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Frequency of diabetic retinopathy
and associated risk factors in Khartoum, Sudan: population based study
Einas S Elwali 1, Ahmed O Almobarak 2, Mona A
Hassan 3, Amir A Mahmooud 3, Heitham Awadalla 4,
Mohamed H Ahmed 5
1Public and Tropical Heath Program,
Graduate College, University of Medical Sciences and Technology, Khartoum,
Sudan
2Department
of Pathology, Faculty of Medicine, University of Medical Sciences and
Technology, Khartoum, Sudan
3Makkah
Eye Complex, Khartoum, Sudan
4Department
of Community Medicine, University of Khartoum, Khartoum, Sudan
5Department of Medicine and HIV
Metabolic Clinic, Milton Keynes University Hospital NHS Foundation Trust,
Eaglestone, Milton Keynes, Buckinghamshire MK 6 5LD, UK
Correspondence to: Mohamed H Ahmed. Department of
Medicine and HIV Metabolic Clinic, Milton Keynes University Hospital NHS
Foundation Trust, Standing Way, Eaglestone, Milton Keynes, Buckinghamshire MK6
5LD, UK. elziber@yahoo.com
Received: 2016-08-24
Accepted: 2017-03-30
Abstract
AIM: To assess the
frequency and associated risk factors of diabetic retinopathy among Sudanese
individuals with diabetes attending Makka Eye complex in Khartoum, Sudan.
METHODS: The cross
sectional hospital based study recruited 316 individuals with diabetes from
Makkah Eye Complex Retina Clinic. Standard questionnaire was used to collect
demographic data, medical history and life style characteristics. Blood samples
were taken to measure HbA1c and lipid profile. Fundus and slit lamp examination
were performed for screening of diabetic retinopathy.
RESULTS: Among 316
participants, 187 (59.2%) were males and 129 (40.8%) were females. The mean age
of participants was 58.7±10.5y. The overall frequency of retinopathy was 261
(82.6%). The percentages of the total participants with proliferative diabetic
retinopathy (PDR) were 126 (39.9%) and non-proliferative diabetic retinopathy
(NPDR) were 135 (42.7%). Importantly, duration of diabetes mellitus (DM) (72.2%
of more than 10y), being on oral hypoglycaemic drugs (versus insulin), and
hypertension were all significant risk factors for diabetic retinopathy (P=0.00,
0.01 and 0.00 respectively). Complications of diabetes like diabetic foot
(17.7%), history of amputation (6.7%) and clinically significant macular edema
(CSME) (47.4%) of the eyes were all significant risk factors (P<0.05).
Logistic regression analysis showed that duration of diabetes, hypertension and
CSME were found to be absolute risk factors (P=0.007, 0.003 and 0.000
respectively). Duration of DM of more than 10y have more than double risk
(OR=2.8), while having hypertension triples the risk of retinopathy (OR=3.1).
CONCLUSION: High rates of
diabetic retinopathy are noted among individuals with diabetes attending Makkah
Eye hospital in capital Khartoum. Urgent strategies are needed to monitor and
treat hypertension and optimize diabetes control in individuals with diabetes.
More investment in diabetes services is urgently needed.
KEYWORDS:
diabetes; Sudan;
diabetic retinopathy; insulin
DOI:10.18240/ijo.2017.06.18
Citation:Elwali ES,
Almobarak AO, Hassan MA, Mahmooud AA, Awadalla H, Ahmed MH. Frequency of
diabetic retinopathy and associated risk factors in Khartoum, Sudan: population
based study. Int J Ophthalmol 2017;10(6):948-954
Article Outline
INTRODUCTION
Diabetic retinopathy (DR) is one of the progressive
microvascular complications of diabetes, which is characterized by signs of
retinal ischemia such as micro aneurysms, haemorrhages, cotton-wool spots
(CWS), intraretinal microvascular abnormalities (IRMAs), venous calibre
abnormalities, and neovascularization and/or signs of increased retinal
vascular permeability[1]. The inevitable consequence of DR is
that it does not only lead to visual impairment but can also compromise the
ability of individuals to manage successfully their disease[2].
Importantly, diabetes is associated with 25 times increased risk of blindness,
especially in those with long duration of diabetes. For instance, in individuals
with diabetes for more than 20y, it was estimated that 77% may have degree of
retinopathy[3].
Depending
on the International Clinical Disease Severity Scale (ICDSS), DR has been
classified into proliferative diabetic retinopathy (PDR) which is further classified
into mild, moderate, severe, and non-proliferative diabetic retinopathy (NPDR)
[4]. In a systemic review included 62 studies from 21
African countries, showed that the prevalence of retinopathy range from 30.2%
to 31.6%; PDR 0.9% to 1.3%, and any maculopathy 1.2% to 4.5%. The systemic
reviewed also showed that data collected from diabetes clinic showed different
result. For instance,
the prevalence range for DR was 7.0% to 62.4%, PDR 0 to 6.9%, and any
maculopathy 1.2% to 31.1%[5].
The prevalence
of DR in Sudan was estimated to be around 17.2% in 1991[6].
Another study carried in outpatient of 3 general hospitals states in Sudan in
1995 for insulin-treated diabetic patients revealed that the prevalence of DR
was 43%, nephropathy was 22% and neuropathy 37%[7].
In Australia, factors associated with DR were duration of diabetes, HbA1c, and
systolic blood pressure[8]. In rural area of India, DR was not
significantly associated with classic features of metabolic syndrome like blood
pressure (BP), body mass index (BMI), level of education; blood concentrations
of cholesterol and high-density lipoproteins. However, prevalence was
significantly associated with higher age, higher blood glucose concentration
and higher HbA1c concentration[9]. The frequency
of DR in Cameroon was 54.1% among patients on antidiabetic medication and 73.9%
among those on insulin treatment, giving an overall frequency of 57.5%[10]. While in South Africa, the prevalence rates for retinopathy, preproliferative diabetic retinopathy (PPDR) and PDR were 24.9%, 19.5% and 5.5%,
respectively and risk factors were high BMI, systolic BP, being on insulin
treatment, high HbA1c and the presence of neuropathy[11].
In Tanzania, the prevalence of any DR
was 27.9% with background diabetic retinopathy (BDR),
PPDR, PDR and maculopathy having a prevalence of 19.1%, 6.0%, 2.9% and 16.1%
respectively. Risk factors identified were duration of diabetes, systolic BP
and random blood sugar[12]. The prevalence of DR in Ethiopia
was 41.4% with marked association with duration of diabetes, fasting blood
sugar, and systemic BP[13]. The prevalence in
Kenya was 35.9% and DR was associated with younger age, male sex, duration and
control of diabetes, and treatment compliance[14].
Unfortunately, limited information is available about the risk factors and
frequency of DR in Sudanese population. Therefore, the aim of this study is to
estimate the frequency and risk factors of DR among Sudanese individuals with
diabetes.
SUBJECTS AND METHODS
A cross sectional hospital based study was carried in
the period between September and December 2015. The study was carried in retina
clinic in Makkah Eye Complex, Riyadh branch in the capital of Khartoum city. It
is a specialized eye centre where patients from all over Sudan come seeking
treatment from different ethnicity and backgrounds. The participants were 316
individuals with diabetes (8.86% with type 1 diabetes and 91.14% with type 2
diabetes) attended the Retina Clinic in Makkah Eye Hospital and were willing to
give their verbal consent during the study period. None of those invited to
participate in this study declined. Makkah Eye Hospital is one of the few eye
hospitals in Sudan that offers advanced retinal therapy in the country. Most of
the patients attended this clinic were referred by medical practioners.
Data Collection
The WHO stepwise
approach for non-communicable diseases surveillance was used for data
collection. The approach had 3 levels: a questionnaire to gather demographic
information; physical measurements including anthropometric and BP and
biochemical tests[15]. All diabetic patients
attended the retina clinic were interviewed according to a standardized
questionnaire that was filled by the investigator and this is to collect
background and personal data of the patient, past medical history and common
symptoms of diabetes.
Inclusion criteria included adults 18y and above.
Exclusion criteria included individuals below 18y and pregnant ladies.
Anthropometric Measures Anthropometric measurements were taken using
standardized techniques and calibrated equipment; measurement tape for waist
circumference, measurement meter for calculating height and electronic weighing
scale for weight measuring. BMI was calculated by the formula: weight in kilograms
divided by height in meters squared. BMI ≤18.5 kg/m2 was defined underweight, 18.5-24.9 kg/m2 as normal, 25-29.9 kg/m2
as overweight and >30 kg/m2 as obesity[16].
Laboratory Measurement Blood samples were collected from each diabetic
patient in Makkah Eye Complex, Retina Clinic, who was willing to participate in
the study and gave his/her verbal consent. The collection was done by a skilled
laboratorist in sterilized condition. Blood sample were separated in 2 vacuum
tubes; Ethylene dinitrilote traacetic acid (EDTA) reagent for HbA1c (Immunoassay
method using Cobas c 111- Roche Diagnostics GmbH, Germany) and lithium reagent
for lipid profile. The laboratory tests for lipid profile were carried in
Makkah Eye Complex integrated laboratory using Cobas c 111 analyser was used for sample
analysis.
Ophthalmic Measures The
investigation was carried by a consultant ophthalmologist included slit lamp
examination for iris neovascularization and dilated fundus examination using 1%
tropicamide eye drop. A
90 D lens will be used to access the fundus and an indirect ophthalmoscope.
The presence of retinopathy was considered to be present if any
characteristic lesion as defined in the Early Treatment Diabetic Retinopathy
Study (ETDRS)[17] will be present: micro
aneurisms (Mas), haemorrhages, CWS, IRMAs, hard exudates (HE), venous beading
and new vessels. The severity of retinopathy was graded as no, mild, moderate,
severe NPDR and PDR according to the International Clinical Diabetic
Retinopathy Disease Severity Scale and unknown if view is obscured by cataract.
The presence of macular oedema and clinically significant macular oedema (CSME)
was graded as described by the ETDRS.
Fundus fluorescein angiography (FFA) and optical
coherence topography (OCT) document the presence of macular oedema and
vitreoretinal interface.
Ethical Consideration Ethics Committee of the University Medical Science and
Technology (UMST) provided the ethical clearance and approval for conducting
the research. Approval from Makkah Eye complex was also taken. Verbal consent
was taken from each participant before enrolment in the research, a full back
ground about the research was offered to the patient, no penalty for refusal as
patient had the right to withdraw at any level. Patients' information's were
kept confidential and codes were assigned to participants.
Statistical Analysis Data
had been cleaned, organized, coded and entered in master sheet in a personal
computer and analysed using the Statistical Package for Social Science (SPSS)
software program [version 21.0 computer program (SPSS, Inc., Chicago, IL,
USA)]. The
main variables analyzed were age, sex, BMI, blood glucose level, BP and a
family history of diabetes mellitus (DM) (first degree
family history), type of medication, duration of diabetes, cholesterol, triglyceride and
HbA1c. Chi-squared test was used to test for significance between proportions
and t and ANOVA tests were used to estimate associations between
continuous variables. P<0.05 was considered statistically significant.
RESULTS
Personal
and Anthropometric Characteristics of the Respondents In 316
diabetic patients enrolled in this study, 187 (59.2%) were male and 129 (40.8%)
were female. The mean age of participants was 58.7±10.5 and
further information can found in Table 1. The study showed that 70.9% of
participants were from urban areas and approximately one third (31.7%) had
higher education level. Importantly, duration of DM (72.2% of more than 10y),
being on oral hypoglycaemic drugs (versus insulin), and hypertension were all
risk factors for DR and with significant statistical P<0.05, Table 1.
Complications of diabetes like diabetic
foot (17.7%), history of amputation (6.7%) and CSME (47.4%) of the eyes
were all risk factors with significant statistical P<0.05 (Table 1).
Percentages of participants with history of smoking and/or alcohol intake
prospectively are 64.4% and 16.8%; both habits had no statistically significant
relationship with risk of DR. In this study antihypertensive medication was
prescribed to 153 individuals (48%). However, only 130 (41.1%) took their
antihypertensive medication regularly, while 23 individuals (6.9%) showed
noncompliance.
Table 1 Association between personal characteristics &
anthropometric measurements of the respondents and development of diabetic
retinopathy
n (%)
|
Factors |
PDR |
NPDR |
No
retinopathy |
Total |
P |
|
Gender |
|
|
|
|
|
|
M |
80
(25.3) |
77
(24.4) |
30
(9.5) |
187
(59.2) |
0.42 |
|
F |
46
(14.6) |
58
(18.4) |
25
(7.8) |
129
(40.8) |
|
|
Residence |
|
|
|
|
|
|
Rural |
33 (10.4) |
47 (14.9) |
12 (3.8) |
92
(29.1) |
0.13 |
|
Urban |
93
(29.4) |
88
(27.8 ) |
43
(13.6 ) |
224
(70.9) |
|
|
Educational level |
|
|
|
|
|
|
Illiterate + school |
77 (24.1) |
99 (31.4) |
40 (12.8) |
216
(68.3) |
0.85 |
|
Higher
education |
49 (15.6) |
36 (11.4) |
15 (4.7) |
100
(31.7) |
|
|
Duration of diabetes (a) |
|
|
|
|
|
|
10 or less |
21 (6.6) |
39 (12.3) |
28 (8.9) |
88
(27.8) |
0.00 |
|
More than
10 |
105
(33.2) |
96
(30.4) |
27
(8.5) |
228
(72.2) |
|
|
Type of medication |
|
|
|
|
|
|
Oral hypoglycaemic |
46 (14.2) |
66 (21.2) |
33 (9.8) |
145
(45.1) |
0.01 |
|
Insulin |
80
(25.6) |
69
(21.5 ) |
22
(6.5 ) |
171
(54.9) |
|
|
Family history of diabetes |
|
|
|
|
|
|
Y |
84 (26.7) |
87 (27.6) |
37 (11.7) |
208
(66.0) |
0.87 |
|
N |
42
(13.0 ) |
48
(15.2 ) |
18
(5.7 ) |
108
(34.0) |
|
|
History of alcohol intake |
|
|
|
|
|
|
Y |
25 (7.6) |
24 (7.6) |
5 (1.6) |
54
(16.8) |
0.33 |
|
N |
101
(32.1) |
111
(35.2) |
50
(15.9) |
262
(83.2) |
|
|
History of smoking |
|
|
|
|
|
|
Y |
38 (14.7) |
53 (16.6) |
22 (7.0) |
113
(35.6) |
0.52 |
|
N |
88
(27.9) |
82
(26.0) |
33
(10.5) |
203
(64.4) |
|
|
hypertension |
|
|
|
|
|
|
Y |
71 (22.5) |
65 (20.6) |
16 (5.1) |
152
(48.1) |
0.00 |
|
N |
55
(17.4) |
70
(22.2) |
39
(12.3) |
164
(51.9) |
|
|
Diabetic foot |
|
|
|
|
|
|
Y |
32 (10.1) |
18 (5.7) |
6 (1.9) |
56
(17.7) |
0.01 |
|
N |
94
(29.7) |
117
(37.0) |
49
(15.5) |
260
(82.3) |
|
|
Amputation |
|
|
|
|
|
|
Y |
15 (4.8) |
4 (1.3) |
3 (0.4) |
22 (6.7) |
0.01 |
|
N |
111
(35.2) |
131
(41.6) |
52
(16.5) |
294 (93.3) |
|
|
CSME |
|
|
|
|
|
|
Y |
48 (14.9) |
92 (29.2) |
11 (3.2) |
151 (47.4) |
0.00 |
|
N |
78
(24.7) |
43
(14.0) |
44
(14.0) |
165 (52.6) |
Frequency and Risk Factors of Retinopathy Total of 261
(82.6%) were found to have DR. The percentages of the total participants with
PDR were 126 (39.9%) and NPDR with 135 (42.7%). Data were cross tabulated
against the various grades of DR as results are shown in Table 2; in order to
determine other significant risk factors. Table 2 showed that age, BMI,
cholesterol, triglyceride and HbA1c were not significant risk factors for DR in
this study (P<0.05).
Table 2 ANOVA analysis to test the association between some of the
expected predictors and risk of having retinopathy
|
Retinopathy
status |
No. |
Mean |
Std. Deviation |
95% CI |
P |
|
|
Lower bound |
Upper bound |
|||||
|
Age (a) |
|
|
|
|
|
|
|
PDR |
126 |
58.1 |
10.5 |
56.2 |
59.9 |
0.52 |
|
NPDR |
135 |
59.5 |
10.3 |
57.8 |
61.3 |
|
|
No retinopathy |
55 |
58.3 |
11.3 |
55.3 |
61.4 |
|
|
Total |
316 |
58.7 |
10.5 |
57.6 |
59.9 |
|
|
BMI (kg/m2) |
|
|
|
|
|
|
|
PDR |
126 |
25.8 |
4.5 |
25.0 |
26.6 |
0.30 |
|
NPDR |
135 |
26.6 |
4.4 |
25.8 |
27.3 |
|
|
No retinopathy |
55 |
25.8 |
4.4 |
24.6 |
26.9 |
|
|
Total |
316 |
26.1 |
4.4 |
25.6 |
26.6 |
|
|
HbA1c (%) |
|
|
|
|
|
|
|
PDR |
126 |
10.2 |
2.8 |
9.7 |
10.8 |
0.60 |
|
NPDR |
135 |
10.1 |
2.2 |
9.7 |
10.5 |
|
|
No retinopathy |
55 |
9.8 |
2.4 |
9.1 |
10.5 |
|
|
Total |
316 |
10.1 |
2.5 |
9.8 |
10.4 |
|
|
Cholesterol
(mg/dL) |
|
|
|
|
|
|
|
PDR |
126 |
161.0 |
62.7 |
149.9 |
172.1 |
0.17 |
|
NPDR |
135 |
169.5 |
63.7 |
158.5 |
180.4 |
|
|
No retinopathy |
55 |
151.3 |
55.4 |
136.3 |
166.3 |
|
|
Total |
316 |
162.9 |
62.01 |
156.0 |
169.8 |
|
|
Triglyceride
(mg/dL) |
|
|
|
|
|
|
|
PDR |
126 |
147.0 |
101.1 |
128.9 |
164.9 |
0.25 |
|
NPDR |
135 |
148.6 |
87.7 |
133.6 |
163.6 |
|
|
No retinopathy |
55 |
125.3 |
73.5 |
105.5 |
145.2 |
|
|
Total |
316 |
143.9 |
91.2 |
133.7 |
154.0 |
|
Logistic Regression to Identify Absolute Predictors of
Diabetic Retinopathy We conducted stepwise
logistic regression for 6 variables that were statistically significant in univariate
analysis in Table 1 in order to identify absolute predictors of DR. Duration of
diabetes, hypertension, and CSME were found to be absolute risk factors with P
value of 0.007, 0.003, 0.000 respectively. Duration of DM of more than 10y have
more than double risk (OR=2.8), while having hypertension triples the risk of
retinopathy (OR=3.1) (Table 3).
Table 3
Logistic regression to identify absolute risk factors associated with
increasing probability of developing diabetic retinopathy
|
Variables |
Odd ratio |
Odd ratio 95.0% CI |
P |
|
|
Lower |
Upper |
|||
|
Duration of
DM |
2.8 |
1.3 |
6.0 |
0.007 |
|
Oral
hypoglycemic |
0.7 |
0.36 |
1.6 |
0.438 |
|
Being
hypertensive |
3.1 |
1.5 |
6.4 |
0.003 |
|
Diabetic
foot |
1.4 |
0.5 |
4.3 |
0.537 |
|
Amputation |
1.1 |
0.2 |
6.3 |
0.894 |
|
Clinically
significant macular edema |
4.2 |
1.9 |
9.1 |
0.000 |
DISCUSSION
In this study we have shown that DR
rate was 82.6% and this higher than the level recorded in Sudan between 1991 and
1995 which was 17.4% and 43% respectively[6-7].
This likely due to associated increase in prevalence of diabetes in Sudan. We
have recently shown that the prevalence of diabetes in urban regions of North
Sudan increased to 19%[18]. Another possible
factor, is an increase in specialize clinics that offer screening for DR in
Sudan[19]. DR is common problem all over the
globe and in particular those who live in low and middle income country[20]. For instance, the prevalence of DR in West India was
78%[21]. The global prevalence of DR was
estimated to be around 34.6%[22]. It is important
to recognise that there was a lot of variation in the incidence of DR across
Africa. For example; the prevalence in Cameroon was in the range between 54.1%
and 73.9%, South Africa 24.9%, Tanzania 27.9%, Ethiopia 41.4%, Malawai 50.1%
and Keyna was 35.9%[10-14,23]. These differences may be attributed to the
differences in the study setting, diagnoses techniques, measurement tools,
cultural background and health seeking behaviour differences. The incidence in
some European and Middle East countries were noted to be relatively low in
comparison with other countries in the world. For instance, DR in Catalonia
(Spain) was 12.3%, Portugal was 16.3% and Oman was 7.9%[24-26]. In UK the prevalence in Scotland was 19.3% and in
Wales it was estimated for type 1 diabetes was 56% and type 2 diabetes was
30.2%[27-28]. In Scotland, retinopathy in people
with type 2 diabetes at screening
was associated with male sex, HbA1c, increase systolic BP and obesity[28]. In studies from five African countries (Ethiopia,
Kenya, Tanzania, South Africa and Cameroon) DR was found to be associated with
high BMI, systolic BP, being on insulin treatment, high HbA1c and the presence
of neuropathy, duration of diabetes, random blood sugar, younger age, male sex,
duration and control of diabetes, and treatment compliance[10-14]. In this study, logistic regression analysis showed
that duration of diabetes, hypertension and associated CSME were found to be
absolute risks for DR. The high prevalence of DR in our
study may be due to poor diabetes control and late referral. Several studies
have shown that HbA1c is risk factor for DR[15-29]. In our study the likely reason for HbA1c was not
risk factor for DR. The both groups with retinopathy and without retinopathy
have poor diabetes control as HbA1c for both groups. There were 9.9% and 9.78%
respectively in comparison with target treatment of 6%-7%. Despite the fact
that rural residence is not a significant factor for DR, approximately one
third of participants were from rural residency in this study. In rural area of India, DR was significantly
associated with higher age, higher blood glucose concentration and higher HbA1c
concentration[9].
The Handan Eye Study (carried in rural areas of China) showed that DR was
associated with longer diabetes duration, hyperglycaemia and high BP[29]. This has
important implications on public health planning in Sudan as urgent strategies are
needed to monitor and treat hypertension and optimize diabetes control in
individuals with diabetes in rural areas.
There is general agreement in the
literature that NPDR was more prevalent than proliferative one[20]. In this study we have shown that NPDR (40.8%) was
more prevalent than PDR (33.4%). Importantly, PDR (33.4%) was higher than the
globally documented prevalence of 6.9% but also lower than 50.5% documented in
West India[20-21]. Different
metabolic factors and diseases were associated with an increased risk of DR. In
different African countries, significant association was found between PDR and
diabetes complications such as diabetic foot, amputation and maculopathy[10-14]. This is probably due to the
association with poor glycaemic control and longer duration of diabetes. This
may also explain the high prevalence of moderate PDR. Visual loss in DR was
noted with an increase with age, in this study CSME was an absolute risk factor
for DR[30]. The prevalence of CSME in Saudia
Arabia was noted to be around 7.2% and DR was associated with similar risk
factors found in our study (longer duration of diabetes, poorly controlled
diabetes, hypertension and insulin use)[31].
Among this study participants; 72.2%
were found having diabetes for more than 10y , and 27.8% had a diabetes for
less than 10y. This may explain in part, in this study duration of diabetes was
strongly significant risk factor for retinopathy and this was supported in most
of the studies carried about DR and suggestions that probably diabetes duration
is the strongest predictor for DR development and progression[32-33]. This is likely due to the
affects of the small blood vessels leading to the diabetes microvascular
complications[34]. In this study, 53.2% of study
participants were on insulin therapy which was found significantly associated
with retinopathy development. It worth mentioning that, insulin therapy
represented advancement on diabetes treatment and resulted in better glycaemic
control, however insulin therapy may be started late or it may have failed in
preventing long term complication of diabetes[35].
The chronic hyperglycaemia associated with DR impairs the regulation of retinal
perfusion which in turn leads to increased susceptibility to injury from
systemic hypertension and this was clearly demonstrated in this study as 48.1%
of diabetic patients were found hypertensive and the effect of hypertension on
progression of retinopathy was highly significant. Moreover this strongly
supports what is documented in the literature about DM and hypertension combination
role in multiplying the risk of macrovascular and microvascular disease[36]. This study is not without limitations. The study
design was a cross-sectional study, so we could not take account of the
temporal relationship between potential risk factors and outcomes. Another
limitation is short duration of the study. Despite these factors, we believe
that this study is novel and its findings reflect the trend of rising frequency
of DR in developing countries.
Frequency of DR in this study was very high among
individual with diabetes. Duration of diabetes, insulin use and hypertension,
diabetic foot and amputations are significant associated factors for DR. More
population based studies and surveillance should be carried out to address the
actual magnitude of the problem. Importantly, awareness and education programs
on DR should be highly encouraged. Early screening programs are of great value
in containing the increasing incidence of DR.
ACKNOWLEDGEMENTS
We are grateful for Makkah Eye
Hospital and Health Insurance Corporation, Khartoum State (HIKS) for full
sponsorship of the cost of investigation of this study.
Foundation: Supported by Makkah Eye Hospital and
Health Insurance Corporation, Khartoum State (HIKS).
Conflicts of Interest: Elwali ES, None; Almobarak
AO, None; Hassan MA, None; Mahmooud AA, None; Awadallah H,
None; Ahmed MH, None.
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