Vernal Keratoconjunctivitis in School Children in Rwanda

Clinical Presentation, Impact on School Attendance, and Access to Medical Care

Stefan K. De Smedt, MD,1 John Nkurikiye, MD,2 Yannick S. Fonteyne, MD,1 Stephen J. Tuft, FRCOphth, MD,3 Clare E. Gilbert, FRCOphth, MD,4 Philippe Kestelyn, MD, PhD5
Objective: We sought to describe the clinical presentation, effect on visual acuity, impact on school attendance, and access to appropriate eye care in children with vernal keratoconjunctivitis (VKC) in Rwanda (Central Africa). Design: Case-control study nested within a cross-sectional survey. Participants: We examined 3041 children; 121 had VKC. Methods: Primary schools were randomly selected and children were interviewed using a questionnaire on VKC-related symptoms. Data on health-seeking behavior and school attendance were recorded. Children received a full eye examination, including visual acuity using a LogMar E Chart. Main Outcome Measures: Description of the clinical ndings, unaided visual acuity, prior attendance for medical eye care, and the impact of VKC on school attendance. Results: Of the 121 children with VKC, 119 (98.4%) had only limbal disease. Ocular itching (n 101; 83.5%) was the predominant symptom and this was seasonal in 66 children (65.4%), constant but with variable intensity in 18 (17.8%), and constant with constant intensity in 17 children (16.8%). Children with VKC were 6 times more likely to have corneal astigmatism 2 diopters in their worse eye (odds ratio [OR], 6.31; 95% condence interval [CI], 3.26 12.26; P 0.001) than controls. Eight affected eyes had astigmatism 4 diopters or irregular astigmatism incompatible with autokeratometry. Although 4 eyes (1.7%) had uncorrected low vision from VKCinduced corneal astigmatism or keratoconus, only 1 child was visually impaired in both eyes. School nonattendance for an ocular reason during the last 3 months was 5 times more likely in children with VKC (n 44; 36.4%) than among those without (n 297; 10.2%; OR, 5.04; 95% CI, 3.40 7.47; P 0.001). Repeating a school year or having ever dropped out of school was not more common among children with VKC than those without. Medical eye care had been sought by 54 (44.6%) children with VKC. Conclusions: This survey of prevalence and treatment of VKC in an African community adds to the argument for better primary eye care, including a safe topical medication. Long-term follow-up of this cohort is required to ascertain the overall risk of sight-threatening complications. Financial Disclosure(s): The authors have no proprietary or commercial interest in any of the materials discussed in this article. Ophthalmology 2012;119:1766 1772 2012 by the American Academy of Ophthalmology.

Vernal keratoconjunctivitis (VKC) is a chronic, bilateral allergic disease of the external eye that predominantly affects the conjunctiva over the upper tarsal plate and/or limbus.1 Characteristic symptoms are intense ocular itching with tearing, mucous secretion, photophobia, and foreign body sensation.2 Vernal keratoconjunctivitis typically affects children in their rst 2 decades and the majority have a good prognosis, because the disease usually resolves spontaneously after puberty. However, potentially sight-threatening corneal changes can occur (i.e., corneal plaques and ulcers, corneal stem cell deciency, keratoconus).3 6 Vernal keratoconjunctivitis occurs

universally, but is more common in hot and dry environments and it is a major cause of hospital attendance by children in many parts of Africa,1,5,7 Asia,8 and the Middle East.3 Although the clinical characteristics have been described in many large hospital case series, these studies are prone to referral bias and there is little information on the spectrum of disease in the community. In addition, the effect of VKC on the school attendance has not been studied in a population-based sample of children. In 2007, we performed a nested, population-based case-control study of 3041 primary school children in Rwanda (Central Africa), reporting a prevalence of VKC of 4%. Male gender, hot
ISSN 0161-6420/12/$see front matter http://dx.doi.org/10.1016/j.ophtha.2012.03.041

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2012 by the American Academy of Ophthalmology Published by Elsevier Inc.

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children were recruited until there were similar numbers of participants from each area. Selected children and their families were invited to participate via public announcements and parent meetings at the schools. The study took place on the school premises, and on the study day the identity of the children was checked against vaccination certicates, medical insurance, or identity cards; only those whose identity was conrmed were included.

climate, and higher economic status were important risk factors.9 We now describe the clinical pattern of VKC, its impact on school attendance, and explore the health-seeking behavior of affected children.

Patients and Methods

The study was performed during the dry season of August to September 2007. The sample size calculation, questionnaire, data recording instruments, and logistics were based on an earlier pilot study. The questionnaire, information sheet, and consent form were translated from English into the local language, Kinyarwanda, and backtranslated by 2 different translators.

Interview and Examination of Children

Children and their parents or guardians were interviewed using a questionnaire based on symptoms related to VKC. Seasonal variation (seasonal/perennial), duration of the condition, data on health-seeking behavior, and progress in education were recorded. Socioeconomic status of the childrens families was evaluated using a socioeconomic questionnaire.9 All children underwent a full eye examination, including visual acuity measurement in each eye separately using a LogMar E Chart, with and without pinhole. Autokeratometry (Nidek KM-500, Gamagori, Japan) was performed and anterior segments were examined with a portable slitlamp examination. Dilated fundoscopy was performed if vision was 20/60 using a pinhole. We dened VKC as the presence of conjunctival papillae 1 mm diameter over the upper tarsal plate and/or limbal papillae. Involvement of 6 clock-hours of the limbus by papillae was classied as severe VKC. Symptoms and signs were scored by the same investigator with a system described by Akpek et al,11 adapted for limbal VKC, and using standard photographs (Fig 1). Astigmatism 2 diopters was considered clinically signicant. A diagnosis of keratoconus was based on clinical signs (Munson sign, central or paracentral stromal thinning) and irregular astigmatism on

Sampling Strategy
Four areas were identied: 1 urban and 1 rural district with a dry hot climate (urban Kicukiro and rural Bugesera), and 1 urban and 1 rural district with a humid moderate climate (urban and rural Muhanga).10 Primary schools located in these areas were randomly selected from the district school lists using a random digit generator sheet according to probability proportional to size. In each school an alphabetical list of pupils aged 7 to 14 years was generated using enrollment documents. Although primary school education is compulsory in Rwanda, we also included and traced children who had dropped out of school, and who were identied after a comparison of the current school registers with registers for the 6 years before the study. Starting from the top of each list,

Figure 1. Standard photographs used for scoring of bulbar hyperemia, tarsal plate papillae, and conjunctival pigmentation.

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keratometry. Fluorescein staining of the cornea and intraocular pressure were not recorded. one-third of children with VKC had a stinging sensation as a daily problem. Half of the children complaining of ocular itch (54.5%; n 55) had experienced the symptom for 3 years. Symptom scores were signicantly associated with each other (P 0.001), except ocular itching and discharge. Ocular itching was seasonal in 65.4% (n 66) of affected children, constant but with variable intensity in 17.8% (n 18), and constant in 16.8% (n 17).

Statistical Analysis
Data were double-entered into a Microsoft Access database and analyzed using STATA-software 9.2 (STATA Corp, College Station, TX). The worst affected eye for each child was used in the analysis of symptoms and signs. The distributions of symptom and sign scores, health-seeking behavior, and school attendance were analyzed using cross-tabulation. To assess the inuence of gender, age group, and severity of VKC on the distribution of symptoms and signs, odds ratios (OR) were calculated with signicance test (P value) and 95% condence intervals (CI). Visual acuity was grouped using World Health Organization categories for visual status: Normally sighted ( 20/60), low vision ( 20/60 but 10/ 200), or blindness ( 10/200).12

Signs
Table 3 shows the distribution of ocular signs of VKC. All children with VKC had perilimbal pigmentation, which was not related to age (P 0.95). Children with VKC were nearly 5 times more likely to develop stage 2 or 3 perilimbal pigmentation (OR, 4.80; 95% CI, 3.20 7.19; P 0.001) and were 6 times more likely to have corneal astigmatism 2 diopters in their worse eye (OR, 6.31; 95% CI, 3.26 12.26; P 0.001). Seven affected eyes had 4 diopters of astigmatism and in 1 eye the cornea was so irregular that autokeratometry was not possible. Keratoconus was only seen in 3 eyes of 2 children, both with VKC. Only 1 child had cataract, but this was not thought to be steroid induced. According to the categories of visual loss as dened by the World Health Organization, only 4 eyes (1.7%, no missing data) had uncorrected low vision from VKC-induced corneal astigmatism or keratoconus; 1 eye was blind from cataract. Only 1 child was visually impaired, from bilateral corneal astigmatism secondary to VKC but without signs of keratoconus.

Ethics
This study was conducted in accordance with the Declaration of Helsinki and was approved by the Rwandan National Ethics Committee. An information sheet was read out to the parents or guardians in Kinyarwanda, after which they were asked to sign a consent form. All medical care related to VKC was provided free of charge.

Results
We examined 3041 children (94.7% participation rate), 121 of whom had VKC (4%). Almost all had pure limbal (bulbar) disease (n 119; 98.4%): 1 child had palpebral disease only and another had mixed limbal and palpebral disease. Thirteen (10.7%) children had limbal papillae in only 1 eye. Most also had a mild palpebral papillary reaction, but with papillae 1 mm in diameter. Giant cobblestone papillae were not observed in this study. One-third of children (n 39; 32.2%) had severe limbal VKC (Table 1) and 4 had complete involvement of the limbus with papillae in 1 eye (Fig 2 available at http://aaojournal.org).

Analysis of Severe VKC

Gender and age were not associated with severe limbal VKC ( 50% limbal involvement with papillae; Table 1). Children with 3 years history of itching were twice as likely to have severe limbal VKC than children with milder symptoms (OR, 2.06; 95% CI, 1.123.81; P 0.018). Tables 2 and 3 show the distribution of symptoms and signs of VKC by severity. Children with severe limbal VKC had signicantly more Trantas dots (P 0.001) and conjunctival pigmentation (P 0.001) than those less severely affected.

School Attendance
More than one-third (36.4%) of children with VKC had missed school for 1 day for an ocular reason in the last 3 months (Table 4). Ocular reasons for missing school were ocular itching, stinging, and photophobia. However, poor vision was not a reported reason. School nonattendance for an ocular reason during the last 3 months

Symptoms
Distribution of the 5 key symptoms of VKC is shown in Table 2. The most frequently reported symptoms were ocular itching, followed by stinging, tearing, photophobia, and discharge. Almost

Table 1. Characteristics of Children with Vernal Keratoconjunctivitis by Level of Severity

Mild VKC n Age groups (yrs) 810 1112 1314 Gender Boys Girls 34 25 23 50 32 % 41.5 30.5 28.0 61.0 39.0 Severe VKC* n 20 9 10 28 11 % 51.3 23.1 25.6 71.8 28.2 n 54 34 33 78 43 Total % 44.6 28.1 27.3 0.1 64.5 35.5 P 0.319

n 121. VKC vernal keratoconjunctivitis. *Dened as 6 clock-hours of limbus involved with papillae.

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Table 2. Distribution of Symptoms among Children with Vernal Keratoconjunctivitis by Level of Severity
Mild VKC n Ocular itch No desire to rub the eyes Once a week desire to rub the eyes Daily desire to rub the eyes Constant desire to rub the eyes Tearing None Wet eyes, but no tears on face Tears on face (intermittently or constant) Stinging sensation None Once a week Daily (intermittently) Daily (constant) Discharge None Small amount At least moderate amount upon awakening Photophobia None Squeezing in bright weather Squeezing even in dark weather Causing the child to stay indoors or to close the eyes most of the times 18 20 28 16 26 42 14 26 35 14 7 52 16 14 32 38 9 3 % 22.0 24.4 34.1 19.5 31.7 51.2 17.1 31.7 42.7 17.1 8.5 63.4 19.5 17.1 39.0 46.3 11.0 3.7 Severe VKC* n 2 7 17 13 10 21 8 7 15 10 7 20 6 13 10 20 5 4 % 5.1 18.0 43.6 33.3 25.6 53.9 20.5 18.0 38.5 25.6 17.9 51.3 15.4 33.3 25.6 51.3 12.8 10.3 n 20 27 45 29 36 63 22 33 50 24 14 72 22 27 42 58 14 7 Total % 16.5 22.3 37.2 24.0 29.8 52.0 18.2 27.3 41.3 19.8 11.6 59.5 18.2 22.3 34.7 47.9 11.6 5.8

VKC vernal keratoconjunctivitis. n 121. *Dened as 6 clock-hours of limbus involved with papillae.

was 5 times more likely to happen among children with VKC (n 44; 36.4%) than those not affected (n 297, 10.2%; OR, 5.04; 95% CI, 3.40 7.47; P 0.001). Children with constant ocular itching (OR, 2.33; 95% CI, 1.27 4.27; P 0.005) and itching for 3 years (OR, 3.71; 95% CI, 1.96 7.01; P 0.001) were signicantly more likely to have missed school than those with a purely seasonal pattern of disease or a shorter duration of symptoms. Although the severity of VKC did not affect school attendance in general (Table 4), children with severe VKC were nearly 7 times more likely to have missed 1 week of school in the previous 3 months than less affected children (OR, 6.75; 95% CI, 1.74 26.23; P 0.001). There was no signicant difference between children with VKC and controls for repeating school years once or twice (n 84 [69.4%] and n 2161 [74.1%], respectively; P 0.25) or having ever dropped out of school (n 2 [1.7%] and n 37 [1.3%], respectively; P 0.72).

services but the difference was not signicant (OR, 1.74; 95% CI, 0.973.13; P 0.061). However, children from prosperous families were almost twice as likely to have sought medical care after adjusting for level of education (OR, 1.85; 95% CI, 1.28 2.66; P 0.001). There were no urban/rural differences in seeking appropriate eye care (P 0.3).

Discussion
Vernal keratoconjunctivitis is a common eye disease in tropical countries, but the majority of studies have been facility based, which are prone to selection bias, because children who are poor and from remote areas are less likely to attend eye departments that are located in urban areas. In a nested population-based case-control study involving primary school children in Rwanda (Central Africa), we conrmed that VKC is more prevalent in hot dry regions and among boys, and is associated with higher economic status.9 A role for parasites in the pathogenesis of VKC has also been reported,1315 but we did not nd such an association, suggesting that the effect of higher economic status on VKC does not act through differences in parasitic intestinal load. Hospitalbased studies undertaken in Europe, Asia, and Africa give conicting results in relation to VKC and atopy (asthma, eczema)8,14,16,17: Our study found that asthma but not eczema was associated with VKC in Rwanda.9 This article is a continuation of this population-based study, and is to the best of

Seeking Medical Care

Fewer than half (n 54, 44.6%) of the children with VKC had sought medical eye care, and of those attending medical services, only 16.7% (n 9) had done this at least twice in the previous 12 months. Only 2 children had taken eye drops in the 3 months before the study. Children with VKC were 7 times more likely to have sought eye care (n 54; 44.6%) than children without the disease (n 278 [9.5%]; OR, 7.65; 95% CI, 5.19 11.29; P 0.001). Children with severe VKC (Table 4) had accessed medical services twice as frequently as those with milder disease (OR, 2.36; 95% CI, 1.35 4.15; P 0.002). Children whose parents were better educated were more likely to have accessed

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Table 3. Signs among Children with Vernal Keratoconjunctivitis by Level of Severity*
Mild VKC Sign Bulbar hyperemia (stage) 0 1 2 or 3 Tarsal plate papillae (stage) 0 1 2 3 Limbal pigmentation (stage) 1 2 3 Limbal follicles (clock-hours) None 1 but 6 6 Conjunctivalization of cornea present Subtarsal scarring present Trantas dots present Shield ulcer present Pseudogerontoxon present Astigmatism 2 diopters present Keratoconus present Cataract present Pseudomembranes present n 38 42 2 33 34 10 2 29 49 3 1 81 0 0 3 2 1 1 5 1 0 0 % 46.3 51.2 2.5 41.8 43.0 12.7 2.5 35.8 60.5 3.7 1.2 98.8 0 0 3.7 2.4 1.3 1.2 6.3 1.2 0 0 n 3 30 6 10 17 10 0 5 25 9 0 0 39 3 5 9 0 3 7 1 1 1 Severe VKC* % 7.7 76.9 15.4 27.0 46.0 27.0 0 12.8 64.1 23.1 0.0 0.0 100.0 7.7 12.8 23.7 0 7.9 20.6 2.6 2.6 2.6 n 41 72 8 43 51 20 2 34 74 12 1 81 39 3 8 11 1 4 12 2 1 1 Total % 33.9 59.5 6.6 5 37.1 44.0 17.2 1.7 1 28.3 61.7 10.0 0 0.8 66.9 32.2 2.5 6.6 9.2 0.8 3.4 9.9 1.7 0.8 0.8 Missing 0

0 0 1 3 2 7 0 0 0

VKC vernal keratoconjunctivitis. n 121. *Dened as 6 clock-hours of limbus involved with papillae.

our knowledge the rst to report the clinical presentation of VKC in an African population. In a large study of the symptoms and signs of VKC from Chad and Djibouti, participants were recruited from both

population-based sources as well as hospital clinics.13 Because we included children who had dropped out of school, we think our results accurately represent the general child population of Rwanda. Although sampling of school chil-

Table 4. School Attendance and Health-Seeking Behavior of Children with Vernal Keratoconjunctivitis by Level of Severity
Mild VKC n Missed school days for eye problem in the last 3 months None 1 week 1 week Have to repeat school years once or twice Dropped out of school Consulted an eye service Never A local health center A general hospital or mobile clinic A specialized eye unit Ever treated by traditional healer 53 27 2 57 2 51 14 6 11 13 % 64.6 32.9 2.5 69.5 2.4 62.2 17.1 7.3 13.4 15.9 n 24 10 5 27 0 16 11 6 6 6 Severe VKC* % 61.5 25.7 12.8 69.2 0 41.0 28.2 15.4 15.4 15.4 n 77 37 7 84 2 67 25 12 17 19 Total % 63.6 30.6 5.8 69.4 1.7 55.4 20.7 9.9 14.0 15.7 P 0.64

0.001 0.965 0.164 0.002

0.925

VKC vernal keratoconjunctivitis. n 121. *Dened as 6 clock-hours of limbus involved with papillae.

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their worst affected eye, we found a much lower percentage in our population-based school survey. This is likely because the current study is population based and so reduces selection bias. However, the incidence of mild corneal complications could have been underestimated in our study because uorescein staining of the cornea was not routinely used. Videokeratography is a more sensitive method for detecting keratoconus and the use of this technique would probably have increased the number detected.22,26 Longterm follow-up of our patients with VKC, including monitoring of their astigmatism, would be of interest because a previous study with long-term follow-up documented a permanent reduction in visual acuity in 6% of patients.21 We have demonstrated that there is an effect of severe VKC on school attendance in Africa. However, because we conducted the studies at the end of the long dry season when VKC was at its peak, we probably measured the maximum impact on school attendance. It may be that VKC does not result in the loss of as much schooling throughout the year. Parameters indicating constant or chronic VKC were associated with the amount of school nonattendance, but severity of VKC did not affect all levels of the school attendance equally, suggesting that school nonattendance is common in this population. This issue could be investigated further by using a control group without VKC matched for age and gender. Repeating school years is apparently common in primary schools in Rwanda, and any inuence of VKC on this could have been masked by other causes. The strength of this study is that it presents the prevalence and the unmet need for diagnosis and treatment of VKC in this African community. Despite the morbidity associated with VKC, the majority (55.4%) of children with VKC in this study had not received medical attention, but this is better than the 90% without medical care reported from Djibouti in 1986.13 Although we did not have detailed information on the treatment being used by children identied with VKC in this study, the treatment options in Rwandese health centers and hospitals are limited to topical corticosteroids, chromoglycate, and occasionally a supratarsal injection of corticosteroid. Additional efforts are needed to increase the proportion of children with VKC who receive appropriate eye care. This could be achieved by providing training for staff in eye care facilities for the diagnosis and treatment of VKC, and possibly by organizing mobile clinics to visit schools. At the same time, although a public health strategy should focus on the supervised use of corticosteroids in the management of this disease balanced against the risk of complications such as cataract, glaucoma, and corneal infection,8 safer alternatives may be topical cyclosporine27 or tacrolimus.28 In conclusion, this study of school children in Rwanda supports other ndings that limbal VKC is the predominant form of the disease in this region. Although VKC caused considerable loss of schooling, it was rarely resulted in permanent loss of vision. Long-term follow-up of this cohort would be required to ascertain the overall risk of sight-threatening complications. The majority of children with VKC had not sought medical attention for their eye condition. This study emphasizes the need for better case identication and treatment in the African community and adds to the argument for better primary eye care, including access to safe topical medications.

dren was based on family names, family cluster bias is unlikely because family names are not inherited in Rwanda. The study was undertaken during the second half of the long dry season when we believe most children with VKC in this region would have had active disease. We used standard photographs to enhance observer agreement for classication of disease severity. Although ocular itching is the characteristic symptom of ocular allergy, it was not uniformly reported in our series, which may be because it can be difcult to assess symptoms in young children.13,14 In Europe and Asia, exacerbations of VKC generally follow a seasonal pattern, but this is not always the case in Africa, suggesting different risk factors and exposures.7,8,18,19 Our results are consistent with other series from Africa that report seasonal variation in severity in up to 40% of patients with VKC.1,5,14 Our study conrms that the limbal form of VKC predominates in central and southern Africa,5 although there is some intraregional variation.13,14,19 However, the palpebral form was reported to be the most frequent presentation in the Democratic Republic of Congo and Nigeria, ranging from 58% to 83%, which is similar to the distribution of the VKC subtypes in Europe and the Americas.7,20 22 In addition, differences in the prevalence of limbal and palpebral VKC subtypes have been observed between different races in countries with a heterogeneous population like the United Kingdom and South Africa, suggesting that genetic factors are more important than environment in determining the expression of the disease.5,16 One of the most striking signs of limbal VKC in black children is hyperpigmentation of the conjunctiva in the interpalpebral zone. Hospital-based case series have reported this sign to be more common in young children with VKC,1,14 not being related to patient symptoms or signs of limbal disease.23 However, we found the opposite: Patients with severe limbal VKC had signicantly more bulbar pigmentation than less severely affected children, although there was no relationship between increased bulbar pigmentation and age. Trantas dots are present in up to 46% of patients in hospital-based case series,14 and tend to be more common in severe limbal VKC, which is consistent with our study.13 In tropical regions, corneal complications develop in 7% to 50% of patients with VKC presenting to a hospital facility,5,8,13,14,24 and these can be caused by 2 different mechanisms. Particularly in Asia, where there is usually a marked palpebral component to the disease, the close apposition of the inamed conjunctiva of the upper lid and the corneal surface is associated with a greater risk of punctate epithelial keratopathy, ulceration and sight threatening vernal plaque.16 In sub-Saharan Africa, however, severe untreated limbal VKC can lead to destruction of the limbal palisades with conjunctivalization of the peripheral cornea, stem cell deciency, pseudogerontoxon, plaque, and stromal melt.25 Because of these corneal changes, VKC is a potentially blinding condition in developing countries. Although some hospital-based case series of VKC report that between 21% and 34% of patients are blind or visually impaired, respectively,3,8 and although 7% of patients with VKC attending our Rwandan eye clinics had low vision in

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References
1. Diallo JS. Tropical endemic limboconjunctivitis [in English, French]. Rev Int Trach Pathol Ocul Trop Subtrop 1976;53: 71 80. 2. Ono SJ, Abelson MB. Allergic conjunctivitis: update on pathophysiology and prospects for future treatment. J Allergy Clin Immunol 2005;115:118 22. 3. Tabbara KF. Ocular complications of vernal keratoconjunctivitis. Can J Ophthalmol 1999;34:88 92. 4. Cameron JA. Shield ulcers and plaques of the cornea in vernal keratoconjunctivitis. Ophthalmology 1995;102:98593. 5. Dahan E, Appel R. Vernal keratoconjunctivitis in the black child and its response to therapy. Br J Ophthalmol 1983;67: 688 92. 6. BenEzra D, Peer J, Brodsky M, Cohen E. Cyclosporine eyedrops for the treatment of severe vernal keratoconjunctivitis. Am J Ophthalmol 1986;101:278 82. 7. Chenge B, Makumyamviri AM, Kaimbo wa Kaimbo D. Tropical endemic limbo-conjunctivitis in Lbumbashi, Democratic Republic of the Congo [in French]. Bull Soc Belge Ophthalmol 2003;290:9 16. 8. Khan MD, Kundi N, Saeed N, et al. A study of 530 cases of vernal conjunctivitis from the North West Frontier Province of Pakistan. Pak J Ophthalmol 1986;2:111 4. 9. De Smedt S, Nkurikiye J, Fonteyne Y, et al. Vernal keratoconjunctivitis in school children in Rwanda and its association with socio-economic status: a population-based survey. Am J Trop Med Hyg 2011;85:7117. 10. Munyakazi A, Ntagaramba JF. Atlas of Rwanda. French ed. Oxford, UK: MacMillan; 2005. 11. Akpek EK, Dart JK, Watson S, et al. A randomized trial of topical cyclosporin 0.05% in topical steroidresistant atopic keratoconjunctivitis. Ophthalmology 2004;111:476 82. 12. World Health Organization. ICF: International Classication of Functioning, Disability and Health. Geneva: World Health Organization; 2001:623. 13. Resnikoff S, Cornand G, Filliard G, Hugard L. Limbal vernal keratoconjunctivitis in the tropics [in English, French]. Rev Int Trach Pathol Ocul Trop Subtrop Sante Publique 1988;65:2172. 14. Sandford-Smith JH. Vernal eye disease in Northern Nigeria. Trop Geogr Med 1979;31:321 8.

15. Ajaiyeoba A. Vernal keratoconjunctivitis and intestinal parasitic infestations in black children. J Natl Med Assoc 2005; 97:1529 32. 16. Tuft SJ, Dart JK, Kemeny M. Limbal vernal keratoconjunctivitis: clinical characteristics and immunoglobulin E expression compared with palpebral vernal. Eye (Lond) 1989;3:420 7. 17. Neumann E, Gutmann MJ, Blumenkrantz N, Michaelson IC. A review of four hundred cases of vernal conjunctivitis. Am J Ophthalmol 1959;47:166 72. 18. Pucci N, Novembre E, Lombardi E, et al. Long eyelashes in a case series of 93 children with vernal keratoconjunctivitis [report online]. Pediatrics 2005;115:e86 91. Available at: http://pediatrics.aappublications.org/content/115/1/e86.long. Accessed March 10, 2012. 19. Everaerts MC, Doutetien C. Chronic tropical endemic limboconjunctivitis (TELC) in southern Benin: epidemiological and meteorological data [in French]. Rev Int Trach Pathol Ocul Trop Subtrop Sante Publique 1993;70:199 214. 20. Ukponmwan CU. Vernal keratoconjunctivitis in Nigerians: 109 consecutive cases. Trop Doct 2003;33:2425. 21. Bonini S, Bonini S, Lambiase A, et al. Vernal keratoconjunctivitis revisited: a case series of 195 patients with long-term followup. Ophthalmology 2000;107:1157 63. 22. Dantas PE, Alves MR, Nishiwaki-Dantas MC. Topographic corneal changes in patients with vernal keratoconjunctivitis. Arq Bras Oftalmol 2005;68:593 8. 23. Rao SK, Meenakshi S, Srinivasan B, Baluswamy S. Perilimbal bulbar conjunctival pigmentation in vernal conjunctivitis: prospective evaluation of a new clinical sign in an Indian population. Cornea 2004;23:356 9. 24. Tuft SJ, Cree IA, Woods M, Yorston D. Limbal vernal keratoconjunctivitis in the tropics. Ophthalmology 1998;105: 1489 93. 25. Buckley RJ. Vernal keratopathy and its management. Trans Ophthalm Soc UK 1981;101:234 8. 26. Totan Y, Hepsen IF, Ceki O, et al. Incidence of keratoconus in subjects with vernal keratoconjunctivitis: a videokeratographic study. Ophthalmology 2001;108:824 7. 27. De Smedt S, Nkurikiye J, Fonteyne Y, et al. Topical ciclosporin in the treatment of vernal keratoconjunctivitis in Rwanda, Central Africa: a prospective, randomised, doublemasked, controlled clinical trial. Br J Ophthalmol 2012;96: 323 8. 28. Tam PM, Young AL, Cheng LL, Lam PT. Topical tacrolimus 0.03% monotherapy for vernal keratoconjunctivitis case series [letter]. Br J Ophthalmol 2010;94:1405 6.

Footnotes and Financial Disclosures

Originally received: December 8, 2011. Final revision: March 22, 2012. Accepted: March 22, 2012. Available online: June 7, 2012.
1 2 3 5

Ophthalmology department, Ghent University Hospital, Belgium.

Manuscript no. 2011-1761.

Ophthalmology Department, Kabgayi Hospital, Muhanga, Rwanda. Ophthalmology Department, King Faisal Hospital, Kigali, Rwanda.

Corneal & External Disease Service, Moorelds Eye Hospital NHS Foundation Trust, London, UK. International Centre for Eye Health, London School of Hygiene and Tropical Medicine, London, UK.

Financial Disclosure(s): The authors have no proprietary or commercial interest in any of the materials discussed in this article. This study was possible thanks to nancial support of FRO (Belgian Funds for Research in Ophthalmology), Light for the World Belgium and CBM-International. Stephen Tuft is supported by a grant from the NIHR Biomedical Research Centre for Ophthalmology, Moorelds Eye Hospital, London, UK. Correspondence: Stefan K. De Smedt, MD, Leopoldstraat 36, 2800 Mechelen, Belgium. E-mail: dr.stefan.desmedt@gmail.com.

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