28 Original article

Intestinal Parasitic Infections and Iron Deficiency Anaemia

among School Children in El Khalige Village, Dakhalia, Egypt

Ahmed M. Mahmoud1, Mohieddin Abdul Fattah2, Tarik I. Zaher1,

Sara A. Abdel-Rahman2, Nahed Mosaad1
1
Tropical Medicine Department, Faculty of Medicine, Zagazig University, Egypt
2
Parasitology Department, Faculty of Medicine, Zagazig University, Egypt

Corresponding Author Background and study aim: Intestinal infection 8%. Ancylostoma duodenale
Sara Abdel-Rahman parasitic infection and iron deficiency (9.8%), Hymenolepis nana and Giardia
anaemia are still nowadays, an important lamblia (7.8%), Strongyloides stercoralis
public health problem worldwide, mainly (5.9%) Entamoeba histolytica and
Mobile: 01222268663
in developing countries. The present study Cryptosporidium (3.9%) each and lastly,
aimed to study the relationships between Enterobius vermicularis, T. trichura and
intestinal parasitic infections and iron Schistosoma mansoni with 2 cases each
E mail: deficiency anaemia in school children 6- (1.9%). The parasitic infection was higher
[email protected] 12yrs. in females (52.6%) more than males
m (47.4%) insignificantly. Anemia was mild
Patients and Methods: A cross-sectional
in infected group with Hb (Mean ± SD)
study was performed among (102) school
11.12±1.35 g/dl. 51% of selected children
Key words: children at e EleKalige Village-Dakahlia.
were anaemic. The prevalence of anemia
anaemia, intestinal Children having signs or symptoms related
parasite, school children, was slightly highly non-significant
to other causes of microcytic
Dakhalia, Egypt prevalent among infected children
hypochromic anemia such as thalassemia,
(52.6%) compared with non infected
diabetes mellitus, cancers, receiving
(50%). Iron deficiency anemia (IDA)
chemotherapy or radiotherapy were
represents 88.5% of anemic cases in all
excluded from the study. Examination of
children, 90% of anemic cases in the
blood and stool were done for all children.
infected children and 87.5% of anemic
Results: The prevalence of parasitic cases in non infected children.
infections was 37% of total 102 school
Conclusion: This study showed a high
children. Parasitic infection was
prevalence of parasitic infections among
subdivided into 3 major group;
the children in the rural areas of Egypt
helminthes, protozoa and mixed infection.
and IDA is associated with intestinal
Overall, helminthes infection was more
parasitic infection.
prevalent 22% compared with both
protozoa infection 8% and mixed

INTRODUCTION intestinal parasites affect 56% of the

Parasitic infection is considered a school children [3].
major public health problem in Due to anaemia, growth retardation
children all over the world. In and some developmental and mental
developing countries, low social and problems, parasitic infections are
financial status of the individual leads considered a dangerous health
to the increase in the prevalence of problem [4].
intestinal parasitic infections [1].
In children (0.5-5.0 yrs), hemoglobin
Epidemiological studies in several
level < 11 g/dl and for children (12-15
countries, has shown around 3.5 billion
yrs) hemoglobin level < 12 g/dl is
people affected globally; 300 million
defined as anaemia [5].
of them are ill, 50% of them being
school age children [2]. In Egypt, the

Mahmoud et al., Afro-Egypt J Infect Endem Dis 2017; 7(1):28-36

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 Original article 29

Anemia is a nutritional disorder worldwide Where

especially in children. In various less developed Z = 1.96 for 95% confidence level.
countries in both Asia and Africa, 40% of children p = expected prevalence of satisfaction (0.50).
are anemic. In the early periods of life of d = precision (Margin of error) = 0.05
children, the Deaths reached 726,000 caused by
Inclusion criteria:
iron deficiency, with the highest percentage in
All children aged 6-12years attending EL-Khalige
Africa and Southeast Asia [6].
primary school were included in this study.
Disturbance in the behavior of the children can
Exclusion criteria:
be occurred due to chronic anemia, due to its
Children suspected to have signs or symptoms
hazard effect upon neurological development in
related to other causes of emicrocytic hypochromic
infants and also reduced scholastic performance
anemia such as thalassemia, or chronic debilitating
in children of school age. Rest-less legs syndrome
diseases as malignancy, chronic renal diseases,
is common in those with iron deficiency anemia,
diabetes mellitus, immune diseases were avoided .
with several symptoms include swelling of the
arms or legs, heartburn, vague bruises, vomiting, A full history through a special sheet was
sweating, pallor and blood in stool [7]. obtained by the investigator after interviewing the
mothers of the selected children and receiving a
The main treatment of anemia is by treatment of
questionnaire. The parents of the children
the underlying disease which in most cases leads
completed consent forms, but because many of
to cure or at least improvement of anemia. So,
them refused to give information about their
World Health Organization depends upon regular
income, we could not interpret the
edeworming of school age children in its control
socioeconomic standards and could not estimate
strategy. Regular treatment reduces the intensity
the amount of taken iron in diet.
of infection and gives a protection to those
already infected [8]. Therefore, this study was All selected children were subjected to the
undertaken to investigate the prevalence of following, Full history taking including: Age,
intestinal parasitic infections in school going Gender, Residence, education attainment, socio-
children in El Khalige village despite the various economic status (father or mother occupation,
precautional measures and also, the relationship household income), medical and drug history,
between intestinal parasitic infections and iron complaint (diarrhea, abdominal pain, anorexia,
deficiency anemias. The results will be taken by nausea, vomiting and anal itching) pallor, jaundice,
the school authority to help them to adopt clubbing, organomegally and ascities.
deworming measures.
Collection of stool samples:
The stool was examined macroscopically for the
PATIENTS AND METHODS presence of blood and mucus or adult worm of
Study type: helminths.
This study was a cross sectional prevalence
The stool was examined microscopically also for
study. The study was conducted from January to
ova and cysts of intestinal parasites by direct wet
December 2016. The practical work was done at
ᶱsmear which was done within twelve hours of
the Department of Tropical Medicine and the
the collection of the sample. Direct examination
Medical eParasitology Department of the Faculty
was performed by wet mount technique using
of Medicine, eZagazig University, Zagazig,
saline, iodine and lacto phenol. In case of
Egypt.
negative samples, concentration technique by
Study area formalin acetone sedimentation method was
The current study was performed at El Kalige done [10]. Baermann’s technique was used for
Village lies 10 kilometers away from EL Mansoura demonstration of eStrongyloides larva [11]. In
city, the village supplied with a clean water addition modified acid fast staining was ᶱdone
supply and central sanitary sewage systems. for demonstrating coccidian parasites like
Cryptosporidium, Isospora.
Sample Size:
The calculated sample size of the study was102 Blood Collection and Determination of Iron
children, using the following formula [9]. Status:
Z2 + P* (1-P) Test performance for Hemoglobin concentrations
n= was done using the Cyanmethemglobin method
d2 to form the stable hemoglobin derivative

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30 Original article

cyanmethemoglobin. The Potassium Ferricyanide were described using number and percent.
converts the Hemoglobin to Methemoglobin by Association between categorical variables was
the action of Potasium Cyanide and was standed for tested by Chi-square test. Continuous variables
3 minutes. For conversion of Hemoglobin to were presented as mean ± SD (standard deviation).
Cyanmethemoglobin, before the absorbance is The two groups were compared with Student t-
measured against a reagents blank at a wave length test while more than two groups compared by
of 540 mm using a Spectrophotometer [12]. ANOVA test. The significance's threshold is
fixed at 5% level (p-value). P-values < 0.05 were
Data were analyzed with SPSS version 21. The
considered significant and > 0.05 was
normality of data was first tested with one-sample
insignificant. But < 0.001 was highly significant.
Kolmogorove - eSmirnov test. Qualitative data

Table 1: Comparison between infected and non-infected group regarding to gender, age and anemia
for 102 school children aged 6-12ys
Infected group (n=38) Non-infected Test of sig. p-
Items (37%) (n=64) (63%) value
No % No %
Sex
Male 18 47.4 26 40.6 X2=.442
p=.506
Female 20 52.6 38 59.4
Age/years
Mean ± SD 8.94±2.19 9.18±1.82 t=.596
Min-Max 6.00-12.00 6.00-12.00 p=.553
Anemia
Anemic 20 52.6 32 50.0 X2=.066
Non anemic p=.797
18 47.4 32 50.0
*p value is significant when p ≤ 0.05

Table 2: Comparison between all selected children, infected and non infected children regarding to
Iron deficiency anemia (IDA) and anemia
Non infected Test of sig.
Total selectedchildren (102) Infected child (38)
Items children(64) p-value
NO % NO % NO %
IDA 46 45 18 47.3 28 43.8 X2= .077
Anemia 52 51 20 52.6 32 50 p=.962
*p value is significant when p ≤ 0.05

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 Original article 31

Table 3: Subtypes of parasitic infection and Comparison between them regarding to gender, age and
anemia
Helminthes group Protozoal group Mixed group
Test of sig.
Items (n=22) (22%) (n=8) (8%) (n=8) (8%)
p-value
No % No % No %
Sex
Male 10 45.4 6 75.0 6 75.0 P=.483
Female 12 54.5 2 25.0 2 25.0 P=.002
Age/years
Mean ± SD 8.68±1.75 8.37±1.50 9.12±1.72
p=.691
Min-Max 6.00-12.00 6.00-10.00 6.00-11.00
Anemia
Anemic 12 54.5 4 50.0 4 50.0
Non anemic 10 45.4 4 50.0 4 50.0 P=.041
*p value is significant when p ≤ 0.05

Parasitic infections
17% 17% H.nana
Oxyuris
4% Strongyloid
9%
Trichuris
Ankylostoma
13% Schistosoma
9%
Entameba
4% 4% Cryptospordium

23% Giardia

Fig. 1: Subtypes of parasitic infections and their prevalence among total infected children (46 cases).

Prevalence of IDA
9%
18% 0%
9% H.nana
Oxyuris
Strongyloides
9% 9%
Trichuris
Ankylostoma
Schistosoma

9% Entameba
Cryptosporidium
9% 28% Giardia

Fig (2): Prevalence of IDA in different subtypes of intestinal parasite

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32 Original article

DISCUSSION results were greater than our study (37%)

(Table1) .
In developing countries, intestinal parasitic
infections are one of the most prevalent The explanation for this result is due to improved
infections and also, have highly spread among sanitation which is the only definitive
school aged children [13]. intervention to eliminate parasitic infection [21].
Sanitation in this village includes sewage
Intestinal parasitic infestations are considered as systems since 1995 which helps the prevention
a serious public health problem as it causes iron of contamination of soil and water and prevent
deficiency anaemia, growth retardation in transmission of parasitic diseases. It is also due
children, and other physical and mental health to periodic anti helminthic therapy. Anti
problems [14]. helmintic treatment reduced morbidity by
Bad effect of ᶱintestinal parasitic infestations on decreasing the worm burden. Regular
child iron status was observed by eHesham et al. chemotherapy in high-risk groups can reduce the
[15] who linked intestinal parasitic infestations levels of infection and also, result in immediate
with significant reduced mean haemoglobin improvement in the growth and the health of the
levels in children. children [22]. Anti-helminthic therapy is given
regularly at the start of each school year by
Prevention of iron deficiency anemia can improve Primary Health Care Unit in this village. Health
performance in school, avoid behavioral alterations, education also participates in the reduction of the
and assure better growth. Longitudinal studies prevalence of parasitic infections. Achievement
reported that children who are anemic in of reduction of infection and reinfection can be
einfancy continue to have poor cognition, long- done by encouraging healthy behaviors [23].
lasting adverse effects on hearing and visual
function, poor school achievement and more Our results reported higher parasitic infection in
behavioral problems [16]. females (52.6%) more than males (47.4%) but
with insignificant difference (Table 1), this was
This cross-sectional survey was carried eout at El in agreement with eRayan et al. [8] who found a
Kalige village, Dakahlia governorate to demonstrate higher parasitic infection in females (59%) more
the relationship between intestinal parasitic than in males (41%) in a study up on 195 rural
infections and iron deficiency anemia in a sample school children. On contrast, Pradhan et al. [13]
of children in this rural area in Dakahlia. Data showed different result as the higher parasitic
showed an interaction between parasitic infection was in males (28.2%) compared with
infections, haemoglobin level suggesting that females (20.2%). This is explained by the
parasites affect serum iron level of surveyed presence of other environmental or behavioral
children. factors other than the gender in parasitosis.
This study was performed on 102 children (44 Generally, the high risk of infection in male is
males, 58 females) aged 6- 12 years. The results due to the increased mobility of the male, while
reported that the prevalence of parasitic in female is due to more soil contact during
infections at this rural area was 37% (47.4% for growing vegetables and eating raw vegetable
males, 52.6% for females) (Table 1). This was in during preparing food [17].
accordance with Sah et al. [17] who recorded This study reported that, the prevalence of
that the prevalence of intestinal parasitic anemia in all selected children was 51% (table
infection was e31.5% in a study performed on 147 2).This was in accordance with Al-Mekhlafi et
school children attending the primary school in al. [24] who reported that the prevalence of
Nebal. The prevalence of parasitic infection was anemia was 48.5% in a study was done on 241
reported by Amare et al. [18] was lower than our school children (7-12) years in Pos Betau,
results (22.7%) in their study on school children Malaysia. Our result was higher than the result of
in Gondar, Ethiopia. a survey conducted by Ngui et al. [25] who
The study performed by Hegazy et al. [19] on reported overall prevalence of anemia 26.2% and
500 preschool children aged 2-6years in Oliveira et al. [26] also found lower results than
Damanhur city, revealed that overall prevalence of our result (21.6%). On contrast, Nabakwe et al.
parasitic infections was 51.8%. Also Worku et al. [27] found that anaemia was extremely high
[20] reported parasitic prevalence 55.6%, both (92%) in Kenya, which could be attributed to the

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 Original article 33

increase in the incidence of malaria in the area of both helminthes and protozoa occurred in 6.7%.
the study. Different result was conducted by Pradhan et al.
[13] showing that the protozoal infection was
Our study reported a high prevalence of anemia in
higher than of the helminthes and mixed
infected children(52.6%) compared with non-
infection (17.5%, 4.6%, 1.5%, respectively). Sah
infected (50%)( table 1,2).This was in agreement
et al. [17] also found that, the infection by
with a study conducted by eHesham et al. [15] to
helminthes (13%) and of protozoa (18.5%) from
assess the relationship between intestinal
the total population of the study.
parasites and nutritional status in Thailand
among 343 children, who showed that, the Anemia was highly non-significantly prevalent
incidence of anemia was high among the infected in helminthes infection (54.5%) compared with
children (59%) than non-infected children (42%). both protozoan and mixed infection (50% each)
Hegazy et al. [19] also reported that prevalence (table3). This coincide with Jardim-Botelho et al.
of anemia was higher in infected children [33] who reported increase prevalence of anaemia
(48.6%) compared with non-infected (28.8%). It associated with helminth infection compared
affects 20% to 50% of the world's population and with both protazoal and mixed infection. Also
it spreads among young children [28]. Alemu et al. [34] showed that helminth parasites
was the obvious cause of high anemia prevalence
This study recorded that overall, 51% of children
compared to individuals with protozoa and
were anemic (Hb<11.5 g/dl). The prevalence of
mixed infections (P<0.0001).
IDA was 45%, which accounted for 88.5% of the
anemic cases (Table 2). Globally, these results Among the helminthes, the highest incidence
were in agreement with the data showed by was Ancylostoma duodenale (33.3%), followed
WHO that, in developing countries, the by Hymenolepis nana (26.6%) (Fig. 1). This
prevalence of IDA is up to 48% of school-age coincides with eJardim-Botelho et al. [33] who
children [29]. This was in accordance with Aini reported also a high incidence of Ancylostoma
et al. [30] who reported that overall, 41.5% of duodenale (69.8%) with the majority of
children were anemic and 36.5% had IDA, which individuals harbouring helminthes infections.
accounted for 88% of anemia in these children. This is in contrast with Gyawali et al. [35] and
On the other hand, lower result was conducted Khanal et al. [36] on studies conducted on school
by Ngui et al. [31] on a total 550 school children children of Nepal. These studies have found
aged 7 - 12 years, 26.2% were anemic and 16.9% Ascaris lumbricoides and Trichuris trichiura as
with IDA . the commonest intestinal helminthes in school
children of Nepal.
Our study reported that IDA was slightly highly
non-significant among infected children with Among the intestinal protozoa, Giardia lamblia
47.3% compared with both non infected (43.8%) was the first one, followed by eEntamoeba
and all selected children (45%) (p=0.962) (Table histolytica and cryptosporidium (fig 1). This was
2). This is explained by the fact that blood loss in accordance with Pradhan et al. [13] who found
(mostly occult bleeding), reduced appetite, impaired that Giardia lamblia was the most common
digestion, and malabsorption may be the reasons (58.6%) among protazoal infection. On contrast,
of poor iron status and iron deficiency anemia eRayan et al. [8] reported different result as
that are frequently observed in children suffering Entamoeba histolytica had the highest
from intestinal parasitic infestations [32]. prevalence (25.3%), then Giardia lamblia
(17.9%).
In our study parasitic infection is sub classified
into 3 major group, helminthes, protozoa and In our study, Ancylostoma duodenale was the
mixed infection. Helminthic group (22), Protazoa most common parasites associated with IDA in
group (8) and 8 cases mixed protozoa and anemic infected children 28% (6/22),followed by
helminthes. Overall helminthes infection were Giardia lamblia 18% (4/22) then Hymenolepis
more prevalent 22% (22/102) compared with nana, Strongyloides stercoralis, Trichuris
both protozoa infection 8% (8/102) and mixed trichiura, Schistosoma mansoni, cryptosporidium
infection 8% (8/102) (Table 3). This coincided 9% (2/22) each (fig 2). This coincides with Aini
with Oliveira et al. [26] who reported that the et al. [30] who showed that the depletion of iron
prevalence of infection by helminths was higher stores was mainly caused by Ancylostoma
than that of protozoa (24.1%, 13.4%) in the duodenale infection. It was reported that anaemia
studied children. While mixed coinfection by was more common among intestinal parasitic

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34 Original article

infected especially, giardiasis. This study was Funding: None.

performed to show the association between Conflicts of interest: None.
haemoglobin, serum iron, serum ferritin Ethical approval:Approved.
concentrations in eOrang Asli children living in
endemic areas of intestinal parasitic infections in
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