Ornon, Bordeaux, France
neurotoxicity effects in infants, and anemia are the primary consequences of exposure to lead (Duran et al. 2009; Iwegbue 2015;
Hariri et al. 2017). In this context, environmental disease outbreaks of Minamata disease were caused by oral intake of MeHg
in fish and itai-itai disease from cadmium in rice (Gunnar et al.
2019). Cadmium has an extremely long biological half-life
(Javed and Usmani 2016). Thus, it can be damaging to humans,
potentially through its concentrations in kidneys (Bernard 2008;
Nookabkaew et al. 2013; Kim et al. 2016). Decreased rate of
glomerular filtration and significant protein urea along with an
important frequency of kidney stone development are the main
effects of oral exposure to Pb (Zhuang et al., 2017). Copper (Cu)
and Zinc (Zn) are essential trace elements with numerous biological functions such as hemoglobin synthesis and enzyme functions (United States Environmental Protection Agency (USEPA)
2012). However, both excess and deficiency of these elements
can result in adverse effects in the human body such as Menkes
and Wilson’s diseases (Tapiero and Kenneth 2003; Sobhan
Heavy metal contamination occurs generally due to industrial activities and especially with metal manufacture. Indeed,
mining is considered the primary source of long-term soil
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pollution (Lourenço et al. 2011; Iwegbue 2015; Kim et al.
2016; Boughattas et al. 2018; Mkhinini et al. 2020). Mine sites
are generally located adjacent to farmlands and rural areas.
Consequently, these are exposed to pollution by heavy metals,
through air and soil deposits, and additionally, through direct
exposure of the villagers to these pollutants via different pathways (Qing et al. 2015; Giri and Kumar 2017; Rezvan et al.
In this regard, the Pb-Zn mining site of Jebel Ressas and its
surrounding agricultural area, located in northeastern Tunisia
have been abandoned, and huge quantities of mining waste
have been left in the open. The site is considered a source of
heavy metal contamination of farmland surrounding the
mines, especially since no specific management was recorded
up to now to minimize heavy metals contamination (Ghorbel
et al. 2014; Boughattas et al. 2017). Consequently, a health
risk may exist for the habitants due to their exposure to heavy
metal contamination via ingestion, inhalation, and dermal
contact (Ghorbel et al. 2014).
Conversely, poultry raised in the Jebel Ressas mine area
could uptake heavy metals from different origins, mainly
through food. Metal residues may be accumulated on their
tissues and eggs (Chowdhury et al. 2011; Abdulkhaliq et al.
2012). Therefore, trace heavy metals can be transferred to
humans through food consumption (De Vries et al. 2007;
Rodrigues et al. 2012). Béjaoui et al. (2016) affirmed the
health risk for Jebal Ressas inhabitants being exposed to Pb
and Cd contamination through spontaneous plants (Malva
sylvestris) consumption and soil direct dust inhalation.
Considering this, food chain models are crucial tools to
evaluate soil contamination risks. Thus, it is essential to
promote models to describe the pathways related to soil
pollution, dietary transfer of hazardous to animals, and human exposure from dietary intake of animal products and
plants. The transfer of chemicals in food chains is in general detailed by bioaccumulation factors (BAFs) and
bioconcentration factors (BCFs). These key factors are
based on the hypothesis of the existence of linear relationships between heavy metal loads in plants (Helaoui et al.
2020), earthworms (Boughattas et al. 2016), birds (Indrajit
et al. 2018), mammals (Syr-Song et al. 2013; Jebali et al.
2014; Banni et al. 2017), and the amounts existing in soil.
However, the use of constant factors, BCF and BAF, is
controversial since some authors retain it not suitable to
describe the transfer of contaminants from soil to plants
in a particular context (Römkens et al. 2009a, 2009b,
Vries et al., 2007). Therefore, more efficient empirical
models have been suggested to depict the soil-plantanimal transfer. To realistically consider differences in the
bioavailability of trace elements in corresponding to several
soil types, important soil properties (pH, organic matter:
OM, clay) have been considered in such models (Krauss
et al. 2002; Efroymson et al. 2001; Römkens et al. 2009b).
Despite the available literature about the effects of hazardous on ecosystem components, a gap of knowledge still exists
on pollutants transfer modeling from the ecosystem to
humans. This should be underlined in a heavily contaminated
context such as old mining sites.
The objective of the present work is the evaluation of human risks after exposure to Pb, Cd, Cu, and Zn from the direct
ingestion of Gallus gallus domesticus, which is the most available and low coast protein source considering the socioeconomic state of the citizens of the Jebel Ressas region.
This evaluation was performed using a predictive modeling
approach considering the supply chain from soil to the final
Materials and methods
Study area and sample collection
Jebel Ressas (JR) mine site was considered in this investigation (Figure S1). JR is located south of the Tunisian capital
“Tunis City” (30 km) and is under a semi-arid climate. The
site includes fields impacted by old mining activities (Pb-Zn
extraction zone).
For the current research, 5 sites were considered:
Four sites (S1, S2, S3, and S4) with a decreasing
polymetallic contamination gradient in the surrounding
area of the old mine.
Site 5: Selected as a reference site and located in ChottMariem, in the center of Tunisia (110 km away from the
mining site). We considered this site because it is used for
organic farming with no source of heavy metals pollution
(Figure S1).
Soil samples were collected from the top 0–30 cm of soil in
the different sites (10 samples from each site) after removing
litter and surface vegetation. Earthworms and plants were also
sampled from each site (n=10 from each site).
A total of 100 chickens (20 from each site) were raised for 6
months (March and July 2017). Soil macro-flora including
earthworms and spontaneous vegetation were their main food
diet. Before their sacrifice, chickens were weighed, and then
they were dissected. All the experimental protocols were carried out in accordance with the principles and recommendations of Directives 86/609/EEC regulating the welfare of laboratory animals (Louhimies 2002; Elkribi-Boukhris et al.
2020). The liver, kidney, lung, and muscle were carefully
removed. Additionally, the blood from the scarified chicken
was sampled. All the samples were then conserved at −80°C
for further analysis. Fresh eggs were collected (20 eggs from
each site) from the five farms that were used for chicken sampling. The eggs were collected and transferred to the
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laboratory in small plastic bags and were kept in a cool, dark
place (+4) until analysis.
Chemical analysis of soils, plants, worms, and chicken
Soil samples were homogenized and sieved (2-mm mesh) and
then dried twice: first air-dried until the weights were constant
and then re-dried at 105°C for 24 h. Soils were then ground
into agate balls for 10 min. All the mineral elements in the soil
were quantified after solubilization by aqua regia (HCl/HNO3)
(NF X 31-415 method).
Plant samples were brushed to eliminate traces of adhering
soil and dust (Válega et al. 2008). Then, they were dried at
60°C until constant weight (Válega et al. 2008). The dried
plant material was ground into zirconium balls for 10 min.
Then, they were mineralized with acid attack digestion with
a mixture of 4:1 (v/v) H2O230% and HNO369% (Aristar® for
trace analysis, VWR Chemicals).
Chicken tissues (muscle, liver, kidney, feather, lung, and
blood) and earthworms were dried to constant weight at
105°C for 48 h and then ground (< 1 μm) using a Retch
Planetary Ball Mill PM 400.
For the eggs, each one was cut into the end of the air cell
using sharp tweezers and dissecting scissors. The shell was
rinsed with distilled water for each egg separately. The content
of each sample was placed in a chemically cleaned glass jar
and the egg white was separated from the yolk. They were
dried at 75°C to obtain constant weight and then, they were
ground into powder.
Aliquots of plant and animal powdered samples were mineralized using a mixture of HNO3 69% and H2O2 30% and
furtherer filtrated and diluted with deionized water.
All extracts were quantified by atomic absorption spectrophotometer (AAS). The solutions were injected into atomic
spectrometry and the elements analyzed were Cd, Pb, Zn, and
Cu (detection limit was 0.02 μg L−1). Samples were tested and
analyzed in triplicates.
A standard reference material (SRM) was used for validation of the analytical procedure, “Tomato leaves 1573a” certified by the National Institute of Standards and Technology.
metals concentration as functions of the total heavy metals
from soils and plants. The p values for the Pearson correlation
coefficients in the regression models were achieved by correlating the metal loads in chicken organs with the total metal
concentrations from the plants and the soil. The p values of the
regression model and the R square of the linear regression
were achieved by correlating the expected and measured
metals loads in chicken’s tissues.
Model overview description
In the present investigation and in order to assess to what
extend heavy metals in soils may present risks for human
health through food consumption, we developed a human exposure chain model. This integrates soil-heavy metal levels,
soil properties, soil-plant transfer, animal intake, transfer to
animal tissues, and human consumption patterns (to evaluate
human hazardous exposure from daily intake). A schematic
overview of the model is provided in Figure S2
(Supplementary data).
Derivation of soil-plant transfer models
Usually, the transfer of metals in food chains is characterized
by bioconcentration factors (BCFs) and bioaccumulation factors (BAFs). The BCF is defined as the ratio of the test metal
concentration in an organism (e.g., plant, earthworm) to the
concentration in soil at a steady state. The BAF is defined as
the ratio of the test metal concentration in an organism to the
concentration in its food at steady state (Jongbloed Ben and
Westerheijden 1994).
BCFsp ¼
½M p
½M s
metal loads in plant (mg kg−1)
total metal loads in soil (mg kg−1)
½M organ
½M f
Model concept and data analysis
The SAS software version 9.4 (Statistical Analysis System
2012) was used to perform all statistical analyses. The data
were subjected to basic statistics, tests for normality and correlation significance, and an analysis of variance. Statistical
comparisons between the different metal loads in the various
matrixes were first controlled using the “Levene” test of the
homogeneity of variance, then by one-way analysis of variance (ANOVA). A forward stepwise multiple linear regression was employed to obtain the models of the organ’s heavy
metal loads in an organism (mg kg −1)
metal loads in feed (mg kg−1)
These factors are calculated assuming that metals in soil
and those in plants, earthworms, mammals, and other target
organisms are linearly correlated (De Vries et al. 2007).
However, better predictions of the hazardous loads in
plants can be retrieved by a nonlinear relationship that considers the contribution of soil properties that controls the
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bioavailability of heavy metals in soils (Adams et al. 2004;
Brus et al. 2002).
Tsp ¼
½M p
½M −n
transfer parameter from soil to plant (mg/kg1−n)
constant rendering the nonlinear relationship
Tsp varies with respect to soil clay content, organic matter,
and pH (Brus et al. 2002; Adams et al. 2004; Rodrigues et al.
2012). Using log10 transformation, Equation (3) can therefore
be presented as:
Log Tsp ¼ I þ α:log ½OM þ β:log ½clay þ γ:log
þ ½M s þ δ:pH
OM is the organic matter content (in percentage, fixed on
3% for all soils) (De Vries et al. 2007; Römkens et al. 2009b;
Boughattas et al. 2016).
Clay is the fraction of clay particles (in percentage, fixed on
25% for all soils) (De Vries et al. 2007).
[M]s is the heavy metal level in the soil (in mg kg−1 of dry
The regression parameters I (intercept) were obtained by
regression analysis: stepwise multiple regression (Römkens
et al. 2009b; De Vries et al. 2007).
Modeling of heavy metal transfer in animal organs
The following food chain model: soil ➔ plant ➔earthworm ➔
chicken. Logarithmic transformation was used based on
Equation (2) which can be therefore presented as:
Log T f −c ¼ I þ α:log I p þ β:log ½I s þ δ:log ½I v ð5Þ
½M chicken−organ ¼
The daily intake (DI) of heavy metals in animal organs
relates to feed consumption (plant-leaf and worm) and soil
ingestion according to Smith (2009) and Rodrigues et al.
(2012). Based on Equation 2, DI is as follows:
DIchicken−organ ¼ ðA þ B þ CÞ*BAFfeed−chicken
We measured the metal loads in plant leaves, soils, and
The calculations were realized on a field-by-field basis
considering that chicken feed at the field all the time
and always at the same sites.
The transfer coefficient of metals from soil to animal organ is equal to the BAFchicken;
Heavy metal uptake from air and water is negligible compared to that of soil and feed (De Vries et al. 2007).
A ¼ C plant−leaf * I plant−leaf = I plant−leaf þ I soil
B ¼ C soil *ðI soil Þ=ðI worm þ I soil Þ
C ¼ C worm *ðI worm Þ=ðI soil þ I worm Þ
Cplant-leaf, Csoil, and Cworm concentration of heavy metal in
leaves of plants, soil, and earthworm, respectively, in mg kg−1
of dry weight.
Iplant-leaf, Isoil, and Iworm are the daily intake of plant leaves,
soil, and earthworm, respectively, by chicken in kg day−1 of dry
A combination of Equations (6), (7), (8), and (9) is used to
calculate the concentration of target heavy metal in chicken
organs (Sobhan 2017):
C plant−leaf * I plant−leaf = I plant−leaf þ I soil þ C soil *ðI soi Þl =ðI worm þ I soil Þ þ C worm *ðI worm Þ=ðI soil þ I worm Þ BAF chicken
Equation 10 is based on the following assumptions:
Tf−c: transfer parameter from food to chickens
The regression parameters I (intercept), α, β, and δ were
estimated by stepwise regression analysis (Römkens et al.
2009b; De Vries et al. 2007).
Ip: daily intake of plants (intake plant) in kg day−1 of dry weight
Is: daily intake of soil in kg day−1 of dry weight
Iv: daily intake of earthworm in kg day−1 of dry weight
Exposure assessment: human estimated daily intake
(EDI), target hazard quotients (THQ), and hazard
index (HI)
Human intake of toxic metals in this study consists of intake
by soil ingestion, consumption of plant leaves, chicken tissues, and eggs consumption.
The EDI of heavy metals for humans was calculated for
three elements (Pb, Cd, and Zn) according to the following
equation, (United States Environmental Protection Agency
(USEPA) 1997):
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the heavy metal concentration (mg kg−1)
ingestion rate (kg day−1)
exposure frequency (365 days/year)
exposure duration
body weight (kg)
averaging time for non-carcinogens (365 days/years)
In our case study, we consider that the Jebel Ressas’ inhabitants are exposed to heavy metal contamination all day. The
above equation changes as follows:
½M х IR
ðmg kg−1 day−1Þ
According to the National Institutes of Health database
(INS, 2015), the following information about the Tunisian
consumer are available:
The average weekly consumption of eggs is 9.3kg/year,
therefore 27.48g/day.
The average daily consumption of chicken is 16.8 kg/
year, therefore 46.03g/day.
The exposure frequency (EF) has been set at 144 days/
year for people who eat chicken and eggs three times a
The duration of exposure (ED) is 70 years (equivalent to
the average lifespan) for adults and 7 years for children.
The average value for adult body weight was considered
65 kg and 25 kg for children for the Tunisian population
Human health risks posed by heavy metal contamination
are generally characterized by the target hazard quotient
(THQ). The following equation determines the THQ based
on the non-cancerous toxic risk (Equation 13):
RfD is the reference dose of individual metal (mg kg−1
day−1). It is applied for Cd, Pb, Cu, and Zn, and the values
are 0.001, 0.0035, 0.04, and 0.3 respectively, as established by
US Environmental Protection Agency (United States
Environmental Protection Agency (USEPA) 2012; Javed
and Usmani 2016).
If the THQ value is under 1, the carcinogenic toxic effects
are considered to be low. When it exceeds 1, the potential
health risks associated with overexposure become concerning.
The HI (hazard index) is used to estimate the total noncarcinogenic health risks (Wilbur Sharon et al. 2004; Javed
and Usmani 2016). To assess the potential health risks posed
by numerous metals, THQs can be added to create a hazard
index (HI) aiming to evaluate the risk of a mixture of toxic
compounds. HI refers to the sum of many THQ for many
hazardous compounds (Equation 14):
HI ¼ THQ1 þ THQ2 þ …… þ THQn
the THQ of an individual metal element;
the hazard index for all investigated metals
Chemical study for determination of heavy metals
(Pb, Cd, Zn, and Cu)
Heavy metal content in soils
Trace element concentrations in the investigated soils are reported in Table 1. Results revealed that S3 is most contaminated with values reaching 214.58 ± 33.53 mg kg−1, 48884 ±
7447.35 mg kg−1, 22913.37 ± 3274.13 mg kg−1, and 5.07 ±
0.45 mg kg−1, respectively, for Cd, Zn, Pb, and Cu. The soil
from S2 recorded heavy metal concentrations with values
77.33 ± 5.67mg kg−1 of Cd, 17399.54 ± 1298mg kg−1 of
Zn, and 8306.25 ± 817.8mg kg−1 of Pb. Regarding S1, the
observed values are within 17.43 ± 0.08mg kg−1 of Cd,
3530.52 ± 33.44mg kg−1 of Zn, 1481.28 ± 13.86mg kg−1 of
Pb, and 2.34± 0.05 mg kg−1 of Cu.
Heavy metal concentration in plant Malva sylvestris
and earthworms Lumbricus sp.
Heavy metal concentrations in Malva sylvestris from the different sites of Jebel Ressas’ mine are presented in Table 2.
Results first demonstrated that the highest levels of Pb were
observed in plants from S3 andS2 with means 425.95 ±
5.01 mg kg−1 and 63.15 ± 3.34 mg kg−1 respectively. Cd
and Zn are accumulated mostly in plants from S3 soil compared to other soils with values 8.96 ± 0.28 mg kg−1 and 1080
± 30 mg kg−1 respectively.
Concerning earthworms Lumbricus sp., Pb content was
below the detection limit in animals from the four JR’s soils
and also in the reference soil. On the other hand, Zn had
recorded the highest values in earthworms from S3 and
S1with means of 4930 ± 1330 mg kg−1 and 1670 ± 60 mg
kg−1, respectively. In addition, earthworms from S3 and S2
accumulated higher Cd concentrations and the values reached
were 33.65 ± 0.82 mg kg−1 and 13.08 ± 0.69 mg kg−1
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Table 1 Heavy metal concentrations (Pb, Cd, Zn, and Cu) in exposed sites (S1, S2, S3, and S4) compared to control site. Data presented as the mean ±
SD. *Significant difference in comparison with the reference site (p <0.05). [Hm], heavy metal concentration
[Hm] (mg kg−1)
Reference site
1481.28±13.86 *
17.43±0.08 *
2.34±0.05 *
2.33±0.18 *
214.58±33.53 *
5.07±0.45 *
0.88±0.13 *
Copper concentrations in plant and earthworm samples
were below the limit of detection.
Heavy metal content in chickens’ tissues and eggs
limit. In addition, the concentration of Zn in lungs and muscles was low in comparison with the other chicken organs.
The kidney revealed the highest level of Pb accumulation in
chickens from S1 and S2, with means 36.73 ± 0.73 mg kg−1 and
27.06 ± 0.065 mg kg−1 respectively. Conversely, the feathers
showed very high Pb values in all exposed sites, and the highest
values were 349.10 ± 13.52 mg kg−1 in site S1 and 68.8 ±
4.18 mg kg−1 and 63.73 ± 7.43 mg kg−1 in sites S2 and S3
respectively. However, the concentration of Pb in the liver, muscle, blood, and eggs was below the detection limit.
The copper concentrations for all chicken samples and eggs
were below the detection limit.
The accumulation of heavy metals in chicken’s tissues exposed to polymetallic polluted soils is presented in Table 3.
Our data revealed that Cd was most accumulated in the liver
(of chickens from S2) and kidneys (of chickens from S1) with
rates of 7.80 ± 0.31 mg kg−1 and 62.93 ± 2.08 mg kg−1 respectively. Additionally, the lung showed an important accumulation rate of Cd in all polluted sites. Moreover, the muscle
recorded the accumulation of Cd, especially in chicken from
S1 (0.15±0.008mg kg−1).
For Zn, the rate of heavy metal accumulation in the liver
was higher than that in the kidney. Thus, the chicken’s liver
from the S1 site showed the highest concentration of Zn with a
value of 2083.45 ± 151. 8mg kg−1. In addition, Zn was noted
mostly in the kidneys of animals from S1 and S4 with values
of 179.08 ± 4. 59mg kg−1 and 140.79 ± 0.25mg kg1, respectively. Interestingly, Zn was the only metal accumulated in
eggs and the other heavy metals were all below the detection
Table S1 summarizes stepwise multiple regression to estimate
regression parameters: I, α, β, γ, and δ. The values of the
coefficient of regression (R2) were between 0.87 and 0.91
and the estimated parameters were significant at the p< 0.05
Table 2 Determination of heavy metals (Pb, Cd, Zn, and Cu)
concentrations in the plant (Malva sylvestris) and the earthworm
(Lumbricus sp.) exposed to the old mine compared to the control site.
Data are presented as mean ± standard deviation; *significant difference
compared with the reference (p <0.05, ANOVA, Tukey). [Hm], heavy
metal concentration
[Hm] (mg kg−1)
Plant (Malva sylvestris )
Earthworm (Lumbricus)
Heavy metal transfer model and associated human
risk assessment
Derivation of soil-plant transfer
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Table 3 Determination of heavy metals (Pb, Cd, Zn, and Cu)
concentrations in the different organs of G. domesticus and eggs grown
in sites from the Jebel Ressas’ old mine. Data are presented as mean ±
[Hm] (mg kg−1)
standard deviation. *Significant difference in comparison with the control
site (p <0.05). [Hm], heavy metal concentration; <LD, under the limit of
level. Our results showed that transfer of Pb and Cd was influenced by the pH with δ=2.68 and δ=0.93, respectively.
However, Zn transfer was influenced by his own concentration in the soil (γ= 0.91).
Calculation of daily intake (DI) and bioaccumulation factor
(BAF) of heavy metals for G. domesticus
A summary calculation of chicken daily intake (DI) of
heavy metals due to the consumption of plants,
earthworms, and soil ingestion is listed in Table 4.
The results showed that the most important DI of heavy
metals was following soil ingestion, especially for Pb,
whose value reached a rate of 2245.51mg day−1 from
the S3 site followed by a rate of 814.01 mg day−1 from
the S2 site. In addition, the DI of Pb following the
consumption of plants was 404.5 E−03 mg day−1 in
chicken from soil S3. However, results showed that
earthworms do not contribute to the intake of lead for
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Table 4 Calculation of daily intake (DI) of heavy metals by the domestic chickens through the ingestion of plant, soil, and earthworms from
Jebel Ressas’ soils, according to Equations 7, 8, and 9
Daily intake (DI) in (mg day−1)
0.3 E−03
0.8 E−03
0.6 E−03
2.7 E−03
3.5 E−03
1.2 E−03
60.0 E−03
7.7 E−03
9.8 E−03
3.1 E−03
0.1 E−03
0.2 E−03
0.4 E−03
404.5 E−03
16.3 E−03
Also, the consumption of plants, earthworms, and soil by
chicken contributes to the intake of Cd, and the rate reached
9.8 E−03 mg day−1 following soil ingestion in the S3 site.
Concerning Zn intake, it was mainly influenced by soil
ingestion with a rate of 2240.57mg day−1 in the S3 site.
Also, plant consumption impacts Zn intake mostly in chicken
from S3, with value coming to 931.74 mg day−1.
Values of bioaccumulation factor (BAF) of heavy metals in
different internal organs of chickens (liver, muscle, kidney,
and lung) are given in Table 5. Our results revealed that Pb
bioaccumulation is observed only in kidneys (1.59 E−04 mg
kg−1), whereas for Cd, we found significant levels in all analyzed organs. However, they do not exceed limits of food
safety and animal health except for Cd in the liver by
1.11 mg kg−1.
Derivation of feed-animal transfer
A summary of the stepwise multiple regression parameters (I,
α, β, and δ) is available in Table 2. An empirical transfer
model following food intake explains the heavy metal levels
Table 5 Calculation of
bioaccumulation (BAF) from
feed to chicken organs in comparison with limit concentrations
for food safety and animal health
limits according to EC (2002) and
De Vries et al. (2007)
variability in chicken organs (0.014<R2< 0.998) between
0.014 and 0.99%.
Significant values of determination coefficient were estimated for the transferred concentration of Cd concentration
in blood (R2= 0.99). The latter was due, in the first level, to the
consumption of earthworms (δ = 0.036).
Additionally, for feathers, liver, kidney, and muscles, the
transferred concentration of Cd was influenced by the consumption of earthworm with δ = 4.6, δ = 5.39, δ = 2.11, and
δ = 0.27 respectively. In the same context, Zn transfer to
internal chicken organs was influenced more by earthworm
Moreover, Pb transfer in the kidney was influenced more
by plant consumption (α= 0.14).
Calculation of the estimated daily intake (EDI), the target
hazard quotient (THQ), and the hazard index (HI)
through the consumption of the chicken and eggs sampled
from Jebel Ressas’ mine site
The values of the estimated daily intake (EDI), the target hazard quotient (THQ), and the hazard index (HI) of heavy metals
via the consumption of chickens and eggs sampled from Jebel
Ressas’ mine site (according to Equations 12, 13, and 14) have
been listed in Table 6. The latter data were calculated only for
Cd and Zn as the remaining elements were not detected in the
chicken muscle and egg samples.
The highest EDI for chicken samples was shown for Cd
(5.58 mg kg−1 day−1) at the S2 site followed by Zn (1.49 mg
kg−1 day−1) at S1 site for adults. Besides, EDI rates for children were up to twice than adult values, reaching 8.93 for Cd
in the S1 site.
Additionally, results demonstrated that numerous THQ
values exceed 1. The highest is for Cd following the consumption of chicken meat with 4.4 at S2 site followed by S1 site
with 2.71, for adults. However, THQ values were three more
times more pronounced for children and reached 11.44 for Cd
in the S2 site.
For adults, the HI values (Figure 1) ranged from 0.67 to
4.74 while for children they are up to twice than adult values
(children HI values range from 1.74 to 12.34) indicating a
BAF (mg kg−1)
Food safety limits (mg kg−1)
Animal health limits (mg kg−1)
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Environ Sci Pollut Res
Table 6 Estimated daily intake (EDI in mg kg−1 day−1), target hazard quotient (THQ), and health risk assessment (HI) of heavy metals through the
consumption of chicken and eggs reared in Jebel Ressas’ old mining site by adults and children
EDI (Zn)
EDI (Cd)
THQ (Zn)
THQ (Cd)
EDI (Zn)
EDI (Cd)
THQ (Zn)
THQ (Cd)
Exposed sites
Control site
notable risk to the health of people living near the old mine
especially children.
One of the major purposes of ecotoxicology is to assess the
transfer of pollutants into the food chain (Hattab et al. 2015;
Banni et al. 2017). This becomes of a major interest in agricultural areas adjacent to mine sites (Boughattas et al. 2016).
With this regard, the present research is, to the best of our
knowledge, the first to use regression and mathematical
models to estimate the transfer of heavy metal contamination
from mine soils to consumed chicken organs and eggs and
consequently, to humans.
In the present study, we investigated a food chain model
constituted by soil as an interface, with plants, earthworms,
and domestic chickens living sedentarily in a mining area.
Interestingly, we worked on 5 sites characterized by a decreasing polymetallic gradient ranging from the old mine dumps to
the agricultural surrounding areas. The first three sites (S1, S2,
and S3) were classified as extremely polluted because of their
location next to the highly polluted dump (Figure S1). Site S4
was moderately polluted, located in an agricultural area
(Boughattas et al. 2016). Soils from sites S1, S2, and S3
contained Pb, Cd, and Zn concentrations exceeding the prescribed standard limits of the CEE Directive (1986) (ElkribiBoukhris et al. 2020).
The results of the present investigation revealed that
chickens reared in the polluted area revealed significant heavy
metal accumulations in their tissues. This might be due to their
direct exposure to heavy metals through the ingestion of contaminated food and/or soil particles, as suggested by Lourenço
et al. (2011), Zhuang et al. (2014), and Giri and Kumar (2017).
Our results revealed that Pb accumulation occurred only in
chicken kidneys and feathers. This can be explained by the
chicken’s ability to eliminate this heavy metal (Zamani et al.
2010; Haziri et al. 2019). Indeed, feathers are considered one
of the optimum ways to eliminate metals from a chicken’s
body (Malik and Zeb 2009; Zamani et al. 2010). For this
reason, numerous researchers use avian feathers for environmental pollution biomonitoring programs. In this study, Pb
and Zn were found in the chicken feather samples from S3
in the concentrations 68.8±4.18 mg kg −1 and 225.63±
20.01 mg kg−1 respectively. These values were higher than
that of Haziri et al. (2019), 15.50 ± 0.45 mg kg−1 and 111.0 ±
2.36 mg kg−1 Pb and Zn respectively were found in the
feathers of domestic chickens reared in the Kosovo industrial
Figure 1 HI due to ingestion of
contaminated chicken and eggs
for adults and children as a
function of site localization of the
studied area
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Environ Sci Pollut Res
Moreover, the concentrations of Cd found in the tissues of
chickens were in decreasing pattern as follows: kidney> liver>
feather> lung> muscle>blood. According to the maximum
permissible levels of trace elements in poultry set by the
European Communities (2006) and FAO/WHO (1989), heavy
metal distribution in organs can be linked to the physiological
functions of each element (Jebali et al. 2014). This is in agreement with Leontopoulos et al. (2015), as well as Indrajit et al.
(2018). These latter authors reported that different tissues of
backyard chickens reared in an industrial area presented pathological issues due to heavy metal accumulation.
Our data may suggest that earthworms have the capacity to
accumulate high levels of heavy metal, especially Cd and Zn.
This was in agreement with the work of Boughattas et al.
(2016), Mkhinini et al. (2020), and Hattab et al. (2015).
Additionally, Osioma and Hamilton-Amachree (2019) revealed that heavy metals were accumulated in earthworm
Lumbricus sp., making it a good bioindicator for soil pollution
as is the case for other annelid species (Bouraoui et al., 2010).
Also, plants from Jebel Ressas accumulated high levels of
Pb. The work of Hattab et al. (2015) showed that Medicago
sativa, plant from Jebel Ressas had accumulated high levels of
heavy metals. Béjaoui et al. (2016) has, also, worked on mallow (Malva sylvestris) as locally grown plants in Jebel Ressas
and wild food for the local population.
Interestingly, our data described a chain model approach to
assess the transfer of heavy metal contamination from soil to
human beings. This model was divided into two main parts:
the first was employed to assess the transfer of soil-plant taking into account the heavy metals loads in soil and its properties (organic matter (OM), pH, clay). The second part used
regression models to derive the transfer of heavy metals into
the tissues of chicken and to analyze the risks that humans
may face from the dietary intake of contaminated chicken.
The multiple regression results, for the derivation of soil-plant
transfer, reported high values of determination factors
(0.87<R2<0.91) from the estimated contribution of pH and heavy
metal concentration in the soil. Therefore, it is concluded that the
transfer of Pb and Cd from soil to plant was further influenced by
the pH of the soil, while Zn transfer was influenced by its concentration in the soil. Accordingly, changes in soil pH cause
variability in the availability of Pb and Cd for plants.
The results of the regression model of the food transfer
(soil, plant, and earthworm) of heavy metals into the tissues
of chicken rendered a determination factor R2 from 0.014 to
0.99. A significant R2 value (0.99) was found for the transfer
of Cd concentration from food to chicken blood. More precisely, Cd transfer in chicken blood happened from the consumption of (in decreasing order) earthworm>soil>plant.
Further, Zn concentration transfer (R2= 0.91) and Cd concentration transfer (R2= 0.5), to chicken kidneys were more influenced by earthworm consumption at the first level, and then
by plant consumption.
The derivation model results showed that heavy metal
transfer to the chicken tissues was influenced mainly by earthworm consumption. Other studies have demonstrated that
heavy metals in plants may contribute to the transfer of Pb
in different parts of chicken such as the kidney, liver, and
feathers. Using regression and mathematical models, Franz
et al. (2008) proved that Cd was transferred from vegetalbased food to cattle kidneys, liver, and meat.
To assess human health risk associated with heavy metal
contamination from chickens and associated eggs in Jebel
Ressas mining area, the EDI, THQ, and HI were calculated.
Results of the EDI of heavy metals suggest that heavy metal
pollution causes health risks to the consumers of Jebel Ressas.
According to the classification of New York State
Department of Health (NYSDOH (New York State
Department of Health) 2007), ratios obtained for analyzing
heavy metals were classified as low for Zn in all sites except
for S1 (which was classified as moderate risk), whereas Cd
was several times higher than the RfD, indicating it to be a
potential health hazard to the public. Our findings are in concordance with the results of Javed and Usmani (2016), which
proved a potential risk of Cobalt (Co) through the consumption of freshwater fish inhabiting a polluted effluent-loaded
Target hazard quotient (THQ) proved that Cd (exceed 1 for
S1, S2, and S3 sites) and Zn in S1 may pose potential health
risks associated with overexposure. For Zn, in the other sites
and Pb and Cu, the risk of non-carcinogenic toxic effects is
assumed to be low. The hazard index (HI) was above the unity
in the mine sites (S1, S2, and S3) and values were between 2.3
and 4.4, which may indicate a possible synergy between trace
elements. Therefore, possible interactions between heavy
metals even for the essential metals could present an alarming
public health risk. Studies have shown that high intake of Zn
induces production of Cu binding proteins (metallothionein)
in intestinal cells and prevents systemic absorption (King
et al., 2006; FDA (Food and Drug Agency) 2011).
The present investigation aimed to develop a model that links
heavy metal content in soil, earthworm, and plant to chicken
dietary exposure in order to assess health risks. Our study
provided clues of the transfer of heavy metals suggesting that
it contributes to their accumulation in the organs of reared
chickens. Also, results revealed a considerable risk to the
health of local inhabitants especially children. Indeed, the calculated HI ranged between 2.58 and 4.74 for adults and
reached 12.34 for children. Therefore, this study highlighted
the crucial role of diets based on chickens grown in the contaminated areas, on health risks for local residents of Jebel
Ressas especially for children.
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Environ Sci Pollut Res
Supplementary Information The online version contains supplementary
material available at
Acknowledgements This work was supported by funds from the
Ministry of Higher Education, Research Laboratory Agrobiodiversity,
and Ecotoxicology (LR21AGR02). The authors thank the University of
Tunis Al Manar, Faculty of Mathematical, Physical and Natural Sciences
of Tunis, Doctoral School “Sciences et Technologies du Vivant et
Sciences de la Terre” for the Research fellowship to the student who
developed the research.
Author contribution Sameh Elkribi-Boukhris (SEB): data curation; formal analysis; investigation; roles/writing—original draft; writing—
review and editing
Naceur M’hamdi (NM): data curation; formal analysis; investigation;
Iteb Boughattas (IB): formal analysis; investigation; supervision
Sondes Helaoui (SH): formal analysis
Cecile Coriou (CC): formal analysis
Sylvie Bussiere (SB): formal analysis
Valerie Sappin-Didier (VS): data curation; funding acquisition; methodology; resources; supervision; validation; roles/writing—original draft;
writing—review and editing
Mohamed Banni (MB): data curation; funding acquisition; methodology; resources; supervision; validation; roles/writing—original draft;
writing—review and editing
Data availability All data generated or analyzed during this study are
included in this published article.
Ethics approval and consent to participate Not applicable.
Consent for publication Not applicable.
Competing interests The authors declare no competing interests.
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