Impact of parasitic infections on nutritional status and micronutrients in Saudi children

Abstract

Background: Micronutrients deficiency is a great problem that is augmented by infection and poor nutrition. Copper, zinc, and iron are trace elements needed for human growth. Objective: To investigate the impact of parasitic infections on nutritional status and serum copper, iron, and zinc in western Saudi children. Subjects and methods: A case-control study included 110 parasitic infected children and 90 age and sex matched controls. Anthropometric measures were evaluated using specific Saudi Arabian growth charts. Parasites were detected in stool specimens using standard microscopic methods. Atomic Absorption Spectrophotometer was used for detection of serum zinc, iron, and copper. Data were analyzed statistically using SPSS version 20. Results: Parasitic infected children showed a statistically significant low weight for age, weight for height, and BMI. Serum zinc, iron, and copper were significantly lower in parasitic infected children than control. Serum zinc has the most significant positive correlation with weight for age, weight for height and BMI for age (r=0.6, 0.6, 0.7), respectively, followed by iron. Malnutrition existed in 34.5% of children with parasitic infections with a significant impact on serum zinc. Multiple linear regression models showed a highly negative effect of parasitic infection and a less negative effect to underweight on serum zinc, copper and iron levels. Conclusion: Studied serum micronutrients especially zinc and iron and anthropometric indices were significantly lower in parasitically infected children.

Full text

Curr Pediatr Res 2017; 21 (1): 1-7 ISSN 0971-9032
www.currentpediatrics.com
Curr Pediatr Res 2017 Volume 21 Issue 1
1
Introduction
In developing countries, there are many health drawbacks
of which the micronutrient deciencies are considered a
great problem that is augmented by infectious diseases
and poor dieting creating a complex cycle in children,
which is difcult to be controlled, especially in pre-
schoolchildren due to their rapid growth rate and needs
[1-3]. Inappropriate ingestion of micronutrients, as well
as hindering its adequate absorption, which is augmented
by illnesses as infections with various parasites eventually
lead to a shortage of valuable trace elements [4,5].
For adequate development and growth, children need vital
micronutrients, the most common of which are copper,
zinc, and iron. They are needed for maintaining a healthy
child with intact immunity as they participate in a lot
of enzymatic and biological processes [6,7]. WHO has
highlighted upon the prevalence of both zinc, and iron in
developing countries, and has estimated that the highest
incidence is among children [8,9].
Parasitic infections, especially that affecting intestines are
widely distributed all over the world and comprise great
health concerns, especially for children in poor regions
in Latin America, Africa, and Asia [10,11]. The link of
poor nutrition and intestinal helminthes infection has been
well recognized by many researchers who settled several
conclusions regarding age groups at greatest risk and the
effect of such infections on growth parameters especially
Impact of parasitic infections on nutritional status and micronutrients in
Saudi children.
Naglaa M Shalaby1,2, Nehad M Shalaby3, Ashraf O Sayed4
1Department of Parasitology, Faculty of Medicine, Mansoura University, Mansoura, Egypt.
2Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi
Arabia.
3Pediatric Department, Faculty of Medicine, Mansoura University, Mansoura, Egypt.
4Department of pediatrics, Children and Women's University Hospital, Minia University, Egypt.
Background: Micronutrients deciency is a great problem that is augmented by infection
and poor nutrition. Copper, zinc, and iron are trace elements needed for human growth.
Objective: To investigate the impact of parasitic infections on nutritional status and serum
copper, iron, and zinc in western Saudi children.
Subjects and methods: A case-control study included 110 parasitic infected children and
90 age and sex matched controls. Anthropometric measures were evaluated using specic
Saudi Arabian growth charts. Parasites were detected in stool specimens using standard
microscopic methods. Atomic Absorption Spectrophotometer was used for detection of
serum zinc, iron, and copper. Data were analyzed statistically using SPSS version 20.
Results: Parasitic infected children showed a statistically signicant low weight for age,
weight for height, and BMI. Serum zinc, iron, and copper were signicantly lower in parasitic
infected children than control. Serum zinc has the most signicant positive correlation with
weight for age, weight for height and BMI for age (r=0.6, 0.6, 0.7), respectively, followed by
iron. Malnutrition existed in 34.5% of children with parasitic infections with a signicant
impact on serum zinc. Multiple linear regression models showed a highly negative effect of
parasitic infection and a less negative effect to underweight on serum zinc, copper and iron
levels.
Conclusion: Studied serum micronutrients especially zinc and iron and anthropometric
indices were signicantly lower in parasitically infected children.
Abstract
Keywords: Parasites, Zinc, Iron, Copper.
Accepted November 02, 2016

Impact of parasitic infections on nutritional status and micronutrients in Saudi children.
Curr Pediatr Res 2017 Volume 21 Issue 1 2
weight and height [12,13]. The intensity and type of
parasitic infection contribute to its effect on nutrition [14].
To check how adequate nutrition the children have, one
should apply anthropometric indexes which highlight the
nutritional status of children; they are benecial because
they are considered a non-invasive, accurate, convenient
and simple tool to quantify the degree of under-nutrition
or over-nutrition [15].
The targets of this research were to check the inuence
of parasitic infections on nutritional condition and serum
zinc, iron, and copper in preschool and school children in
the Kingdom of Saudi Arabia.
Subjects and Methods
Study Area
This research was performed in the western area of Saudi
Arabia. The nature of its climate is cool in winter, hot in
summer. The annual least and the highest temperature is
(20°C) and (48°C), respectively.
Study Design
A case-control study was undertaken over one year from
August 2014 to September 2015 after obtaining ethical
approval from the Research and Ethic Committee of
Faculty of Applied Medical Sciences, King Abdul-Aziz
University, Jeddah, Saudi Arabia. Also, an informed
consent was taken from the parents of those children
joined the study.
Subject Sampling
This research work was done on 110 children infected
with different parasites known by their positive stool
analysis. Their ages were from 2-15.5 years. The studied
groups were 60 males and 50 females. A control group
was included with 90 parasite free healthy children 52
were males and 38 were females with matched age and
sex. They were enrolled from children, attending different
clinics for a regular check-up. The following inclusion and
exclusion criteria were applied:
Inclusion criteria
• Children of both sexes.
• Ages were from 2 up to 15 years.
• Underweight or normal weights were only
considered.
• No history of vitamins or mineral received by
participant children for 6 months preceding the study.
Exclusion criteria
• Overweight, obesity.
• Underweight due to chronic diseases as congenital
heart problems, endocrine disorders, tumors.
• Children received mineral-vitamin supplements in
the last 6 months. All exclusion criteria were set
to rule out any confounders that could affect our
results.
Both groups were submitted to the following:
A) Nutritional assessment: The children were nearly
naked wearing no shoes while measuring of weight to
the nearest 100 gram using a digital electronic scale and
of height with a portable anthropometric stadiometer
(Seca) to the nearest 0.1 cm. All measurements were
undertaken by the same person and recorded as the mean
of three consecutive readings. Anthropometric indices
were used to estimate the children's nutritional status
as follows: The Body Mass Index (BMI) was calculated
from a child's weight in kilograms and height in meters
(kg/m2) for school-aged children, Weight-for-Height
(WFH) for preschool children, Weight-for-Age (WFA)
and Height-for-Age (HFA).They were plotted on age-
sex specic Saudi growth charts [16]. Underweight,
stunting, and wasting was dened by values below
the 5th centile line for WFA, HFA, and WFH or BMI,
respectively.
B) Detection of parasites in stool: Standard steps were
used in collecting stool specimens in a clean leak proof
stool cups. All data of participating children including
name, age, sex serial number, and date of sample
collection was recorded obviously on the stool cups. Just
after collection, direct wet smear using iodine, saline, and
lacto-phenol cotton blue, was performed. Subsequently,
formalin-ethyl acetate sedimentation was done in the
stool sample and examined by direct wet smear (as
previous) and modied Ziehl-Neelsen stain [17]. The
parasitological examination was performed by two senior
clinical laboratory technicians, independently at the
laboratory of Parasitology, King Abdul-Aziz University
Hospital. According to their parasitological stool results,
parasitically infected children were classied into protozoa
and helminthes types.
C) Biochemical estimation: For estimating serum
micronutrient levels, zinc, iron and copper, blood
specimens were taken by phlebotomists with minimal
veno-stasis after overnight fasting to determine the levels
of micronutrients. Five milliliters of cubital venous blood
samples were collected in sterile tubes and centrifuged for
15 min. Sera were separated and stored in Eppendorfs at
−20°C until analysis was done at the Analytical Chemistry
Unit, Faculty of Applied Medical Sciences, King Abdul-
Aziz University. The concentrations of Zinc, Iron, and
Copper of serum samples were determined by Contr
AA 700 High-Resolution Continuum Source Atomic
Absorption Spectrophotometer [18].
Statistical Analysis
IBM SPSS software package (Statistical Package for Social
Sciences, version 20 for Windows) was used to analyze
data. Continuous variables were presented as median
(interquartile ranges); categorical variables as numbers and
percentages. A one-sample Kolmogorov-Smirnov test was
used to assess whether the data were normally distributed.
The majority of the variables does not follow a normal
distribution (P<0.05), they were non parametric variables,
thus the results are presented as median (interquartile

Naglaa/Nehad/Sayed
Curr Pediatr Res 2017 Volume 21 Issue 1
3
ranges). Categorical data were analyzed for comparison
using chi-square tests or Fisher’s exact test, if chi-squared
test is not suitable when the expected values in any of the
cells of a contingency table are below 5; Continuous data
which not normally distributed were compared using the
Mann-Whitney test. Spearman correlation analysis was
used to assess the correlation between anthropometric
measurements and serum iron, zinc and copper in children
with parasitic infections.
A stepwise multiple linear regression analyses were
calculated to assess the effects of parasitic infections, BMI
for age, weight for age, height for age and age and sex on
the serum levels of zinc, iron and copper.
At 5% level of signicance, P-value less than 0.05 were
considered signicant in all analysis. Cut-off value for,
iron, copper, zinc, was dened at their serum levels of 60
μg/dl, 75 μg/dl, 75 μg/dl, respectively [19].
Results
Table 1 show that a hundred and ten children with parasitic
infections 93 protozoa and 17 helminthes infections and 90
healthy controls were included in the study. Patients with
parasitic infections revealed a statistically signicant low
Weight-for-Age (WFA), Weight-for-Height (WFH) and
Body Mass Index (BMI) p<0.001; based on a cutoff value
(<5th percentile). A statistically signicant low levels of
zinc, iron, and copper, were also identied, compared to
healthy control group p<0.01.
A Box plot distribution illustrated for the median, 25th-
75th interquartile ranges of serum Zinc, Iron, and copper,
62, (54-68); 22 (20-35); 83 (78-88) (µg/dl), respectively,
in children with parasitic infections (Figure 1).
Table 2 shows how the parasitic infections were prevalent
in the 110 studied children. Five types of a single protozoan
infection were identied in 75% of children: Giardia lamblia
was the most prevalent protozoa (n=34), followed by
Entamoeba hisotolytica (n=21), Cryptosporidium parvum
Table 1. Comparison between parasitic infections and
controls participating in the study
Variable
Parasitic
infections
(n=110)
Healthy
Controls
(n=90)
p
Age, years 9 (5.5-12.6) 8 (5-12) 0.5
Gender
Male
Female
60 (55.5%)
50 (45.5%)
52 (58%)
38 (42%) 0.7a
Weight, kg 24 (17.2-
37.9) 26 (18.8-39.1) 0.25
Height, cm 126(108-
146) 126 (104-144) 0.9
BMI for age 15.8 (13.9-
18)
17.9 (16.3-
19.9) 0.1
BMI centile 25(2.9-50) 50 (50-50) 0.001*
Weight for age 10 (2.9-25) 50 (25-50) 0.001*
Height for age 25 (10-50) 25 (25-50) 0.1
Weight for height 50 (8.8-50) 75 (50-90) 0.01*
Serum Zinc,
µmol 62 (54-68) 78 (73-83) 0.001*
Serum Iron, µmol 22 (20-35) 33 (30-35) 0.001*
Serum Copper,
µmol 83 (78-88) 89 (83-93) 0.001*
Parasites
Protozoa
Helminthes
93 (85%)
17 (15%)
--
--
--
--
Notes: Continuous variables are presented as median
(interquartile ranges); Categorical variables are numbers
with percentages
Abbreviations: BMI, Body Mass Index. aChi-square test;
others are Mann-Whitney Test
*P is signicant
Figure 1. Box plot distribution of serum levels of Zinc, Iron and Copper (µg/dl) in children with parasitic infections: upper
horizontal line of box=75th percentile; lower horizontal line of box=25th percentile; horizontal bar within box=median;
square within box=mean; vertical lines out of the box=minimum and maximum

Impact of parasitic infections on nutritional status and micronutrients in Saudi children.
Curr Pediatr Res 2017 Volume 21 Issue 1 4
(n=12), Entamoeba coli (n=9), and Isospora (n=4). Two
protozoan infection was identied in each patient in 12%
of children: Giardia lamblia and Entamoeba hisotolytica
(n=7), Giardia lamblia and Cryptosporidium parvum (n=6).
Two helminthes were identied in 15% of infected children:
Ascaris (n=10) and Hymenolepis nana (n=7).
No statistically signicant difference was noted
between protozoa and helminthes infections, concerning
anthropometric measurements and micronutrients in
serum (zinc, Iron, and copper) (Table 3).
Correlations between serum micronutrients and
anthropometric measurements in children with parasitic
infections are shown in Table 4, serum zinc has the
most signicantly positive correlation with weight for
age, weight for height and BMI for age (r=0.6, 0.6, 0.7;
respectively, p<0.001). While serum iron, has a less
signicant positive correlation with weight for age, weight
for height and BMI for age (r=0.3) for all anthropometric
measures (p<0.003). Serum copper has also a weak but
signicant positive correlation shown only with weight
for age, otherwise, no signicant correlations with other
anthropometric indices.
The most parameters affecting serum zinc negatively in
stepwise multiple linear regression model were parasitic
infection and underweight (B1=-12.95 and B2=-0.18, with
a p<0.001 and 0.01, respectively), while BMI for age had
a signicant positive effect on serum zinc level (B3=2.18,
p<0.001), with an R2 of the model of 0.63.Also, parasitic
infection showed a large negative effect (B1=-3.64, p<0.01)
and a small negative effect of underweight (B2=-0.18,
p<0.03) on serum copper level. In serum copper, parasitic
infection had a negative effect (B1=-3.65, p<0.001), a
weak negative effect to underweight, had on serum copper
(B2=-0.18, p<0.03) with R2 of 0.19.Similarly, parasitic
infection and underweight, had a negative effect on iron
serum level, (B1=-8.9, and B2=-0.13, with a p<0.001 and
0.003, respectively).
Table 5 shows that 34.5% of children with parasitic
Anthropometric
index Serum Iron Serum Zinc Serum
copper
Weight-for-age 0.4
(p<0.001)*
0.6
(p<0.001)*
0.2
(p<0.03)*
Height-for-age 0.3
(p<0.05)* 0.1 (p>0.5) 0.08
(p>0.5)
Weight-for-height 0.3
(p<0.003)*
0.6
(p<0.001)* 0.1 (p>0.3)
BMI for age 0.3
(p<0.007)*
0.7
(p<0.0001)*
0.1 (p>0.
4)
*P is signicant
Table 4. Correlations between anthropometric measurements
and serum iron, zinc and copper in children with parasitic
infections (n=110).
Parasite species No %
Giardia lamblia 34 31
Entamoeba hisotolytica 21 19
Cryptosporidium parvum 12 11
Entamoeba coli 98.2
Isospora 4 3.5
Giardia lamblia & Cryptosporidium
parvum 65.5
Giardia lamblia & Entamoeba
hisotolytica 76.4
Ascaris 10 9
Hymenolepis nana 76.4
Table 2. Prevalence and type of protozoa and helminthes
infections in studying children (n=110)
Table 3. Comparison of protozoa and helminthes infections
regarding some anthropometric measurements, serum
Zinc, Iron, and Copper (n=110)
Variable Protozoa
(n=93)
Helminthes
(n=17) p
Weight for age
≥ 5th centile
<5th centile
(underweight)
51 (69%)
42(31%)
13 (94%)
4 (6%)
X2 =2.8a
0.07
Height for age
≥ 5th centile
<5th centile (stunted)
80 (86%)
13 (14%)
16 (94%)
1 (6%)
X2 =0.7
0.30b
Weight for height
≥ 5th centile
<5th centile (wasted)
68 (77%)
25 (23%)
15 (88%)
2 (12%)
X2=1.8
0.15b
BMI centile
≥ 5th centile
<5th centile (wasted)
59 (69%)
34 (31%)
14 (94%)
3 (6%)
X2=1.1
0.23a
Serum zinc
Low
Normal
52 (56%)
41 (44%)
11 (65%)
6 (35%)
X2=0.45
0.35a
Serum Iron
Low
Normal
88 (95%)
5 (5%)
15 (88%)
2 (12%)
X2=0.08
0.6 b
Serum Copper
Low
Normal
4 (4%)
89 (96%)
1 (6%)
16 (94%)
X2=0.09
0.58b
aChi-square test; bFisher’s test
Malnourished
(n=38)
Nourished
(n=72) p
Serum Zinc
Low
Normal
32 (84%)
6 (16%)
15 (21%)
57 (79%)
0.001*
X2=40.8
Serum Iron
Low
Normal
36 (95%)
2(5%)
69 (96%)
3 (4%)
0.60
X2=0.07
Serum Copper
Low
Normal
3 (8%)
35 (92%)
1 (1%)
71 (99%)
0.40
X2=0.49
*P is signicant
Table 5. Serum micronutrients in infected children
according to their nutritional status (n=110)

Naglaa/Nehad/Sayed
Curr Pediatr Res 2017 Volume 21 Issue 1
5
infections had malnutrition and there was a statistically
signicant difference of serum zinc between the
malnourished and nourished children with parasitic
infections (p<0.001). However, in the two studied groups,
they were not statistically different as regard the serum
iron and copper.
Discussion
Trace elements deciencies and poor nutrition dramatically
hinder adequate human health and socio-economic
development. Both developed and developing countries
are interested in the burden of trace elements deciency
disorders, the highest prevalence is found in Sub-Saharan
Africa and South Asia [20].
In the present study, zinc, iron and copper serum levels
were signicantly lower in parasitic patients compared to
controls. The path physiology is not clearly understood;
however, micronutrients deciencies may be linked to
malabsorption due to mucous affection. Patients with
Giardiasis, in particular, may have intestinal lesions
caused by Giardia trophozoites may impair intestinal zinc
absorption to a great extent. Additionally, infection by
various parasites affects obviously the level of serum zinc
due to its shifting to the liver [21]. Besides, the intestinal
parasites use carbohydrates, lipids, minerals, vitamin and
other food sources of the host in order to gain essential
energy of the life cycle [22].
The results of the present study are comparable with those
reported recently by Arbabi et al. [23] they found that
serum levels of trace elements such as magnesium, zinc,
and copper were reduced with infection by Giardia lamblia
and in enterobiasis. These ndings were supported by
many other researches which claried the poor absorption
of several micronutrients caused by intestinal parasites
[24,25]. Some studies not only showed that patients with
parasitic infections had micronutrients deciencies, but
also their treatment with anti-parasitic medications had
improved their serum levels [26,27]. For example, Olivares
et al. [28] reported that serum copper, zinc, and magnesium
deciencies have signicantly improved three months after
treatment of patients with Enterobius vermicularis and
Giardia lamblia infections. Similarly, another study from
Mexico reported that eradication of Giardia lamblia led to
a marvelous increase in the mean serum zinc levels after
treatment for six months in Mexican schoolchildren [29].
In the present study, serum iron was signicantly lower
in patients with parasitic infections than children of the
healthy group; the observed results are similar to earlier
researches which stated that there was a decient status of
iron in the sera of parasite infected children [30,31].
In contrast to the results of the present study, some other
studies reported a controversial association between
parasitic infections and micronutrients. Results of a study
from Turkey revealed that children with giardiasis had
increased serum levels of copper, whilst zinc and iron
levels were low [26]. Similar ndings were reported by
other researchers [32-35]. Such controversial results of
several studies could be explained by the inability of the
body to store zinc causing a decrease in its level to a great
extent. Conversely, the storage of copper is mainly in its
binding form to ceruloplasmin which is considered one of
the important acute phase reactant that increases in various
infections explaining why serum level of copper increases
during such conditions. In the present study, low serum
copper could be explained also that many children are
underweight or stunted and have inadequate ingesting of
foods with high bioavailability of copper such as meat,
poultry, and sh that is evidently found with poor nutrition.
In this study, serum iron levels were remarkably lower
(p<0.0001) in children having parasitic infections than
the control group. The outcomes of the current study were
also similar to those reported by other studies [26,32].
In the current research, 35% of parasites infected children
were malnourished (wasted and or stunted) versus 65%
nourished. It was demonstrated that serum zinc was the
only micronutrient signicantly lower in malnourished
than the nourished ones (p<0.001). Correlation analysis
between serum micronutrients and the anthropometric
measurements shown positive signicant correlations
of serum iron and zinc with most of anthropometric
measurements (weight-for-age, weight- for-height and
BMI-for-age). On the contrary, serum copper did not
have a signicant correlation with all anthropometric
measurements, except with weight for age (r=0.2). Many
researchers observed the same as well [1,36]. Furthermore,
multiple linear regression model shown a highly negative
effect of parasitic infection (B1=-12.95, B1=-3.64, -8.9,
respectively) and a less negative effect to underweight
(B2=-0.18, -0.13) on serum zinc, copper and iron levels.
Some reasons may be responsible for the low iron
deciency in this study, such as a combination of reduced
intake, decient absorption. It cannot be ignored that the
parasitic infection has a systemic effect and parasites
utilize iron, which is essential for their growth and
multiplication [37]. Iron deciency anemia is estimated
by WHO at approximately half of children whose ages
ranged from 4 to 15 years old in developing countries
[38]. As mentioned before, zinc cannot be stored in the
body so its serum level could be easily dropped, especially
in susceptible pre-schoolchildren because of their higher
growth demands. The zinc deciency prevalence was
estimated by WHO. It was 31%, ranging from 4 to 73%
across various areas all over the world [39]. In the present
study, anthropometric measurements indicated that 84%
of children with malnutrition who are short, and or wasted
have a signicant lower zinc concentration versus 21%
in normally nourished children. Many reporters dened
that short stature and decreased height-for-age was mainly
affected by decient levels of serum zinc as it is considered
one crucial factor in the metabolism of nucleic acids and
hence the protein synthesis, consequently impeding the
whole process of growth in children [4,40].
One of the striking observations of the present study is no
signicant difference of serum iron and copper between
the malnourished and normally nourished groups in

Impact of parasitic infections on nutritional status and micronutrients in Saudi children.
Curr Pediatr Res 2017 Volume 21 Issue 1 6
children with parasitic infections. The explanations for this
result could be related to other factors, not investigated,
such as heavy parasitic infections, small number of study
children or some dietetic factors, for example, decreased
bioavailability of most minerals and increased levels of
phytate in the food due to the consumption of a diet based
mainly on plants [41].
The present study is not without limitations; rst, the
dietary intake of the children have not been monitored,
nor calculated, since the ingestion of low bioavailability
food of most of the micronutrients may contribute to
deciencies of serum zinc and iron especially in children
living in low socioeconomic status, this occurs because
of inhibition of absorption by phytates, polyphenols
and oxalates, which are found in diets mainly based on
plants [41]. The main inhibitor is phytate; it can bind
divalent minerals such as Zn2+ and Fe2+, thus hindering
their body absorption [42]. Another limitation is
the study did not involve developmental milestones
assessment, other studies, recently, have focused on
the relationship between intestinal parasitic infection,
malnutrition, and child development. Investigators from
Jamaica demonstrated improved academic performance
in children who had been dewormed with anthelmintic
drugs [43,44].
Conclusion
Serum micronutrients: zinc, iron and copper and
anthropometric indices were signicantly lower in
children with parasitic infections than controlled
children group. Multiple regression analysis showed
that parasitic infection and underweight had a negative
effect on all micronutrients studied. However, they were
no signicant differences of micronutrients between
protozoa and helminthes infections. Serum zinc andiron
correlated positively with most of the anthropometric
indices; however, serum copper only had a weak positive
correlation with weight for age. Further large studies
are recommended to clarify more the relations between
parasitic infections, micronutrients, development and
cognition in children.
Acknowledgement
Many thanks to laboratory technicians for their valuable
help in carrying out this work.
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Correspondence to:
Nehad MS,
Pediatric Department,
Faculty of Medicine,
Mansoura University,
Mansoura, 35516,
Egypt.
Tel: 00201093988813
E-mail: amahalawy2002@yahoo.com