J Community Health DOI 10.1007/s10900-014-9878-y
ORIGINAL PAPER
Prevalence and Profile of Ophthalmic Disorders in Oculocutaneous Albinism: A Field Report from South-Eastern Nigeria N. N. Udeh • B. I. Eze • S. N. Onwubiko • O. C. Arinze • E. N. Onwasigwe • R. E. Umeh
Ó Springer Science+Business Media New York 2014
Abstract To assess the burden and spectrum of refractive and non-refractive ophthalmic disorders in south-eastern Nigerians with oculocutaneous albinism. In a populationbased survey in Enugu state, between August, 2011 and January, 2012, albinos were identified using the database of the Enugu state’s Albino Foundation, and mass mediabased mobilisation. The participants were enrolled at the Eye Clinics of the University of Nigeria Teaching Hospital and Enugu State University of Science and Technology Teaching Hospital using a defined protocol. Relevant socio-demographic and clinical data were obtained from each participant. Descriptive and comparative statistics were performed. Statistical significance was indicated by p \ 0.05. The participants (n = 153; males, 70) were aged 23.5 ? 10.4 SD years (range 6–60 years). Both refractive and non-refractive disorders were present in all participants. Non-refractive disorders comprised nystagmus, foveal hypoplasia, hypopigmented fundi and prominent choroidal vessels in 100.0 % participants; and strabismus in 16.3 % participants. Refractive disorders comprised astigmatism -73.2 % eyes, myopia -23.9 % and hypermetropia 2.9 %. Spherical refractive errors ranged from 14.00 DS to ?8.00 DS while astigmatic errors ranged from All the listed authors participated in data collection, analysis and interpretation, contributed significantly to the intellectual content of the manuscript, and approved the final version for submission. N. N. Udeh B. I. Eze (&) S. N. Onwubiko E. N. Onwasigwe R. E. Umeh Department of Ophthalmology, University of Nigeria Teaching Hospital, Ituku-Ozalla, PMB 01139, Enugu, Nigeria e-mail: [email protected] O. C. Arinze Department of Ophthalmology, Federal Teaching Hospital, Abakaliki, Nigeria
-6.00 DC to ?6 DC. Mixed refractive and non-refractive disorder i.e. presenting visual impairment was present in 100.0 % participants. Overall, refractive error was associated with non-possession of tertiary education (OR 0.61; 95 % CI 0.38–0.96; p = 0.0374). There is high prevalence of refractive, non-refractive and mixed ophthalmic disorders among albinos in south-eastern Nigeria. This underscores the need for tailored provision of resources to address their eye care needs, and creation of needs awareness amongst them. Keywords Albinism Refractive Non-refractive Disorder Nigeria
Introduction Albinism is an inherited autosomal recessive disorder of melanin synthesis characterised by generalised (oculocutaneous albinism, OCA) or eye-specific (ocular albinism, OA) hypopigmentation of melanin-containing tissues in the body [1]. The defect in melanin synthesis could be total— tyrosinase negative or partial-tyrosinase positive. Based on underlying specific gene mutation responsible for various phenotypic variants, a genetic dimension has been added to classification of albinism [2] e.g. mutations of tyrosinase gene (TYR), tyrosinase-related protein gene (TYRP1), MATP gene, Melanosomal G protein-coupled receptor gene and the P gene. Albinism, irrespective of clinical type, has a worldwide prevalence of 1/3900–1/15,000 [1, 3–5] In Nigeria, although all the clinical variants exist, with an prevalence of 1/1,100, the most common variant is OCA4 [6]. Melanin is critical for the normal development of human eyes inutero [7] and its deficiency causes major cellular,
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anatomic and functional defects during ocular development, especially visual development [7]. Visual impairment requiring spectacle or low vision aids correction is common in albinos [8–11], however, in an appreciable proportion of cases, vision remains sub-normal even with optimal optical correction [9–11]. Previous reports have found variations in prevalence, profile, and severity of refractive errors among various albino populations. The prevalent refractive errors reported include myopia— 9.5–90 % [5, 10, 12], hypermetropia—2.4–30.8 % [10, 11, 13, 14], and astigmatism—80–100 % [10–12, 15]. The common non-reactive ophthalmic features in albinos include: nystagmus, strabismus, diaphenous iris, foveal hypoplasia and prominent choroidal vessels [10, 11, 13, 14, 17–20]. Mixed refractive/non-refractive disorder, represented by visual impairment for far or near, is very common in albinos, with reported prevalences frequently higher than 50 % [13, 14, 17–20]. To mitigate the functional handicaps inherent in albinism-associated ophthalmic disorders, reliable populationbased data on these disorders is indispensable. To achieve this, unrestricted access to vision care is a mandatory prerequisite [19]. Especially in sub-Saharan Africa, there is paucity of data on the prevalence, profile and severity of refractive and non-refractive ophthalmic disorders among people living with albinism. Consequently, the investigators embarked on a population-based survey of albinos in south-eastern Nigeria to assess the prevalence and profile of refractive, non-refractive and mixed ophthalmic disorders among albinos south-eastern Nigeria. The findings will provide the evidence base, for eye care planners and providers, to enable rational resource allocation during planning for eye care in this at-risk but underserved population. Additionally, it will introduce or strengthen the rationale for eye care needs awareness creation among albinos in the study area and under similar settings elsewhere.
Methods Background Enugu State is located in Nigeria’s south-east geo-political zone. Other States in the zone include Abia, Imo, Anambra and Ebonyi. It is sub-divided into 17 administrative subunits or Local Government Areas (LGAs). With a population of 3,267,837 (males 1,596,042; females 1,671,795), [21] it lies in the tropical rainforest climatic belt, with patches of derived savannah, and has two seasons of the year, rainy and dry seasons. In Enugu state, there are two major public tertiary eye care facilities i.e. the Eye clinics of the University of Nigeria Teaching Hospital (UNTH),
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Ituku-Ozalla, and Enugu State University of Science and Technology Teaching Hospital (ESUTH) Parklane, Enugu. Eye care services are also provided by other public, mission and privately-owned eye care facilities, which are located mainly in the state’s capital, Enugu urban. This study, a descriptive population-based cross-sectional survey of people with albinism, was conducted in Enugu state, south-eastern Nigeria, between August 2011 and January 2012. Inclusion Criteria Persons diagnosed with oculocutaneous albinism, who gave direct or surrogate (for minors) voluntarily consents to participate in the study. Ethics Prior to commencement of the study, ethics clearance was obtained from UNTH’s and ESUTH’s Medical and Health Research Ethics Committee (Institutional Review Board). Study approval was also obtained from the Albino Foundation, Enugu State Chapter. Sample Size and Sampling A minimum sample size of 138 was assumed based on 90 % prevalence of simple myopia among albinos reported in a previous Nigerian study [5], and an error bound of 5 %. However, all the available 153 eligible enrolees were recruited. Recruitment of Participants The study subjects were recruited with assistance of the Albino Foundation, Enugu State Chapter, and the traditional rulers of the state’s component communities. Additional mobilisation strategies used included repeated announcements in hospitals, schools, churches, major markets, motor parks and the mass media. The announcements contained health messages informing the public of the study and its potential benefits, and specifically directing albinos to report to the Eye Clinics of UNTH and ESUTH, on designated work days and time, for participation in the study. Study Instrument This was a pretested questionnaire/proforma specifically designed for the survey. A pre-test was conducted on 10 randomly selected members of the Enugu State Albino Foundation, and a pilot study carried out thereafter on another 10 participants. Participants in the pretest and pilot were excluded from the final survey.
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Study Procedures Participants’ socio-demographic (age, gender, education, occupation and marital status) data were obtained in an inperson questionnaire-guided interview administered by the researchers. Subsequently, each participant had an initial comprehensive ophthalmic examination including unaided (presenting) monocular distance visual acuity (Vision 2020 Low Vision Resource Centre [LVRC] LogMAR test chart) at 4 M and near acuity (Vision 2020 LVRC LogMAR Test Card for near) at 40 cm for the right and then the left eye. Where applicable, the visual acuity tests were repeated with participant’s corrective spectacle. This was followed by pentorch (Keeler Instruments Ltd, London, UK) examination of the ocular anterior segment, direct ophthalmoscopy (Welch Allyn Inc., Skaneateles Falls, NY, USA), binocular indirect ophthalmoscopy (Keeler Instruments Ltd, London, UK), slit lamp biomicroscopy (Topcon Inc, Tokyo, Japan), slit lamp-assisted ?78D (Volk Optical, London, UK) fundus examination and fundus photography (Optoangiocam 9.1.4, Opto, South Africa). Subsequently, each participants had an objective refraction using an autorefractor (Huvitz CR 7000, Seoul, South Korea). This was subjectively refined using trial lenses and frame, both contained in a trial lens box (Keeler Instruments Ltd, London, UK). Jackson’s cross–cylinder (Keeler Instruments Ltd, London, UK), Duochrome and Worths Four Dot chart (Keeler Instruments Ltd, London, UK) were used as needed. Where cycloplegic refraction is indicated, automated objective cycloplegic refraction, using the auto-refractor (Huvitz CR 7000, Seoul, South Korea) was performed after satisfactory cycloplegia using 3-day tds regimen of Gutt Atropine (Ashford laboratories Ltd, Macau, China), and subjective post-cycloplegia test 3 weeks afterwards. The best corrected visual acuity (BCVA) and the lens power that achieved this (spectacle prescription) were both recorded. If the BCVA for distance, after subjective refraction, was worse than LogMAR 0.5 (6/18), the subject was further tested using a distance low vision device. (Vision 2020 Low Vision Resource Centre [LVRC] telescopes of 39, 49, 69 or 89—magnification. The BCVA achieved was recorded in each case. If the presenting near VA was worse than LogMAR 0.4 (equivalent of N5), near vision was corrected using trial frames and lenses. If the best corrected near visual acuity (BCNVA) was worse than LogMAR 0.4 (equivalent of N8 i.e. newspaper print size), after the near correction, the participant was subjected to low vision assessment for near vision using high power plus lenses from the trial lens box, or magnifiers-hand held (39, 49), stand (39, 79, 99), bar (1.59) and telescopes (39, 49, 69, 89) (Vision 2020 Low Vision Resource Centre [LVRC]). The unaided and
BCNVA, and the power of the lens used to achieve the BCNVA were recorded. Data Analysis Data was entered into and analysed using the Statistical Package for Social Sciences (SPSS) computer software, version 18.0. (SPSS Inc, Chicago, Illinios, USA). Descriptive statistics yielded frequencies, percentages and proportions; For inter-group comparisons to test for significance of observed differences, the student t test was used for continuous while the Chi square test was used for categorical variables. For all comparisons, a p \ 0.05 with the associated odds ratios and 95 % confidence intervals were considered statistically significant.
Results Socio-Demographic Characteristics The participants (n = 153), comprised 83 (54.2 %) females and 70 (45.8 %) males (sex ratio: M:F = 1:1.1) aged 23.4 ± 10.4 SD year (range 6–60 years) with a modal Table 1 Socio-demographic characteristics of participants Characteristic
n (%), n = 153
Age (years) 1–10
20 (13.0)
11–20 21–30
38 (24.8) 70 (45.8)
31–40
16 (10.5)
41–50
5 (3.2)
51–60
4 (2.6)
Sex Male
70 (45.8)
Female
83 (54.2)
Marital status Single Married
140 (91.5) 13 (8.5)
Educational status None Primary
2 (1.3) 28 (18.3)
Secondary
39 (25.5)
Tertiary
84 (54.9)
Occupation Unemployed/Students Civil servant
124 (81.0) 15 (9.8)
Trading
7 (4.6)
Artisan
4 (2.6)
Retired
1 (0.7)
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age group of 21–30 years. The majorities of the participants had tertiary education—84 (54.9 %) were unemployed/students—124 (81.0 %) and were single—140 (91.5 %). Table 1 show their age, sex distribution and their socio-economic profile. Clinical Profile All-153 (100.0 %) the participants had sub-normal presenting distant and near visual acuities. At presentation, the majorities of participants had moderate visual impairment for unaided distance—217 (70.9 %) and near—254 (83.0 %) vision. Table 2 shows the distribution of presenting mono-ocular visual acuities in 306 eyes of 153 participants.
Table 2 Type-specific distribution of refractive errors in 306 eyes of the 153 participants Type of refractive error Myopia Hypermetropia
73 (23.9) 9 (2.9) 35 (11.4)
Compound myopic astigmatism
79 (25.8)
Compound hypermetropic astigmatism
32 (10.5)
Mixed astigmatism
78 (25.5)
Total (%)
Fig. 1 Profile of non-refractive and miscellaneous disorders in 306 eyes of 153 participants
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All-306 (100.0 %) ’ eyes of the participants had nystagmus, hypopigmented fundus, foveal hypoplasia and prominent choroidal vessels. Of the 25/153 (16.4 %) participants with strabismus, 9/25 (36.0 %) had esotropia while 16(64.0 %) had exotropia. The participants’ profile of non-refractive abnormalities is shown in Fig. 1. Refractive Disorders The presence of refractive error was universal in all -306 (100.0 %) eyes. Astigmatism, present in 224 (73.2 %) and most frequently of the compound myopic type-79/224 (35.3 %, was the most common error while hypermetropia-9/ 306 (2.9 %) was the least common. The range of spherical refractive errors was -14.00 DS to ?8.00 DS, while astigmatic errors ranged from -6.00 DC to ?6 DC. Table 2 reports the profile of refractive errors among the participants.
n (%), n = 306 eyes
Astigmatism Simple astigmatism
Non-refractive Disorders
306 (100.0)
Mixed Refractive and Non-refractive Disorders A presenting visual impairment for far and near, representing combined refractive and non-refractive etiologies, was present in all-306 (100.0 %) eyes. Moderate visual impairment was the most prevalent category of visual impairment, accounting for 217 (70.9 %) eyes with impaired distance vision and 254 (83.0 %) eyes with impaired near vision (Table 3).
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Miscellaneous Non-albinism-Related Disorders
Discussion
These were seen in minority of participants and comprised pterygium, pingueculum and ptosis (Fig. 1). Overall, presence of refractive error was significantly associated with non-possession of tertiary education (OR 0.61; 95 % CI 0.38–0.96; p = 0.0374). However, typespecific associations with age and gender were not statistically significant (all ps [ 0.05) (Table 4).
The majorities of the participants were single females aged 30 years or younger, who possessed tertiary education and were frequently students or unemployed. A similar age distribution was observed in Europe [22], Tanzania [3], South African [23] and Nigeria [24] in studies among albinos. The higher tendency of younger people to seek for medical solution to their health or visual disability may account for this [25]. The observed educational profile, consistent with the participants’ age distribution, probably reflects the reported normal reading ability [22, 26] and intellectual development among persons with OCA [18]. However, this challenges the findings by Okoro et al [5]. that myopia, a common refractive anomaly in albinism, is associated with intellectual impairment Therefore, the present data do not support the need for creating special learning environment for albinos. The predominance of unemployed participants is consistent with job-related stigmatisation of albinos reported by Hong et al. [3] and Ezillo [27] This probably reflects the public’s poor knowledge and attitudes on albinism [3]. The investigators recommend public awareness creation on albinism to mitigate the public’s poor knowledge and attitudinal disposition. Astigmatism, frequently of the compound myopic and mixed types, was the most prevalent refractive
Table 3 Categories of presenting visual acuities in 306 eyes of 153 participants Presenting visual acuity
n (%), n = 306
Distance visual acuity (DVA) Normal Vision (DVA C 6/12)
0 (0.0)
Mild visual impairment (DVA \ 6/12–6/18)
1 (0.3)
Moderate visual impairment (DVA \ 6/18–6/60)
217 (70.9)
Severe visual impairment (DVA \ 6/60–3/60)
56 (18.3)
Blindness (DVA \ 3/60)
32 (10.5)
Near visual acuity (NVA) Normal vision (CN6)
0 (0.0)
Mild visual impairment (N8–N10)
12 (4.0)
Moderate visual impairment (N12–N24)
254 (83.0)
Severe visual impairment (\N36)
39 (12.7)
Blindness
Table 4 Association between participants’ demographics and types of refractive error
1 (0.3)
Refractive error
Percent with refractive error
Percent without refractive error
Odds ratio (95 % CI)
p value (Fisher’s exact test)
32 5
87 29
2.13 (0.76–5.99) Reference
0.1765
Male
29
111
0.72 (0.42–1.24)
0.2817
Female
44
122
Ref
Myopia Age (years) \30 C30 Gender
Hypermetropia Age (years) \30
3
116
0.47 (0.08–2.89)
C30
2
36
Ref
0.5952
Gender Male
5
135
1.5 (0.39–5.69)
Female
4
162
Ref
\30
84
35
0.62 (0.25–1.56)
C30
27
7
Ref
106
34
1.27 (0.76–2.12)
118
48
Ref
0.7368
Astigmatism Age (years)
Gender Male Female
0.3684
0.3685
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abnormality followed by myopia and hypermetropia. The dominance of astigmatic refractive error in the present survey is consistent with previous reports [10– 13, 28] but differs from a preponderance of simple myopia reported by Okoro [5] in another Nigerian cohort 20 years earlier, and Wildsoet et al’s [13] series wherein hypermetropia was more frequent than myopia. While the observed high prevalence of refractive disorders is attributable to arrested/impaired emmetropisation in albinism [13], between-survey differences in prevalence and distribution of refractive disorders may be attributed to differences in accuracies of diagnostic facilities i.e. manual versus automated refraction. The ranges of astigmatic and spherical refractive errors in the present study agree with those reported in previous studies [9, 10, 13, 14]. The present data underscores the need for provision and unrestricted access to facilities for accurate diagnosis and optimal correction of albinism-associated refractive disorders. Additionally, albino-specific barriers to uptake of these refraction services should be identified and overcome [16]. Of the non-refractive disorders, nystagmus, foveal hypoplasia, hypopigmented fundus and prominent choroidal vessels were universal findings in the study cohort while strabismus was the least common. All participants had nystagmus in contrast to a previous study by Wolf et al. [19] where most of the participants (57.9 %) in that study had obvious nystagmus. The difference in criteria for nystagmus definition between the present study and Wolf et al.’s may account for this discordance. While the present study defined nystagmus as any involuntary to and fro eye movement, whether obvious or detected only at the slit lamp examination, Wolf et al. [19] categorised their subjects’ nystagmus into ‘absent or minimum ’ (barely detectable on slit lamp examination) and obvious nystagmus. The finding of foveal hypoplasia in all participants is similar to other studies [5, 14, 30]. This may be accounted for by the common aetiology of all forms of albinism resulting in absent or varying macular pigment and foveal hypoplasia. Strabismus was found in 8.2 %) of the eyes examined, exotropia being the most common Type. This is comparatively lower than the previously reported prevalence figures which ranged from 27–53 %. [12, 19, 30–32] The differences between surveys in cohorts’ clinical characteristics, particularly nystagmus-predisposing refractive and accommodative disorders might explain the observed differences. In the present report, the higher prevalence of exotropia suggests that delayed refractive correction of optical visual loss probably predisposed to amblyopia and its associated exo-deviation of the eyes. The discordance between the findings of this study and various others underscores the need for uniform case definition criteria while reporting the ophthalmic features of albinism, and holistic reporting of both refractive and non-refractive disorders to
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enable informed/contextual interpretation of study findings. Similarly, presenting visual impairment for far and near, a mixed refractive and non-refractive disorder was present in all participants. This is similar to previous observations [9, 10, 29] but partially agrees with the finding of Kutzbach and associates [17] who had some participants with normal presenting visual acuity. Although the exact cause of visual impairment in people with albinism is unknown, foveal hypoplasia, nystagmus and refractive error have been implicated. Additionally, amblyopia, resulting from delay in refractive correction, might be contributory. This implies that, beyond timely refractive correction, other visual/optical aids to alleviate the visual consequences of these abnormalities should be made widely available and accessible to albinos. Miscellaneous non-albinism-related ophthalmic disorders comprising pterygium, pingueculum, and ptosis were seen in a minority of participants. This finding could not be compared with other related surveys as none reported comparable data. This underscores the need for future investigators to identify and adequately manage co-morbid miscellaneous disorders with potentially adverse visual or ocular health implications.
Conclusion There is high prevalence of refractive, non-refractive and mixed ophthalmic disorders among albinos in Enugu, Nigeria. To alleviate the visual consequences of these disorders, the investigators recommend timely provision of, unrestricted access to, and needs awareness creation among albinos on, appropriate eye care services. Acknowledgments The authors acknowledge the assistance of the Albino Foundation (TAF) Enugu State Chapter, Drs. Oguama Felix, Okeh Ada, Eze Joy N, Ogbonnaya O and Dr. Ama for logistic support. The authors declare no external funding support for this work. Conflict of interest
None declared.
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19. Wolf, B. A., Rubin, S. E., & Kodsi, S. R. (2005). Comparison of clinical findings in pediatric patients with albinism and different amplitudes of nystagmus. Journal of AAPOS, 9, 363–368. 20. Summer, C. G. (2009). Albinism: classification, clinical characteristics and recent findings. Optometry and Vision Science, 86, 659–662. 21. 2006 Population and Housing Census of the Federal Republic of Nigeria. Official Gazette of Federal Republic of Nigeria, 96(2), 2009. 22. Collins, B., & Silver, J. (1990). Recent experiences in management of visual impairment in Albinism. Ophthalmic Genetics, 11(3), 225–228. 23. Kromberg, J. G., Castle, D., Zwane, E. M., & Jenkins, T. (1989). Albinism and skin cancer in Southern Africa. Clinical Genetics, 36, 43–52. 24. King, R. A., Creel, D., Cervenka, J., et al. (1980). Albinism in Nigeria with delineation of new recessive oculocutaneous type. Clinical Genetics, 17, 259–270. 25. Cullinan, T. R. (1977). The epidemiology of visual disability. Studies of visually disabled people in the community. HSRU Report, 28, 136–137. 26. National Organization of Albinism and Hypopigmentation (NOAH). Information for parent and children with Albinism. http://www.albinism.org Accessed December 28, 2010. 27. Ezeilo, B. N. (1989). Psychological aspects of albinism: an exploratory study of Nigerian (Igbo) albino subjects. Social Science and Medicine, 29(9), 1129–1131. 28. Yahalom, C., Tzur, V., Blumenfeld, A., Greifner, G., Eli, D., Rosenmann, A., et al. (2012). Refractive profile in oculocutaneous albinism and its correlation with final visual outcome. British Journal of Ophthalmology, 96(4), 537–539. 29. Watkins, S. (1972). Albinism in Nigeria. Lancet, 1, 203. 30. Merrill, K. S., Lavoie, J. D., King, R. A., & Summers, C. G. (2004). Positive angle kappa in albinism. Journal of AAPOS, 8, 237–239. 31. Merrill, K., Hogue, K., Downes, S., Holleschau, A. M., Kutzbach, B. R., MacDonald, J. T., et al. (2011). Reading acuity in albinism: Evaluation with MNREAD charts. Journal of AAPOS, 15, 29–32. 32. Lee, K. A., King, R. A., & Summers, C. G. (2001). Stereopsis in patients with albinism: clinical correlates. Journal of Pediatric Ophthalmology and Strabismus, 5, 98–104.
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ORIGINAL PAPER
Prevalence and Profile of Ophthalmic Disorders in Oculocutaneous Albinism: A Field Report from South-Eastern Nigeria N. N. Udeh • B. I. Eze • S. N. Onwubiko • O. C. Arinze • E. N. Onwasigwe • R. E. Umeh
Ó Springer Science+Business Media New York 2014
Abstract To assess the burden and spectrum of refractive and non-refractive ophthalmic disorders in south-eastern Nigerians with oculocutaneous albinism. In a populationbased survey in Enugu state, between August, 2011 and January, 2012, albinos were identified using the database of the Enugu state’s Albino Foundation, and mass mediabased mobilisation. The participants were enrolled at the Eye Clinics of the University of Nigeria Teaching Hospital and Enugu State University of Science and Technology Teaching Hospital using a defined protocol. Relevant socio-demographic and clinical data were obtained from each participant. Descriptive and comparative statistics were performed. Statistical significance was indicated by p \ 0.05. The participants (n = 153; males, 70) were aged 23.5 ? 10.4 SD years (range 6–60 years). Both refractive and non-refractive disorders were present in all participants. Non-refractive disorders comprised nystagmus, foveal hypoplasia, hypopigmented fundi and prominent choroidal vessels in 100.0 % participants; and strabismus in 16.3 % participants. Refractive disorders comprised astigmatism -73.2 % eyes, myopia -23.9 % and hypermetropia 2.9 %. Spherical refractive errors ranged from 14.00 DS to ?8.00 DS while astigmatic errors ranged from All the listed authors participated in data collection, analysis and interpretation, contributed significantly to the intellectual content of the manuscript, and approved the final version for submission. N. N. Udeh B. I. Eze (&) S. N. Onwubiko E. N. Onwasigwe R. E. Umeh Department of Ophthalmology, University of Nigeria Teaching Hospital, Ituku-Ozalla, PMB 01139, Enugu, Nigeria e-mail: [email protected] O. C. Arinze Department of Ophthalmology, Federal Teaching Hospital, Abakaliki, Nigeria
-6.00 DC to ?6 DC. Mixed refractive and non-refractive disorder i.e. presenting visual impairment was present in 100.0 % participants. Overall, refractive error was associated with non-possession of tertiary education (OR 0.61; 95 % CI 0.38–0.96; p = 0.0374). There is high prevalence of refractive, non-refractive and mixed ophthalmic disorders among albinos in south-eastern Nigeria. This underscores the need for tailored provision of resources to address their eye care needs, and creation of needs awareness amongst them. Keywords Albinism Refractive Non-refractive Disorder Nigeria
Introduction Albinism is an inherited autosomal recessive disorder of melanin synthesis characterised by generalised (oculocutaneous albinism, OCA) or eye-specific (ocular albinism, OA) hypopigmentation of melanin-containing tissues in the body [1]. The defect in melanin synthesis could be total— tyrosinase negative or partial-tyrosinase positive. Based on underlying specific gene mutation responsible for various phenotypic variants, a genetic dimension has been added to classification of albinism [2] e.g. mutations of tyrosinase gene (TYR), tyrosinase-related protein gene (TYRP1), MATP gene, Melanosomal G protein-coupled receptor gene and the P gene. Albinism, irrespective of clinical type, has a worldwide prevalence of 1/3900–1/15,000 [1, 3–5] In Nigeria, although all the clinical variants exist, with an prevalence of 1/1,100, the most common variant is OCA4 [6]. Melanin is critical for the normal development of human eyes inutero [7] and its deficiency causes major cellular,
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anatomic and functional defects during ocular development, especially visual development [7]. Visual impairment requiring spectacle or low vision aids correction is common in albinos [8–11], however, in an appreciable proportion of cases, vision remains sub-normal even with optimal optical correction [9–11]. Previous reports have found variations in prevalence, profile, and severity of refractive errors among various albino populations. The prevalent refractive errors reported include myopia— 9.5–90 % [5, 10, 12], hypermetropia—2.4–30.8 % [10, 11, 13, 14], and astigmatism—80–100 % [10–12, 15]. The common non-reactive ophthalmic features in albinos include: nystagmus, strabismus, diaphenous iris, foveal hypoplasia and prominent choroidal vessels [10, 11, 13, 14, 17–20]. Mixed refractive/non-refractive disorder, represented by visual impairment for far or near, is very common in albinos, with reported prevalences frequently higher than 50 % [13, 14, 17–20]. To mitigate the functional handicaps inherent in albinism-associated ophthalmic disorders, reliable populationbased data on these disorders is indispensable. To achieve this, unrestricted access to vision care is a mandatory prerequisite [19]. Especially in sub-Saharan Africa, there is paucity of data on the prevalence, profile and severity of refractive and non-refractive ophthalmic disorders among people living with albinism. Consequently, the investigators embarked on a population-based survey of albinos in south-eastern Nigeria to assess the prevalence and profile of refractive, non-refractive and mixed ophthalmic disorders among albinos south-eastern Nigeria. The findings will provide the evidence base, for eye care planners and providers, to enable rational resource allocation during planning for eye care in this at-risk but underserved population. Additionally, it will introduce or strengthen the rationale for eye care needs awareness creation among albinos in the study area and under similar settings elsewhere.
Methods Background Enugu State is located in Nigeria’s south-east geo-political zone. Other States in the zone include Abia, Imo, Anambra and Ebonyi. It is sub-divided into 17 administrative subunits or Local Government Areas (LGAs). With a population of 3,267,837 (males 1,596,042; females 1,671,795), [21] it lies in the tropical rainforest climatic belt, with patches of derived savannah, and has two seasons of the year, rainy and dry seasons. In Enugu state, there are two major public tertiary eye care facilities i.e. the Eye clinics of the University of Nigeria Teaching Hospital (UNTH),
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Ituku-Ozalla, and Enugu State University of Science and Technology Teaching Hospital (ESUTH) Parklane, Enugu. Eye care services are also provided by other public, mission and privately-owned eye care facilities, which are located mainly in the state’s capital, Enugu urban. This study, a descriptive population-based cross-sectional survey of people with albinism, was conducted in Enugu state, south-eastern Nigeria, between August 2011 and January 2012. Inclusion Criteria Persons diagnosed with oculocutaneous albinism, who gave direct or surrogate (for minors) voluntarily consents to participate in the study. Ethics Prior to commencement of the study, ethics clearance was obtained from UNTH’s and ESUTH’s Medical and Health Research Ethics Committee (Institutional Review Board). Study approval was also obtained from the Albino Foundation, Enugu State Chapter. Sample Size and Sampling A minimum sample size of 138 was assumed based on 90 % prevalence of simple myopia among albinos reported in a previous Nigerian study [5], and an error bound of 5 %. However, all the available 153 eligible enrolees were recruited. Recruitment of Participants The study subjects were recruited with assistance of the Albino Foundation, Enugu State Chapter, and the traditional rulers of the state’s component communities. Additional mobilisation strategies used included repeated announcements in hospitals, schools, churches, major markets, motor parks and the mass media. The announcements contained health messages informing the public of the study and its potential benefits, and specifically directing albinos to report to the Eye Clinics of UNTH and ESUTH, on designated work days and time, for participation in the study. Study Instrument This was a pretested questionnaire/proforma specifically designed for the survey. A pre-test was conducted on 10 randomly selected members of the Enugu State Albino Foundation, and a pilot study carried out thereafter on another 10 participants. Participants in the pretest and pilot were excluded from the final survey.
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Study Procedures Participants’ socio-demographic (age, gender, education, occupation and marital status) data were obtained in an inperson questionnaire-guided interview administered by the researchers. Subsequently, each participant had an initial comprehensive ophthalmic examination including unaided (presenting) monocular distance visual acuity (Vision 2020 Low Vision Resource Centre [LVRC] LogMAR test chart) at 4 M and near acuity (Vision 2020 LVRC LogMAR Test Card for near) at 40 cm for the right and then the left eye. Where applicable, the visual acuity tests were repeated with participant’s corrective spectacle. This was followed by pentorch (Keeler Instruments Ltd, London, UK) examination of the ocular anterior segment, direct ophthalmoscopy (Welch Allyn Inc., Skaneateles Falls, NY, USA), binocular indirect ophthalmoscopy (Keeler Instruments Ltd, London, UK), slit lamp biomicroscopy (Topcon Inc, Tokyo, Japan), slit lamp-assisted ?78D (Volk Optical, London, UK) fundus examination and fundus photography (Optoangiocam 9.1.4, Opto, South Africa). Subsequently, each participants had an objective refraction using an autorefractor (Huvitz CR 7000, Seoul, South Korea). This was subjectively refined using trial lenses and frame, both contained in a trial lens box (Keeler Instruments Ltd, London, UK). Jackson’s cross–cylinder (Keeler Instruments Ltd, London, UK), Duochrome and Worths Four Dot chart (Keeler Instruments Ltd, London, UK) were used as needed. Where cycloplegic refraction is indicated, automated objective cycloplegic refraction, using the auto-refractor (Huvitz CR 7000, Seoul, South Korea) was performed after satisfactory cycloplegia using 3-day tds regimen of Gutt Atropine (Ashford laboratories Ltd, Macau, China), and subjective post-cycloplegia test 3 weeks afterwards. The best corrected visual acuity (BCVA) and the lens power that achieved this (spectacle prescription) were both recorded. If the BCVA for distance, after subjective refraction, was worse than LogMAR 0.5 (6/18), the subject was further tested using a distance low vision device. (Vision 2020 Low Vision Resource Centre [LVRC] telescopes of 39, 49, 69 or 89—magnification. The BCVA achieved was recorded in each case. If the presenting near VA was worse than LogMAR 0.4 (equivalent of N5), near vision was corrected using trial frames and lenses. If the best corrected near visual acuity (BCNVA) was worse than LogMAR 0.4 (equivalent of N8 i.e. newspaper print size), after the near correction, the participant was subjected to low vision assessment for near vision using high power plus lenses from the trial lens box, or magnifiers-hand held (39, 49), stand (39, 79, 99), bar (1.59) and telescopes (39, 49, 69, 89) (Vision 2020 Low Vision Resource Centre [LVRC]). The unaided and
BCNVA, and the power of the lens used to achieve the BCNVA were recorded. Data Analysis Data was entered into and analysed using the Statistical Package for Social Sciences (SPSS) computer software, version 18.0. (SPSS Inc, Chicago, Illinios, USA). Descriptive statistics yielded frequencies, percentages and proportions; For inter-group comparisons to test for significance of observed differences, the student t test was used for continuous while the Chi square test was used for categorical variables. For all comparisons, a p \ 0.05 with the associated odds ratios and 95 % confidence intervals were considered statistically significant.
Results Socio-Demographic Characteristics The participants (n = 153), comprised 83 (54.2 %) females and 70 (45.8 %) males (sex ratio: M:F = 1:1.1) aged 23.4 ± 10.4 SD year (range 6–60 years) with a modal Table 1 Socio-demographic characteristics of participants Characteristic
n (%), n = 153
Age (years) 1–10
20 (13.0)
11–20 21–30
38 (24.8) 70 (45.8)
31–40
16 (10.5)
41–50
5 (3.2)
51–60
4 (2.6)
Sex Male
70 (45.8)
Female
83 (54.2)
Marital status Single Married
140 (91.5) 13 (8.5)
Educational status None Primary
2 (1.3) 28 (18.3)
Secondary
39 (25.5)
Tertiary
84 (54.9)
Occupation Unemployed/Students Civil servant
124 (81.0) 15 (9.8)
Trading
7 (4.6)
Artisan
4 (2.6)
Retired
1 (0.7)
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age group of 21–30 years. The majorities of the participants had tertiary education—84 (54.9 %) were unemployed/students—124 (81.0 %) and were single—140 (91.5 %). Table 1 show their age, sex distribution and their socio-economic profile. Clinical Profile All-153 (100.0 %) the participants had sub-normal presenting distant and near visual acuities. At presentation, the majorities of participants had moderate visual impairment for unaided distance—217 (70.9 %) and near—254 (83.0 %) vision. Table 2 shows the distribution of presenting mono-ocular visual acuities in 306 eyes of 153 participants.
Table 2 Type-specific distribution of refractive errors in 306 eyes of the 153 participants Type of refractive error Myopia Hypermetropia
73 (23.9) 9 (2.9) 35 (11.4)
Compound myopic astigmatism
79 (25.8)
Compound hypermetropic astigmatism
32 (10.5)
Mixed astigmatism
78 (25.5)
Total (%)
Fig. 1 Profile of non-refractive and miscellaneous disorders in 306 eyes of 153 participants
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All-306 (100.0 %) ’ eyes of the participants had nystagmus, hypopigmented fundus, foveal hypoplasia and prominent choroidal vessels. Of the 25/153 (16.4 %) participants with strabismus, 9/25 (36.0 %) had esotropia while 16(64.0 %) had exotropia. The participants’ profile of non-refractive abnormalities is shown in Fig. 1. Refractive Disorders The presence of refractive error was universal in all -306 (100.0 %) eyes. Astigmatism, present in 224 (73.2 %) and most frequently of the compound myopic type-79/224 (35.3 %, was the most common error while hypermetropia-9/ 306 (2.9 %) was the least common. The range of spherical refractive errors was -14.00 DS to ?8.00 DS, while astigmatic errors ranged from -6.00 DC to ?6 DC. Table 2 reports the profile of refractive errors among the participants.
n (%), n = 306 eyes
Astigmatism Simple astigmatism
Non-refractive Disorders
306 (100.0)
Mixed Refractive and Non-refractive Disorders A presenting visual impairment for far and near, representing combined refractive and non-refractive etiologies, was present in all-306 (100.0 %) eyes. Moderate visual impairment was the most prevalent category of visual impairment, accounting for 217 (70.9 %) eyes with impaired distance vision and 254 (83.0 %) eyes with impaired near vision (Table 3).
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Miscellaneous Non-albinism-Related Disorders
Discussion
These were seen in minority of participants and comprised pterygium, pingueculum and ptosis (Fig. 1). Overall, presence of refractive error was significantly associated with non-possession of tertiary education (OR 0.61; 95 % CI 0.38–0.96; p = 0.0374). However, typespecific associations with age and gender were not statistically significant (all ps [ 0.05) (Table 4).
The majorities of the participants were single females aged 30 years or younger, who possessed tertiary education and were frequently students or unemployed. A similar age distribution was observed in Europe [22], Tanzania [3], South African [23] and Nigeria [24] in studies among albinos. The higher tendency of younger people to seek for medical solution to their health or visual disability may account for this [25]. The observed educational profile, consistent with the participants’ age distribution, probably reflects the reported normal reading ability [22, 26] and intellectual development among persons with OCA [18]. However, this challenges the findings by Okoro et al [5]. that myopia, a common refractive anomaly in albinism, is associated with intellectual impairment Therefore, the present data do not support the need for creating special learning environment for albinos. The predominance of unemployed participants is consistent with job-related stigmatisation of albinos reported by Hong et al. [3] and Ezillo [27] This probably reflects the public’s poor knowledge and attitudes on albinism [3]. The investigators recommend public awareness creation on albinism to mitigate the public’s poor knowledge and attitudinal disposition. Astigmatism, frequently of the compound myopic and mixed types, was the most prevalent refractive
Table 3 Categories of presenting visual acuities in 306 eyes of 153 participants Presenting visual acuity
n (%), n = 306
Distance visual acuity (DVA) Normal Vision (DVA C 6/12)
0 (0.0)
Mild visual impairment (DVA \ 6/12–6/18)
1 (0.3)
Moderate visual impairment (DVA \ 6/18–6/60)
217 (70.9)
Severe visual impairment (DVA \ 6/60–3/60)
56 (18.3)
Blindness (DVA \ 3/60)
32 (10.5)
Near visual acuity (NVA) Normal vision (CN6)
0 (0.0)
Mild visual impairment (N8–N10)
12 (4.0)
Moderate visual impairment (N12–N24)
254 (83.0)
Severe visual impairment (\N36)
39 (12.7)
Blindness
Table 4 Association between participants’ demographics and types of refractive error
1 (0.3)
Refractive error
Percent with refractive error
Percent without refractive error
Odds ratio (95 % CI)
p value (Fisher’s exact test)
32 5
87 29
2.13 (0.76–5.99) Reference
0.1765
Male
29
111
0.72 (0.42–1.24)
0.2817
Female
44
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Ref
Myopia Age (years) \30 C30 Gender
Hypermetropia Age (years) \30
3
116
0.47 (0.08–2.89)
C30
2
36
Ref
0.5952
Gender Male
5
135
1.5 (0.39–5.69)
Female
4
162
Ref
\30
84
35
0.62 (0.25–1.56)
C30
27
7
Ref
106
34
1.27 (0.76–2.12)
118
48
Ref
0.7368
Astigmatism Age (years)
Gender Male Female
0.3684
0.3685
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abnormality followed by myopia and hypermetropia. The dominance of astigmatic refractive error in the present survey is consistent with previous reports [10– 13, 28] but differs from a preponderance of simple myopia reported by Okoro [5] in another Nigerian cohort 20 years earlier, and Wildsoet et al’s [13] series wherein hypermetropia was more frequent than myopia. While the observed high prevalence of refractive disorders is attributable to arrested/impaired emmetropisation in albinism [13], between-survey differences in prevalence and distribution of refractive disorders may be attributed to differences in accuracies of diagnostic facilities i.e. manual versus automated refraction. The ranges of astigmatic and spherical refractive errors in the present study agree with those reported in previous studies [9, 10, 13, 14]. The present data underscores the need for provision and unrestricted access to facilities for accurate diagnosis and optimal correction of albinism-associated refractive disorders. Additionally, albino-specific barriers to uptake of these refraction services should be identified and overcome [16]. Of the non-refractive disorders, nystagmus, foveal hypoplasia, hypopigmented fundus and prominent choroidal vessels were universal findings in the study cohort while strabismus was the least common. All participants had nystagmus in contrast to a previous study by Wolf et al. [19] where most of the participants (57.9 %) in that study had obvious nystagmus. The difference in criteria for nystagmus definition between the present study and Wolf et al.’s may account for this discordance. While the present study defined nystagmus as any involuntary to and fro eye movement, whether obvious or detected only at the slit lamp examination, Wolf et al. [19] categorised their subjects’ nystagmus into ‘absent or minimum ’ (barely detectable on slit lamp examination) and obvious nystagmus. The finding of foveal hypoplasia in all participants is similar to other studies [5, 14, 30]. This may be accounted for by the common aetiology of all forms of albinism resulting in absent or varying macular pigment and foveal hypoplasia. Strabismus was found in 8.2 %) of the eyes examined, exotropia being the most common Type. This is comparatively lower than the previously reported prevalence figures which ranged from 27–53 %. [12, 19, 30–32] The differences between surveys in cohorts’ clinical characteristics, particularly nystagmus-predisposing refractive and accommodative disorders might explain the observed differences. In the present report, the higher prevalence of exotropia suggests that delayed refractive correction of optical visual loss probably predisposed to amblyopia and its associated exo-deviation of the eyes. The discordance between the findings of this study and various others underscores the need for uniform case definition criteria while reporting the ophthalmic features of albinism, and holistic reporting of both refractive and non-refractive disorders to
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enable informed/contextual interpretation of study findings. Similarly, presenting visual impairment for far and near, a mixed refractive and non-refractive disorder was present in all participants. This is similar to previous observations [9, 10, 29] but partially agrees with the finding of Kutzbach and associates [17] who had some participants with normal presenting visual acuity. Although the exact cause of visual impairment in people with albinism is unknown, foveal hypoplasia, nystagmus and refractive error have been implicated. Additionally, amblyopia, resulting from delay in refractive correction, might be contributory. This implies that, beyond timely refractive correction, other visual/optical aids to alleviate the visual consequences of these abnormalities should be made widely available and accessible to albinos. Miscellaneous non-albinism-related ophthalmic disorders comprising pterygium, pingueculum, and ptosis were seen in a minority of participants. This finding could not be compared with other related surveys as none reported comparable data. This underscores the need for future investigators to identify and adequately manage co-morbid miscellaneous disorders with potentially adverse visual or ocular health implications.
Conclusion There is high prevalence of refractive, non-refractive and mixed ophthalmic disorders among albinos in Enugu, Nigeria. To alleviate the visual consequences of these disorders, the investigators recommend timely provision of, unrestricted access to, and needs awareness creation among albinos on, appropriate eye care services. Acknowledgments The authors acknowledge the assistance of the Albino Foundation (TAF) Enugu State Chapter, Drs. Oguama Felix, Okeh Ada, Eze Joy N, Ogbonnaya O and Dr. Ama for logistic support. The authors declare no external funding support for this work. Conflict of interest
None declared.
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