The
Distribution of Intestinal Parasites Among Turkish
Children Living in a Rural Area
.........................................................................................................................
Gulnaz Culha1, Cahit Ozer2
1. Asisst. Prof. Dr., Department of Parasitology,
Mustafa Kemal University School of Medicine
2. Asisst. Prof. Dr., Deparment of Family Medicine,
Mustafa Kemal University School of Medicine
Correspondence to:
Asisst. Prof. Dr. Gulnaz CULHA
Mustafa Kemal University School of Medicine,
Deparment of Parasitology
Antakya/HATAY TURKEY
Phone:+90 326 2148661
Fax:+90 326 2148214
e-mail: gulnazculha@yahoo.com
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ABSTRACT
Background:
The aim of this study was to determine
the prevalence of intestinal parasites
in children and to evaluate its association
with socio-economic and environmental
factors.
Methods:
Stool samples and cellulose tape slides
of children between 1-16 years of ages
living in a rural area in Antakya were
investigated. Stool samples were examined
by using the direct wet mount, iodine
method, and sedimentation techniques.
Results:
One hundred and ninenty-nine (51.3%) of
the 388 children included in the study
were male, and the mean age was 6,8±3,4
years (minimum 1, maximum 16). Most of
the families (87.4 %) were from the lowest
socio-economical level and almost all
of the mothers (96.4%) were housewives.
One hundred and fifty-three (39.4%) stool
specimens and 114 (29.4%) cellulose tape
slides were considered as positive. The
most frequently detected parasites were
Enterobius vermicularis (29.4%), Blastocystis
hominis (19.8%), Giardia intestinalis
(16.5%). No statistical significance was
observed in relation to intestinal parasites
detected in tape slides and stool samples
and; gender (p=0,906 and p=0,751), maternal
occupation (p=0,075 and p=0,410), paternal
occupation (p=0,355 and p=0,354), conditions
of the residence [i.e having a garden
(p=0,185 and p=0,733) and stable (p=0,523
and p=0,851), water supply (p=0,675 and
p=0,218), having pets or animals (p=0,856
and p=0,429), having a separate room for
each sibling (p=0,927 and p=0,079)] and,
having symptoms indicating intestinal
parasites (p=0,126 and p=0,611).
Conclusion:
High prevalences of intestinal parasites
in children living in lower socioeconomic
conditions showed that parasitosis remains
a public health problem in Antakya.
Key words:
childhood, intestinal parasites, prevalence,
personal hygiene, socio-economical status.
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Intestinal parasitosis is
still an important public health problem in
underdeveloped or developing countries(1).
Incidence of intestinal parasitosis is affected
by various factors, such as personal hygiene,
dietary habits, education level of the community,
socioeconomic conditions, climate and environmental
factors. Also non-hygienic living conditions
give rise to parasitic infections in children(2).
Intestinal parasites are more frequently encountered
during childhood, since hygenic habits have
not been fully developed(3,4).
The World Health Organization
estimates that more than one billion people
of the world's population is chronically infected
with soil-transmitted helminths and 450 million
are ill as a result of these infections, the
majority being children(5,6). Non-hygienic
living conditions give rise to parasitic infections
in children. These infections are regarded as
serious public health problems, as they cause
iron deficiency anemia, growth retardation in
children and other physical and mental health
problems(7).
Previous studies at various
institutions in Turkey revealed high prevalances
of intestinal parasitic infections among the
following populations: 6-16 years old (10.8%),
12-16 years old (48.0%), 7-15 years old (55.1%),
and 6-12 years old (88.0%)(8,9).
Hatay province is in an underdeveloped
region of southern Turkey. A number of studies
indicate that G. intestinalis and E. vermicularis
were endemic in children(10,11).
But there is no study revealing association
between intestinal parasitic infections and
sociodemographic factors.
In this study we aimed to
investigate intestinal parasitic infections
among children between 1-16 years of ages, and
relation with the sociodemographic, environmental
factors, behavioral habits and complaints in
a small village near to Antakya, where the sanitary
conditions are very poor, and most of the children
studied reside near pools of sewerage.
Setting
This study was performed in rural areas of Antakya,
which is located in southern Anatolia. Antakya
is a big city with a population of 140 thousand
and has a mild climate whereby temperature rises
to about 35-40 C degrees in summer days. Sanitary
conditions are insufficient in large parts of
the city. We randomly selected a village representing
a rural area of the city. We calculated the
sample size as 369 (CI: 95%, predicted prevalence
40%). Six hundred and ten children between 1-16
living in the village comprised the study sample.
Data Collection
The 388 stool samples and cellulose tape slides
of all children between 1-16 years of ages living
in the study area were collected. Educational
material explaining how to supply a stool specimen
and a cellulose tape slide, was given to parents
of each child. Sociodemographic data including
age, gender, residence, parental occupation,
number of siblings, environmental factors, housing
conditions, and quality of water supply were
noted. Complaints of abdominal pain, nausea
/ vomiting, lack of appetite, abdominal distention,
intestinal dismotility, salivation during sleeping,
headache, irritability in sleeping, perianal
itching, teeth grinding and, history of parasitic
infections were also noted. An informational
document about the study, including how to supply
a stool specimen and cellulose tape slide, was
given to every mother.
Laboratory Methods
The cellulose tape slides were prepared in our
laboratory. Two slides were prepared for each
child. All the mothers collected slides for
examination in the early morning prior to bathing
or defecation. On the same day a nurse practitioner
collected the slides for microscopic examination.
All plastic vials were also labeled in our laboratory.
All 388 stool specimens (0.5-1.5 gr) were collected
and transported to the laboratory within the
same day. Stool samples were examined for the
presence of parasites by direct wet mount, Lugol's
iodine solution and formaline-ethyl acetate
sedimentation techniques(6).
Total number of children included in the study
was 388. 199 (51.3%) of them were male, mean
age was 6,8±3,4 years (minimum 1, maximum
16). Three hundred and fifty five (91.5 %) of
the children have at least one sibling. Most
of the parents (87.4 %) reported that they have
very low income.
Almost all of the mothers (96.4%) were housewives.
No statistical significance was observed in
relation to intestinal parasites detected in
tape slides and stool samples and gender (p=0.906
and p=0.751), maternal occupation (p=0.075 and
p=0.410), paternal occupation (p=0.355 and p=0.354),
conditions of the residence [i.e having a garden
(p=0.185 and p=0,733) and stable (p=0.523 and
p=0.851), water supply (p=0.675 and p=0.218),
having pets or animals (p=0.856 and p=0,429),
having a separate room for each sibling (p=0.927
and p=0.079)] and, having symptoms indicating
intestinal parasites (p=0.126 and p=0.611) (Table
1). 153 (39.4%) stool specimens and 114 (29.4%)
cellulose tape slides were positive. The most
frequently observed parasites were Enterobius
vermicularis (29.4%), Blastocystis hominis (19.8%),
and Giardia intestinalis (16.5%). The frequencies
of parasites in the age groups are shown in
Table 2.
| Table
1 Intestinal
parasites, socioeconomic factors, and related
symptoms |
|
Features |
Cellulose tape slide |
Stool specimen |
|
n (%) |
p |
n (%) |
p |
|
Gender |
|
0.906 |
|
0.751 |
|
Male |
59 (29.6) |
|
80 (40.2) |
|
|
Female |
55 (29.1) |
|
73 (38.6) |
|
|
Family Income |
|
0.421 |
|
0.048 |
|
Very low |
102 (30.1) |
|
140 |
|
|
Low |
12 (24.5) |
|
13 |
|
|
Maternal
occupation |
|
0.075 |
|
0.410 |
|
Worker |
1 (7.1) |
|
7 (50.0) |
|
|
Unemployed |
113 |
|
146 (39.0) |
|
|
Paternal
occupation |
|
0.355 |
|
0.354 |
|
Worker |
106 (30.5) |
|
137 (39.4) |
|
|
Food |
4 (23.5) |
|
9 (52.9) |
|
|
Unemployed |
4 (17.4) |
|
7 (30.4) |
|
|
Sleeping outside |
|
0.064 |
|
0.538 |
|
Yes |
6 (54.5) |
|
3 (27.3) |
|
|
No |
108 (28.7) |
|
149 (39.4) |
|
|
House with a garden |
|
0.185 |
|
0.733 |
|
Yes |
95 (28.2) |
|
134 (39.5) |
|
|
No |
19 (37.3) |
|
19 (37.3) |
|
|
Having a separate room |
|
0.927 |
|
0.079 |
|
Yes |
43 (29.7) |
|
49 (33.1) |
|
|
No |
71 (29.2) |
|
104 (42.8) |
|
|
Stable around the residence |
|
0.523 |
|
0.851 |
|
Yes |
80 (31.8) |
|
110 (39.1) |
|
|
No |
34 (28.5) |
|
43 (40.2) |
|
|
Water supply |
|
0.675 |
|
0.218 |
|
Tap |
113 (29.6) |
|
149 (39.0) |
|
|
Well |
1 (16.7) |
|
4 (66.7) |
|
|
Keeping animals (domestic
or pet) |
|
0.856 |
|
0.429 |
|
Yes |
31 (28.7) |
|
46 (42.5) |
|
|
No |
83 (29.6) |
|
107 (38.2) |
|
|
Enuresis |
|
0.344 |
|
0.799 |
|
Yes |
34 (27.4) |
|
48 (38.7) |
|
|
No |
78 (32.2) |
|
97 (40.1) |
|
|
Diarrhea |
|
0.253 |
|
0.377 |
|
Yes |
10 (22.2) |
|
15 (33.3) |
|
|
No |
104 (30.5) |
|
137 (40.2) |
|
|
Symptoms |
|
0.126 |
|
0.611 |
|
Yes |
51 (33.8) |
|
62 (41.1) |
|
|
No |
62 (26.5) |
|
90 (38.5) |
|
| Table
2 Parasites
according to age groups |
|
Parasites |
Infant
n=22 |
Toddler
n=166 |
School Child
n=163 |
Adolescent
n=37 |
Total
n (%) |
|
E. vermicularis |
2 |
37 |
60 |
15 |
114 (29.4) |
|
B.hominis |
6 |
31 |
32 |
8 |
77 (19.8) |
|
G.intestinalis |
1 |
25 |
34 |
4 |
64 (16.5) |
|
E.coli |
|
10 |
9 |
4 |
23 (5.9) |
|
D.dentriticum * |
1 |
3 |
3 |
1 |
8 (2.1) |
|
E.hystolytica |
|
3 |
3 |
1 |
7 (1.8) |
|
H.nana |
|
3 |
3 |
|
6 (1.5) |
|
A.lumbricoides |
|
1 |
1 |
|
2 (0.5) |
|
C.mesnili |
|
|
1 |
|
1 (0.3) |
|
I butchii |
|
|
1 |
|
1 (0.3) |
|
Total |
9 |
76 |
87 |
18 |
189 (47.7) |
|
Stool Specimen positive |
8 |
63 |
70 |
12 |
153 (39.4) |
* False positive
In the present study, we aimed to determine
the prevalence of intestinal parasites in children
between 1-16 living in a rural area of our region,
and to evaluate its association with socio-economic
and environmental factors. It was found that
153 (39.4%) stool specimens and 114 (29.4%)
cellulose tape slides were positive. The most
frequently observed parasites were Enterobius
vermicularis (29.4%), Blastocystis hominis (19.8%),
and Giardia intestinalis (16.5 %). Enterobiasis
occurs worldwide mostly in schoolchildren. E.
vermicularis infection is transmitted by hand
to mouth or person to person directly. In the
study area, children are living in low hygiene
conditions. Lack of enough sanitary knowledge,
behaviour and attitudes such as handwashing,
bathing, food preparation were thought to be
possible causes of auto infection. The higher
prevalance of E. vermicularis could be explained
by the highly infectious nature of parasites.
Non-hygienic living conditions give rise to
parasitic infections in children; socioeconomic
status is the best indicator for prevalence
of such infections. Intestinal parasites are
transmitted either directly through the contamination
of water, soil and food by feces, or indirectly
through poor hygienic and living conditions(12,13).
G. intestinalis was a common intestinal parasite
among our study participants. This protozoa
was the common intestinal parasite living in
the contaminated water, an important risk factor
for the Giardiasis in Hatay region. This may
be a reason for the high prevelance of G. intestinalis
in our study population.
The rate of intestinal parasitosis ranges from
23.8% to 80%, based on the geographical region.
According to the studies from western Anatolia
(Aegean region), prevalance of intestinal parasites
is between 18.5%and 48.7%. This ratio ranges
between 18.4% and 62.9% in different countries(8,9).
It is well known that parasitic diseases are
more common in communities with low socio-economic
conditions(4). These infections deteriorate
the psychological and physical development of
the children. The majority of the positive cases
were from underdeveloped countries and developing
regions where a sewerage system was not present
and using natural spring water for drinking(14-16).
The rate of E. vermicularis mostly depends
on socioeconomic situations, education level,
and personel hygiene and dietery habits. Çulha
has investigated the prevalance of E. vermicularis
in 70 children between 0-7 years of age and
60 boys and 55 girls between 7-17 years in three
different institutions of Hatay Orphanage. Prevalence
of E. Vermicularis was found to be 71.4 % in
0-7 age group, 0.08 % in boys and 0.14 % in
girls between 7-17 age group. This is the only
study which has been done for more than ten
years for the determination of the prevalance
of E.vermicularis in Hatay region(11).
The infection rate was similar in both sexes
(p=0.906 and p=0.751). In infected groups the
mean age of the children was found to be 7.7±3.2
years and in uninfected groups 6.4±3.4
years.
Although there was no association between age
of the children and prevalence of intestinal
parasites detected in stool samples (p=0.769),
E. vermicularis were significantly more prevalent
in elder children.
Infections with intestinal parasites and malnutrition
are common in developing countries and with
the exception of hookworm; intestinal parasites
affect mostly children(17). The accelerated
and unplanned growth of many cities in developing
countries has created, in urban slums and shanty
towns, sanitary conditions which may be as favorable
for transmission of some intestinal parasites
as those found in most poor and remote, rural
areas(1,14,18).
Okyay et al(8) collected 456 stool
specimens from 7-14 year old schoolchildren
from Aydin to identify an association between
socio-demographic and environmental factors,
behavioral habits and also related complaints.
145 students (31.8%) were infected with one
or more intestinal parasites. 29 (6.4%) of the
students were infected with more than one parasite,
26 (5.7%) with two parasites and 3 (0.7%) with
three parasites. The result of this study revealed
that the three most common parasites were E.vermicularis,
G.intestinalis, and E.coli. They also found
that intestinal parasite prevalence was higher
in rural areas, in children with less than primary
school educated mothers, in children who use
hands for washing the anal area after defecation,
and in children who seldom or never use toilet
paper.
Çeliksöz and colleagues reported
that E.vermicularis were positive in 15.6% of
participants with cellophane slides and Taenia
spp eggs were positive in 1.6% of participants
in a study comprising 2,200 school children
in 6 schools in Sivas(19).
Ulukanligil et al(15) investigated
intestinal parasites in a total of 1820 schoool
children in three primary schools between 7-14
years of age. The prevalance of helminthic infections
were 77.1% of the schoolchildren in shanty towns,
53.2% in apartment districts and 53.1% in rural
areas. They found that Ascaris lumbricoides
was the most prevalant species and that was
followed by Trichuris trichura, Hymenolepis
nana and Taenia species in three schools. Sanitation
surveys indicated that the tap water was limited
in shantytown schools, in shantytowns and rural
areas, whereas the school in the apartment area
was well sanitised.
In our study we found that 153 (39.4%) stool
specimens and 114 (29.4%) cellulose tape slides
were positive. The most frequently observed
parasites were Enterobius vermicularis (29.4%),
Blastocystis hominis (19.8%), Giardia intestinalis
(16.5%).
In the present study no relation was observed
between water supply and parasites identified.
Thus we think that parasites were transmitted
either directly through the contamination of
soil and food by faeces, or indirectly poor
living conditions. We investigated the relationship
between sociodemographic data and environmental
factors. No relation was identified between
the presence of intestinal parasites and gender,
maternal and, paternal occupation, housing conditions,
keeping animals, and parasite related symptoms.
Very low family income was found to be a risk
factor for having parasites. As a matter of
fact all the participants were from a low socio-economical
status, but we dichotomised the group as low
and very low income according to their reports.
We have so many limitations. We select a low
socio-economical group of patients from a rural
area of our region. Their living conditions
are almost homogenous. The study group represents
their socio-economical class but homogenity
of the participants may lead low statistical
significance between the risk factor previously
reported. Our study may actually have underestimated
the true prevalence of parasitic infections
because we carried out the study in a relatively
small sample and observed one stool sample and
a tape slide.
To our knowledge the present study is the only
study in Hatay region about intestinal parasites
in children. Thus the present study will provide
information about prevalence of intestinal parasites
in children living in lower socioeconomic conditions,
risk factors and alert health authorities to
the matter. In conclusion, parasitic infections
remain a serious health problem in our region.
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