research article vernal keratoconjunctivitis in public primary...

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Research Article Vernal Keratoconjunctivitis in Public Primary School Children in Nigeria: Prevalence and Nomenclature Roseline E. Duke, 1 Friday Odey, 2 and Stefan De Smedt 3 1 University of Calabar Teaching Hospital, Calabar Children’s Eye Center, Department of Ophthalmology, Calabar, Cross River State, Nigeria 2 University of Calabar Teaching Hospital, Department of Pediatrics, Calabar, Cross River State, Nigeria 3 Department of Ophthalmology, AZ Sint-Maarten Hospital, Mechelen, Belgium Correspondence should be addressed to Roseline E. Duke; [email protected] Received 18 March 2016; Accepted 21 June 2016 Academic Editor: Huibert Burger Copyright © 2016 Roseline E. Duke et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. is study sought to add to the body of information on the prevalence and pattern of vernal keratoconjunctivitis (VKC) among school aged children in Cross River State, Nigeria. Method. A cross-sectional survey of children in public primary schools in Cross River State, Nigeria, was studied for VKC. Five schools were included, using a multistage sampling technique. Comprehensive eye examinations were conducted in one thousand two hundred and twenty-six (1226) school children. Main Outcome Measures/Results. e mean age of the population of 1226 school attending children was 9.62 ± 2.324. e prevalence of VKC was 18.1% in this population study. e ratio of males to females is 1.8 : 1. e clinical grading of the 223 children with VKC is as follows: 43 (19.3%) quiescent, 134 (60.1%) mild, 44 (19.7%) moderate, and 2 (0.9%) severe VKC. e clinical types reported are as follows: limbal 67 (30.0%), tarsal 105 (47.1%), and mixed 51 (22.9%). e clinical types were used to describe a modified nomenclature. Conclusions. Vernal keratoconjunctivitis is a commonly occurring chronic condition and an important public health problem. A simple diagnostic nomenclature for describing VKC for primary health care workers is recommended. 1. Introduction Vernal keratoconjunctivitis (VKC) is an important public health problem especially in the hot and dry regions in Africa [1, 2]. It is a chronic allergic eye disease that occurs predominantly in children and is responsible for causing moderate-to-severe visual impairment in children. Tremen- dous progress has been made in combatting measles, vitamin A deficiency, and ophthalmia neonatorum in some lower and middle income countries in the last decades, so that these conditions are no longer regarded as leading causes of corneal blindness in this part of the world [1, 3, 4]. Other conditions such as VKC are becoming a more important cause of corneal visual impairment and blindness [2]. Although rare in temperate regions VKC represents an important cause of hospital referral in many parts of Africa and Asia including Nigerian children [5–7]. A prevalence between 2 and 6% is reported in various parts of Africa [8]. It was identified as the most common conjunctival disease in children seen in hospitals and school children in Nigeria [5, 8]. Furthermore, VKC is reported to be responsible for the highest percentage (21.0%) of general eye clinic attending children in Africa and a cause of school nonattendance [6, 9]. e clinical course of this disease is usually benign and self-limiting, with vision in most children normal, but a group of patients in about 10% of cases will face very debilitating and sight threatening complications which may sometimes manifest in adulthood and cause blindness as well as visual impairment [2, 10]. In addition, the quality of life of afflicted children is affected because they are limited in doing their preferred activities, in the attempt to avoid worsening of their disease [11]. Because of these risks it is important to diagnose and manage VKC correctly at the primary eye care level already by using a more practical classification of the disease [2]. is study sought to determine the prevalence and pat- tern of VKC among public primary school children in Cross Hindawi Publishing Corporation Epidemiology Research International Volume 2016, Article ID 9854062, 6 pages http://dx.doi.org/10.1155/2016/9854062

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Page 1: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

Research ArticleVernal Keratoconjunctivitis in Public Primary SchoolChildren in Nigeria Prevalence and Nomenclature

Roseline E Duke1 Friday Odey2 and Stefan De Smedt3

1University of Calabar Teaching Hospital Calabar Childrenrsquos Eye Center Department of Ophthalmology CalabarCross River State Nigeria2University of Calabar Teaching Hospital Department of Pediatrics Calabar Cross River State Nigeria3Department of Ophthalmology AZ Sint-Maarten Hospital Mechelen Belgium

Correspondence should be addressed to Roseline E Duke drroselinedukegmailcom

Received 18 March 2016 Accepted 21 June 2016

Academic Editor Huibert Burger

Copyright copy 2016 Roseline E Duke et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Objective This study sought to add to the body of information on the prevalence and pattern of vernal keratoconjunctivitis(VKC) among school aged children in Cross River State Nigeria Method A cross-sectional survey of children in public primaryschools in Cross River State Nigeria was studied for VKC Five schools were included using a multistage sampling techniqueComprehensive eye examinations were conducted in one thousand two hundred and twenty-six (1226) school children MainOutcome MeasuresResults The mean age of the population of 1226 school attending children was 962 plusmn 2324 The prevalenceof VKC was 181 in this population studyThe ratio of males to females is 18 1 The clinical grading of the 223 children with VKCis as follows 43 (193) quiescent 134 (601) mild 44 (197) moderate and 2 (09) severe VKC The clinical types reportedare as follows limbal 67 (300) tarsal 105 (471) and mixed 51 (229) The clinical types were used to describe a modifiednomenclatureConclusions Vernal keratoconjunctivitis is a commonly occurring chronic condition and an important public healthproblem A simple diagnostic nomenclature for describing VKC for primary health care workers is recommended

1 Introduction

Vernal keratoconjunctivitis (VKC) is an important publichealth problem especially in the hot and dry regions inAfrica [1 2] It is a chronic allergic eye disease that occurspredominantly in children and is responsible for causingmoderate-to-severe visual impairment in children Tremen-dous progress has been made in combatting measles vitaminA deficiency and ophthalmia neonatorum in some lower andmiddle income countries in the last decades so that theseconditions are no longer regarded as leading causes of cornealblindness in this part of the world [1 3 4] Other conditionssuch as VKC are becoming a more important cause ofcorneal visual impairment and blindness [2] Although rarein temperate regions VKC represents an important cause ofhospital referral in many parts of Africa and Asia includingNigerian children [5ndash7] A prevalence between 2 and 6 isreported in various parts of Africa [8] It was identified as

the most common conjunctival disease in children seen inhospitals and school children in Nigeria [5 8] FurthermoreVKC is reported to be responsible for the highest percentage(210) of general eye clinic attending children in Africa anda cause of school nonattendance [6 9] The clinical course ofthis disease is usually benign and self-limiting with visionin most children normal but a group of patients in about10 of cases will face very debilitating and sight threateningcomplications which may sometimes manifest in adulthoodand cause blindness as well as visual impairment [2 10] Inaddition the quality of life of afflicted children is affectedbecause they are limited in doing their preferred activities inthe attempt to avoid worsening of their disease [11]

Because of these risks it is important to diagnose andmanage VKC correctly at the primary eye care level alreadyby using a more practical classification of the disease [2]

This study sought to determine the prevalence and pat-tern of VKC among public primary school children in Cross

Hindawi Publishing CorporationEpidemiology Research InternationalVolume 2016 Article ID 9854062 6 pageshttpdxdoiorg10115520169854062

2 Epidemiology Research International

River State Nigeria and to develop a classification of VKCsuitable in primary health care settings

2 Method

21 Study Setting The study was conducted in Calabar SouthLocal Government Area (LGA) one of the 18 LGAs in CrossRiver State Nigeria between September and December 2014in the early dry season It has an area of 264 km2 a densityof 7254 inhabitantskm and a population of 191630 [12]Calabar South is located within longitudes 8∘151015840 East and8∘251015840 East and latitudes 4∘541015840 North and 4∘581015840 North CrossRiver State belongs to tropical rainfall belt where rainfallis usually seasonal and at times very heavy ranging from1300mmsqm to 3000mmsqm Calabar South records anaverage annual rainfall amount of 3000mm and relativehumidity of above 85 [13] Mean annual temperature of30∘C prevails over Cross River State except on the ObuduPlateau where the climate is subtemperate with temperaturesranging from 15∘C to 23∘C The vegetation ranges frommangrove swamps through rainforest to derived savannahand mountain parkland The area is characterized by doublemaxima rainfall that climaxes in the months of July andSeptember

The people of Calabar South Local Government Area arepredominantly fishermenwomen farmers petty traders andcanoe carvers and it is the most densely populated and poorarea in the southern senatorial district of the state English isthe lingua franca as this was one of the early British colonizedareas of the state In addition the Calabar South LocalGovernment Area has residents from neighboring statesliving in the area (Calabar South Local Government Area)Primary school education is considered free in Cross RiverState therefore it is expected that primary school childrenin this population will be included in eye examinationsconducted in schools There are 21 public primary schoolswithin the LGAwhich have one to six arms In Calabar SouthLocal Government Area there are 11 primary health centres6 health posts 1 general eye clinic and a tertiary child eyecare facility There is the Cross River State eye care serviceincluding an active child eye care program

22 Study Population The study population were publicprimary school attending pupils in Calabar South LocalGovernment Area of Cross River State The inclusion criteriawere children aged 4 years to 15 years in public primaryschools and children who did not attend school on the dayof examination for any reason Exclusion criteria were othercauses of allergic conjunctivitis Vernal keratoconjunctivitiswas differentiated from the milder forms of allergic eye diseasethat is seasonal allergic conjunctivitis (SAC) and perennialallergic conjunctivitis (PAC) by the presence of limbal andorgiant tarsal papillae This differentiated VKC from atopickeratoconjunctivitis (AKC) happens more in an older agegroup and was differentiated from VKC history of atopy inthe face and elbows using the Hanifin and Rajka DiagnosticCriteria for Atopic Dermatitis (AD)

The study design was cross-sectional

23 Sample Size Calculation The sample size calculation for asingle proportionwhere the population isgt10000 gave a totalsample for the cross-sectional study as 1500 children in fiveschoolsThiswas calculated thus the standardnormal deviateof 196 was used with a prevalence of outcome of interest(VKC) as 3 and a level of precision of 5The nonresponserate was set at 10These resulted in a sample size calculationof 50 children per class For public schools where there aresix class sets a total of 300 children were seen per schoolThesampling frame was composed of a list of all public primaryschools in the Calabar South Local Government Area as wellas a list of the children registered in the primary schoolclasses Some of the children that did not attend school on theday of the visit were traced and visited Parents were invitedon the day for the school visit to be interviewed An informedconsent was taken from parentsguardians

24 SamplingMethod Multistage samplingmethodwas usedto recruit participants for the proposed study in public schoolfacilities in Calabar South Local Government AreaThere are21 primary schools in Calabar South Local Government AreaIn the first stage five public primary schools were randomlyselected by balloting from the list of 21 schools In the secondstage simple random sampling method (through balloting)was used to select the classes in the chosen schools With theuse of an existing register from the selected schools class setswere used from primary one (1) through primary six (6) toselect the 6 classes to be used for the study For recruitment ofchildren into the study systematic random samplingwas usedto select 50 children per class if the number of children wasmore than 50 leading to the recruitment of 300 students perschool The identity of each child was cross-checked againstthe class register which is in the custody of the class teacherCases of VKC were sought and identified within the targetedpopulation of 1500 children We also traced some childrenwho were not in school on the day of the examination andwhose home we could access

25 Interview and Examination of All Children

Demographic and Clinical Data Collected Parentscaregiverswere interviewed and eye examinations were conducted onevery child by the research team that included an ophthalmicnurse optometrist and ophthalmologist Demographic dataincluded school information (name and address of schoolclass teachers name class arm and environmental temper-ature on day of school visit) pupil demography (name andunique ID of child age gender tribe address who the parentlives with religion school grade number of siblings pupilposition in family siblings with similar problems parentswith similar problems father andmotherrsquos income and occu-pation and if they have a mobile phone) Clinical data col-lected include detailed ocular and systemic history anthro-pometric measurements dermatological examinations res-piratory examinations vision assessment autorefractionPlacidorsquos disc eyelid tear assessment conjunctiva corneawith fluorescein dye and lens and optic nerve assessment Allexaminations were conducted by the same ophthalmologistreducing interobserver error

Epidemiology Research International 3

26 Operational Definition Vernal eye disease was defined asthe spectrum of tarsal limbal and mixed vernal keratocon-junctivitis It is equivalent to the term VKC as used in otherstudies Vernal conjunctivitis (VC) is defined as the presenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate It is equivalent to the type tarsal vernal Vernalkeratoconjunctivitis (VKC) is defined as the presence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate in addition to limbal papillae with or without the pres-ence of Trantas dots It is equivalent to the type mixed vernalin other studies Vernal limbitis (VL) is defined as the absenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate and compulsorily limbal papillae It is equivalentto the type limbal vernal Severe vernal keratoconjunctivitis(SVKC) was diagnosed if children have persistent symptomsand signs (diffuse palpebral conjunctival edema thickeningwith papillary hypertrophy giant papillary conjunctivitisand limbal infiltration of 180 or more) Clinical grading wasaccording to that described by Bonini et al [14] At eachschool visit theNigeriaMeteorological Agency recorded dailyforecast of temperature was documented and expressed indegrees centigrade

27 Data Management or Analysis Data was entered intoa Microsoft Excel sheet and analyzed using the StatisticalPackage for the Social Sciences (SPSS) for Windows (version20 SPSS Inc Chicago IL USA) Descriptive statistics (fre-quencies proportions means and standard deviation) wasused to summarize the variables while inferential statistics(chi-square test and Pearsonrsquos correlation coefficient formeasure of associations and correlation) was applied to testthe significant association between categorical variables Ata confidence level of 95 the level of significance was set at119875 lt 005

3 Results

A total of 1500 children were expected to be investigated in 5public primary schools

One hundred and twenty-three (82) children wereregistered in the schools but not present in the schools on thedays of examination Eight children of them could be tracedto their homes These children did not have VKC and wereabsent from school for family reasonsThe remainingmissingchildren could not be traced due to logistic challengesOne hundred and fifty-one (151) parentscaregivers were notavailable to give informed consent Therefore a total of 1226children (1218 children in addition to the 8 children foundat home) were interviewed and examined comprehensivelyTable 1 shows the demography of the general population ofchildren and the VKC population studied

31 Prevalence VKC was seen in 223 children resulting ina prevalence of 181 Males accounted for 145 (65) andfemales 78 (35)Themean ageswere 93plusmn239 and 932plusmn212formales and females respectively whichwas not statisticallysignificant (119875 = 0094) The ratio of males to females is 18 1This was also not statistically significant (119875 = 0166) Table 1shows the age and gender distribution

Table 1 Age and gender distribution in the general school and VKCpopulations

Age range (yrs)gender Frequency Percent (100)AgeGeneral population1ndash5 13 116ndash10 809 66011ndash15 404 339Total 1226 100

Mean age 962 plusmn 2324VKC population1ndash5 7 316ndash10 156 7011ndash15 60 269Total 223 100

Mean ageMales 93 plusmn 239

Female 932 plusmn 212

GenderGeneral populationMale 638 52Female 588 48Total 1226 1000

VKC populationMale 145 65Female 78 35Total 223 100

32 Grade Clinical Types and Suggested Nomenclature Thegrading of vernal keratoconjunctivitis is described in Table 2There was a general reduction in the frequency of VKC asthe primary school class of the child increased this appearedto be a trend Table 3 shows the clinical types of VKC andsuggested diagnostic nomenclatureThe relationship betweenthe frequency of diagnosis of VKC and the environmentaltemperature at the school on the day of examination isreported in Table 4 There was a significant increase in thefrequency of diagnosis of VKC as environmental temperatureincreased (119875 lt 0001)

4 Discussion

VKC is a common recurrent bilateral allergic ocular inflam-mation in which IgE mediated mechanism plays a roleaffecting children and young adults in their first two decades

Information on VKC in several countries including Nige-ria has been based mainly on hospital data Most hospitalstudies show a prevalence between 2 and 6 [5 6] amongpatients of all ages Our study found a population VKC-prevalence of 181 among primary school children (pleasesee Table 1) This is much higher than the prevalence (4-5)reported by the few available population-based studies withsimilar design fromAfrica [15 16] Our study prevalencemaybe higher because of the population-based study design withminimal selection bias In addition quiescent (193) and

4 Epidemiology Research International

Table 2 Clinical grading of vernal keratoconjunctivitis [14]

Clinical grade Left eye Right eye0 (quiescent) absence ofsymptoms 43 (193) 43 (193)

1 (mild) presence of symptomswith no corneal involvement 134 (601) 136 (610)

2 (moderate) presence ofsymptoms + photophobia withno corneal involvement

44 (197) 42 (188)

3 (severe) presence of symptoms+ photophobia mild-to-moderatesuperficial punctatekeratopathycorneal involvement

2 (09) 2 (09)

4 (very severe) presence ofsymptoms + photophobia +diffuse superficial punctatekeratopathycorneal ulcer

0 (00) 0 (00)

Total 223 (1000) 223 (1000)

Table 3 Clinical types of VKC and new diagnostic nomenclature

Clinical type of VKC New diagnostic nomenclature Number ()Limbal Vernal limbitis 67 (300)Tarsal Vernal conjunctivitis 105 (471)Mixed Vernal keratoconjunctivitis 51 (229)Total 223Current name of eyecondition New name for eye condition

Vernalkeratoconjunctivitis Vernal eye disease

mild (601) cases of VKC were included in the study as thisis what was seen in the population during the duration andseason of the study (Table 2) These grades are reported ashaving been very common [17] Moreover to further explainour high prevalence it is reported that the incidence of ocularallergy which will affect a prevalence report is underreported[18] Furthermore parents are most unlikely to take theirchildren to a hospital for quiescent and mild cases of VKCTherefore these grades of VKC will go unaccounted for inhospital data Like a similar study from Rwanda our studydescribed VKC as it presents itself in the population [9]which has the 0ndash14-year age range constituting 42 of thepopulation [19]

Though there was no statistical significance in the gendermore males were clinically affected Our study corroboratesthe information that males are said to be more affected Thisfollows the general pattern seen in Nigeria as well as in somecountries [13 20 21]The onset of VKC is usually after the ageof 5 years the condition eventually resolves around pubertyonly rarely persisting beyond the age of 25 years [10]

The diagnosis of VKC is usually made on clinical exam-ination based on the patientrsquos history and the presence oftypical clinical signs and symptoms [14]Themain symptomsinclude intense ocular itching which may be associated with

lacrimation photophobia foreign body sensation and burn-ingThickmucus discharge from the eyes and eyelid droppingalso occur The symptoms may occur throughout the yearbut are characteristically worse during the dry season In thisstudy the most common clinical type was the tarsal type ofVKC Palpebral forms are said to bemore prevalent in Europeand the Americas whereas mixed and limbal forms are moreseen in Asia and Africa respectively with some geographicvariation and probably hospital attending bias [15]

A tailored approach has earlier been recommended forthe treatment of VKC [22] The diagnosis VKC currentlyrefers to all the three clinical types presently described inliterature Even though the name VKC implies all cases ofthe disease having corneal involvement the situation is notso in most cases especially in the quiescent and mild casesA simple was to understand and practice diagnostic nomen-clature for VKC is suggested (please see Table 4) Such asimple classification aswe propose could easily guide primarycare workers in the clinicalmanagement including treatmentdecision on the use of steroids inVKCThis new classificationallows a swift diagnosis correct therapy and evaluation ofthe prognosis in VKC Further this classification may alsoreflect the onset and the potential for progression of thedisease as the years go by with the disease evolving to apersistent chronic sight threatening condition different fromthe innocuous mild or quiescent disease [10] In summarythis new diagnostic classification identifies different clinicalentities with different referral criteria and possible clinicaloutcome It is also suggested that vernal eye disease couldrefer to the entire spectrum of the clinical types and replacethe term vernal keratoconjunctivitis as presently called whichrefers to tarsal limbal and mixed VKC Further vernalconjunctivitis (VC) is defined as the presence of conjunctivalpapillae of gt1mm diameter over the upper tarsal plate It isequivalent to the type tarsal vernal

Vernal keratoconjunctivitis (VKC) is defined as the pres-ence of conjunctival papillae of gt1mm diameter over theupper tarsal plate in addition to limbal papillae with orwithout the presence of Trantas dots It is equivalent to themixed type Vernal limbitis (VL) is defined as the absence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate and compulsorily limbal papillae or Trantas dot It isequivalent to the type limbal of VKC In order for VKC to bemanaged at the primary eye care level the diagnosis shouldbe unambiguous and the clinical description may need to bematched with treatment modalities and referral criteria

Various risk factors for the development of VKC havebeen investigated and reported [2 10] These include ocularendocrine genetic neurogenic hot dry climate and highsocioeconomic status ones as risk factors It has been reportedthat VKC may be seen all year round however hot climatespredispose to VKC [15] Further it is reported by Boniniet al that about 23 of patients have a perennial formof VKC from onset and more than 60 have additionalrecurrences [10] This study was conducted during the firsthalf of the dry season different from a similar study whichwas conducted during the second half of the dry season[15] The catalyst for progression to more severe disease aswell as the occurrence of exacerbations is still to be well

Epidemiology Research International 5

Table 4 Relationship between primary school environmental temperature and clinical type of vernal keratoconjunctivitis

Schooltemp ∘C Clinical types of vernal keratoconjunctivitis Chi-square 119875 valueLimbal Tarsal Mixed Total

GPSMA27 5 (388) 24 (229) 12 (235) 41 (184) 33928 lt0001lowast

ECPS30 26 (388) 8 (76) 12 (235) 46 (206)GPSA29 13 (194) 23 (219) 10 (196) 46 (206)HTPS34 16 (239) 43 (410) 12 (235) 71 (318)LPS23 7 (104) 7 (67) 5 (98) 19 (85)lowastStatistically significant GPSMA = Government Primary School Mayne Avenue ECPS = Emmanuel Church Primary School GPSA = Government PrimarySchool Academy HTPS = Holy Trinity Primary School LPS = Lutheran Primary School

defined however suggested causes of exacerbation are saidto be from allergenic reexposure andor sunlight windand dust [23 24] Even though the average temperature forthe day was not taken but rather the temperature at thetime of eye examinations this measure when aggregatedfrom different schools visited suggests that we can have arepresentative idea of the trend with temperature (Table 4)Furthermore it suggests that as the dry season progresseswith increasing temperature one may likely see a rise in casepresentations of VKC Our study therefore tends to supportthe fact that there may be seasonality and that a progressiveincrease in environmental temperature in a hot and dryclimate may be one factor that encourages exacerbation ofdisease especially in the limbal type This is consistent withother series from Africa which report seasonal variation inseverity in up to 40 of patients with VKC [7] furthersuggesting that some of the mild cases of VKC may becomemoderate or severe enough to present to hospital later asthe environmental temperature increases Nevertheless theaetiology and pathophysiology of VKC and predisposing riskfactors for visual impairment still remain unclear

Some limitations of the study include the fact that eyeexamination was done by only one ophthalmologist with-out corroboration by another independent clinician Thisis important since diagnosis of VKC is clinical and thereare other diseases within the group of allergic conjunctivi-tis diseases such as perennial and seasonal conjunctivitisrhinoconjunctivitis atopic keratoconjunctivitis and giantpapillary conjunctivitis [10] However this is a common clini-cal conditionwith characteristic features in this environmenttherefore missing a diagnosis is most unlikely Obtainingsociodemographic information from parents and guardiansincluding consent may have been hampered by traditionalbeliefs Lastly only 80 of the targeted population wasstudiedwhich is a limitation of the study Someof the childrenwho could not be visited in their homes andwhohad droppedout of school may have had VKC This group of people havebeen seen to have a high incidence of VKC and it is a cause ofschool nonattendance [9] such childrenwere not representedin this study

In conclusion this population-based study which esti-mates the probability of the children being affected by VKCat this point in time shows a high prevalence and also gives anidea of the burden of this chronic disease and the implicationfor health services This affirms alongside other studies thatVKC is an important public health problem in Nigeria A

modified simple and practical diagnostic nomenclature issuggested for use by primary health care workers

Ethical Approval

Ethical approval was obtained from the Cross River StateMinistry of Health Ethical Review Board and the study wasconducted in accordance with the Declaration of Helsinki

Competing Interests

The authors declare that they have no competing interests

References

[1] R Duke E Otong M Iso et al ldquoUsing key informants toestimate prevalence of severe visual impairment and blindnessin children in Cross River State Nigeriardquo Journal of AAPOS vol17 no 4 pp 381ndash384 2013

[2] S De Smedt G Wildner and P Kestelyn ldquoVernal keratocon-junctivitis an updaterdquo British Journal of Ophthalmology vol 97no 1 pp 9ndash14 2013

[3] C Gilbert and A Foster ldquoChildhood blindness in the contextof VISION 2020 the right to sightrdquo Bulletin of the World HealthOrganization vol 79 no 3 pp 227ndash232 2001

[4] P Gogate K Kalua and P Courtright ldquoBlindness in child-hood in developing countries time for a reassessmentrdquo PLoSMedicine vol 6 no 12 Article ID e1000177 2009

[5] C U Ukponmwan ldquoVernal keratoconjunctivitis in Nigerians109 consecutive casesrdquo Tropical Doctor vol 33 no 4 pp 242ndash245 2003

[6] R Duke ldquoPediatric eye care common causes of blindness andvisual impairment in children in a hospital settingrdquoMary SlessorJournal of Medicine vol 9 no 2 pp 63ndash67 2009

[7] J H Sandford-Smith ldquoVernal eye disease in Northern NigeriardquoTropical and Geographical Medicine vol 31 no 3 pp 321ndash3281979

[8] A I Ajaiyeoba ldquoPrevalence of atopic diseases in Nigerian chil-dren with vernal kerato-conjunctivitisrdquoWest African Journal ofMedicine vol 22 no 1 pp 15ndash17 2003

[9] S K De Smedt J Nkurikiye Y S Fonteyne S J Tuft C EGilbert and P Kestelyn ldquoVernal keratoconjunctivitis in schoolchildren in Rwanda clinical presentation impact on schoolattendance and access tomedical carerdquoOphthalmology vol 119no 9 pp 1766ndash1772 2012

[10] S Bonini M Coassin S Aronni and A Lambiase ldquoVernalkeratoconjunctivitisrdquo Eye vol 18 no 4 pp 345ndash351 2004

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

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Evidence-Based Complementary and Alternative Medicine

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Page 2: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

2 Epidemiology Research International

River State Nigeria and to develop a classification of VKCsuitable in primary health care settings

2 Method

21 Study Setting The study was conducted in Calabar SouthLocal Government Area (LGA) one of the 18 LGAs in CrossRiver State Nigeria between September and December 2014in the early dry season It has an area of 264 km2 a densityof 7254 inhabitantskm and a population of 191630 [12]Calabar South is located within longitudes 8∘151015840 East and8∘251015840 East and latitudes 4∘541015840 North and 4∘581015840 North CrossRiver State belongs to tropical rainfall belt where rainfallis usually seasonal and at times very heavy ranging from1300mmsqm to 3000mmsqm Calabar South records anaverage annual rainfall amount of 3000mm and relativehumidity of above 85 [13] Mean annual temperature of30∘C prevails over Cross River State except on the ObuduPlateau where the climate is subtemperate with temperaturesranging from 15∘C to 23∘C The vegetation ranges frommangrove swamps through rainforest to derived savannahand mountain parkland The area is characterized by doublemaxima rainfall that climaxes in the months of July andSeptember

The people of Calabar South Local Government Area arepredominantly fishermenwomen farmers petty traders andcanoe carvers and it is the most densely populated and poorarea in the southern senatorial district of the state English isthe lingua franca as this was one of the early British colonizedareas of the state In addition the Calabar South LocalGovernment Area has residents from neighboring statesliving in the area (Calabar South Local Government Area)Primary school education is considered free in Cross RiverState therefore it is expected that primary school childrenin this population will be included in eye examinationsconducted in schools There are 21 public primary schoolswithin the LGAwhich have one to six arms In Calabar SouthLocal Government Area there are 11 primary health centres6 health posts 1 general eye clinic and a tertiary child eyecare facility There is the Cross River State eye care serviceincluding an active child eye care program

22 Study Population The study population were publicprimary school attending pupils in Calabar South LocalGovernment Area of Cross River State The inclusion criteriawere children aged 4 years to 15 years in public primaryschools and children who did not attend school on the dayof examination for any reason Exclusion criteria were othercauses of allergic conjunctivitis Vernal keratoconjunctivitiswas differentiated from the milder forms of allergic eye diseasethat is seasonal allergic conjunctivitis (SAC) and perennialallergic conjunctivitis (PAC) by the presence of limbal andorgiant tarsal papillae This differentiated VKC from atopickeratoconjunctivitis (AKC) happens more in an older agegroup and was differentiated from VKC history of atopy inthe face and elbows using the Hanifin and Rajka DiagnosticCriteria for Atopic Dermatitis (AD)

The study design was cross-sectional

23 Sample Size Calculation The sample size calculation for asingle proportionwhere the population isgt10000 gave a totalsample for the cross-sectional study as 1500 children in fiveschoolsThiswas calculated thus the standardnormal deviateof 196 was used with a prevalence of outcome of interest(VKC) as 3 and a level of precision of 5The nonresponserate was set at 10These resulted in a sample size calculationof 50 children per class For public schools where there aresix class sets a total of 300 children were seen per schoolThesampling frame was composed of a list of all public primaryschools in the Calabar South Local Government Area as wellas a list of the children registered in the primary schoolclasses Some of the children that did not attend school on theday of the visit were traced and visited Parents were invitedon the day for the school visit to be interviewed An informedconsent was taken from parentsguardians

24 SamplingMethod Multistage samplingmethodwas usedto recruit participants for the proposed study in public schoolfacilities in Calabar South Local Government AreaThere are21 primary schools in Calabar South Local Government AreaIn the first stage five public primary schools were randomlyselected by balloting from the list of 21 schools In the secondstage simple random sampling method (through balloting)was used to select the classes in the chosen schools With theuse of an existing register from the selected schools class setswere used from primary one (1) through primary six (6) toselect the 6 classes to be used for the study For recruitment ofchildren into the study systematic random samplingwas usedto select 50 children per class if the number of children wasmore than 50 leading to the recruitment of 300 students perschool The identity of each child was cross-checked againstthe class register which is in the custody of the class teacherCases of VKC were sought and identified within the targetedpopulation of 1500 children We also traced some childrenwho were not in school on the day of the examination andwhose home we could access

25 Interview and Examination of All Children

Demographic and Clinical Data Collected Parentscaregiverswere interviewed and eye examinations were conducted onevery child by the research team that included an ophthalmicnurse optometrist and ophthalmologist Demographic dataincluded school information (name and address of schoolclass teachers name class arm and environmental temper-ature on day of school visit) pupil demography (name andunique ID of child age gender tribe address who the parentlives with religion school grade number of siblings pupilposition in family siblings with similar problems parentswith similar problems father andmotherrsquos income and occu-pation and if they have a mobile phone) Clinical data col-lected include detailed ocular and systemic history anthro-pometric measurements dermatological examinations res-piratory examinations vision assessment autorefractionPlacidorsquos disc eyelid tear assessment conjunctiva corneawith fluorescein dye and lens and optic nerve assessment Allexaminations were conducted by the same ophthalmologistreducing interobserver error

Epidemiology Research International 3

26 Operational Definition Vernal eye disease was defined asthe spectrum of tarsal limbal and mixed vernal keratocon-junctivitis It is equivalent to the term VKC as used in otherstudies Vernal conjunctivitis (VC) is defined as the presenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate It is equivalent to the type tarsal vernal Vernalkeratoconjunctivitis (VKC) is defined as the presence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate in addition to limbal papillae with or without the pres-ence of Trantas dots It is equivalent to the type mixed vernalin other studies Vernal limbitis (VL) is defined as the absenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate and compulsorily limbal papillae It is equivalentto the type limbal vernal Severe vernal keratoconjunctivitis(SVKC) was diagnosed if children have persistent symptomsand signs (diffuse palpebral conjunctival edema thickeningwith papillary hypertrophy giant papillary conjunctivitisand limbal infiltration of 180 or more) Clinical grading wasaccording to that described by Bonini et al [14] At eachschool visit theNigeriaMeteorological Agency recorded dailyforecast of temperature was documented and expressed indegrees centigrade

27 Data Management or Analysis Data was entered intoa Microsoft Excel sheet and analyzed using the StatisticalPackage for the Social Sciences (SPSS) for Windows (version20 SPSS Inc Chicago IL USA) Descriptive statistics (fre-quencies proportions means and standard deviation) wasused to summarize the variables while inferential statistics(chi-square test and Pearsonrsquos correlation coefficient formeasure of associations and correlation) was applied to testthe significant association between categorical variables Ata confidence level of 95 the level of significance was set at119875 lt 005

3 Results

A total of 1500 children were expected to be investigated in 5public primary schools

One hundred and twenty-three (82) children wereregistered in the schools but not present in the schools on thedays of examination Eight children of them could be tracedto their homes These children did not have VKC and wereabsent from school for family reasonsThe remainingmissingchildren could not be traced due to logistic challengesOne hundred and fifty-one (151) parentscaregivers were notavailable to give informed consent Therefore a total of 1226children (1218 children in addition to the 8 children foundat home) were interviewed and examined comprehensivelyTable 1 shows the demography of the general population ofchildren and the VKC population studied

31 Prevalence VKC was seen in 223 children resulting ina prevalence of 181 Males accounted for 145 (65) andfemales 78 (35)Themean ageswere 93plusmn239 and 932plusmn212formales and females respectively whichwas not statisticallysignificant (119875 = 0094) The ratio of males to females is 18 1This was also not statistically significant (119875 = 0166) Table 1shows the age and gender distribution

Table 1 Age and gender distribution in the general school and VKCpopulations

Age range (yrs)gender Frequency Percent (100)AgeGeneral population1ndash5 13 116ndash10 809 66011ndash15 404 339Total 1226 100

Mean age 962 plusmn 2324VKC population1ndash5 7 316ndash10 156 7011ndash15 60 269Total 223 100

Mean ageMales 93 plusmn 239

Female 932 plusmn 212

GenderGeneral populationMale 638 52Female 588 48Total 1226 1000

VKC populationMale 145 65Female 78 35Total 223 100

32 Grade Clinical Types and Suggested Nomenclature Thegrading of vernal keratoconjunctivitis is described in Table 2There was a general reduction in the frequency of VKC asthe primary school class of the child increased this appearedto be a trend Table 3 shows the clinical types of VKC andsuggested diagnostic nomenclatureThe relationship betweenthe frequency of diagnosis of VKC and the environmentaltemperature at the school on the day of examination isreported in Table 4 There was a significant increase in thefrequency of diagnosis of VKC as environmental temperatureincreased (119875 lt 0001)

4 Discussion

VKC is a common recurrent bilateral allergic ocular inflam-mation in which IgE mediated mechanism plays a roleaffecting children and young adults in their first two decades

Information on VKC in several countries including Nige-ria has been based mainly on hospital data Most hospitalstudies show a prevalence between 2 and 6 [5 6] amongpatients of all ages Our study found a population VKC-prevalence of 181 among primary school children (pleasesee Table 1) This is much higher than the prevalence (4-5)reported by the few available population-based studies withsimilar design fromAfrica [15 16] Our study prevalencemaybe higher because of the population-based study design withminimal selection bias In addition quiescent (193) and

4 Epidemiology Research International

Table 2 Clinical grading of vernal keratoconjunctivitis [14]

Clinical grade Left eye Right eye0 (quiescent) absence ofsymptoms 43 (193) 43 (193)

1 (mild) presence of symptomswith no corneal involvement 134 (601) 136 (610)

2 (moderate) presence ofsymptoms + photophobia withno corneal involvement

44 (197) 42 (188)

3 (severe) presence of symptoms+ photophobia mild-to-moderatesuperficial punctatekeratopathycorneal involvement

2 (09) 2 (09)

4 (very severe) presence ofsymptoms + photophobia +diffuse superficial punctatekeratopathycorneal ulcer

0 (00) 0 (00)

Total 223 (1000) 223 (1000)

Table 3 Clinical types of VKC and new diagnostic nomenclature

Clinical type of VKC New diagnostic nomenclature Number ()Limbal Vernal limbitis 67 (300)Tarsal Vernal conjunctivitis 105 (471)Mixed Vernal keratoconjunctivitis 51 (229)Total 223Current name of eyecondition New name for eye condition

Vernalkeratoconjunctivitis Vernal eye disease

mild (601) cases of VKC were included in the study as thisis what was seen in the population during the duration andseason of the study (Table 2) These grades are reported ashaving been very common [17] Moreover to further explainour high prevalence it is reported that the incidence of ocularallergy which will affect a prevalence report is underreported[18] Furthermore parents are most unlikely to take theirchildren to a hospital for quiescent and mild cases of VKCTherefore these grades of VKC will go unaccounted for inhospital data Like a similar study from Rwanda our studydescribed VKC as it presents itself in the population [9]which has the 0ndash14-year age range constituting 42 of thepopulation [19]

Though there was no statistical significance in the gendermore males were clinically affected Our study corroboratesthe information that males are said to be more affected Thisfollows the general pattern seen in Nigeria as well as in somecountries [13 20 21]The onset of VKC is usually after the ageof 5 years the condition eventually resolves around pubertyonly rarely persisting beyond the age of 25 years [10]

The diagnosis of VKC is usually made on clinical exam-ination based on the patientrsquos history and the presence oftypical clinical signs and symptoms [14]Themain symptomsinclude intense ocular itching which may be associated with

lacrimation photophobia foreign body sensation and burn-ingThickmucus discharge from the eyes and eyelid droppingalso occur The symptoms may occur throughout the yearbut are characteristically worse during the dry season In thisstudy the most common clinical type was the tarsal type ofVKC Palpebral forms are said to bemore prevalent in Europeand the Americas whereas mixed and limbal forms are moreseen in Asia and Africa respectively with some geographicvariation and probably hospital attending bias [15]

A tailored approach has earlier been recommended forthe treatment of VKC [22] The diagnosis VKC currentlyrefers to all the three clinical types presently described inliterature Even though the name VKC implies all cases ofthe disease having corneal involvement the situation is notso in most cases especially in the quiescent and mild casesA simple was to understand and practice diagnostic nomen-clature for VKC is suggested (please see Table 4) Such asimple classification aswe propose could easily guide primarycare workers in the clinicalmanagement including treatmentdecision on the use of steroids inVKCThis new classificationallows a swift diagnosis correct therapy and evaluation ofthe prognosis in VKC Further this classification may alsoreflect the onset and the potential for progression of thedisease as the years go by with the disease evolving to apersistent chronic sight threatening condition different fromthe innocuous mild or quiescent disease [10] In summarythis new diagnostic classification identifies different clinicalentities with different referral criteria and possible clinicaloutcome It is also suggested that vernal eye disease couldrefer to the entire spectrum of the clinical types and replacethe term vernal keratoconjunctivitis as presently called whichrefers to tarsal limbal and mixed VKC Further vernalconjunctivitis (VC) is defined as the presence of conjunctivalpapillae of gt1mm diameter over the upper tarsal plate It isequivalent to the type tarsal vernal

Vernal keratoconjunctivitis (VKC) is defined as the pres-ence of conjunctival papillae of gt1mm diameter over theupper tarsal plate in addition to limbal papillae with orwithout the presence of Trantas dots It is equivalent to themixed type Vernal limbitis (VL) is defined as the absence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate and compulsorily limbal papillae or Trantas dot It isequivalent to the type limbal of VKC In order for VKC to bemanaged at the primary eye care level the diagnosis shouldbe unambiguous and the clinical description may need to bematched with treatment modalities and referral criteria

Various risk factors for the development of VKC havebeen investigated and reported [2 10] These include ocularendocrine genetic neurogenic hot dry climate and highsocioeconomic status ones as risk factors It has been reportedthat VKC may be seen all year round however hot climatespredispose to VKC [15] Further it is reported by Boniniet al that about 23 of patients have a perennial formof VKC from onset and more than 60 have additionalrecurrences [10] This study was conducted during the firsthalf of the dry season different from a similar study whichwas conducted during the second half of the dry season[15] The catalyst for progression to more severe disease aswell as the occurrence of exacerbations is still to be well

Epidemiology Research International 5

Table 4 Relationship between primary school environmental temperature and clinical type of vernal keratoconjunctivitis

Schooltemp ∘C Clinical types of vernal keratoconjunctivitis Chi-square 119875 valueLimbal Tarsal Mixed Total

GPSMA27 5 (388) 24 (229) 12 (235) 41 (184) 33928 lt0001lowast

ECPS30 26 (388) 8 (76) 12 (235) 46 (206)GPSA29 13 (194) 23 (219) 10 (196) 46 (206)HTPS34 16 (239) 43 (410) 12 (235) 71 (318)LPS23 7 (104) 7 (67) 5 (98) 19 (85)lowastStatistically significant GPSMA = Government Primary School Mayne Avenue ECPS = Emmanuel Church Primary School GPSA = Government PrimarySchool Academy HTPS = Holy Trinity Primary School LPS = Lutheran Primary School

defined however suggested causes of exacerbation are saidto be from allergenic reexposure andor sunlight windand dust [23 24] Even though the average temperature forthe day was not taken but rather the temperature at thetime of eye examinations this measure when aggregatedfrom different schools visited suggests that we can have arepresentative idea of the trend with temperature (Table 4)Furthermore it suggests that as the dry season progresseswith increasing temperature one may likely see a rise in casepresentations of VKC Our study therefore tends to supportthe fact that there may be seasonality and that a progressiveincrease in environmental temperature in a hot and dryclimate may be one factor that encourages exacerbation ofdisease especially in the limbal type This is consistent withother series from Africa which report seasonal variation inseverity in up to 40 of patients with VKC [7] furthersuggesting that some of the mild cases of VKC may becomemoderate or severe enough to present to hospital later asthe environmental temperature increases Nevertheless theaetiology and pathophysiology of VKC and predisposing riskfactors for visual impairment still remain unclear

Some limitations of the study include the fact that eyeexamination was done by only one ophthalmologist with-out corroboration by another independent clinician Thisis important since diagnosis of VKC is clinical and thereare other diseases within the group of allergic conjunctivi-tis diseases such as perennial and seasonal conjunctivitisrhinoconjunctivitis atopic keratoconjunctivitis and giantpapillary conjunctivitis [10] However this is a common clini-cal conditionwith characteristic features in this environmenttherefore missing a diagnosis is most unlikely Obtainingsociodemographic information from parents and guardiansincluding consent may have been hampered by traditionalbeliefs Lastly only 80 of the targeted population wasstudiedwhich is a limitation of the study Someof the childrenwho could not be visited in their homes andwhohad droppedout of school may have had VKC This group of people havebeen seen to have a high incidence of VKC and it is a cause ofschool nonattendance [9] such childrenwere not representedin this study

In conclusion this population-based study which esti-mates the probability of the children being affected by VKCat this point in time shows a high prevalence and also gives anidea of the burden of this chronic disease and the implicationfor health services This affirms alongside other studies thatVKC is an important public health problem in Nigeria A

modified simple and practical diagnostic nomenclature issuggested for use by primary health care workers

Ethical Approval

Ethical approval was obtained from the Cross River StateMinistry of Health Ethical Review Board and the study wasconducted in accordance with the Declaration of Helsinki

Competing Interests

The authors declare that they have no competing interests

References

[1] R Duke E Otong M Iso et al ldquoUsing key informants toestimate prevalence of severe visual impairment and blindnessin children in Cross River State Nigeriardquo Journal of AAPOS vol17 no 4 pp 381ndash384 2013

[2] S De Smedt G Wildner and P Kestelyn ldquoVernal keratocon-junctivitis an updaterdquo British Journal of Ophthalmology vol 97no 1 pp 9ndash14 2013

[3] C Gilbert and A Foster ldquoChildhood blindness in the contextof VISION 2020 the right to sightrdquo Bulletin of the World HealthOrganization vol 79 no 3 pp 227ndash232 2001

[4] P Gogate K Kalua and P Courtright ldquoBlindness in child-hood in developing countries time for a reassessmentrdquo PLoSMedicine vol 6 no 12 Article ID e1000177 2009

[5] C U Ukponmwan ldquoVernal keratoconjunctivitis in Nigerians109 consecutive casesrdquo Tropical Doctor vol 33 no 4 pp 242ndash245 2003

[6] R Duke ldquoPediatric eye care common causes of blindness andvisual impairment in children in a hospital settingrdquoMary SlessorJournal of Medicine vol 9 no 2 pp 63ndash67 2009

[7] J H Sandford-Smith ldquoVernal eye disease in Northern NigeriardquoTropical and Geographical Medicine vol 31 no 3 pp 321ndash3281979

[8] A I Ajaiyeoba ldquoPrevalence of atopic diseases in Nigerian chil-dren with vernal kerato-conjunctivitisrdquoWest African Journal ofMedicine vol 22 no 1 pp 15ndash17 2003

[9] S K De Smedt J Nkurikiye Y S Fonteyne S J Tuft C EGilbert and P Kestelyn ldquoVernal keratoconjunctivitis in schoolchildren in Rwanda clinical presentation impact on schoolattendance and access tomedical carerdquoOphthalmology vol 119no 9 pp 1766ndash1772 2012

[10] S Bonini M Coassin S Aronni and A Lambiase ldquoVernalkeratoconjunctivitisrdquo Eye vol 18 no 4 pp 345ndash351 2004

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

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Page 3: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

Epidemiology Research International 3

26 Operational Definition Vernal eye disease was defined asthe spectrum of tarsal limbal and mixed vernal keratocon-junctivitis It is equivalent to the term VKC as used in otherstudies Vernal conjunctivitis (VC) is defined as the presenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate It is equivalent to the type tarsal vernal Vernalkeratoconjunctivitis (VKC) is defined as the presence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate in addition to limbal papillae with or without the pres-ence of Trantas dots It is equivalent to the type mixed vernalin other studies Vernal limbitis (VL) is defined as the absenceof conjunctival papillae of gt1mm diameter over the uppertarsal plate and compulsorily limbal papillae It is equivalentto the type limbal vernal Severe vernal keratoconjunctivitis(SVKC) was diagnosed if children have persistent symptomsand signs (diffuse palpebral conjunctival edema thickeningwith papillary hypertrophy giant papillary conjunctivitisand limbal infiltration of 180 or more) Clinical grading wasaccording to that described by Bonini et al [14] At eachschool visit theNigeriaMeteorological Agency recorded dailyforecast of temperature was documented and expressed indegrees centigrade

27 Data Management or Analysis Data was entered intoa Microsoft Excel sheet and analyzed using the StatisticalPackage for the Social Sciences (SPSS) for Windows (version20 SPSS Inc Chicago IL USA) Descriptive statistics (fre-quencies proportions means and standard deviation) wasused to summarize the variables while inferential statistics(chi-square test and Pearsonrsquos correlation coefficient formeasure of associations and correlation) was applied to testthe significant association between categorical variables Ata confidence level of 95 the level of significance was set at119875 lt 005

3 Results

A total of 1500 children were expected to be investigated in 5public primary schools

One hundred and twenty-three (82) children wereregistered in the schools but not present in the schools on thedays of examination Eight children of them could be tracedto their homes These children did not have VKC and wereabsent from school for family reasonsThe remainingmissingchildren could not be traced due to logistic challengesOne hundred and fifty-one (151) parentscaregivers were notavailable to give informed consent Therefore a total of 1226children (1218 children in addition to the 8 children foundat home) were interviewed and examined comprehensivelyTable 1 shows the demography of the general population ofchildren and the VKC population studied

31 Prevalence VKC was seen in 223 children resulting ina prevalence of 181 Males accounted for 145 (65) andfemales 78 (35)Themean ageswere 93plusmn239 and 932plusmn212formales and females respectively whichwas not statisticallysignificant (119875 = 0094) The ratio of males to females is 18 1This was also not statistically significant (119875 = 0166) Table 1shows the age and gender distribution

Table 1 Age and gender distribution in the general school and VKCpopulations

Age range (yrs)gender Frequency Percent (100)AgeGeneral population1ndash5 13 116ndash10 809 66011ndash15 404 339Total 1226 100

Mean age 962 plusmn 2324VKC population1ndash5 7 316ndash10 156 7011ndash15 60 269Total 223 100

Mean ageMales 93 plusmn 239

Female 932 plusmn 212

GenderGeneral populationMale 638 52Female 588 48Total 1226 1000

VKC populationMale 145 65Female 78 35Total 223 100

32 Grade Clinical Types and Suggested Nomenclature Thegrading of vernal keratoconjunctivitis is described in Table 2There was a general reduction in the frequency of VKC asthe primary school class of the child increased this appearedto be a trend Table 3 shows the clinical types of VKC andsuggested diagnostic nomenclatureThe relationship betweenthe frequency of diagnosis of VKC and the environmentaltemperature at the school on the day of examination isreported in Table 4 There was a significant increase in thefrequency of diagnosis of VKC as environmental temperatureincreased (119875 lt 0001)

4 Discussion

VKC is a common recurrent bilateral allergic ocular inflam-mation in which IgE mediated mechanism plays a roleaffecting children and young adults in their first two decades

Information on VKC in several countries including Nige-ria has been based mainly on hospital data Most hospitalstudies show a prevalence between 2 and 6 [5 6] amongpatients of all ages Our study found a population VKC-prevalence of 181 among primary school children (pleasesee Table 1) This is much higher than the prevalence (4-5)reported by the few available population-based studies withsimilar design fromAfrica [15 16] Our study prevalencemaybe higher because of the population-based study design withminimal selection bias In addition quiescent (193) and

4 Epidemiology Research International

Table 2 Clinical grading of vernal keratoconjunctivitis [14]

Clinical grade Left eye Right eye0 (quiescent) absence ofsymptoms 43 (193) 43 (193)

1 (mild) presence of symptomswith no corneal involvement 134 (601) 136 (610)

2 (moderate) presence ofsymptoms + photophobia withno corneal involvement

44 (197) 42 (188)

3 (severe) presence of symptoms+ photophobia mild-to-moderatesuperficial punctatekeratopathycorneal involvement

2 (09) 2 (09)

4 (very severe) presence ofsymptoms + photophobia +diffuse superficial punctatekeratopathycorneal ulcer

0 (00) 0 (00)

Total 223 (1000) 223 (1000)

Table 3 Clinical types of VKC and new diagnostic nomenclature

Clinical type of VKC New diagnostic nomenclature Number ()Limbal Vernal limbitis 67 (300)Tarsal Vernal conjunctivitis 105 (471)Mixed Vernal keratoconjunctivitis 51 (229)Total 223Current name of eyecondition New name for eye condition

Vernalkeratoconjunctivitis Vernal eye disease

mild (601) cases of VKC were included in the study as thisis what was seen in the population during the duration andseason of the study (Table 2) These grades are reported ashaving been very common [17] Moreover to further explainour high prevalence it is reported that the incidence of ocularallergy which will affect a prevalence report is underreported[18] Furthermore parents are most unlikely to take theirchildren to a hospital for quiescent and mild cases of VKCTherefore these grades of VKC will go unaccounted for inhospital data Like a similar study from Rwanda our studydescribed VKC as it presents itself in the population [9]which has the 0ndash14-year age range constituting 42 of thepopulation [19]

Though there was no statistical significance in the gendermore males were clinically affected Our study corroboratesthe information that males are said to be more affected Thisfollows the general pattern seen in Nigeria as well as in somecountries [13 20 21]The onset of VKC is usually after the ageof 5 years the condition eventually resolves around pubertyonly rarely persisting beyond the age of 25 years [10]

The diagnosis of VKC is usually made on clinical exam-ination based on the patientrsquos history and the presence oftypical clinical signs and symptoms [14]Themain symptomsinclude intense ocular itching which may be associated with

lacrimation photophobia foreign body sensation and burn-ingThickmucus discharge from the eyes and eyelid droppingalso occur The symptoms may occur throughout the yearbut are characteristically worse during the dry season In thisstudy the most common clinical type was the tarsal type ofVKC Palpebral forms are said to bemore prevalent in Europeand the Americas whereas mixed and limbal forms are moreseen in Asia and Africa respectively with some geographicvariation and probably hospital attending bias [15]

A tailored approach has earlier been recommended forthe treatment of VKC [22] The diagnosis VKC currentlyrefers to all the three clinical types presently described inliterature Even though the name VKC implies all cases ofthe disease having corneal involvement the situation is notso in most cases especially in the quiescent and mild casesA simple was to understand and practice diagnostic nomen-clature for VKC is suggested (please see Table 4) Such asimple classification aswe propose could easily guide primarycare workers in the clinicalmanagement including treatmentdecision on the use of steroids inVKCThis new classificationallows a swift diagnosis correct therapy and evaluation ofthe prognosis in VKC Further this classification may alsoreflect the onset and the potential for progression of thedisease as the years go by with the disease evolving to apersistent chronic sight threatening condition different fromthe innocuous mild or quiescent disease [10] In summarythis new diagnostic classification identifies different clinicalentities with different referral criteria and possible clinicaloutcome It is also suggested that vernal eye disease couldrefer to the entire spectrum of the clinical types and replacethe term vernal keratoconjunctivitis as presently called whichrefers to tarsal limbal and mixed VKC Further vernalconjunctivitis (VC) is defined as the presence of conjunctivalpapillae of gt1mm diameter over the upper tarsal plate It isequivalent to the type tarsal vernal

Vernal keratoconjunctivitis (VKC) is defined as the pres-ence of conjunctival papillae of gt1mm diameter over theupper tarsal plate in addition to limbal papillae with orwithout the presence of Trantas dots It is equivalent to themixed type Vernal limbitis (VL) is defined as the absence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate and compulsorily limbal papillae or Trantas dot It isequivalent to the type limbal of VKC In order for VKC to bemanaged at the primary eye care level the diagnosis shouldbe unambiguous and the clinical description may need to bematched with treatment modalities and referral criteria

Various risk factors for the development of VKC havebeen investigated and reported [2 10] These include ocularendocrine genetic neurogenic hot dry climate and highsocioeconomic status ones as risk factors It has been reportedthat VKC may be seen all year round however hot climatespredispose to VKC [15] Further it is reported by Boniniet al that about 23 of patients have a perennial formof VKC from onset and more than 60 have additionalrecurrences [10] This study was conducted during the firsthalf of the dry season different from a similar study whichwas conducted during the second half of the dry season[15] The catalyst for progression to more severe disease aswell as the occurrence of exacerbations is still to be well

Epidemiology Research International 5

Table 4 Relationship between primary school environmental temperature and clinical type of vernal keratoconjunctivitis

Schooltemp ∘C Clinical types of vernal keratoconjunctivitis Chi-square 119875 valueLimbal Tarsal Mixed Total

GPSMA27 5 (388) 24 (229) 12 (235) 41 (184) 33928 lt0001lowast

ECPS30 26 (388) 8 (76) 12 (235) 46 (206)GPSA29 13 (194) 23 (219) 10 (196) 46 (206)HTPS34 16 (239) 43 (410) 12 (235) 71 (318)LPS23 7 (104) 7 (67) 5 (98) 19 (85)lowastStatistically significant GPSMA = Government Primary School Mayne Avenue ECPS = Emmanuel Church Primary School GPSA = Government PrimarySchool Academy HTPS = Holy Trinity Primary School LPS = Lutheran Primary School

defined however suggested causes of exacerbation are saidto be from allergenic reexposure andor sunlight windand dust [23 24] Even though the average temperature forthe day was not taken but rather the temperature at thetime of eye examinations this measure when aggregatedfrom different schools visited suggests that we can have arepresentative idea of the trend with temperature (Table 4)Furthermore it suggests that as the dry season progresseswith increasing temperature one may likely see a rise in casepresentations of VKC Our study therefore tends to supportthe fact that there may be seasonality and that a progressiveincrease in environmental temperature in a hot and dryclimate may be one factor that encourages exacerbation ofdisease especially in the limbal type This is consistent withother series from Africa which report seasonal variation inseverity in up to 40 of patients with VKC [7] furthersuggesting that some of the mild cases of VKC may becomemoderate or severe enough to present to hospital later asthe environmental temperature increases Nevertheless theaetiology and pathophysiology of VKC and predisposing riskfactors for visual impairment still remain unclear

Some limitations of the study include the fact that eyeexamination was done by only one ophthalmologist with-out corroboration by another independent clinician Thisis important since diagnosis of VKC is clinical and thereare other diseases within the group of allergic conjunctivi-tis diseases such as perennial and seasonal conjunctivitisrhinoconjunctivitis atopic keratoconjunctivitis and giantpapillary conjunctivitis [10] However this is a common clini-cal conditionwith characteristic features in this environmenttherefore missing a diagnosis is most unlikely Obtainingsociodemographic information from parents and guardiansincluding consent may have been hampered by traditionalbeliefs Lastly only 80 of the targeted population wasstudiedwhich is a limitation of the study Someof the childrenwho could not be visited in their homes andwhohad droppedout of school may have had VKC This group of people havebeen seen to have a high incidence of VKC and it is a cause ofschool nonattendance [9] such childrenwere not representedin this study

In conclusion this population-based study which esti-mates the probability of the children being affected by VKCat this point in time shows a high prevalence and also gives anidea of the burden of this chronic disease and the implicationfor health services This affirms alongside other studies thatVKC is an important public health problem in Nigeria A

modified simple and practical diagnostic nomenclature issuggested for use by primary health care workers

Ethical Approval

Ethical approval was obtained from the Cross River StateMinistry of Health Ethical Review Board and the study wasconducted in accordance with the Declaration of Helsinki

Competing Interests

The authors declare that they have no competing interests

References

[1] R Duke E Otong M Iso et al ldquoUsing key informants toestimate prevalence of severe visual impairment and blindnessin children in Cross River State Nigeriardquo Journal of AAPOS vol17 no 4 pp 381ndash384 2013

[2] S De Smedt G Wildner and P Kestelyn ldquoVernal keratocon-junctivitis an updaterdquo British Journal of Ophthalmology vol 97no 1 pp 9ndash14 2013

[3] C Gilbert and A Foster ldquoChildhood blindness in the contextof VISION 2020 the right to sightrdquo Bulletin of the World HealthOrganization vol 79 no 3 pp 227ndash232 2001

[4] P Gogate K Kalua and P Courtright ldquoBlindness in child-hood in developing countries time for a reassessmentrdquo PLoSMedicine vol 6 no 12 Article ID e1000177 2009

[5] C U Ukponmwan ldquoVernal keratoconjunctivitis in Nigerians109 consecutive casesrdquo Tropical Doctor vol 33 no 4 pp 242ndash245 2003

[6] R Duke ldquoPediatric eye care common causes of blindness andvisual impairment in children in a hospital settingrdquoMary SlessorJournal of Medicine vol 9 no 2 pp 63ndash67 2009

[7] J H Sandford-Smith ldquoVernal eye disease in Northern NigeriardquoTropical and Geographical Medicine vol 31 no 3 pp 321ndash3281979

[8] A I Ajaiyeoba ldquoPrevalence of atopic diseases in Nigerian chil-dren with vernal kerato-conjunctivitisrdquoWest African Journal ofMedicine vol 22 no 1 pp 15ndash17 2003

[9] S K De Smedt J Nkurikiye Y S Fonteyne S J Tuft C EGilbert and P Kestelyn ldquoVernal keratoconjunctivitis in schoolchildren in Rwanda clinical presentation impact on schoolattendance and access tomedical carerdquoOphthalmology vol 119no 9 pp 1766ndash1772 2012

[10] S Bonini M Coassin S Aronni and A Lambiase ldquoVernalkeratoconjunctivitisrdquo Eye vol 18 no 4 pp 345ndash351 2004

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

4 Epidemiology Research International

Table 2 Clinical grading of vernal keratoconjunctivitis [14]

Clinical grade Left eye Right eye0 (quiescent) absence ofsymptoms 43 (193) 43 (193)

1 (mild) presence of symptomswith no corneal involvement 134 (601) 136 (610)

2 (moderate) presence ofsymptoms + photophobia withno corneal involvement

44 (197) 42 (188)

3 (severe) presence of symptoms+ photophobia mild-to-moderatesuperficial punctatekeratopathycorneal involvement

2 (09) 2 (09)

4 (very severe) presence ofsymptoms + photophobia +diffuse superficial punctatekeratopathycorneal ulcer

0 (00) 0 (00)

Total 223 (1000) 223 (1000)

Table 3 Clinical types of VKC and new diagnostic nomenclature

Clinical type of VKC New diagnostic nomenclature Number ()Limbal Vernal limbitis 67 (300)Tarsal Vernal conjunctivitis 105 (471)Mixed Vernal keratoconjunctivitis 51 (229)Total 223Current name of eyecondition New name for eye condition

Vernalkeratoconjunctivitis Vernal eye disease

mild (601) cases of VKC were included in the study as thisis what was seen in the population during the duration andseason of the study (Table 2) These grades are reported ashaving been very common [17] Moreover to further explainour high prevalence it is reported that the incidence of ocularallergy which will affect a prevalence report is underreported[18] Furthermore parents are most unlikely to take theirchildren to a hospital for quiescent and mild cases of VKCTherefore these grades of VKC will go unaccounted for inhospital data Like a similar study from Rwanda our studydescribed VKC as it presents itself in the population [9]which has the 0ndash14-year age range constituting 42 of thepopulation [19]

Though there was no statistical significance in the gendermore males were clinically affected Our study corroboratesthe information that males are said to be more affected Thisfollows the general pattern seen in Nigeria as well as in somecountries [13 20 21]The onset of VKC is usually after the ageof 5 years the condition eventually resolves around pubertyonly rarely persisting beyond the age of 25 years [10]

The diagnosis of VKC is usually made on clinical exam-ination based on the patientrsquos history and the presence oftypical clinical signs and symptoms [14]Themain symptomsinclude intense ocular itching which may be associated with

lacrimation photophobia foreign body sensation and burn-ingThickmucus discharge from the eyes and eyelid droppingalso occur The symptoms may occur throughout the yearbut are characteristically worse during the dry season In thisstudy the most common clinical type was the tarsal type ofVKC Palpebral forms are said to bemore prevalent in Europeand the Americas whereas mixed and limbal forms are moreseen in Asia and Africa respectively with some geographicvariation and probably hospital attending bias [15]

A tailored approach has earlier been recommended forthe treatment of VKC [22] The diagnosis VKC currentlyrefers to all the three clinical types presently described inliterature Even though the name VKC implies all cases ofthe disease having corneal involvement the situation is notso in most cases especially in the quiescent and mild casesA simple was to understand and practice diagnostic nomen-clature for VKC is suggested (please see Table 4) Such asimple classification aswe propose could easily guide primarycare workers in the clinicalmanagement including treatmentdecision on the use of steroids inVKCThis new classificationallows a swift diagnosis correct therapy and evaluation ofthe prognosis in VKC Further this classification may alsoreflect the onset and the potential for progression of thedisease as the years go by with the disease evolving to apersistent chronic sight threatening condition different fromthe innocuous mild or quiescent disease [10] In summarythis new diagnostic classification identifies different clinicalentities with different referral criteria and possible clinicaloutcome It is also suggested that vernal eye disease couldrefer to the entire spectrum of the clinical types and replacethe term vernal keratoconjunctivitis as presently called whichrefers to tarsal limbal and mixed VKC Further vernalconjunctivitis (VC) is defined as the presence of conjunctivalpapillae of gt1mm diameter over the upper tarsal plate It isequivalent to the type tarsal vernal

Vernal keratoconjunctivitis (VKC) is defined as the pres-ence of conjunctival papillae of gt1mm diameter over theupper tarsal plate in addition to limbal papillae with orwithout the presence of Trantas dots It is equivalent to themixed type Vernal limbitis (VL) is defined as the absence ofconjunctival papillae of gt1mmdiameter over the upper tarsalplate and compulsorily limbal papillae or Trantas dot It isequivalent to the type limbal of VKC In order for VKC to bemanaged at the primary eye care level the diagnosis shouldbe unambiguous and the clinical description may need to bematched with treatment modalities and referral criteria

Various risk factors for the development of VKC havebeen investigated and reported [2 10] These include ocularendocrine genetic neurogenic hot dry climate and highsocioeconomic status ones as risk factors It has been reportedthat VKC may be seen all year round however hot climatespredispose to VKC [15] Further it is reported by Boniniet al that about 23 of patients have a perennial formof VKC from onset and more than 60 have additionalrecurrences [10] This study was conducted during the firsthalf of the dry season different from a similar study whichwas conducted during the second half of the dry season[15] The catalyst for progression to more severe disease aswell as the occurrence of exacerbations is still to be well

Epidemiology Research International 5

Table 4 Relationship between primary school environmental temperature and clinical type of vernal keratoconjunctivitis

Schooltemp ∘C Clinical types of vernal keratoconjunctivitis Chi-square 119875 valueLimbal Tarsal Mixed Total

GPSMA27 5 (388) 24 (229) 12 (235) 41 (184) 33928 lt0001lowast

ECPS30 26 (388) 8 (76) 12 (235) 46 (206)GPSA29 13 (194) 23 (219) 10 (196) 46 (206)HTPS34 16 (239) 43 (410) 12 (235) 71 (318)LPS23 7 (104) 7 (67) 5 (98) 19 (85)lowastStatistically significant GPSMA = Government Primary School Mayne Avenue ECPS = Emmanuel Church Primary School GPSA = Government PrimarySchool Academy HTPS = Holy Trinity Primary School LPS = Lutheran Primary School

defined however suggested causes of exacerbation are saidto be from allergenic reexposure andor sunlight windand dust [23 24] Even though the average temperature forthe day was not taken but rather the temperature at thetime of eye examinations this measure when aggregatedfrom different schools visited suggests that we can have arepresentative idea of the trend with temperature (Table 4)Furthermore it suggests that as the dry season progresseswith increasing temperature one may likely see a rise in casepresentations of VKC Our study therefore tends to supportthe fact that there may be seasonality and that a progressiveincrease in environmental temperature in a hot and dryclimate may be one factor that encourages exacerbation ofdisease especially in the limbal type This is consistent withother series from Africa which report seasonal variation inseverity in up to 40 of patients with VKC [7] furthersuggesting that some of the mild cases of VKC may becomemoderate or severe enough to present to hospital later asthe environmental temperature increases Nevertheless theaetiology and pathophysiology of VKC and predisposing riskfactors for visual impairment still remain unclear

Some limitations of the study include the fact that eyeexamination was done by only one ophthalmologist with-out corroboration by another independent clinician Thisis important since diagnosis of VKC is clinical and thereare other diseases within the group of allergic conjunctivi-tis diseases such as perennial and seasonal conjunctivitisrhinoconjunctivitis atopic keratoconjunctivitis and giantpapillary conjunctivitis [10] However this is a common clini-cal conditionwith characteristic features in this environmenttherefore missing a diagnosis is most unlikely Obtainingsociodemographic information from parents and guardiansincluding consent may have been hampered by traditionalbeliefs Lastly only 80 of the targeted population wasstudiedwhich is a limitation of the study Someof the childrenwho could not be visited in their homes andwhohad droppedout of school may have had VKC This group of people havebeen seen to have a high incidence of VKC and it is a cause ofschool nonattendance [9] such childrenwere not representedin this study

In conclusion this population-based study which esti-mates the probability of the children being affected by VKCat this point in time shows a high prevalence and also gives anidea of the burden of this chronic disease and the implicationfor health services This affirms alongside other studies thatVKC is an important public health problem in Nigeria A

modified simple and practical diagnostic nomenclature issuggested for use by primary health care workers

Ethical Approval

Ethical approval was obtained from the Cross River StateMinistry of Health Ethical Review Board and the study wasconducted in accordance with the Declaration of Helsinki

Competing Interests

The authors declare that they have no competing interests

References

[1] R Duke E Otong M Iso et al ldquoUsing key informants toestimate prevalence of severe visual impairment and blindnessin children in Cross River State Nigeriardquo Journal of AAPOS vol17 no 4 pp 381ndash384 2013

[2] S De Smedt G Wildner and P Kestelyn ldquoVernal keratocon-junctivitis an updaterdquo British Journal of Ophthalmology vol 97no 1 pp 9ndash14 2013

[3] C Gilbert and A Foster ldquoChildhood blindness in the contextof VISION 2020 the right to sightrdquo Bulletin of the World HealthOrganization vol 79 no 3 pp 227ndash232 2001

[4] P Gogate K Kalua and P Courtright ldquoBlindness in child-hood in developing countries time for a reassessmentrdquo PLoSMedicine vol 6 no 12 Article ID e1000177 2009

[5] C U Ukponmwan ldquoVernal keratoconjunctivitis in Nigerians109 consecutive casesrdquo Tropical Doctor vol 33 no 4 pp 242ndash245 2003

[6] R Duke ldquoPediatric eye care common causes of blindness andvisual impairment in children in a hospital settingrdquoMary SlessorJournal of Medicine vol 9 no 2 pp 63ndash67 2009

[7] J H Sandford-Smith ldquoVernal eye disease in Northern NigeriardquoTropical and Geographical Medicine vol 31 no 3 pp 321ndash3281979

[8] A I Ajaiyeoba ldquoPrevalence of atopic diseases in Nigerian chil-dren with vernal kerato-conjunctivitisrdquoWest African Journal ofMedicine vol 22 no 1 pp 15ndash17 2003

[9] S K De Smedt J Nkurikiye Y S Fonteyne S J Tuft C EGilbert and P Kestelyn ldquoVernal keratoconjunctivitis in schoolchildren in Rwanda clinical presentation impact on schoolattendance and access tomedical carerdquoOphthalmology vol 119no 9 pp 1766ndash1772 2012

[10] S Bonini M Coassin S Aronni and A Lambiase ldquoVernalkeratoconjunctivitisrdquo Eye vol 18 no 4 pp 345ndash351 2004

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

Epidemiology Research International 5

Table 4 Relationship between primary school environmental temperature and clinical type of vernal keratoconjunctivitis

Schooltemp ∘C Clinical types of vernal keratoconjunctivitis Chi-square 119875 valueLimbal Tarsal Mixed Total

GPSMA27 5 (388) 24 (229) 12 (235) 41 (184) 33928 lt0001lowast

ECPS30 26 (388) 8 (76) 12 (235) 46 (206)GPSA29 13 (194) 23 (219) 10 (196) 46 (206)HTPS34 16 (239) 43 (410) 12 (235) 71 (318)LPS23 7 (104) 7 (67) 5 (98) 19 (85)lowastStatistically significant GPSMA = Government Primary School Mayne Avenue ECPS = Emmanuel Church Primary School GPSA = Government PrimarySchool Academy HTPS = Holy Trinity Primary School LPS = Lutheran Primary School

defined however suggested causes of exacerbation are saidto be from allergenic reexposure andor sunlight windand dust [23 24] Even though the average temperature forthe day was not taken but rather the temperature at thetime of eye examinations this measure when aggregatedfrom different schools visited suggests that we can have arepresentative idea of the trend with temperature (Table 4)Furthermore it suggests that as the dry season progresseswith increasing temperature one may likely see a rise in casepresentations of VKC Our study therefore tends to supportthe fact that there may be seasonality and that a progressiveincrease in environmental temperature in a hot and dryclimate may be one factor that encourages exacerbation ofdisease especially in the limbal type This is consistent withother series from Africa which report seasonal variation inseverity in up to 40 of patients with VKC [7] furthersuggesting that some of the mild cases of VKC may becomemoderate or severe enough to present to hospital later asthe environmental temperature increases Nevertheless theaetiology and pathophysiology of VKC and predisposing riskfactors for visual impairment still remain unclear

Some limitations of the study include the fact that eyeexamination was done by only one ophthalmologist with-out corroboration by another independent clinician Thisis important since diagnosis of VKC is clinical and thereare other diseases within the group of allergic conjunctivi-tis diseases such as perennial and seasonal conjunctivitisrhinoconjunctivitis atopic keratoconjunctivitis and giantpapillary conjunctivitis [10] However this is a common clini-cal conditionwith characteristic features in this environmenttherefore missing a diagnosis is most unlikely Obtainingsociodemographic information from parents and guardiansincluding consent may have been hampered by traditionalbeliefs Lastly only 80 of the targeted population wasstudiedwhich is a limitation of the study Someof the childrenwho could not be visited in their homes andwhohad droppedout of school may have had VKC This group of people havebeen seen to have a high incidence of VKC and it is a cause ofschool nonattendance [9] such childrenwere not representedin this study

In conclusion this population-based study which esti-mates the probability of the children being affected by VKCat this point in time shows a high prevalence and also gives anidea of the burden of this chronic disease and the implicationfor health services This affirms alongside other studies thatVKC is an important public health problem in Nigeria A

modified simple and practical diagnostic nomenclature issuggested for use by primary health care workers

Ethical Approval

Ethical approval was obtained from the Cross River StateMinistry of Health Ethical Review Board and the study wasconducted in accordance with the Declaration of Helsinki

Competing Interests

The authors declare that they have no competing interests

References

[1] R Duke E Otong M Iso et al ldquoUsing key informants toestimate prevalence of severe visual impairment and blindnessin children in Cross River State Nigeriardquo Journal of AAPOS vol17 no 4 pp 381ndash384 2013

[2] S De Smedt G Wildner and P Kestelyn ldquoVernal keratocon-junctivitis an updaterdquo British Journal of Ophthalmology vol 97no 1 pp 9ndash14 2013

[3] C Gilbert and A Foster ldquoChildhood blindness in the contextof VISION 2020 the right to sightrdquo Bulletin of the World HealthOrganization vol 79 no 3 pp 227ndash232 2001

[4] P Gogate K Kalua and P Courtright ldquoBlindness in child-hood in developing countries time for a reassessmentrdquo PLoSMedicine vol 6 no 12 Article ID e1000177 2009

[5] C U Ukponmwan ldquoVernal keratoconjunctivitis in Nigerians109 consecutive casesrdquo Tropical Doctor vol 33 no 4 pp 242ndash245 2003

[6] R Duke ldquoPediatric eye care common causes of blindness andvisual impairment in children in a hospital settingrdquoMary SlessorJournal of Medicine vol 9 no 2 pp 63ndash67 2009

[7] J H Sandford-Smith ldquoVernal eye disease in Northern NigeriardquoTropical and Geographical Medicine vol 31 no 3 pp 321ndash3281979

[8] A I Ajaiyeoba ldquoPrevalence of atopic diseases in Nigerian chil-dren with vernal kerato-conjunctivitisrdquoWest African Journal ofMedicine vol 22 no 1 pp 15ndash17 2003

[9] S K De Smedt J Nkurikiye Y S Fonteyne S J Tuft C EGilbert and P Kestelyn ldquoVernal keratoconjunctivitis in schoolchildren in Rwanda clinical presentation impact on schoolattendance and access tomedical carerdquoOphthalmology vol 119no 9 pp 1766ndash1772 2012

[10] S Bonini M Coassin S Aronni and A Lambiase ldquoVernalkeratoconjunctivitisrdquo Eye vol 18 no 4 pp 345ndash351 2004

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

6 Epidemiology Research International

[11] M Sacchetti I Baiardini A Lambiase et al ldquoDevelopment andtesting of the quality of life in children with vernal keratocon-junctivitis questionnairerdquo American Journal of Ophthalmologyvol 144 no 4 pp 557ndash563e2 2007

[12] Nigerian National Population Gazett Clan Edict Formation 1stedition 1976

[13] D I Eni and J Efiong ldquoSeasonal variation in hydrochemicalparameters of ground water in calabar soyth Cross River StateNigeriardquo British Journal of Arts and Social Sciences vol 3 no 1pp 2046ndash9578 2011

[14] S Bonini M Sacchetti F Mantelli and A Lambiase ldquoClinicalgrading of vernal keratoconjunctivitisrdquo Current Opinion inAllergy and Clinical Immunology vol 7 no 5 pp 436ndash441 2007

[15] S De Smedt J Nkurikiye Y Fonteyne et al ldquoVernal kerato-conjunctivitis in school children in Rwanda and its associationwith socio-economic status a population-based surveyrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no4 pp 711ndash717 2011

[16] S Resnikoff G Cornand G Filliard and L Hugard ldquoLimbalvernal conjunctivitis in the tropicsrdquo Revue Internationale duTrachome vol 3-4 pp 53ndash71 1988

[17] A Lambiase S Minchiotti A Leonardi et al ldquoProspectivemulticenter demographic and epidemiological study on vernalkeratoconjunctivitis a glimpse of ocular surface in Italianpopulationrdquo Ophthalmic Epidemiology vol 16 no 1 pp 38ndash412009

[18] A Leonardi F Busca L Motterle et al ldquoCase series of 406vernal keratoconjunctivitis patients a demographic and epi-demiological studyrdquo Acta Ophthalmologica Scandinavica vol84 no 3 pp 406ndash410 2006

[19] E J Aniah and P B Utang ldquoPopulation structure educationalfacilities and environmental implications in the Cross RiverRegion NigeriardquoGlobal Journal of Social Sciences vol 3 no 1-2pp 47ndash51 2004

[20] E N Onwasigwe R E Umeh N O Magulike and C NOnwasigwe ldquoVernal conjunctivitis in Nigeria childrenrdquo OrientJournal of Medicine vol 6 pp 21ndash23 1994

[21] S Majekodunmi ldquoVernal conjunctivitis in Nigerian childrenrdquoJournal of Pediatric Ophthalmology and Strabismus vol 15 no3 pp 176ndash178 1978

[22] M Sacchetti A Lambiase F Mantelli V Deligianni ALeonardi and S Bonini ldquoTailored approach to the treatment ofvernal keratoconjunctivitisrdquo Ophthalmology vol 117 no 7 pp1294ndash1299 2010

[23] A Leonardi ldquoAllergy and allergic mediators in tearsrdquo Experi-mental Eye Research vol 117 pp 106ndash117 2013

[24] V M Utz and A R Kaufman ldquoAllergic eye diseaserdquo PediatricClinics of North America vol 61 no 3 pp 607ndash620 2014

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Research Article Vernal Keratoconjunctivitis in Public Primary …downloads.hindawi.com/journals/eri/2016/9854062.pdf · 2017. 7. 17. · Research Article Vernal Keratoconjunctivitis

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom