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Abstract

Background: In children, conjunctivitis is the most widespread ocular surface disease. It is referred to any inflammatory condition of the conjunctiva. Conjunctivitis was the most common associated comorbidities that had an influence on the health of children.
Diyala Journal of Medicine 58 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Conjunctivitis among Rural and Urban School Children in
Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha (MSc)1
Abstract
Background: In children conjunctivitis is the most widespread ocular surface disease. It is
referred to any inflammatory condition of the conjunctiva. Conjunctivitis was the most
common associated comorbidities that had an influence on the health of children.
Objective: To compare the prevalence of allergic and infective conjunctivitis among school
children in the rural & urban Regions of Erbil Governorate / Iraq.
Patients and Methods: A cross-sectional study was performed from the 1st Sep 2018 end
of May 2019 in primary schools in the rural area of Makhmur district and urban districts in
Erbil Governorate .From every suspected case of clinically conjunctivitis, a sample for
bacterial culture was gained by winding a thin cotton micro swab moistened in brain heart
infusion broth over the lower fornix of the conjunctival sac.After culturing on blood,
chocolate, and MacConkey agars, the colonies were specified and identified by using Gram
staining technique, morphological, biochemical & Analytical Profile Index (API)
tests.Allergic conjunctivitis was diagnosed clinically. The Kurdish & Arabic versions of
International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire were used.
MS excel package and SPSS 20 software was used for analysis.
Results: The total numbers of urban and rural School children who had shared in this study
were 1129 and 1093 respectively. The prevalence of infective conjunctivitis in both urban &
rural children was as such: 127(11.2%) & 211(19.3%).The rates of positive culture in both
were: urban 69, 54.3%; rural 143, 67.8 %( p≤ 0.01). Staphylococcus aureus was the most
common pathogen isolated, urban: 37(53.6%) rural: 79(55.2%).Infective conjunctivitis was
distributed significantly in young ages and in male students (p≤0.05).Regarding allergic
conjunctivitis: the prevalence of allergic conjunctivitis were: urban 247(21.9%), rural
81(7.4%).Allergic conjunctivitis was more distributed in older ages and male children, but this
was not-significant .itching was complained by all student.
Conclusion: Infectious conjunctivitis among rural school children is still a major public
health problem. While higher percentage of allergic conjunctivitis among urban school
children was noted.
Keywords:Schoolchildren,Conjunctivitis,Rural,Urban,allergicconjunctivitis,Erbil.
Corresponding Author: Nabaz.shakir@epu.edu.iq
Received: 4th August 2019
Accepted: 17th September 2019
DOI:https://doi.org/10.26505/DJM.18014850804
1 Medical Technical Institute - Erbil Polytechnic University- Erbil - Iraq.
Diyala Journal of Medicine 59 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Introduction
Conjunctivitis refers to any inflammatory
status of the conjunctiva [1]. It is commonly
caused by bacteria or viruses; in addition to ,
chemical irritants, conventional eye
medicament or allergy may play a role in
causing conjunctivitis [2][3] .It has been
estimated that 6 million patients diagnosed
with acute conjunctivitis in the United States
each year, with the cost of treating such cases
alone about $380860 million per year [4].
Conjunctivitis is the most prevalent ocular
surface disease, predominately in children
[2].It may readily disseminate in daycare
centers and school 'classes leading to
deprivation from attendance and
consequently from the educational process
[5].
Numerous US state health departments
order students to be cured with local
antibiotic eye drops preceding the resumption
back to school regardless of the potential &
implicit reason of conjunctivitis [4][6].
Allergic conjunctivitis (AC) is defined as
inflammation of the conjunctiva induced by
allergy [7]. AC comprises a series of events
which starts when the conjunctiva displays an
antigen-specific response with Th-2 upon
contact with an allergen, liberating cytokines
and yielding IgE. IgE then binds to mast cells
which break down; generating histamines,
prostaglandins, platelet-activating factor,
more cytokines and other intermediaries. The
signs and symptoms of AC result from the
activation of inflammatory cells by these
intermediaries [7][8]. For example, when
histamine links to H1 receptors on nerve
endings, it gives rise to itching; while in case
of attachment to H2 receptors located on
blood vessels in the conjunctiva, the
consequence will be vasodilation and
lacrimation [9]. The process could be boosted
and turn into persistent in nature with
cumulative mobilization of neutrophils and
eosinophil’s by mast-cell generated cytokines
and Th-2 cytokines respectively [8] [9].The
present study aimed to compare the
prevalence and some aspects of conjunctivitis
(infective & allergic) in both urban and rural
school' children.
Patients and Methods
Study protocol
This study was a cross sectional study in
which school ’children were screened for
conjunctivitis. It was performed from the
period between September 2018 to May 2019
in primary schools of rural Makhmur district
in Erbil Governorate and urban districts in
Erbil city. Makhmur district is situated 67
kms south- west of Erbil city in Erbil
province. Nine schools had been selected to
achieve such a study including four schools
in the rural Makhmur district and five
schools in the urban Erbil city.
Ethical considerations
This study was approved by the Ethics
Committee of Erbil Medical Technical
Institute, Erbil Polytechnic University, Iraq.
Health Directorate of Erbil, Education
Directorate of Erbil. The parental
endorsements in both written and oral forms
were acquired for their children to be
enrolled in the study. The students were
informed about study’s objectives and they
Diyala Journal of Medicine 60 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
could withdraw thereof if they wished so to
do.
Study population
Inclusion criteria in this study were all
children in the selected schools of aged 7-12
years while exclusion criteria were eye
trauma, recent eye surgery, patients who are
on systemic, local antibiotic and
chemotherapy.
Study design
All children were examined by an
ophthalmologist referred from Rizgary
Hospital. For each child suspicious of having
bacterial conjunctivitis, a sample for bacterial
culture was gained by winding a thin cotton
micro swab moistened in brain heart infusion
broth over the lower fornix of the
conjunctival sac. All swabs were inoculated
on blood, chocolate and MacConkey agars,
the colonies were then specified by
employing Gram staining technique, and
identified by using routine morphological,
biochemical tests and API tests [10] [11].
The diagnosis of bacterial conjunctivitis was
based on: (i) mucous or mucopurulent
discharge in the involved eye; (ii) positive
bacterial culture [11], [12] [13]. Diagnosis of
allergic conjunctivitis was achieved by
noticing symptoms of bilateral itchiness and
either burning sensation, tearing, ropy/clear
mucinous discharge, or photophobia [9][14].
The ocular signs hinged on the presence of at
least two of these: papillae, redness,
brownish limbal hyperpigmentation, visible
limbal spots and chemises [15]. The Kurdish
& Arabic versions of ISAAC (International
Study of Asthma and Allergies in Childhood
[7][8] questionnaire were prepared and
distributed and collected through each
daycare center. Parents filled out the ISAAC
questionnaire at home and returned it within
few days. For each case of infectious
conjunctivitis, a questionnaire was applied to
obtain demographic information regarding
age, sex, duration of infection, features of the
infection like pus, visual acuity, redness,
irritation and history of any drug, or previous
eye operation.
Statistical analysis
The data analysis was performed using
descriptive statistics, including frequency,
and frequency percentage. Comparisons were
made using Chi x2 test using standard
equations. The results were reported with
p≤0.05 or p≤0.01 as the accepted level of
significance accordingly.
Results
The total numbers of urban and rural
primary school pupils who had included in
this study were1129 and1093 respectively.
Out ofthe1129 and1093 examined, 127
(11.2%) and 211(19.3%) had features of
infective conjunctivitis while 247(21.9 %)
and 81(7.4%) had signs and symptoms of
allergic conjunctivitis Table(1). It is noted
here that allergic conjunctivitis was more
prevalent in urban school children while the
percent of infective conjunctivitis was higher
in rural school children.
Diyala Journal of Medicine 61 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Table (1): Distribution of infective& allergic conjunctivitis in urban and rural school children
Diagnosis
Urban
N %
Rural
N %
Infective conjunctivitis
127 11.2
211 19.3
Allergic conjunctivitis
247 21.9
81 7.4
No conjunctivitis
755 66.9
801 73.3
Total
1129 100
1093 100
In this study,all conjunctival swabs from
children who had features of conjunctivitis
were subjected for culturing on Blood agar
base, MacConky agar and Chocolate agar.
The results of culturing of both urban and
rural samples were as such illustrated in
Table (2).
Sixty nine (54.3% ) of the urban isolate
yield positive culture growth while regarding
the samples from rural children 143(67.8%)
swabs showed positive culture results . In
both urban and rural, Staphylococcus aureus
was the most common isolated bacteria. The
isolated bacterial species from urban swabs
were as such: (37, 53.6%) isolates of
Staphylococcus aureus,(17, 24.6%) isolates
of Staphylococcus epidermidis, (12, 17.4%)
isolates of Psuedomonous aeruginosa and
(3,4.4%) isolates of Haemophilus influenza.
While the isolated bacterial species from
rural samples were as such: (79,55.2%)
isolates of Staphylococcus aureus,
(41,28.7%) isolates of Staphylococcus
epidermidis , (23,16.1%) isolates of
Psuedomonous aeruginosa and (0,0%)
isolates of Haemophilus influenza .The
differences in the distribution of positive and
negative culture results in both urban and
rural samples were highly significant (p≤
0.01).
Table (2): Distribution of positive, negative results and bacterial isolates in urban and rural school
children
Results
Urban
N %
Rural
N %
Positive
69 54.3
143 67.8
Negative
58 45.7
68 32.2
Total
127 100
211 100
Statistical analysis
df=1 chi square value= 6.126 Highly significant(p≤ 0.01)
Bacterial isolates
Staphylococcus aureus
37 53.6
79 55.2
Staphylococcus epidermidis
17 24.6
41 28.7
Psuedomonous aeruginosa
12 17.4
23 16.1
Haemophilus influenzae
3 4.4
0 0
Total
69 100
143 100
Diyala Journal of Medicine 62 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Tables (3) & (4) illustrate the distribution
of infective conjunctivitis according to age
ranges and gender in both urban and rural
school children. The highest frequency of
infection was in the age range of 6-8 years of
both urban and rural children (47, 37%), (69,
32.7%) respectively. The highest frequency
of infection was in the males of both urban
and rural children (83, 65.3%), (112, 53.1%)
respectively. The differences in the
distribution of infective conjunctivitis in
these different age ranges and in both genders
were significant (p≤0.05).
Table (3): Distribution of infective conjunctivitis according to the age range in urban and rural school
children
Age range (years)
Urban
N %
Rural
N %
Total
6- 8*
47 37
69 32.7
116
>8-10
40 31.5
53 25.1
93
>10-12
29 22.8
47 22.3
76
>12-14
11 8.7
42 19.9
53
Total
127 100
211 100
338
df=3 chi square value =8.0034 *significant (p≤ 0.05)
Table (4): Distribution of infective conjunctivitis according to the gender in urban and rural school
children
Gender
Urban
N %
Rural
N %
Total
Male*
83 65.3
112 53.1
195
Female
44 34.7
99 46.9
143
Total
127 100
211 100
338
df=1 chi square value =4.893 *significant (p≤ 0.05)
Tables (5) & (6) illustrate the distribution
of allergic conjunctivitis in both age ranges
& gender of pupils in the study. The highest
percent was in the age group of ˃ 12-14
years (81, 32.8 %) in urban while it was (34,
42%) in rural. The highest percent of
children afflicted with allergic conjunctivitis
were in males as followings urban (136 ,
65.3% ) and rural ( 45, 53.1%) In spite of the
increasing percent of allergic conjunctivitis
with increasing ages and in male children in
both urban and rural cases, It is noted here
that the differences in the distribution of
allergic conjunctivitis in both different age
ranges and gender were not significant (p
0.05) .In Table (7), the frequency of the
major symptoms and signs of allergic
conjunctivitis is illustrated; students suffered
multiple symptoms. Itching was the most
frequent symptom which was complained by
all urban and rural school children.
Diyala Journal of Medicine 63 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Table (5): Distribution of allergic conjunctivitis according to the age range in urban and rural school
children
Age range (years)
Urban
N %
Rural
N %
Total
6- 8
37 15
7 8.6
44
>8-10
59 23.9
11 13.6
70
>10-12
70 28.3
29 35.8
99
>12-14
81 32.8
34 42
115
Total
247 100
81 100
328
df=3 chi square value =7.4545 Non-significant (p 0.05)
Table (6): Distribution of allergic conjunctivitis according to the gender in urban and rural school
children
Gender
Urban
N %
Rural
N %
Total
Male
136 65.3
45 53.1
181
Female
111 34.7
36 46.9
147
Total
247 100
81 100
338
df=1 chi square value =0.006 Non-significant (p 0.05)
Table (7): Frequency of major features of Allergic Conjunctivitis in urban and rural school children
Features
Urban
Number %
Rural
Number %
Itching
247 100
81 100
Redness
185 74.9
64 79
Grittiness
120 48.6
43 53.1
Tearing
110 44.5
30 37
Clear Mucinous Discharge
97 39.3
21 25.9
Discussion
To our knowledge, this is the first
comparative study on the prevalence of
conjunctivitis among urban and rural
childhood students in Erbil. Bacterial
conjunctivitis is the most widespread pattern
of infective conjunctivitis [2].Such
conjunctivitis manifests when the pathogenic
bacteria vanquish conjunctival defenses
leading to inflammation. Microbial
populations in the normal flora of the
conjunctiva can shelter the eye by restraining
colonization of pathogenic organisms [16].
Considerable studies displayed that metabolic
outcomes of the normal flora can curb the
growth of pathogens [11] [17] [18].
Diyala Journal of Medicine 64 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Bacterial conjunctivitis can be contracted
directly from infected persons or can result
from abnormal proliferation and generation
of the local conjunctival flora [2].
Contaminated fingers, oculogenital spread,
and contaminated fomites are wide spread
ways of transporting [13]. In addition, special
conditions such as compromised tear
production, perturbation of the natural
epithelial hurdle, abnormality of adnexal
structures, trauma, and immunosuppressed
situations are more susceptible to bacterial
conjunctivitis [17] [18].
Rural school children had a higher rate of
infective conjunctivitis (19.3%) with higher
rate of bacterial isolation (67.8%). This ratio
of 19.3% was higher than that was marked by
Ohnsman on their study on American
children in which the rates were (13.5%)
[16]. The present result was less than from
studies achieved by Liang Q, Lu X,et al.
;Yang B, Li X, et al. in China and Mohager,
et al. in Sudan in which the rates were 34%,
22.6% and 59.2% respectively[17] [18] [10].
The high ratio of positive bacterial growth
(67.8%) of rural swabs conclude that
bacterial conjunctivitis is still the most
common cause of infective conjunctivitis
.This result is in accordance with that of [20]
[21] . The causes of the absence of bacterial
growth in clinically diagnosed cases might be
bacterial causes which are not identified by
the conventional laboratory parameters or a
nonbacterial causes like viruses and fungi
[11].
The ration of bacterial conjunctivitis in
children living the rural district of Makhmur
was higher than that of children living in
urban Erbil. This is probably linked with
poor hygienic practices. Considerable studies
stated that recurrence, allocation and reasons
of acute bacterial conjunctivitis are affected
by age; climate, social conditions in addition
to other factors manipulating the propagation
of microbiologic agents in patients with
conjunctivitis include geographic location,
season, age and associated synchronous
maladies [3][11][17] [18][19]. The present
study illustrated that Gram positive cocci is
the most common isolates. The higher ratio
of Staphylococci isolation in this study is in
harmony with the study by Rahama et al. in
Iraq which determined that Staphylococcus
aureus showed the highest percentage
(20.5%) of isolation [19]. Another study by
Al-Dorri which was achieved in Tikrit, Iraq
concluded that Staphylococcus aureus had
the highest percentage of occurrence (42%),
followed by Streptococcus pneumoniae
(27%) and Staphylococcus epidermidis
(12%) [20].In conformity with the current
results, a study in Egypt by Hashish et al. had
concluded Staphylococcus aureus was the
most commonly isolated organism either
separately or in the course of a mixed
infection (24.65%) followed by
Streptococcus pneumoniae in(21.83%),
Pseudomonas aeruginosa in (12.68%) [21].
The higher ratio of Staphylococci isolation
in this study is in harmony with the study by
Cao et al. in China which determined that
Staphylococci are the most recurrent
microorganisms giving rise to infectious
conjunctivitis in children, followed by
Diyala Journal of Medicine 65 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
Coryneform spp. bacteria and Enterobacteria
spp. [22].Other studies in Iraq by Al-Rubaey
et al.; Alash SA. showed that Haemophilus
influenzae & Pseudomonas aeruginosa
represented the highest among the isolates
respectively [23] [24].
Many studies reported that the frequency,
etiology, distribution and causes of acute
bacterial conjunctivitis are influenced by age;
climate, social conditions and coexisting
epidemic diseases in addition to other factors
influencing the prevalence of microbiologic
agents in patients with conjunctivitis include
geographic location, season, age and
associated concurrent illness [2] [11] [17].
The present study clarified that infective
conjunctivitis affects younger ages and male
students significantly. These results are in
concert with that of Okesola et al.; Mohager
et al.; Tesfaye et al.; Salman MS. where a
higher prevalence of infective conjunctivitis
was present in the young age group with
male predominance [3] [10] [12] [25].The
reason for this observance may be related to
the high contagiosity of infective
conjunctivitis and its affiliation with close
contact between patients, a situation common
in kindergartens, schools and childcare [11]
[19]. Additionally boys are more exposed to
environmental contaminants as they spend
most of their time outdoors; in contrast to
girls they stay indoors due to cultural, social
as well as religious reasons [17] [21] [25].
Regarding allergic conjunctivitis, the
prevalence of allergic conjunctivitis in urban
and rural children samples were 21.9%, 7.4%
respectively. The present study, to the best of
our knowledge, is the first to report on the
significant burden of allergic conjunctivitis in
school children in the city of Erbil. The city
is facing a numerous environmental
challenges due to the rapid urbanization. The
burdens of allergic conjunctivitis and related
allergic diseases have been increasing
worldwide. It is speculated that
environmental factors are essentially
responsible for this increase [8] [26] [27]. As
a result of the environmental degradation,
children especially in urban cities in
developing countries are facing a range of
new dilemma of allergic diseases including
allergic conjunctivitis [28].
Allergic conjunctivitis is a condition
seldom associated with visual loss; however,
it is important from the perspective of quality
of life [8].
Estimates of prevalence of this allergic
condition have been published previously in
various studies. A study conducted among
1280 primary-school children in the Bushehr
region of Iran found that 12.5% of the
children had allergic conjunctivitis [28]. A
survey of a sample of 38, 955 children in
Korea showed a prevalence of about 10% for
rhino- conjunctivitis [29].Several studies
have consistently related the increase in
allergic conditions to urbanization. Because
of environmental deteriorations, especially in
urban cities within developing countries, air
pollutants like urban dust contain polycyclic
aromatic hydrocarbons which have been
embroiled in allergic conjunctivitis [7] [27]
[29]. For example, in Mongolia, a
population-based survey revealed a striking
Diyala Journal of Medicine 66 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
association between the prevalence of
allergic conjunctivitis and the extent/degree
of urbanization, the prevalence was 9.3% in
villages, 12.9% in rural towns and 18.4% in
the cities [30]. A small hospital-based case-
control study conducted in Nigeria identified
living close to major commercial centers as a
risk factor for chronic allergic conjunctivitis
as it increases the risk of exposure to smoke
and other air pollutants [14].
The present study showed an increasing
older age prevalence of allergic
conjunctivitis although the differences in the
distribution between different age groups was
non-significant .Other studies had found a
strong association between age and
prevalence of allergic conjunctivitis as the
older age had more prevalence [27] [28] [29].
The high prevalence in the present study in
older child strengthens the argument that an
increasing duration of exposure increases the
risk of this disease in addition [27] [29].
When examined for gender, a male
predilection was seen in this study. However,
it was statistically not significant. The
association between gender and allergic
conjunctivitis remains non- conclusive [27]
[28].
The relatively high disease burden among
boys in our study is consistent with the
findings of other studies and it could be
because boys are more exposed to
environmental pollutants as they spend most
of their time outdoors; by contrast girls by
and large stay indoors due to cultural, social
as well as religious reasons [27] [29] [30]
[31] [32]. The current study stated that
itching was the main symptom which was
complained by students with allergic
conjunctivitis .This result is comparable to
those results obtained by the studies [28] [30]
[31]. Itching is a recurrent and almost
invariably marks that the inflammation of the
conjunctiva is allergic in origin [8] [9] [15].
This annoyance may swerve a child’s
attentiveness from the teacher to rubbing the
eye to alleviate the symptoms and this may
influence the process of learning [32].
The limitation of the present study were,
the impact of seasonal differences in the
ocular morbidity, the questionnaire used for
reconnoitering for cases of allergic
conjunctivitis had the restrictions of fulfilling
the credibility of answers provided, using the
conventional procedures for bacterial
identification, diagnosis of allergic
conjunctivitis was achieved mainly clinically,
while it was better if sensitization tests were
applied for more precise identification of
such cases.
Conclusions
It was concluded from this study that
allergic and bacterial conjunctivitis was the
most common associated comorbidities that
had an influence on the health of children.
The present study suggests that checking of
school children for ocular problems should
be carried out at organized periods and it
should be one of the leading ingredients of
the school health program. For this, school
teachers should be educated and trained in
recognizing common eye problems among
school children so that these children can be
referred for instant treatment. They should
Diyala Journal of Medicine 67 Vol.18.Issue 1,April 2020
Conjunctivitis among Rural and Urban School Children in Erbil Governorate/ Iraq
Nabaz Fisal Shakir Agha
also impart awareness regarding ocular
hygiene among school children.
Acknowledgements
Author would like to thank the Health and
Education Directorates of Erbil and the heads
of the selected basic schools for giving
permission to conduct the study. Special
thanks are directed to Rizgary Hospital for
their aids. The author appreciates the co
operation of parents who allowed children to
participate in the study.
Conflict of interest
The author acknowledges no conflict of
interest in this study
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