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145]

Original Article

Dry Eye Syndrome and Allergic Conjunctivitis in the

Pediatric Population
Handan Akil, Fatih Celik1, Fatih Ulas2, Ilknur Surucu Kara3

ABSTRACT Access this article online

Website:
Purpose: To assess the comorbidity of dry eye syndrome(DES) and changes in corneal www.meajo.org
curvature in children with allergies. DOI:
Materials and Methods: This prospective, comparative, and observational interventional study 10.4103/0974-9233.167814
included 49patients, who presented to the Ophthalmology Clinic of a State Hospital in Turkey.
Quick Response Code:
There were 25patients with clinically diagnosed seasonal allergic conjunctivitis(AC)(with
complaints of itching and papilla formation of conjunctiva; AC group) and 24 healthy
children(control group). There with no significant differences in age between groups. Using
the ocular surface disease index (OSDI) questionnaire, we performed tear film breakup
time(BUT), central reflex tear meniscus height(TMHR) measurement, Schirmer test on
both groups and evaluated keratometry(K1, K2) and spherical equivalent(SE).
Results: Patients ranged in age from 6 to 18years(median age, 11.79years; 46.9% male;
53.1% female). The papillary reaction was severe in 10% of patients with AC. The prevalence
of dry eye in children with AC was 12%. There was no statistically significant difference
between groups for K1, K2, and SE(P > 0.05, all comparisons). BUT was statistically
different(P=0.004) between groups, indicating that a higher OSDI the tear film BUT was
lower( =0.567). Statistically, significant negative moderate correlations were found between
papillary reaction and the Schirmer test, BUT, and TMHR( =0.454, 0.412, 0.419, and
P=0.001, 0.003, 0.002, respectively).
Conclusions: The evaluation of pediatric patients with AC requires further attention to ensure
an adequate diagnosis of DES.

Key words: Allergic Conjunctivitis, Dry Eye, Tear Breakup Time, Tear Meniscus Height

INTRODUCTION form of ocular allergy is seasonal allergic conjunctivitis(SAC),

accounting for 90% of cases. The most prevalent allergens in SAC

A llergic diseases are among the most common disorders

in children, and ocular allergy represents one of the most
common ocular conditions encountered in clinical practice. The
are grass, tree, and weed pollen and outdoor molds.2,3 Although
the signs and symptoms of SAC usually are mild, it may hinder
school performance, work productivity, everyday tasks, such as
prevalence of allergic diseases in children aged 6 to 14years varies reading resulting in an overall reduction in the quality of life.
significantly from 0.3% to 20.5%, and is gradually increasing.1
This increase may be due to genetics, air pollution in urban Recently, more attention is being paid to dry eye, and the
areas, pets, and early childhood exposure.1 The most common
This is an open access article distributed under the terms of the Creative Commons
Ophtalmology Clinic, Gorele State Hospital, Giresun, AttributionNonCommercialShareAlike 3.0 License, which allows others to remix, tweak, and
build upon the work noncommercially, as long as the author is credited and the new creations are
1
Ophtalmology Clinic, Nizip State Hospital, Gaziantep, 2Department licensed under the identical terms.
of Ophtalmology, Abant Izzet Baysal Medical Faculty, Bolu,
For reprints contact: reprints@medknow.com
3
Paediatrics Clinic, Gorele State Hospital, Giresun, Turkey
Corresponding Author: Dr.Handan Akil, Cite this article as: Akil H, Celik F, Ulas F, Kara IS. Dry eye syndrome and
Gorele State Hospital, Giresun, Turkey. allergic conjunctivitis in the pediatric population. Middle East Afr J Ophthalmol
2015;22:467-71.
Email:handanakil84@gmail.com

2015 Middle East African Journal of Ophthalmology | Published by Wolters Kluwer - Medknow 467
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Akil, etal.: Dry Eye Syndrome in Children with Allergic Conjunctivitis
number of symptomatic patients has been increasing. Dry
eye syndrome(DES) is caused by a heterogeneous group of
diseases which share a functional tear deficit due to reduced
production or excessive evaporation, associated with ocular
discomfort symptoms which could limit the daily activities of
affected patients.4 Traditionally, DES and AC are regarded as
two different diseases. However, recent literature has shown
both conditions share similar characteristics, including several
signs and symptoms.5 Pflugfelder etal.6 suggested that activated
Tcells and an increase in inflammatory cytokines such as
epidermal growth factor, interleukin1(IL1), and IL8,
damage goblet cells and conjunctival epithelial, which account
for a reduction of mucin production and subsequent decrease
of tear film breakup time(BUT). Many reports have shown an
instability of mucins and decreased BUT in AC and suggested
that upregulation of inflammation affects the tear balance.7,8
Corneal mechanical changes, related with the complex allergic
process, may lead to stromal thinning, and may increase the
corneal curvature.
In this study, we evaluated tear dynamics and keratometry(K1, K2)
in patients with SAC, to determine whether clinically diagnosed
patients have concomitant DES and changes in corneal
curvature.
MATERIALS AND METHODS
Sixty children were examined for this study, but 11 children
were excluded because they were uncooperative during the
examination. Hence, 25 children with clinically diagnosed
AC(AC group) and 24 agematched healthy children(control
group) were enrolled in this study. The patients were seen
from May 2014 to June 2014 which is allergy season in our
region. AC was diagnosed according to past history, clinical
symptoms such as ocular itching, redness, tearing, or ocular
pain, and slitlamp examinations showing filamentous(mucous)
discharge, chemosis, hyperemia, or papillae of the palpebral
conjunctiva. Patients excluded from the study were those who
had systemic and ocular diseases, which required any kind of
medical or surgical treatment with an adverse effect on the tests
for dry eye during examinations. This study received ethical
approval from Erzincan University Research Ethics Committee.
The research complies with the declaration of Helsinki of the
World Medical Association, and informed consent was obtained
from each subject and their parents after a full explanation
of the procedures. We examined the ocular discomfort using
the validated ocular surface disease index(OSDI) developed
by Schiffman etal.9 which comprises 12 questions on ocular
irritation symptoms related to dry eye disease and its impact
on visual function. The survey was administered to all patients
(we request parents to help us) by the same researcher in simple
and easily understandable terms so that all the patients were
able to score the intensity of their symptoms. After the OSDI
468 Middle East African Journal of Ophthalmology, Volume 22, Number 4, October - December 2015
questionnaire was completed, autokeratometry was performed
with a tabletop autorefractometer(Canon RKF1).
The patients were explored in a softly lit room with a temperature
of 25C(77F) and a humidity of 40%. Dry eye was confirmed
by means of a set of tests performed in successive manner: Tear
film BUT, tear meniscus height reflex(TMHR) measurement
and the Schirmer test. The conjunctiva and cornea were
examined using a slitlamp. Afluorescein strip(fluorescein,
HaagStreit International Co., Ltd, Koeniz, Switzerland) was
moistened with a saline solution and touched the inferior fornix.
The patients were instructed to blink, and the precorneal tear
film was examined under bluelight illumination. The time in
seconds between the last blink and the appearance of a random
dry spot was recorded by a stopwatch as the BUT10 and 10 s or
less was considered abnormal.
The tear meniscus, which is formed between the lid surface
and the bulbar conjunctiva, is present along the inferior lid
margin. Assessment of the TMH is used universally by eye
care practitioners as part of routine ocular assessments. 11
Of the TMH parameters studied, central TMHR seems to
be the most useful, due to its relationship with subjective
assessment while presenting an easy endpoint for the clinician.
TMHR was measured at the 6 oclock position as the
distance between the darker edge of the lower eyelid and
the upper limit of the brightest reflex of the meniscus, with
the observation and illumination systems set at 0, without
tilting the illumination column. TMHR values<0.1 mm
were considered abnormal.12
The Schirmer tear test is the most common and easily performed
test for the evaluation of DES. The Schirmer I test(without
anesthesia) measures both basal and reflex tearing, and the
Schirmer II test(with anesthesia) measures only the basal
secretion of tearing with topical anesthesia. Schirmer with
anesthesia test for basal secretion was applied with a filter
strip(SNO* Strips, Lab Chauvin, Aubenas, France) located
inferotemporally without touching the cornea and is considered
abnormal if wetting of the strip was 5 mm or less in 5min.
Patients having at least severe to very severe grades from the
OSDI questionnaire and two positive results for the clinical
tests for dry eye in both eyes were considered dry eye positive.
All statistical analyses were performed with SPSS/PC 21.0(IBM
Corp., Armonk, NY, USA). The mean, median, and standard
deviation from each data set were calculated for general statistical
reporting. The MannWhitney Utest and independent sample
ttest were used. To determine the correlation between the
objective tests and the papillary reaction, OSDI Spearmans
correlation analysis was used as appropriate. AP<0.05 was
considered statistically significant.
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Akil, etal.: Dry Eye Syndrome in Children with Allergic Conjunctivitis

RESULTS Table1: Ocular surface disease severity according to OSDI scores

Group OSDI score Severity level
In this study, patients ranged in age from 6 to 18years(meanSD OSDI mild 0-0.25 Mild
of age for all subjects. The mean was 11.793.7years for both OSDI moderate 0.26-0.50 Moderate
OSDI severe 0.51-0.75 Severe
groups combined and 11.182.5years for the AC group and OSDI very severe 0.76-1.00 Very severe
10.944.3years for the control group. Twentythree(46.9%) OSDI: Ocular surface disease index
children were male, and 26(53.1%) were female. There was
no statistically significant difference between groups for age and
gender(P>0.05, both comparisons). Table2: Distribution of 25patients based on ocular surface
disease severity
The results referring to clinical disease severity criteria are Group Percentage CI 95%
presented in Table1. Most of AC group were classified as OSDI Moderate 48 24-72
Severe 48 24-72
moderate and severe, followed by very severe[Table2]. Very severe 4 2-6
CI: Confidence interval
All the patients in the AC group had itchy and red eyes. The
papillary reaction was severe in 10%(5 of 50 of eyes) in the
AC group. The Schirmer test was abnormal in 10%(5 of 50 of Table3: Statistical findings of pediatric patients with and
eyes) in the AC group, BUT was<10 s in 40%(20 of 50 eyes) without dry eye symptoms
of the AC group. TMHR was 0.10.05 in the AC group and Parameters n MeanSD P*
0.250.16 in the control group. TMHR was abnormal in K1(D)
Control 48 42.711.74 0.052
36% (18 of 50 eyes) of the AC group. The prevalence of dry eye AC(+) 50 43.331.4
in the AC group was 24%(6 of 25patients). The odds ratios K2(D)
for Schirmer test, BUT, and TMHR were 5.18, 15.3 and 6.7, Control 48 43.511.9 0.100
respectively(the 95% confidence intervals were: 1.5916.91, AC(+) 50 44.061.4
SE
3.370.43, and 2.0921.77, respectively). The present study Control 48 0.271.3 0.549
found no statistically significant differences between groups for AC(+) 50 0.421.2
the K1, K2 values and spherical equivalent(SE)(P=0.052, Schirmer(mm)
0.1, 0.549, respectively). Kvalues were higher in the AC group Control 48 18.53.1 <0.001
AC(+) 50 11.744.32
compared to the control group[Table3]. BUT(s)
Control 48 14.292.52 <0.001
There were statistically significant difference between groups AC(+) 50 11.33.4
for the Schirmer test, BUT, and TMHR(P<0.001 for all TMHR(mm)
Control 48 0.250.16 <0.001
comparisons). The Schirmer test, BUT, and TMHR values AC(+) 50 0.10.05
were lower in the AC group compared to the control group. *A Pvalue of 0.05 or less considered statistically significant. K1: Keratometer
No statistically significant correlations were found in the height reading of corneal meridian 1, K2: Keratometer reading of corneal meridian2,
of the lacrimal meniscus and Schirmer II test with the OSDI SE:Spherical equivalent, BUT: Breakup time, TMHR: Central reflex tear
meniscus height, D: Diopter, SD: Standard deviation
values( =0.186, 0.267, and P=0.256, 0.586, respectively).
In what concerns clinical disease severity criteria, only BUT
exhibited a statistically significant negative correlation with the The diagnosis of ocular surface disease begins with a patient
OSDI values( = 0.567; P=0.004). history and the large variety of symptoms related to the disease.
Pediatric patients with DES tend to complain less about their
Statistically significant negative moderate correlation was found symptoms than adult patients hence, DES is commonly
between papillary reaction and the Schirmer test, BUT, TMHR overlooked in children. We chose the OSDI questionnaire for
( = 0.454, 0.412, 0.419 and P=0.001, 0.003, 0.002, collecting data from children because it is a only survey that can
respectively). The negative values indicate that there is a linear evaluate the frequency of symptoms and their impact on the
relation between papillary reaction and dry eye tests, but the visual function.9 The questions were divided into three subscales:
opposite relation remains untrue. Hence, the patients with papillary Symptoms (three questions); environmental triggers (three
reaction had lower values for Schirmer test, BUT, and TMHR. questions) and; visionrelated function(six questions). Although,
patient symptombased surveys in adults are useful to study a
DISCUSSION disease and as a followup tool, objective tests can offer greater
precise to determine lacrimal production(Schirmer test) and
The results of the study revealed that AC in the pediatric ocular surface alterations(tear film alterations with vital stains).13
population may cause tear film dysfunction. AC was diagnosed Further studies are required to validate the questionnaire in
based on past history, and clinical symptoms. children.

Middle East African Journal of Ophthalmology, Volume 22, Number 4, October - December 2015 469
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Akil, etal.: Dry Eye Syndrome in Children with Allergic Conjunctivitis
The effects of conjunctivitis on the ocular surface and tear
balance have been discussed in many reports.8,14 Increased
inflammatory cytokines are associated with goblet cell loss
and tear volume insufficiency. Current classification systems
divide DES into two major categories: Aqueous deficient(tear
volume insufficiency) and; evaporative dry eye(meibomian gland
dysfunction and posterior blepharitis).15 The discussion so far
generally refers to an aqueous deficient dry eye.
There are many instances in the literature connecting tear
film dysfunction with AC. One study theorizes that tear film
dysfunction is a possible complication of the ocular allergic
disease.14 Our study concurs with previous reports that AC
is the initial condition and predisposes to DES.16,17 Closer
evaluation of ocular allergy indicated it may be more common
in the pediatric population whereas DES is uncommon. Studies
support the observation that AC establishes an environment
that generates a dry ocular surface.17 The present study found
6 children with dry eye, accounting for 24% of children with
AC. This rate for a dry eye was lower than previous studies18
and could be related to the diagnostic criteria for DES or the
pediatric population in our study.
We performed Schirmer II test, tear film BUT, and TMHR as
objective tests. Schirmer II after topical anesthesia with 0.5%
proparacaine hydrochloride eye drops is objective and has
greater reliability than without anesthesia in reflecting the status
of the dry eye. Additionally, the diagnostic value in patients with
aqueous deficient DES was even higher, providing meaningful
evidence for the diagnosis and treatment of dry eye.19 The
Schirmer test was abnormal in 10%(5 of 50 eyes) of the AC
group. In dry eye patients, lower tear volume, and reduced tear
secretion were welldocumented.11,13,15 We evaluated TMHR
to determine the deficiency of tear volume in children with AC.
We found statistically significant differences for the Schirmer
test, BUT, and TMHR between groups. Clinical practice has
not shown a correlation between the subjective symptoms and
objective findings in assessing the dry eye patient. However,
regardless of the poor association between symptoms and the
traditional objective clinical measures, we have observed that
tear film BUT was closely correlated with patient perception
of the severity of the disease. Our study indicated a negative
moderate correlation between papillary reaction caused by AC
and objective tests.
Some studies reported that the complex allergic process
involving biochemical(enzymes and enzymatic inhibitors)
and cellular(apoptosis) disturbance leads to stromal thinning,
causing an increase in corneal curvature and consequently
myopic astigmatism.20 In susceptible individuals, a longterm
allergic disease with a chronic traumatic factor on the corneal
epithelium could be related to keratoconus. For example, Kim
etal.21 found that persistent and chronic corneal trauma on
470 Middle East African Journal of Ophthalmology, Volume 22, Number 4, October - December 2015
the corneal epithelium(in this particular situation, itching or
chronic trauma provoked by giant papillae), induces a silent
and chronic inflammatory process, leading to progressive loss of
stromal mass and consequently to less biomechanical resistance,
and thus to anterior corneal steepening, decreasing the optical
competence of the anterior corneal surface. Scientific data
support the observation that chronic AC may be a risk factor for
myopic refractive error. We found that there was no statistically
significant difference for K1, K2, and SE values between groups.
However mean keratometry for the AC group was higher than
the control group. Conjunctivitis in this study was not severe,
and its duration may have been short because most cases were
SAC. Hence, the conjunctivitis may not cause any cytological
damage to the ocular surface.
The main limitation of our study was the small sample size
of the study group. Additionally, this study was performed in
a small district of the country, by the same examiner. In the
pediatric population, confirmation of DES with these tests was
troublesome. We examined 60 children during the study but
for accurate analysis of data we excluded the uncooperative
cases. Another limitation of our study was a lack of allergy
testing(e.g.,skin prick tests, etc.) on the clinically diagnosed
patients with AC. Allergists can perform skin testing for specific
allergens by scratch tests or intradermal injections of the
allergen. In vitro tests for immunoglobulin E antibodies to
specific allergens are widely used. Allergic tests would aid in
differentiating intrinsic and extrinsic forms and therefore, be
helpful for treatment. However, the diagnosis of ocular allergy
is primarily clinical,22 so our results should be valid.
CONCLUSION
AC could be complicated by DES in the pediatric population.
In such cases, artificial tears may improve the conditions of
the ocular anterior segment. The present study is valuable for
assessing the relationship between DES and AC in the pediatric
population. Our results merit attention because there are little
data on the prevalence of dry eye in this age group with AC.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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