187

189

Residual Levels of Some Heavy Metals in Fish Flesh and Water from
El-Manzala Lake, Egypt

A. M. Ahmed and M. M. Hussein*

Department of Food Hygiene & Control; Department of Animal Hygiene,
Nutrition & Behavior; Faculty of Vet. Med., Suez Canal University, Egypt

(Received 3/7/1423H.; accepted for publication 6/2/1424H.)

Abstract .The level of four heavy metals cadmium (Cd), Copper (Cu), Lead (Pb) and Mercury (Hg) in flesh of
Mugil cephalus and Tilapia nilotica as well as water samples (90 each) collected from six different sites of El-
Manzala lake, Egypt were evaluated. The results of this study revealed that the mean Cd, Cu, Pb and Hg levels
in the water samples was significantly lower (P < 0.05) than the mean residuals levels in flesh of M. cephalus
and T. nilotica samples. The mean residuals levels of cadmium were 0.60, 0.77 and 0.54 ppm/wet weight for
M. cephalus, T. nilotica and water, respectively. 11.1% of M. cephalus, 18.6% of T. nilotica and 10.4% of water
samples had Cd residuals level exceeding the permissible limit. The mean residual levels of Copper were 1.76,
1.94 and 1.28 ppm/wet weight for M. cephalus, T. nilotica and water, respectively. Cu residuals levels in all M.
cephalus and T. nilotica sample were within the action limit, while 6.4% of water samples exceeded the action
limit. Meanwhile, The mean residuals level of Lead was 1.51, 1.74 and 1.12 ppm/wet weight for M. cephalus,
T. nilotica and water respectively. 20.5% of M. cephalus, 36% of T. nilotica and 28.9% of water samples had
Pb residuals level exceeded the permissible limit. The mean residuals levels of mercury were 0.34, 0.17 and
0.08 ppm/wet weight for M. cephalus, T. nilotica and water, respectively. 5.1% of M. cephalus, 13% of T.
nilotica and 9.2% of water samples had Hg residuals levels exceeding the permissible limit. These findings
recommend that improved water quality control and periodically environmental monitoring are necessary in
El-Manzala lake. In addition, recommendations regarding the acceptable number of fish meals to be consumed
weekly from the health authorities should be taken to fish consumers, especially children and pregnant woman,
to control the accumulative effect of heavy metals.

Introduction

Fish, as human food, are considered as a good source of protein,

polyunsaturated fatty acids (particularly omega-3 fatty acids), calcium, zinc, and iron
[1]. In the future, seafood will even be a more important source of food protein than they
are today and the safety for human consumption of products from aquaculture is of
public health interest [2]. Metal residues problems in the fish flesh are serious, as reflect
by the high metal concentrations recorded in the water and sediments [3]. Recently,
assessment of heavy metals residues in fish flesh has been the purpose of many

187
188 A.M. Ahmed and M.M. Hussein

researches in
 Residual Levels of Some Heavy Metals … 189

different countries: Norway [4]; Malaysia [5]; Greece [6]; Mexico [7]; Turkey [8]; USA
[9] and Egypt [10 and 11].

El-Manzala Lake, Egypt is the largest lake in the Nile Delta, situated between
the Damietta Nile Branch and the Suez Canal. The average total area of the lake is 950
km2 with an average two-meter depth [12]. El-Manzala lake mainly receives the water
from Bahr El-Baqar drain (75%) which carries heavy metals rich sewage from four
governorates, Cairo, Qallyobia, Sharkia and Dakhalia [13]. This lake is considered as
one of the major site of commercial and recreational fisheries in Egypt.

Heavy metal residues in fish flesh and its hazard effects on the health of people
are a matter of great concern to food hygienists. The most non-essential heavy metals of
particular concern to fish and surface water are cadmium (Cd), Copper (Cu), lead (Pb)
and mercury (Hg) which have the way to fish flesh mainly via gills [14 and 15],
subsequently to safe guard the fish consumers, periodical evaluation of heavy metals
residual level in the fish flesh and water from expected polluted area are of major
importance [16 and 17].

The objective of this study was to evaluate cadmium, copper, lead and mercury
contents of Tilapia nilotica, Mugil cephalus fleshes and water from El-Manzala Lake,
Egypt.

Material and Methods

1) Samples collection
Mullet, Mugil cephalus (90); Bolti, Tilapia nilotica (90) and water (90) samples
were collected at quarterly intervals during a period of January, 2001 to January, 2002
from 6 different sites and average depth 1.5m (15 samples from each site) at El-Manzala
Lake, Egypt. The average weight of fish samples were 150g  12, while water sample
was 150mL. The samples were sent to the laboratory for preparation and analysis. All
equipment surfaces and utensils which used in this study were cleaned thoroughly with
detergent, rinsed with water, dried and then rinsed with 2-propanol solution. The samples
were stored at –2C prior to analysis.

2) Mineral analysis
2.1. Cd, Cu and Pb analysis
Cd, Cu and Pb were determined according to AOAC [18]. Fish flesh was minced
and well mixed, then approximately 1.0g was placed in a 150 mL beaker and 10mL
concentrated nitric acid was added. After a short soaking period, 5mL of 60% perchloric
acid was added and the mixture was slowly heated on a hot plate until the conclusion of
growth (approximately 2h). The mixture was then heated until the appearance of dense
white fumes that indicate the nitric acid had evaporated and perchloric acid had reached
its boiling point. The mixture was cooled, 10mL of 25% hydrochloric acid was added
and the solution was transferred to a 100mL volumetric flask that was subsequently
brought to volume with deionized water. Assessment of metals level in prepared samples
190 A.M. Ahmed and M.M. Hussein

were carried out using an atomic absorption spectrophotometer (Model 3100, Perkin-
Elmer, Norwalk, Conn , USA) operated under conditions given by EPA [19]. Instruments
parameters were: flow rate, 1.5mL/min; sample pump tube, 0.48 mL/min; pump speed,
90 to 100 rpm; sample uptake time, 17 to 21s; flush time, 30s; integration time, 10s;
wash time, 30s; background correction, on; and automatic blank subtraction, on. The
lower limits of detection were: Cd, 0.10 ppm; Cu, 0.10 ppm and Pb, 0.50 ppm.

2.2. Hg Analysis
Hg was determined according to APAH. [20]. Analysis of Hg was performed by
placing 1.0 fish flesh in a 150 mL beaker and adding 10mL concentrated nitric acid.
After a short soaking interval, 5 mL concentrated sulfuric acid was added and the
mixture was heated in a microwave digestor (CEM, Matthews, N.C. USA) using preset
instrument setting. The digested mixture was then cooled and transferred to a 100mL
volmetric flask and brought to volume with deionized water. The elemental analysis for
Hg was performed using a PSA atomic fluorescence spectrophotometer (Model, Merlin,
P.S. Analytical LTC, Princeton, N.J., USA) equipped with a PSA random access
autosampler. Instrument setting were: argon carrier (500mL/min; 99.9999% purity
grade); argon sheath (300mL/min); argon dryer gas (3L/min); solution #1=2.5%
stannous chloride (Reagent grade, Fisher Scientific); solution #2=2% nitric acid
(Reagent grade, Fisher Scientific). The lower limit of detection for Hg using this method
was 0.001 ppm.

3) Water analysis
Each sample was put in screw-capped tube and boiled for 1-3 h at 130C till
complete dryness. Ten mL of concentrated nitric acid was added to the sample and
boiled close to dryness then diluted to 20 mL with deionzied water. The solution was
filtrated, transferred to 100 mL volumetric flask, marked and stored refrigerated till
analysis. Cd, Cu and Pb were determined according to APHA [21] method using an
Electothermal atomic absorption spectrophotometer (Model 3100, Perkin-Elmer,
Norwalk, Conn , USA). The lower limits of detection were: Cd, 0.0001 ppm; Cu, 0.10
ppm and Pb, 0.001 ppm. Hg was determined according to APHA [21] method using Cold
vapor atomic absorption spectrophotometer (Model 3100, Perkin-Elmer, Norwalk, Conn,
USA). The lower limit of detection was 0.002 ppm.

4. Statistical analysis
Data were subjected to a one-way analysis of variance using SPSS program
[22] to perform the analysis.

Results and Discussion

The results of this study revealed that the mean Cd, Cu, Pb and Hg residuals level in
water samples was significantly (P < 0.05) lower than the mean residuals level in flesh
of M. cephalus and T. nilotica samples (Table, 1-4). There are direct relationships
between heavy metals residuals level in fish flesh and metals pollution level in domestic
 Residual Levels of Some Heavy Metals … 191

or agricultural wastes in Bahar el-baker and Sharkia governorates, which represent one
of the sources of El-Manzala lake [23]. Opinions differ regard the residuals level of
heavy metals in the water and their relation to the residuals level in fish flesh. Kock and
Hofer [16] reported that even low concentrations of heavy metal in the water may result
in high concentrations in fish flesh. However, other [3] reported that despite high metal
levels in the seawater and sediments, concentrations of Cd and Pb in fish flesh did not
exceed permissible levels. It is observed that flesh of Tilapia nilotica samples had
significantly (P < 0.05) higher levels of Cd, Pb and Hg than the flesh of M. cephalus
samples (Table, 1,3,4). These findings are in agreement with results of Rashed, [11]. He
added that Tilapia nilotica was used as a good bioassay indicator for the water pollution
with heavy metals.

Table 1. Cadmium residues (ppm/wet weight) in flesh of M. cephalus and T. nilotica and water Samples
from El-Manzala lake
LOD* Mean  S.D. Maximum P.L.**
Item
M. cephalus 0.10 0.60a  0.04 1.04 0.50

T. nilotica 0.10 0.77b  0.46 1.93 0.50

Water 0.0001 0.54c  0.67 2.02 0.70

LOD* = Lower Limit of Detection

P.L.** = Permissible Limit (WHO, 1990 & 1993)
Means in the same column bearing different superscript are significantly different (P < 0.05)
n = 90

Table 2. Copper residues (ppm/wet weight) in flesh of M. cephalus and T. nilotica and water samples
from El- Manzala lake
LOD* Mean  S.D. Maximum P.L.**
Item
M. cephalus 0.10 1.76a  0.81 6.29 20.00

T. nilotica 0.10 1.94a  1.11 7.48 20.00

Water 0.10 1.28b  0.92 3.61 2.00

LOD* = Lower Limit of Detection

P.L.** = Permissible Limit (WHO, 1990 & 1993)
Means in the same column bearing different superscript are significantly different (P < 0.05)
n = 90

Table 3. Lead residues (ppm/wet weight) in flesh of M. cephalus and T. nilotica and water samples from
El- Manzala lake
LOD* Mean  S.D. Maximum P.L.**
Item
192 A.M. Ahmed and M.M. Hussein

M. cephalus 0.50 1.51a  0.64 2.34 2.00

T. nilotica 0.50 1.74b  1.01 4.55 2.00

Water 0.001 1.12c  1.06 3.66 0.50

LOD* = Lower Limit of Detection

P.L.** = Permissible Limit (WHO, 1990 & 1993)
Means in the same column bearing different superscript are significantly different (P < 0.05)
n = 90

Table 4. Mercury residues (ppm/wet weight) in flesh of M. cephalus and T. nilotica and water samples
from El- Manzala lake
LOD* Mean  S.D. Maximum P.L.**
Item
M. cephalus 0.001 0.34a  0.02 0.41 0.50

T. nilotica 0.001 0.17b  0.11 0.57 0.50

Water 0.002 0.08c  0.02 0.90 0.005

LOD* = Lower Limit of Detection

P.L.** = Permissible Limit (WHO, 1990 & 1993)
Means in the same column bearing different superscript are significantly different (P < 0.05)
n = 90

Cadmium was detected in 90%, 95.6% and 85.6% of M. cephalus, T. nilotica and
water samples respectively (Table, 5). Mean Cd level was 0.60, 0.77 and 0.54 ppm for
M. cephalus, T. nilotica and water samples respectively (Table, 1). Abou-Arab et al. [10]
reported Cd residues in sardines and mackerel were 0.086 and 0.077 ppm respectively.
Galab [24] detected the levels of 0.053 and 0.008 ppm Cd in the fish flesh and water of
Manzala lake respectively, whereas, Medani and Ahmed [17] reported 1.04 ppm of Cd in
80% of the water samples, such level exceeded the permissible limit for Cd. It is clear
that the Cd level was higher in fish flesh than those obtained by other [10; 17 and 24],
which could be interpreted as the reported metals pollution in the sources of El-Manzala
lake [23]. Gutenmann et al. [25] indicates that a frequently used food safety limit for Cd
in food is 2 ppm. In 1993, Food and Agriculture Organization (FAO) limit for Cd is 0.5
ppm. WHO [26 and 27] indicated that Cd permissible limit is 2.0 ppm for seafood and
0.70 ppm for water. 11.1% of M. cephalus, 18.6% of T. nilotica and 10.4% of water
samples (Table, 1) had Cd residuals level that exceed the permissible limit set by WHO
[26 and 27]. Apparently Cd level in the water samples (Table, 1) was significantly (P <
0.05) lower than that of M. cephalus and T. nilotica. On the other hand, T. nilotica had
significantly (P < 0.05) higher Cd content than M. cephalus. Cd has effects on fish and
their consumers. It acts as a fish stressor, leading to metabolic alterations in Tilapia
nilotica, which increased glucose concentration in white muscle and phosphofructo
kinase in red muscle. Cd significantly decreased total protein concentrations in liver and
 Residual Levels of Some Heavy Metals … 193

white muscle regardless of tissue glycogen levels [29]. On human, ingestion of Cd can
be associated with salivation, choking attacks, persistent vomiting, abdominal pains,
spasms of the anal sphincter, vertigo and loss of consciousness [30].

Table 5. Occurrence of cadmium; copper; lead and mercury in the flesh of M.

cephalus and T. nilotica and water from El-Manzala Lake
Mugil cephalus Tilapia nilotica Water
n = 90 n = 90 n = 90
N.D P. < > P.L. N.D P. < > N.D P. < >
Metal . No. P.L. (%) . No. P.L. P.L. . No. P.L. P.L.
(%). (%) (%) (%). (%) (%) (%) (%). (%) (%) (%)
Cd 9 81 72 9 4 86 70 16 13 77 69 8
(10) (90) (88. (11.1) (4.4) (95. (81. (18. (14. (85. (89. (10.
9) 6) 4) 6) 4) 6) 6) 4)
Cu 0 90 90 0 0 90 90 0 12 78 73 5
(0) (100 (10 (0) (0) (10 (10 (0) (13. (86. (93. (6.4)
) 0) 0) 0) 3) 7) 6)
Pb 2 88 70 18 1 89 57 32 0 90 64 26
(2.2 (97. (79. (20.5) (1.1 (98. (64) (36) (0) (100 (71. (28.
) 8) 5) ) 9) ) 1) 9)
Hg 12 78 74 4 5 85 74 11 14 76 69 7
(13. (86. (94. (5.1) (5.6) (94. (87) (13) (15. (84. (90. (9.2
3) 7) 9) 4) 6) 4) 8) )
N. D. = Non Detected P. No. = Positive No.
< P. L. = Lower Than Permissible Limit > P. L. = Higher Than Permissible Limit

Copper was found in all samples 100% of M. cephalus and T. nilotica samples and
in 86.7% of water samples (Table, 5). Mean Cu level were 1.76, 1.94 and 1.28 ppm for
M. cephalus, T. nilotica and water samples respectively (Table 2). It is seem that the Cu
contents of El-Manzala lake was lower than the past few years, Medani and Ahmed [17]
reported that mean Cu level in water of El-Manzala lake was 3.55 ppm and 82% of the
examined water samples exceeded the permissible limit of WHO. It is may be due to
governmental effort for control the copper based industrial wastes from the way to the
sources of El-Manzala lake before treatment. Abou-Arab et al. [10] indicated that the
1983 FAO Cu limit is 20.0 ppm. WHO [26 and 27] indicated that Cu permissible limit is
20 ppm for fish and 2.00 ppm for water. According to WHO action limit, Cu residual
level in all M. cephalus and T. nilotica samples was within the action limit. On the other
hand, 5 (6.4%) of water samples exceeded the permissible limit of WHO (Table, 5). It is
clear from the obtained results that mean Cu level of water was significantly (P > 0.05)
lower than the mean Cu level in flesh of M. cephalus and T. nilotica (Table, 2).

Cu occurs in foods in many chemical forms and has important role in the
physiological activities of living bodies. Abou-Arab et al. [10] reported Cu residues in
194 A.M. Ahmed and M.M. Hussein

sardines and mackerel of 0.086 and 0.077 ppm respectively. Cu considered as public
health hazard if abnormal high level of Cu is ingested. Cu may cause Mediterranean
anemia, hemochromatosis, liver cirrhosis and Wilson’s disease [31].

Lead was detected in 97.8%, 98.9% and 100% of M. cephalus, T. nilotica and water
samples respectively (Table, 5). The mean Pb level were 1.51, 1.74 and 1.12 ppm for M.
cephalus, T. nilotica and water samples respectively (Table 3). Galab [24] detected the
level of Pb in the fish flesh and water of Manzala lake by 0.70 and 0.352 ppm
respectively, while Medani and Ahmed [17] reported that Pb level in water of El-
Manzala lake was 2.61 ppm and 90% of the water samples exceeded the permissible
limit of WHO.Abou-Arab et al. [10] reported mean Pb residue in whole sardines and
mackerel of 11.1 and 12.6 ppm respectively. Hodson et al. [32] indicated that the
Canadian Pb limit of 10 ppm was discontinued, but that the British limit remains at 2
ppm for fish. Abou-Arab et al. [10] indicated that the FAO limit (1983) is 2.0 ppm.
WHO [26 and 27] indicated that Pb permissible limit is 2.0 ppm for seafood, and 0.50
for water. According to this action limit, 20.5% of M. cephalus, 36% of T. nilotica and
28.9% of water samples had Pb residual levels that exceed the permissible limit (Table,
5). It is observed that the mean Pb level in water was lower (P < 0.05) than the mean Pb
residual level in fish flesh samples (Table, 3). Industrial and agricultural discharges are
the primary sources of Pb pollution in Egypt [33]. Pb is identified as a serious public
health problem particularly for children. The adverse toxic effect caused by Pb on human
was recognized [34]. Neurological defects, renal tubular dysfunction, anemia are the
most characterize of Pb poisoning [35, p. 87].

Mercury was detected in 86.7%, 94.4% and 84.4% of M. cephalus, T. nilotica and
water samples respectively (Table, 5). Mean Hg level were 0.34, 0.17 and 0.08 ppm for
M. cephalus, T. nilotica and water samples respectively (Table 4). Such values were far
less than those reported by Galab [24] for the flesh of Claris lazera and water samples
from El-Manzala lake. It could be interpreted as the different in the feeding behavior of
Claris lazera than other fish as well as the governmental effort for control the sources of
the El-Manzala lake. Food and Drug Administration (FDA) set an action limit for Hg in
seafood of 0.5 ppm in 1969, but this was increased to 1ppm in 1978 [36]. However,
WHO [26 and 27] indicated that Hg permissible limit is 0.50 ppm for seafood and 0.005
ppm for water. Subsequently, 5.1% of M. cephalus, 13% of T. nilotica and 9.2% of water
samples had Hg content that exceed the permissible limit (Table, 5). Hg is readily
absorbed and predominantly (90 to 100%) found in fish tissue bound to protein in the
organic form as methylmercury [19]. Methylmercury is a public health hazard, which
causes neurological impairment and kidney damage [37, p. 437]. In addition, seafood
having concentration level that exceed the limit incriminated in Hg were poisoning
(Minamata disease) in Japan [2]. People eating contaminated fish with Hg subjected to
Neurological disorders and Minamata disease [38]. It is confirmed that the major health
impacts caused by Hg level affect people who are not working directly in Hg related
industry but who have a regular fish diet that has Hg residues above the permissible limit
[39].
 Residual Levels of Some Heavy Metals … 195

Advisory actions should be issued to warn at-risk populations like children and
pregnant or lactating women to avoid over consumption of fish, which hunted from El-
Manzala Lake to prevent the accumulative effects of the heavy metals. Although there
are reduction in the heavy metals contents of El-Manzala lake when compared to the past
few years, more governmental efforts still needed to control environmental pollution and
improve the water quality of El-Manzala Lake.

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[38] Lodenius, M. and Malm, O. “Mercury in the Amazon.” J. Rev. Environ. Contam. Toxicol., 157 (1998),
25-52.
[39] Quiroga, I., Chincheros, J. and Courau, P. “Mercury Distribution in Waters and Fishes of the Upper
Madeira Rivers and Mercury Exposure in Riparian Amazonian Populations.” J. Sci. Total Environ., 260,
1-3 (2000), 73-86.

‫ مصر‬- ‫متبقيات بعض العناصر المعدنية الثقيلة في لحوم الساماك والمياه من بحيرة المنزلة‬
‫بواساطة‬

‫علي معوض أحمد و *محمود حسين‬

،‫ *قسم الصحة والتغذيه وسلوكيات الحيوان‬، ‫قسم الرقابة الصحية علي الغأذية‬
‫ جمهورية مصر العربية‬، ‫ جامعة قناة السويس‬، ‫كلية الطب البيطري‬
 ‫… ‪Residual Levels of Some Heavy Metals‬‬ ‫‪197‬‬

‫)قدم للنشر في ‪ 3/7/1423‬هـ ؛ وقبل للنشر في ‪ 6/2/1424‬هـ(‬

‫ملخص البحث‪ .‬تم في هذه الدراسة تقدير مستوي متبقيات الكككادميوم والنحككاس‬
‫والرصاص والزئبق في تسعين عينة من كل مكن أسكماك البيكاض والبلطكي والميكاه‬
‫من ستة مواقع مختلفة في بحيرة المنزله بجمهورية مصككر العربيككة‪ .‬وقككد تككبين مككن‬
‫الدراسة ان مستوي تركيز كككل مككن الكككادميوم والنحككاس والرصككاص والزئبككق فككي‬
‫عينات المياة كان أقل معنويا عن مستوي التركيز لنفس هككذه العناصككر الثقليككة فككي‬
‫لحوم اسماك البياض والبلطي‪ .‬وقد أوضحت الدراسككة أن متوسككط مسككتوي تركيككز‬
‫الكادميوم كان ‪ 0.60‬و ‪ 0.77‬و ‪ 0.54‬جزء في المليون في لحككوم أسككماك البيككاض‬
‫والبلطي والمياه علي التوالي وكان مستوي الكككادميوم فككي ‪%11.1‬كك و ‪%18.6‬كك و‬
‫‪%10.4‬ك من عينات أسماك البياض والبلطي والمياه علكي التكوالي يزيكد عكن الحكد‬
‫القصي المسموح به من قبل منظمة الصحة العالمية‪ .‬وكان متوسط مستوي تركيز‬
‫النحاس ‪ 1.76‬و ‪ 1.94‬و ‪ 1.28‬جزء في المليون في لحوم أسماك البياض والبلطي‬
‫وعينات المياه علي التوالي وكان مستوي تركيز النحاس لعينات السككماك يقككع فككي‬
‫الحد المسموح به في حين كان هناك عدد ‪%6.4‬كك مككن عينككات الميككاه تحتككوي علككي‬
‫نسبة تركيز أعلي من الحككد القصككي المسككموح بككه‪ .‬كككان متوسككط مسككتوي تركيككز‬
‫الرصككاص ‪ 1.51‬و ‪ 1.74‬و ‪ 1.12‬جككزء فككي المليككون فككي لحككوم أسككماك البيككاض‬
‫والبلطي وعينات المياه علي التوالي وكان مستوي الرصاص فككي ‪%20.5‬كك و ‪%36‬‬
‫و ‪%28.9‬كك من عينات أسماك البياض والبلطي والمياه علي التوالي يزيد عككن الحككد‬
‫القصى المسموح به‪ .‬كان متوسككط مسككتوي تركيككز الزئبككق ‪ 0.34‬و ‪ 0.17‬و ‪0.08‬‬
‫جزء في المليون في لحوم أسماك البياض والبلطككي وعينككات الميككاه علككي التككوالي‬
‫وأما نسبة العينات التي بها متبقيات زئبق تزيد عككن الحككد المسككموح بككه فقككد كككانت‬
‫‪ %5.1‬و ‪ %13‬و ‪ %9.2‬من عينات أسماك البياض والبلطي والمياه علي التوالي‪.‬‬
‫وفي ضوء هذه النتائج أوصت الدراسة علي أهمية المراقبة البيئية الدورية وتحسككين‬
‫جودة المياه في بحيرة المنزلككة‪ .‬وكككذلك أوصككت باتخككاذ إجككراءات أخككري مككن قبككل‬
‫السلطات الصحية بشأن مستهلكي السكماك خصوصكا الطأف ال والنسكاء الحوامكل‬
‫عن ضرورة تحديد الكميككات الككتي يوصككي باسككتهلكها أسككبوعيا مككن اسككماك بحيككرة‬
‫المنزلة لتجنب الثأر التراكمي والخطورة الصحية للعناصر الثقيلة‪.‬‬