Journal of King Saud University – Science 34 (2022) 101748

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Original article

Comprehensive environmental assessment of heavy metal

contamination of surface water, sediments and Nile Tilapia in Lake
Nasser, Egypt
Roquia Rizk a,b, Tatjána Juzsakova a, Manel Ben Ali c, Mohamed Ali Rawash d, Endre Domokos a, Amor Hedfi c,
Mohammed Almalki c, Fehmi Boufahja e,⇑, Hesham M Shafik f, Ákos Rédey a
a
Research Centre for Biochemical, Environmental and Chemical Engineering, Sustainability Solutions Research Lab, University of Pannonia, Egyetem str. 10, H-8200 Veszprém,
Hungary
b
Biochemisrty Department, Faculty of Agriculture, Cairo University, Egypt
c
Department of Biology, College of Sciences, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
d
Department of Animal Science, Georgikon Faculty, Hungarian University of Agricultural and Life Science, Keszthely 8630, Hungary
e
University of Carthage, Faculty of Sciences of Bizerte, LR01ES14 Laboratory of Environment Biomonitoring, Coastal Ecology and Ecotoxicology Unit, 7021 Zarzouna, Tunisia
f
Department of Botany, Faculty of Science, Port Said University, Port Said 41522, Egypt

a r t i c l e i n f o a b s t r a c t

Article history: Heavy metals cause deleterious effects on human health and drastically alter the biogeochemical cycles
Received 15 June 2021 within freshwater habitats. The main human activities leading to heavy metal contamination of various
Revised 12 November 2021 aquatic ecosystems comprise the industry, agriculture, urbanization, transport and mining. Lake Nasser is
Accepted 29 November 2021
the main freshwater source in Egypt, usually polluted from upstream human activities from the hydro-
Available online 6 December 2021
graphic basin of the River Nile. The current study surveyed the impact of heavy metals contamination
(i.e., Cd, Zn, Pb and Cu) in water, sediment and two Nile Tilapia (Oreochromis niloticus) fish organs (liver
Keywords:
and muscles) at six sampling sites along Lake Nasser. Additionally, the effects of heavy metals bioaccu-
Heavy metal contamination
Water quality
mulation in the aquatic ecosystem, via water, sediments and fish organs were investigated. The conclu-
Sediment sion is that the water of Lake Nasser is safe for use in terms of human consumption, agricultural
Fish consumption utilization and public sanitation.
Lake Nasser Ó 2021 The Authors. Published by Elsevier B.V. on behalf of King Saud University. This is an open access
article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction worldwide economics, including the one of Egypt (Duan and

Bastiaanssen, 2015).
Lake ecosystems comprise inland water bodies that lack any Lake Nasser was formed in 1964 following the construction of
direct exchange with oceans and share many ecological and bio- the Aswan High Dam in Upper Egypt. Aswan High Dam was con-
geochemical processes that are commonly within the classic structed for several purposes, such as for water storage given ade-
framework definition of limnology (Bhateria and Jain, 2016). quate water input along the year, to overcome floods and for clean
Any alteration in lakes’ environmental status or water quality energy (i.e. hydropower) generation. Lake Nasser is the largest
will inadvertently impact not only the water body per se, but source of freshwater in Egypt accounting for about 95% of the total
equally the human population from adjacent areas (Hedfi et al., Egyptian freshwater budget (Rizk et al., 2020). The lake is about
2013). The human usage of lake waters, such as for drinking water 300 km long and represents the world’s largest embankment
supply, irrigation, fishing and clean-energy generation impact the dam (Abd Ellah, 2020). This lake is very important for the economy
of Egypt, given the absence of the appreciable rainfall regime and
the agriculture dependence entirely on irrigation (Rizk et al.,
⇑ Corresponding author.
2020). Hence, the need for appropriate monitoring techniques to
E-mail address: [email protected] (F. Boufahja).
be implemented in order to check the water quality on a regular
Peer review under responsibility of King Saud University.
basis is of primary importance.
Among various types of pollutants, heavy metals are of major
concern, given not only the wide array of compounds with multi-
Production and hosting by Elsevier faceted effects on lake ecosystems, but equally their various input

https://doi.org/10.1016/j.jksus.2021.101748
1018-3647/Ó 2021 The Authors. Published by Elsevier B.V. on behalf of King Saud University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

pathways, such as the bedrock weathering, hydrodynamic pro- webs. However, most of these studies rather focused on one com-
cesses and atmospheric deposition. The government administra- pound at a time, therefore precluding their synergic interactions
tion of Aswan region restricted severely the use of agricultural within both the lake ecosystem and within fish tissues, despite a
fertilizers, discharge of household and industrial wastewater general acknowledgment of this information gap. Therefore, in
(Ideriah et al., 2012). Therefore, the main source of heavy metals the current study, we tried to fulfill this knowledge gap through
in Lake Nasser comprises mainly the suspended organic matter a holistic investigation of the distribution of these heavy metals
boosted by floodwaters and those generated by improper land in water, sediment, and fish in Lake Nasser, as well as through
use along River Nile hydrographic basin, particularly in Ethiopia assessing their accumulation rates in various fish organs. To under-
(Farhat and Aly, 2018). The sedimentation of suspended organic stand the ecological risk related to heavy metal contamination, we
matter, to which heavy metals are intimately bound, is a compli- calculated the metal pollution index (MPI). The MPI provides com-
cated process, usually increasing significantly in reservoirs. The prehensive information about the metal toxicity in a particular
high sedimentation rates in this lake represent a very serious envi- sample and offers an understanding of the quality of the aquatic
ronmental and economic issue that must be sorted out in a sustain- environment. The current study comprises a continuation of previ-
able manner. The main source of sediments comes from the ous ecotoxicological investigations carried in Lake Nasser (Rizk
highlands, where the erosion processes carry them downstream et al., 2020).
via the river straight into the lake. Most of the deposited sediment
on the bottom of the lake comprises silt, with some traces of sands 2. Materials and methods
(ElKobtan et al., 2016). The heavy metals in aqueous solution do
not always exhibit direct toxic effects on the environment; instead, 2.1. Study area
they tend to (bio) accumulate and to persist in the environment.
Moreover, these compounds are not biodegradable and cause Six sites were carefully selected within the main channel of
detrimental effects on the environment and human health Lake Nasser for water sampling, fish catching and sediment collec-
(Ntakirutimana et al., 2013). Several techniques were developed tion, starting from site Abu-Simbel (1) in the south, followed by
in time to assess the heavy metal effects bound to sediments, such Armina (2), Tushka (3), Korosko (4), Kalabsha (5) and High Dam
as the geological accumulation index (Imam et al., 2020), sediment site (6) situated in the northern part of the lake (Fig. 1).
enrichment agent, contamination factor and degree of
contamination.
2.2. Sampling procedures
Historically, the worldwide fish consumption increased directly
with the interest in its nutritional value, mainly as a source of valu-
2.2.1. Water samples
able proteins. Dietary guidelines in the United Kingdom recom-
Water samples were collected in polyethylene bottles (2 L)
mend the consumption of fish and fish-based products at least
according to Cornell et al. (2016). The samples were acidified with
twice a week to meet the daily requirements of polyunsaturated
nitric acid to prevent organic matter alteration by bacterial activity
fatty acids (Clonan et al., 2012). Given that fish fill upper positions
and transferred in an ice-box to the laboratory of Botany Depart-
within aquatic food webs, the heavy metals can bioaccumulate in
ment, Faculty of Science of Port Said University.
their biomass via food, water and sediments in significant amounts
(Zhao et al., 2012), with direct toxic effects to humans (Castro-
2.2.2. Sediment samples
González and Méndez-Armenta, 2008). The human contamination
Three replicates of sediments were collected with the aid of an
with heavy metals via fish consumption leads sometimes to liver
electronic vibrational core sampler tube (vibracorers), which
and kidney failures and cardiovascular diseases, to name just a
enables sampling efficiently to a depth of eight meters (USGS,
few of the induced detrimental health effects.
2005). Following the packing of sediment samples in polythene
This led to the implementation of numerous international
bags and chilled in an ice box, they were transported to the labo-
screening approaches with the aim of estimating the quality of fish
ratory for further analysis. The samples were dried overnight at
meat, as well as to survey the health of aquatic ecosystems (Meche
105 °C to constant weight for heavy metal analysis.
et al., 2010). Essential metals, such as zinc and copper fulfill impor-
tant physiologic roles; however, their bioaccumulation beyond cer-
tain thresholds becomes highly toxic for humans. Non-essential 2.2.3. Fish samples
metals, such as lead, cadmium and mercury are nonetheless extre- Nile Tilapia (Oreochromis niloticus) is a native fish species to
mely dangerous for both humans and environment (Bawuro et al., Egypt and one of the most common fish used in the Egyptian cui-
2018). These non-essential metals bioaccumulate in any given sine and in fisheries in Aswan governorate. A total of 30 individuals
organism, leading to tissue damages, followed by a wide series of were collected by local fisherman in March 2019.
disorders and significant toxic effects along food webs. Heavy met-
als are non-biodegradable and once released in aquatic habitats, 2.3. Sample preparation
they are absorbed into sediment or accumulate in biota. Usually,
the fish are more prone to accumulate significant amounts of 2.3.1. Water samples
heavy metals from water and food in various tissues (Weber The concentration of heavy metals in water samples was mea-
et al., 2013). Moreover, they absorb significant concentrations of sured according to APHA (2012) standards, with the aid of an
heavy metals even when their amount in aqueous form is below Atomic Absorption Spectrophotometer (AAS).
the detection limit of routine chemical analyses (Imam et al.,
2020). Therefore, various fish organs represent important targets 2.3.2. Sediment samples
for properly assessing the health of the aquatic environment from The digestion of sediment was performed based on USEPA
this perspective. The accumulation rate of heavy metals such as (2010) standards. Fifteen mL of concentrated HNO3, HF and HClO4
lead, zinc, copper and cadmium in several tissues of the iconic fish were mixed into a Teflon beaker with 0.5 g of sediment. The sam-
Nile Tilapia (Oreochromis niloticus) from Lake Nasser was previ- ples were sealed afterwards with a lid and kept for 3 h at room
ously investigated (Rashed, 2001). The main findings of these stud- temperature, then evaporated until they turned into a liquid solu-
ies were that these heavy metals are cycled within the lake tion. Following that, 5 ml of HClO4 was added and vaporized to
ecosystem along with the energy and nutrients flows through food drought. Concentrated HCl (10 ml) was added to samples and
2
R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Fig. 1. Sampling sites and main water supplies/inlets and discharge/outlet points of Nasser Lake.

placed back on a hot plate until the solution became clear. Then, it 2.4. Atomic Absorption spectroscopic measurement
was filtered and supplemented with deionized water up to 100 ml
in a volumetric flask. Heavy metal concentrations were measured with the aid of an
AAS (Model ICE series 3000 AAS) with a GF 5000 graphite furnace
in water, sediment and fish samples. In case of fish samples, the
2.3.3. Fish samples
precision of the analytical procedure was checked by using stan-
Various fish organs were extracted through dissection. Muscle
dard reference materials (dogfish muscle (DORM 4) and liver
and liver organs were removed and their preparation for the mea-
(DOLT 5) Canadian Research Council) in five replicates. The preci-
surement of heavy metals was carried according to Hlavay (1996).
sion of analysis was calculated according to Farkas et al. (2007).
Therefore Cd, Cu, Pb and Zn contents were measured according to
Krishnamurty et al. (1976). First, the samples were dried and then
digested on steam bath at approximately 80 °C for 3 h, followed by 2.5. Metal pollution index (MPI)
the addition of 14 ml of concentrated HNO3 and 7 ml of 30 % H2O2,
in this order. All samples were diluted to 50 ml with ultra-distilled To assess the metal pollution, the metal pollution index (MPI)
water and stored in polyethylene containers at room temperature was used according to (Abdel-Khalek et al., 2016) using the follow-
until further measurements. ing equation:

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

MPI ¼ ðCM 1  CM2  CM_ 3        :  CM n Þ 1/nWhere, CM1 is the 3.2. Assessment of environmental prominence of minerals in sediment
concentration value of first concerned metal, CM2 is the concentra- stores in comparison to SQGs
tion value of second concerned metal, CM3 is the concentration of
third concerned metal and CMn is the concentration of nth metal Table 3 summarizes the measured values of heavy metals in
(mg/kg dry wt) in the tissue sample of a certain samples. sediment and compares them to quality guideline values, which
comprise the minimum critical concentrations, which is repre-
sented by the toxic effect threshold (TET). The concentration of
2.6. Model evaluation
copper varies between 13 and 21.8 mg.g1; high concentrations
were recorded at site 3 (21.8 mg.g1), followed by the site 6
In this study, a comprehensive evaluation method was used to
(21 mg.g1). However, the lowest copper concentration was
evaluate the correlation between the contamination with heavy
recorded at site 1 (13 mg.g1). The concentrations of zinc were high
metals and sample types (i.e., water, sediment, liver and muscles)
in all investigated sampling sites. To determine the state of metal
of investigated items. The main evaluation indexes included the
pollution, the Sediment Quality Guidelines (SQGs) were applied
coefficient of determination (R2), and Pearson correlation coeffi-
as reference. SQGs were derived from the sediment quality pollu-
cient (Corr).
tant concentrations using Chemical and Biological Impact Database
(Jones et al., 1997; USEPA, 1999).
3. Results and discussion However, the usage of SQGs simultaneously with municipal
data requires caution. This is important especially in the risk eval-
Lake Nasser is the largest source of freshwater in Egypt. How- uation of heavy metal loads from sediment samples. The recorded
ever, there are no point pollution sources with heavy metals in values are well correlated with the water flow along a south to
its hydrographic basin. The lake receives heavy metals via anthro- north latitudinal gradient. In conclusion, the sediment from Lake
pogenic activities, such as fishing activities, sewage pollution, fish- Nasser can be considered safe for agriculture activities as well as
ing boats and cruise ships, as well as others which are disposed off for aquatic biota (Imam et al., 2020).
in wastes directly into the Sudanese main stem of River Nile
(Darwish, 2013). The copper, zinc, lead and cadmium were selected
in this study according to the recommendations of Egyptian Water 3.3. Heavy metal concentrations in fish organs
Administration. High concentrations of copper and zinc are
needed, as opposed to lead and cadmium which require low Fish length and net body weight were ranged between 21.5 and
dosages, to cause severe environmental and human health issues. 32.8 cm and 225.5–500.5 g in weight, respectively (Table S1).
Humans are exposed to these heavy metals via consumption of Table 4 shows the concentrations of Cu, Zn, Cd and Pb in fish
water and fish, which bioaccumulate in various tissues, leading muscles compared to the standards of heavy metal levels of the
to both acute and chronic intoxications. European Community (EC, 2005), Food and Agriculture Organiza-
tion (FAO, 2012), FAO/WHO limits (FAO/WHO, 2011), World Health
3.1. Heavy metals concentrations in water Organization (WHO, 1989) and Ministry of Agriculture, Fisheries
and Food of UK (MAFF, 2000). The copper concentrations varied
Table 1 presents the mean concentrations of heavy metals dis- between 1.2 mg.g1 at site 1 to 9.17 mg.g1 at site 3. The zinc con-
solved in water in the six sampling sites of Lake Nasser. Which centrations exhibited the highest concentration (15.70 mg.g1) at
were below the limits imposed by the Egyptian Governmental site 3 and the lowest (8.5 mg.g1) at site 1.
Decree No. 92/2013 (GD, 2013) and by environmental quality stan- The cadmium concentrations recorded the lowest concentra-
dards (EQS, 2008) (Directive 2008/105/EC) of European Union, as tions (0.15 mg.g1) at sites 1 and 2. In site 3 agriculture activities
well as by the aquatic life suitability standard of Canada (CCME, affect water quality, influencing directly water and sediment
2007). dwelling biota.
Sites 3 and 6 exhibited the highest heavy metal concentrations, Table S2 shows the concentrations of cadmium, zinc and lead
whereas the site 1 showed the lowest. The measured values of which are within the certified limits of standard samples. Regard-
heavy metals from the current study were compared to those from ing copper, both standard fish samples (DORM 4 and DOLT 5) were
different countries in Table 2. In comparison with the registered below certified values and within acceptable limits (96.11 % confi-
heavy metal concentrations in various worldwide lakes, it can be dence level). Table S3 presents the concentrations of heavy metals
concluded that the heavy metal concentrations in Lake Nasser in fish liver. The highest heavy metal concentrations (Cu, Zn and
are in fact significantly lower compared to Kenya (Outa et al., Cd) in fish liver were measured at site 6, in the northern part of
2020), China (Jiang et al., 2018), USA (An and Kampbell, 2003), Lake the lake (28.90, 58.10 and 0.50 mg.g1, respectively) whereas the
Constance (Petri, 2006), Lake Geneva (La CIPEL, 2015) and Lake lowest values were recorded at site 1, in the southern part of the
Balaton (Nguyen et al., 2005). lake (Cu: 13.80, Zn: 37.50 and Cd: 0.3 mg.g1 respectively). The low-

Table 1
Concentration of Heavy metals in Lake Nasser and national and international guideline limit values according to various standards.

Heavy metal concentrations (mg.L1) Measuring sites in Lake Nasser limit values, mg/L
1 2 3 4 5 6
a b c
Abu-Simble Armina Tushka Korosko Kalabsha High Dam EG (GD 2013) EQS CCME, 2007
Cu 0.80 2.68 6.700 2.67 1.98 4.70 10 10 4.00
Zn 7.13 7.56 11.80 7.66 9.00 9.11 10 10 50.00
Cd 0.025 0.025 0. 065 0.03 0.03 0.06 1.0 0.08 1.00
Pb 0.01 0.02 0.040 0.03 0.03 0.04 10 1.2 10.00
a
EG (GD 2013) Egyptian Governmental Decree No. 92/2013.
b
EQS, 2008 (Environmental Quality Standards in the Field of Water Policy, Directive 2008/105/EC).
c
CCME, 2007 (Canadian Council of Ministers of the Environment For the Protection of Aquatic Life).

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Table 2
Global overview of mean heavy metals concentrations in water of different water bodies in different countries.

Lake Location /concentration (mg element.L-1) Pb Cd Zn Cu References

Nasser Lake 0.028 0.039 8.70 3.26 current study
Constance Lake (Germany, Switzerland and Austria) 0.050 0.250 1.500 1.100 Petri (2006)
Baikal Lake (Russia) 1.5 7 1–5 1 Shiretorova et al. (2020)
Vemband Lake (India) 3.94 1.63 74.93 7.31 Shylesh Chandran et al. (2019)
Caizi Lake (China) 2.42 0.12 34.33 2.54 Jiang et al. (2018)
LosMolinos Lake (Argentina) 0.07 – 3.75 0.67 Griboff et al. (2018)
Geneva Lake (shared between Switzerland and France) <0.050 0.005 – 0.770 La CIPEL (2015)
Lake Balaton (Hungary) 0.040 0.002 0.970 0.460 Nguyen et al. (2005)
Lake Texoma, Oklahoma–Texas (USA) <15 20 59 24 An and Kampbell (2003)
Lake Victoria (Kenya) 1.054 0.070 144 1.568 Outa et al. (2020)
Lake Victoria (Mwanza and Winam Gulfs) 22–823 0–70 18–50 – Ogoyi et al. (2011)
Tana Lake (Ethiopia) 3–6 30–60 110–160 110–150 Brihanu (2016)
Tanganyika Lake (Tanzania) 7–120 < 10.00 10.00 < 6.00 Chale (2002)

Table 3
Heavy metals concentrations in sediment of Lake Nasser and sediment quality guidelines for selected heavy metals.

Elements concentrations (mg.kg1) Measuring sites/heavy metal concentrations alongside Lake Nasser *SQG
1 2 3 4 5 6
a b c d e
Abu-Simble Armina Tushka Korosko Kalabsha High Dam TEC PEC PEL SEL TEL
Cu 13.00 15.80 21.80 18.00 18.00 21.00 31.0 149 197 110 86
Zn 19.00 25.00 45.00 30.00 38.00 40.00 121 459 315 820 540
Cd 0.165 0.178 0.35 0.27 0.31 0.356 0.99 4.98 3.53 10.0 3.00
Pb 0.95 2.00 3.00 2.00 2.00 3.00 – 128 91 250 170
MPI 2.49 3.44 5.57 4.16 4.54 5.23

*SQG: Sediment quality guideline (Jones et al., 1997; USEPA, 1999).

a
TEC: Threshold effect concentration (MacDonald et al., 2000).
b
PEL: Probable effect level for dry weight (USEPA, 1999).
c
SEL: Severe effect level for dry weight (Persaud et al., 1992).
d
TET: Toxic effect threshold for dry weight (MacDonald et al., 2000).
e
PEC: Probable effect concentration (MacDonald et al., 2000).

est lead concentration was recorded at site 2 (0.1 mg.g1) and the for the future development of agricultural activities in the region
highest at site 3 (2.1 mg.g1). and efficient water management in Egypt.

3.4. Heavy metal distributions among Lake Nasser 3.4.1. Copper

Copper content in water, sediment and both fish muscle and
Heavy metals distribution along the lake offers a better under- liver has represented in Fig. 2. It highlights the lowest copper con-
standing of the level of lake contamination (Hasimuna et al., 2021). centrations with blue, which is the best water quality in terms of
This way, the contamination with heavy metals and where the contamination with this heavy metal, whereas the yellow high-
highest concentrations are to be expected is much better repre- lights indicate high concentrations. The decreasing copper concen-
sented. An overall picture as this may help authorities to draw peo- trations in studied samples are in liver > sediment > muscle >
ple’s attention to the potential risk of heavy metal contamination water. Sediment and liver samples exhibited higher concentrations
(Turan et al., 2020). Such mapping can help with proper implemen- in the lake (13–21.8 and 13.8–28.9 mg.kg1 respectively), support-
tation of preventive measures. However, it is necessary to empha- ing the hypothesis of its bioaccumulation in fish liver and sedi-
size the fact that currently there are no heavy metal contamination ments. Some researchers indicated that elevated levels of heavy
sources in Lake Nasser hydrographic basin, providing a solid basis metals such as Zn and Cu in surface sediments come from mine

Table 4
Heavy metals concentrations in fish muscle of Nile Tilapia (Oreochromis niloticus) of Lake Nasser and comparison of HMs concentration values with standard levels stipulated by
different regulations.

Elements Concentration Measuring sites Standard levels(mg.kg1)

(mg.kg1) a b c d e
1 Abu- 2 3 4 5 6 High EC FAO FAO/WHO, WHO MAFF
Simble Armina Tushka Korosko Kalabsha Dam 2005 2012 2011 1989 2000
Cu 1.20 2.25 9.17 2.25 5.26 6.18 10 30 30 30 20
Zn 8.50 12.78 15.70 13.20 13.65 14.9 – 30 40 100 50
Cd 0.15 0.15 0.23 0.18 0.20 0.24 0.05 0.05 0.5 1 0.2
Pb 0.10 0.20 0.50 0.20 0.20 0.50 0.20 0.5 0.5 2 2
MPI 0.63 0.96 2.02 1.02 1.30 1.82
a
EC, 2005 (European Community, Commission Regulation No. 78/ 2005).
b
FAO, 2012 (Food and Agriculture Organization, Animal Feed Resource Information System, 2012).
c
FAO /WHO limit 2011 (The Joint FAO/WHO Expert Committee on Food Additives, WHO Technical Report Series 960).
d
WHO, 1989 (Heavy Metals Environmental Aspects, 1989 Environment Health Criteria. No. 85).
e
MAFF, 2000 (Ministry of Agriculture, Fisheries and Food, Aquatic Environment Monitoring of UK, Report No. 52, 2000).

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Fig. 2. Copper distributions along the lake in water, sediment, fish muscle and fish liver.

effluents, vehicular emission and commercial and industrial induce potential synaptic damage and several malfunction impli-
sources (Decena et al., 2018). cations in fish, as neurotoxicity. Moreover, exposure to lead has a
negative effect on the immune responses in fish (Lee et al.,
3.4.2. Zinc 2019). Fig. 4 highlights the lead concentrations in water, sediment,
As shows in Fig. 3, zinc concentrations in water, sediment, fish fish muscle and fish liver; the blue color refers to the lowest con-
muscle and fish liver has been illustrated. Blue color highlights the centrations, indicating the best water quality with respect to this
lowest Zn concentration, which indicates the best water quality heavy metal, whereas the yellow color indicates high values. The
with respect to this heavy metal, whereas the yellow indicates high gradient of lead concentrations in samples is in the following order
concentrations. The sequence of Zn concentrations in the samples sediment > liver > muscle > water. The results show that water
were in the order of liver > sediment > muscle > water. The results exhibited the lowest concentrations (Table 1), whereas the sedi-
show that water exhibited the lowest concentration (Table 1), ment and liver samples exhibited the higher concentrations in
whereas sediment and liver samples exhibited the highest values the lake (0.2–3 and 0.9–2.1 mg.kg1 respectively).
(19–45 and 37.5–58.10 mg.kg1 respectively). The results show
that zinc concentrations in the edible tissues of fish were within 3.4.4. Cadmium
the normal variation according to the Canadian fish standard (51. Cadmium induces harmful effect on living cells, their mem-
60 ± 2.80 mg.kg1) (Table S2). brane deterioration and destroys the DNA structure. Such severe
damage result from the displacement of this heavy metals from
3.4.3. Lead its original binding sites (Igiri et al., 2018). Fig. 5 shows cadmium
The accumulation of lead in fish tissues can induce oxidative concentrations in water, sediment, fish muscle and fish liver. The
stress due to production of Reactive Oxygen Species (ROS), which blue color refers to its lowest concentrations, whereas the yellow
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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Fig. 3. Zinc distribution along the lake in water, sediment, fish muscle and fish liver.

indicates the highest values. The gradient of cadmium concentra- The northern part of the lake showed the higher contamination
tions in samples is sediment > liver > muscle > water. The results with heavy metals compared with the southern part, except site 3
showed that water exhibited the lowest concentrations (Table 1), which is highlighted by yellow in Fig. 6. The high recorded values
whereas the sediment and liver samples exhibited the highest con- for all measured heavy metals in this site are perhaps related to the
centrations in the lake (0.3–0.5 and 0.18–0.356 mg.kg1 respec- ongoing agricultural activities in Tushka region, nearby Tushka
tively). Trace concentrations of this metal can negatively affect spillway outlet. The overall water quality of Lake Nasser is below
the metabolism and growth of fish by altering their DNA structure, maximum permissible levels of international standards and speci-
causing dysfunction, disruption of cell membranes, inhibition of fications. Therefore, it can be concluded that the water of Lake Nas-
enzyme activities and oxidative phosphorylation. Equally, it ser is safe for human consumption, agricultural activities and
induces direct toxic effects in humans, through food intake. Cad- animal husbandry. Maintaining the water quality of the lake
mium bioaccumulation was reported to induce nephrotoxicity within these acceptable values represents an important mission
and cause a specific renal failure as well as other associated health for the sustainable development in Egypt, therefore all necessary
issues (Ismail and Rizk, 2016). actions must be implemented for the protection of Lake Nasser.
The evaluated MPIs ranged from 0.63 mg/kg to 6.40 mg/kg with Fig. S1 shows the correlation between the contamination with
the mean of 3.54 mg/kg. The highest MPI value has been reported heavy metals and the types (i.e., water, sediment, liver and mus-
in fish liver samples at sites 6 and 3 (6.40 and 6.23 respectively) cles) of investigated items. The cluster tree shows a high positive
and in sediment was at sites 3 and 6 (5.57 and 5.23 respectively), correlation between zinc and lead concentrations in water and
while the lower MPI value were in fish Muscles at site 1 (0.63 mg/ its accumulation in sediment and fish liver (0.9 and 0.81; 0.94
kg) (Fig. S2). The findings of MPI in the present study were much and 0.93, respectively). The correlation between copper concentra-
lower than that of Rutilus rutilus in Pluszne Lake (Luczynska tions in water and fish muscle (0.88) was higher than that of liver
et al., 2018). samples (0.73). The copper is directed towards cell tissues in

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Fig. 4. Lead distribution along the lake in water, sediment, fish muscle and fish liver.

higher amounts than it does in liver, in order to participate in the lake. One major advantage of the current study, as opposed to
protective role of the antioxidant enzymes. On the other hand, cop- other previous attempts, was the high accuracy of heavy metal
per concentration in water exhibited a high positive correlation measurements by using certified reference materials (CRM) within
with sediment (0.91), given that the latter usually adsorbs the dis- certain ranges.
solved metals. In case of cadmium, the results showed a positive
correlation between its concentration in water and in fish muscle, 4. Conclusions
sediment and fish liver (0.91, 0.82 and 0.73 respectively). Fig. S1
confirms the increased risk for cadmium, because this element Lake Nasser serves as the national water reservoir in Egypt.
does not accumulate in the sediment in a large amount. However, Heavy metal analyses in water, sediment and edible parts of fish
it does accumulate in muscle in greater proportion. That is empha- indicated that water quality is excellent and that the fish are safe
size that Cadmium is not essential for fishes’ metabolic processes, for human consumption. The sediment fulfilled a major role by
and is potentially dangerous at lower concentrations compared to absorbing dissolved metals from the aqueous form. The concentra-
the essential metalloids (Delahaut et al., 2020). Fish organs com- tion of heavy metals in fish muscles and livers meets the specifica-
prise an effective target for predicting the effects of water pollu- tions stipulated by international limits. Therefore, continuous
tants, as a result of the positive correlation between the monitoring and management actions must be carried to support
bioaccumulation of heavy metals in fish tissues and their concen- appropriate decision-making in assessing the health of Lake Nas-
tration in water. Therefore, the current study emphasized the ser. The current study also strongly suggests that legal actions
importance of better understanding of heavy metals bioaccumula- are needed to be implemented by authorities to overcome pollu-
tion in fish organs. Moreover, another aim of this survey was to tion in the adjacent areas of Lake Nasser by reducing future pollu-
provide a comprehensive image of the heavy metal status in this tion levels. However, given that the current survey focused solely

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

Fig. 5. Cadmium distribution along the lake in water, sediment, fish muscle and fish liver.

Fig. 6. General overview on Lake Nasser of mean concentrations of heavy metal distribution in water.

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R. Rizk, Tatjána Juzsakova, M. Ben Ali et al. Journal of King Saud University – Science 34 (2022) 101748

on a single fish species, future studies should widen their scope by Delahaut, V., Rašković, B., Salvado, M.S., Bervoets, L., Blust, R., De Boeck, G., Hu, Y.i.,
2020. Toxicity and bioaccumulation of Cadmium, Copper and Zinc in a direct
including other aquatic organisms, such as other common fish spe-
comparison at equitoxic concentrations in common carp (Cyprinus carpio)
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1371/journal.pone.0220485.t00210.1371/journal.pone.0220485.t00310.1371/
The authors extend their appreciation to the deanship of scien- journal.pone.0220485.t00410.1371/journal.pone.0220485.s001.
Duan, Z., Bastiaanssen, W.G.M., 2015. A new empirical procedure for estimating
tific research for funding this article by Taif University Research intraannual heat storage changes in lakes and reservoirs: Review and analysis of
Supporting Project number (TURSP-2020/225), Taif University, 22 lakes. Remote Sens. Environ. 156, 143–156.
Taif, Saudi Arabia. EC, 2005. European Community, Commission regulation No. 1881/2006. Setting
maximum levels for certain contaminants in foodstuffs (pp. OJ, L364/5). Official
J. Eur. Union.
Declaration of Competing Interest ElKobtan, H., Salem, M., Attia, K., Ahmed, S., Abou El-Magd, I., Tang, X.,
2016. Sedimentological study of Lake Nasser; Egypt, using
integratedimproved techniques of core sampling, X-ray diffraction and
The authors declare that they have no known competing finan-
GISplatform. Cogent. Geosci. 2 (1), 1168069. https://doi.org/10.1080/
cial interests or personal relationships that could have appeared 23312041.2016.1168069.
to influence the work reported in this paper. EQS, 2008. The European Parliament and the Council of the European Union.
Directive 2008/105/EC of the European Parliament and of the Council of 16
December 2008 on Environmental Quality Standards in the Field of Water
Acknowledgements Policy, Amending and Subsequently Repealing Council Directives 82/176/EEC,
83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive
This work was supported by the Tunisian Ministry of the High 2000/60/EC of the European Parliament and of the Council, L 385; Author:
Strasbourg, 2008, 84-97.
Education and Scientific Research. The authors extend their appre- FAO, 2012. Food and Agriculture Organization Animal Feed Resource Information
ciation to the deanship of scientific research for funding this article System (AFRIS) The state of world fisheries and aquaculture, http://www.fao.
by Taif University Research Supporting Project number (TURSP- org/ag/AGA/AGAP/FRG/afris/default.htm 28. FAO (2013) Food and Agriculture
Organization Compilation of legal limits for hazardous substances in fish and
2020/225), Taif University, Taif, Saudi Arabia. fishery products. FAO Fishery Circular No. 464. Food and Agriculture
Organization 2013. pp. 5e100.
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