July 2009 East African Journal of Ophthalmology

Diabetic retinopathy prevalence and its association with

microalbuminuria and other risk factors in patients with Type 1 and Type
2 diabetes in Dar es Salaam, Tanzania.

AUTHORS
Lutale J. K1–3, Thordarson H4 , Sanyiwa A2, Mafwiri M2, Vetvik K1 and Krohn J5

1
Institute of Medicine, University of Bergen, Norway
2
Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania
3
Centre for International Health, University of Bergen, Norway
4
Department of Medicine, Haukeland University Hospital, Bergen, Norway
5
Department of Clinical Medicine, University of Bergen, Norway

Correspondence and reprints:

J.K. Lutale, Muhimbili University of Health and Allied Sciences (MUHAS) and the Institute of Medicine,
Haraldsplass Hospital, Ulriksdal 8, N-5009 Bergen, Norway, Email: kente315@yahoo.com

ABSTRACT
Objectives: The study was done to determine the prevalence of diabetic retinopathy
in Dar es Salaam and its association with microalbuminuria, demographic features,
metabolic control and some cardiovascular risk factors.
Design: A cross sectional study.
Setting: Muhimbili Hospital
Methods: Eighty six Types 1 (T1D) and 141 Type 2 (T2D) consecutive diabetic patients
were reviewed. Presence and severity of diabetic retinopathy were evaluated by
indirect ophthalmoscopy, and the relationship between retinopathy and diabetes
duration, body mass index (BMI), blood pressure (BP), serum creatinine, cholesterol,
HbA1c and albuminuria was analysed.
Results: The prevalence of any grade of retinopathy was 18.6% (4.7% in T1D and
27% in T2D). Presence of retinopathy was significantly associated with diabetes
duration. T2D with retinopathy had significantly higher systolic BP (p<0.01),
diastolic BP (p<0.05) and serum creatinine level (p<0.05) than those patients
without retinopathy. Albuminuria was the strongest predictor of retinopathy in
T2D, (p<0.001).
Conclusion: Retinopathy was associated with albuminuria, BP, and diabetes duration
but not with the metabolic control.

INTRODUCTION among African diabetic patients 4,5.

Patterns of diabetic retinopathy vary
geographically. In industrialized countries
like the USA and European countries, diabetic
retinopathy and macular degeneration are the
main causes of blindness in adults1,2. However
in sub-Saharan Africa and developing countries
of Asia and South America, other causes like
cataract, vitamin A deficiency, trachoma
and onchorcerciasis are the major causes of
blindness3. However, with the worldwide increase
of diabetes especially in developing countries,
the prevalence of diabetic retinopathy is also
expected to increase. Available prevalence
studies report a wide range in the prevalence
of diabetes retinopathy ranging from 9 to 55%
Although diabetic retinopathy can develop
in any person with diabetes, important risk
factors, like the duration of diabetes, the degree
of diabetes control, the blood pressure, and the
level of serum lipids have been reported 6,7.
Microalbuminuria also has been documented to
be associated with development and progression
of diabetic retinopathy. These determinants of
diabetic retinopathy are less defined among
diabetic patients in the sub-Saharan Africa.
There are scanty reports on separate prevalences
for retinopathy among type 1 and type 2 African
diabetic patients. The aims of this study were to
determine the magnitude of diabetic retinopathy

3
East African Journal of Ophthalmology
in patients with type 1 and type 2 diabetes and to
analyse the association with microalbuminuria,
metabolic control, sociodemographic features,
and some cardiovascular risk factors.
METHODS
Patients attending the Muhimbili outpatient
diabetic clinic for their regular visits and who
accepted to participate in the study were
included. Each patient was interviewed
using a standardized questionnaire. Patients
were recruited in two steps: 204 consecutive
patients attending the clinic for epidemiological
assessment and 68 consecutive patients who
were 30 years or younger on insulin therapy,
to get additional number of type 1 patients.
Muhimbili Hospital is the national referral and a
university teaching hospital. All patients gave
written informed consent before enrolment in
the study.
Patients were clinically classified into type 1 and
type 2 diabetes according to the 1997 World
health organization 8 based on clinical criteria,
using information from the patient’s diabetes
sheet and data collected at enrolment. Patients
not fitting into the clinical features of either type
were classified as undetermined.
The study protocol was approved by the Scientific
and Publication Committee at the Muhimbili
University College of Health Sciences (MUCHS)
and the Norwegian Regional Medical Research
Ethics Committees of Western Norway. The work
was done in accordance with the amended 2000
Helsinki declaration.
Ophthalmologic examination: Eye examinations
including visual acuity (Snellens chart placed at
6m) and intraocular pressure (using applanation
tonometry) were performed in all recruited
patients. Visual acuity was described according to
the visual standards of the International Council
of Ophthalmology using the 6m notation9.
Both pupils of each patient were dilated using
topical tropicamide 0.5%. Lens examination
was done with a slit lamp. The presence or
absence of cataract was reported with no further
grading.
Fundus examination was performed by slit lamp
biomicroscopy using a diagnostic contact lens.
4
July 2009
Due to the unavailability of a fundus camera
at the centre, fundus photography was not
done. The degree of diabetic retinopathy was
determined by a clinical classification system
according to the type of lesions detected on
fundoscopy 10 (Table 1). The findings in the eye
with the most severe retinopathy were used for
classification. Patients with dense cataract in
both eyes were not included in the retinopathy
staging.
Table 1: Classification of diabetic retinopathy
according to ophthalmoscopic findings
1 No diabetic retinopathy
2 Mild non-proliferative diabetic retinopathy
• Microaneurysms
• Dot and blot haemorrhages
• Hard (intra-retinal) exudates
3 Moderate - to -severe non-proliferative
diabetic retinopathy comprised of lesions
above, plus:
• cotton-wool spots
• venous beading and loops
• intraretinal microvascular abnormalities (IRMA)
4 Proliferative retinopathy
• Neovascularisation of the retina, optic disc or iris
• Fibrous tissue adherent to the retinal surface
• Retinal detachment
• Vitreous haemorrhage
• Pre- retinal haemorrhage
5 Maculopathy
• Macular oedema
• Ischaemic maculopathy
Blood presure measurements: Blood pressure
was measured with a suitable mercury
sphygmomanometer with a 10 x 22cm cuff.
After a 10 minutes rest with the patient in the
sitting position, blood pressure was measured
two times at 5 minutes interval. The 1st and the
5th Korotokoff sound were used to determine the
systolic (systolic BP) and diastolic blood pressure
(diastolic BP) measurements respectively. The
second blood pressure measurement was used
as the actual blood pressure for the individual.
Hypertension was defined as systolic BP ≥140
and /or diastolic BP of ≥90 mmHg or the use of
anti-hypertensive medication 8.
July 2009
Body weight / height: Weight was measured
without shoes or heavy clothing with a SECCA®
scale and recorded to the nearest 0.5 kilogram.
Height was determined to the nearest 0.5 cm
with a rigid measure against a vertical wall.
Body mass index (BMI) was calculated as weight
(kg) / height (m2). Patients with a BMI < 18.5
were regarded as underweight, those with a
BMI of 18.5-24.9 as normal weight, 25-29.9 as
overweight and ≥30 as obese. The waist-to-hip
ratio (WHR) was calculated from measurements
of waist and hip circumferences.
Blood sample collection and storage: A morning
sample of 6-9 mls of venous blood was drawn
from each subject and centrifuged within 2 hours
of collection. The sera were frozen at -80°C and
transported to Haukeland University Hospital,
in a dry ice-filled container at temperatures
between -50°C to-70°C. Samples reached their
destination within 24 hours and were kept at
-80°C.
Blood glucose and HbA1c measurement: Capillary
blood glucose was measured using a HemoCue
AB glucose analyzer (Angelholm, Sweden). The
measuring range is 0–22 mmol/l; all readings above
22 mmol/l are displayed as ≥22 mmol/l. HbA1c was
measured immunochemically using DCA 2000®+
(Bayer Health Care AG, Leverkusen, Germany) 11. The
instrument is standardized against the DCCT method
and was certified in 1996 12. Quality was controlled
using standard solutions. The room temperature was
not above 30°C. The instrument displays all readings
as percentages, with test ranges of 2.5–14%. All
readings above 14% are given as > 14%. Blood
glucose and HbA1c measurements were done at the
Muhimbili diabetic clinic.
Biochemical assays: Biochemical tests were
analysed on a BM/ Hitachi 917 Auto Analyzer
(Boehringer Diagnostics, Mannheim, Germany)
using kits supplied by Boehringer Mannheim
(Mannheim, Germany). Serum creatinine was
measured by the modified kinetic method by
Jaffé, serum cholesterol by the CHOD-PAP
method and serum triglycerides by the GPO-
PAP method.
Urine collection and urinary albumin concentration
assays: Two overnight urine specimens were
collected on two consecutive nights. Samples
were also screened microscopically for features
of urinary tract infections. Samples found to
be infected were discarded, the patients treated
5
East African Journal of Ophthalmology
accordingly and after a week of cure allowed
to re-submit another sample. The samples were
then frozen at -800C until they were analysed
for microalbuminuria and urine creatinine.
Urine albumin and creatinine concentrations
were determined at the Haukeland University
Hospital using an automated immunoturbidity
method (anti-human serum albumin obtained
from Dako, Oslo, Norway) with sensitivity of
2.3mg/L and inter- and intraassay coefficients of
variation of 4.4% and 4.3%, respectively (Dade
Boehring Marburg Gmbh, USA). An average
of the two readings was used to determine the
final urinary albumin excretion rate (AER). AER
was then categorised as normoalbuminuria
(< 20µg/min), microalbuminuria (20-200µg/
min), and macroalbuminuria (> 200µg/min).
Urinary creatinine was measured using the Jaffé
method.
Statistical analysis: Statistical analysis was
performed using the Statistical Package for
Social Sciences (SPSS) software, version 14
(SPSS, Inc., Chicago, IL, USA). Continuous data
were reported as mean ± 2 standard deviations
and categorical data as proportions, and
variables with skewed distribution the median ±
range were used. Groups were compared using
unpaired t-test, Fisher exact test or Chi-square
test and Mann-Whitney test as appropriate.
Logistic regression analysis was used to
quantify the association between covariates
and the presence of diabetic retinopathy. Two-
tailed p-values less than 0.05 were considered
statistically significant.
RESULTS
Sociodemographic characteristics of the study
population: Two hundred and seventy one were
enrolled, and 45.7% were men. Eight patients
did not complete the study and were excluded.
In 14 patients, the type of diabetes could not
clearly be determined and they were excluded
from the present study population, as were
22 patients who did not have eye examination
done. The final study population thus consisted
of 141 type 2 and 86 type 1 diabetic patients.
There was no significant sex difference in any
diabetes group.
Table 2 shows the basic patients characteristics.
Type 2 diabetic patients were significantly
older (p<0.001), had longer diabetes duration
(p<0.05) and had higher BMI (p<0.001) and
WHR (p<0.001) than type 1 patients.
East African Journal of Ophthalmology July 2009

Table 2: Socio- demographic characteristics and ophthalmoscopic findings in type 1 and type 2
diabetic patients

Variable Type 1 diabetes Type 2 diabetes

Number (%) 86 (37.9) 141 (62.1)

Age at inclusion (years) ‡ 20.8 (4-45) 51.8 (23.5-85) ***
Male, N (%)‡‡ 43 (50) 65 (45.8)
Diabetes duration (years) ‡ 3.0 (0-17) 4 (0-25)*
Smoking N (%)‡‡
Current smoker 2 (2.3) 4 (2.7)
Ex-smoker 1 (1.2) 25(17)
Never smoked 83(96.5) 112(79.4)
BMI kg/m2 N (%)‡‡ 19.4 (3.9) 27.8 (4.7) ***
Obesity (BMI >30) N (%)‡‡ 1 (1.1) 40 (36.7)***
WHR (cms) # 0.86 (0.07) 0.94 (0.1) ***

Ophthalmoscopic findings N (%)‡‡

Normal 76 (88.4) 69(48.9) ***
Mild NPR 3 (3.5) 21(14.8) **
Severe NPR 0 12 (8,5) ***
Maculopathy 1 (1.2) 3 (2.1)
Proliferative retinopathy 0 2 (1.4)
Any grade retinopathy 4 (4.7) 38 (26.9)***
Cataract 8 (9.3) 51 (36.2)***

Data expressed as median (min-max) and mean (SD) as appropriate

*p<0.05, **p < 0.01, ***p < 0.001, # Unpaired t-test, ‡ Mann-Whitney test, ‡‡ Fisher’s exact test

Retinopathy prevalence: The overall prevalence
of any diabetic retinopathy among the study
population was 18.1%. In type 1 diabetic patients
the prevalence of any retinopathy and proliferative
retinopathy were 4.7% and 0%, respectively. The
corresponding figures for patients with type 2
diabetes were 26.9% and 1.4% (p<0.001). The
prevalence of maculopathy was 1.2% in type 1
diabetic and 2.1% in type 2 diabetes patients,
(p<0.05). Type 2 patients had significantly higher
proportion of all grades of retinopathy than type
1 patients. No type 1 patient was found to have
severe NPR or proliferative retinopathy while
8.5% and 1.4% of type 2 diabetic patients
had severe NPR and proliferative retinopathy,
respectively (Table 2).
Association of retinopathy with clinical and
biochemical parameters: Patients with
retinopathy had a significant longer duration of
diabetes compared to those without retinopathy
with a median of 10 versus 3 years (p<0.01) for
type 1 patients, and a median of 7 versus 3.7
years (p<0.01) for type 2 patients. Likewise,
the proportion of patients with abnormal AER
was significantly higher in type 2 patients with
retinopathy than in those without retinopathy
(68.0% versus 32.4%, p<0.001), but not in
type 1 patients. Type 2 patients with retinopathy
had significantly higher systolic BP (p<0.01),
diastolic BP (p<0.05), and serum creatinine
level (p<0.05) than type 2 patients without
retinopathy (Table 3).

6
July 2009 East African Journal of Ophthalmology

Table 3: Demographic, cardiovascular, biochemical characteristics and visual acuity of diabetic

patients, according to presence or absence of retinopathy

Variable Type 1 diabetes Type 2 diabetes

No retinopathy Retinopathy No retinopathy Retinopathy

Number (%) ‡‡ 82 (96.5) 4 (4.7) 103 (73.0) 38 (27)**

Male N (%) ‡‡ 39 (47.6) 3 (75) 43 (41.7) 17 (44.7)
Age at inclusion (yrs)
{median(min-max)}‡ 21 (8-45) 25 (20-32) 52 (8-85) 54 (39-80)
Diabetes duration (yrs)
{median (min-max)‡ 3 (0-14) 10 (4 - 17)** 3.7(0-25) 7 (0.2-25)**
SBP mmHg {median(min-max)‡ 109 (88-140) 112 (72-120) 134 (90-210) 142 (110-200)**
DBP mmHg {median(min-max)}‡ 74 (50-110) 64 (50-77) 84(52-136) 90 (60-120)*
Serum Creatinine mmol/l
{median(min-max)}‡ 46.5(14-88) 54.5 (53-56) 68 (37-136) 74.5 (6-234)*
HbA1c % {median(min-max)}‡ 13.7(6.3->14) 9.7 (8.4-10.9) 9.7 (4.4->14) 10.5 (5.2->14)
Proportion abnormal AER N (%)‡‡ 10 (100) 0 8(32.4) 17 (68)***

Visual acuity N (%)‡‡

Normal vision (6/4-6/9) 76 (92.6) 3 (75) 63 (61.2) 22 (57.9)
Mild vision loss (6/10-6/18) 4 (4.9) 1 (25) 18 (17.5) 5 (13.2)
Moderate Vision loss (6/24-6/48) 1 (1.2) 0 14 (13.6) 5 (13.2)
Severe vision loss (6/60-3/60) 0 0 5 (4.9) 1 (2.6)
Profound vision loss (2/60) 0 0 0 2 (5.3)
Blindness
(1/60 to no light perception) 1 (1.2) 0 3 (2.9) 3 (7.9)

p-value - * p <0.05, ** p <0.01, ***p< 0.001 ‡ Mann-Whitney test, ‡‡ Fisher’s exact test

The proportion of patients developing any
retinopathy increased with longer duration of the
disease in type 2 diabetes (Figure 1). Twenty-
one percent of type 2 patients with diabetes
duration less than or equal to one year, had
developed retinal changes, mainly mild NPR.
Figure 1: The percentage of patients with type
2 diabetes developing any grade of retinopathy
at different diabetes durations
Most of the patients had normal vision; only
7(3.1%) patients, (one with type 1 diabetes
and 6 with type 2 diabetes) were found to be
completely blind i.e. visual acuity of 1/60 to no
light perception. In general, the type 2 diabetic
patients had lower visual acuity and significant
more cataract (p<0.001) than type 1 patients.
Regression analysis: Logistic regression analysis
in type 2 patients was performed using presence
of retinopathy as the dependent variable and
diabetes duration, age at inclusion, gender,
BMI, HbA1c, SBP and DBP, serum creatinine
and cholesterol as the covariates (Table 4).
A univariate logistic regression analysis
demonstrated a highly significant association
between diabetes duration, systolic BP, serum
creatinine (all p<0.01) and albuminuria
(p<0.001).

7
East African Journal of Ophthalmology July 2009

Table 4: Logistic regression analysis of retinopathy in type 2 diabetic patients by social demographic
and metabolic factors

Covariates Retinopathy Univariate Adjusted*

(Yes) N (%) OR (95% CI) p-value OR (95% CI) p-value

Age inclusion (yrs) 38 (27.1) 1.014 (0.982-1.047) 0.4

Diabetes duration 38 (27) 1.108 (1.036-1.185) 0.003
BMI (kg/m2)- 38 (27.7) 1.001 (0.926-1.083) 0.978
HbA1c % 38 (27) 1.063 (0.914-1.237) 0.427
SBP (mmHg) 38 (27) 1.021 (1.005-1.038) 0.008
DBP (mmHg) 38 (27) 1.028 (0.998-1.058) 0.069
S. creatinine (mmol/l) 38 (27.1) 1.019 (1.004-1.035) 0.014
S. cholesterol (mmol/l) 38 (27.1) 1.268 (0.946-1.698) 0.112
Albuminuria
AER – normal 21 (18.1) 1.00 1.0
AER- abnormal 17 (68) 9.613 (3.666-25.210) 0.000 8.667 (3.278-22.915) 0.000

*Results from the forward Wald stepwise selection. Predictors in the model age, diabetes duration
systolic BP, serum creatinine, total cholesterol and albumin excretion rate

A forward stepwise (Wald) multivariate logistic
regression analysis by elimination procedure
was used with the best fit model to identify
factors that might independently predict
development of retinopathy. Diabetes duration,
systolic BP, serum creatinine and albuminuria
were used in the model as covariates. Presence
of albuminuria OR (95% CI) [8.667 (3.278-
22.915), p<0.001] emerged as the strongest
predictor for the development of retinopathy.
Logistic regression analysis in type 1 patients
was not performed due to small numbers of
patients with retinopathy.
DISCUSSION
In this study we investigated the occurrence
of diabetic retinopathy and its determinants
among Tanzanian diabetic patients in Dar es
Salaam. The prevalence of retinopathy in our
type 2 patients (18.1%) was within the range of
previous reports on diabetic retinopathy from
Africa, which varies from 9 to 55%13-15. There
are few reports on the prevalence of retinopathy
among type 1 diabetic African patients for
comparison purposes 16. Most studies give
combined prevalences of retinopathy for type 1
and type 2 diabetes; however we found that the
prevalence of retinopathy in our type 1 diabetic
patients (4.7%) was lower than previously
reported. In a study from Dakar, the prevalence
of retinopathy among type 1 patients with
diabetes duration of 5.3 years was 12.7% 16. The
reason for the lower prevalence in our study is
unknown, but could be explained by differences
in the care of patients or other demographic
variables in the study population.
Diabetes duration has been considered the
strongest predictor for development and
progression of retinopathy 17,18. In patients with
type 1 diabetes, the duration of the disease
among those with retinopathy was significantly
longer than in patients without retinopathy
(10 versus 3 years). Previous studies show
that retinopathy can occur during the early
years after diagnosis of type 1 diabetes19-21
though rarely before 5 years19. Likewise, there
was a significant association between duration
of diabetes and the presence of any grade of
retinopathy in patients with type 2 diabetes.
Patients with retinopathy had significantly longer
diabetes duration than those without retinopathy
(7 versus 3.7 years). Other African studies have
also shown the association of disease duration
in type 1 and type 2 diabetes and the presence
of diabetic retinopathy 13,14,22,23. In Nigeria, the
prevalence of retinopathy was found to increase
with the duration of diabetes, being 12.7%,
16.8% and 20 % in patients with duration less
than 5 years, between 5 and 10 years and
greater than 10 years, respectively 23.
The level of glycaemic control is also an
important determinant of diabetic retinopathy.
Several studies have shown that improved
glycaemic control leads to reduced frequency of
diabetic retinopathy 24-27. In our study however,

8
July 2009
there was no correlation between the level of
glycaemic control and diabetic retinopathy in
neither type 1 nor type 2 diabetic patients.
In fact, type 1 patients with retinopathy had
lower levels of HbA1c than the type 1 patients
without retinopathy, but the difference was not
statistically significant. Similarly, in studies from
Ethiopia 22 and Zambia28, the presence of diabetic
retinopathy did not correlate with the degree
of glycaemic control. However in Nigeria, the
degree of glycaemic control appeared poorer in
the diabetic patients with retinopathy compared
to those without, thought not significantly
different23. The lack of association between
metabolic control could be related to the cross
sectional design of our study or the generally
short duration of diabetes.
Hypertension is another well known risk factor
associated with diabetic retinopathy. As in other
studies among African diabetic patients15,22,29,
systolic and diastolic BP were significantly higher
in type 2 diabetic patients with retinopathy. In
our study this relationship with blood pressure
in our study was not demonstrated in the type
1 patients.
Albuminuria was significantly associated with
the presence of diabetic retinopathy in type
2 patients but not in type 1 patients. In
multivariate regression analysis, albuminuria
was identified as the strongest predictor for
retinopathy in type 2 diabetic patients, (OR
(95% CI) 8.667 (3.278-22.915, p< 0.001). A
correlation between albuminuria and retinopathy
has been reported both for type 1 and type
2 diabetic patients in previous reports from
Western countries30-33 and Africa15,34. In a study
from Nigeria, Agaba et al. found that background
diabetic retinopathy occurred in 62.5% of
newly diagnosed type 2 diabetic patients with
microalbuminuria compared to 36.4% of those
without microalbuminuria (p< 0.05) 34.
The relatively small number of type 1 diabetes
patients with retinopathy in our study could
have masked relationships between some of
the risk factors and the frequency of diabetic
retinopathy.
CONCLUSION
In this cross sectional study, we have reported
separate prevalences for retinopathy among
T1D and T2D African patients, many give
9
East African Journal of Ophthalmology
combined prevalences. The prevalence of
diabetic retinopathy in T2D (24.1%) appears to
be in the range of combined levels previously
reported from Africa and of T2D from Western
countries. However the prevalence of retinopathy
in our type 1 diabetic patients (4.7%) was lower
than previously reported. Diabetic retinopathy
was associated with diabetes duration, blood
pressure, and albuminuria. There was however
a lack of correlation with the metabolic control.
ACKNOWLEDGEMENTS
We thank Dr. Z.G. Abbas, and the staff at the
Muhimbili Diabetic and Eye clinics who assisted
in this study. We appreciate the statistical
assistance of G.E. Eide.
CONFLICT OF INTEREST
DECLARATION
None of the authors have any conflict of interest
to disclose in relation to the present study
SOURCE OF SUPPORT
The study was supported in part by Novo Nordisk
Scandinavia A/S, Oslo, Wyeth Lederle Norge,
Oslo, and the Diabetes Research Foundation,
Department of Medicine, Haraldsplass Deaconal
Hospital, Bergen, Norway.
REFERENCES
1 Palmberg, D.E. Diabetes retinopathy. Diabetes.
1977; 26: 703-709.
2 Retinopathy Working Party. A protocol for
screening diabetic retinopathy in Europe. Diab.
Med. 1991; 8: 263-267.
3 King, H., Aubert, R.E. and Herman, WH. Global
burden of diabetes: 1995-2025 prevalences,
numerical estimates and projections. Diab. Care.
1998; 21: 1414-1431.
4 Neuhann, H., Water-Neuhann, C., Lyaruu, I.
et al. Diabetes care in Kilimanjaro region: clinical
presentation and problems of patients of the
diabetic clinic at the regional referral hospital-
an inventory before structured intervention.
Diab. Med. 2002; 19: 509-513.
5 Gebre-Yohannes, A. and Rahlenbeck, S.I.
Glycaemic control and its determinants in
diabetic patients in Ethiopia. Diabetes Res. Clin.
Pract. 1997; 35: 129-134.
6 The Diabetes Control and Complication Trial
Research Group. The effect of intensive
treatment of diabetes on the development of
long-term complications in insulin-dependent
diabetes mellitus. N. Eng. J. Med. 1993; 329:
977-986.
7 UK Prospective Diabetes Study Group.Tight blood
pressure control and the risk of macrovascular
and microvascular complications in type 2
East African Journal of Ophthalmology
diabetes. UKPDS 38. Br. Med. J. 1998; 317:
703-713.
8 WHO. International Society of Hypertension
guidelines for the management of hypertension.
J. Hypertens. 1999; 17: 151-183.
9 International Council of Ophthalmology report:
Visual standards Aspects and ranges of vision
loss with emphasis on population surveys.
Accessed on ICO website: http://icopph.org/
pdf/visualstandardsreport.pdf 2002: 1-35.
10 John, G. and O’shea, R. Harvey. Current
perspective of diabetic retinopathy: A photo-
essay for health professionals. http://medweb.
bham.ac.uk/easdec/eyetextbook/dminternet.
htm 2002.
11 Hiar, C.E. Clinical summary report. Clinical
performance of DCA 2000+ hemoglobin A1c
system six-minute assay. Bayer Diagnostic
Division 1-7, April 1998.
12 The Diabetes Research in Children Network
(DirectNet) Study Group. Comparison of
fingerstick hemoglobin A1c levels assayed by
DCA2000 with the DCCT/EDIC central laboratory
assay: results of a Diabetes Research in Children
Network (DirectNet) Study. Pediatric. Diabetes.
2005; 6: 13-16.
13 Erasmus, R.T., Oyeyinka, G. and Arije, A.
Microalbuminuria in non-insulin-dependent
(type 2) Nigerian diabetics: relation to glycaemic
control, blood pressure and retinopathy.
Postgrad. Med. J. 1992; 68: 638-642.
14 Rotimi, C., Daniel, H., Zhou J. et al. Prevalence
and determinants of diabetic retinopathy
and cataracts in West African type 2 diabetes
patients. Ethn. Dis. 2003; 13: S110-117.
15 Sobngwi, E., Mbanya, J.C., Moukouri, E.N. and
Ngu, K.B. Microalbuminuria and retinopathy in a
diabetic population of Cameroon. Diabetes Res.
Clin. Pract. 1999; 44: 191-196.
16 Ndiaye, M.R., Cisse, A., De Mederos, M. et al.
Prevalence of diabetic retinopathy at the Dakar
University Hospital Center. Dakar. Med. 1999;
44: 158-161.
17 Klein, R., Klein, B.E., Moss, S.E. et al. The
Wisconsin Epidemiologic Study of Diabetic
Retinopathy. XIV. Ten-year incidence and
progression of diabetic retinopathy. Arch.
Ophthalmol. 1994; 112: 1217-1228.
18 Fong, D.S., Aiello, L., Gardner, T. et al. Retinopathy
in diabetes. Diabetes Care. 2004; 27 Suppl 1:
S84-87.
19 Klein, R., Klein B. E., Moss, S. E. et al. The
Wisconsin Epidemiologic Study of Diabetic
Retinopathy. IX. Four-year incidence and
progression of diabetic retinopathy when age at
diagnosis is less than 30 years. Arch. Ophthalmol.
1989; 107: 237-243.
20 Bouhanick, B., Bellane-Chantelat, C., Salle, A.
et al. Proliferative retinopathy in patients with
type 1 diabetes of less than 5 years’ duration.
Diabetes Metab. 2002; 28: 141-144.
21 Malone, J.I., Morrison, A.D., Pavan, P.R. and
Cuthbertson, D.D. Prevalence and significance
10
July 2009
of retinopathy in subjects with type 1 diabetes
of less than 5 years’ duration screened for the
diabetes control and complications trial. Diabetes
Care. 2001; 24: 522-526.
22 Seyoum, B., Alanamu, R. A., Beluwoye, B. et al.
Retinopathy in patients of Tikur Anbessa Hospital
diabetic clinic. Ethiop. Med. J. 2001; 39: 123-
131.
23 Erasmus, R.T., et al. Diabetic retinopathy in
Nigerians: relation to duration of diabetes, type
of treatment and degree of control. East Afr.
Med. J. 1989; 66: 248-254.
24 The relationship of glycemic exposure (HbA1c)
to the risk of development and progression
of retinopathy in the diabetes control and
complications trial. Diabetes. 1995; 44: 968-
983.
25 Younis, N., Broadbent, D.M., Harding, S.P. and
Vora, J.R. Prevalence of diabetic eye disease in
patients entering a systematic primary care-
based eye screening programme. Diabet. Med.
2002; 19: 1014-1021.
26 The effect of intensive treatment of diabetes on
the development and progression of long-term
complications in insulin-dependent diabetes
mellitus. The Diabetes Control and Complications
Trial Research Group. N. Engl. J. Med. 1993;
329: 977-986.
27 Intensive blood-glucose control with
sulphonylureas or insulin compared with
conventional treatment and risk of complications
in patients with type 2 diabetes (UKPDS 33).
UK Prospective Diabetes Study (UKPDS) Group.
Lancet. 1998; 352: 837-853.
28 Rolfe, M. Diabetic eye disease in Central Africa.
Diabetologia. 1988; 31: 88-92.
29 Klein, R., Kleinn B. E. K., Moss, S. E. et al.
The Wisconsin epidemiologic study of diabetic
retinopathy. III. Prevalence and risk of diabetic
retinopathy when age at diagnosis is 30 or more
years. Arch. Ophthalmol. 1984; 102: 527-532.
30 Vigstrup, J. and Mogensen, C.E. Proliferative
diabetic retinopathy: at risk patients identified
by early detection of microalbuminuria. Acta.
Ophthalmol. (Copenh) 1985; 63: 530-534.
31 Gall, M.A ., Rossing, P., Skott, P. et al.
Prevalence of micro- and macroalbuminuria,
arterial hypertension, retinopathy and large
vessel disease in European type 2 (non-insulin-
dependent) diabetic patients. Diabetologia.
1991; 34: 655-661.
32 Klein, R., Klein, B.E., Moss, S. and DeMets, D.L.
Proteinuria in diabetes. Arch. Intern. Med. 1988;
148: 181-186.
33 Marshall, S.M. and Alberti, K.G. Comparison
of the prevalence and associated features of
abnormal albumin excretion in insulin-dependent
and non-insulin-dependent diabetes. Q. J. Med.
1989; 70: 61-71.
34 Agaba, E.I., Agaba, P.A. and Puepet, F.H.
Prevalence of microalbuminuria in newly
diagnosed type 2 diabetic patients in Jos Nigeria.
Afr. J. Med. Sci. 2004; 33: 19-22.