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Graefes Arch Clin Exp Ophthalmol (2015) 253:655661

DOI 10.1007/s00417-015-2943-0

PEDIATRICS

Refractive errors, visual impairment, and the use of low-vision


devices in albinism in Malawi
M. Schulze Schwering & N. Kumar & D. Bohrmann &
G. Msukwa & K. Kalua & P. Kayange & M. S. Spitzer

Received: 23 October 2014 / Revised: 13 January 2015 / Accepted: 14 January 2015 / Published online: 12 February 2015
# Springer-Verlag Berlin Heidelberg 2015

Abstract 0.98 (0.33) logMAR to 0.77 (0.15) logMAR after refraction


Background This study focuses on the refractive implications (p<0.001). The best improvement of VA was achieved in pa-
of albinism in Malawi, which is mostly associated with the tients with mild to moderate myopia. Patients with albinism
burden of visual impairment. The main goal was to describe who were hyperopic more than +1.5 D hardly improved from
the refractive errors and to analyze whether patients with al- refraction. With the rule (WTR) astigmatism was more present
binism in Malawi, Sub-Saharan Africa, benefit from (37.5 %) than against the rule (ATR) astigmatism (3.8 %).
refraction. Patients with astigmatism less than 1.5 D improved in 15/32
Methods Age, sex, refractive data, uncorrected and best- of cases (47 %) by 2 lines or more. Patients with astigmatism
corrected visual acuity (UCVA, BCVA), colour vision, con- equal to or more than 1.5 D in any axis improved in 26/54 of
trast sensitivity, and the prescription of sunglasses and low cases (48 %) by 2 lines or more.
vision devices were collected for a group of 120 albino indi- Conclusions Refraction improves visual acuity of children
viduals with oculocutaneous albinism (OCA). Refractive er- with oculocutaneous albinism in a Sub-Saharan African pop-
rors were evaluated objectively and subjectively by retinosco- ulation in Malawi. The mean improvement was 2 logMAR
py, and followed by cycloplegic refraction to reconfirm the units.
results. Best-corrected visual acuity (BCVA) was also
assessed binocularly.
Keywords Albinism . Refractive error . Visual acuity .
Results One hundred and twenty albino subjects were exam-
Low vision . Sub-Saharan Africa
ined, ranging in age from 4 to 25 years (median 12 years), 71
(59 %) boys and 49 (41 %) girls. All exhibited horizontal
pendular nystagmus. Mean visual acuity improved from

Introduction

M. Schulze Schwering (*) : K. Kalua : P. Kayange : M. S. Spitzer Albinism refers to a heterogenous group of hypopigmentation
c/o College of Medicine, University of Malawi, P Bag 360, Blantyre disorders; more than 100 genes influence the pigmentation of
3, Blantyre, Malawi
e-mail: mssoculus@web.de
hair, skin, and eyes of mice, and it is at least as likely that as
many genes are involved in humans [1]. The
M. Schulze Schwering : M. S. Spitzer hypopigmentation disorder is only classified as albinism in
University Eye Hospital Tbingen, Schleichstr. 1216, humans if there is reduced vision, nystagmus, iris translucen-
72076 Tbingen, Germany
cy, macular hypoplasia, and anomalous optic chiasm. The
N. Kumar : G. Msukwa : K. Kalua albino retina has less cone axons in the central retina than that
Lions Sight First Eye Hospital, Post dot net, Blantyre 3, PO Box E in normal pigmented individuals [24]. In Sub-Saharan Africa
180, Blantyre, Malawi (SSA), the most common form of albinism is the tyrosinase-
positive form, oculocutaneous albinism type II (OCA 2) (12).
D. Bohrmann
Mechanical and Automotive Engineering, Trier University of Especially in SSA, the hypopigmentary phenotype distin-
Applied Sciences, Trier, Germany guishes the affected individuals as different in a black
656 Graefes Arch Clin Exp Ophthalmol (2015) 253:655661

population, sometimes resulting in problems of acceptance normal room lighting conditions. Distance visual acuity was
and integration as reported from various African countries measured and recorded first binocularly then uniocularly.
[57]. Another distinguishing feature has recently been de- Unaided visual acuity was followed by objective examina-
scribed by Kiprono and colleagues in northern Tanzania: in- tion of the refractive conditions by dry (undilated) retinoscopy
dividuals affected by albinism have a higher number of performed under diminished room lighting conditions by clos-
colony-forming units, which is associated with sun-damaged ing the window curtains. Results of retinoscopy were refined
skin [8]. by subjective correction, and the VA in each eye was mea-
Numerous previous studies showed a wide range of refrac- sured with best correction possible.
tive errors in patients with albinism [912]. The goal of our Dry retinoscopy was followed by measuring and prescrib-
study was to describe the refractive errors and the benefit of ing of telescopes over best correction of refractive error for the
refraction for Sub-Saharan patients in Malawi, and to compare best eye; the target vision for prescribing telescopes for the
our results with previous international data. It adds to the best eye was set as 6/12 Snellens notation or 0.3 LogMAR.
scientific knowledge in the field of ophthalmology by study- Vision less than 6/18 (<0.5 logMAR) with best correction in
ing refractive errors in the largest sample of SSA albino pa- the best eye was graded as a low-vision child (low vision).
tients so far. Moreover, it should be clarified whether refrac- In order to standardize data on the causes of blindness in
tion and the prescription of glasses improves visual acuity children, we used a classification system with standard defi-
(VA) in this underserved patient population. nitions and methodology developed by the International Cen-
tre for Eye Health (ICEH) in collaboration with WHO [13].
This was followed by a near-vision function test (unaided;
first uniocularly and then binocularly), and the readings were
Material and methods recorded using the Bailey Lovie near-vision charts (E, num-
ber, and alphabetic and picture types); the distance between
The project was funded by the Malawian Ministry of Educa- the patients eye and the reading chart was measured using a
tion under the MIEP (Ministry of Education Programme) pro- simple ruler, and the readings were recorded. This was follow-
gramme. The target group was government primary school ed by measuring the uniocular and binocular near vision with
children. The programme was initiated by choosing itinerary best correction, and readings were recorded. For near-vision
teachers. These are teachers trained at Montfort University, anomalies, an appropriate optical device (magnifiers etc.) and
Malawi on special needs from the southern & central region nonoptical devices (large print, felt-tip pen etc.) were
of Malawi. They are trained on measuring visual acuity, prescribed.
briefed on ocular diseases leading to low vision, and trained A simple colour vision test was performed under normal
on different types of low vision devices (LVDs) and usage. room lighting conditions by using a set of four primary colour
Ethical approval was obtained from the College of Medi- pencils consisting of red, green, yellow, and blue colours, two
cine Research Committee (COMREC). The study adhered to of them each, and one colour pencil out of eight was given to
the tenets of the Declaration of Helsinki. All the albino chil- the child to match the same colour out of the remaining seven
dren were informed about the program well in advance at their pencils, and repeated with each colour to identify the matching
respective schools, with the consent of parents and the respec- colour. This test was aimed to rule out the basic colour vision
tive head teachers specifically for the project, and were given functionality of albino children.
an appointment for the examination of their eyes. Some par- The colour vision test followed by contrast sensitivity as-
ents accompanied their children for the examination of their sessment witha Lea picture chart at 1.6 m distance holding the
eyes to the respective schools on the appointment day. The chart vertically under normal room lighting conditions, and
majority of the children were being examined for the first the readings were recorded.
time; some had been examined a few years before and given Contrast sensitivity was followed by recording the inter-
corrective spectacles, but the children were not using them pupillary distance for each child. This was followed by dilat-
because they were damaged or were broken. ing the childs eyes using cyclopentolate eye drops for
All identified children during the period 2010 to 2012 with cycloplegic refraction. Finally, cycloplegic refraction was per-
visual defects at each school were given an appointment with formed to compare the dry retinoscopy and subjective
our team for assessment. The team was allowed to assess a correcting results, and the final spectacle prescription was
maximum of only ten children per day for quality assessment. given.
A well-ventilated room with curtains for altering the room The screening ended with training the child on spectacle
lighting conditions was identified in all the respective schools and LVD usage. All identified children were given a free pair
for assessment and the team used Bailey Lovie flip charts of LVDs and spectacles. A file containing recommendations
consisting of E, numeric, and alphabetic and picture types for parents and teachers of each child with low vision was
at 4 m distance for distance visual acuity assessment under handed over to the respective school head teacher for safe-
Graefes Arch Clin Exp Ophthalmol (2015) 253:655661 657

Table 1 Age, sex, pupillary distance (PD) with standard deviation, SD Table 3 Influence of refraction correlated to the age of the children

Male: n (%) Female: n (%) Total: n (%) Subjects (n in group) Age (years) Difference uncorrected/corrected
VA log MAR (average, BE)
Sex 71 (59 %) 49 (41 %) 120 (100 %)
Mean age (years) 12.7 (4.0) 12.2 (3.2) _ 4 6 0.15
PD (SD) 60.1 (4.4) 60.1 (4.3) _ 3 7 0.20
10 8 0.27
SD standard deviation 6 9 0.12
12 10 0.23
keeping. These children are being followed up every year on 15 11 0.18
the usage and condition of the LVDs. In addition, their perfor- 11 12 0.24
mance at school is followed up by the head teacher producing 11 13 0.09
each childs file that was given for safekeeping, and the team 9 14 0.11
recording the follow-up measurements in the same file. 8 15 0.33
Regression analysis was performed for the correlation of 10 16 0.33
right and left eyes, visual acuity, and refractive error. The 6 17 0.38
relative difference between the VA before and after was
6 18 0.08
analysed with ANOVA using JMP statistical software (version
3 19 0.15
10.0, SAS Institute Inc, Cary, NC, USA). A p<0.05 was con-
1 22 0.30
sidered to indicate a statistically significant difference.
One hundred and twenty albino subjects were examined, Average improvement ranged from 0.11 to 0.38 logMAR units (age 6 to
ranging in age from 4 to 25 years (median 12 years). All 22 years). There was no clear age-dependency of refraction-associated
exhibited horizontal pendular nystagmus. They were attend- VA improvement
ing schools covering a wide range of communities in southern
and central Malawi including Blantyre urban, Blantyre rural, Results
Zomba, Machinga, Balaka, Salima, Lilongwe urban and Li-
longwe rural. Results are shown in Tables 1, 2, 3, 4, and 5, and Figs. 1, 2, 3,
Refractive errors and visual acuity data were collected for 4, 5, and 6.
both eyes of most subjects, although nystagmus and/or age One hundred and twenty albino subjects were examined,
limitations precluded complete sets of data being obtained ranging in age from 4 to 25 years (median 12 years), 71 boys
for five subjects. (59 %) and 49 girls (41 %). All exhibited horizontal pendular
Visual acuity was measured using a black-on-white Bailey nystagmus. Mean pupillary distance was 60.1 mm in boys and
Lovie chart following standard procedure and recorded in girls. Colour vision was tested in 98 children, of whom none
logMAR format. Uncorrected visual acuity (UCVA) was tak- had deficiencies. Contrast sensitivity of 1.25 at 50 cm was
en in both eyes and in each eye as well as binocular BCVA. present in 98 children. Tinted glasses were prescribed for
106 of 120 children (88.3 %). The children of whom neither
colour vision, nor contrast sensitivity tests was taken were
either not cooperative taking it or were too young to under-
Table 2 Visual acuity data and refractive error with standard deviation, stand the test. Low-vision devices were prescribed for 114
SD

Eyes N logMAR (SD)


Table 4 Astigmatism (104/120): with the rule (WTR), against the rule
VA BE uncorrected 94/120 (78 %) 0.98 (0.33) (ATR)
BE corrected 94/120 (78 %) 0.77 (0.15)
N Percentage
Eyes N D (SD)
Refractive error, R 120 4.54 (5.77) WTR 39 37.5
best sphere ATR 4 3.8
L 120 4.37 (5.47) No astigmatism 61 58.7
Refractive R 120 1.09 (1.43) Total 104 100
astigmatism
L 120 1.23 (1.40) With the rule (WTR) astigmatism was more present (37.5 %) than against
Refractive error, R 120 4.09 (5.72) the rule (ATR) astigmatism (3.8 %). We considered each patient astigmatic
Equivalent sphere only if he had simple myopic or hyperopic astigmatism. All the com-
L 120 3.87 (5.36) pound myopic and hyperopic astigmatism we have taken as spherical
equivalent and assumed as spherical correction
658 Graefes Arch Clin Exp Ophthalmol (2015) 253:655661

Table 5 Prescription of
LVDs in Malawian Magnification Prescriptions (n=115)
patients with albinism
2 11
3 45
4 55
115/120 albino patients 5 4
received telescopes

children: 11 with twofold magnification, 45 with threefold, 55


with fourfold and three with fivefold.
Fig. 2 Correlation of visual acuity (logMAR) and spherical equivalent of
the right eye (RE). Spherical equivalent and uncorrected visual acuity do
not correlate with each other (correlation coefficient of 0.4)
Refraction
6/12 with LVDs we divided the best-corrected vision by target
Of 120 patients (n=240 eyes) with albinism, 71 were male and vision to get the desired telescope magnification, 36/12 = 3x
49 female. The mean average sphere was 3.26 D, median telescope (36 derives from 6/36 best corrected vision and 12
1.5 D, with a range from 30.00 D to + 16 D. The mean from the target vision with LVDs). Likewise with 6/60: then
average cylinder was 0.99, median 1.0 D, with a range from the target telescope power was 60/12=5x tele.
6 D to + 3.5 D. The pupillary distance (n=120) ranged from
52 to 70 mm (median 60 mm). The uncorrected visual acuity
(UCVA) of both eyes (n=120) ranged from 0.2 to 2.0 (median Discussion
0.9 0.3). The best-corrected visual acuity (BCVA) of both
eyes (n=120) ranged from 0.1 to 1.2 (median 0.8 0.16). In our study of a Sub-Saharan African (SSA) albino popula-
VA improvement after correcting for refractive errors was tion in Malawi, we retrospectively analysed the refractive er-
as follows: 23/94 (24 %) showed no benefit from refraction; rors of 120 patients with the inherited form of oculocutaneous
30/94 (32 %) improved by 1 line (VA measured in logMAR albinism (OCA). To our knowledge, this is the first study ever
units), 18/94 (20 %) by 2 lines, and 23/94 (24 %) patients in this region on refractive errors in children with albinism.
improved by 3 lines or more. Significant improvement was We examined 120 patients, which means that this is one of the
achieved in some patients with myopia and astigmatism largest groups of albinos worldwide ever examined for refrac-
higher than 1.5 D in any axis. Patients with high to mild tive errors. The main outcome is that that refraction is improv-
myopia (range 19.5 to 1.0 D) improved by 2 lines or more, ing visual acuity of children with oculocutaneous albinism in
patients with astigmatism less than 1.5 D improved in 15/32 of Malawi. The biggest improvement was achieved in patients
cases (47 %) by 2 lines or more. Patients with astigmatism whowere myopic between 1 and 7.5 diopters.
equal to or more than 1.5 D in any axis improved in 26/54 of These findings are almost in line with those of Anderson
cases (48 %) by 2 lines or more. Most mild hyperopic patients and colleagues [9]: They examined 35 patients, and the mean
did not improve, or only up to 1 line. binocular VA at distance was 20/80.9 (0.6 logMAR) corrected
LVDs were given with the target vision of 6/12 with tele- and 20/107.6 (0.7 logMAR) uncorrected (p<0.001). Wildsoet
scopes. E.g. if a patient improved to 6/36 with best spectacle and colleagues described the same finding, with all subjects
correction in the best eye, as our target vision for the child was (n=25) showing a reduced visual acuity with a mean of 0.9
logMAR units [12]. They emphasized that the higher the re-
fractive error, the more their patients tended to show poorer

Fig. 1 Refractive error relationship between right and left eye.


Refractive errors of the right and the left eye of the same patient Fig. 3 Best eye with emmetropia, myopia, hyperopia (sum=120) or
correlated highly with each other (correlation coefficient of 0.90) astigmatism 1.5 D
Graefes Arch Clin Exp Ophthalmol (2015) 253:655661 659

Fig. 4 Improvement in lines as a function of refraction VA taken (n= were myopic between 7.5 and 1 diopters. The VA in patients with
94/120, 78 %). This diagram shows the improvement in lines after albinism who were hyperopic more than +1.5 D did almost not improve
refraction. The biggest improvement could be achieved in patients who after refraction

visual acuities. We were nopt able to observe this phenome- (58.3 %). The mean refractive error in spherical equivalent
non, as BCVA improved at least by 1 line after refraction in for the right eye was 4.09 D (5.72 SD), for the left eye
most of our patients. 3.87 D (5.36 SD) (Table 2). The strong correlation of both
In our study, we were able to show that the benefit of eyes of the respective patient is shown in Fig. 1. The observa-
refraction might even be higher, and found a mean improve- tion that myopia was encountered most frequently is one in-
ment by two logMAR units: mean visual acuity improved teresting result of our study, as myopia can be regarded as a
from 0.98 (0.33) logMAR to 0.77 (0.15) logMAR after refrac- phenomenon of more urban and postmodern societies than in
tion (p<0.001). the one investigated by us, in which children spend many
Our findings are in contrast to the findings of Eball and hours every day outdoors. Guo and colleagues examined
colleagues from Cameroon, who examined the biggest SSA 681 children in China. They concluded that less outdoor
group of patients with albinism so far [14]. They retrospec- activity, more indoor studying, older age, maternal myopia,
tively analysed the refraction of 35 patients by automatic re- and urban region of habitation were associated with longer
fraction. They concluded that the degree of refractive error did ocular axial length and myopia in primary school children in
not influence the corrected visual acuity. However, we found Greater Beijing. They also emphasized that remaining out-
significant improvement in myopic patients, especially in doors for a longer time (e.g., during school) may reduce the
those with mild to moderate myopia. The Cameroonian col- high prevalence of myopia in the young generation in Beijing
leagues also concluded that astigmatic patients did not dem- [15]. This stands in contrast to our children, who are coming
onstrate improvement regardless of the type of astigmatism. from rural African settings with many outdoor activities and
In contrast to this, we found that patients with astigmatism less only few reading opportunities. The broader myopic range has
than 1.5 D improved in 47 % by 2 lines or more. Patients with also been described by other study groups such as Yaholam
astigmatism equal to or more than 1.5 D in any axis improved et al. in Israel [16]. They found that among OCA II patients
in 48 % by 2 lines or more (Fig. 5). We, like others, also with albinism mean values were: hypermetropia 3.2 2.5 D;
observed that with the rule (WTR) astigmatism was more myopia 3.8 4.5 D and astigmatism 1.8 1.0 D. In their
commonly present (37.5 %) than against the rule (ATR) astig- study, the mean best-corrected visual acuity (BCVA) was
matism (3.8 %) (Table 3). 0.48 0.2 logMAR units. According to the WHO guidelines
We found refractive errors of all entities, of which myopia [13] this means mild or no visual impairment (VI). W were
was the most commonly encountered refractive error unable to find such a mild degree in our Malawian patients,

Fig. 5 Improvement in lines as a


function of astigmatism VA
taken (n=94/120, 78 %. Patients
with astigmatism less than +1.5 D
improved in 15/32 of cases
(47 %) by 2 lines or more.
Patients with astigmatism equal to
or more than +1.5 D in any axis
improved in 26/54 of cases
(48 %) by 2 lines or more
660 Graefes Arch Clin Exp Ophthalmol (2015) 253:655661

Conflict of interest All authors certify that they have NO affiliations


with or involvement in any organization or entity with any financial
interest (such as honoraria; educational grants; participation in speakers
bureaus; membership, employment, consultancies, stock ownership, or
other equity interest; and expert testimony or patent-licensing arrange-
ments), or non-financial interest (such as personal or professional rela-
tionships, affiliations, knowledge or beliefs) in the subject matter or ma-
terials discussed in this manuscript.
Authorship according to ICMJE guidelines M Schulze Schwering,
N Kumar, K Kalua, and P Kayange: designed study
M Schulze Schwering, N Kumar, and K Kalua: collected data
M Schulze Schwering, N Kumar, D. Bohrmann, M Spitzer, and P
Kayange: did study analysis
M Schulze Schwering, M Spitzer, and P Kayange: edited manuscript
for submission.
Fig. 6 Overall distribution of improvement in lines. (0=zero lines; 1=1 M Schulze Schwering, N Kumar, D Bohrmann, G Msukwa, K Kalua,
line; 2 = 2 lines; 3 = 3 lines). VA was improved by refraction in M Spitzer, and P Kayange: Reviewed manuscript before submission
approximately 75 % of patients M Schulze Schwering, N Kumar, G Msukwa, M Spitzer, K Kalua, and
P Kayange: agreed to manuscript being published.

Competing interests None.


who all had to be classified as visually impaired (VI) regard-
less of whether they were uncorrected or with best-corrected
visual acuity.
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