Assessment of Color Vision in Diabetic Patients
Tarek
M Radwan, Ehab M Ghoneim, Waleed A Ghobashy, Ahmed A Orma
Tarek M Radwan,
Ehab M Ghoneim, Waleed A Ghobashy, Ahmed A Orma, Ophthalmology Department, Faculty of Medicine, Suez Canal
University, Egypt
Correspondence to: Ehab M Ghoneim, MD
PhD, Professor of ophthalmology,
Ophthalmology Department, Faculty of Medicine, Suez Canal University, Egypt
Email: ehabghoneim@hotmail.com
Telephone: +201223639848
Received: December 26,
2014
Revised: March 13, 2015
Accepted: March 18, 2015
Published online: June 1, 2015
ABSTRACT
Aim: To assess the
changes in color vision in diabetic patients in different stages of diabetic
retinopathy compared to healthy individuals.
MATERIALS AND
METHODS: This
cross-sectional comparative study included sixty-eight eyes of 40 diabetic
patients, divided into four subgroups (10 patients / group)at different stages
of diabetic retinopathy (Eighteen of them had maculopathy)as well as 20 eyes of
10 healthy individuals as controls. Diabetic retinopathy and maculopathy were
assessed clinically by direct and indirect fundus examination along with
fluorescein fundus angiography, optical coherence tomography. Color vision was
assessed quantitatively by Ishihara pseudo iso-chromatic plates test and
qualitatively by Farnsworth D-15 test.
Results: Only two control
eyes (10%) failed the Ishihara pseudo iso-chromatic plates test, compared to 19
diabetic eyes (27.9%), 14 eyes (20.58%) were suspects. Also just two control
eyes (10%) failed the Farnsworth d-15 test while 34 (50%) diabetic eyes failed
the test showing; with Tritanopia was the most encountered color vision defect.
We find that color vision defects also increases with increasing disease
duration, severity of diabetic retinopathy, increased macular thickness and
presence of maculopathy, while type of diabetes shows no significant effect.
Conclusion: Diabetes
mellitus has a clear negative effect upon the color vision in both qualitative
as assessed by Farnsworth FD-15 test and quantitative manner as assessed by
Ishihara PIP test leading to loss of color vision perception with a varying
degree in relation to the type of diabetes and disease duration from patients
medical history, degree of retinopathy, presence of maculopathy by Fundus
examination+FFA and the increased macular thickness by OCT when compared to
normal healthy individuals.
© 2015 ACT. All
rights reserved.
Key words: Color vision; Diabetes mellitus; Diabetic retinopathy;
Maculopathy; Tritanopia; Ishihara PIP; Farnsworth d-15; Color vision defects;
Screening
Radwan TM, Ghoneim
EM, Ghobashy WA, Orma AA. Assessment of Color Vision in Diabetic Patients. International Journal of Ophthalmic Research 2015; 1(1): 19-23
Available from: URL: http://www.ghrnet.org/index.php/ijor/article/view/1001
INTRODUCTION
Diabetes mellitus is one of the most important factors of impaired
vision. In 2013, 382 million people developed diabetes; 350 millions of them
suffer from type II diabetes[1,2,3].
Prevalence of
diabetic retinopathy (DR)among diabetic patients aged 30 years and above is
54.65%, with the commonest presentation of diabetic retinopathy is mild non
proliferative diabetic retinopathy (NPDR) followed by, moderate NPDR, NPDR with
cystoid macular edema(CSME), severe NPDR, proliferative diabetic retinopathy
(PDR) and finally PDR with CSME[4].
Many studies
reported that screening patients with type I diabetes showed that 56% of them
have DR. With 11.2%, suffer sight threatening DR while in type II diabetes,
30.3% of patients have DR and only 2.9% are endangered with sight threatening
diabetes[5].
After initial
reports of altered color vision in patients with diabetes[6], a
number of experimental studies have been conducted to assess this association[7,8].
This study was
carried out in order to evaluate the effect of progression of DR upon the color
vision in both quantitative and qualitative manner.
MATERIALS
AND METHODS
Sixty-eight eyes of 40 diabetic patients, divided into four subgroups
(10 patients/group) at different stages of diabetic retinopathy (Eighteen of
them had maculopathy with exclusion of clinically significant macular edema) as
well as 20 eyes of 10 healthy individuals as controls. Patients were recruited
among those attending the ophthalmology outpatient clinic of Suez Canal
University Hospital in Ismailia, Egypt. Diabetic adults aged between 25 and 70
years with clinically diagnosed DR, were included.(The sample size is
calculated according to the following equation:
N = 2 (Z+ Z)2 X p-
q- / (p1-p2)2 [1]
Where:
n =
number per group.
Z = the value of
standard normal distribution for type I error probability for sided test and
equals 1.96.
Z = the value of
standard normal for the desired statistical power 80% and equals 0.84.
p-
= (P1 + P2)/2
q-
= 1- P-
p1 =
prevalence of color vision defects among male diabetic patients = 30 -80 %[2,3,4,5].
p2=
prevalence of color vision defects among male controls= 8%[6].
N = 10
subjects per group.
Total N = 50
Subjects (40 patients in diabetic sub-groups and 10 normal individuals in
control group).
For all
patients we took detailed history regarding type, onset of diabetes and any
visual complaints or previous eye procedures. Then patients were examined for
their refraction via retinoscopy, Best corrected visual acuity (BCVA) with
Snellen chart, IOP using Goldman applanation tonometer. Anterior segment
examination was carried out through Haag Streit -type slit lamp and fundus was
examined with +90 D lens as well as indirect ophthalmoscopy.
Patients with
known history of congenital color vision defect, previous laser
photocoagulation or intravitreal pharmacologic therapy; patients with aphakia,
pseudophakia, corneal opacities, amblyopia and clinically significant macular
edema were excluded as well as those with BCVA less than 6/60, myopic > 4
diopters or their intraocular pressure (IOP) more than 21 mm Hg.
To classifiy
DR according to ETDRS, we performed color fundus photography and fluorescein
angiography for patients with clinical findings of DR. In addition, we utilized
spectral domain OCT (Carl Zeiss Meditec, Jena, Germany) for measuring central
macular thickness.
Ishihara
Pseudo-iso-chromatic plate test was used as a quantitative test for detection
of defective color vision test
results analyzed as follows:
Plates 1- 15
determine the normality or defectiveness of color vision.
If
4 or less plates are red wrong, colour vision is regarded normal.
If 5-7 plates
are red wrong. Patient is a suspect of colour vision deficiency.
If 8 or more
plates are red wrong, colour vision is regarded deficient, while Farnthsworth
D-15 test was the qualitative test for detection of the type of the color
vision deficiency through analysis of the caps arrangement as follows:
Normal result
– No cross-lines.
Protanope – cross-lines parallel to
protan axis.
Deutanope –
Cross-lines parallel to Deutan axis.
Tritanope –
Cross-lines parallel to tritan axis.
Non specific colour
vision defect – cross-lines does not obey any axis.
Ethical
approval was acquired from the Suez Canal University research ethics committee.
An informed consent was taken from every patient participating in the study
after complete and detailed discussion of risk and benefits of his/her
inclusion in the study in accordance to the declaration of Helsinki.
Data were
analyzed with SPSS version 16. A p value of <0.05 was considered
statistically significant. The normality of data was first tested with
one-sample Kolmogorov-Smirnov test.
RESULTS
Diabetic patients in the study had ages between 35 to 72 years, with a
mean of 55.5±9.49 years, while controls ranging from 45 to 65 years, with a
mean of 54.2±6.59 years with a p value of 0.565. 39 (57.4%) were of type
II diabetes mellitus. The mean duration of diabetes mellitus was 11.28±4.35
year ranging from 5 to 22 years. Average macular thickness of diabetic patients
was 230.71±28.06 µm with a ranging from 115 to 312 µm; with only 26.5% had
maculopathy. In the Ishihara pseudo iso-chromatic plates test; only 51% of
diabetic patients passed the test, 28% failed and the remaining 21% were
suspects, with gradual increase in deficiencies with the progression of DR. In
contrary; 90% of controls passed and only 10% (Table 1). Qualitative color
assessment showed that 10% of controls failed the Farnsworth D-15 test due to
Protanopia, while 50% of the diabetics failed the test, with variable
dyschromatopsia mainly Tritanopia and combined color vision deficiencies with
fewer Protanopia and Deutanopia (Tables 2 and 3). The stratification of color
vision deficiencies types in different stages of DR showed gradual increase in
both Tritanopia and combined color vision deficiency in NPDR with progression
of DR stages with total color blindness appearing only in PDR (Table 4).
Duration of diabetes due to the relation between Duration and progression of DR
and increased macular thickness (Table 5) with p value of ≤ 0.001* and presence of maculopathy (Table 6) with a P value of 0.001*
were found to increase the presence of color vision defects; type of diabetes
had no clear effect on color vision (Table 7).
DISCUSSION
Diabetic retinopathy is a potentially sight threatening disease and a
major cause of blindness in patients under the age of 60 years. The highly
demanding work environment now days makes normal color vision an increasingly
essential asset. The increase in diabetes incidence in developing countries,
with its possible negative impact on color vision may have its sequel on labor
force and daily activities and represents a strong socioeconomic burden. This
study was conducted for better understanding for diabetic associated effect
upon color vision. Patients were recruited above age of 30 years to enable
better correlation to diabetes duration effect upon color vision deficiency as
well as the effect of aging as did Lakowski et al and Lombrial et al in their
studies[15,16].
The mean
duration of diabetes mellitus was 11.28±4.35 SD year ranging from 5 to 22 years
which was longer than the group studied by Klein et al with average
duration of 7.45 years[17].
As expected; DR severity increased with both age and duration of
diabetes, and this was highly significant from statistical point of view (P≤0.001). This was documented by many previous studies[18,19,20,21].
Among diabetics;
only 51% passed 21% were suspectsand 28% failed. This means that 49% of them
were either defective orborderline defective color vision.Mäntyjärviclaimed 62%
of diabetic patients got defective color vision the inequality may result from the
sampling technique we used in the study intending to equally represent each DR
stage equally to other groups while Mäntyjärvi minded the toll of DM with no
special care for the stages of DR as we focused in our study[22].
Ten percent of
controls failed Ishihara test. This almost three folds the numberreported by
Khalaj et al.,(3.49%) in his studies. The difference may be explained by the
fact that Khalajand his colleagues depended merely on history taking for
diagnosing color deficiency while we examined our patients to confirm our
findings[23].
In this work;
10% of controls failed the Farnsworth D-15 test showing Protanopia, while 50%
of diabetics did so. Fong[13] reported similar results, others
reported varying results as 30% Lombrial et al[11] 70%
Lakowski et al[24] and 80% Roy et al[10],
though the varying results they all agree upon the impact of diabetes upon the
color vision and the variation is mostly because the varying sampling,
inclusion and exclusion criteria, stage of retinopathy and maculopathy.
In this study
we found that the most frequent color vision deficiency among diabetics was the
Tritan deficiency 19.1%.Color deficiency in the form of Deutan and Protan were
equal (3% each), combined color deficiency was found in 19.1% while total color
blindness was responsible for 2.9%, showing no observable variations from most
of the pre-mentioned studies. Different values yet same arrangement were
noticed when comparing type 1 and type 2 diabetes and the presence and absence
of maculopathy.
The quality of
color vision defects in the diabetic acquired dyschromatopsia was the aim of
several studies, Sadiqulla et al[25] reported a red- green
loss pattern prevailing then total color blindness, Shin et al[26]
reported a Blue-yellow loss pattern, the same reported by Patz et aland Ma´ar et
al[27,28] which was
further explained by thepsychophysical measurements which show that the three cone types
red, green and blue are present in the approximate proportion 40:20:1,
respectively, in the control retina and are randomly distributed in the cone
matrix[29], Leading to early loss of blue color then combined
Tritanopia and Deutanopia then Protanopia at last in contrary to congenital
color vision deficiency pattern with Protanopia prevailing.
This study included both Type 1 and type
2 diabetes mellitus, while most studies was exclusively to type 1 diabetes only
or type 2 diabetes as did Lakowski et al[15], Bresnick[30]
and Aspinall et al[12] Our results showed no
statisticallysignificant difference between type 1 and type 2 diabetes
regarding their effect on color vision impairement.(The results about
differences between type 1 and 2 DM were not found in this study) IDDM 48.3%
passed and in NIDDM 53.8% (Table 7)
Regarding the
different stages of retinopathy, Tritan deficiency was the most frequent,
Protan and Deutan were less frequent. It was also found that with increasing
severity of retinopathy there was a gradual increase in combined color
deficiency while total color blindness was only present in the PDR. Same
chronological relation was reported by Marré and Birch et al[31,32].
The average
OCT measured macular thickness of the diabetic patients in this study was
230.71±28.06 µm and ranging from 115-312 µm, while Sadiqulla et al[25]
reported an average of 276 µm and range of 198-388 µm and Sasaki et al[33]
reported an average of 273.7±17.8 μm, Goeble et al[34]
reported and average of 283 µm and Oshima[35] reported an average of
283 µm. Lower value of the average macular thickness in our study could be due
to the criteria of selection excluding diabetic patient with BCVA less than
6/60. Also, the methodology used by Sadiqulla[25] to include the
diabetic patients whom already diagnosed to suffer color vision deficiency which was reported to be correlated with
increased average macular thickness on other hands almost all the studies
including diabetic patients reported increase in average macular thickness when
compared to normal individuals like the results of Goeble et al[34].
Macular
thickness has shown a gradual yet non-significant increase in the stages of
diabetic retinopathy as well as a weak positive correlation identified between
the average macular thickness and the duration of diabetes which is also
reported by Oshima et al[35] with no studies found to
contradict this finding.
In this study
we have concluded a highly statistical significance (P≤0.001) between the increase in macular thickness and in the
deterioration of color vision, which is similar to the reports of Sadiqulla et
al and Shin et al[25,26].
In patients
with diabetic maculopathy 83.3% have color vision deficiency, while in those
free from maculopathy only 38% sufferedcolor vision deficiency. Birch[36]
research raised the percentage to 90% and to even 100% by using the Birch
Tritan plates, which explains the higher percentage due to the higher test
sensitivity.
In conclusion
diabetic retinopathy induce varying degree of color vision defects with a varying
degree in relation to the type of diabetes, degree of retinopathy, the duration
of illness, presence of maculopathy and the increased macular thickness when
compared to normal healthy individuals.
ACKNOWLEDGMENTS
Patients included from our outpatient clinic at Suez Canal university
hospital.
CONFLICT OF INTERESTS
The author has no conflicts of interest to declare.
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