Regional Studies in Marine Science 62 (2023) 102943

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Arsenic, mercury, cadmium and lead contents in Algerian continental

and marine farming fish and human health risk assessment due to
their consumption
Boubeker Khellaf a , Leila Bouayad a , Ali Benouadah b , Taha Mossadek Hamdi a ,
∗
Rachida Chekri c , Petru Jitaru c ,
a
Laboratory of Food Hygiene and Quality Insurance System, High National Veterinary School, 16270 Algiers, Algeria
b
Laboratory of material sciences and environment, University of Algiers 1, 16000 Algiers, Algeria
c
ANSES, Laboratory of Food Safety, F-94701, Maisons-Alfort, France

article info a b s t r a c t

Article history: This study evaluates the level of arsenic (As), mercury (Hg), cadmium (Cd) and lead (Pb) in the flesh
Received 2 January 2023 of grey & red tilapia, sea bream & bass reared in sea and continental waters from four Algerian
Received in revised form 13 March 2023 aquaculture farms. For this purpose, 145 fish samples, 15 samples of fish feed and 20 samples of
Accepted 26 March 2023
farms waters were analysed using an accredited method based on inductively coupled plasma-mass
Available online 3 April 2023
spectrometry. The most abundant contaminant found in the fish samples was As (0.39–1.56 mg kg−1
Keywords: wet weight (wet wt)) followed by Hg (0.02–0.08 mg kg−1 wet wt). A negative correlation was observed
Reared fish between the As level and the fish size, while this correlation was found to be positive for Hg. The levels
Algerian continental and marine farms of Pb and Cd were very low in all fish species, generally below the quantification limit. In fish feed, the
Trace elements contaminants levels were consistently higher compared to those in fish muscle, ranging from 0.03 to
Health risk assessment 0.09 mg kg−1 (wet wt) for Hg and from 0.9 up to 1.7 mg kg−1 (wet wt) for As. A positive correlation
between the contaminant level in feed and in the fish muscle was observed only for As. The levels
of Pb, Cd and Hg in the farming waters samples were below the detection limits, whereas As was
quantified only in the water samples of Bejaia and Chlef farms (0.11 and 0.08 mg kg−1 , respectively).
The estimated daily intake and the target hazard quotient related to the consumption of the fish species
analysed in this study indicate no non-carcinogenic adverse effects on humans. The carcinogenic risk
related to As in red tilapia (3.75 × 10−4 ) and sea bream (2.03 × 10−4 ) exceeded the acceptability
thresholds (10−4 ). This indicates that over their lifetime, an individual consuming the above mentioned
fish species, may be at a higher risk to develop cancer.
© 2023 Elsevier B.V. All rights reserved.

1. Introduction they have the potential to disrupt physiological functions such

as endocrine signalling and enzyme activity, which can lead to
Aquaculture is a growing industrial sector contributing signifi- adverse health effects in humans (Arisekar et al., 2020).
cantly to the food industry becoming an important source of high Mass poisoning due to the ingestion of food contaminated
quality proteins and omega 3 fatty acids (Chandra et al., 2001). with toxic trace metals have occurred in several countries, such
Although the health benefits of a diet including fish are well as the ItaiItai syndrome endemic to the Jinzu River region (China),
known, fish may also contain toxic substances, including trace caused by Cd poisoning and manifested by osteomalacia and os-
elements. Since fish have a relatively high rank in the aquatic teoporosis associated with kidney dysfunction (Jarno, 2011) and
food chain, the risk of bioaccumulation of trace metals is rather the intoxication with methylmercury derivatives of the villagers
high, especially in large/predatory fish (Kandyliari et al., 2021). of Minamata Bay, Japan (Colas et al., 2011).
Fish may accumulate toxic elements such as cadmium (Cd), lead Assessment of trace elements in the edible parts of farmed fish
(Pb), mercury (Hg) and arsenic (As) from the aquatic food web, has been a major environmental focus in different countries such
seawater and from the sediments (El-Moselhy et al., 2014). These as Algeria (Lounas et al., 2021), Malaysia (Taweel et al., 2011),
trace elements have no known role in biological systems, but China (Cheung et al., 2008) and Greece (Elisavet et al., 2019).
However, none of these studies has established a correlation be-
∗ Corresponding author. tween the accumulation of trace elements in fish and the farming
E-mail address: petru.jitaru@anses.fr (P. Jitaru). mode (marine or continental farms).

https://doi.org/10.1016/j.rsma.2023.102943
2352-4855/© 2023 Elsevier B.V. All rights reserved.
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

Fig. 1. Location of the aquaculture farms of this study.

In Algeria, there are no studies assessing the levels of these of the farmed fish by these toxic elements, an analysis of the feed
contaminants in continental fish farms. Similarly, several marine fish and the water in the farming area was carried out for the first
fish farms have never been studied neither the environmental time in Algeria in this work.
contamination (feed, water) prevailing in fish farms and the levels Fish farming in Algeria has been developing to achieve food
of these contaminants in fish. It has often been argued that the security in terms of fish products. Currently, the active and pro-
preservation of the quality of the aquatic environment guarantees ductive aquaculture farms cannot export farmed fish to other
the quality of the product (Kalantzi et al., 2016). countries. This sector is not developed on the whole national
In this context, it is important to assess if the trace element territory. This study highlights the critical points of this sector
accumulation in fish is influenced by the farming mode (ma- in terms of chemical pollution (contamination of farmed fish,
rine or continental) and by environmental contamination (feed fish feed and water in the farming area by As, Hg, Cd and Pb).
and water) as a possible sources of metal element pollution in Additionally, the sanitary risk related to these contaminants due
farmed fish. The metallic elements are naturally present in the to the consumption of the fish species investigated here is also
biosphere, they come from volcanic activities, mechanical and addressed.
chemical erosion of rocks and soil leaching. They follow a geo-
chemical cycle that ends in the aquatic environment (continental 2. Material and methods
or sea water) (Garret Robert, 2000). However, the large quantity
of these metallic elements is mainly of anthropic origin due to the 2.1. Samples collection
increase of industrial, agricultural and domestic discharges, port
activities and maritime transport (European Environment Agency, A total of 180 samples including 145 fish, 15 feed and 20 water
2006). This can lead to contamination of waters in farming areas, samples from the farm areas were collected between March and
especially for marine fish farms studied due to their location October 2021. Amongst the fish samples, 36 sea-bass and 24 sea-
near ports which could be a potential source of contamination. bream were sampled from the marine fish farm of Chlef, 34 sea
In continental farms, the potential source of water contamination bream samples from the marine fish farm of Bejaia, 27 samples
would be the use of fertilizers due to their location in agricultural of grey tilapia from the continental fish farm of Ain Defla and
areas. The second possible source of contamination of farmed 24 red tilapia samples from the continental fish farm of Algiers.
fish in all studied farms with these toxic elements is the feed. The rearing cycle started in October 2020, marketing from July
The use of raw materials such as fish tissue and fish oil in the 2021 and the end of the cycle was around December 2021. The
preparation of fish feed can contribute to their contamination. period of fishing and marketing is generally longer than 5 months,
The study conducted by Kalantzi et al. (2016) reported relatively depending on the market demand and the volume of the annual
high levels of these elements in the feed of sea bass and sea bream production of fish in the farm. We collected several samples at
reared in Greece. different times, even after the commercialization of the fish until
The main objective of this study is to assess the levels of Pb, almost the end of the rearing cycle in order to have samples of
Cd, Hg and As in the muscle tissue of sea bream (Sparus aurata), the largest fish.
sea bass (Dicentrarchus labrax), grey tilapia (Oreochromis niloticus) Four farms we chosen for this study, from which two were ma-
and red tilapia (resulting from the crossing of O. niloticus & O. rine farms (in the regions of Chlef and Bejaia) and two continental
mossambicus) reared in four Algerian farms located in different farms (regions of Algiers and Ain Defla) (Fig. 1). Sampling was
geographical areas that have never been studied before. carried out according to the recommendations of (EC) 333/2007
The choice of fish species as subjects of study is motivated by (Anon, 2007) regulation and 96/23/EC directive (Anon, 1996).
the fact that in Algeria, they are the most consumed farmed fish. Each farm was considered a lot and subdivided into sub-
Sea bream and sea bass are reared in marine environments, while lots based on annual production. One-third of the samples were
grey tilapia and red tilapia are reared in fresh water in continental collected from the farms before the fish reached market size, and
fish farms (Ministry of Fisheries and Fishery Resourcesof Algeria, the remaining two-thirds were fish ready to market. We opted
2020). for this sampling plan to be in the same conditions of sampling
The correlation between the accumulation of Pb, Cd, Hg and As applicable to fish. Also, to be as close as possible to the reality of
in fish and the farming mode (marine and continental) was also the field concerning these farmed fish. Furthermore, in order to
investigated. In order to determine the sources of contamination study the correlations between fish contamination by these ETM
2
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

and fish size, we have taken samples according to the size/age of Table 1
®
the fish (before and after marketing). In addition, we have taken Results of trueness obtained for the analysis of CRM ERM CE278k (muscle
tissue) by ICP-MS.
samples from fish feed and water to look for potential sources of
Analyte Certified CIa Measured ±SDb
fish contamination. (mg kg−1 ) (mg kg−1 ) (mg kg−1 , n = 27)
In the studied fish farms, the marketing of fish starts at the
As 6.70 5.20 – 8.20 6.20 ± 0.20
age of 9 months, which corresponds to a minimum commercial Hg 0.071 0.055 – 0.087 0.072 ± 0.004
size/minimum commercial weight of ≈ 18 cm/150 g for tilapia, Pb 2.18 1.69 – 2.67 2.16 ± 0.08
20 cm/150 g for sea bream and ≈ 25 cm/180 g for sea bass, as Cd 0.336 0.26 – 0.41 0.31 ± 0.008
recommended by the (EC) 1967/2006 (Anon, 2006) regulation and a
CI : confidence interval.
the Algerian regulation N◦ 04-86 (Anon, 2004). b
SD : standard deviation.
In order to assess the origin of eventual fish contamination, the
levels of trace elements in fish feed and in the farming water were Table 2
also measured. For this purpose, a total of 15 feed samples and Results of trueness obtained for the analysis of the CRM SRM 1640a (natural
20 water samples collected from the farm sites were analysed. water) by ICP-MS.
For fish feed, we collected 3 feed samples for each fish species (≈ Analyte Certified mass Measured mass
fraction ±Ua fraction ±SD
100 g ×15), except for sea bream which is raised in two different (µgkg −1 , k = 2) (µgkg −1 , n = 3)
fish farms (n = 6). The samples were collected from different
As 8.01 ± 0.067 8.16 ± 0.58
feed bags just before they were fed to the fish. In addition, 5 Pb 12.01 ± 0.04 12.43 ± 0.15
water samples were taken at each fish farm from the surface Cd 3.96 ± 0.072 3.70 ± 0.20
water (depth of no more than 20 cm) in the floating cages (marine a
U: expanded uncertainty.
farms) and in the ponds (continental farms) (≈ 100 ml × 20). The
feed and water samples were collected at the same time as the
fish samples at different periods, almost at the beginning, middle
and at the end of rearing cycle (March–October 2021). All samples Hg, 0.0002/0.0007 mg kg−1 for Cd and 0.0006/0.002 mg kg−1 for
were packed in polyethylene bags, identified and transported to Pb.
the laboratory in ice containers. The method accuracy and precision were assessed on a daily
basis by the analysis of two certified reference materials (CRM),
namely ERM-CE278k (European reference material, European
2.2. Sample preparation
Commission, muscle tissue) and NIST-1640a (National institute
of standards & technology, Natural Water) (see Tables 1 and 2).
The fish from the same farm and of similar age were measured,
Confidence interval (CI) was calculated using the certified
weighed and sorted by size. All not edible parts were removed
value (M) of the CRM such as:
(viscera, head, bones, skin and fins) to obtain a sample of ∼ = [ ]
100 g of flesh. The resulting samples were freeze-dried and then CVR × M
CI = M ± k ×
ground individually using an agate mortar and pestle. Freeze- 100
dried fish flesh, feed and water samples were stored in a sterile,
hermetically sealed, and properly labelled 100-ml polypropylene with k = 3 (p = 99%) and CVR , the intermediate precision
bottles at 4◦ C until the analysis period (April and July 2022) to coefficient of variation (CVR = 7.5 %).
avoid any change in their chemical composition.
2.4. Statistical analysis
2.3. Determination of trace elements by ICP-MS
The results are reported in mg kg−1 wet weight (wet wt) for
Samples were analysed using an accredited method described the fish flesh, mg kg−1 raw weight for fish feed and mg kg−1 for
by (Chevallier et al., 2015). The analyses were performed in the water samples.
the Trace Metals and Minerals unit of the French Agency for Statistical analyses were carried out using the software IBM
Food, Environmental and Occupational Health & Safety (ANSES) SPSS Statistics 20, with a level of significance set at α = 0.05 to
in Maisons-Alfort, France. calculate the means, standard deviation, minimum and maximum
Briefly, ∼
= 0.3 g of the freeze-dried fish sample or fish feed values. The Shapiro–Wilk and Kolmogorov–Smirnov normality
and ∼= 4 g of water are weighed and placed in a quartz di- tests were used (p < 0.005: the data do not follow a normal dis-
gestion vessels. Then, 3 mL of ultrapure nitric acid (HNO3 , 67% tribution). Therefore, the non-parametric tests (Mann–Whitney
v/v, VWR chemicals Prolabo) are added to each vessel; the ves- test and the Kruskal–Wallis test with independent samples) were
sels are hermetically sealed, shaken well and left overnight at used to compare the levels of Pb, Cd, Hg and As in fish mus-
room temperature. Further, 3mL of ultrapure water (18.2 mΩ cle (according to species, size, and farming mode) and in fish
cm) are added before placing the vessels in a closed microwave feed. However, no statistical test was used to compare the water
programmed for digestion in four successive steps: 1 min at samples due to the low levels recorded, so there is no need to
500 W, 10 min at 800 W, 10 min at 1000 W and then cooling compare contamination between farms.
during 20 min. The resulting digest samples are transferred to For the levels between the limit of detection (LOD) and the
polypropylene tubes and filled with ultrapure water up to a limit of quantification (LOQ), the average of the LOD and LOQ
volume of 50 mL. were used for statistical analyses, whereas 12 LOD was taken into
The determination of Pb, Cd, Hg and As levels was carried out account for the levels <LOD.
by inductively coupled plasma-mass spectrometry (ICP-MS). For
this purpose, six standards solutions containing respectively: 0, 2, 2.5. Sanitary risk assessment
5, 7.5, 10 and 20 µgL−1 of As, Pb, Cd and Hg were used for the
external calibration. To assess the risk related to the consumption of the farmed
Limits of detection and quantification (LOD/LOQ), calculated fish investigated in this study, we calculated the estimated daily
on a wet-weight basis were 0.001/0.004 mg kg−1 for both As and intake (EDI), the target hazard quotient (THQ) and the hazard
3
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

index (HI) (United States Environmental Protection Agency, 2000)

as well as the carcinogenic risk (CR) (Saha et al., 2016).
The estimated daily intake (EDI in µg/kg/day) was calculated
using Eq. (1) (United States Environmental Protection Agency,
2000) taking in to account an Algerian adult weight of 60 kg and
a consumption of 9.7 g of fish per day (Mehouel et al., 2019):
C × DC
EDI = (1)
BW
where:
C, mean concentration of the trace element in the fish flesh
(µg g−1 );
DC, daily (fish) consumption (9.7 g day−1 );
BW, mean body weight of the Algerian population (60 kg).
The Target Hazard Quotient (THQ) was calculated using the
Eq. (2) (United States Environmental Protection Agency, 2000):
EFr × ED × FIR × C × 10−3
THQ = (2)
RFD × BW × ATn
where:
THQ, risk associated with a single element;
EFr, exposure frequency (set as 365 days year−1 ); Fig. 2. Mean levels ± standard deviation (mg kg−1 wet wt) of As and Hg in
fish muscle according to farming mode (p < 0.05).
ED, exposure duration (70 years) equivalent to the life ex-
pectancy at birth;
BW, average body weight (60 kg for adults);
FIR, seafood ingestion rate in Algeria (9.7 g/person/day)
(Mehouel et al., 2019);
C, contaminant level in the sample (mg kg−1 wet wt);
RFD, oral reference dose of Cd, Hg, Pb and As fixed by USEPA,
as follows: 10−3 ; 1.6 × 10−4 ; 4 × 10−3 ; 3 × 10−4 mg/kg/day, re-
spectively (United States Environmental Protection Agency, 2000);
ATn, average exposure time for non-carcinogens (365 days/year
× 70 years).
THQ <1 indicates that the daily exposure is unlikely to cause
non-carcinogenic adverse effects in human health during a life-
time, while THQ ≥ 1 indicates possible non-carcinogenic adverse
effects (United States Environmental Protection Agency, 2000).
The hazard index (HI) or total THQ (TTHQ) is determined to
assess the risk associated with multiple contaminants that cause
a non-carcinogenic adverse effect on an organism.
HI is the total THQ (TTHQ) and it is calculated by summing
the THQs of the measured contaminants (Eq. (3)) (United States
Environmental Protection Agency, 2000):
HI = TTHQ = THQ(As) + THQ(Hg) + THQ(Cd) + THQ(Pb) (3)
Global exposures estimated using hazard quotients <1 are un-
likely to result in any non-carcinogenic adverse health effects
over a lifetime of exposure and are normally considered accept- Fig. 3. Mean levels ± standard deviation (mg kg−1 wet wt) of As and Hg in
able (United States Environmental Protection Agency, 2000). fish muscle according to fish size (p < 0.05).
The carcinogenic risk (CR) is estimated as the lifetime proba-
bility that an individual will develop cancer following exposure
to a potential carcinogen. CR is calculated as described by Saha 3. Results and discussion
et al. (2016) Eq. (4).
The mean levels of Pb, Cd, Hg and As measured in the fish
CR = CSF×EDI (4) analysed in this study are reported in Table 3. A comparison of our
where CSF are the cancer slope factors (As: 15 × 10−4 , Cd: results obtained with those reported by other studies is provided
63 × 10−4 and Pb: 85 × 10−7 (µg/kg/day)−1 ) (Raknuzzaman in Table 4.
et al., 2016). Figs. 2 and 3 show the mean levels of As and Hg in fish muscles
The total cancer risk (TCR) was calculated by summing the in- according to the farming mode and fish size, respectively. Cd and
dividual cancer risks of multiple carcinogens (Bamuwamye et al., Pb levels were very low in all fish species sampled (data not
2015) Eq. (5). shown). Fig. 4 shows the mean concentrations of studied trace
elements in fish feed.
TCR = CR(As) + CR(Cd) + CR(Pb) (5)
where the acceptable levels of CR or TCR range are from 10−4 to 3.1. Arsenic
10−6 ; CR or TCR values >10−4 are unacceptable and those <10−6
indicate a negligible risk of cancer an individual’s lifetime (Varol Arsenic is the most abundant contaminant found in the dif-
et al., 2017). ferent samples (fish, feed and water) analysed in this study. The
4
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

Table 3
Trace elements concentrations (mean ±standard deviation, mg kg−1 wet wt) in fish muscle according to species and farm location.
Farming mode Marine Continental
Fish species Sea bass Sea bream Sea bream +sea Red tilapia Grey tilapia
bass
Farm location Chlef Bejaia Chlef Chlef+Bejaia Chlef Algiers Ain Defla
Number of samples 36 34 24 58 60 24 27
Mean size (cm)Min–max 29 24 25 24 27 24 23
(20–32) (16–27) (15–30) (15–30) (15–32) (15–32) (14-31)
Mean weight (g)Min–max 300 210 235 220 275 240 210
(120–410) (60–370) (80–450) (60–450) (80–450) (60–550) (60-490)
As mean 0.39±0.10a 0.80±0.10b 0.88 ± 0.36 0.84±0.25a 0.59±0.34b 1.56±0.57a,b 0.42±0.40a,b
min–max 0.28–0.67 0.60–1.1 0.52–2.2 0.52–2.2 0.28–2.2 0.65–2.7 0.025-1.20
Hg mean 0.080±0.020a 0.050±0.010b 0.053 ± 0.023 0.051±0.019a 0.066±0.023b 0.073±0.028a,b 0.020±0.020a,b
min–max 0.024–0.11 0.015–0.079 0.014–0.089 0.014–0.089 0.014–0.11 0.026- 0.11 <LODc -0.056
Cd mean <LOQd <LOQ <LOQ <LOQ <LOQ 0.001 ± 0.001 <LOQ
min–max <LODe -0.001 <LOD-0.002 <LOD-0.002 <LOD-0.002 <LOD-0.002 <LOQ-0.002 <LOD-<LOQ
Pb mean <LOQf 0.004 ± 0.005 <LOQ 0.003 ± 0.004 <LOQ 0.003 ± 0.002 <LOQ
min–max <LODg -0.005 <LOQ-0.029 <LOD-0.004 <LOD-0.029 <LOD-0.005 <LOQ-0.011 <LOQ-0.004
a
significant differences between species (p < 0.05).
b
significant differences between sites (p < 0.05).
c
LOD (Hg) = 0.001 mg kg−1 .
d
LOQ (Cd) = 0.0007 mg kg−1 .
e
LOD (Cd) = 0.0002 mg kg−1 .
f
LOQ (Pb) = 0.002 mg kg−1 .
g
LOD (Pb) = 0.0006 mg kg−1 .

highest As levels were measured in fish reared in continental

farms compared to marine farms (see Table 3 and Fig. 2). Its
highest levels (1.56 ± 0.57 mg kg−1 wet wt) was measured in
the red tilapia reared in the continental farm of Algiers, followed
by sea bream reared in the marine farms of Chlef and Bejaia
(0.88 ± 0.36 mg kg−1 and 0.80 ± 0.10 mg kg−1 , respectively) and
grey tilapia reared in continental water in Ain Defla (0.42 ± 0.40
mg kg−1 ). Sea bass reared at sea in Chlef showed the lowest
concentration (0.39 ± 0.10 mg kg−1 ) (p < 0.05).
A negative correlation (p < 0.05) between As content and
the fish size was observed in this study. Actually, the highest
As levels were measured in fish of pre-market size and not in
fish ready to market (Fig. 3). Previous studies have reported also
negative correlation between trace element concentrations in fish
tissues and fish size (Henry et al., 2004). These results corroborate
previous studies (Table 4) that reported relatively high As levels
in fish (Zhang et al., 2016). Our results for tilapia are consistent
with the results reported by the study of Cheung et al. (2008)
Fig. 4. Mean levels ± standard deviation (mg kg−1 raw weight) of Pb, Cd, Hg
in five tilapia farms in China (0.42–2.24 mg kg−1 ) and the study and As in fish feed.
of Avigliano et al. (2016) on two wild fish species in Argentina
where they recorded values ranging from 0.35 to 1.30 mg kg−1 .
However, in Greece, Kalantzi et al. (2016) had reported higher
as As in fish depends on several parameters such as ecological
values in farmed sea bass (0.42–1.06 mg kg−1 ) and farmed sea
factors (season, pH and temperature of the water, etc.), the indi-
bream (0.98–2.99 mg kg−1 ).
viduals’ life cycle (Rajeshkumar et al., 2018; Batvari et al., 2016)
It is worth to underline that inorganic As is generally absorbed
and also the size of the fish. Therefore, the negative correlation
via the water column and food while to organic As species (e.g. ar-
between As content and fish size is most probably related to the
senobetaine) are absorbed only via the food, the latter species
high metabolic activity of younger fish, which is known to be an
accumulating at high concentrations in muscle tissue (Hong et al.,
important factor in the accumulation of trace elements in fish
2014). Therefore, the lower levels of As measured in marine and
(Henry et al., 2004).
continental farm water, in contrast to the high concentrations in
fish feed, suggests that the contamination is foodborne.
The levels of As in the farms water samples were <LOD, except 3.2. Mercury
for the marine farms of Bejaia and Chlef (0.11 ± 0.03 mg kg−1 and
0.08 ± 0.05 mg kg−1 , respectively) whereas in fish feed (Fig. 4), Mercury is the second abundant element found in the fish
As levels are high, ranging from 0.90 ± 0.30 to 1.7 ± 0.5 mg kg−1 . samples analysed in this study, after As. The highest Hg levels
It is worth to note that a positive correlation was observed were measured in seabass reared in the Chlef farm (0.08 ± 0.02
between the As levels in the fish feed and its concentration in the mg kg−1 ) and in red tilapia from Algiers farm (0.073 ± 0.028 mg
muscle tissue in all fish species. The level of a trace element such kg−1 ), followed by sea bream reared in the Chlef and Bejaia farms
5
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

Table 4
Levels of As, Hg, Cd and Pb in muscle tissue (mg kg−1 wet wt) of farming fish and comparison with other studies and regions.
Species Region As Hg Cd Pb Reference
Algeria Algiers 1.56 0.07 0.001 0.003 This study
Ain Defla 0.42 0.02 <LOQ <LOQ
Zambia Farm1 0.04 0.007 0.001 0.008 Simukoko et al. (2022)
Farm 2 0.03 0.002 0.001 0.007
Farmed tilapia
Egypte // 0.94 0.08 0.29 Hamada et al. (2018)
Malaysia // // 0.002 0.023 Taweel et al. (2011)
Taiwan 1.27 // 0.01 0.14 Ling et al. (2013)
Sanjiao 2.24 0.02 0.71 2.15
China Guangzhou 0.78 0.01 0.25 2.42 Cheung et al. (2008)
Shipai 0.42 0.03 1.57 4.73
Changan 1.29 0.01 0.43 7.74
Maipo 1.84 0.02 0.08 0.55
Bejaia 0.80 0.05 <LOQ 0,004 This study
Algeria
Chlef 0.89 0.053 <LOQ <LOQ
Farmed seabream Algiers, Tizi 3.52 // 0.004 0.003 Lounas et al. (2021)
Ouzou, Ain
temouchent
Aegean and // 0.03 0.002 0.06 Elisavet et al. (2019)
Greece Crete Sea
AegeanSea 1 2.99 0.10
<LOD <LOD Kalantzi et al. (2016)
AegeanSea 2 0.98 0.02
IonianSea 2 1.84 0.04
Algeria ; Chlef farm 0. 39 0.08 <LOQ <LOQ This study
Aegean and // 0.05 0.001 0.06 Elisavet et al. (2019)
Farmed seabass Crete Sea
Greece
AegeanSea 1 1.06 0.07
AegeanSea 2 0.42 0.06 <LOD <LOD Kalantzi et al. (2016)

IonianSea 1 1.05 0.06

IonianSea 2 0.94 0.06
Algeria : Chlef and Bejaia farms 0.67 0.06 <LOQ 0.002 This study
Farmed seabream and seabass
Tunisia : 4 farms in the Northeast // 0.06 0.04 0.05 Chouba et al. (2016)
Croatia : AdriaticSea 2.57 0.17 0.02 0.14 Rozic et al. (2014).

Note: <LOQ : results between the limit of detection (LOD) and the limit of quantification (LOQ): Cd (0.0002, 0.0007), Pb (0.0006,0.002)., <LOD : results below the
LOD.

(0.05 ± 0.02 mg kg−1 and 0.05 ± 0.01 mg kg−1 , respectively). The 3.3. Cadmium and lead
lowest levels were measured in grey tilapia reared in Ain Defla
(0.02 ± 0.02 mg kg−1 ). In the Chlef farm, the sea bream was less Cadmium and Pb levels were very low in both fish samples and
contaminated than the seabass (see Table 3) (p < 0.05). in the farm waters (Table 3). There were no significant differences
These results are compatible with the levels reported in the between marine and continental fish farms neither between pre-
literature, which range from 0.002 ± 0.001 mg kg−1 to 0.94 ± 0.1 market size fish and those ready-to-market fish (data not shown)
mg kg−1 in farmed tilapia, 0.02 to 0.17 mg kg−1 in farmed sea (p > 0.05).
bream and sea bass (Table 4). Elisavet et al. (2019) in Greece The levels of Pb and Cd are also lower than those reported
recorded values of 0.05 mg kg−1 in farmed sea bass and 0.03 mg in most studies focusing on farmed fish (Table 4). Most levels of
kg−1 in farmed sea bream, these results are slightly lower than Pb and Cd were <LOQ, except for red tilapia from Algiers’ conti-
ours for the same species. However, for farmed Tilapia, the results nental farm (Cd = 0.001 ± 0.001 mg kg−1 , Pb = 0.003 ± 0.002
reported by Hamada et al. (2018) in Egypt (0.94 mg kg−1 ) were mg kg−1 ) and for sea bream from Bejaia marine farm (Pb =
higher than our results. 0.004 ± 0.005 mg kg−1 ). The results reported by Elisavet et al.
It is also worth to note that the highest Hg levels were mea- (2019) in Greece regarding Cd and Pb contamination in farmed
sured in fish from marine farms compared to continental farms sea bass (0.001 and 0.06 mg kg−1 ) and farmed sea bream (0.02
(Fig. 2) and also in fish ready to market compared to fish of and 0.06 mg kg−1 ) respectively, were higher to the results we
pre-market size (Fig. 3). recorded for the same species. For farmed tilapia, Taweel et al.
The correlation between Hg content and the fish size was (2011) reported a Cd and Pb contamination rate of 0.002 and
positive, in contrast to the case of As. However, Hg was weakly 0.023 mg kg−1 , respectively. These results are higher than those
detected in fish feed (Fig. 4) and not detected at all in farm observed in this study.
waters. These variations in Hg levels suggest that the bioaccu- The low levels of Pb and Cd in the fish samples could be related
mulation depends on the fish species, its physiological capacity to the nature of the tissues (muscle) considered for analysis;
of assimilation and excretion, its anatomy (size) and the duration actually, it is known that the tropism of metallic elements is
of exposure to the pollutants (Casadevall et al., 2017). higher for organs and viscera than for muscle (Kojadinovic et al.,
6
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

2007). In the study by Latif et al. (2022), it was reported that Table 5
the Pb level was lower in muscle tissues than in gill, liver and Estimated dietary intake (EDI) (µg/kg/BW/day), estimated weekly intake (EWI)
(µg/kg/BW/week), target hazard quotient (THQ) and hazard index (HI) for As,
intestine. Similarly, the study of Ishak et al. (2020) showed that Hg, Cd and Pb in studied fish species.
the highest levels of Pb and Cd were in gills, bones and the lowest EDI EWI THQ HI
in the muscle tissues.
As 0.14 0.95 0.45
Cadmium and Pb levels measured in the fish feed were rela- Sea bream Hg 0.008 0.060 0.050 0.50
tively high (Fig. 4). It is worth to note that in the selected farms, Cd 7 × 10−5 5 × 10−4 7 × 10−5
an intensive rearing system is used, the fish feed consisting of a Pb 4 × 10−4 0.003 10−4
mixture of ingredients designed to provide all nutrients needed As 0.063 0.45 0.21
for fish growth. Our results in terms of Pb and Cd in fish feed Sea bass Hg 0.012 0.090 0.075 0.28
corroborate with the results in the study by Kalantzi et al. (2016) Cd 7 × 10−5 5 × 10−4 7 × 10−5
Pb 2 × 10−4 0.002 5 × 10−5
reporting similar data in the feed of sea bream and sea bass reared
in the three aquaculture farms in Greece. These authors found the As 0.064 0.45 0.21
Grey tilapia Hg 0.003 0.020 0.019 0.23
same pattern of contamination of fish feed with Pb, Cd, Hg and
Cd 7 × 10−5 5 × 10−4 7 × 10−5
As as in our study. Pb 2 × 10−4 0.002 5 × 10−5
It is likely that fish feed contamination with trace elements As 0.25 1.75 0.83
such as Pb, Cd, Hg and As arises from the raw materials such as Red tilapia Hg 0.011 0.080 0.070 0.90
fish tissues and fish oil used for the preparation of the fish feed. Cd 2 × 10−4 0.002 2 × 10−4
These raw materials contain all the nutrients to cover the nutri- Pb 4 × 10−4 0.003 10−4
tional needs of fishes but they also contain toxic trace elements
such as Pb, Cd, Hg and As (Medale et al., 2013).
2017 (Food and Agriculture Organization of the United Nations,
3.4. Trace element levels in continental and sea farm waters 2020). This very low threshold is due to several factors: the low
production which does not cover the demand, the food habits
The analysis of all water samples collected from both con- of the population where fish is not a common food source, the
tinental and marine farms showed levels of As, Hg, Cd and Pb high cost of fish and the low purchasing power of the Algerian
<LOD, with the exception of As, whose highest levels were of population.
0.11 ± 0.03 mg kg−1 and 0.08 ± 0.05 mg kg−1 in the marine The EWI values were <PTWI established by European Food
farms of Bejaia and Chlef, respectively. Safety Authority (As, Cd, Pb: 2.5 µg/kg/week) and Joint FAO/WHO
These results were lower than those reported in the study of Expert Committee on Food Additives (inorganic As, Hg, Cd and
Avigliano et al. (2015) in five areas in Argentina, the reported Pb: 15, 5, 7, 25 µg/kg/week, respectively (European Food Safety
levels of As, Hg, Cd and Pb were ranged (3.9 to 367, 0.07 to 0.63, Authority, 2011; Joint FOA/WHO Expert Committee on Food Ad-
0.17 to 1.0 and 0.9 to 8.22 µg L−1 , respectively). ditives, 2011). In addition, the THQ and HI were overall <1. These
The results could be related to the location of the continental data indicate the absence of risk of non-carcinogenic adverse
farms, which are far from anthropogenic and natural sources effects for the Algerian population consuming the fish analysed
of pollution. Nevertheless, the marine farms are located in the in our study, although relatively high As levels were found in
Mediterranean Sea, which is one of the most polluted seas in some samples. It is known that As is present in fish mainly in the
the world, due to maritime transport and oil accidents (Euro- form of arsenobetaine (non-toxic), whereas its toxicity is mainly
pean Environment Agency, 2006). In addition, the Algerian coasts manifested by inorganic species such as As(III) and As(V) (Taylor
have been considered the most polluted in the Mediterranean, et al., 2017).
hosting industries that dump large amounts of chemical waste Although we took into account the total concentration in As,
into the sea (European Environment Agency, 2006). Nevertheless, the THQ and HI results were not alarming for the Algerian popula-
the trace elements may be concentrated in aquatic compartments tion. Other studies, such as the study conducted by Kalantzi et al.
other than seawater, particularly in sediments (Tessier, 2012). (2016) who estimated that 10% of the total As is inorganic on sea
According to the EU regulation 2455/2001/EC (Anon, 2001), Pb, bream and sea bass reared in four farms in Greece, their results
Cd and Hg are identified as priority hazardous substances, and in term of THQ related to As were lower than those reported
they are subject to a target of zero discharge into seawater. Nine in this study on the same species. The study by Avigliano et al.
other trace elements presenting health risks were also proposed (2019) who estimated that 20% of the total As is inorganic on
in the report 42 of the Academy of Sciences (1998), among them wild fish. The THQAs estimated in Brazil and Argentina recorded
As (Bourrelier and Berthelin, 1999). values of 1.58 and 0.57 respectively. These findings were superior
to our results, except that the THQAs of farmed tilapia was higher
3.5. Risk evaluation for consumers than THQAs found in Argentina. In addition, our results in terms
of EWI and THQ related to As, Hg, Cd and Pb on farmed tilapia
The mean levels of Pb, Cd, Hg and As measured in the farm were higher than those reported on the same specie reared in
fish samples of this study were used to calculate the estimated two farms in Zambia (Simukoko et al., 2022).
daily intake (EDI), estimated weekly intake (EWI), target hazard The estimated carcinogenic risk (CR) and total carcinogenic
quotient (THQ) and hazard index (HI) values (Table 5). These risk (TCR) related to the exposure to As, Pb and Cd due to the
parameters provide an indication of the risk health due to the consumption of various fish species are also listed in Table 6. The
presence of these substances in the edible part of the fish upon CR for Hg were not calculated in this study due to the unavailabil-
ingestion. ity of data in terms of cancer slope factor because this element is
It should be noted that the annual consumption of fish in not classified as a carcinogen through food consumption.
Algeria estimated at 3.56 kg per year and per Algerian inhabitant The CR values estimated for As (Table 6) exceeded the ac-
in 2016 (Mehouel et al., 2019) was lower than the fish consump- ceptability thresholds (10−4 -10−6 ) in red tilapia (CR(As) ∼
= TCR =
tion rate in Brazil and Argentina: 9.6 and 4.8 kg/person/year, 3.8 × 10−4 ) and in sea bream (CR(As) ∼
= TCR = 2.03 × 10−4 ). These
respectively (Avigliano et al., 2019), while the universal average results may indicate a slightly higher lifetime risk of developing
has increased from 9.0 kg in 1961 to 20.3 kg per capita in cancer by the persons consuming these fish. However, it should
7
B. Khellaf, L. Bouayad, A. Benouadah et al. Regional Studies in Marine Science 62 (2023) 102943

Table 6 consumption was not likely to have harmful non-carcinogenic

Estimation of carcinogenic risks (CR) and total carcinogenic risks (TCR) for an effects on the humans. Nevertheless, a slight risk to developing
Algerian adult (60 kg).
cancer during the lifetime due to total As present in red tilapia
CR TCR
and sea bream was identified. However, it should be noted that
As 2.0 × 10−4 the toxicity of As is mainly manifested by inorganic species that
Sea bream 2.0 × 10−4
Cd 0.44 × 10−6
are found in small amounts in fish compared to its organic form.
Pb 0.34 × 10−8
Nevertheless, the study must be pursuit by carrying out arsenic
As 0.95 × 10−4
Sea bass 0.95 × 10−4 speciation analysis to determine its chemical forms and hence ac-
Cd 0.44 × 10−6
Pb 0.17 × 10−8 curately assess the toxicological and the carcinogenic risks related
As 0.96 × 10−4
to inorganic rather to total As.
Grey tilapia 0.96 × 10−4
Cd 0.44 × 10−6
Pb 0.17 × 10−8 CRediT authorship contribution statement
As 3.8 × 10−4 −4
Red tilapia 3.8 × 10
Cd 0.13 × 10−5 Boubeker Khellaf: Conceptualization, Data curation, Formal
Pb 0.34 × 10−8 analysis, Investigation, Methodology, Supervision, Validation,
Writing – original draft, Writing – review & editing. Leila
Bouayad: Conceptualization, Data curation, Formal analysis,
Funding acquisition, Investigation, Methodology, Project admin-
be noted that these results were obtained taking into account
istration, Resources, Supervision, Validation, Writing – original
the total As levels and not the inorganic species (arsenite (As3+ )
draft, Writing – review & editing. Ali Benouadah: Data cura-
and arsenate (As5+ )), which are the most toxic As species. It is
known that the concentration of As is generally high in fish, with tion, Methodology, Supervision, Validation, Writing – review
a dominance of the organic form arsenobetaine at 95% of total & editing. Taha Mossadek Hamdi: Data curation, Funding
As (Jabeen and Javed, 2011). Nevertheless, Avigliano et al. (2019) acquisition, Methodology, Supervision, Validation, Writing –
estimated that toxic inorganic As ranges between 1% and 20% of review & editing. Rachida Chekri: Data curation, Methodology,
total As. Supervision, Validation, Writing – review & editing. Petru Ji-
The estimated CR of Cd and Pb in all fish species and those taru: Conceptualization, Data curation, Formal analysis, Funding
of As in sea bass and grey tilapia (CR(As) ∼
= TCR ∼= 0.96× 10−4 ) acquisition, Investigation, Methodology, Project administration,
were found to be either within the acceptance threshold or lower Resources, Supervision, Validation, Writing – original draft,
(Table 6). Writing – review & editing.
This indicates a negligible risk of developing cancer during
an individual’s lifetime related to these toxic trace elements. Declaration of competing interest
The carcinogenic risk (CR) via consumption of farmed sea bream
has already been reported in other regions of Algeria (Algiers, The authors declare that they have no known competing finan-
Tizi Ouzou and Ain Temouchent) by Lounas et al. (2021). They cial interests or personal relationships that could have appeared
reported CR values for As (2.55 × 10−4 ), Cd (1.22 × 10−5 ) and to influence the work reported in this paper.
Pb (1.11 × 10−8 ) slightly exceeding the maximum acceptable
threshold only for As; these results are close to those obtained Data availability
in our study for sea bream reared in Bejaia and Chlef (Table 6).
Our results in term of CR related to As, Hg, Cd and Pb on farmed No data was used for the research described in the article.
tilapia were higher than those reported on the same specie reared
in two farms in Zambia (Simukoko et al., 2022). Also, our results Acknowledgements
in term of CR (As) were superior to the results recorded in the
study conducted by Kalantzi et al. (2016). The authors thank the DGRSDT, Algeria for the financial sup-
The results of THQ, HI and CR vary from study to another port and Nathalie Marchond (Anses) for the technical support.
study due to the variable contamination of fish in aquaculture
productions. In our study, where total As was considered, the References
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species. In order to correctly estimate the risks incurred by the Anon, 1996, Regulation (EC) N◦ . 96/23/EC, Council directive 96/23/EC of 29
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4. Conclusion Anon, 2001, Regulation (EC) N◦ . 2455/2001, Decision N◦ 2455/2001/EC of the
European Parliament and of the Council of 20 November 2001, establishing
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8
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